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The length of the snow-free season is a key factor regulating plant phenology and shaping plant community composition in cold regions. While global warming has significantly advanced the time of snowmelt and the growth period at all elevations in the Swiss Alps, it remains unclear if it has altered the likelihood of frost risk for alpine plants. Here, we analyzed the influence of the snowmelt timing on the risk of frost exposure for subalpine and alpine plants shortly after snowmelt, i.e., during their most vulnerable period to frost at the beginning of their growth period. Furthermore, we tested whether recent climate warming has changed the risk of exposure of plants to frost after snowmelt. We analyzed snow and air temperature data in the Swiss Alps using six weather stations covering the period 1970–2016 and 77 weather stations covering the period 1998–2016, spanning elevations from 1418 to 2950 m asl. When analyzed across all years within each station, our results showed strong negative relationships between the time of snowmelt and the frequency and intensity of frost during the most vulnerable period to frost for subalpine and alpine plants, indicating a higher frost risk damage for plants during years with earlier snowmelt. However, over the last 46 years, the time of snowmelt and the last spring frost date have advanced at similar rates, so that the frequency and intensity of frost during the vulnerable period for plants remained unchanged.
Unchanged risk of frost exposure for subalpine and alpine plants
after snowmelt in Switzerland despite climate warming
Geoffrey Klein
&Martine Rebetez
&Christian Rixen
&Yann Vitasse
Received: 14 February 2018 / Revised: 17 May 2018 / Accepted: 23 June 2018 /Published online: 12 July 2018
#ISB 2018
The length of the snow-free season is a key factor regulating plant phenology and shaping plant community composition in cold
regions. While global warming has significantly advanced the time of snowmelt and the growth period at all elevations in the
Swiss Alps, itremains unclear if it has altered the likelihood of frost risk for alpine plants. Here, we analyzed the influence of the
snowmelt timing on the risk of frost exposure for subalpine and alpine plants shortly after snowmelt, i.e., during their most
vulnerable period to frost at the beginning of their growth period. Furthermore, we tested whether recent climate warming has
changed the risk of exposure of plants to frost after snowmelt. We analyzed snow and air temperature data in the Swiss Alps using
six weather stations covering the period 19702016 and 77 weather stations covering the period 19982016, spanning elevations
from 1418 to 2950 m asl. When analyzed across all years within each station, our results showed strong negative relationships
between the time of snowmelt and the frequency and intensity of frost duringthe most vulnerable period to frost for subalpine and
alpine plants, indicating a higher frost risk damage for plantsduring years with earlier snowmelt. However, over the last 46 years,
the time of snowmelt and the last spring frost date have advanced at similar rates, so that the frequency and intensity of frost
during the vulnerable period for plants remained unchanged.
Keywords Air temperature .Alpine plants .Frost risk .Global warming .Snowmelt .Snow cover
In mountainous regions, a significant decline of the snow cov-
er has been reported worldwide over the last decades (Park et
al. 2012; Pederson et al. 2013;Xuetal.2016), including the
European Alps (Klein et al. 2016;Marty2008;Valtand
Cianfarra 2010). Since the beginning of the 1970s in the
Swiss Alps, the shortening of the snow cover duration found
at elevations greater than 1100 m asl was mainly caused by
earlier snowmelt in spring, and, to a lower extent, by later
snow onset in autumn (Klein et al. 2016), in connection with
a stronger temperature warming in spring than in autumn
(Rebetez and Reinhard 2008; Serquet et al. 2013).
The timing of snowmelt, which greatly fluctuates from year
to year irrespective of elevation (Klein et al. 2016; Wheeler et al.
2014), is the main driver triggering the onset of growth of most
alpine plant species in spring (Gerdol et al. 2013; Inouye 2008;
Jonas et al. 2008; Sherwood et al. 2017; Vitasse et al. 2017).
The snow depth accumulated during winter was also found to
play a role in the abundance of flowers, as well as in the prob-
ability of frost damage in spring when the snow becomes too
thin to sufficiently protect overwintering plant tissues against
extreme low temperatures (Inouye et al. 2002). Conversely, a
deeper snow cover tends to delay the time of snowmelt, and
therefore shifts alpine plant growth to a warmer period of the
year with possibly fewer frost events (Jonas et al. 2008).
The beginning of the growing season for alpine plants is
primarily controlled by the timing of snowmelt and the
Electronic supplementary material The online version of this article
( contains supplementary
material, which is available to authorized users.
*Geoffrey Klein
Institute of Geography, University of Neuchatel,
Neuchatel, Switzerland
WSL Swiss Federal Institute for Forest, Snow and Landscape
Research, Neuchatel, Switzerland
WSL Institute for Snow and Avalanche Research SLF,
Davos, Switzerland
WSL Swiss Federal Institute for Forest, Snow and Landscape
Research, Birmensdorf, Switzerland
International Journal of Biometeorology (2018) 62:17551762
subsequently air temperatures (Vitasse et al. 2017). On aver-
age, a duration of 2 to 3 weeks after the time of snowmelt was
observed before the beginning of plant height growth in the
Swiss Alps in snowbed conditions, corresponding roughly to
an accumulation of 100 growing degree days (abbreviated
GDD 100 thereafter) (Vitasse et al. 2017). Hence, the few days
following the time of snowmelt are critical for alpine plants, as
it is the period when plants lose progressively their freezing
resistanceacquired during winter and thus, when they become
most vulnerable to freezing damages (Rixen et al. 2012;
Sherwood et al. 2017). Nevertheless, at elevations above
2000 m asl, temperature below frost resistance of fully devel-
oped tissues of plants can still occur throughout the whole
growing season (Körner 2003).
During winter, snow cover insulates alpine plants from
freezing temperature (Körner 2003), so that the timing of
snowmelt in spring determines when plant tissues are exposed
to atmospheric air temperature and potentially with freezing
temperatures. Freezing resistance of common plant species
from the European Central Alps inducing 100% of mortality
in the plant tissues was reported to range from 4to16 °C,
with an average freezing resistance of 9 °C for most species
(Ladinig et al. 2013; Taschler and Neuner 2004).
Species growing at sites with little snowprotection, such as
ridges, are typically more freezing resistant than species grow-
ing under snowbed conditions (Nagy and Grabherr 2009). The
high interannual variability of the time of snowmelt shown in
Klein et al. (2016) might also alter the freezing resistance of
alpine and subalpine plants, which has been linked to the
fluctuations of the snow depth during the onset of spring
(Palacio et al. 2015).
Warming air temperatures since the 1970s have consider-
ably advanced the spring onset of growth below the treeline in
Western and Central Europe (Ahas et al. 2002;Menzeletal.
2006; Vitasse et al. 2018b), but little is known concerning
alpine plants in the Alps, as, to the best of our knowledge,
no long-term series of phenological observations are available
for plants above the treeline in these regions. Besides, only a
few studies describe the climatic conditions shortly after the
snowmelt in alpine and subalpine regions (Inouye 2008;
Inouye et al. 2002; Jonas et al. 2008; Wheeler et al. 2014),
likely due to the difficulty to obtain accurate meteorological
data at such elevations.
