Introduction

Climate shifts are leading to rapid, species-specific changes in phenology and ecosystem productivity (Boisvenue & Running, 2006; Menzel et al., 2006; Yang & Rudolf, 2010; Thackeray et al., 2016). In temperate forests, changes in the timing of spring leaf-out, autumn leaf-senescence and bud set are modifying water, energy and carbon cycles (Peñuelas et al., 2009; Richardson et al., 2013), with extended growing seasons increasing net ecosystem carbon uptake by up to 9.8 gC m^-2 day^-1 (Keenan et al., 2014). Therefore, understanding the interaction between climate change and temperate forest phenology is pivotal to improving forecasts of community dynamics and carbon sequestration.

The past few decades have seen delays in the onset of temperate autumn phenology, but these changes are much smaller in magnitude compared to the advances in spring leaf-out observed during the same period (Gill et al., 2015; Piao et al., 2019). This is unexpected, given that experiments have demonstrated a high sensitivity of leaf senescence to autumn warming, with phenological responses even surpassing the temperature sensitivity (days per °C) of spring leaf-out (Fu et al., 2018). One possible explanation for this discrepancy is that other factors may counterbalance the effects of autumn warming, with some studies finding that earlier leaf-out leads to earlier leaf senescence (Fu et al., 2014; Keenan & Richardson, 2015; Zani et al., 2020). This connection between spring and autumn phenophases could be due to developmental and nutrient constraints that affect carbon source-sink dynamics in temperate trees (Paul & Foyer, 2001; Zani et al., 2020; Zohner et al., 2023; Gessler & Zweifel, 2024).

The Solstice-as-Phenology-Switch hypothesis, supported by experiments and monitoring data, posits that warmer air temperatures before the summer solstice accelerate tree growth and development, leading to an earlier onset of leaf senescence, whereas warmer temperatures after the solstice slow the progression of leaf senescence (Zohner et al., 2023). This reversal in temperature effects provides an explanation for the less pronounced shifts in autumn phenology compared to spring (Piao et al., 2019). The effect reversal after the solstice points to the role of photoperiod in regulating plant physiology (Bauerle et al., 2012), with trees becoming increasingly responsive to cooling temperatures as days continue to shorten. The precise timing of this reversal appears to be flexible and has been advancing in recent decades, potentially due to faster development driven by climate warming (Zohner et al., 2023). For temperate trees, the key outcomes of development are production of viable seeds, cessation of primary and secondary growth, and maturation of tissues including leaf or flower buds (bud set) ready for overwintering before the onset of frost (Rohde & Bhalerao, 2007; Tanino et al., 2010; Cooke et al., 2012). Because opportunities for development will vary among years, the timing of the temperature effect reversal should be flexible. However, this flexibility has yet to be demonstrated in processes directly related to development such as autumn bud set.

In this study, we investigate how changes in air temperature around the summer solstice affect primary growth cessation, using bud set as a key physiological marker for the end of primary growth and the beginning of autumn phenology (Zohner & Renner, 2019). Specifically, we explore the effects of pre- and post-solstice cooling, and of daytime versus nighttime cooling, on bud set timing. Diel temperature variations are relevant because trees mainly grow at night when temperatures and water deficit are lower than during the day (Zweifel et al., 2021). Between 1950 and 2004, nighttime temperatures rose faster than daytime temperatures (Vose et al., 2005), but from 1991 to 2020 this appears to have reversed (Zhong et al., 2023). We also experimentally created early-leafing vs. late-leafing trees to assess whether slowed early-season development postpones the reversal date of temperature effects on autumn phenology (Fig. 1). As depicted in our conceptual model (Fig. 1), tree individuals are dynamic systems that continuously integrate and adapt their physiological responses to environmental conditions over time. Their responses to temperature between June and August and between day and night are therefore expected to differ, an expectation tested in this study.

Figure 1.

Results

Experiment 1

Linear mixed-effects modelling showed that across all treatments, late-leafing trees cooled during spring experienced a delay to their bud set of 4.6 ± 1.3 days (mean ± 2 SE). Across all treatment pairings, the mean bud set date for the late-leafing group always occurred later than for the early-leafing group (Fig. S2). On average, each day delay in spring leaf-out was associated with a delay of 0.24 ± 0.06 days in bud set timing.

The effect of July cooling differed strongly between the early- and late-leafing trees: Within the early-leafing group, moderate cooling in July lead to a small, non-significant delay in bud set compared to the ambient July treatment (1.4 ± 2.6 days). July cooling had a much greater impact on late-leafing trees, leading to a 4.9 ± 2.6-day delay in bud set compared to the ambient July treatment in the late-leafing group.

