Plant Biology ISSN 1435-8603
RESEARCH PAPER
Seed longevity and fire: germination responses of an exotic perennial herb in NW Patagonian grasslands (Argentina) J. Franzese & L. Ghermandi Laboratorio Ecotono, Instituto de Investigaciones en Biodiversidad y Medioambiente, San Carlos de Bariloche, Argentina
Keywords Plant invasion; post-fire recruitment; Rumex acetosella; seed age; sheep’s sorrel; soil seed bank. Correspondence J. Franzese, Lab. Ecotono, Universidad Nacional del Comahue, Quintral 1250, San Carlos de Bariloche (8400), Argentina. E-mail:
[email protected] Editor D. Byers Received: 29 June 2010; Accepted: 31 December 2010 doi:10.1111/j.1438-8677.2011.00447.x
ABSTRACT Fire affects grassland composition by selectively influencing recruitment. Some exotic species can increase their abundance as a consequence of fire-stimulated seed germination, but response may depend on seed age. Rumex acetosella L. (Polygonaceae, sheep’s sorrel) is a cosmopolitan herb that has invaded NW Patagonia’s grasslands. This species forms persistent soil seed banks and increases after disturbances, particularly fire. We studied how fire and seed longevity influence R. acetosella germination. In 2008, we conducted laboratory experiments where we exposed different-aged seeds (up to 19 years old) to heat, smoke, charcoal, ash and control treatments. Total percentage germination and mean germination time depended on both seed age and fire treatment. Germination of younger seeds decreased with increasing temperature. There was no general pattern in germination responses of different-aged seeds to smoke, charcoal and ash. While smoke improved the germination of fresh seeds, charcoal decreased germination. Germination of untreated seeds was negatively correlated with seed age, and mean germination time increased with seed age. In most treatments, fresh seeds had lower germination than 1–5year-old seeds, indicating an after-ripening requirement. Smoke stimulates R. acetosella germination, causing successful recruitment during post-fire conditions. Fresh seeds are particularly responsive to fire factors, possibly because they have not experienced physical degradation and are more receptive to environmental stimuli. Knowing the colonisation potential from the soil seed bank of this species during post-fire conditions will allow us to predict their impact on native communities.
INTRODUCTION Fire can affect the composition of plant communities by selectively influencing recruitment (Whelan 1995; Bond & Van Wilgen 1996). Many exotic plant species increase in abundance after fire (Groves & Burdon 1986; Cronk & Fuller 1995; Mack et al. 2000). This increase suggests that exotic species possess certain traits that allow them to successfully respond to this disturbance, favouring their persistence or spread in the community. A stimulation of seed germination of some exotic species by fire might be expected, as happens with many native species (Dixon et al. 1995; Roche et al. 1997; Read et al. 2000). Certain fire-related abiotic factors provide physical or chemical stimuli for seeds and potentially promote germination. The effect of heat and smoke on seed germination of species from fire-prone environments has been studied because these ‘fire factors’ can help to break seed dormancy (Mallik & Gimingham 1985; Valbuena et al. 1992; Dixon et al. 1995; Reyes & Casal 2002). Heat can desiccate and crack seed coats or stimulate embryo development (Keeley & Keeley 1987; van Staden et al. 2000), while smoke can chemically scarify the seed coat or produce changes in membrane permeability (Brown & van Staden 1997; Egerton-Warburton 1998; Keeley & Fotheringham 1998). The latter effect may
