Microclimatic variation regulates seed germination phenology in alpine plant communities

Abstract

1 INTRODUCTION

Plant phenology describes the cyclical patterns of growth and developmental phases (Hopp, 1974) which are responsive to climate change (Scranton & Amarasekare, 2017). In seasonal climates, plant reproductive strategies and phenology have strong implications for species fitness, which in turn affect community composition (Donohue, 2005; Poschlod et al., 2013). Studies focusing on reproductive phenology have centred on flowering time, seed maturation and dispersal onset, describing a fast-slow continuum of reproductive phenology (Segrestin et al., 2018, 2020). Comparatively few studies have focused on germination phenology, despite being a sensitive and irreversible process fundamental for regeneration (Baskin & Baskin, 2014). Early season germination can benefit individuals with longer growing seasons (Donohue et al., 2010) and give a competitive edge in the use of limited resources versus individuals germinating later (Verdú & Traveset, 2005). However, early germination also involves higher mortality risks (Thomson et al., 2017) due to warm spells or frost events compared to a more conservative strategy of delayed germination (ten Brink et al., 2020). Germination phenology is therefore a key trait for regeneration, influencing population and community dynamics in response to environmental changes (Huang et al., 2016; Kimball et al., 2011; Levine et al., 2011). Common adaptations to regulate germination phenology include bet-hedging strategies that spread mortality risk with several germination pulses (Simons, 2011); responses to environmental cues that trigger germination under a certain amount of temperature, moisture or light (Baskin & Baskin, 2014; Donohue et al., 2010); or a combination of both (Graham et al., 2014).

Germination phenology has been studied in annual species from unpredictable water-dependent communities (Gremer & Venable, 2014; Kimball et al., 2011; ten Brink et al., 2020; Thomson et al., 2017), but environmental regulation of germination phenology is also expected in other systems influenced by seasonality and climate change (Walck et al., 2011). One important example is found in alpine and arctic ecosystems, where seed production and germination are strongly influenced by microclimatic conditions (Mondoni et al., 2022). Alpine areas are characterized by short growing seasons and display changing climatic conditions at different spatial scales (Körner, 2021). Under these circumstances, germination phenology is of vital importance to match favourable conditions and to prevent unsuitable winter climate during seed regeneration (Gremer et al., 2020). The global ‘alpine germination syndrome’ has been characterized by a general requirement of cold-wet stratification followed by warm temperatures (Fernández-Pascual et al., 2021). This cold-wet stratification has dormancy-alleviating properties and it is assumed to happen under snow, which additionally provides thermal insulation from freeze–thaw winter events (Decker et al., 2003). Post-winter germination has been strongly influenced in snow manipulation experiments (Drescher, 2014; Drescher & Thomas, 2013) possibly because with no snow protection, temperatures drop below zero and the development of freezing tolerance has a potential fitness cost for species (Agrawal et al., 2004). In high-elevation areas with Mediterranean-like climates, species may follow a ‘Mediterranean germination syndrome’ in which seeds germinate immediately after dispersal if water is available, but also show enhanced germination with cold-wet stratification and relatively high temperatures (Giménez-Benavides et al., 2005; Giménez-Benavides et al., 2018). Despite these general syndromes, germination strategies are known to vary in response to local elevation gradients (Fernández-Pascual et al., 2017), light exposures (Wagner & Simons, 2009), bedrock type (Tudela-Isanta, Fernández-Pascual, et al., 2018; Tudela-Isanta, Ladouceur, et al., 2018) or successional stages, for example in glacier forelands (Schwienbacher et al., 2012).

At the local scale, the topographic heterogeneity of alpine landscapes translates into a mosaic of microclimatic conditions (Jiménez-Alfaro et al., 2024; Scherrer & Körner, 2011) with sharp temperature and snow-melting gradients (Körner, 2021) even within a few centimetres (Graham et al., 2012). The impact of microclimatic variation on germination phenology is expected to be strong, but the few studies that have considered this have shown contrasting results. By comparing germination patterns between alpine snowbed specialists (sheltered areas with snow accumulation, short growing season but low risk of frost and no water shortage) and fellfields (exposed areas where wind reduces the accumulation of snow resulting in soil freezing, frost damage and drought); Shimono and Kudo (2005) found no differences in the response of 27 alpine species to temperature and light in Japan. In contrast, Rosbakh et al. (2022) found different germination responses to temperature among 72 species along a snowmelt gradient in the Caucasus. This suggests that germination patterns in alpine landscapes may differ in systems representing different ecological gradients or regional features (e.g. ecological, or evolutionary history). Nevertheless, germination experiments are limited by fixed temperature conditions commonly used in incubation chambers (e.g. 12-h cycles of 20/10 and 15/5°C), which are decoupled from the continuous temperature cycles occurring in nature. To draw more robust conclusions about germination strategies in alpine areas, we need detailed climatic data (Shimono & Kudo, 2005) and accurate experimental settings mirroring real field conditions in the best possible way (Hoyle et al., 2015).

In this study, we investigate germination phenology of 54 alpine species influenced by either temperate or Mediterranean macroclimatic conditions within the same ecoregion. Our main aim was to understand how microclimatic variation affects germination phenology and the potential implications of such responses to plant regeneration in alpine communities. By conducting a continuous seasonal experiment in the laboratory, using temperature data series measured in the field, our experimental approach focused on mimicking two contrasting microclimatic regimes: (i) fellfield conditions occurring in open and exposed areas subjected to wind, freeze and thaw cycles without snow protection, with warmer and longer growing seasons; and (ii) snowbed conditions in areas with dense plant cover, long snow cover and cooler and shorter growing seasons. We complemented the laboratory data with field sowing experiments for a subset of species. First, we asked at what extent contrasting microclimatic regimes modify germination phenology. We hypothesized that fellfield conditions will result in higher total germination due to a longer growing season, earlier germination due to higher temperatures, and lower or no germination during winter due to below freezing temperatures. In contrast, the snowbed conditions will show lower total germination due to shorter growing season, delayed germination due to lower temperatures, and germination under winter (snow-covered) conditions due to temperature not dropping below 0°C. Second, we ask whether alpine species from temperate and Mediterranean climates show similar phenological responses. We hypothesized that species from the temperate community will germinate better after cold stratification and under warmer temperatures, in concordance with the global ‘alpine germination syndrome’ while the species from the Mediterranean community will germinate mainly in autumn and at warmer temperatures, following the ‘Mediterranean germination syndrome’. However, it is unclear whether the individual responses of alpine species will follow these syndromes homogenously, and whether germination phenology tested in the field will align with the results obtained in the laboratory.