1
Declining global warming effects on the phenology of spring
1
leaf unfolding
2
Yongshuo H Fu
1,2
, Hongfang Zhao
1
, Shilong Piao
1,3,4
, Marc Peaucelle
5
, Shushi Peng
1,5
, Guiyun
3
Zhou
6
, Philippe Ciais
5
, Mengtian Huang
1
, Annette Menzel
7,8
, Josep Peñuelas
9,10
, Yang Song
11
,
4
Yann Vitasse
12,13,14
, Zhenzhong Zeng
1
, Ivan A Janssens
2
5
6
1
Sino-French Institute for Earth System Science, College of Urban and Environmental Sciences, Peking
7
University, Beijing 100871, China
8
2
Centre of Excellence PLECO (Plant and Vegetation Ecology), Department of Biology, University of
9
Antwerp, Universiteitsplein 1, B-2610 Wilrijk, Belgium
10
3
Key Laboratory of Alpine Ecology and Biodiversity, Institute of Tibetan Plateau Research, Chinese Academy
11
of Sciences, Beijing 100085, China
12
4
Center for Excellence in Tibetan Earth Science, Chinese Academy of Sciences, Beijing 100085, China
13
5
Laboratoire des Sciences du Climat et de l'Environnement, CEA CNRS UVSQ, Gif-sur-Yvette, France
14
6
School of Resources and Environment, University of Electronic Science and Technology of China, Chengdu,
15
China
16
7
Ecoclimatology, Technische Universität München, Freising, Germany
17
8
Technische Universität München, Institute for Advanced Study, Lichtenbergstraße 2a, 85748 Garching,
18
Germany
19
9
CREAF, Cerdanyola del Vallès, Barcelona 08193, Catalonia, Spain
20
10
CSIC, Global Ecology Unit CREAF -CSIC-UAB, Cerdanyola del Vallès, Barcelona 11 08193, Catalonia,
21
Spain
22
11
Department of Atmospheric Sciences, University of Illinois, Urbana, IL 61801, USA
23
12
University of Neuchatel, Institute of Geography, Neuchatel, Switzerland
24
13
WSL Swiss Federal Institute for Forest, Snow and Landscape Research, Neuchatel, Switzerland
25
14
WSL Institute for Snow and Avalanche Research SLF, Group Mountain Ecosystems, Davos, Switzerland
26
Revised manuscript for Nature
27
August 12, 2015
28
29
This document is the accepted manuscript version of the following article:
Fu, Y. H., Zhao, H., Piao, S., Peaucelle, M., Peng, S., Zhou, G., … Janssens, I. A.
(2015). Declining global warming effects on the phenology of spring leaf unfolding.
Nature, 526(7571), 104-107. https://doi.org/10.1038/nature15402
2
Earlier spring leaf unfolding is a frequently observed response of northern trees to climate
1
warming
1,2,3,4
. Many deciduous tree species require chilling for dormancy release, and
2
warming-related reductions in chilling may counteract the advance of leaf unfolding in
3
response to warming
5,6
. Empirical evidence for this, however, is limited to saplings or twigs
4
in climate-controlled chambers
7,8
. Using long-term in situ observations of leaf unfolding for
5
seven dominant European tree species at 1,245 sites, we show here that the apparent
6
response of leaf unfolding to climate warming (S
T
, expressed in days advance per °C) has
7
significantly decreased from 1980 to 2013 in all monitored tree species. Averaged across all
8
species and sites, S
T
decreased by 40% from 4.0 ± 1.8 days °C
-1
during 1980-1994 to 2.3 ±
9
1.6 days °C
-1
during 1999-2013. The declining S
T
was also simulated by chilling-based
10
phenology models, albeit with a weaker decline (24%-30%) than observed in situ. The
11
reduction in S
T
is likely to be partly attributable to reduced chilling. Nonetheless, other
12
mechanisms may also play a role, such as ‘photoperiod limitation’ mechanisms that may
13
become ultimately limiting when leaf unfolding dates occur too early in the season. Our
14
results provide empirical evidence for a declining S
T
, but also suggest that the predicted
15
strong winter warming in the future may further reduce S
T
and therefore result in a
16
slowdown in the advance of tree spring phenology.
