Lichens are more tolerant against winter warming stress than vascular and non-vascular plants: Insights from an alpine field experiment

Abstract

1 INTRODUCTION

Arctic and alpine areas warm at an amplified rate and winters are changing faster than summers (AMAP, 2021; Landrum & Holland, 2020). Changes in the frequency and characteristics of climatic extremes are important for vegetation, altering carbon dynamics, species composition and overall ecosystem function faster than long-term temperature changes (Bokhorst et al., 2015; Gaines & Denny, 1993; Jentsch et al., 2007). The stimulating response of vegetation to warmer and longer summers may even be reversed or opposed by the effects of extreme weather events (Berner et al., 2020; Callaghan et al., 2022; Panchen et al., 2022).

Winter warming events are short-lived climatic events, from hours to several days, where temperatures are unseasonably high (Johansson et al., 2011; Pascual & Johansson, 2022). Such events are often accompanied by winter rain, which have been found to be increasing in parts of Norway, mostly in the southwest high elevations, central mountains and northern Norway (Pall et al., 2019). This is consistent with combined effects of increased precipitation and more precipitation falling as rain in a warming climate. Moreover, warm winter events are among the most impactful extreme events for arctic-alpine ecosystems (Coulson et al., 2000; Treharne et al., 2019). The term winter warming event is here used to describe winter climatic events of up to 1 week where temperatures cross the 0°C threshold.

Winter warming events induce vegetation stress through two main physical processes, although they often coincide: thaw–freeze and ice encasement. Thaw–freeze relates to snow melt and thawing of vegetation during the winter warming event, followed by vegetation refreeze after the winter warming event ends. Melting of the insulating snow layer exposes the vegetation to warm temperatures and can reduce winter dormancy and cold-hardiness, with the risk of freeze damage and frost drought when cold temperatures return (Bokhorst et al., 2011; Rixen et al., 2022). Ice encasement occurs when freezing of rain and meltwater accumulated during winter warming events encase vegetation in ice. This reduces the cells' gas exchange with the ambient air and can lead to accumulation of carbon dioxide (CO₂), lactic acid and ethanol (Andrews, 1996). The ability and adaption to survive in anoxic conditions during ice encasement differ between species and may deviate from the species' tolerance to thaw–freeze (Bjerke, Elvebakk, et al., 2018; Crawford et al., 1994).

The effects of winter warming events on vascular plants that rely on an insulating snow cover in winter have been thoroughly investigated; their responses differ between species and phenological strategies (Bokhorst et al., 2018) and life stages (Ósvaldsson et al., 2022), and can shift ecosystem carbon balance from a carbon sink to a source (Treharne et al., 2019). However, less is known about how winter warming events impact non-vascular photoautotrophs (NVPs), that is lichens, bryophytes, and free-living algae and cyanobacteria, even though they are crucial for biodiversity, carbon cycling and nitrogen fluxes of arctic-alpine ecosystems (Porada et al., 2023; Street et al., 2013). With no root system or vascular tissue, NVPs rapidly adapt their metabolic activity to fluctuations in water availability and environmental conditions (Lange et al., 2001). This plasticity can be beneficial during rapid temperature change and allows for higher resilience against winter stress than the more seasonally driven vascular plants (Bokhorst et al., 2023; Lenné et al., 2010). Activity increase and associated loss of winter hardiness during the event appear to be decisive for the stress response (Bokhorst et al., 2018). We anticipate considerable variation in tolerance to winter stress among lichens and bryophyte species due to their diverse strategies and functional traits (Asplund et al., 2021). For example, the annual growth of lichens with no distinct phenological stages can be advantageous during winter warming events, as opposed to bryophytes that develop new shoot apices that may be vulnerable to freeze damage if growth is activated (Bjerke et al., 2011).

With increased frequency and severity of winter warming events, vegetation on the already snow limited ridges may be more exposed to cold winter temperatures (Niittynen et al., 2020). How resilient ridge vegetation is to extreme events is still uncertain, particularly for vegetation dominated by lichens and other NVPs. Considering recent declines in lichen ground cover (Chagnon & Boudreau, 2019; Fraser et al., 2014; Vanneste et al., 2017), a deeper understanding of the role of winter warming events is crucial in predicting the future of these ecosystems. Through a field experiment, we evaluate how the stress from thaw–freeze and ice encasement may affect summertime ecophysiology of widespread alpine vascular plants, lichens, and bryophytes.

Based on our current knowledge on winter warming events and reported ecosystem responses, we hypothesize that:

1. Winter warming events causing thaw–freeze or ice encasement are stressful to alpine heath and ridge vegetation, manifesting as reduced ecophysiological activity and growth in the following summer.
2. Thaw–freeze is more detrimental to vegetation than ice encasement because of increased reactivation during the event and increased freezing stress after the event.
3. Lichens are more tolerant than bryophytes and vascular plants against the stress from thaw–freeze and ice encasement.