Received: 15 February 2021 | Accepted: 1 June 2021

DOI: 10.1111/gcb.15767

PRIMARY RESEARCH ARTICLE

Comparison of the distribution and phenology of Arctic

Mountain plants between the early 20th and 21st centuries

Andrew S. MacDougall1,2 | Paul Caplat3 | Johan Olofsson2,4 | Matthias B. Siewert2,4 |

1 1 1 2
Colin Bonner | Ellen Esch | Malie Lessard-­Therrien | Hannah Rosenzweig |
Anne-­Kathrin Schäfer2 | Pia Raker2 | Hassan Ridha2 | Kjell Bolmgren2 | Thore C. E. Fries5 |
Keith Larson2,4

1
Department of Integrative Biology,
University of Guelph, Guelph, ON, Canada Abstract
2
Climate Impacts Research Centre, Umeå Arctic plants are adapted to climatic variability, but their long-­term responses to
University, Umeå, Sweden
3
warming remain unclear. Responses may occur by range shifts, phenological adjust-
School of Biological Sciences, Queen's
University, Belfast, Northern Ireland ments in growth and reproduction, or both. Here, we compare distribution and phe-
4
Department of Ecology and nology of 83 arctic and boreal mountain species, sampled identically in the early 20th
Environmental Science, Umeå University,
(1917–­1919) and 21st centuries (2017–­2018) from a region of northern Sweden that
Umeå, Sweden
5
Abisko Natural Science Station has warmed significantly. We test two compensatory hypotheses to high-­latitude
warming—­upward shifts in distribution, and earlier or extended growth and reproduc-
Correspondence
Andrew S. MacDougall, Department of tion. For distribution, we show dramatic upward migration by 69% of species, averag-
Integrative Biology, University of Guelph, ing 6.1 m per decade, especially boreal woodland taxa whose upward expansion has
Guelph, ON, Canada.
Email: asm@uoguelph.ca reduced arctic montane habitat by 30%. Twenty percent of summit species showed
distributional shifts but downward, especially moisture-­associated snowbed flora.
Keith Larson, Climate Impacts Research
Centre, Umeå University, Umeå, Sweden. For phenology, we detected wide inter-­annual variability in the onset of leafing and
Email: keith.larson@umu.se
flowering in both eras. However, there was no detectable change in growing-­season
Funding information length, relating to two mechanisms. First, plot-­level snow melt data starting in 1917
Natural Sciences and Engineering
demonstrated that melt date, rather than vernal temperatures, better predicts plant
Research Council of Canada; Swedish
Research Council for Sustainable emergence, with snow melt influenced by warmer years having greater snowfall—­
Management (FORMAS), and Umeå
warmer springs did not always result in earlier emergence because snowbeds can
University
persist longer. Second, the onset of reproductive senescence between eras was simi-
lar, even when plant emergence was earlier by a month, possibly due to intensified
summer heat stress or hard-­wired ‘canalization’ where senescence occurs regardless
of summer temperature. Migrations in this system have possibly buffered arctic spe-
cies against displacement by boreal expansion and warming, but ongoing temperature
increases, woody plant invasion, and a potential lack of flexibility in timing of senes-
cence may foreshadow challenges.

KEYWORDS
arctic flora, climate change, historical data, migration, mountain, phenology, resiliency

Thore C. E. Fries: Deceased 1930.

5070 | © 2021 John Wiley & Sons Ltd wileyonlinelibrary.com/journal/gcb Glob Change Biol. 2021;27:5070–5083.

