Earlier snowmelt and warming lead to earlier but not necessarily more plant growth
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Earlier snowmelt and warming lead to earlier but not necessarily more plant growth
Carolyn Livensperger 2
Heidi Steltzer 1
Anthony Darrouzet-Nardi 0
Patrick F. Sullivan 4
Matthew Wallenstein 2
Michael N. Weintraub 3
Associate Editor: Colin M. Orians
0 Department of Biological Sciences, University of Texas at El Paso , El Paso, TX 79968 , USA
1 Biology Department, Fort Lewis College , Durango, CO 81301 , USA
2 Department of Ecosystem Science and Sustainability, Colorado State University , Fort Collins, CO 80523 , USA
3 Department of Environmental Sciences, University of Toledo , Toledo, OH 43606 , USA
4 Environment and Natural Resources Institute, University of Alaska Anchorage , Anchorage, AK 99508 , USA
Climate change over the past 50 years has resulted in earlier occurrence of plant life-cycle events for many species. Across temperate, boreal and polar latitudes, earlier seasonal warming is considered the key mechanism leading to earlier leaf expansion and growth. Yet, in seasonally snow-covered ecosystems, the timing of spring plant growth may also be cued by snowmelt, which may occur earlier in a warmer climate. Multiple environmental cues protect plants from growing too early, but to understand how climate change will alter the timing and magnitude of plant growth, experiments need to independently manipulate temperature and snowmelt. Here, we demonstrate that altered seasonality through experimental warming and earlier snowmelt led to earlier plant growth, but the aboveground production response varied among plant functional groups. Earlier snowmelt without warming led to early leaf emergence, but often slowed the rate of leaf expansion and had limited effects on aboveground production. Experimental warming alone had small and inconsistent effects on aboveground phenology, while the effect of the combined treatment resembled that of early snowmelt alone. Experimental warming led to greater aboveground production among the graminoids, limited changes among deciduous shrubs and decreased production in one of the dominant evergreen shrubs. As a result, we predict that early onset of the growing season may favour early growing plant species, even those that do not shift the timing of leaf expansion.
Arctic tussock tundra; climate change; plant phenology; plant production; seasonality
Seasonality in temperate to polar ecosystems is shifting
through earlier seasonal warming and changes in
precipitation regimes that lead to earlier snowmelt
et al. 2006; Hayhoe et al. 2007; Ernakovich et al. 2014)
Plant communities are responding through changes in
timing of life-cycle events such as leaf expansion and
flowering (i.e. phenology)
(Fitter and Fitter 2002;
Thompson and Clark 2008)
, shifts in species relative abundance
(Harte and Shaw 1995; Willis et al. 2008)
, species’ range
(Walther et al. 2005; Gottfried et al. 2012)
greater aboveground plant production
Smith 2001; Wang et al. 2012)
. These observations
of altered seasonality and plant community changes
correspond to a period of increasing global temperatures,
but experiments are still needed to determine
mechanisms and develop predictive models as climate change
(Pau et al. 2011; Richardson et al. 2012)
Temperature and photoperiod are known plant
phenological cues that determine the timing of spring events,
such as bud burst, leaf emergence and canopy
development, and flowering
(Cleland et al. 2007; Ko¨ rner and
Basler 2010; Polgar and Primack 2011)
warming studies using different techniques, such as
active warming through overhead infrared heaters or
passive warming with open-top chambers (OTCs),
demonstrate that many species begin growth and flowering
earlier in warmed versus control plots
(Cleland et al.
2006; Sherry et al. 2007; Reyes-Fox et al. 2014)
responses can vary with some species not shifting or
delaying the timing of spring events under warmed
(Hollister et al. 2005a; Reyes-Fox et al. 2014;
Marchin et al. 2015)
. Similarly, long-term observations
of phenological response to climate warming over time
show an overall advance in timing of spring of an
estimated 5 – 6 days 8C21 (Wolkovich et al. 2012), but with
(Fitter and Fitter 2002; Menzel
et al. 2006)
. The variation in response suggests that
phenology is cued by other environmental variables (e.g.
photoperiod) for species within and across diverse plant
communities from tundra, grassland and forest biomes.