In a warmer climate, three different scenarios for the risk of
frost exposure for alpine plants could be expected (Vitasse et
al. 2018a): (i) an increase of the risk of frost exposure due to a
faster advance of the phenology compared to the frost-free
period, (ii) a decrease of the risk of frost exposure because
of a faster advance of the frost-free period compared to phe-
nology, (iii) no change in the risk of frost exposure due to a
similar advance of both phenology and frost-free period. With
a slower warming of minimum air temperatures compared to
maximum air temperatures during spring above 800 m in the
Swiss Alps over the last five decades (Vitasse et al. 2018a)and
an earlier time of snowmelt (Klein et al. 2016), the risk of frost
exposure for subalpine and alpine plants may not necessarily
decrease during their growth period in spring in a warmer
climate. Below the treeline in the Swiss Alps, the risk of frost
exposure and potential damage for some tree species has al-
ready increased during their leaf-out and flowering period at
elevations higher than 800 m over the period 19752016,
despite climate warming (Vitasse et al. 2018a). Hence, in-
creasing frequency of potentially damaging freezing events
might increase frost injuries (Wheeler et al. 2014), reduce
growth (Wipf et al. 2009), or increase the mortality of sensi-
tive frost plant species, such as shown for several species in
the Rocky Mountains (Inouye 2008).
Here, we examined long-term air temperature and snow
depth measurements in the Swiss Alps at six weather stations
during the period 19702016, together with data from another
meteorological network of 77 weather stations covering the
period 19982016, both located at elevations ranging from
1418 to 2950 m asl. We focused our analysis on events with
daily freezing temperatures below 4 °C during a period of
3 weeks enclosing the GDD 100, i.e., the most vulnerable
period for subalpine and alpine plants when growth begins.
Specifically, we aimed at (i) examining how the risk of frost
exposure for plants is related to the time of snowmelt, both in
its frequency and intensity, and (ii) testing whether the inten-
sity and the occurrence of frost events have changed over the
last five decades, when temperatures and the time of snowmelt
have significantly increased and advanced.
Materials and methods
Study sites
We analyzed air temperature and snow data from two inde-
pendent weather networks both located in Switzerland. One of
them was the IMIS network (Intercantonal Measurement and
Information System), which consists of high-elevation auto-
matic weather stations set up by the Swiss Federal Institute for
Snow and Avalanche Research (SLF). This network was
started in the beginning of the 1990s with a few stations and
has been steadily developed until reaching 103 stations in
2016. We selected 77 stations, ranging from 1630 to 2950 m
asl (Fig. 1), that covered a temporal period from 1998 to 2016
and provided accurate daily snow depth and temperature data
for at least 80% of the years during this period.
From the second and long-term weather network used in
this study, we selected 11 weather stations from the Swiss
Federal Office of Meteorology and Climatology
(MeteoSwiss) providing more than 45 years of daily snow
data and described in Klein et al. (2016). From these 11 weath-
er stations, we selected six stations covering the period 1970
1756 Int J Biometeorol (2018) 62:17551762
2016 that provided daily temperature data in at least 90% of
the years and that were situated at approximately the same
altitude range than the IMIS weather stations, i.e., ranging
from 1418 to 2540 m asl (Fig. 1).
Temperature and snow data
All climatic parameters analyzed during the vulnerable period
for subalpine and alpine plants were calculated for all stations
and years that provide at least 80% of available data during
that period. For the MeteoSwiss stations, daily snow depth
was manually recorded every morning, whereas daily mini-
mum and maximum air temperatures were automatically mea-
sured. For the IMIS stations, snow depth was automatically
monitored every half hour through an ultrasonic sensor situ-
ated 6 m above the ground (SR50, Campbell Scientific, USA).
Daily morning snow depth values were then extracted for a
better comparison with the MeteoSwiss stations. Temperature
and snow data for both networks were manually checked and
tested for outliers and missing data.
Each year was considered as the period ranging from 1
September until 31 August of the following year. For each
year, the time of snowmelt was defined as the first snow-free
day after an at least 40-day snow-covered period (~ 6 weeks)
from 1 September until 31 August, following the methodolo-
gy used by Klein et al. (2016).
Data analysis and statistics
In this study, we analyzed the risk of frost exposure for plant
species growing through the altitudinal range of both IMIS
and MeteoSwiss selected stations, i.e., from 1418 to 2950 m
asl, which includes both subalpine and alpine plant species.
We defined the vulnerable period for alpine plants as the
weeks enclosing the time when an accumulation of 100 degree
days was reached since the time of snowmelt (GDD 100),
corresponding roughly to the onset of growth at plant commu-
nity scale (Vitasse et al. 2017). Specifically, we considered the
duration of this vulnerable period as the time ranging from
7 days before the GDD 100 to 14 days following this GDD
100, corresponding to a total duration of 21 days. Choosing a
shorter or a longer period (7 or 14 days before and after the
GDD 100) for defining the duration of this period did not
change the final results.
Among the two networks, non-relevant vulnerable periods
for plants were found for 4 stations-years, because the GDD
WFJ 254 0
GRH 1970
DAV 1560
GRC 1550
SMM 1418
YBR 2 17 01
VLS 2 207 0
VIN2 2730
VDS 2 23 90
TUM2 2195
TUJ3 22 20
TIT2 2140
TAM 3 2 1 7 0
STN 2 29
STH 2 17 80
SPN3 2420
SHE2 1850
SCB 2 17 70
SCA 3 23 30
SCA2 2030
SAA 2 24 80
PUZ 2 21 95 PMA 2 2 430
OFE2 2360
OBW2 24
OBM2 2110
NEN2 23 25
NAS2 2350
MUT2 2 474
MUO2 2 083
MUN2 2 210
MTR2 189 0 MES2 238 0
MEI2 221 0
MAE2 2165 LUK2 2550
KLO 2 21 40
ILI 2 2 02 0
HTR3 2200
HTR2 215 0
GOR2 2950
GOM3 2430
GOM2 2450
GAN2 2717
GAD2 2060
FRA2 2100
FNH2 2240
FLU2 2390
FIR2 2110
FAE 2 1 9 7 0
ELM2 2050
DAV2 2560
CON2 2 230
CMA2 2 330
BER2 2450
BED3 2100
ARO 3 26 10
ARO2 2850
ANV3 2590
ALI 2 171 6
ROA2 187 0
BED 2 24 50
ANV2 2630
0 30609012015
IMIS stations
MeteoSwiss stations
WSL/LWF, Flurin Sutter, 2018
Source: B FS GEO STAT / Bundesamt für L andest opographi e
Fig. 1 Map of Switzerland showing the location and elevation of the 83 weather stations of both IMIS and MeteoSwiss networks used in the analyses
Int J Biometeorol (2018) 62:17551762 1757
100 was not reached before 1 September that defines the be-
ginning of the following year and were thus discarded from
the analysis (for the IMIS network: station GAN2 at 2717 m
asl in 1999 and 2004 and for the MeteoSwiss network: station
WFJ at 2540 m asl in 1978 and 1980).
For calculating the day of the year (abbreviated DOY here-
after) of the GDD 100 from the time of snowmelt, we first
computed the daily mean temperature for both networks,
based on the mean of the daily minimum and maximum air
temperature. We then accumulated all daily mean temperature
values >0 °C from the time of snowmelt, until reaching
100 °C.
Yearly snowmelt date anomalies of each IMIS and
MeteoSwiss weather station were determined by calculating
the difference between the yearly time of snowmelt and the
mean time of snowmelt of each station over the period 1998
2016, if at least 50% of the snowmelt dates were available.