MACDOUGALL et al.
1 | I NTRO D U C TI O N
The arctic climate is one of the most rapidly changing on the planet,
having warmed by 2–­3°C over the last century with projected in-
creases towards 4–­5°C (IPCC, 2013; Nogues-­Bravo et al., 2007; Post
et al., 2019; Sala et al., 2000). These changes have significant conse-
quences for arctic flora, including on high-­latitude mountains where
warming can be especially pronounced (Lenoir et al., 2008; Prevey
et al., 2019; Steinbauer et al., 2018), growing seasons short, and
the availability of high-­elevation refugia finite (Prevey et al., 2019;
Steinbauer et al., 2018).
The biological impacts of a changing arctic climate, on mountain
plants and more broadly, will be dictated by their ability to maintain
growth and reproduction. This occurs by at least two pathways: spa-
tial shifts across generations (hereafter ‘migration’), progressively
moving northward, uphill, or both, and phenological adjustments
that better match growth and reproduction to changes including
warmer and earlier springs, drier summers, extended periods of au-
tumn warmth, and altered precipitation dynamics including snowfall
(e.g. Assmann et al., 2019; Chapin et al., 2012; Lesica & McCune,
2004; Rosbakh et al., 2021; Wookey et al., 1993). However, the ca-
pacity for resilience emerging from these mechanisms, historically
and going forward, remains unclear. The persistence of high-­latitude
plants is strongly dictated by distributional range and phenology,
given the compressed growing season of the arctic climate (Harsch
et al., 2009). There are numerous traits that could well-­equip Arctic
species for rapid adjustments to warming, such as early emergence,
delayed reproduction, or extended leafing senescence (e.g. Thomas
et al., 2020). These same traits could also predict species loss, if
climatic change exceeds the trait-­based limits of adjustment or if
change favours suites of larger-­and faster-­growing competitively su-
perior southern invaders (e.g. Alexander et al., 2015, 2018). If high-­
latitude plants cannot phenologically adjust, then multi-­generational
upward or northward shifts via migration will be needed to maintain
the climatic envelope, escape southern invaders, or both.
It has been difficult to empirically determine whether plants are
successfully adjusting to a changing arctic climate, given an absence
of long-­term data especially prior to recent decades when warming
has accelerated (Steinbauer et al., 2018). There is some evidence for
both migration and phenological shifts (Lenoir et al., 2008; Rosbakh
et al., 2021), but there has also been wide variability in response
(Myers-­Smith et al., 2015). For example, sometimes shrub-­ and
tree-­lines advance in elevation or latitude but many times they do
not (Harsch et al., 2009; Myers-­Smith et al., 2015; Van Bogaert
et al., 2011). The same holds for changes in species richness of cold-­
adapted plants—­there has been reports of increases (Klanderud &
Birks, 2003), losses (Engler et al., 2011; Wilson & Nilsson, 2009),
and no change (Vanneste et al., 2017). Furthermore, research
tends to target the front of the range (expansion), whereas range
changes may derive more from the back (contraction) especially if
climate impacts are channelled through altered species interactions
(Rumpf et al., 2019; Van Bogaert et al., 2011). In this latter case,
phenological changes alone will not buffer responses to warming
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5071
if warm-­tolerant species are sweeping in from behind—­only north-
ward or upward range expansion by arctic flora would maintain
persistence. Phenologically, there has been an understandable
emphasis on early flowering given the advancement of growing
seasons globally (Ellwood et al., 2013), but growing-­season length
and senescence also impact plant fitness and are less investigated
especially in the arctic (Prevey et al., 2019). Even the so-­c alled
‘Arctic greening’ in high-­latitude plant communities, involving ex-
tended growing seasons and increased net primary production, has
not been universally detected (Berner et al., 2020; Pauchard et al.,
2016; Post et al., 2019). In total, these uncertainties on migrational
and phenological plant responses limit our ability to predict future
impacts of a warming Arctic (Niskanen et al., 2019).
Here, we present evidence of distributional and phenological
adjustments by 83 arctic and boreal mountain flora in northern
Scandinavia between the early 20th and 21st centuries, testing two
primary compensatory hypotheses to long-­term arctic warming—­
upward migration and earlier and extended growth and reproduc-
tion (e.g. Arft et al., 1999; Bjorkman et al., 2015; Choi et al., 2019).
Climate conditions in this region have changed dramatically, espe-
cially since the 1980s (Figure 1), while the Arctic Mountain plants
of northern Scandinavia have been modelled to undergo substan-
tial species loss and range contraction (Niskanen et al., 2019). Our
work centres on a unique long-­term dataset, identically sampled at
the same plot locations every 5 days during the growing seasons
of 1917–­1919 and 2017–­2018 along an elevational gradient strad-
dling both Arctic and Boreal biomes in the Scandes Mountains (Fries,
1925). Using data on shifts in elevational occurrence, the onset and
senescence of leafing and flowering, the timing of plot-­level snow
melt by elevation, along with species-­specific plant traits and local
daily climate from 1913 to present, we test the relative importance
of migration and phenology for plant persistence between the two
eras of the study. Our distributional analysis includes data on the
maximum and minimum range limits of each species, allowing us to
determine whether change happens more at higher elevation, where
direct temperature effects should be most limiting, or towards the
mountain base where climate impacts should be channelled through
species interactions especially invasion by southern Boreal taxa.
We also test differences in the richness and composition of summit
vegetation, given the large body of historical summit studies from
elsewhere in Europe showing that mountain-­top plant communi-
ties often respond rapidly to climate change (e.g. Gottfried et al.,
2012; Matteodo et al., 2013; Parolo & Rossi, 2008; Pauli et al., 2012;
Steinbauer et al., 2018).
2 | M E TH O D S
Work was conducted in two sampling periods on a 900 m transect
on Mount Nuolja (1169 m ASL) in Abisko National Park, Sweden lo-
cated 195 km north of the Arctic Circle (68.3495°N, 18.8312°E). The
study area occurs within a rain shadow of the Scandes Mountains,
with long-­term (1913–­2018) precipitation averaging 307 mm per
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5072 MACDOUGALL et al.

