Original articleAdaptation to boreal forest wildfire in herbs: Responses to post-fire environmental cues in two Pulsatilla species
Highlights
► Pulsatilla species demonstrated complex responses to post-fire environmental cues. ► There were no interactive effects of post-fire cues in non-fire-related Ranunculus. ► Possible adaptive down-regulation of growth after high-intensity fire is discussed.
Introduction
Human-induced changes to long-term disturbance regimes may constitute a major threat to the persistence of ecosystems where taxa have evolved to cope with and benefit from natural disturbance events. Boreal and hemiboreal forests are biomes where regular severe disturbance has been an important evolutionary process affecting many species (Shafi and Yarranton, 1973, Kuuluvainen, 2002, Reier et al., 2005, Kalliovirta et al., 2006). Among these are certain herbaceous plants that are believed to rely on periodic forest wildfire for seed germination and seedling establishment (Granström and Schimmel, 1993, Uotila, 1996, Kalamees et al., 2005, Ruokolainen and Salo, 2006, Risberg and Granström, 2009). For such species, contemporary forest management practices may be detrimental and could even bring about an increased risk of extinction. Before active fire prevention and suppression began in the mid-19th century, natural fires started by lightning strikes occurred with an average interval of 50–150 years, depending on soil properties, topography, forest age, and human impact (Zackrisson, 1977, Engelmark, 1984, Wallenius et al., 2004, Olsson et al., 2010). Nowadays, human intervention has significantly reduced the area of forest that is burned annually and lengthened the fire interval throughout the boreal zone (Johnson et al., 2001, Ward et al., 2001, Axelsson et al., 2002, Uotila and Kouki, 2005).
In boreal forests dominant ericaceous vegetation and mosses can negatively influence the establishment of certain vascular plants, with stagnant growth of seedlings often observed in the presence of ericaceous undergrowth (Pellissier, 1993, Thiffault et al., 2004, Nilsson and Wardle, 2005, LeBel et al., 2008). Various mechanisms including allelopathic interference (Mallik, 2003, Mallik, 2008), reduced soil N mineralisation (Nilsson and Zackrisson, 1992, Zackrisson et al., 1996, Castells et al., 2005), soil enzyme inhibition (Joanisse et al., 2007) and direct resource competition (Jäderlund et al., 1997, Mallik and Prescott, 2001) have been put forward to explain this phenomenon. Moreover, several studies have highlighted the importance of polyphenol-rich ericoid humus. Polyphenols form stable complexes with protein, thereby reducing soil N mineralisation and retarding nutrient cycling and the growth of tree seedlings (Ponge et al., 1998, Wardle et al., 1998, Hättenschwiler and Vitousek, 2000). In addition, feathermosses (such as Hylocomium splendens and Pleurozium schreberi) which are able to efficiently uptake nutrients from precipitation, throughfall and litter decomposing on the surface of mosses (Brown and Bates, 1990, Longton, 1992), can prevent the leaching of nutrients to lower soil horizons and can form a barrier between seedlings and the mineral soil (Chapin et al., 1987, Steijlen et al., 1995, Zackrisson et al., 1997, LePage et al., 2000).
Hence, one of the most pronounced effect of forest wildfire on field-layer vegetation is through the destruction of the moss and litter layer, which can considerably enhance the recruitment of forest herbs as a result (Schimmel and Granström, 1996). Nonetheless, forest fire has several other consequences that might also enhance the recruitment of fire-adapted boreal forest herbs (Skre et al., 1998, Schimmel and Granström, 1996, Engelmark, 1999). The detoxifying and rejuvenating effect of fire may be due in part to the effect of charcoal, which is capable of absorbing secondary metabolites such as the humus polyphenols produced by ericaceous vegetation (Zackrisson et al., 1996, Wardle et al., 1998, Nilsson and Wardle, 2005). Light conditions for herbaceous plants improve considerably after fire (Uotila, 1996, Engelmark, 1999, Kalamees et al., 2005) and various soil properties are also affected, including increased decomposition of plant litter and humus, cation availability, pH and soil microbial activity, and enhanced cycling of nitrogen (Wardle et al., 1998, Certini, 2005).
Pulsatilla patens (L.) Mill. (Eastern Pasque Flower, synonym Anemone patens L., Ranunculaceae) is a boreal herbaceous plant species that may be dependent on a periodic fire regime (Uotila, 1969, Esseen et al., 1992). While there is no firm evidence that P. patens is strictly fire-dependent, the species can survive extensive forest fires (Uotila, 1996), and prescribed burning has been shown to enhance its germination and establishment (Kalamees et al., 2005).
Among the multitude of ecological factors connected with forest fire, it is unclear which play a key role in the recruitment of boreal herbs in general and, more specifically, of P. patens. It is also unclear whether plants require specific adaptations in order to benefit from aspects of wildfire. An alternative scenario is that any herbaceous perennial plant that is suppressed by ericoid litter and moss might benefit from the effect of fire. To answer these questions, we designed an experiment including P. patens and two other herbaceous species: Pulsatilla pratensis and Ranunculus polyanthemos. P. pratensis is taxonomically and ecologically close to P. patens but is known to prefer grasslands and is rarely found growing in wooded habitats. Thus, it is reasonable to expect that this species should not demonstrate specific adaptations to post-fire conditions. R. polyanthemos belongs to the same family as the Pulsatilla species and is morpologically similar to them, but it grows in moist grasslands where specific adaptations to wildfire should not enhance fitness in any way.