In our analysis, we considered frost events below C
during the vulnerable period for plants, as this threshold cor-
responds to the lowest freezing resistance of numerous com-
mon plant species from the European Central Alps, typically
growing in snowbed conditions where the IMIS stations are
located (Ladinig et al. 2013; Taschler and Neuner 2004). The
intensity of frost was calculated by extracting the absolute
minimum air temperature occurring during this vulnerable
period. The last frost day of the season was defined as the last
occurrence of frost below 4 °C for each year (1 September
31 August).
General spatial and temporal patterns analyzed in this
study were tested across all stations within each IMIS and/
or MeteoSwiss network, by using mixed effect models
with stations or elevation as a random effect. Different
model types were tested for each analysis (linear and
non-linear models, such as polynomial or exponential
models). The best model for each relationship was then
selected based on the lowest Akaike information criterion
(AIC). Comparisons between each model (mixed or fixed
effect models) were conducted using ANOVA to test
whether they significantly differ. Detailed statistics of each
selected mixed effect model are presented in Supplementary
Material (Online Resource 1).
All individual temporal analyses reported in this study were
performed for each MeteoSwiss station, by applying the non-
parametric Theil-Sen estimator slope, combined with a Mann-
Kendall significance test over the common temporal period
for all six stations (19702016), as most of the analyzed pa-
rameters were not following a normal distribution (verified
using Shapiro tests). No consistent breakpoints were detected
(tested by step-wise regressions) in the temporal trends for all
parameters and stations over the study period.
All analyses, tables and figures were performed using R 3.3
(R Core Team 2016) and the following R-packages: EnvStats,
Kendall, Hmisc, nlme, and plotrix.
Temporal trends of the monthly minimum
and maximum air temperatures
A global increase of the monthly mean minimum air tempera-
tures was detected over the study period at the six MeteoSwiss
stations in the Swiss Alps, but with strong disparities across
seasons (Online Resource 2). While only slight warming was
detected during winter, minimum air temperatures increased
considerably during spring and summer, especially during the
snowmelt period from April to June, with rates ranging on
average from + 0.42 ± 0.05 °C decade
to + 0.72 ± 0.06 °C
in May and April, respectively (Fig. 2). Similar re-
sults were found for the warming rate of mean maximum air
temperatures, with slightly higher values than for minimum air
temperatures in spring, ranging from + 0.52 ± 0.13 °C de-
in April, and with
lower values from September to December (Fig. 2).
Relationships between snowmelt and frost frequency
and intensity within stations
The mixed effect models, both with stations or elevation as a
random effect, showed significant exponential and linear relation-
ships across all stations for both IMIS and MeteoSwiss networks
(P< 0.001), between snowmelt anomalies and frost frequency or
Fig. 2 Estimated trends (slope per decade) with associated standard
errors for the monthly mean minimum (blue bars) and maximum air
temperatures (red bars), averaged from the six MeteoSwiss stations over
the period 19702016 and calculated from the Theil-Sen tests. The
significance level of the Theil-Sen slopes was calculated with Mann-
Kendall tests and is indicated with stars (*P< 0.05, **P< 0.01, and
1758 Int J Biometeorol (2018) 62:17551762
frost intensity during the vulnerable period for subalpine and al-
pine plants across the study years (Fig. 3).Theearlierthetimeof
snowmelt, the more frequent and intense the frost events during
the vulnerable period for plants in the Swiss Alps, irrespective of
elevation, the temporal period analyzed (19982016 or 1970
2016), or the network used (IMIS or MeteoSwiss).
Temporal trends of the frost day frequencies
and intensities
The date corresponding to the GDD 100 after the time of
snowmelt has advanced significantly across all six available
MeteoSwiss stations during the period 19702016, when
using both stations or elevation as a random effect (P<
0.001) (Fig. 4a). Individual rates per station ranged from
4.3 ± 0.1 to 7.0 ± 0.1 days decade
(Online Resource 3).
However, no significant general patterns were found for the
temporal variations of the frequency or intensity of frost dur-
ing the vulnerable period for plants over the period 1970
2016 (respective pvalues of 0.45 and 0.13) (Fig. 4b, c).
Occurrence of the last frost day of the season
The last frost day of the season (1 September-31 August) advanced
significantly during the period 19702016 across all six
MeteoSwiss stations, when using both stations or elevation as a
random effect (P< 0.001) (Fig. 5a). These trends ranged from
1.0 ± 0.2 to 10.0 ± 0.4 days decade
depending on stations
(Online Resource 3). As both the time of snowmelt (see Klein et
al. 2016) and the occurrence of the last frost day of the season
advanced over the last five decades at similar rates, we did not find
any general pattern across all six MeteoSwiss stations for the du-
ration of the period between the time of snowmelt and the occur-
rence of the last frost day of the season (Pvalue 0.32) (Fig. 5b).
Relationship between snowmelt and frost exposure
for plants
Through the analysis of two independent high-elevation
weather networks in the Swiss Alps over the period 1970
2016, our study demonstrates the strong connection between
the time of snowmelt and the spatial and temporal distribution
of the risk of frost events during the early growing season for
subalpine and alpine plants. Specifically, our analysis focused
on the most vulnerable period for plants to freezing events, i.e.,
the time shortly after snowmelt occurring generally between
spring and early summer in subalpine and alpine regions.
Fig. 3 Relationships within
stations between snowmelt
anomalies and frost frequency (a,
b) or frost intensity (c, d) during
the vulnerable period for plants,
separated for each IMIS and
MeteoSwiss networks over the
periods 19982016 and 1970
2016, respectively. The black line
corresponds to the predicted
values from the best mixed effect
model (with stations as a random
effect), plotted when significant at
Int J Biometeorol (2018) 62:17551762 1759
On average, we found that in years with early snowmelt,
the frequency and intensity of frost were higher, regardless
of elevation. This finding is in agreement with results of
previous studies conducted in the Rocky Mountains
(Inouye 2008; Inouye et al. 2002)orintheSwissAlps
(Wipf et al. 2009). Our results were consistent across both
IMIS and MeteoSwiss networks and showed a consistent
relationship between snowmelt and frost risk, whether we
looked at numerous stations over a short period of time or at
only a few stations over 46 years. Our results were also
consistent for stations located in dryer or more humid re-
gions (data not shown), according to the yearly mean pre-
cipitations map in Switzerland over the 19812010 period
(MeteoSwiss website, unpublished work).
Despite a very high interannual variability of both plant
phenology and snowmelt timing, our methodology for ana-
lyzing the risk of frost exposure for subalpine and alpine
plants provided robust results, as findings were very similar
when testing different durations for the vulnerable period
around the GDD 100. This approach may thus be mainly
valid for alpine species inhabiting snowbed conditions,
where plants are generally more sensitive to frost, but also
for species which are able to start their growth before the time
of snowmelt, such as Crocus albiflorus, one of the first spe-
cies to start growing and flowering when the snow cover
becomesverythin(Rixenetal.2008). It may, however, be
less valid for species inhabiting ridge habitats (e.g.,
Loiseleuria procumbens), which are generally more freezing
resistant than snowbed species. Our findings suggest that
early snowmelt and a long growing season are not necessar-
ily beneficial for plants, as during such years, plants are more
exposed to freezing temperatures during the vulnerable peri-
od of initial growth. Furthermore, earlier phenology was
found to be a costly strategy for certain alpine plants when
their habitat faces temperature warming (Scheepens and
Stöcklin 2013).