2.5 (a) Annual temperature 1913– 2019 4.0 (b) March –May
Spring
2018

2.0
1.5

0
Spring
2017
0.5
2018
–2.0
Temperature oC

2017

– 0.5
4
–4.0
1918 (c) June– Sept
13.0

Summer
– 1.5 2018
11.0

1919
Summer

– 2.5
1917
9.0 March-May
M
Ma rch
ch-M
ch May 2017

7.0
– 3.5 June-Sept
Jun
Ju ne-Se
Sep
Sept
1915 1925 1935 1945 1955 1965 1975 1985 1995 2005 2015 1925 1945 1965 1985 2005
Year

F I G U R E 1 Long-­term mean temperature trends from Abisko, Sweden—­1913–­2018, including our 5 years of sampling in red. All fitted
polynomials are best fit and demonstrate significant warming especially since the late 1980s for overall annual temperature (F3,38712 = 34.06,
p < 0.0001), early-­season (March–­May; F3,6462 = 39.13, p < 0.0001), and summer (June–­September; F3,9748 = 40.6, p < 0.0001). Error bars
are 1 SE [Colour figure can be viewed at wileyonlinelibrary.com]

year and mean annual temperatures of −0.5°C. About 50% of an-
nual precipitation falls as snow typically between October–­April.
Snowbeds can persist well into the summer months, depending on
elevation and annual snowfall. All climate data come from a meteor-
ological station at Abisko Scientific Research Station, near the base
of the transect (388 m ASL)—­data were measured every 3 h from
1913–­2004, and then hourly since (Callaghan et al., 2010; Kohler
et al., 2006). Long-­term trajectories of warming over the 20th and
early 21st centuries at the station show increases, overall (warmer
by 2.31°C since 1917) and by season, although these trends are not
linear (Figure 1; Figure S1). The most consistent period of increased
warming has been since the 1980s; before then inter-­decadal warm-
ing was more variable including extended cold winters during the
1950s–­1970s (Figure S1).
Vegetatively, the Abisko region straddles the boreal and arctic
biomes of northern Scandinavia. Boreal areas of Abisko are currently
dominated by the subalpine mountain birch forest (Betula pubescens),
with some pine (Pinus sylvestrus). Unforested arctic-­alpine areas are
most often confined to mires and the upper mountainous slopes, in-
cluding Mt. Nuolja (Figure S2a), with a high diversity of dwarf shrub
and herbaceous arctic plants (Table S1). The region has been widely
grazed by domesticated reindeer for centuries with varying intensi-
ties and land use practices especially since the 1800s (Emanuelsson,
1987). Major predators have largely been eliminated. Our study site
on Mt. Nuolja lacks melting glacial beds and has some of the low-
est levels of anthropogenic-­based nitrogen deposition in Europe
(Dentener, 2006)—­both can otherwise accelerate uphill colonization
of mountain plants, confounding tests of migrational responses to
climate.
The study transect consists of 20 contiguous permanent moni-
toring plots established from base to summit in 1916 (Figure S2). All
work during 1917–­1919 was conducted in 78 subplots within the 20
plots (each plot evenly subdivided into four subplots, except at the
summit), with data amalgamated to the plot level for analysis (Fries,
1925). These subplot data were subsequently lost; thus, all historical
comparisons in this paper are among-­plot. The plots are separated
by an average of 18.6 m of elevation depending on the steepness
of the mountain face (range 8.9–­63.06 m). Sampling began on May
25th in all years, with the longest period of sampling during the first
era of survey in 1918 (May 25th–­August 31st). Sampling ended ear-
lier in 1917 (August 7th) and 1919 (June 24th).
Sampling from 1917 to 1919 monitored seasonal trajectories
of plant phenology, including onset and senescence of leafing and
flowering, for all species at 5-­day intervals. The repeated visitation
of plots allowed accurate identification of all species, with sufficient
frequency to capture the timing of phenophase transition. The fre-
quency of plot re-­visitation every 5 days, however, demanded lo-
gistical trade-­offs given the mountainous and often snow-­covered
terrain with many dozens of species. To that end, all phenological
data were assessed at the plot level, thus ignoring the abundance
and phenological variation of species within plots. For example, the
timing of leaf senescence for a species would be determined by the
first observation of senescence by any individual of that species
in that plot. If that species was found in 10 plots on the transect,

