Research Paper _ revised versionLeafy season length is reduced by a prolonged soil water deficit but not by repeated defoliation in beech trees (Fagus sylvatica L.): comparison of response among regional populations grown in a common garden
Introduction
Phenology describes the timing of recurrent biological events in response to seasonal variations in climate. Phenology is one of the plant traits where responses to climate change are the most visible (Menzel et al., 2006). Since 1950, shifts in phenology have been observed and used as evidence of global warming (Menzel and Fabian, 1999; Menzel, 2000; Sparks et al., 2000; Peñuelas et al., 2002; Menzel et al., 2020). For instance, in vineyards, historical recordings of harvest dates helped to detect changing temperatures over several centuries (Chuine et al., 2004).
Leaf phenology events such as bud-burst (BB) and leaf senescence are particularly important in deciduous forest trees because they determine the length of the leafy season and consequently the duration of new carbon production by assimilation that is essential for biomass production (Richardson et al., 2010). The leaf phenology of perennial plants is expected to optimize their carbon gain (Manzoni et al., 2015; Vico et al., 2015) and water uptake (Zapater et al., 2013). Leaf senescence implies nutrient resorption from leaves to perennial organs. It usually happens before autumn frosts and nutrient resorption efficiency affects leaf production during the following year (Estiarte and Peñuelas, 2015).
In the two last decades, numerous experimental and modelling approaches have been developed to understand the drivers of leaf phenology and its variations with climate (Cooke et al., 2012). Leaf phenology is strongly controlled by local temperature (Hunter and Lechowicz, 1992; Peaucelle et al., 2019). To summarize, in temperate tree species, BB results from the succession of two phases: i) breaking endodormancy by the fulfilment of chilling temperature requirements and ii) the accumulation of warm temperatures (forcing temperature) during the ecodormancy phase (Lang et al., 1987). The temperature requirements during the two phases are species-specific (Kramer, 1995; Chuine and Cour, 1999; Morin et al., 2009; Vitasse et al., 2009a; Basler and Körner, 2014; Schuster et al., 2014; Zohner and Renner, 2014; Dantec et al., 2014; Laube et al., 2014; Fu et al., 2015). Moreover, in some tree species like beech, photoperiod may also interact with temperature to determine bud-burst date, though the mechanisms of this interaction remain unclear (Heide, 1993; Partanen et al., 1999; Körner and Basler, 2010; Vitasse and Basler, 2013; Basler and Körner, 2014; Laube et al., 2014; Hamilton et al., 2016; Fu et al., 2019b). Day-length may interact negatively with heat requirements during ecodormancy to avoid that BB occurred too late (if abnormally cold spring) or too early (if warm spring) (Fu et al., 2019b).
The role of climate as a driver of leaf senescence (i.e. yellowing and shedding) is less well understood than that of spring phenology (Richardson et al., 2013). Long-term investigations on the links between leaf-senescence and air temperature have sometimes revealed a delay in leaf senescence in response to global warming, sometimes an advance, and sometimes no effect at all (Peñuelas et al., 2002; Menzel et al., 2006; Morin et al., 2009). A recent meta-analysis showed that leaf senescence seemed to be particularly dependent on October temperatures, a warmer autumn leading to delayed senescence (Gill et al., 2015). Several models have been designed to predict leaf-yellowing or leaf-shedding while considering both temperature and photoperiod (Delpierre et al., 2009), or only temperature (Richardson et al., 2006; Keenan and Richardson, 2015) but more complex interactions among factors, including soil water availability should be integrated for accurate predictions (Xie et al., 2018; Liu et al., 2019). Furthermore, leaf senescence may also affect spring bud-burst timing the following year (Nielsen and Jorgensen, 2003; Heide, 2003), and BB timing could impact the leaf senescence timing of the current year (Fu et al., 2014; Keenan and Richardson, 2015).
Extreme drought events occurred more frequently in Europe in the last decades (e.g.1976, 2003, 2018, and 2019) and their frequency and severity are projected to increase under future climate scenarios (IPCC 2014). Experiments that directly evaluate the effects of soil water deficit on leaf phenology are scarce and present contrasted results. Leaf unfolding responses to rainfall seem to be positive, i.e. a later unfolding date with higher water availability (Peñuelas et al. 2004; Adams et al., 2015). Ogaya and Peñuelas (2004) showed that a 15% reduction in soil water availability induced by a rainfall exclusion system, delayed all the phenophases in Arbutus Toledo but not in Quercus ilex or in Phillyrea latifolia. Another more drastic rainfall exclusion experiment reducing rainfall by 50% in autumn showed no impact on leaf development the following spring for Quercus ilex whereas a 58% reduction in rainfall during spring led to severe aborting of buds (Misson et al., 2011). How soil water deficits interact with warm temperature in leaf senescence is complex; the two parameters have yet to be disentangled (Estiarte and Peñuelas, 2015; Liu et al., 2019). Escudero and Del Arco (1987) showed that soil water deficit induced earlier leaf fall, but Pallardy and Loewenstein (2004) observed that this response was species dependent. Estrella and Menzel (2006) also observed advanced leaf senescence during autumn drought, though leaf yellowing date may be dependent on climatic drivers occurring not only during autumn but also throughout the leafy season (Liu et al., 2019).