Fig. 4 Temporal variations of the yearly aGDD 100 calculated from the
time of snowmelt and frost bfrequencies, and cintensities calculated
during the vulnerable period for plants across the six MeteoSwiss
stations over the period 19702016. The black line corresponds to the
predicted values from the best mixed effect model (with stations as a
random effect), plotted when significant at P<0.05
Fig. 5 Temporal trends of the
yearly alast frost day of the
season and bduration between
this last frost day and the time of
snowmelt across all six
MeteoSwiss stations over the
period 19702016. The black line
corresponds to the predicted
values from the best mixed effect
model (with stations as a random
effect), plotted when significant at
1760 Int J Biometeorol (2018) 62:17551762
Trends in temperatures, timing of snowmelt,
and frost exposure
We found that both minimum and maximum air temperatures
have increased over the period 19702016 for all six
MeteoSwiss stations used in this study, and particularly during
the period where snowmelt generally occurs at these eleva-
tions (AprilJune), with average rates exceeding 0.5 °C de-
for the maximum air temperatures. This result is con-
sistent with previous studies, showing similar temperature
trends during spring and summer (Rebetez and Reinhard
2008). The high consistency observed among the six
MeteoSwiss stations indicates a general warming that may
not be related to local climate conditions only. The stronger
temperature increase observed in spring, corresponding to the
mean snowmelt period, could be partly explained by the
snow-albedo positive feedback loop described by Scherrer et
al. (2012). This aforementioned study showed that around the
snow line in the Swiss Alps, a spring day without snow cover
is on average 0.4 °C warmer than a spring day with snow
cover at the same location (Scherrer et al. 2012).
Despite the strong relationships found between snowmelt
anomalies and the frequency or intensity of frost events during
the vulnerable period for subalpine and alpine plants, no con-
sistent temporal trends were found for the frequency or inten-
sity of frost over the period 19702016. The stable frost ex-
posure risk for plants found in this study may be explained by
the compensatory effect of a similar increase in minimum and
maximum air temperatures observed over the period 1970
2016. Increasing maximum air temperatures have contributed
to the advance of both snowmelt and spring phenology, while
increasing minimum temperatures have delayed the last po-
tentially damaging frost, resulting in an overall unchanged
risk of frost damage.
A faster worldwide increase of maximum air temperatures
than minimum air temperatures in spring in high-elevation re-
gions (Rangwala et al. 2013), as well as a reduction of the snow
cover thickness and duration at all elevations in the Swiss Alps,
strongly connected to temperature warming (Schmucki et al.
2015;Stegeretal.2013) are expected over the next decades.
This prediction, following the general trends of temperature
warming and snowmelt observed since 1970 in the Swiss
Alps, suggests that the risk of frost exposure for subalpine
and alpine plants might not be reduced and may even increase
in the near future. Longer growing seasons with unchanged
risk of frost damage may help plants adapted to such harsh
environment to persist longer when more competitive lowland
species migrate upslope (Matteodo et al. 2013; Steinbauer et al.
2018), as plants have generally a stronger freezing resistance at
higher elevation (Sierra-Almeida et al. 2009). An increase in
plant height and biomass production is also expected by the
end of the century in the Swiss Alps, in connection with an
earlier time of snowmelt and onset of growth for plants, but
without taking into account the risk of frost exposure for plants
(Rammig et al. 2010; Carlson et al. 2017).
However, with the predicted reduction in snow cover du-
ration over the next decades, we may expect that the snow
cover will become too thin, removing the snow insulation
effect against late frost events, eventually resulting in an in-
crease of the frost exposure for plants. Warming air tempera-
tures was also shown to increase the freezing sensitivity of
plants during the beginning of their growing season (Martin
et al. 2010). With future climate warming and a weaker
protecting effect of the snow cover against frost, the risk of
exposure to frost damage for subalpine and alpine plants may
increase over the next decades.
The time of snowmelt is a major factor determining the expo-
sure of subalpine and alpine plants to late frost events, as
plants become coupled with surrounding air temperature. By
using long-term series of snow and temperature parameters at
high-elevation in the Swiss Alps, we showed that an early time
of snowmelt generally leads to an increasing frequency and
intensity of frost during the vulnerable period for plants, irre-
spective of elevation or the temporal period analyzed (1998
2016 or 19702016). However, despite climate warming and
the general decline of both snowmelt timing and last frost day
of the season in the Swiss Alps, our study suggests that the
frequency and intensity of frost during the vulnerable period
for plants have remained unchanged over the period 1970
2016. This absence of trends may be explained by the similar
increase of minimum and maximum air temperatures found
over the same period, which has shifted spring phenology and
the last occurrence of potentially damaging frost to a same
extent. Longer growing season with unchanged risk of frost
damage may help plants adapted to such harsh environment to
persist longer, whereas new thermophile species colonizing
from lowlands areas could experience severe frost slowing
down their upward shift. It remains a future research challenge
if our results also hold in a global context of different alpine
climates. In oceanic regions with unpredictable climate, frost
can occur at any time of the year and hence, the freezing
resistance of plants can be higher than in regions with predict-
able snow cover (Bannister 2007; Bannister et al. 2005; Venn
et al. 2013). Understanding the role of frost events in different
climates will considerably improve our predictions of vegeta-
tion changes under ongoing climate.
Acknowledgements We are grateful to Christoph Marty for providing
IMIS temperature and snow data and to MeteoSwiss for providing
long-term series of temperature and snow data. We also thank Flurin
Sutter for drawing the map of the selected stations shown in Fig. 1and
Bradley Carlson for his editorial improvements of the manuscript.
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... However, this may not be the case at high elevations where the influence of warming on the probability of freezing events is more complicated and uncertain. With increasing annual or seasonal mean temperature, the occurrence of growing-season freezing events was found to increase in central Chilean Andes (Sierra-Almeida and Cavieres, 2010) and southeast Tibet (Shen et al., 2018) or to remain unchanged in Swiss Alps (Rixen et al., 2012;Klein et al., 2018). Due to the low-temperature photoinhibition resulting from the combination of freezing temperature at night and high solar radiation in daytime (Johnson et al., 2004;Coop and Givnish, 2008), the increase of early-season freezing events may seriously hamper seed-based seedling establishment above treeline (Shen et al., 2014). ...
... Globally, the decrease of snow cover in mountainous areas has been observed in recent decades, in which the shorter snow cover duration is mainly due to the earlier snow melting in spring (Pederson et al., 2013;Klein et al., 2016;Xu et al., 2016). It has been reported that shallower snow pack and earlier snow melting are associated with earlier start of the growing season (Vaganov et al., 1999;Huang et al., 2019), which may result in higher frequency and intensity of frost in the early growing season (Klein et al., 2018). To our knowledge, however, there is lack of long-term and continuous measurements of microclimate factors to examine how the variations of growing season onset and snow cover drive the spatiotemporal variability of growing-season freezing events at alpine treelines. ...
... Over the past 40 years, the weakening of Indian summer monsoon and the reduction of cloud cover on the south side of the Himalayas have increased the incoming solar radiation in daytime but reduced the downward long-wave radiation at night (Yue et al., 2020), suggesting that the early-season freezing events may increase and the treelines may remain stable as observed in Sigdel et al. (2018). In the Swiss Alps, however, the maximum of global radiation occurs in summer (June and July) and the radiative cooling effect in the early growing season (April and May) can be mitigated by high cloud cover and low global radiation (Rottler et al., 2019), which explains why the early-season freezing events show no relation to increased temperature and advanced growing season in recent decades (Rixen et al., 2012;Klein et al., 2018). ...