The influence of snow cover on plant phenology is less
well understood, in part because temperature change
due to climate change and experimental warming
influence when an area becomes snow-free. Development of
early emerging species may be closely synchronized with
timing of snowmelt in Arctic and alpine ecosystems
(Galen and Stanton 1995; Høye et al. 2007)
, and indeed,
later snowmelt due to increased snow depth has been
shown to delay bud break of deciduous shrubs
et al. 2008; Sweet et al. 2014)
. However, few experiments
have examined the isolated effects of early snowmelt and
summer warming in the Arctic or alpine, and often these
effects are confounded either by the use of warming
treatments such as OTCs to accelerate snowmelt or by
the snow removal that reduces water inputs
Multifactor global change experiments have shown
that plant production is sensitive to manipulations of
abiotic factors, including air and soil warming, nutrients,
CO2 and precipitation
(Fay et al. 2003; Zavaleta et al. 2003;
Dukes et al. 2005; Dawes et al. 2011)
. Response to these
factors is complex, with variation across plant
communities due to differences in limiting factors (Smith et al.
2015), and variation within communities due to
differences in functional group responses
(Zavaleta et al.
2003; Wahren et al. 2005; Muldavin et al. 2008)
. In the
Arctic, production is strongly limited by nutrient
availability, which in turn is sensitive to temperature and ongoing
changes in the timing of seasonal climatic events such as
snowmelt, soil thaw, the onset of freezing and snowfall
(Billings and Mooney 1968; Weintraub and Schimel
. In recent years, both observational and
experimental studies have linked increased production,
specifically that of deciduous shrubs and graminoids, to
(Tape et al. 2006; Walker et al.
2006; Forbes et al. 2010; Elmendorf et al. 2012b; Sistla
et al. 2013)
. However, a number of experiments that
have manipulated summer temperature in both Arctic
and alpine regions did not find a consistent increase in
community-level aboveground net primary production
(ANPP); rather, individual species or functional groups
varied in their response
(Chapin et al. 1995; Harte and
Shaw 1995; Hollister et al. 2005b)
. Evergreen shrubs
have responded to warming with positive, negative or
no changes in production
(Hollister et al. 2005b; Walker
et al. 2006; Campioli et al. 2012)
, and they may be less
likely to show short-term growth responses due to their
conservative growth strategy
(Chapin and Shaver 1996;
Starr et al. 2008)
Changes in plant production may also be expected to
vary in relation to changes in the timing of growth; for
example, earlier leaf expansion may lead to greater
(Richardson et al. 2010)
. There is evidence that
phenological ‘tracking’ of climate change across biomes
can result in positive growth responses, through
increased abundance, production or flowering effort
(Cleland et al. 2012)
. However, physiological constraints
and interactions of the affected species may prevent
some plants from taking advantage of an earlier start
to the growing season
(Schwartz 1998; Richardson et al.
2010; Polgar and Primack 2011)
. One such constraint
could be negative impacts of exposure to cold
temperatures and freezing damage if snow melts early
2008; Wipf et al. 2009)
. Differences in the onset and
duration of plant growth can also vary due to differences in
plant community composition; for example, deciduous
shrub-dominated communities in Arctic tundra were
shown to have longer peak growing seasons and greater
carbon uptake than evergreen/graminoid communities in
the same region (Sweet et al. 2015).
In the Arctic, climate is changing at a faster rate than in
other regions, a trend that is expected to continue
(Christensen et al. 2013)
. Rapidly increasing air
temperature ( 1 8C decade21)
(Christensen et al. 2013)
snowmelt (3 – 5 days decade21) and later snowfall are
changing the seasonality of this ecosystem
et al. 2000; Ernakovich et al. 2014)
observations via remote sensing suggest that vegetation
phenology in the Arctic is indeed advancing and plant
production is increasing
(Myneni et al. 1997; Jia et al.
2003, 2009; Fraser et al. 2011; Zeng et al. 2011)
snowmelt, especially in combination with warmer
temperatures in early spring, should benefit plant
growth, since it is the time of year with the greatest
light and nutrient availability
(Weintraub and Schimel
2005; Edwards and Jefferies 2013)
experiments are needed to determine how shifts in seasonality
will affect phenology of Arctic species, and how changes
in phenology affect plant productivity and future
In Arctic tussock tundra, we established a 3-year study
in which we altered seasonality through the independent
and combined manipulation of air temperature and
timing of snowmelt. We examined the response of spring
phenology and plant production for key tundra species
and hypothesized that:
(1) The timing of snowmelt and temperature are cues for
initiating plant growth. We predicted that leaf
appearance and expansion would advance due to
early snowmelt and air warming for all species.