In contrast to July cooling, the effects of August cooling did not differ between early- and late-leafing trees, advancing bud set in all treatment groups (Fig. 2b). Cooling in August lead to a 4.5 ± 2.6-day and 4.4 ± 2.6-day advancement in bud set for early- and late-leafing trees, respectively. The extreme cooling treatments showed similar patterns, although slightly less clearly (Fig. S3). Effects of absolute and relative growth on bud set date can be found in the supporting information (Figs. S4-S5). Bud set timing had no effect on final bud length (Fig. S6).

Figure 2.

Experiment 2

Linear mixed-effects modelling showed that pre-solstice full-day (day and night) cooling delayed autumn bud set by 4.1 ± 3.6 days (mean ± 2SE) (Fig. 3). Pre-solstice nighttime cooling had a similar effect, delaying bud set by 4.2 ± 3.6 days. By contrast, pre-solstice daytime cooling had no significant effect on bud set (0.2 ± 3.7 days). Post-solstice full-day cooling advanced autumn bud set by 5.2 ± 3.6 days. Similarly, post-solstice daytime cooling advanced bud set by 5.3 ± 4.3 days. Conversely, post-solstice nighttime cooling delayed bud set by 3.8 ± 3.5 days.

Figure 3.

Discussion

In this study, we conducted experiments on European beech to test how primary growth cessation and bud set respond to monthly and diel temperature changes around the summer solstice. We found large differences in the responses between trees subjected to daytime versus nighttime cooling before and after the solstice (Fig. 3) and between early- and late-leafing trees (Fig. 2). These differences suggest that early-season developmental timing not only influences the timing of autumn bud set per se, but also plays a critical role in determining the timing of the summer solstice effect reversal. Therefore, our findings support our conceptual model (Fig. 1), highlighting development as a key factor underpinning the Solstice-as-Phenology-Switch hypothesis. In the following sections, we discuss the effects of pre-solstice and post-solstice air temperature on development, along with the distinct impacts of daytime versus nighttime temperature variations.

Early-season development rates alter responses to late-season temperature

Our trans-solstice climate manipulation experiments showed that trees delayed their aboveground primary growth cessation (bud set) in response to slow/late early-season development (delayed spring leaf-out). Regardless of the summer cooling treatments, late-leafing trees consistently set buds after their early-leafing counterparts (Fig. S2), with each day delay in spring leaf-out delaying bud set by an average of 0.24 days. This is in line with previous studies demonstrating a tight linkage between within-year variations in spring and autumn phenology (Fu et al., 2014; Keenan & Richardson, 2015; Signarbieux et al., 2017), likely governed by developmental constraints (Zohner et al., 2023), buildup of water and nutrient stress (Paul & Foyer, 2001; Buermann et al., 2018; Bigler & Vitasse, 2021), or leaf aging (Lim et al., 2007).

July cooling induced a delay in bud set dates 3.5 times greater in late-leafing trees compared to early-leafing ones (4.9 versus 1.4 days delay), which agrees with the expectations derived from our conceptual model (Fig. 1). As we had expected, the natural interannual variation in early-season development causes year-to-year differences in the point at which cool temperatures switch from delaying bud set to advancing it. This offers a physiological explanation for the advancement in the effect reversal timing observed between 1966 and 2015 in Fagus sylvatica, Aesculus hippocastanum, Quercus robur, and Betula pendula (Zohner et al., 2023).

August cooling induced comparable advances in bud set timing in both early- and late-leafing trees (4.4-4.5 days). As trees become increasingly responsive to cooling with shortening days (Delpierre et al., 2009; Körner et al., 2016), they exhibit increasingly similar responses to late-season (August) cooling, regardless of their prior developmental speeds (Fig. 1). That the differences in the responses of early-leafing and late-leafing trees to cooling diminishes between July and August suggests tree individuals are dynamic systems that continuously integrate and adapt their physiological responses to environmental conditions over time.

Effects of daytime vs. nighttime temperature

Our experiments showed that daytime and nighttime temperatures had different effects on primary growth cessation before and after the summer solstice: Before the solstice, daytime cooling had no impact on the timing of bud set, while nighttime cooling and full-day cooling delayed bud set by 4.2 and 4.1 days, respectively (Fig. 3). Given that experimental cooling reduced photosynthesis by 69-83% across all treatments (Fig. S9), these findings underscore the role of developmental processes—such as cell division and expansion—which mostly occur at night (Zweifel et al., 2021; Fig. 4a). The developmental arrest induced by night cooling—and therefore also by full-day cooling—likely slowed bud growth and maturation, effectively extending the growing season.

Figure 4.