make seeds more sensitive to endogenous hormones, decreasing the level of hormones required to trigger germination (Brown & van Staden 1997; van Staden et al. 2000). However, these and other fire-related abiotic factors, such as charcoal and ash, also can have inhibitory or neutral effects on seeds (Gonza´lez-Rabanal & Casal 1995; Reyes & Casal 1998; Keeley & Keeley 1999; Buhk & Hensen 2006; Dayamba et al. 2008). Plant species that form persistent seed banks have ecological advantages (Harper 1977; Thompson 1992; Thompson et al. 1997). Through the accumulation of different-aged seeds in soil, plant populations increase their genetic diversity and can persist in the community (Harper 1977; McCue & Holtsford 1998; Barrett et al. 2005). Species with persistent soil seed banks can germinate after wildfires even if they have not produced seeds that year. Although the role of persistent seed banks in the recovery of plant communities after fires is recognised (Ferrandis et al. 1999; Gonzalez & Ghermandi 2008), little research has been conducted about how the interaction between seed longevity and fire cues affects germination of species from fire-prone ecosystems (Roche et al. 1997; Reyes & Casal 2001; Newton et al. 2006) and we found no studies focused on exotic species. Understanding germination responses of different-aged seeds of exotic species after exposure to fire cues may provide valuable information about
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their colonisation potential from the soil seed bank during secondary succession and, together with complementary species information, allow prediction of their impact on the native community. In Northwest Patagonian semiarid grasslands (Argentina), fire and other disturbances have favoured the entrance and spread of exotic species (Rapoport & Brion 1991; Gobbi et al. 1995; Ezcurra & Brion 2005). Rumex acetosella L. (Polygonaceae, sheep’s sorrel) is a cosmopolitan ruderal herb that has successfully invaded this region (Gobbi et al. 1995). This species forms persistent soil seed banks (Ghermandi 1992, 1997; Thompson et al. 1997) and according to Thompson’s North West Europe database, R. acetosella is one of the top 100 species when considering maximum seed longevity in soil (>26 years, Thompson et al. 1997). In some grassland communities, R. acetosella can be the third or fourth most abundant species in the soil seed bank (Ghermandi 1992; Gonzalez & Ghermandi 2008). This perennial herb produces one-seeded fruits (achenes, hereafter seeds) with a thick persistent coat that might restrict germination (Ferrandis et al. 1999). Rumex acetosella abundance increases after disturbance, mainly through resprouting from rhizomes (Putwain & Harper 1970; Fonda 1974; Granstro¨m 1987; Ghermandi et al. 2004), and massive seedling recruitment of this species has also been documented after fire (Dollenz 1991; Gobbi et al. 1995; Ferrandis et al. 1999). These observations suggest that fire promotes the germination of seeds stored in the soil seed bank, facilitating R. acetosella colonisation and spread (Dollenz 1991; Ferrandis et al. 1999). Few authors have studied the separate effects of heat and smoke on R. acetosella germination (Granstro¨m & Schimmel 1993; Tsuyuzaki & Miyoshi 2008), and none have examined the effect of charcoal and ash or the effects of these fire factors on different-aged seeds. We conducted laboratory experiments to investigate how the interaction between fire effects and seed age affects germination of R. acetosella. We hypothesised (i) that abiotic factors related to fire promote R. acetosella germination by breaking seed dormancy; and (ii) that such a germinationpromoting effect will be influenced by seed age. We also studied the effect of seed weight on germination. MATERIAL AND METHODS Study area