(2) The timing of snowmelt and temperature affect
plant production. We predicted that early snowmelt
and warmer temperatures would increase production
of deciduous shrub, graminoid and forb species,
but would not change production of evergreen
(3) The timing of plant growth affects plant production.
We predicted that earlier leaf expansion would lead
to greater aboveground biomass at peak season.
The experiment was conducted near Imnavait Creek on
the North Slope of Alaska, close to the Arctic Long-Term
Ecological Research (LTER) site at Toolik Field Station.
The plant community at Imnavait is moist acidic tussock
tundra, characterized by the tussock forming sedge
Eriophorum vaginatum and a high moss cover, including
Hylocomium spp., Aulacomnuim spp. and Dicranum spp.
Associated species include another sedge, Carex
bigelowii, the deciduous shrubs Betula nana and Salix pulchra,
the evergreen shrubs Ledum palustre, Vaccinium
vitis-idaea and Cassiope tetragonum, and a variety of
forbs [see Supporting Information—Table S1]. The old
( 120 000 – 600 000 years; Whittinghill and Hobbie
, acidic soil (mean pH of 4.5) at this site is underlain
by continuous permafrost, with an uneven surface layer
of organic material 0 – 20 cm thick
(Walker et al. 1994)
and variable soil moisture.
For 3 years (2010– 12), snowmelt was accelerated in five
8 × 12 m plots using radiation-absorbing black 50 %
shade cloth that was placed over the snowpack in late
April – early May. The dark fabric accelerated melt and
allowed for minimal disturbance of the snowpack. The
fabric was removed when plots became 80 % snow-free
(determined by daily visual estimates). In 2012, we
achieved a 10-day acceleration in the timing of snowmelt
with early snowmelt plots becoming snow-free on May 16
and control plots snow-free on May 26. Snow was melted
4 and 15 days earlier in 2010 and 2011, respectively. As
plots became snow-free, (OTCs were deployed on
subplots within the accelerated snowmelt and control
areas. The OTCs are hexagonal chambers with sloping
sides, constructed of Plexiglas material that allows
transmittance of wavelengths of light in the visible spectrum,
enabling passive warming primarily through trapping
(Marion et al. 1997)
. Open-top chambers
warmed air temperatures by an average of 1.4 8C in
2012. Further details of treatment effects on air
temperature, soil temperature and soil moisture are available in
Supporting Information—Table S2. The approximate
area of both control and warming subplots was 1 m2.
Treatments were replicated five times in a full factorial,
randomized split-plot design. Treatment abbreviations
are as follows throughout the article: control (C), warming
(W), early snowmelt (ES) and combined (W × ES).
Five individuals of seven species were marked in each
subplot and phenology events were monitored every
2 –3 days from snowmelt through mid-August.
Observations of ‘leaf appearance’ and ‘leaf expansion’ were
recorded for each individual. Although definitions of
events varied between functional groups, we generally
considered leaf appearance to be the first observation
of new green leaves and leaf expansion to be when an
individual had a leaf that was fully expanded or had
reached a previously determined size. For deciduous
shrubs (B. nana and S. pulchra), leaf appearance was
recorded at the first observed leaf bud burst, and leaf
expansion when an individual had at least one fully
unfurled leaf anywhere on the plant. Similarly, evergreen
shrub (L. palustre and V. vitis-idaea) leaf appearance was
recorded when the first leaf bud was visible, and full leaf
expansion occurred when at least one leaf bud was fully
open and leaves unfurled. Eriophorum vaginatum retains
green leaf material over winter and often begins growth
of new leaves and re-greening of old leaves before snow is
(Chapin et al. 1979)
. Therefore, we
recorded leaf appearance (new leaves .1 cm length)
for E. vaginatum on the day of snowmelt, but did not
consider this as a treatment effect. Rather than continuously
measuring leaf length to record full leaf expansion, we
determined leaf expansion for E. vaginatum to have
occurred when a new leaf reached .4 cm length. We
only considered growth of new leaves, which were
identified as those with no senescent material at the leaf tip.
We followed similar protocol for C. bigelowii leaf
appearance (new leaf .1 cm length) and leaf expansion (new
leaf .4 cm length), but leaf appearance was considered
a treatment effect. First leaf appearance for the forb
P. bistorta was marked when leaves were visible
(generally .1 cm length) and leaf expansion when leaves
were fully unrolled and .5 cm length.