Few data have demonstrated why early-season freezing events may increase under a warmer climate at alpine treelines, which is critical to understand the key limiting factors determining treeline dynamics under future climate warming. Here we test the hypothesis that the increase of early-season freezing events under a warmer climate is mainly associated with advanced onset of growing season and enhanced radiative cooling effect in the pre-monsoon season. We conducted 11-year observations of microclimate factors across north-facing and south-facing treelines in the Sergyemla Mountains, southeast Tibet. We found that the frequency, intensity, and duration of early-season freezing events were generally higher under a warmer climate on the south-facing slope or in the warmer years within a slope, in which the frequency of early-season freezing events significantly increased with increasing annual mean air-temperature. During 2006–2016, the frequency, intensity and duration of early-season freezing events typically showed a negative correlation with the onset date of growing season, while their frequency was positively correlated with the early-season global radiation. In each of both slopes, global radiation was significantly higher and long-wave radiation balance was much more negative on days with daily minimum air-temperature (Tmin) < 0 °C than with Tmin > 0 °C, indicating the generality of radiative cooling effect on early-season freezing events at high elevations. Our data support the hypothesis, revealing physical mechanisms for the increase of early-season freezing events with climate warming. The physical mechanisms should provide a general explanation for the topography-dependent pattern of tree species distribution and alpine treeline stability under climate warming in high mountainous regions like the Himalayas.
... Climate change shapes alpine vegetation and plant diversity in different ways. For instance, the increase in temperatures recorded in the last decades [21,22] has consistently altered alpine and nival species' distribution. In several European alpine plant communities, a general increase in species richness [23][24][25] was registered and it was explained as a "thermophilization process", which consists of the upward shifting of thermophilic plants towards higher altitudes [23,[26][27][28][29][30][31][32][33][34][35], or as a "range-filling process", performed by species dispersing from existing neighbor communities within the same elevation belt [36,37]. ...
... Considering the consistent and heterogeneous changes ongoing on alpine ecosystems, likely related with both the increase in temperatures [21,22] and the reduction in annual rainfalls [1,42,[48][49][50][51], the present work sets out to explore vegetation dynamics on alpine Mediterranean calcareous grasslands and swards in central Apennines (Italy). Through a re-visitation vegetation study (after 18 years), we explored the temporal changes in two alpine communities in the Maiella National Park (MNP) that are representative of the central Apennine's alpine belt: Apennine stripped grasslands, growing on steep slopes, and wind edge swards, both included in the 6170 EU Habitat "alpine and subalpine calcareous grasslands" [52,53]. ...
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Global change threatens alpine biodiversity and its effects vary across habitat types and biogeographic regions. We explored vegetation changes over the last 20 years on two Mediterranean alpine calcareous grasslands in central Apennines (Italy): stripped grasslands (EUNIS code E4.436) with Sesleria juncifolia growing on steep slopes, and wind edge swards (EUNIS code E4.42) with Carex myosuroides. Based on a re-visitation of 25 vegetation plots of 4 × 4 m, we assessed changes in overall and endemic plant species cover and richness by nonparametric Kruskal-Wallis test. We explored changes in structure and ecology using growth forms and Landolt indicators for temperatures. We identified species' contribution to temporal changes using the similarity percentage procedure (SIMPER). The results evidenced a significant decline in all species cover and richness on both plant communities with a significant decline in alpine and endemic species and in hemicryptophytes with rosette and scapose ones on stripped grasslands, as well as a decline in subalpine and suffruticose chamaephytes species on wind edge swards. Such biodiversity loss, so far observed only in the warmest and Southern Mediterranean summits of Europe, is likely attributable to the combined effect of higher temperatures; the increase in the vegetative period; and the decrease in water availability, which is particularly severe in calcareous regions. Our study suggested the vulnerability of the analyzed alpine ecosystems to global change and the importance of monitoring activities to better understand vegetation trends and adaptation strategies in subalpine, alpine, and nival ecosystems.
... The effect of temperature was found to be a decisive factor in the change of phenological dates of SOS and POS, in agreement with Ganjurjav et al. [69] and Ren et al. [63], also influencing phenology spatially [70]. Consequently, the rise in temperatures recorded in the 2001-2021 time frame could also have had an indirect effect on the advancement of the SOS date by causing an advancement in the snowmelt dates recorded in recent years [71], without the risk of increasing frost exposure [72]. Snow melt and snow cover are indeed decisive in determining the length of the growing season and the phenological development of high-altitude and high-latitude grasslands [73,74], also influencing water availability or thermal conditions by soil insulation [75]. ...
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The use of very long spatial datasets from satellites has opened up numerous opportunities, including the monitoring of vegetation phenology over the course of time. Considering the importance of grassland systems and the influence of climate change on their phenology, the specific objectives of this study are: (a) to identify a methodology for a reliable estimation of grassland phenological dates from a satellite vegetation index (i.e., kernel normalized difference vegetation index, kNDVI) and (b) to quantify the changes that have occurred over the period 2001–2021 in a representative dataset of European grasslands and assess the extent of climate change impacts. In order to identify the best methodological approach for estimating the start (SOS), peak (POS) and end (EOS) of the growing season from the satellite, we compared dates extracted from the MODIS-kNDVI annual trajectories with different combinations of fitting models (FMs) and extraction methods (EM), with those extracted from the gross primary productivity (GPP) measured from eddy covariance flux towers in specific grasslands. SOS and POS were effectively identified with various FM×EM approaches, whereas satellite-EOS did not obtain sufficiently reliable estimates and was excluded from the trend analysis. The methodological indications (i.e., FM×EM selection) were then used to calculate the SOS and POS for 31 grassland sites in Europe from MODIS-kNDVI during the period 2001–2021. SOS tended towards an anticipation at the majority of sites (83.9%), with an average advance at significant sites of 0.76 days year−1. For POS, the trend was also towards advancement, although the results are less homogeneous (67.7% of sites with advancement), and with a less marked advance at significant sites (0.56 days year−1). From the analyses carried out, the SOS and POS of several sites were influenced by the winter and spring temperatures, which recorded rises during the period 2001–2021. Contrasting results were recorded for the SOS-POS duration, which did not show a clear trend towards lengthening or shortening. Considering latitude and altitude, the results highlighted that the greatest changes in terms of SOS and POS anticipation were recorded for sites at higher latitudes and lower altitudes.
... At the alpine scale, this earlier snow removal-induced frost exposure is probably, for the moment, mostly visible in Southern regions and/or at low altitude. For instance, in the Swiss Alps (northernmost and innermost compared to the French Alps), Klein et al. (2018) have found that the frost risk to plants during their early development stage has been unchanged over the last decades, due to the fact that minimum and maximum air temperatures have risen at approximately the same rate, which has advanced in the same way the phenology of alpine plants and the latest frost events. ...
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Summer mountain pastures (also called alpages ) are a central element for many agro-pastoral livestock systems in the alpine region, by providing the feedstock for herds during the summer transhumance. However, vegetation phenology and productivity in mountain pastures are increasingly affected by climate hazards exacerbated by climate change, such as early snow removal, late frost events, or droughts. Difficulties can then arise to match animal demand with forage resource on alpages and, in the long term, threaten the sustainable management of these highly multifunctional socio-ecological systems. To help agro-pastoral actors adapt, an essential step is to quantify the risk of impacts on the forage resource, due to an increased occurrence or intensity of climate hazards. Exposure to climate hazards on alpages is defined locally by topographic aspects in combination with the broader influence of the regional climate. Our work therefore aimed at providing a tailored assessment of potential climate risk for the forage resource at the individual scale of each alpage in the French Alps. To this end, we developed agro-climatic indicators based on atmospheric and snow cover data accounting for geographic and topographic conditions, and applied them to a database providing unique spatially explicit information at the alpage level. For the first time, we introduce a description of agro-climatic conditions and provide a classification of agro-climatic profiles of alpages in the French Alps, ranging from low to high potential risk for the forage resource, mainly following a North-South gradient combined with altitude. We also bring insights on the evolutions of the climate risk with climate change and discuss management implications for agro-pastoral livestock systems using alpages . We finally present a web-based visualization tool that aim at communicating agro-climatic profiles and their evolution to practitioners and at assisting decision makers in understanding climate-related risks on the alpages of the French Alps.