Seeds were collected in a semi-arid grassland in northwest Patagonia, Argentina (4103¢19¢ S, 7101¢50¢ W). Mean annual precipitation is 580 mm, of which 60% falls in autumn and winter (Mediterranean precipitation regime), and mean annual temperature is 8.6 C (Meteorological Station, San Ramon ranch). The grassland is dominated by the perennial tussock grasses Stipa speciosa Trin. et Rupr var. major (Speg) and Festuca pallescens (St. Yves) Parodi. The dominant shrubs are Fabiana imbricata Ruiz et. Pavo´n, Mulinum spinosum (Cav.) Pers. and Senecio bracteolatus Hook et Arnott (Ghermandi et al. 2004). Vegetation cover is approximately 60% and the gaps (inter-tussock areas) are colonised by herbaceous species (Ghermandi & Gonzalez 2009). The most abundant native herbs are the annuals Triptilion achilleae Ruiz et. Pavo´n, Plagyobothrys verrucosus (Phil.) 866
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Johnst. and Microsteris gracilis (Hook.), whereas the most abundant exotic herbs are the annuals Erophila verna (L.) Chevall. and Holosteum umbellatum L., and the perennial Rumex acetosella L. Seed collection
Seeds were collected from randomly selected individuals in 13 different years: 1989, 1993–1996, 2000, 2001 and 2003– 2008. At the time of the experiments, seed ages were <1, 1, 2, 3, 4, 5, 7, 8, 12, 13, 14, 15 and 19 years old. Seeds were stored in paper bags at room temperature until the experiments were performed. Only those seeds that felt full and firm when they were gently squeezed were used in the experiments (viability by pressure method, Zuluaga et al. 2004). Experimental design Effect of fire and seed age on seed germination
To study the effect of fire and seed age on R. acetosella germination, in October 2008 we exposed seeds to heat (60, 90 and 120 C), smoke, charcoal, ash (hereafter ‘fire treatments’) and control treatment. We used five replicates of 10 seeds by fire treatment and year of seed collection (5 replicates · 10 seeds · 7 treatments · 13 seed ages = 4550 seeds). Because seed weight is correlated with germination percentage (Grime et al. 1981; Leishman & Westoby 1994), we weighed five groups of 10 seeds per year of collection. For the heat treatments, seeds were placed in an oven for 5 min at 60, 90 or 120 C. The temperatures selected were within the temperature range that seeds buried in the superficial soil layers experience during grassland fires (J. Franzese unpublished data; Wright & Bailey 1982). We exposed the seeds to dry heat, because fires occur during summer when the superficial soil is dry. For the smoke treatment, seeds were exposed to smoke for 10 min (Pe´rez-Ferna´ndez & Rodrı´guez-Echeverrı´a 2003). The smoke came from combustion of biomass belonging to the dominant grassland species. The plant material was burned inside a 200-l drum, which was connected to a 100-cm3 box through a galvanised tube. The box contained shelves on which the samples were located (Dixon et al. 1995). Charcoal and ash were obtained from the combustion of biomass corresponding to the dominant grassland species. For the charcoal and ash treatments, we applied 4 ml of 10 gÆl)1 of pulverised charcoal solution or ash solution, respectively, to each sample (Buhk & Hensen 2006). Samples in the control group were not treated with heat, smoke, charcoal or ash. After treatment, seeds were placed in Petri dishes on simple filter paper and treated with pulverised fungicide (Carbendazim, Punch Quı´mica, Buenos Aires, Argentina), watered with 4 ml distilled water (except for samples from the charcoal and ash treatments), and wrapped in transparent film to reduce evaporation. Those filter papers that dried out during the experiment were re-hydrated. The Petri dishes were placed in a germination chamber for 2 months, simulating an autumn photoperiod: March: Day: 7–20 h, 18.1 C ⁄ Night: 4.7 C; April: Day: 8–19 h, 13.5 C ⁄ Night: 2.0 C. Diurnal temperatures for March and April corresponded to the mean maximum monthly temperatures in
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Seed longevity and fire: effects on Rumex acetosella germination
the study site, while night temperatures were mean minimal temperatures of each month (Baskin & Baskin 1998). We monitored seed germination weekly during the first month and biweekly during the second month.