A destructive harvest to measure plant production, as
characterized by growth of individuals in the current
year, was carried out on the same species for which
phenology was observed. The seven species chosen
represented four functional groups and comprised the
majority of vascular plant cover at our site [see
Supporting Information—Table S1]. The harvest took place in the
third year of treatments at peak growing season, which
was determined by phenology observations and analysis
of daily normalized difference vegetation index
measurements showing that peak greenness (i.e. full canopy
development) had occurred in each treatment (C.
Livensperger and H. Steltzer, unpublished data). Randomly
selected individuals were clipped in the field, and then
taken back to the laboratory where old and new growth
was separated and biomass measured. Eight individuals
each of B. nana, S. pulchra and L. palustre, and 16
individuals each of V. vitis-idea, E. vaginatum, C. bigelowii and
P. bistorta were collected from each subplot and pooled
by species. Plant material was separated by tissue type,
dried at 60 8C for 48 h and weighed.
Mean individual production for each species was
calculated as the sum of current years’ biomass divided by the
number of individuals collected. Current years’ biomass
included leaves, new stems and secondary growth for
shrub species. For graminoids and a forb, all live
aboveground plant tissue was used, which may have included
some growth from previous years for E. vaginatum and
C. bigelowii. We calculated current annual secondary
stem growth for B. nana, S. pulchra and L. palustre as a
proportion of standing stem biomass, using previously
determined annual growth rates of woody stems from
the nearby Toolik Lake LTER site
(Bret-Harte et al. 2002)
For these species, leaves contributed more to total
biomass than the calculated secondary growth. Secondary
growth for the remaining shrub species, V. vitis-idaea, is
negligible and, therefore, was left out of production
calculation for this species
stem biomass, excluding current seasonal growth, for
individual shrub stems varied among plots and likely is
a result of variation prior to when the experiment was
established. To control for this variation and better detect
treatment effects, individual production data are
presented in relation to standing stem biomass excluding
current annual growth (i.e. g new production/g standing
For all analyses, the experiment was treated as a blocked
split-plot design, where a large early snowmelt plot
paired with an equally sized control plot comprise a single
block. Plant responses and environmental variables were
analysed using a mixed-model analysis of variance
(ANOVA; SAS v 9.2, SAS Institute, Inc., Cary, NC, USA),
with early snowmelt (ES) as the main plot factor and
warming (W) as the within plot factor. A random effect
of block was included to control for inherent variation
between the five replicates. All data were checked for
normality and were found to meet the assumptions
of ANOVA. Linear regression was used to analyse the
relationship between phenology and plant growth.
Early snowmelt was a strong driver of change in both the
timing and rate of leaf appearance and expansion. These
events advanced due to early snowmelt alone for all
species except the forb, P. bistorta (Fig. 1), and the amount
of change in timing varied between events, species
and functional groups. The largest change in timing was
a 10-day advance in leaf expansion for E. vaginatum
(Fig. 1), corresponding to the 10-day advance in
snowmelt through our snow manipulation. Leaf appearance
and expansion of evergreen and deciduous shrubs were
significantly earlier due to early snowmelt alone,
advancing by 1 – 8 days for B. nana, S. pulchra, L. palustre and
V. vitis-idaea (Fig. 1, Table 1). The advancement of leaf
appearance versus leaf expansion differed in magnitude
for S. pulchra, V. vitis-idaea and C. bigelowii, by increasing
the number of days between leaf appearance and leaf
expansion by 2 – 5 days. For example, in the early
snowmelt treatment, leaf appearance for S. pulchra occurred
8 days earlier than the control, while leaf expansion
advanced by only 3 days. For deciduous shrubs, evergreen
shrubs and the forb, the shift in phenology was less than
the 10-day advance in snowmelt, increasing the number
of days after snowmelt to when canopy development
(i.e. leaf expansion) began; this effectively slowed the
rate of plant production (Fig. 2, Table 2). The sedges,
E. vaginatum and C. bigelowii, did not follow this pattern,
with no evidence of a change in the number of days
between leaf appearance and expansion (Fig. 2).