After the solstice, daytime and nighttime cooling of 8°C elicited opposite responses. Trees subjected to post-solstice daytime cooling and full-day cooling set their buds earliest, more than five days earlier on average than the control group. As days shorten, the temperature threshold inducing this growth cessation must be lower at night, otherwise trees would risk prematurely ending their growing season due to the daily minimum temperatures occurring at night (Fig. 4b). This may explain why post-solstice nighttime cooling delayed, rather than advanced, bud set: Cooling of 8°C was sufficient to trigger overwintering responses when applied during the day but not during the night (see Fig. S10 for a conceptual schematic). It is also possible that daytime cooling indirectly triggered bud set by reducing photosynthesis (Fig 4a). Such a mechanism is based on the assumption that trees will prioritise dormancy induction over growth once photosynthesis is not possible anymore (Körner et al., 2016). Indeed, downregulation of photosynthesis has previously been reported to accelerate senescence (Krieger-Liszkay et al., 2019), although this may simply follow a reduction in growth activity (Paul & Foyer, 2001). However, reduced photosynthesis has also been linked to delayed senescence in both observational (Meng et al., 2023) and experimental studies (Vitasse et al., 2021; Zohner et al., 2023). Therefore, the direct effects of post-solstice photosynthesis on autumn phenology still need to be clarified.

Nighttime cooling always led to a delay in bud set of approximately four days (Fig. 3). As trees mainly grow at night (Zweifel et al., 2021), colder nighttime temperatures slow down key developmental processes such as meristematic activity, tissue expansion and maturation, which in turn likely caused the delays in primary growth cessation (Fig. 4). Cold autumn nights also delay growth cessation and slow bud development in Populus, Pinus and Picea species (Kramer, 1956; Malcolm & Pymar, 1975; Kalcsits et al., 2009). Given the consistency of the effect reversal across Northern Hemisphere temperate forests (Zohner et al., 2023), and the patterns seen in previous experiments (Kramer, 1956; Malcolm & Pymar, 1975; Kalcsits et al., 2009; Zohner et al., 2023), our results likely are generalisable across temperate tree species.

In conclusion, earlier primary growth cessation in temperate trees under climate change can be explained by higher developmental rates under warmer temperatures, an effect predominantly driven by nighttime temperatures (since trees primarily grow at night). Ultimately, to better predict future growing season lengths, models must begin to account for the differential impacts of the annual and daily temperature cycles that temperate zone trees are physiologically adapted to.

Materials and Methods

Experiment 1

To test the antagonistic effects of early-season development and late-season air temperature on autumn primary growth phenology, we set up an experimental population (n = 267) of 40-60 cm tall European beech (Fagus sylvatica L.) trees in Zurich, Switzerland in 2023. The trees were sourced from a local nursery, and each tree was placed individually in a 20 L plastic pot containing a 1:1:1 sand / peat / organic soil mixture with a Nitrogen (N) concentration of ∼65 g m^-3, a Phosphate (P₂O₅) concentration of ∼140 g m^-3, and a Potassium (K₂O) concentration of ∼400 g m^-3. Individual trees were assigned randomly to one of 10 treatment groups (26 ≤ n ≤ 27). Treatment groups were cooled at different times of the year, using different cooling levels (Table 1). To arrest spring development and thereby generate early-leafing and late-leafing individuals, some trees were placed outside under ambient conditions, while others were cooled in climate chambers from 4 April to 24 May. The chambers were set to a low of 2°C at night and a high of 7°C during the day, following a simulated day-night cycle of temperature and light availability (13 h photoperiod at ∼4,300 lux). Temperatures around 5°C are associated with low rates of growth and development processes such as cell division, expansion and maturation (Körner, 2003; Tumajer et al., 2021). From 24 May to 21 June, all trees were kept outside under ambient conditions in a randomised block design. All trees were monitored to observe their individual leaf-out dates, which was defined as the date when >50% of their leaves had unfolded, corresponding to BBCH15 (Capdevielle-Vargas et al., 2015).

Table 1.

During the summer treatments, control trees were placed outside under natural ambient conditions. We did not use climate chambers for the control groups because warm conditions in these chambers can introduce unique physiological stressors—such as aphid infestations—not present in cold chambers (Bezemer et al., 1998). We noticed increased aphid abundance in control chambers during experiment 2, however these stressors did not appear to affect autumn phenology (see Experiment 2). The July treatments took place directly after the summer solstice from 22 June to 23 July. Treated trees were placed in climate chambers set to a low of 2°C at night and a high of 7°C during the day or a low of 8°C at night and a high of 13°C during the day depending on their cooling level (extreme and moderate, respectively). Trees in the chambers experienced a photoperiod of 16 h at ∼7,300 lux. The extreme cooling was designed to severely impair cell division, expansion, and maturation as described above. Additionally, under this temperature regime, photosynthesis should be reduced by >40% (Körner, 2006). The moderate cooling regime should still impair growth and development in temperate deciduous trees as well as reducing photosynthesis by at least 30% (Körner, 2003, 2006; Lenz et al., 2014). The August treatments took place from 24 July to 25 August under the same conditions as the July treatments except with a 15 h photoperiod. For the remainder of the experiment, all trees were kept outside in a randomised block design. Throughout the experiment, all trees were watered frequently to ensure constant water supply (Fig. S1).