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Data analysis
To assess how fire treatments and seed age affect seed germination, we used a two-way ancova with fire treatment (heat: 60, 90 and 120 C, smoke, charcoal, ash and control) and seed age (<1, 1, 2, 3, 4, 5, 7, 8, 12, 13, 14, 15, 19 years old) as factors, and mean seed weight per sample as a covariate. anova contrasts and post hoc Dunnett tests were carried out to test how fire treatments affected germination in differentaged seeds. The relationships between seed germination (control treatment) and seed weight, and between seed germination (control treatment) and seed longevity were determined using Spearman correlations. Finally, we calculated mean germination time (MGT) for each seed age and fire treatment as:
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P ti ni MGT (days) ¼ P ni where ti is the number of days starting from the date of sowing, and ni is the number of seeds germinated on each day (Dayamba et al. 2008). A two-way ancova (mean seed weight per sample as covariate) was performed to test significant differences in MGT. Replicates with no germination were excluded. The tests carried out to assess how fire treatments affected the MGT in different-aged seeds were: anova for MGT data of <1-, 7- (log-transformed prior the analysis), 8-, 12-, 13- and 14-year-old seeds, and Kruskal–Wallis for data of the remaining seed ages. We used the post hoc Dunnett tests and comparisons of mean ranks for all groups after anova or Kruskal–Wallis analysis, respectively. RESULTS Rumex acetosella germination percentage depended on both seed age and fire treatment (Seed age F12,363 = 68.3, P < 0.001; Fire F6,363 = 30.0, P < 0.001; Seed age · Fire F72,363 = 3.18, P < 0.001). Seeds of all ages germinated even after exposure to the highest temperature. However, germination in the younger seeds decreased with increasing temperatures (Fig. 1A–C). Although 20% more fresh seeds (<1 year old) exposed to 90 C germinated than in the control (Fig. 1 B), this increase was not statistically significant (Dunnett, P = 0.12). There was no pattern in the germination responses among different-aged seeds to smoke, charcoal and ash (Fig. 1D–F). Smoke and charcoal had significant and contrasting effects on germination of fresh seeds: while smoke promoted their germination (control = 68% versus smoke = 90%; Dunnett, P < 0.1; Fig. 1D), charcoal decreased germination (control = 68% versus charcoal = 46%; Dunnett, P < 0.1; Fig. 1E). Charcoal decreased the germination of 12year-old seeds by 30% compared with the control (Dunnett, P < 0.1). Ash decreased germination of 13-year-old seeds by 36% (Dunnett, P < 0.05; Fig. 1F). Germination in the control treatment did not show any correlation with seed weight (Spearman R = )0.13, P = 0.28),
Fig. 1. Differences in germination percentage between fire treatments and control. An increase in germination indicated that more seeds germinated after a fire treatment than in the control, while a decrease in germination indicates that fewer seeds germinated. Germination percentage in control treatments by seed age are given in Fig. 2. Symbols show statistically significant differences between the fire treatments and the control. Statistical comparison by factorial ANCOVA and ANOVA contrasts (post hoc Dunnet test). #P < 0.1; *P < 0.05; **P < 0.01; ***P < 0.001.
but showed a negative correlation with seed age (Spearman R = )0.66, P < 0.01; Fig. 2). However, the oldest seeds had relatively high germination (38% ± 9.7, mean ± SE; Fig. 2). Mean seed weight ranged from 0.5 to 0.7 mg. The mean germination time (MGT) of R. acetosella was also influenced by seed age and fire treatment (Seed age F12, 342 = 49.8, P < 0.001; Fire F6,342 = 72.8, P < 0.001; Seed age · Fire F72, 342 = 3.65, P < 0.001). Seeds younger than 8 years had different germination behaviour compared to seeds older than 8 years. The former group of seeds reached
Fig. 2. Seed germination percentage and seed weight (mg) of differentaged seeds (control treatment).
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Fig. 3. Cumulative germination percentage in the fire treatments in a: Control, b: 60 C, c: 90 C, d: 120 C, e: Smoke, f: Charcoal and g) Ash. A: Seed younger than 8 years; B: Seed older than 8 years.