Warming also advanced the timing of leaf appearance
and expansion for most species, but to a lesser extent
than early snowmelt (Fig. 1, Table 1). All of the deciduous
shrub and graminoid species advanced leaf phenology
with warming alone, but only by 1 or 2 days (Fig. 1,
Table 1). Evergreen shrubs showed contrasting responses
to warming: leaf appearance for V. vitis-idaea advanced
by 3 days, while L. palustre leaf expansion was delayed
for 2 days (Fig. 1, Table 1). Warming generally did not
alter phenology in relation to the timing of snowmelt
(Fig. 2, Table 2). One exception is that warming led to
significantly faster leaf expansion following snowmelt for
B. nana, effectively speeding plant production.
Phenological responses to the combination of early
snowmelt and warming were generally comparable
with the response to early snowmelt alone (Figs 1 and
2), and the interactive effect of warming × early
snowmelt on phenology was never significant (Table 1). For
evergreen shrubs, leaf appearance occurred earliest with
the combined treatment, which was 1 – 3 days earlier
than in snowmelt and warming alone (Fig. 1).
Although phenological events often occurred earlier in
the year due to earlier snowmelt and warming, an
increase in individual production was rarely observed.
Rather, responses to early snowmelt and warming varied
within and among functional groups. Differences were
rarely significant (Table 3), in part due to the challenge
of quantifying plant production in an ecosystem with
high spatial variation.
However, the magnitude of change often represented a
high proportion of production in this low productivity
system. Deciduous shrub species differed in their response,
with S. pulchra decreasing individual production by 6 –
11 % and B. nana showing little change across the three
treatments (Table 3). Evergreen shrub species increased
individual production by 28 and 8 % for L. palustre and
V. vitis-idaea, respectively, due to early snowmelt
(Table 3). Individual production of P. bistorta, the forb,
was highly variable within treatments; for example,
control plants ranged from 36 to 297 mg biomass. The most
evident response for this species was a large, but
nonsignificant, decrease (36 %) in production due to early
snowmelt (Table 3).
The effect of warming on production was statistically
significant for two species and led to the largest
proportional changes (Fig. 3, Table 3). Both graminoid species
responded positively to warming. Mean individual
production for E. vaginatum increased by 36 %, which was
the greatest proportional increase of any species (Fig. 3,
Table 3). When early snowmelt and warming were
combined, E. vaginatum increased individual production by
27 % relative to the control (Fig. 3, Table 3). The other
graminoid, C. bigelowii, increased individual production
by 17 % with warming and 24 % with warming and
early snowmelt, although these increases were not
significant (Fig. 3, Table 3). An evergreen shrub,
V. vitis-idaea, had relatively large decreases relative to
the control with warming (21 %) and the combined
treatment (42 %), and the main effect of warming was
significant (Table 3).
Phenology and production relationship
Across all species and for all treatments, earlier leaf
expansion was associated with increased production
(Fig. 4, y ¼ 135.52–0.81x, R2 ¼ 0.09, P ¼ 0.0021). This
relationship reflects differences in the timing of leaf expansion
among growth forms and the response of individual plant
production to early snowmelt and warming. Species varied
in the timing of leaf expansion by 40 days, a range that was
expanded by 14 days due to altered seasonality. Early
expanding species (E. vaginatum and C. bigelowii) had
increases in production, while later expanding species
(L. palustre and V. vitis-idaea) had some increases
and also large decreases in production as a result of
warming. Across functional groups, warming drove the
relationship between timing of leaf expansion and
individual production, as shown by significantly negative
regression slopes within the warming and combined
treatments (Fig. 5; C: y ¼ 262.7 + 0.41x, R2 ¼ 0.01,
P ¼ 0.53; ES: y ¼ 43.16 – 0.24x, R2 ¼ 0.01, P ¼ 0.547;
W: y ¼ 188.66 – 1.11x, R2 ¼ 0.13, P ¼ 0.03; W × ES:
y ¼ 200.26 – 1.23x, R2 ¼ 0.24, P ¼ 0.005). Within
functional groups, there was no relationship between the
timing of leaf expansion and individual production,
despite earlier leaf expansion due to early snowmelt
and warming (Fig. 6; deciduous shrubs: y ¼ 216.43 –1.37x,
R2 ¼ 0.06, P ¼ 0.202; evergreen shrubs: y ¼ 2606.13 +
3.37x, R2 ¼ 0.08, P ¼ 0.129; graminoids: y ¼ 50.74 – 0.18x,
Our results showed consistent advancement of leaf
appearance and expansion, indicating that spring
phenology of moist acidic tundra species is sensitive to early
snowmelt and warming, which is consistent with our
first hypothesis. Warmer temperatures have been
shown to advance spring phenology in other systems,
particularly for deciduous shrubs where budburst is well
predicted by growing degree-days
(Polgar and Primack
. However, we found that species were more
responsive to early snowmelt, by advancing timing of
events to a greater extent than with warming alone.