... We used climatic data recorded at the automatic weather station (AWS) Segl-Maria (Swiss National Basic Climatological Network), the closest station to our study sites providing a long climatic data series (1864-2018) including monthly air temperature, monthly total precipitation and total annual snow cover (Scherrer et al. 2013). Data from this AWS are representative of the climatic trends for the Swiss Alps (Klein et al. 2016(Klein et al. , 2018 and specifically of the climatic trends of upper Valtellina, as confirmed by statistically significant linear regressions against data from the four main AWSs in operation across our study area, which individually have shorter data series (Supporting information). ...
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Shrub encroachment, a globally recognized response to climate warming, usually involves late successional species in mountain environments, without alteration to climax communities. We show that a major ecosystem change is occurring in the European Alps across a 1000 m elevation gradient, with pioneer hygrophilous Salix shrubs, previously typical of riparian forests, wetlands and avalanche ravines, encroaching into the climax communities of subalpine and alpine belts shrublands and grasslands, as well as snowbeds, pioneer vegetation and barren grounds in the nival belt. We analyzed Salix recruitment through dendrochronological methods, and assessed its relationships with climate and atmospheric CO2 concentration. The dendrochronological data indicated that Salix encroachment commenced in the 1950s (based on the age of the oldest Salix individuals, recruited in 1957), and that it was correlated with increasing atmospheric CO2 concentration, spring warming and snow cover decrease. Hygrophilous Salix shrubs are expanding their distribution both through range filling and upwards migration, likely achieving competitive replacement of species of subalpine and alpine climax communities. They benefit from climate warming and CO2 fertilization and are not sensitive to spring frost damage and soil limitations, being observed across a gradient of soil conditions from loose glacial sediments in recently deglaciated areas (where soils had not had sufficient time to develop) to mature soils such as podzols (when colonizing late successional subalpine shrublands). Salix encroachment may trigger ecosystem and landscape transformations, promoting the development of forests that replace pre-existing subalpine shrublands, and of open woodlands invading alpine grasslands and snowbeds, making the alpine environment similar to sub-Arctic and Arctic areas. This results in a new threat to the conservation of the plant species, communities and landscapes typical of the alpine biota, as mountain ranges such as the Alps provide limited opportunities for upward migration and range-shift.
... In a comparison of arctic and alpine plant species, Oberbauer et al. [26] also found that many species are not just tracking temperature but rather perform a conservative phenology that suggests a modulating role of photoperiod. Comparing snowmelt date and the occurrence and severity of freezing events soon after snowmelt over the past 46 years, Klein et al. [27] found no enhanced risk by frost in the Swiss Alps. This conclusion rests on the assumption that plants are tracking snowmelt data so that they arrive at similar developmental stages soon after snowmelt irrespective of when snowmelt occurs. ...
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The alpine belt hosts the treeless vegetation above the high elevation climatic treeline. The way alpine plants manage to thrive in a climate that prevents tree growth is through small stature, apt seasonal development, and ‘managing’ the microclimate near the ground surface. Nested in a mosaic of micro-environmental conditions, these plants are in a unique position by a close-by neighborhood of strongly diverging microhabitats. The range of adjacent thermal niches that the alpine environment provides is exceeding the worst climate warming scenarios. The provided mountains are high and large enough, these are conditions that cause alpine plant species diversity to be robust against climatic change. However, the areal extent of certain habitat types will shrink as isotherms move upslope, with the potential areal loss by the advance of the treeline by far outranging the gain in new land by glacier retreat globally.
... Hence, with the documented earlier onset of snowmelt occurring in response to warmer winter and spring temperatures in documented in the European Alps (Beniston, 2012;Hall et al., 2015;Klein et al., 2016), surface pond embryos may be exposed to a greater risk of frost, which in turn would influence embryonic survival (Beattie, 1987;Frisbie et al., 2000;Muir et al., 2014) and population dynamics. This phenomenon has been observed for plants (Inouye, 2008), where the change in last spring frost timing is slower than the shift in plant phenology, leading to higher plant mortality Pardee et al., 2019; but see Klein et al., 2018 for evidence of consistent advances in snowmelt timing and last spring frost, leading to unchanged plant exposure to frost frequency and intensity). ...
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The alarming decline of amphibians around the world calls for complementary studies to better understand their responses to climate change. In mountain environments, water resources linked to snowmelt play a major role in allowing amphibians to complete tadpole metamorphosis. As snow cover duration has significantly decreased since the 1970s, amphibian populations could be strongly impacted by climate warming, and even more in high elevation sites where air temperatures are increasing at a higher rate than at low elevation. In this context, we investigated common frog ( Rana temporaria ) breeding phenology at two different elevations and explored the threats that this species faces in a climate change context. Our objectives were to understand how environmental variables influence the timing of breeding phenology of the common frog, and explore the threats that amphibians face in the context of climate change in mountain areas. To address these questions, we collected 11 years (2009–2019) of data on egg-spawning date, tadpole development stages, snowmelt date, air temperature, rainfall and drying up of wetland pools at ∼1,300 and ∼1,900 m a.s.l. in the French Alps. We found an advancement of the egg-spawning date and snowmelt date at low elevation but a delay at high elevations for both variables. Our results demonstrated a strong positive relationship between egg-spawning date and snowmelt date at both elevations. We also observed that the risk of frost exposure increased faster at high elevation as egg-spawning date advanced than at low elevation, and that drying up of wetland pools led to tadpole mortality at the high elevation site. Within the context of climate change, egg-spawning date is expected to happen earlier in the future and eggs and tadpoles of common frogs may face higher risk of frost exposure, while wetland drying may lead to higher larval mortality. However, population dynamics studies are needed to test these hypotheses and to assess impacts at the population level. Our results highlight climate-related threats to common frog populations in mountain environments, but additional research should be conducted to forecast how climate change may benefit or harm amphibian populations, and inform conservation and land management plans in the future.
... Spring phenology is advancing under climate change (Fu et al., 2014;Roberts et al., 2015;Thackeray et al., 2016). However, advances in the timing of key spring phenological events such as bud-burst can be greater than the advance in the date of the latest spring frost (Klein et al., 2018;Vitasse et al., 2018), andZohner et al. (2020) found that latespring frost risk has increased in Europe since 1959. Furthermore, some environmental factors, such as photoperiod, will not vary under climate change and interactions may be important. ...
Genetic variation and phenotypic plasticity play a role in determining the performance of a tree provenance at a planting site. This paper explores their relative importance in determining growth, phenology and tree form in a broad geographic sample of 42 British provenances of common ash (Fraxinus excelsior L.) grown at two contrasting trial sites. We found significant genetic differences for tree height, timing of leaf flushing and leaf senescence, and stem forking among the provenances. These followed a clear latitudinal and climatic cline, where the northern provenances were shorter, their leaves flushed later and senesced earlier than the southern provenances. Provenance explained a much larger proportion of the variance for spring phenology (63 per cent) than for autumn phenology (15 per cent). The effect of the planting site was contrasting between spring and autumn: spring phenology showed very little plasticity, while autumn phenology presented higher levels of phenotypic plasticity. This could indicate that for ash spring phenology is under stronger selective pressure. We found a correlation between tree height, leaf phenology and forking, with early flushing provenances tending to be taller and more forked, which could reflect repeated frost damage. The findings underline the complexity of predicting performance in novel environments and demonstrate that small gains in tree growth may be counteracted by detrimental effects on stem form, a key contributor to timber value, due to susceptibility to the contemporary environment.