greater cumulative germination in a shorter period of time (between the days 0–5 or 0–11) in almost all fire treatments (Fig. 3Aa–f and g) than the second group of seeds (Fig. 3B). As an exception, exposure to 120 C for 5 min delayed and decreased germination of seeds of any age (Figs 3Ad, 3Bd and 4C). In most treatments, the fresh seeds (<1 year old) had lower germination percentages than 1–5-year-old seeds (Fig. 3A). DISCUSSION Fire-related factors can produce diverse germination responses in different-aged seeds of Rumex acetosella. Our results support the hypothesis that some fire-related factors 868
promote germination of this species, and the hypothesis that fire effects are mediated in part by seed age. Seed weight did not influence germination patterns. R. acetosella seeds required an after-ripening period of at least 1 year to reach higher germination percentages. Accordingly, most seeds collected only a few months before the experiment (fresh seeds) had lower germination than 1–5year-old seeds. Similar after-ripening requirements have been found in this (Dollenz 1991; Van Assche et al. 2002) and other Rumex species (Van Assche et al. 2002). However, an exposure to smoke for 10 min stimulated germination of the fresh seeds, overcoming their after-ripening requirement. Smoke can promote germination through substituting certain compounds or treatments required for seed germination or
Plant Biology 13 (2011) 865–871 ª 2011 German Botanical Society and The Royal Botanical Society of the Netherlands
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Seed longevity and fire: effects on Rumex acetosella germination
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Fig. 4. Differences in mean germination time (days, mean) between fire treatments and control. An increase in MGT indicated that seeds in a fire treatment germinated more slowly than the control, while a decrease in MGT indicates that seeds in a fire treatment germinated more rapidly than the control. MGT (days) in control treatment by seed age: 19 years = 58, 15 years = 57, 14 years = 16, 13 years = 33, 12 years = 47, 8 years = 9, 7 years = 16, 5 years = 10, 4 years = 7, 3 years = 7, 2 years = 5, 1 year = 10 and <1 year = 7. Symbols show statistically significant differences between the fire treatments and the control. Statistical comparisons by factorial ANCOVA, ANOVA (for <1-, 7-, 8-, 12-, 13- and 14-year-old seed data; post hoc Dunnet test) and Kruskal–Wallis test (for the remaining seed ages; post hoc test Comparisons of mean ranks for all groups). # P < 0.1; *P < 0.05; **P < 0.01; ***P < 0.001.
by sensitising the embryo to hormones that induce germination (Brown & van Staden 1997). In contrast to our results, a recent study by Tsuyuzaki & Miyoshi (2008) found no stimulation of germination by smoke in fresh seeds of R. acetosella. These apparent contrasting results may have been caused by different lengths of exposure to smoke (1 h versus 10 min): variation in exposure time to smoke may change germination for a species (Pe´rez-Ferna´ndez & Rodrı´guez-Echeverrı´a 2003; Reyes & Casal 2006; Gonzalez et al. 2010). Heat had a neutral effect on germination of seeds older than 7 years, but inhibited germination in younger seeds. The higher moisture content of the younger seeds is likely to have increased heat conductivity within the seed, killing the embryo. Granstro¨m & Schimmel (1993) found that pre-wetted seeds of R. acetosella were more sensitive to high temperatures than dry seeds. Moreover, no seeds germinated after exposure to temperatures higher than 60 C among pre-wetted seeds, or temperatures higher than 75 C in seeds stored dry prior to heat exposure. In contrast to our methods, these authors exposed R. acetosella seeds to wet heat by immersing the seeds in hot water. Our seeds germinated after exposure to much higher temperatures than those reported by Granstro¨m & Schimmel (1993) when we exposed the seeds to dry heat.
Fresh seeds increased their germination when they were exposed to an intermediate temperature (90 C for 5 min), constituting an exception within seeds younger than 7 years of age. Although it was observed only as a trend, it is interesting to highlight the similarity to other results obtained by Tsuyuzaki & Miyoshi (2008), who increased germination in fresh R. acetosella seeds by approximately 13% after heating the seeds to 75 C for 25 min. R. acetosella appears to have an optimum range of temperature for breaking dormancy that depends on exposure time and includes 75 and 90 C. Interactions between heat and smoke can influence seed germination in predetermined ways (Thomas et al. 2003). We cannot infer the potential that this interaction would have on R. acetosella germination based on the results obtained here, but we consider that it would be an interesting study. The chemical change in the seed environment produced by charcoal and ash was neutral or negative for R. acetosella germination. Unlike smoke (Adkins & Peters 2001), charcoal and ash were alkaline (J. Franzese unpublished data), and the increased pH in the germination medium could inhibit germination, as has been suggested for other species from fire prone-systems (Gonza´lez-Rabanal & Casal 1995; Henig-Sever et al. 