MACDOUGALL et al.
then there would be 10 data points for that species at each sampling
period.
In addition to phenological shifts, the percent coverage of snow
per plot was also repeatedly measured every 5 days—­this was con-
ducted given the importance for the timing of snow melt by eleva-
tion for arctic plant phenology (e.g. Semenchuk et al., 2016; Wookey
et al., 2009). A 50 m measuring chain was sequentially laid, plot by
plot, along the entire mountain transect, with % snow cover deter-
mined by the distance of the chain contacting snow versus open
ground. This procedure was used in 1917–­1919 and again in 2017,
before switching to a Trimble R8 dGPS in 2018 to measure the lo-
cations of areas within the plots that were snow covered. We also
include snow melt data collected in 2019 using identical methods.
The transect plot markers were periodically maintained as re-
cently as the 1960s, enabling relocation of 59 of the 78 subplot poles
along the transect in 2016. Areas without poles were easy to identify
given the detailed description of distance and bearing between the
poles (Fries, 1925), and because the piles of rocks used to support
the missing poles remained evident. We were thus able to conduct
our contemporary surveys in the exact locations of the 1917–­1919
work, with one exception. In 1964, a chairlift was installed that bi-
sected the gradient within the birch woodland at ~650 m ASL; three
of the poles were laterally shifted by ~10 m in the summer of 1964,
perpendicular to the axis of the gradient. We used these data, de-
spite the shift.
During 2017 and 2018, the survey protocols for phenology and
snow cover from 1917 to 1919 were followed identically. Using the
exact plot locations, we were able to detect the altered plot-­level
distribution and performance of each species. This included mea-
surements at the mountain summit, which included plots 19 and 20
at an elevation from 1157 to 1184 m. For migration, we were able
to determine changes in mean plot distribution, shifts in the upper
maximum plot occurrence, changes in the lower minimum of occur-
rence, and whether species ranges have expanded or contracted
from the top, the bottom, or both. We also recorded the presence
of small juvenile plants, in areas where large-­sized reproductively
actively plants are currently absent. For phenological change, we
pooled 55,016 observations from 83 vascular plant species deriv-
ing from the repeated species-­specific plot visitation every 5 days
in both eras. Given that sampling ended earlier in 1917 and 1919,
we primarily compared phenology between 1918 and 2017–­2018 as
these years had complete data for emergence, flowering, and senes-
cence. We were able to include the 1917 and 1919 data to test dif-
ferences in emergence of leafing and flowering, especially whether
there were detectable advancements in one or both phenophases in
the modern era versus the early 20th century.
The data from 1917–­1919 included 156 species (Fries, 1925), rep-
resenting 47% of all species known from Abisko National Park at the
time (Fries, 1919). During the 2017–­2018 sampling period, an addi-
tional 15 species were recorded and all the previously reported spe-
cies were observed on the transect or nearby on the mountain. The
83 species chosen for our study were selected based on their pres-
ence in both eras and occurring in three or more plots. We eliminated
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5073
morphologically cryptic taxa or those that have undergone consider-
able taxonomic reclassification as a precautionary measure because
of uncertainty about their identification in the original dataset (e.g.
Anthoxanthum odoratum vs. A. alpinum, some sedges and willows).
Overall, there was a wide range in plot frequency per species (n/20
plots), with occupancy among the 83 species averaging 40%.
We classified the 83 species into four habitat categories, to test
whether species responses unfolded in definable ‘syndromes’ based
on established affinities with temperature and soil moisture (Table
S1). Boreal flora derived from forested habitats with southerly distri-
bution centres—­these taxa tend be expanding rapidly into the warm-
ing Arctic (Bjorkman et al., 2018; Vuorinen et al., 2017). Soil moisture
classifications centred on taxa with ‘broad’ tolerances including xeric
conditions, and cold-­affiliated ‘mesic’ species that are typically asso-
ciated with moist soils derived from seeps and melting snowbeds.
We also determined major traits of leaf biomass, leaf surface area,
and plant height for each species, testing whether plant morphology
predicted migrational response over time. Data were combined from
the TRY and the Tundra Trait Team databases (Bjorkman et al., 2018;
Kattge et al., 2011).
All phenology stages were defined by Fries (1925). The phenol-
ogy classification for each species was determined for six response
variables: first observed onset of leafing species−1 plot−1, first ob-
servation of leaf senescence species−1 plot−1, first observed onset
of flowering species−1 plot−1, first observation of flower senescence
species−1 plot−1, and the duration of leafing and flowering based on
the differences between onset and senescence for each species.
Senescence was defined as detectable changes in leaf or flower co-
lour, or the onset of visible wilting. For each of the six responses,
we calculated log response ratios derived from differences in means
among plots for the two sampling periods.
Changes in elevational occurrence were calculated by compar-
ing differences in plot presence/absence between the two sampling
periods. As described, we lacked exact measures of where individ-
ual plants occurred within a plot, but we did know the elevations of
the plots they occupied. We thus calculated change based on those
plot elevations. For example, a species occurring in plots 1–­3 in 1918
would have a mean elevation of 437.02 m based on the three start-
ing elevations of the plots (418.2, 436.3, and 456.6 m). If that same
species was found in plot 8–­10 in 2017, then its current mean eleva-
tion would be 705.5 m and its change over time would be +287 m (or
28.7 m per decade). We calculated elevational shifts in the maximum
and minimum plots of occurrence, by taking the differences of these
two measures between the time periods.
We used aerial drone imagery to test relationships among esti-
mated plant productivity (NDVI), elevation, and species distribution,
given that standing biomass can represent plant–­plant competitive
dynamics especially at lower elevations including larger plant in-
fluencing ground level temperature, light, and the timing of snow
melt. Aerial imagery was collected between 23 and 27 June 2018
using an eBee fixed-­wing drone (senseFly) in combination with a
Sequoia multi-­spectral sensor (Parrot) and a SONY DSC-­W X220
RGB camera. NDVI was calculated from the multi-­spectral sensor
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5074 MACDOUGALL et al.