... During the 20th century Phenological and elevational shifts in the Alps in Western Europe, air temperatures warmed more in winter compared to summer (Moberg et al., 2006), but this ratio reversed by the end of the 20th and early 21st century . Hence, several studies have shown that summer and spring have warmed more than autumn and winter since the 1970s (Rebetez & Reinhard, 2008;Klein et al., 2018;Vitasse et al., 2018a). Since the end of the 1980s, maximum air temperatures have been increasing more than minimum temperatures in connection with the decrease in European air pollution and particulate matter, especially in spring and at mid and high elevations (Rebetez & Reinhard, 2008;Vitasse et al., 2018a). ...
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Mountain areas are biodiversity hotspots and provide a multitude of ecosystem services of irreplaceable socio‐economic value. In the European Alps, air temperature has increased at a rate of about 0.36°C decade−1 since 1970, leading to glacier retreat and significant snowpack reduction. Due to these rapid environmental changes, this mountainous region is undergoing marked changes in spring phenology and elevational distribution of animals, plants and fungi. Long‐term monitoring in the European Alps offers an excellent natural laboratory to synthetize climate‐related changes in spring phenology and elevational distribution for a large array of taxonomic groups. This review assesses the climatic changes that have occurred across the European Alps during recent decades, spring phenological changes and upslope shifts of plants, animals and fungi from evidence in published papers and previously unpublished data. Our review provides evidence that spring phenology has been shifting earlier during the past four decades and distribution ranges show an upwards trend for most of the taxonomic groups for which there are sufficient data. The first observed activity of reptiles and terrestrial insects (e.g. butterflies) in spring has shifted significantly earlier, at an average rate of −5.7 and −6.0 days decade−1, respectively. By contrast, the first observed spring activity of semi‐aquatic insects (e.g. dragonflies and damselflies) and amphibians, as well as the singing activity or laying dates of resident birds, show smaller non‐significant trends ranging from −1.0 to +1.3 days decade−1. Leaf‐out and flowering of woody and herbaceous plants showed intermediate trends with mean values of −2.4 and −2.8 days decade−1, respectively. Regarding species distribution, plants, animals and fungi (N = 2133 species) shifted the elevation of maximum abundance (optimum elevation) upslope at a similar pace (on average between +18 and +25 m decade−1) but with substantial differences among taxa. For example, the optimum elevation shifted upward by +36.2 m decade−1 for terrestrial insects and +32.7 m decade−1 for woody plants, whereas it was estimated to range between −1.0 and +11 m decade−1 for semi‐aquatic insects, ferns, birds and wood‐decaying fungi. The upper range limit (leading edge) of most species also shifted upslope with a rate clearly higher for animals (from +47 to +91 m decade−1) than for plants (from +17 to +40 m decade−1), except for semi‐aquatic insects (−4.7 m decade−1). Although regional land‐use changes could partly explain some trends, the consistent upward shift found in almost all taxa all over the Alps is likely reflecting the strong warming and the receding of snow cover that has taken place across the European Alps over recent decades. However, with the possible exception of terrestrial insects, the upward shift of organisms seems currently too slow to track the pace of isotherm shifts induced by climate warming, estimated at about +62 to +71 m decade−1 since 1970. In the light of these results, species interactions are likely to change over multiple trophic levels through phenological and spatial mismatches. This nascent research field deserves greater attention to allow us to anticipate structural and functional changes better at the ecosystem level.
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Snow is an important driver of ecosystem processes in cold biomes. Snow accumulation determines ground temperature, light conditions and moisture availability during winter. It also affects the growing season’s start and end, and plant access to moisture and nutrients. Here, we review the current knowledge of the snow cover’s role for vegetation, plant-animal interactions, permafrost conditions, microbial processes and biogeochemical cycling. We also compare studies of natural snow gradients with snow manipulation studies, altering snow depth and duration, to assess time scale difference of these approaches. The number of studies on snow in tundra ecosystems has increased considerably in recent years, yet we still lack a comprehensive overview of how altered snow conditions will affect these ecosystems. In specific, we found a mismatch in the timing of snowmelt when comparing studies of natural snow gradients with snow manipulations. We found that snowmelt timing achieved by manipulative studies (average 7.9 days advance, 5.5 days delay) were substantially lower than those observed over spatial gradients (mean range of 56 days) or due to interannual variation (mean range of 32 days). Differences between snow study approaches need to be accounted for when projecting snow dynamics and their impact on ecosystems in future climates.
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Globally accelerating trends in societal development and human environmental impacts since the mid-twentieth century1-7are known as the Great Acceleration and have been discussed as a key indicator of the onset of the Anthropocene epoch6. While reports on ecological responses (for example, changes in species range or local extinctions) to the Great Acceleration are multiplying8, 9, it is unknown whether such biotic responses are undergoing a similar acceleration over time. This knowledge gap stems from the limited availability of time series data on biodiversity changes across large temporal and geographical extents. Here we use a dataset of repeated plant surveys from 302 mountain summits across Europe, spanning 145 years of observation, to assess the temporal trajectory of mountain biodiversity changes as a globally coherent imprint of the Anthropocene. We find a continent-wide acceleration in the rate of increase in plant species richness, with five times as much species enrichment between 2007 and 2016 as fifty years ago, between 1957 and 1966. This acceleration is strikingly synchronized with accelerated global warming and is not linked to alternative global change drivers. The accelerating increases in species richness on mountain summits across this broad spatial extent demonstrate that acceleration in climate-induced biotic change is occurring even in remote places on Earth, with potentially far-ranging consequences not only for biodiversity, but also for ecosystem functioning and services.
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One hundred years ago, Andrew D. Hopkins estimated the progressive delay in tree leaf-out with increasing latitude, longitude, and elevation, referred to as "Hopkins' bioclimatic law." What if global warming is altering this well-known law? Here, based on ∼20,000 observations of the leaf-out date of four common temperate tree species located in 128 sites at various elevations in the European Alps, we found that the elevation-induced phenological shift (EPS) has significantly declined from 34 d⋅1,000 m-1 conforming to Hopkins' bioclimatic law in 1960, to 22 d⋅1,000 m-1 in 2016, i.e., -35%. The stronger phenological advance at higher elevations, responsible for the reduction in EPS, is most likely to be connected to stronger warming during late spring as well as to warmer winter temperatures. Indeed, under similar spring temperatures, we found that the EPS was substantially reduced in years when the previous winter was warmer. Our results provide empirical evidence for a declining EPS over the last six decades. Future climate warming may further reduce the EPS with consequences for the structure and function of mountain forest ecosystems, in particular through changes in plant-animal interactions, but the actual impact of such ongoing change is today largely unknown.