To observe the effects of our treatments on the development of overwintering buds, we monitored bud growth to derive bud set dates, our marker for the cessation of primary aboveground development and the beginning of autumn phenology, for all trees. On each tree, the terminal bud of the primary shoot and the terminal bud on a random lateral stem were selected and tagged for measurement. Each selected bud was measured to 0.01 mm precision using a digital calliper (CD-P8”M, Mitutoyo Corp, Japan). We measured all buds on a regular basis from 4 July to 2 November. Bud set was defined as the date when each bud reached 90% of its own maximum length, which is considered to be an indicative stage of aboveground primary growth cessation (Signarbieux et al., 2017; Zohner & Renner, 2019). Bud lengths were linearly interpolated between measurement dates to derive the date at which they reached the 90% threshold.

Experiment 2

To observe the effects of pre- and post-solstice daytime and nighttime temperature on bud set phenology, we set up an experimental population (n = 180) of four-year-old Fagus sylvatica trees in Zurich, Switzerland in 2022. The trees were sourced from a local nursery and each tree was placed individually in a 20 L plastic pot containing a 1:1:1 sand / peat / organic soil mixture with a Nitrogen (N) concentration of ∼65 g m^-3, a Phosphate (P₂O₅) concentration of ∼140 g m^-3, and a Potassium (K₂O) concentration of ∼400 g m^-3.

The ambient control treatment consisted of 36 trees exposed to natural ambient conditions. The remaining eight treatments were each applied to 18 trees and included cooling in climate chambers with simulated ambient day length (16 h) and light intensity (∼6,900 lux). The pre-solstice cooling treatments were applied between 22 May and 21 June. The post-solstice cooling treatments were applied between 22 June and 21 July. The pre- and post-solstice treatments included four levels each: Chamber control, where the trees were continuously subjected to 20°C; Day cooling, where trees were subjected to 8°C in the daytime and 20°C at night; Night cooling, where trees were subjected to 20°C in the day and 8°C at night; Full-day cooling, where trees were continuously subjected to 8°C (Table 2). Due to warm temperatures, chamber control trees were subject to an increase in aphid abundance, however this did not alter their bud set timing (see data analyses). After treatment, all trees were placed in a randomised block design outside under ambient conditions. Soil moisture content was regulated by frequent watering. We measured all buds on a weekly basis from 25 August to 3 November following the same methodology as in experiment 1. We also measured leaf-level CO₂ assimilation rates (see Zohner et al., 2023 for methodology).

Table 2.

Data analyses

For experiment 2, we performed a one-way ANOVA that showed no significant differences between the bud set dates of the ambient, pre-chamber and post-chamber control groups (F_2,136 = 0.346, p =0.708, see Fig. S7). Therefore, for the following analyses we treated all three control treatments as one control treatment with 72 trees. For both experiments we ran linear mixed-effects models using treatment as a categorical fixed effect, bud type (apical vs. lateral) as a random effect and bud set day-of-year, absolute bud growth or relative bud growth as the response variable. Effect sizes were calculated in comparison to the corresponding control treatment, i.e., all early-leafing treatments were compared to the early-leafing control treatment and all late-leafing treatments were compared to the late-leafing control. Absolute and relative bud growth were calculated as:

Where:

min length = the first measured bud length

max length = the measured bud length when the bud first surpassed 90% of its final length

To determine the sensitivity of autumn bud set timing to spring leaf-out timing, we ran a linear mixed-effects model using leaf-out day-of-year as the fixed predictor variable, bud type and summer temperature treatment as random effects, and bud set day-of-year as the response variable.

Data availability

The code and data for this study will be made available upon request or at Zenodo on publication of the manuscript.

Supplementary figures and tables

Figure S1.

Figure S2.

Figure S3.

Figure S4.

Figure S5.

Figure S6.

Figure S7.

Figure S8.

Figure S9.

Figure S10.

Table S1.

Table S2.

Acknowledgements

C.M.Z. was supported by the SNF Ambizione Fellowship programme (no. PZ00P3_193646) and T.W.C. by DOB Ecology and the Bernina Foundation.

Additional information

Author contributions

D.R. conceived and developed the study, conducted the experiments and analyses, and wrote the manuscript. C.M.Z equally contributed to the conception and development of the study, contributed to the experiments and analyses, and the text. L.M., H.M., Z.W. and Y.Z. contributed to the conception and implementation of the first experiment. R.B. contributed to the conception and implementation of the second experiment. T.W.C. and S.S.R. contributed to the text. All authors provided comments and approved the final manuscript.