and radiometrically calibrated using Mosaic Mill reflectance targets.
The imagery was georeferenced to >10 known DGPS locations of
equally distributed poles along the transect visible in the imagery.
Pix4dmapper was used for post-­processing of the imagery (Pix4D).
A 2 m resolution digital elevation model (© Lantmäteriet) was used
to derive terrain variables in SAGA GIS (Conrad et al., 2015). These
variables included slope, wind exposition index, SAGA wetness
index, and annual potential incoming solar radiation. NDVI and ter-
rain variables were extracted on a per pixel basis along a 10 m wide
buffered band along the 20 plots.
Our primary analyses (1918 vs. 2017–­2018) centred on testing
our two main hypotheses on upward migration and earlier leafing
and flowering, by describing the magnitude and direction of ele-
vational and phenological changes among the 83 species using log
proportional change in means (log response-­ratios) between the
two study periods. For our broader analysis of emergence (1917–­
1919 vs. 2017–­2018), we used ANOVA to test the relative effect of
year and era on the day of first observation of leaves and flowers
for each species—­these response data were log transformed given a
non-­normal bias in the data caused by the rapid emergence of many
species immediately following snow melt. We used principle compo-
nents analysis to examine relationships between major plant traits
and the extent of mean, maximum, and minimum elevational change
for the four major habitat groupings of plants. We used linear re-
gression to test relationships between elevation and snow melt by
year and season; how elevation influenced the timing of the onset,
duration, and senescence of leafing and flowering; and to deter-
mine associations between species-­specific distributional changes
at the maximum and minimum elevations of occurrence. We used
multiple correspondence analysis to test associations between four
vegetation classes based on temperature and moisture, and whether
species were lost, gained, or remain unchanged between the two
sampling eras. All analyses were conducted using JMP 14.0 (SAS
Institute Inc., 1989–­2019).
3 | R E S U LT S
The most detectable changes between the two eras of study were
migrational rather than phenological. Compared to 1918, 95% of the
83 species had altered mean distributions along the montane gradi-
ent (Figure 2). Most of these shifts have been upward, affecting 69%
of all taxa. There has been significant widening of species ranges,
averaging 7.5 m per decade and mostly explained by increases in
upper range limits. There were four species lost from the transect
(Table S1), although each currently resides nearby on the mountain
(Larson, unpublished data)—­we thus found no evidence of local ex-
tirpation despite pronounced warming in recent decades (Figure 1;
Figure S1). Conversely, there were 15 new occurrences since 1917–­
1919, mostly larger-­sized herbaceous plants with Boreal affiliations
(Table S1).
Although many species had higher average ranges, there was no
single shared response by all taxa (Figure 2). While mean range shifts
averaged 6.1 m decade−1, variation among species ranged 10-­fold.
Some species climbed ~½ km over the last century while others de-
scended to the same extent. Furthermore, higher mean range shifts
were associated with two responses: contraction from the bottom
or expansion at the top (contraction: F1,82 = 6.1, p < 0.02; expansion:
F1,82 = 21.1, p < 0.0001). Few species demonstrated both responses
such that increases in upper and lower occurrence limits were not
consistently related (F1,82 = 1.4; p = 0.24). Range contraction from
the base of the mountain by arctic-­affiliated taxa was presumably
related to an inability to persist in expanding woodland and shrub
thickets (Figures 2 and 3), especially in areas formerly characterized

F I G U R E 2 Distributional changes in mean elevation and range width for 83 species along a 900 m elevational gradient on Mt. Nuolja
Sweden—­1918 versus 2017. Species are grouped based on habitat affiliations of temperature (arctic and boreal) and moisture (broad
tolerance and mesic obligate; Table S1), following the maps of Mossberg et al. (1992) and the altitudinal limits of alpine species from Heintze
(2013), Kilander (1955), and Mossberg and Stenberg (2018). Arctic species of moister soils (green) are commonly associated with melting
snowbeds at our site. The black dots are the mean range and elevation changes of each species, surrounded by two-­dimensional density
contours (bivariate nonparametric density) for visualization purposes. Arrows indicate predominant qualitative responses within each of the
habitat groups [Colour figure can be viewed at wileyonlinelibrary.com]
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MACDOUGALL et al. 5075

(a) (b)