In this study, we focussed on possible adaptations of herbaceous plants to three aspects of the environment that are influenced by recent forest wildfire: the amount of ericoid litter on the forest floor, the presence of charcoal and the light climate. We did not address fire survival strategies in our experiment since adaptations for surviving high temperatures and other direct physical impacts of wildfire are highly specific (Rowe, 1983, Wahid et al., 2007) and would have demanded an entirely different experimental design. We used a factorial design to determine (i) whether the presence of ericoid litter in boreal forest soil has a direct negative impact on the germination and growth of P. patens (and the two other species included for comparison); and (ii) whether post-fire accumulation of charcoal mitigates the effect of ericoid litter. Since improvement of light conditions may also play an important role in the complex effect of forest fire on herbs, we included lighting treatments as an additional factor in the experiment.
Specifically, we tested the following working hypotheses:
- 1)
If P. patens, a species inhabiting boreal forests, is fire-adapted and able to respond to environmental cues in a post-fire situation, it will exhibit responses to the presence of both ericoid litter and charcoal in the soil; responses will be less pronounced in the more grassland-bound congener, P. pratensis, and absent in the purely grassland species, R. polyanthemos.
- 2)
Since acquisition of photosynthetically active radiation (PAR) is more closely related to herbaceous neighbours in P. pratensis and R. polyanthemos than in P. patens, the former species will show greater plasticity in root–shoot allocation and elongation in their response to shading.
Section snippets
Study species
P. patens is about 8–30 cm high, long-lived perennial herb with a deep taproot and a vertical, branched rhizome. Its leaf rosettes emerge in early spring after anthesis through growth of lateral buds on the rhizome before withering in autumn (Jonsson et al., 1991). It grows in the dry forests and steppe of the eastern hemisphere, from eastern Europe to central Siberia (Hultén and Fries, 1986, Jalas and Suominen, 1989). Several small isolated populations in central Europe and northwestern Europe
Results
The effects of experimental treatments on plant biomass and shoot morphology are shown in Table 1. The addition of ericoid litter had a clear positive effect in all species, and plants grew larger in well illuminated conditions, though in P. pratensis this effect was not significant. There was a significant interactive effect of charcoal and litter treatments on the biomass of both Pulsatilla species – when charcoal was added without simultaneous litter addition, it had a detrimental effect on
Discussion
The first conspicuous and somewhat surprising result of the experiment was the clear and significant positive effect of adding ericoid litter to the soil. Polyphenol-rich ericoid litter and humus has been considered toxic for herbs and has been shown to inhibit the germination and growth of vascular plants (Zackrisson and Nilsson, 1992, Ponge et al., 1998, Wardle et al., 1998, Hättenschwiler and Vitousek, 2000). In our experiment, it was evident that the positive effect of litter addition,
Acknowledgements
We thank Gea Kiudorf for her technical assistance during the additional experiment, John Davison and Marina Semchenko for comments on the manuscript and for linguistic advice. This study was financed by the Estonian Science Foundation (grants 6229, 7576 and 8039) and the University of Tartu (grant 0119).
References (63)
- et al.
The role of polyphenols in terrestrial ecosystem nutrient cycling
Trends Ecol. Evol.
(2000) - et al.
Kalmia removal increases nutrient supply and growth of black spruce seedlings: an effect fertilizer cannot emulate
For. Ecol. Manage.
(2008) - et al.
A continuous record of fire covering the last 10,500 calendar years from southern Sweden – the role of climate and human activities
Palaeogeogr. Palaeoclimatol. Palaeoecol.
(2010) - et al.
Methods for studying vesicular–arbuscular mycorrhizal root colonization and related root physical properties
- et al.
The effect of timing of forest fire on phenology and seed production in the fire-dependent herbs Geranium bohemicum and G. lanuginosum in Sweden
For. Ecol. Manage.
(2009) - et al.
Population structure and population dynamic of Pulsatilla patens (L.) Mill. in relation to vegetation characteristics
Flora
(2006) - et al.
Understorey vegetation in spruce-dominated forests in eastern Finland and Russian Karelia: successional patterns after anthropogenic and natural disturbances
For. Ecol. Manage.
(2005) - et al.
Comparative water relations and photosynthesis of mycorrhizal and nonmycorrhizal Bouteloua gracilis H. B. K. Lag ex stead
New Phytol.
(1981) - et al.
Changes in mixed deciduous forests of boreal Sweden 1866–1999 based on interpretation of historical records
Landsc. Ecol.
(2002) - et al.
Reproductive biology of Pulsatilla patens (Ranunculaceae)
Am. Midl. Nat.
(1975)