Untangling winter chilling and spring forcing effects on spring phenology of subtropical tree seedlings

Highlights

• Temperature effect was experimentally tested on the spring phenology of five subtropical trees.

• Survival of deciduous trees was not affected by reduced chilling conditions.

• Longer chilling reduced day count and heat requirement for budburst and leaf-out.

• Species order in budburst and leaf-out changed under varying chilling and forcing mixes.

Abstract

Global warming is having an unprecedented impact on plant phenology and vitality worldwide, potentially leading to significant changes in the food web, carbon, water cycling and ecosystem functions. Environmental drivers explaining spring phenology, mainly including temperature (chilling in late autumn and winter and forcing in late winter and spring) and photoperiod, have been extensively investigated in temperate trees, but these factors have been rarely studied in subtropical forests and their potential effects are therefore relatively unknown. This knowledge gap is especially important to fill because these ecosystems harbor the largest portion of the world's biodiversity. In this study, we sought to test the effects of chilling (low vs. high) and forcing temperatures (20 vs. 25 °C) on spring phenology for seedlings of five subtropical woody species using six climate chambers. We compared forcing requirements for budburst and leaf-out in the different treatments by calculating the number of degree days achieved from the start of the experiment to the time of budburst and leaf-out, and we examined seedlings’ survival under the different treatments. Although the survival of subtropical seedlings was found to be little affected by variation in chilling or forcing, longer chilling duration and warmer forcing temperature led to a lower forcing requirement for budburst, which advanced both budburst and leaf-out. This suggests that the seedlings experienced a non-linear accumulation of forcing with generally a higher efficiency at 25 °C than at 20 °C. Interestingly, shorter exposure to chilling conditions disrupted the sequence of budburst / leaf-out timings among the study species. This study confirms that the sensitivity of spring leaf phenology to forcing and chilling is not only found in temperate perennial plants but also in subtropical trees that undergo a dormancy period. It offers new perspectives for a comprehensive analysis of subtropical plant phenology in response to global climate change.

Introduction

Climate change has already affected plant seasonal cycles in most of the extra-tropical regions, with the trend having accelerated since the 1980s (Vitasse et al., 2018; Fu et al., 2019; Piao et al., 2019; Menzel et al., 2020; Wang et al., 2020a; Vitasse et al., 2022). Changes in plant phenology have major impacts on ecosystem structure and function through species interactions, community assembly, and species invasions as well as on climate itself through changes in the carbon and water cycles (Wray and Elle, 2016; Cortes-Flores et al., 2017; Richardson, 2019; Buonaiuto and Wolkovich, 2021). Unlike temperate regions where extensive research has been performed with long-term field observations and climate chamber experiments, subtropical and tropical trees have only recently begun to be studied (Kaewthongrach et al., 2020; Xu et al., 2021; Zhang et al., 2021a).

Several factors have been shown to influence the budburst and leaf-out of temperate woody species, with a general consensus that three factors are of greatest concern with respect to climate change: temperature, including winter cool temperatures (chilling) and warm spring temperatures (forcing), photoperiod, and precipitation (Dai et al., 2014; Laube, 2014; Flynn and Wolkovich, 2018; Vitasse et al., 2018). With insufficient winter chilling, the forcing requirement for budburst / leaf-out is expected to increase, partially counteracting the advance in spring phenology due to spring warming (Wang et al., 2020b), and possibly explaining why the phenological sensitivity of temperate trees to spring temperatures seems to have decreased in recent decades (Fu et al., 2015a; Zhang et al., 2022), though this may also be due to the non-linearity of the temperature effect (Wolkovich et al., 2021; Walde et al., 2022). The rare studies which have explored the environmental cues of spring phenology in subtropical species have found that chilling is far more influential than photoperiod for regulating budburst and leaf-out timings (Shi et al., 2017; Du et al., 2019; Song et al., 2020), but the relative importance of the effects of chilling and forcing on subtropical woody tree seedlings has not yet been thoroughly analyzed. Therefore, it remains unknown whether longer chilling and warmer forcing temperatures result in a lower forcing requirement for subtropical trees and whether these conditions increase plant vitality and survival rates.

The species-specific sensitivity of phenology to temperature can mean that varying winter and spring weather conditions can alter the timing of budburst / leaf-out in different ways for different species. For example, studies in both temperate and subtropical regions have shown that a lack of chilling during winter significantly increases the forcing requirement for budburst in species having a high chilling requirement, thereby resulting in a different chronological sequence of when species achieve budburst and leaf-out (Laube et al., 2014; Song et al., 2020). However, it remains unclear whether higher forcing temperatures in spring could also lead to changes in the sequence of when particular species achieve spring phenology milestones.

Researchers have used either seedlings or cuttings as substitutes for adult individuals to explore the environmental cues of spring phenology when using manipulative experiments (Vitasse and Basler, 2014; Hänninen et al., 2019; Zhang et al., 2021b; Baumgarten et al., 2021). However, there are several limitations when using twig cutting experiments. First, although cuttings are physiologically closer to adult trees (Vitasse, 2013), cuttings may disrupt hormonal signals, which may create artefacts when studying later stages than bud swelling and budburst (Vitasse and Basler, 2014). Second, cuttings cannot be used to test the legacy effect of winter warming on leaf phenology, for instance, whether earlier leaf-out in response to a warm winter could translate into earlier leaf senescence and even earlier leaf-out in the following year (Fu et al., 2014). Finally, cuttings may work better with temperate trees that presumably have a deeper winter dormancy (buds are possibly fully decoupled from the plant during winter) but perhaps less so for subtropical trees that tend to have much weaker dormancy. Previous studies have used different sampling dates to obtain samples of buds having experienced different amounts of chilling (Laube et al., 2014; Primack et al., 2015; Song et al., 2020), but this method would appear to equate or confound "amount of chilling" with "time since the twig was cut", meaning that twigs cut at different times could not be subjected to the other treatment and measurements simultaneously.

In this study, we conducted a climate chamber experiment to investigate the effects of different winter chilling and spring forcing conditions on seedlings of five subtropical woody species. We aimed to: (i) quantify spring budburst and leaf-out phenology's forcing requirement for subtropical species under different winter chilling and spring forcing conditions; and (ii) examine whether the order in which the species achieved budburst / leaf-out varied under the different experimental conditions. Based on recent studies conducted on subtropical trees, we anticipate that the forcing requirement for budburst / leaf-out should increase with a reduction of chilling, as is the case with temperate trees. We expect the sequence in which species achieve budburst / leaf-out to be reshuffled under the different climatic conditions, thereby reflecting the differences in species-specific sensitivity to chilling.