17
18
The phenology of spring leaf unfolding influences regional and hemispheric-scale carbon
19
balances
2
, the long-term distribution of tree species
9
, and plant-animal interactions
10
. Changes in
20
the phenology of spring leaf unfolding can also exert biophysical feedbacks on climate by
21
modifying the surface albedo and energy budget
11,12
. Recent studies have reported significant
22
advances in spring phenology as a result of warming in most northern hemisphere regions
1,3,4
.
23
Climate warming is projected to further increase
13
, but the future evolution of the phenology of
24
spring leaf unfolding remains uncertain — in view of the imperfect understanding of how the
25
underlying mechanisms respond to environmental stimuli
12,14
. In addition, the relative
26
contributions of each environmental stimulus, which together define the apparent temperature
27
sensitivity of the phenology of spring leaf unfolding (advances in days per degree Celsius
28
warming, S
T
), may also change over time
6,8,15
. An improved characterization of the variation in
29
3
phenological responses to spring temperature is thus valuable, provided that it addresses temporal
1
and spatial scales relevant for regional projections.
2
Numerous studies have reported advanced spring leaf unfolding which matches warming trends
3
over recent decades
1,3,4
. However, there is still debate regarding the linearity of leaf unfolding
4
response to the climate warming
6,7
. Recent experimental studies of warming using saplings have
5
shown that S
T
weakens as warming increases
7
. Experimental manipulation of temperature for
6
saplings or twigs, however, might elicit phenological responses that do not accurately reflect the
7
response of mature trees
16,17
. We therefore investigated the temporal changes in S
T
in adult trees
8
monitored in situ and exposed to real-world changes in temperature and other climate variables.
9
These long-term data series were obtained across Central Europe from the Pan European
10
Phenology Project (http://www.pep725.eu/). Data were collected from 1,245 sites for seven
11
dominant tree species (see methods and the distribution of the sites in Extended Data Fig. 1). The
12
aims of our analysis are to determine the temporal changes in S
T
at the species level during 1980-
13
2013, a period during which Europe has substantially warmed
13
, and to relate these changes in S
T
14
to differences in other physiological and environmental factors.
15
16
For each species at each observation site, we first determined the preseason length as the period
17
before leaf unfolding for which the partial correlation coefficient between leaf unfolding and air
18
temperature was highest (see methods). We used a gridded climate dataset, including daily
19
maximum and minimum air temperature, precipitation and absorbed downward solar radiation,
20
with a spatial resolution of 0.25º (approximately 25 km)
18
. The optimal length of the preseason
21
ranged between 15 days and four months across the seven species (Extended Data Fig. 2), in
22
agreement with earlier results
1,14
. We then calculated the average temperature during the
23
preseason for each year at each site and calculated S
T
using ordinary least squares linear
24
regression for the entire period and for two 15-year periods, namely 1980-1994 and 1999-2013,
25
that had slight difference in preseason lengths (Extended Data Fig. 3a). The leaf unfolding dates
26
were negatively correlated with the preseason temperature, with a mean linear correlation
27
coefficient of -0.61±0.16, determined using the preseason defined from the time period 1980-
28
2013. Almost all individual tree-level correlations were negative (99.7%) and the vast majority of
29
these correlations was statistically significant at P<0.05 (93.4%) (Extended Data Fig. 4). In line
30
4
with previous studies
1,4
, the timing of leaf unfolding substantially advanced in all species for
1
1980-2013, with an average advancing rate of 3.4 ± 1.2 days °C
-1
across all species-sites
2
(hereafter, a positive value indicates advancement) (Fig. 1a). But the surprising result is that S
T
3
significantly decreased by 40.0% from 4.0 ± 1.8 days °C
-1
during 1980-1994 to 2.3 ± 1.6 days °C
-
4
1
during 1999-2013 (t=-37.3, df=5473, P<0.001) (Fig. 1b). All species show similar significant
5
decreases in S
T
(Fig. 1a), although the extent of reduction was species-specific. For example,
6
Aesculus hippocastanum (see caption to Fig. 1 for English common names) had the largest
7
decrease in S
T
(-2.0 days °C
-1
), while S
T
decreased only slightly (but still significantly) in Fagus
8
sylvatica (-0.9 days °C
-1
) (Fig. 1a). Similar results were also obtained using a fixed preseason
9
length determined either in the time period 1980-1994 or in 1999-2013 (Extended Data Fig. 3b
10
and 3c). The declining S
T
could, however, also have been an artifact resulting from the
11
‗encroachment‘ of leaf unfolding dates into the preseason period that was used to calculate the
12
temperature sensitivity. We therefore calculated the number of ‗encroachment days‘ and found it
13
is very small compared to the pre-season length even in the warmest period (Extended Data Fig.