1996). However, this hypothesis needs to be tested, because the observed germination responses could have been produced by other chemical cues. Furthermore, sensitivity to charcoal and ash depended on seed age. We do not know why 12- and 13-year-old seeds, but not other ages, were sensitive to these fire factors. Fresh seeds were particularly responsive to several fire factors, possibly because they have not experienced physical degradation and are more receptive to environmental stimulus. Seed age and fire cues not only affected total germination, but also the mean germination time (MGT). However, seed age had the most influence on germination time. We detected two general responses mainly associated with the age of seeds: short germination time in seeds younger than 8 years, and long germination time in the older seeds. The increase of MGT with higher seed age observed in R. acetosella is a common pattern found in many species (Dell’Aquila 1987; Gasque & Garcı´a-Fayos 2003). As seeds age, many structural proteins and enzymes degrade and the rate of protein synthesis decreases, negatively affecting seed physiology and consequently germination time (Dell’Aquila 1994). Only one fire factor, 120 C for 5 min, had a consistent effect on germination time, increasing it irrespective of seed age. Longer germination times have been associated with loss of seedling vigour (Dell’Aquila 1987). The oldest untreated seeds of R. acetosella produced seedlings with a radicle length <1 cm, whereas the radicle of seedlings from younger seeds was at least 2-cm long (J. Franzese, unpublished data). Seedlings lacking vigour are less likely to survive environmental hazards (e.g. predation, desiccation, freezing, etc.; Gilbert et al. 2001; Franzese et al. 2009). Although the artificial storage conditions of seeds at ambient temperature are different from those in soil, we consider that, in time, viability of seeds will be similarly affected. Old seeds of R. acetosella might germinate in the field after fires but, compared to young seeds, they are less likely to establish successfully once germinated. Although seedling recruitment from old seeds would still be important, due to their relative contribution to the seed bank, fresh seeds are generally closer to the surface in the soil profile
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(Harper 1977). We therefore think that they may have a significantly greater role in subsequent post-fire populations. Our results suggest that smoke stimulates the germination of fresh seeds, producing successful recruitment of R. acetosella during post-fire conditions. The fact that seeds produced just before fire occurrence may be more important to R. acetosella invasion than the seed bank accumulated over time, highlights the importance of studying how meteorological conditions and other environmental hazards affect seed production (number and quality). Furthermore, the effects of indirect fire cues (e.g. opening of canopy gaps and increasing daily temperature fluctuations) on germination of this species should be considerate in future research. These studies would provide additional information to understand the potential germination responses of this invasor perennial herb after summer fires. ACKNOWLEDGEMENTS The authors acknowledge constructive comments on an earlier version of two anonymous referees and the Associate Editor, Diane Byers. We thank Charlotte Reemts and Daniel Simberloff for the English corrections and comments on the manuscript. We also thank Dominik Marty and Andrew Hodgson (ranch managers) who allowed us to perform our study at San Ramo´n. The study was funded by Universidad Nacional del Comahue (Project B131), Agencia de Promocio´n Cientı´fica y Tecnolo´gica (PICTO 36894), and Consejo de Investigaciones Cientı´ficas y Tecnolo´gicas. REFERENCES Adkins S.W., Peters N.C.B. (2001) Smoke derived from burnt vegetation stimulates germination of arable weeds. Seed Science Research, 11, 213–222. Barrett L.G., He T., Lamont B.B., Krauss S.L. (2005) Temporal patterns of genetic variation across a 9-year-old aerial seed bank of the shrub Banksia hookeriana (Proteaceae). Molecular Ecology, 14, 4169–4179. Baskin C.C., Baskin J.M. (1998) Seeds: ecology, biogeography, and evolution of dormancy and germination, 1st edition. Academic Press, San Diego, USA. Bond W.J., Van Wilgen B.W. (1996) Fire and plants, 1st edition. Chapman & Hall, London, UK. Brown N.A.C., van Staden J. (1997) Smoke as a germination cue: a review. Plant Growth Regulation, 22, 115–124. Buhk C., Hensen I. (2006) ‘‘Fire seeders’’ during early post-fire succession and their quantitative importance in south-eastern Spain. Journal of Arid Environments, 66, 193–209. Cronk C.B., Fuller J.L. (1995) Plant invaders, 1st edition. Chapman & Hall, London, UK. Dayamba S.D., Tigabu M., Sawadogo L., Oden P.C. (2008) Seed germination of herbaceous and woody species of the Sudanian savanna-woodland in response to heat shock and smoke. Forest Ecology and Management, 256, 462–470. Dell’Aquila A. (1987) Mean germination time as a monitor of the seed ageing. Plant Physiology and Biochemistry, 25, 761–768. Dell’Aquila A. (1994) Wheat seed ageing and embryo protein degradation. Seed Science Research, 4, 293–298.