(c)
(i) Migr on differences
Range width (m) B Range minimum (m )
200 60
B

100
0
A A

0 -40

(ii) Trait differences

Leaf dry mass (g) B Plant height (m) B
60 0.40
B

AB
40
0.20

20 A
A
A A

0 Broad Mesic Broad Mesic Broad Mesic Broad Mesic

Arc Boreal Ar c Boreal

F I G U R E 3 (a) Principal coordinate relationships among migration changes 1918–­2017 (black), broad habitat groupings as per Figure 2
(red), and major morphological plant traits (blue). Trait data are from the TTT databases (Bjorkman et al., 2018). Overall, we see that larger
boreal plants, both woody and herbaceous, have wider distributional ranges largely associated with higher maximum range occurrence
since 1918. By contrast, arctic flora has narrower ranges associated with higher minimum elevations via displacement by boreal taxa,
warming at the mountain base, or both. (b) Differences in mean migration responses (1918–­2017) and traits among arctic and boreal plants
of mesic and broad soils. Upper-­case letters indicate significant differences among habitat classes, using Tukey's tests. The panel showing
changes in range minimum demonstrates the lowest elevational occurrence for arctic species has generally increased up the mountain while
boreal species have decreased, although differences among classes were not significant (F3,82 = 2.06; p=0.1135). Error bars show ±1 SE. (c)
Relationship between vegetation abundance and productivity per plot, based on NDVI and elevation on the Mount Nuolja transect. The best
fit is represented by the green polynomial (F2,19 = 35.3; p < 0.0001), encapsulating relatively high NDVI up to the present-­day shrub line, and
rapidly declining towards the summit. NDVI data were measured summer 2019. Dashed lines show the upper limit of the shrub zone in 1918
and 2017 [Colour figure can be viewed at wileyonlinelibrary.com]
 |
5076
Dimension 2 (8.2%, ʎ = 0.02)
Species lost
Mesic arcc
Mesic boreal
Species
gained
Broad boreal
Species unchanged
Broad arcc
Dimension 1 (91.8%, ʎ = 0.25)
F I G U R E 4 Century-­long changes in the composition of plant species on the summit of Mount Nuolja, Sweden, between 1917–­1919
and 2017–­2018, using Multiple Correspondence Analysis testing associations between four vegetation classes based on temperature and
moisture, and whether species were lost, gained, or remain unchanged. Differences were significant, with trends towards Broad boreal
and Mesic boreal species at the summit, and the loss of mesic arctic species which are now associated with lower elevation snowbeds
tend to persist longer into the growing season (n = 54, df = 6, R 2 = 0.15; Likelihood ratio Chi-­square = 14.8, p = 0.021; Pearson ratio 14.5,
p = 0.025). [Colour figure can be viewed at wileyonlinelibrary.com]
as open habitat but now with significantly greater standing biomass
(Figure 3c; Figure S2).
At the mountain summit, there were small net changes in overall
species richness but high turnover since 1917–­1919. There were 17
new summit species, mostly boreal taxa, which coincided with the
loss of 20% of species formerly present (Figure 4; Table S2). Loss
from the summit were mostly mesic arctic species of wetter and
cooler vernal conditions (Figure S4). These taxa were largely dis-
placed to lower elevations (Figure 2) where snowbeds persist lon-
ger (Figure 5). Interestingly, there was not a dramatic change in the
timing of snow melt at the summit since the early 1900s—­the sum-
mit has always become snow-­free earlier in the season compared
to downslope, presumably due to high wind and solar exposure
(Figure 5; Figure S2; Table S3).
Downslope, the treeline was higher by 63 m since 1918, subsum-
ing the former zone of shrubs (Figure S2). That shrub zone, however,
expanded even more and is now 123 m higher. Overall, expansion
of the forest and shrub zones has decreased the open alpine zone
by ~30% since 1918 (Figure S2). This upward expansion of woody
plants into high-­elevation open areas appears to be ongoing, with
a number of forest species including birch trees found recruiting in
all plots above the shrubline including the summit plots (Figure 6).
Snow melt dynamics among the 5 years examined varied strongly
by elevation and by year, but not by ‘era’ in the sense that trends in
the early 1900s and present-­day were similar (Figure 5a,b). Our data
for local long-­term winter weather (defined as November–­March
each year), combined with our plot-­level snow melt data, clearly
illustrate the well-­established positive connection between higher
winter temperatures and increased precipitation (F1,528 = 19.47;
p < 0.0001)—­warmer winters typically experience more snowfall.
There was variation in snowbed persistence with elevation, with
middle of the transect maintaining snow the longest into the summer
(Figure 5b). This trend has not changed over the last century with the
lower and warmer forested areas and upper and more exposed sum-
mit becoming snow-­free weeks or even months earlier (May 25th
snow melt [year, elevation]: F5,119 = 1.63; p = 0.157; Figure 5).
13652486, 2021, 20, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/gcb.15767 by Inst of Business Management, Wiley Online Library on [08/11/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
MACDOUGALL et al.
There was wide inter-­annual variability in phenology between
1918 and 2017–­2018, but no overall change in community-­level phe-
nological duration (Figure 7a,b). Similarly, our more extensive com-
parison of emergence between 1917–­1919 and 2017–­2018 showed
wide inter-­annual variability but with relatively smaller differences
among eras especially for leafing (Figure S3). The net effect is a simi-
lar pattern of plant emergence relative to snow melt, with high inter-­
annual variability depending on winter temperatures but no overall
difference in snow melt starting time on May 25th or by elevation
over the growing season (Figure 5).
For example, winter 2017 was warmer with more precipitation
(Figure S1), extending the spring melt period that, in turn, delayed
plant emergence compared to 1918. By contrast, 2018 had a cold
and dry winter with little snow (Figure 5; Figure S1) such that many
plots were snow-­free in late May—­predictably, emergence of leaf-
ing and flowering was many days faster in 2018 than 1918 or 2017.
However, this earlier emergence did not lead to longer phenological
duration. Duration was maintained by a tight connection between
emergence and senescence—­species that started earlier also ended
earlier, for both leafing and flowering (Figure 7). The net effect was
that the duration of growing season, defined as emergence to senes-
cence, was largely unchanged between 2017 and 2018 versus 1918
(F2,602 = 2.28; p = 0.104), although emergence in 2018 was almost
30 days earlier on average per species compared to 2017 (Figure 7).
4 | DISCUSSION
We tested for changes in the distribution and phenology of Arctic
Mountain plants between two sampling periods spanning 100 years.
Given pronounced local warming especially since the 1980s, we
anticipated a high likelihood of upward range shifts, a dramatic al-
teration towards earlier and extended leafing and flowering, and
possibly significant displacement of arctic-­affiliated flora. Overall,
we did observe pronounced range shifts by most species, accom-
panied by the invasion of southern-­affiliated flora. Phenologically,
 |