Timing of snowmelt has been shown to be a cue for spring
phenology in Arctic and alpine ecosystems
(Arft et al.
1999; Steltzer et al. 2009)
, but experiments often
confound the effects of warming and timing of snowmelt.
Arctic species generally have a wide range of
physiological tolerance, allowing spring growth to occur despite
temperatures at or near freezing (Billings and Mooney
1968), and our experiment shows that early snowmelt
can advance phenology independent of warming.
Along with clear advances in spring phenology, we also
observed slower rates of leaf expansion for many species
in response to early snowmelt, supporting the
conservative growth strategy demonstrated by many Arctic and
alpine species to compensate for interannual variation
in snowmelt timing
(Billings and Mooney 1968)
Surprisingly, only one species, B. nana, expanded its leaves at a
faster rate with warming. It may be that soil temperature,
which warmed to a lesser extent than air temperature
[see Supporting Information—Table S2], is an additional
cue for rate of leaf expansion for most species. Plants that
expand leaves early may be susceptible to frost damage if
temperatures remain cold or freezing events occur
(Inouye 2008; Wipf et al. 2009)
Production responses to warming and early snowmelt
were dependent on growth form and individual species.
One functional group (graminoids) matched our
predicted direction of response, while others did not (forbs
and deciduous and evergreen shrubs). Previous warming
experiments have also shown interspecific variation
within tundra communities, with graminoids and
deciduous shrubs showing rapid change relative to evergreen
shrubs and forbs
(Chapin and Shaver 1985; Chapin et al.
1995; Hollister et al. 2005b)
. The response of graminoids
in our study was consistent with these experiments, with
both E. vaginatum and C. bigelowii increasing production
in response to warming and early snowmelt. Although we
measured biomass of individual tillers, new tiller
recruitment is another likely mechanism by which either
graminoid species could have increased biomass (Chapin and
Shaver 1985). Graminoids were the only functional
group that maintained their growth rates when snow
was melted early, which may confer an advantage in
accessing early-season nutrient pulses, and
consequently increasing production in the same year
et al. 1986)
. Our results are generally consistent with
past work on E. vaginatum, which showed that
earlyseason air warming leads to accelerated leaf growth
and earlier arrival at peak biomass (Sullivan and Welker
2005). Our observation that graminoids were also able
to advance timing of early-season phenology to a greater
extent than the other functional groups may be due to
their ability to initiate growth underneath the snowpack
and therefore have new leaves present at snowmelt in
addition to green leaves that have overwintered
et al. 1979)
Warming resulted in a large decrease in production for
the evergreen shrub, V. vitis-idaea, a species that has
shown much variability in response to warming in
(Chapin et al. 1995; Arft et al. 1999;
Zamin et al. 2014)
. A meta-analysis of warming
experiments across the Arctic suggests that evergreen shrub
response to warming depends on soil moisture regime,
with plants in moist soils more often decreasing in
(Elmendorf et al. 2012a)
. Regardless, the large
change in production that we observed was unexpected
because evergreen shrubs have a conservative growth
strategy, demonstrated by slower growth rates, lower
specific leaf area and lower photosynthetic capacity
than other species in the tundra community
and Shaver 1996; Starr et al. 2008)
. A decrease in new
leaf biomass by V. vitis-idaea could be related to conditions
in previous years, because evergreen shrub growth relies in
part on nutrients stored in old leaves (Billings and Mooney
1968). Alternatively, V. vitis-idaea may be a poorer
competitor than deciduous species (e.g. B. nana) for increased
nutrients under warmed conditions
(Shaver et al. 2001)
Evergreen shrubs have the ability to access early-season
(McKane et al. 2002; Larsen et al. 2012)
and photosynthesize under the snowpack (Starr and
Oberbauer 2003), which may explain why both species
increased production in response to early snowmelt,
similar to graminoids. However, this does not explain
why V. vitis-idaea would show the opposite response
when early snowmelt was combined with warming.