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We combined imagery from multiple sources (MODIS, Landsat-5, 7, 8) with land cover data to test for long-term (1984-2015) greening or browning trends of vegetation in a temperate alpine area, the Ecrins National Park, in the context of recent climate change and domestic grazing practices. We showed that over half (56%) of the Ecrins National Park displayed significant increases in peak normalized difference vegetation index (NDVI max) over the last 16 years (2000-2015). Importantly, the highest proportional increases in NDVI max occurred in rocky habitats at high elevations (> 2500 m a.s.l.). While spatial agreement in the direction of change in NDVI max as detected by MODIS and Landsat was high (76% overlap), correlations between log-response ratio values were of moderate strength (approx. 0.3). In the context of above treeline habitats, we found that proportional increases in NDVI max were higher between 1984 and 2000 than between 2000 and 2015, suggesting a slowing of greening dynamics during the recent decade. The timing of accelerated greening prior to 2000 coincided with a pronounced increase in the amount of snow-free growing degree-days that occurred during the 1980s and 1990s. In the case of grasslands and low-shrub habitats, we did not find evidence for a negative effect of grazing on greening trends, possibly due to the low grazing intensity typically found in the study area. We propose that the emergence of a longer and warmer growing season enabled high-elevation plant communities to produce more biomass, and also allowed for plant colonization of habitats previously characterized by long-lasting snow cover. Increasing plant productivity in an alpine context has potential implications for biodiversity trajectories and for ecosystem services in mountain landscapes. The presented evidence for long-term greening trends in a representative region of the European Alps provides the basis for further research on mechanisms of greening in alpine landscapes.
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Climate change can have a broad range of effects on ecosystems and organisms, and early responses may include shifts in vegetation phenology and productivity that may not coincide with the energetics and forage timing of higher trophic levels. We evaluated phenology, annual height growth, and foliar frost responses of forbs to a factorial experiment of snow removal (SR) and warming in a high-elevation meadow over two years in the Rocky Mountains, United States. Species included arrowleaf balsamroot (Balsamorhiza sagittata, early-season emergence and flowering) and buckwheat (Eriogonum umbellatum, semi-woody and late-season flowering), key forbs for pollinator and nectar-using animal communities that are widely distributed and locally abundant in western North America. Snow removal exerted stronger effects than did warming, and advanced phenology differently for each species. Specifically, SR advanced green-up by a few days for B. sagittata to >2 wk in E. umbellatum, and led to 5- to 11-d advances in flowering of B. sagittata in one year and advances in bud break in 3 of 4 species/yr combinations. Snow removal increased height of E. umbellatum appreciably (~5 cm added to ~22.8 cm in control), but led to substantial increases in frost damage to flowers of B. sagittata. Whereas warming had no effects on E. umbellatum, it increased heights of B. sagittata by >6 cm (compared to 30.7 cm in control plots) and moreover led to appreciable reductions in frost damage to flowers. These data suggest that timing of snowmelt, which is highly variable from year to year but is advancing in recent decades, has a greater impact on these critical phenological, growth, and floral survival traits and floral/nectar resources than warming per se, although warming mitigated early effects of SR on frost kill of flowers. Given the short growing season of these species, the shifts could cause uncoupling in nectar availability and timing of foraging.
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Global warming has strong impacts on snow cover, which in turn affects ecosystems, hydrological regimes and winter tourism. Only a few long-term snow series are available worldwide, especially at high elevation. Here, we analyzed several snowpack characteristics over the period 1970–2015 at eleven meteorological stations, spanning elevations from 1139 to 2540 m asl in the Swiss Alps. Snow cover duration has significantly shortened at all sites, on average by 8.9 days decade−1. This shortening was largely driven by earlier snowmelt (on average 5.8 days decade−1) and partly by later snow onset but the latter was significant in only ~30 % of the stations. On average, the snow season now starts 12 days later and ends 26 days earlier than in 1970. Overall, the annual maximum snow depth has declined from 3.9 to 10.6 % decade−1 and was reached 7.8 ± 0.4 to 12.0 ± 0.4 days decade−1 earlier, though these trends hide a high inter-annual and decadal variability. The number of days with snow on the ground has also significantly decreased at all elevations, in all regions and for all thresholds from 1 to 100 cm. Overall, our results demonstrate a marked decline in all snowpack parameters, irrespective of elevation and region, and whether for drier or wetter locations, with a pronounced shift of the snowmelt in spring, in connection with reinforced warming during this season.
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Himalayan mountain glaciers and the snowpack over the Tibetan Plateau provide the headwater of several major rivers in Asia. In situ observations of snow cover extent since the 1960s suggest that the snowpack in the region have retreated significantly, accompanied by a surface warming of 2–2.5 °C observed over the peak altitudes (5000 m). Using a high-resolution ocean–atmosphere global climate model and an observationally constrained black carbon (BC) aerosol forcing, we attribute the observed altitude dependence of the warming trends as well as the spatial pattern of reductions in snow depths and snow cover extent to various anthropogenic factors. At the Tibetan Plateau altitudes, the increase in atmospheric CO2 concentration exerted a warming of 1.7 °C, BC 1.3 °C where as cooling aerosols cause about 0.7 °C cooling, bringing the net simulated warming consistent with the anomalously large observed warming. We therefore conclude that BC together with CO2 has contributed to the snow retreat trends. In particular, BC increase is the major factor in the strong elevation dependence of the observed surface warming. The atmospheric warming by BC as well as its surface darkening of snow is coupled with the positive snow albedo feedbacks to account for the disproportionately large role of BC in high-elevation regions. These findings reveal that BC impact needs to be properly accounted for in future regional climate projections, in particular on high-altitude cryosphere.
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In alpine environments, the growing season is severely constrained by low temperature and snow. Here, we aim at determining the climatic factors that best explain the interannual variation in spring growth onset of alpine plants, and at examining whether photoperiod might limit their phe- nological response during exceptionally warm springs and early snowmelts. We analysed 17 years of data (1998–2014) from 35 automatic weather stations located in subalpine and alpine zones ranging from 1560 to 2450 m asl in the Swiss Alps. These stations are equipped with ultrasonic sensors for snow depth measurements that are also able to detect plant growth in spring and summer, giving a unique opportunity to analyse snow and climate effects on alpine plant phenology. Our analysis showed high phenological variation among years, with one exceptionally early and late spring, namely 2011 and 2013. Overall, the timing of snowmelt and the beginning of plant growth were tightly linked irrespective of the elevation of the station. Snowmelt date was the best predictor of plant growth onset with air temperature after snowmelt modulating the plants’ development rate. This multiple series of alpine plant phenology suggests that currently alpine plants are directly tracking climate change with no major photoperiod limitation.
Winters and early springs are predicted to become warmer in temperate climates under continued global warming, which in turn is expected to promote earlier plant development. By contrast, there is no consensus about the changes in the occurrence and severity of late spring frosts. If the frequency and severity of late spring frosts remain unchanged in the future or change less than spring phenology of plants does, vulnerable plant organs (dehardened buds, young leaves, flowers or young fruits) may be more exposed to frost damage. Here we analyzed long-term temperature data from the period 1975–2016 in 50 locations in Switzerland and used different phenological models calibrated with long-term series of the flowering and leaf-out timing of two fruit trees (apple and cherry) and two forest trees (Norway spruce and European beech) to test whether the risk of frost damage has increased during this period. Overall, despite the substantial increase in temperature during the study period, the risk of frost damage was not reduced because spring phenology has advanced at a faster rate than the date of the last spring frost. In contrast, we found that the risk of frost exposure and subsequent potential damage has increased for all four species at the vast majority of stations located at elevations higher than 800 m while remaining unchanged at lower elevations. The different trends between lower and higher elevations are due to the date of the last spring frost moving less at higher altitudes than at lower altitudes, combined with stronger phenological shifts at higher elevations. This latter trend likely results from a stronger warming during late compared to earlier spring and from the increasing role of other limiting factors at lower elevations (chilling and photoperiod). Our results suggest that frost risk needs to be considered carefully when promoting the introduction of new varieties of fruit trees or exotic forest tree species adapted to warmer and drier climates or when considering new plantations at higher elevations.