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MACDOUGALL et al. 5077

F I G U R E 5 Percentage snow cover

per plot for the years of 1917–­1919 and
2017–­2019, with mean temperature
averages per date (°C). Colours indicate
temperature ranges from colder (blue) to
warmer (red). (a) Mean percent snow of all
plots by date and (b) mean percent snow
cover by elevation for May 25th for the
early 20th (red) and early 21st centuries
(blue), with less at lower elevations in
areas dominated by woody plants and at
the exposed mountain summit [Colour
figure can be viewed at wileyonlinelibrary.
com]

however, there was wide inter-­annual variability but no detectable
pronounced differences in length of growing season between the
two survey periods—­relationships among snow melt, the onset of
leafing and flowering, and the timing of senescence were similar in
both eras. We also observed no evidence of species loss from the
mountain overall—­all taxa seen in the early 1900s were present
in the plots or, if displaced, still occurred nearby on the mountain.
These data represent a rare opportunity to look back in time, to test
for resilience mechanisms in arctic flora involving migration and phe-
nological adjustments against significant warming. They reveal that
distributional shifts, including range contraction, have likely helped
to maintain persistence, especially against the upward expansion of
southern-­affiliated plants. However, ongoing invasion by boreal taxa
into the remaining open arctic habitat, and a potential lack of flex-
ibility in the timing of senescence raise uncertainties about future
response trajectories.
One limitation in quantifying past climate responses in the arctic
is a rarity of spatially precise long-­term data. A warming arctic can
be more productive and highly invaded by southern taxa yet vari-
ability in these patterns can be widespread for reasons that are not
always clear (Berner et al., 2020; Myers-­Smith et al., 2020). These
mixed responses could reflect lags created by long generation times
of plants, the possibility that substantial change occurred prior to
onset of most studies, or that range impacts are localized, thus af-
fecting some portions of the range more than others. We observed
evidence suggesting the influence of each of these factors, providing
 |
5078
insight on the magnitude of change for arctic plants and the under-
lying causal mechanisms.
For species distributions, the average mean range shift of 6.1 m
−1
higher per decade was less than the 11 m decade estimate of Chen
et al. (2011) but identical to Parmesan and Yohe (2003). These higher
mean ranges reflect both upward migration and contraction from the
lower range limits, with few species demonstrating both responses.
Changes in maximum elevation have commonly been used to esti-
mate overall montane range shifts but can be biased if they reflect
rare uphill dispersal—­our work shows that mean and maximum range
shifts closely align. At the summit, we observed limited net change in
species richness, a finding contrary to other studies reporting signif-
icant gains or reductions in richness by a range of mechanisms (e.g.
Niskanen et al., 2019; Steinbauer et al., 2018; Thuiller et al., 2008,
2005). We did observe, however, significant underlying species turn-
over with the downward displacement of mesic arctic taxa being
offset by the colonization of wind dispersed taxa and arctic plants
with broad habitat tolerances including xeric conditions. Finally, our
migration data illustrate an array of species-­specific responses in-
cluding expansion, contraction, or retreat, demonstrating that single
drivers of distributional change in arctic flora are unlikely. For ex-
ample, the upper range limit of mesic species Oxyria digyna dropped
by 114 m since 1917–­19 but its mean elevation only changed +10 m
because of a similarly large contraction from below (204 m higher)—­
the small change in mean distribution hides a narrowing range width
by 318 m.
Despite these variable species-­level changes in distribution, we
did detect several broad response syndromes—­rapidly climbing bo-
real species invading from lower elevations, a small group of arc-
tic species whose mean distribution shifted downhill, and a group
of arctic species with higher mean distributions driven mostly by
low-­elevation contraction. Invading southern species were plants
typical of Boreal Scandinavia, with distributional centres below the
Arctic Circle including the widespread canopy tree B. pubescens and
a suite of woody shrubs especially non-­Arctic species of Salix. This
13652486, 2021, 20, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/gcb.15767 by Inst of Business Management, Wiley Online Library on [08/11/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
MACDOUGALL et al.
F I G U R E 6 Invasion of boreal genera
above the maximum extent of the
shrubline on Mount Nuolja, Sweden. Each
dot represents the location of a seedling
or stunted individual of a species where
no mature adults exist. The bottom
axis, at ~600 m, represents the upper
elevation limit of the current tree-­and
shrubline [Colour figure can be viewed at
wileyonlinelibrary.com]
expansion of woody trees and shrubs is consistent with observations
in arctic landscapes globally (Myers-­Smith et al., 2011). There was
also a compliment of invading herbaceous flora mostly of the forest
understory, which have been reported as expanding to higher lati-
tudes and elevations elsewhere (Pauchard et al., 2016), and are gen-
erally taller and faster growing than most arctic flora. Interestingly,
many of these advancing boreal species are palatable to reindeer,
with preferential grazing elsewhere acting to stabilize arctic com-
munities against their establishment (Olofsson et al., 2009). Indeed,
reindeer herds persist on Mount Nuolja, sometimes in large num-
bers, but do not occur at the consistently high densities seen else-
where in the Scandes Mountains, and seemingly not in high enough
densities to resist tree and shrub expansion. In particular, the use of
the lower parts of the transect by reindeer has decreased since the
1917–­1919 due in part to changes in herding practices (Callaghan
et al., 2013)—­this may play a contributing role in the upward invasion
of plants at our site that might be resisted elsewhere (e.g. Sorensen,
1941).
The second response group was arctic flora of mesic habitats,
with generally narrower and lower range occurrences including dis-
placement from the summit. There have been previous reports of
montane flora descending with climate warming, with lower slopes
having higher moisture availability (Crimmins et al., 2011). We
suspect this is the case at our site. A key factor for summer mois-
ture availability, at the summit in particular, is melting snowbeds.
Interestingly, our data show no substantial change in the timing of
snow melt at the summit or down slope. What has changed, how-
ever, are local temperatures such that plants are almost certainly
experiencing warmer and possibly drier conditions whenever they
first emerge and throughout the growing season. This suggests that
the persistence of mesic arctic species may be increasingly linked
to snowbeds, which last longer at lower elevations. We lack direct
data to test this association, but it is consistent with reports from
elsewhere globally where plant responses to warming are shaped by
moisture availability (e.g. Gilbert et al., 2020).
 |

