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

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

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