Production of deciduous shrubs and a forb did not show
clear responses to warming or early snowmelt. It may be
that the 3-year duration of our study did not allow enough
time for B. nana or S. pulchra to show significant changes
in production. Short- and long-term responses to
warming in the moist acidic tundra have been shown to vary,
in part because of slow recruitment and establishment
of new individuals
(Hollister et al. 2005b)
. For example,
observations from the ITEX experiments showed that
community changes in deciduous shrubs did not become
significant until after 4 years of warming (Walker et al.
2006). However, since we measured growth at an
individual (rather than community) level in order to detect
within-season changes of biomass accumulation, the
response of deciduous shrubs may be more likely
attributed to nutrient availability in that year. If evergreen
shrubs were able to access nutrient pulses early in the
season before deciduous shrubs, it may help explain
why the latter showed little response, specifically when
snow was melted early. The one forb tested in this
experiment, P. bistorta, had highly variable results which may
have obscured any treatment effects.
While the magnitude of temporal shifts is often a focus
of phenological studies, our results suggest that evolved
strategies within the plant community also play an
important role in determining responses to altered
seasonality. We predicted that earlier leaf expansion would
lead to greater production, and we found that this was
true for early expanding species but not later expanding
species. This demonstrates that temporal niche
partitioning influences species’ responses to environmental
change. A previous study
(Cleland et al. 2012)
plant responses to warming and found that
phenologically flexible species (able to ‘track’ climate change) had
positive performance responses (e.g. increased
abundance and production). Our results are only partially
consistent with this result. In our study, changes in
phenology alone did not always result in a change in
production. Rather, community patterns of leaf expansion, along
with warming-driven increases and decreases in ANPP
(Fig. 5), contributed to a negative relationship between
spring phenology and production (Fig. 4). If this
relationship was representative of differences in functional
groups alone, we would expect the relationship to hold
among control plots, which was not the observed result
(Fig. 5). Differences in the ability of species to shift the
timing and rate of leaf expansion may affect competitive
interactions and subsequently influence future plant
(Richardson et al. 2010; Cleland
et al. 2012)
. Specifically, E. vaginatum, which was able to
green rapidly and maintain its growth rate, may have a
competitive advantage. Further, we predict that species
that occupy early-season temporal niches across diverse
ecosystems may increase in abundance under altered
Changes in vegetative phenology, regardless of changes
in production, have important implications for
functioning of Arctic ecosystems. Phenological shifts can affect
competition among species, and differential responses
of individual species may determine future plant
community structure. Changes in Arctic plant communities have
the potential to affect multiple aspects of ecosystem
function, including (i) carbon cycling, by altering the
balance between ecosystem-scale photosynthesis and
(Shaver et al. 1992; Hobbie et al. 2000)
surface energy balance and feedbacks to the climate system,
through change in albedo and seasonal changes in leaf
area (Pen˜ uelas et al. 2009; Ric
hardson et al. 2013
(iii) trophic relationships that may become decoupled
if plant phenology responds to a changing climate
differently than vertebrate and invertebrate herbivores
Post and Forchhammer 2008
Høye et al. 2013
study suggests that an earlier spring as indicated by
satellite data may be driven by early greening species
such as E. vaginatum and C. bigelowii. These species
have the advantage of being able to respond rapidly
and positively to changes in seasonality, and may
increase in abundance in tundra ecosystems as earlier
snowmelt and warmer springs continue.
Sources of Funding
Funding for the Snowmelt Project was provided by the
National Science Foundation Office of Polar Programs
Grants #PLR-1007672, 0902096 and 0902184. Additional
funding for C.L. was provided by a National Science
Foundation Graduate Research Fellowship.
Contributions by the Authors
M.N.W., M.W., P.F.S., A.D.-N. and H.S. designed and
implemented the experiment. C.L., A.D.-N. and H.S. collected
data. C.L. and H.S. analysed the data and wrote the
manuscript, and all authors contributed to revisions.
Conflict of Interest Statement
We thank two anonymous reviewers for comments that
improved the quality of this manuscript.
The following additional information is available in the
online version of this article —
Table S1. Species composition at Imnavait Creek. Per
cent cover estimates are averaged over subplots for the
entire experimental site.
Table S2. Microclimate variables in all 3 years of the
experiment (2010 – 12). Air temperature, soil temperature
and soil moisture were measured with automated
sensors at each subplot throughout spring and summer,
and are presented here as means over the observation
period + 1 SEM.
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