Elsevier

Acta Oecologica

Volume 38, January 2012, Pages 1-7
Acta Oecologica

Original article
Adaptation to boreal forest wildfire in herbs: Responses to post-fire environmental cues in two Pulsatilla species

https://doi.org/10.1016/j.actao.2011.08.002Get rights and content

Abstract

Although boreal forests are biomes which are characterized by periodical forest wildfires, very little is known about adaptations to fire in forest herbs. We investigated whether a putatively fire-dependent herbaceous species – Pulsatilla patens – demonstrated adaptive responses to environmental cues that reflect differences in pre-fire and post-fire environments (the presence of ericoid litter and charcoal, and light levels). For comparison, we included in the experiment a close congeneric species that is less bound to forest ecosystems (Pulsatilla pratensis) and a morphologically similar mesic grassland species from the same family (Ranunculus polyanthemos), as examples of species for which adaptations to fire should be of lower value, or of no value at all, respectively. The addition of ericoid litter to the soil generally enhanced plant growth, suggesting that its negative effect on plant germination and growth is not as widespread as previously thought. In both Pulsatilla species charcoal without forest litter retarded plant growth, but in combination with ericoid litter the negative effect disappeared or was even replaced by a slightly positive effect. Such an interactive effect was absent in the grassland species R. polyanthemos. The response of Pulsatilla species to different post-fire signals may be explained by adaptive down-regulation of growth after high-intensity fire – small plant size can be advantageous in sparse and well illuminated field-layer vegetation – and intense growth in the more competitive situation following weak fire. An additional experiment demonstrated that the effects of fire-related treatments were not mediated by differential AM infection.

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)

  • D.H. Brown et al.

    Bryophytes and nutrient cycling

    Bot. J. Linn. Soc.

    (1990)
  • E. Castells et al.

    Effects of plant leachates from four boreal understorey species on soil N mineralization, and white spruce (Picea glauca) germination and seedling growth

    Ann. Bot.

    (2005)
  • G. Certini

    Effects of fire on properties of forest soils: a review

    Oecologia

    (2005)
  • F.S. Chapin et al.

    The role of mosses in the phosphorus cycling of an Alaskan black spruce forest

    Oecologia

    (1987)
  • J.R. Ellis et al.

    Drought resistance of wheat plants inoculation with VA mycorrhizas

    Plant Soil

    (1985)
  • O. Engelmark

    Forest fires in the Muddus National Park (northern Sweden) during the past 600 years

    Can. J. Bot.

    (1984)
  • O. Engelmark

    Boreal forest disturbances

  • P.A. Esseen et al.

    Boreal forests – the focal habitats of Fennoscandia

  • W.L. Fineblum et al.

    Tradeoff between resistance and tolerance to herbivore damage in a morning glory

    Nature

    (1995)
  • A. Granström et al.

    Heat effects on seeds and rhizomes of a selection of boreal forest plants and potential reaction to fire

    Oecologia

    (1993)
  • W. Huang et al.

    Resource allocation to defence and growth are driven by different responses to generalist and specialist herbivory in an invasive plant

    J. Ecol.

    (2010)
  • E. Hultén et al.

    Atlas of North European Vascular Plants. North of the Tropic of Cancer

    (1986)
  • A. Jäderlund et al.

    Interference of Vaccinium myrtillus on establishment, growth, and nutrition of Picea abies seedlings in a northern boreal site

    Can. J. For. Res.

    (1997)
  • G.D. Joanisse et al.

    Soil enzyme inhibition by condensed litter tannins may drive ecosystem structure and processes: the case of Kalmia angustifolia

    New Phytol.

    (2007)
  • E.A. Johnson et al.

    Wildfire regime in the boreal forest and the idea of suppression and fuel buildup

    Conserv. Biol.

    (2001)
  • O. Jonsson et al.

    Operation of dichogamy and herkogamy in five taxa of Pulsatilla

    Holarctic Ecol.

    (1991)
  • R. Kalamees et al.

    The effects of fire and stand age on seedling establishment of Pulsatilla patens in a pine-dominated boreal forest

    Can. J. Bot.

    (2005)
  • M. Kalliovirta et al.

    Population structure of a threatened plant, Pulsatilla patens, in boreal forests: modelling relationships to overgrowth and site closure

    Biodivers. Conserv.

    (2006)
  • R.E. Koske et al.

    A modified procedure for staining roots to detect VA mycorrhizas

    Mycol. Res.

    (1989)
  • T. Kuuluvainen

    Disturbance dynamics in boreal forests: defining the ecological basis of restoration and management of biodiversity

    Silva Fenn.

    (2002)
  • Cited by (0)

    View full text