This study revealed that seedlings of temperate tree species have an earlier spring phenology than conspecific canopy trees, and this discrepancy was enhanced when they were moved up to the canopy height. The phenological discrepancy was remarkable, as it reached up to more than a month depending on species. Thus, I invalidated the hypothesis that seedlings exhibit earlier phenology as a result of a vertical temperature gradient, but rather demonstrated that the difference in phenology can only be caused by ontogenic differences between seedlings and adults. Here, I observed earlier flushing in seedlings grown at canopy height relative to those grown at ground level (on average 5.5 d earlier). Augspurger (2004) found the opposite pattern in Aesculus glabra when moving seedlings to the top of a barn roof (7 m height), and suggested that the earlier flushing of the understory relative to conspecific canopy trees may result from the vertical temperature gradient occurring from the ground to the canopy. To my knowledge, this is the only study in which seedlings have been translocated to an elevated position, although this upward shift was not sufficient to reach the canopy height (20–25 m). However, the results found here are not inconsistent with the results obtained from the previous study as, in both cases, the vertical temperature profile may explain the phenological shift found between seedlings grown at ground level and those grown in an upper vertical position: in the previous study, temperature was recorded as 0.4–0.7°C colder above the roof than in the understory, delaying the phenology of the seedlings growing above the roof, whereas, in the present study, the temperature recorded at canopy layer was, on average, 1°C warmer than in the understory, resulting in a slightly earlier flushing of seedlings grown at canopy height relative to seedlings grown in the understory. The vertical temperature gradient within forests is expected to increase from understory to crown area during periods of strong positive net radiation (in spring and summer) and to decrease in winter when the radiation balance is negative, although this pattern is strongly related to different factors, such as slope exposure, stand density and species composition of the canopy (Geiger et al., 2003). Here, I found that the mean, minimum and maximum temperatures increased gradually from ground to canopy height irrespective of the season, but this effect was more pronounced in spring and summer (data not shown). A similar vertical temperature profile has also been reported in mixed conifer forest in Sierra Nevada (Rambo & North, 2009). The vertical temperature pattern found here in the mixed study forest might partly result from the topography of the site (north-facing slope), which makes the incoming radiation heat the top of the trees earlier in the morning than it does for the understory environment. The phenological shift of −3 to −9 d found here for a c. 1°C difference in mean spring temperature is similar to that found in previous studies, which observed a phenological shift in seedlings of Fagus sylvatica, Acer pseudoplatanus, Prunus avium, Fraxinus excelsior and Quercus petraea ranging from −2.4 to −6.3 d per degree of warming in early spring (Vitasse et al., 2010, 2013).
Earlier flushing in seedlings and saplings has been interpreted as an opportunistic strategy to capture sufficient light for growth before canopy closure. Overall, my results support the hypothesis of a shift in timing of leaf emergence with increasing tree age in order to enhance performance throughout the life cycle of the tree (Seiwa, 1999a). Although risky in relation to late spring frosts, the advanced ontogenesis allows seedlings and saplings to start their development in optimal light conditions before canopy closure, enhancing their growth and, subsequently, their competitive ability (Gill et al., 1998; Augspurger, 2008; Lopez et al., 2008). However, later bud burst in adults reduces the likelihood of frost damage, particularly in reproductive organs, thus exerting a fitness benefit. Accordingly, my results highlight a remarkably large phenological difference between seedlings and adults within species, probably enhanced by a warm period in early spring (end of March) allowing seedlings to flush, followed by a cooler period in the first half of April, slowing the bud development of adults (the last 2 wk of March were, on average, 3°C warmer than the first 2 wk of April, Fig. 2a). Further investigations are necessary to examine whether there is only an absolute difference between phenology of understory and conspecific canopy trees or, more likely, whether they also differ in their phenological response to the main environmental factors regulating bud burst of temperate tree species, that is, air temperature, and, for some late successional species, a combination of temperature and photoperiod (Körner & Basler, 2010; Polgar & Primack, 2011). Yet, the second hypothesis seems to be more plausible as, here, I found that the ranking of the date of leaf emergence among species was similar within the three categories of seedling, but different in the adult group. This suggests that the dormancy cycle of the buds may be affected by the age of the plant (Cooke et al., 2012). In temperate tree species, the thermal time to bud burst is known to decrease with increased duration of previous chilling, down to a minimal thermal time when buds are considered to be ‘fully chilled’ (Murray et al., 1989; Falusi & Calamassi, 1996; Cannell, 1997; Hannerz et al., 2003). This relationship has been documented for three of the five tree species selected in this study, namely P. avium, T. platyphyllos and F. sylvatica (Lyr et al., 1970; Murray et al., 1989), with P. avium probably having the lowest requirement of chilling for a full rest completion, whereas F. sylvatica is known to have a high requirement of chilling for dormancy release as well as a photoperiodic control (reviewed in Vitasse & Basler, 2013). In our study, the vertical gradient of temperature from the ground to the canopy might have led to different fulfilment of chilling requirement between understory and canopy trees. Yet, this is unlikely, because the vertical profile of temperature found here was less pronounced in winter during endodormancy than in early spring during the experiment (0.37°C warmer at the canopy during December 2011–January 2012, data not shown). Furthermore, in the study site (north-facing slope at c. 580 m asl), the amount of chilling was likely to exceed the chilling requirement of the study species to fully release bud dormancy (see air temperature during winter in Fig. 2). More likely, seedlings may have a shallower bud dormancy than mature trees, resulting in a lower requirement of chilling for dormancy release and/or a lesser interaction with the increase in photoperiod in early spring for photoperiod-sensitive tree species, and so could flush earlier in response to a temperature increase in spring. In other words, bud rest completion is likely to occur later for adults than for juvenile trees, as suggested by Hanninen et al. (2007).
As, in natural conditions, mature trees may currently not experience sufficient unusual climatic events (such as a lack of chilling in winter) to accurately calibrate phenological models for future predictions, there is a renewed interest in the performance of experimental studies to improve the calibration of the parameters of such models by manipulating chilling and forcing temperatures in controlled growth chambers (e.g. Harrington et al., 2010; Morin et al., 2010; Fu et al., 2012), or even photoperiod, as future climate is expected to be warmer at a shorter photoperiod (Caffarra et al., 2011a,b; Basler & Körner, 2012). For obvious practical reasons, these studies are conducted on juvenile trees or cuttings (but see Hanninen et al., 2007). The results obtained from these studies may therefore not be valuable for the inference of model parameters for the prediction of forest phenology in the future, because of the strong ontogenic effects operating on tree phenology, as demonstrated by the present study. Further investigations need to be performed on cuttings and rooted cuttings obtained from adult trees to examine whether their phenology responds similarly to environmental conditions as adult trees, and therefore whether they can be used as a substitute for mature trees in warming and photoperiod experiments to infer the phenological responses of forests to climate change (Basler & Körner, 2012).