14
3d and 3e). Because the time scale of the analysis could affect the estimates of S
T
19
, we also
15
calculated S
T
using 10-year intervals (instead of 15 years) and found consistent results, i.e., S
T
16
significantly decreased between the 1980s and the last decade for all species except Tilia cordata
17
(Extended Data Fig. 5a). We further calculated S
T
with a 15-year moving window from 1980 to
18
2013 and found a significant decrease (P<0.01) for each of the seven species (Fig. 1c). S
T
19
decreased by an average of 0.7 days °C
-1
per decade across all species. Similar results were also
20
reached when a 10-year interval was used (Extended Data Fig. 6). These results suggest a
21
significant change in the response of leaf unfolding to the ongoing climate warming in all studied
22
tree species in Central Europe.
23
24
Since there is no single accepted theory to account for the decreased S
T
over the period 1980-
25
2013, we propose three mutually non-exclusive hypotheses: (1) adaptation to increased variance
26
in spring temperature, (2) photoperiodic limitations (due to earlier leaf unfolding) overriding
27
temperature controls, and (3) reduced duration and/or sum of cold temperatures during dormancy,
28
a ‗lost chilling‘ mechanism.
29
30
5
The first hypothesis relates to possible effects of an increased variance in temperature. A recent
1
study reported substantial spatial differences in S
T
, with smaller absolute values at sites with a
2
higher variance of local spring temperature
20
. Trees may indeed develop conservative strategies
3
(or higher phenological plasticity) of spring leaf unfolding in places where temperature fluctuates
4
more, in order for instance to avoid spring frost damage
21
. The observed declining S
T
could
5
therefore partly result from an increase in the variance in spring temperature. However, the
6
variance in spring temperature only significantly increased at sites of two species and decreased
7
for all the other species except Fraxinus excelsior (Fig. 2a). This suggests that increased variance
8
in spring temperature cannot account for the decreased S
T
. We further studied the fluctuations in
9
daily mean temperature and diurnal temperature amplitude (T
max
- T
min
) over the preseason for
10
the two periods 1980-1994 and 1999-2013, and for three groups of sites with comparable mean
11
annual temperature (MAT). The fluctuations in daily temperature and diurnal temperature
12
amplitude during the preseason were similar during the two time periods between which S
T
13
declined (Extended Data Fig. 7), suggesting that altered temperature variability is not an obvious
14
cause for the declining apparent temperature sensitivity of leaf unfolding.
15
16
Precocious leaf unfolding in warm springs may increase the risk of late frost events for trees
21
. To
17
overcome this risk during warm springs, many species have evolved a protective mechanism
18
related to photoperiod
22
, which hinders the warming response when days are still short and the
19
risk for subsequent frost events is thus high. Our second, alternative, hypothesis to account for
20
the observed decrease in S
T
in recent decades is therefore a change in the relationship between
21
chilling accumulation and heat requirement, due to the shortening days as warming advances leaf
22
unfolding. However, we did not observe changes in S
T
with latitude, neither across all species,
23
nor for individual species (Extended Data Fig. 8), as one may expect if photoperiod was a strong
24
co-limitation of leaf unfolding. Nonetheless, we have no evidence to exclude photoperiod as a
25
controlling mechanism for the decline of S
T
since different populations may have different
26
genetic adaptations to photoperiod
23
. In addition, the lack of relation between S
T
and latitude may
27
have been because the response of spring phenology to photoperiod can be associated with many
28
confounding factors, such as tree age
17
, successional niche
23
(although there is some
29
contradictory evidence
8
), xylem anatomy
24
, or chilling conditions
8
. We can therefore not
30