During the growing season, a prolonged soil water deficit limits water and carbon uptake by trees (Cowan, 1982; Farquhar and Sharkey, 1982) and slows down nutrients uptake and phloem transports (Sevanto, 2014; Dannoura et al., 2019). The question remains, however, whether these modifications affect leaf phenology. Indeed, in spring, for the establishment of new organs, deciduous trees use carbon reserves (Barbaroux and Bréda 2002; Hoch et al., 2003; Gilson et al., 2014) and nutrient reserves (El Zein et al., 2011a; Bazot et al., 2016) and need water to remobilize these reserves towards the sink organs (i.e, buds and leaves). During leaf senescence, nutrients are resorbed from the leaves towards perennial organs, and this also implies important fluxes (Estiarte and Penuelas, 2015) which may be disrupted by severe soil water deficits.
Finally, phenology is also controlled by complex interactions between genetic and environmental factors. Indeed, studies on beech species have shown differences in leaf phenology among populations from a large climatic gradient within the distribution area of species (Von Wuelish et al., 1995; Zohner and Renner, 2014; Harter et al., 2015; Schueler and Liesebach, 2015; Kramer et al., 2017) or along altitudinal clines (Vitasse et al., 2009a; Vitasse et al., 2009b). These results suggest that leaf phenology in beech trees is adapted to large variations in climatic conditions, and this capacity could help populations to cope with climate change. However, the phenotypic plasticity and adaptive capacity of populations at a regional scale within a small climatic range have rarely been investigated. Moreover, it is important to study to what extent this adaptation could be challenged by recurrent extreme events, like droughts.
In the present study, we used a common garden experiment to investigate the variability of leaf phenology among regional beech (Fagus sylvatica L.) populations along a small latitudinal gradient of 140 km in lowlands located in the central area of the European beech distribution range (North-eastern France). We also compared the response of these populations to repeated soil water deficit or defoliation events. Our main aim was to assess whether or not leaf phenology would be modified by disturbances i) in tree water status and/or ii) in tree carbon and nitrogen status. For three years, these statuses were experimentally modified by provoking recurrent prolonged soil water deficits in a rain exclusion system or annually repeated defoliation. In response to these constraints, carbon assimilation was reduced either by stomatal closure under soil water deficit or by reducing leaf area under defoliation. We examined the impact of these constraints on the mean tree BB and LY, on the length of growing season (GS) and on leaf unfolding and leaf yellowing dynamics. We analyzed these traits in the offspring of six regional beech populations. We addressed three questions: (1) Do three years of soil water deficit and defoliation modify budburst and leaf-yellowing days and dynamics in beech trees? (2) How does leaf phenology vary among regional populations? (3) Do prolonged soil water deficits and repeated defoliation modify leaf phenology similarly in all regional populations?
Section snippets
Study site, plant material and treatments
In October 2006, beechnuts from Fagus sylvatica L. trees were collected on the ground in six forests in Lorraine (North-eastern France) along a latitudinal gradient of 140 km (Fig. 1). For each forest, seed collection was conducted in plots of at least 0.5 ha, which included at least 20 mother trees with at least 120 seeds on the ground (E Silva, 2010). All the beechnuts collected in a forest were combined in order to constitute a population. After being rehydrated to a water content of 30-34%
Bud-burst and leaf-yellowing responses to soil water deficit and defoliation
The trees in the control and defoliation treatments were irrigated and REW was maintained above a 40% threshold (Fig. 2). In the MWD treatment, REW was maintained below 40% from June 2014 until June 2016, with a minimum of 12% at the end of the 2014 and 2015 summers. In 2016, a very rainy spring caused a rise in groundwater and a transitory increase in REW in this treatment, which exceeded 40% between DOY160 and DOY220. In the SWD treatment, REW was maintained below 40% all the three years with
Annual variability of leaf phenology in beech trees
Over the three years of our experiment, for the beech trees in the control treatment, the maximal inter-annual variability in bud-burst date was 14 days. LY seems to play an important role on the GS length in beech trees since GS was more strongly dependent on LY than on BB. This was also observed by Vitasse et al. (2009a) on beech populations along an altitudinal gradient. Consequently, LY date variability could significantly impact the annual carbon balance in beech trees.
Conclusion
Our study suggests that beech trees present a local variation of leaf phenology, even within a small latitudinal gradient, and that different populations have different phenological response to soil water deficit. The impact of drought on both bud-burst and leaf yellowing dates leads to a shorter growing season and suggests that soil water content should be taken into account more often in studies of inter-annual phenological variability, particularly in the context of future climate change
Declaration of Competing Interest
None.
Acknowledgements
The authors thank Thierry Paul for the overseeing of the tree planting and roof construction. The authors thank Fabrice Bonne and the Master's students (Mylène Hardy, Hakima Ammour, Marie Doron and Sirine Rommani) who helped to the phenology measurements. The authors also warmly thank i) the middle-school students and their teachers (Collège Duvivier in Einville-au-Jard) invested in the Survivors mediation project supported by Labex ARBRE, and the CPIE (Centre Permanent d'Initiatives pour
Funding
The experiment and operating costs were funded by the French National Research Agency (ANR), (“Investissements d'Avenir” program [ANR-11-LABX-0002-01, Laboratory of Excellence ARBRE] within the framework of the Mepib-Death multidisciplinary project) and the Lorraine Region Project [Survival, contract n°12000453]. PA Chuste received a PhD grant from the Laboratory of Excellence ARBRE.
Data accessibility
The data are available from the authors upon request.
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