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Dixon K.W., Roche S., Pate J.S. (1995) The promotive effect of smoke derived from burnt native vegetation on seed germination of Western Australian plants. Oecologia, 101, 185–192. Dollenz O.A. (1991) Capacidad de colonizacio´n de Rumex acetosella L. (vinagrillo) en comunidades perturbadas. Anales del Instituto de la Patagonia Serie Ciencias Naturales, 20, 61–67. Egerton-Warburton L.M. (1998) A smoke-induced alteration of the sub-testa cuticle in seeds of the post-fire recruiter, Emmenanthe penduliflora Benth. Journal of Experimental Botany, 49, 1317–1327. Ezcurra C., Brion C. (2005) Plantas del Nahuel Huapi. Cata´logo de la Flora Vascular del Parque Nacional Nahuel Huapi, Bariloche, Argentina. Ferrandis P., Herranz J.M., Martinez-Sa´nchez J.J. (1999) Fire impact on a maquis soil seed bank in Caban˜eros National Park (Central Spain). Israel Journal of Plant Sciences, 47, 17–26. Fonda R.W. (1974) Forest succession in relation to river terrace development in Olympic National Park, Washington. Ecology, 55, 927–942. Franzese J., Ghermandi L., Bran D. (2009) Postfire shrub recruitment in a semi-arid grassland: the role of microsites. Journal of Vegetation Science, 20, 251–259. Gasque M., Garcı´a-Fayos P. (2003) Seed dormancy and longevity in Stipa tenacissima L. (Poaceae). Plant Ecology, 168, 279– 290. Ghermandi L. (1992) Caracterizacio´n del banco de semillas de una estepa en el noroeste de Patagonia. Ecologı´a Austral, 2, 39–46. Ghermandi L. (1997) Seasonal patterns in the seed bank of a grassland in north-western Patagonia. Journal of Arid Environments, 35, 215–224. Ghermandi G., Gonzalez S. (2009) Diversity and functional group gap dynamics affected by drought and fire in Patagonia grasslands. Ecoscience, 16, 408–417. Ghermandi L., Guthmann N., Bran D. (2004) Early post-fire succession in Northwestern Patagonia grasslands. Journal of Vegetation Science, 15, 67–76. Gilbert G.S., Harms K.E., Hamill D.N., Hubbell S.P. (2001) Effects of seedling size, El Nin˜o drought, seedling density, and distance to nearest conspecific adult on 6-year survival of Ocotea whitei seedlings in Panama´. Oecologia, 127, 509–516. Gobbi M., Puntieri J., Calvelo S. (1995) Post-fire recovery and invasion by alien plant species in a South American woodland–steppe ecotone. In: Pysˇek P., Prach K., Rejma´nek M., Wade M. (Eds), Plant invasions: general aspects and special problems. SPB Academic Publishing, Amsterdam, The Netherlands, pp 105–115. Gonzalez S., Ghermandi L. (2008) Postfire seed bank dynamics in semiarid grasslands. Plant Ecology, 199, 175–185. Gonzalez S., Franzese J., Ghermandi L. (2010) Role of fire on Patagonian grasslands: changes in aboveground vegetation and soil seed bank. In: Heider M., Mu¨ller T. (Eds), Advances in environmental research. Nova Science Publishers, New York, USA, pp 243–264. Gonza´lez-Rabanal F., Casal M. (1995) Effect of high temperatures and ash on germination of ten species from gorse shrubland. Vegetatio, 116, 123–131. Granstro¨m A. (1987) Seed viability of fourteen species during five years of storage in a forest soil. Journal of Ecology, 75, 321–331.
Plant Biology 13 (2011) 865–871 ª 2011 German Botanical Society and The Royal Botanical Society of the Netherlands
Franzese & Ghermandi
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Plant Biology 13 (2011) 865–871 ª 2011 German Botanical Society and The Royal Botanical Society of the Netherlands
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