13652486, 2021, 20, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/gcb.15767 by Inst of Business Management, Wiley Online Library on [08/11/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
MACDOUGALL et al. 5079

2017
(a) (b)
60

40
Flowering
20
Leafing

End of phenophase compared to 1918

0

– 20

– 40

– 60

60 2018
40

20

0 Flowering
Leafing
–20

–40

–60

-70 – 50 – 30 – 10 0 10 30 50 70
Days shorter days longer
Start of phenophase compared to 1918

F I G U R E 7 (a) Comparison of phenological emergence, senescence, and duration by elevation for combined phenological stages, 1918
versus 2017 (blue) and 2018 (red), testing the hypothesis that recent decades of warming would see earlier and more extended phenophase
activity. Phenological onset for 2017 was generally later than 1918 because of pronounced late winter snow accumulation, which delayed
leaf emergence and flowering. The opposite pattern occurred in 2018, with snow melt 1 month earlier than 1918. Despite that, the
durations of phenology for 2017 and 2018, relative to 1918, are largely overlapping (average 2017: 1.98 days shorter [SE = 1.1]; average
2018: 1.21 [SE = 1.2]) and did not differ (F1,602 = 3.67; p = 0.06). Shaded bands indicate 1 ± SE for the overall mean of all species. Error bars
indicate 1 ± SE for each species. (b) Relationship between phenological emergence and senescence for leafing versus flowering, for 1918–­
2017 (top) and 1918–­2018 (bottom). Despite pronounced differences in winter climate (Figure S1), snow melt (Figure 5), and emergence
and senescence, the timing of the two phenophases are significantly associated in both years (2017: F1,264 = 10.4, p < 0.0001; 2018:
F1,264 = 4.56, p = 0.03). This tight pairing in both years occurred despite flowering duration in 2017, for example, being shorter than 1918
while leafing duration was longer; flowering duration in 2018 was similar to 1918 while the duration of leafing was much longer. Shaded
bands indicate 1 ± SE for the overall mean of all species. Points are for each species [Colour figure can be viewed at wileyonlinelibrary.com]

Finally, there was a response group of arctic species associ-
ated with areas of open meadow between the treeline and summit.
Although these species can have broad habitat affinities and the
magnitude of their distributional shifts since the early 1900s varies,
they are generally unified by having higher mean range occurrences
driven by displacement from lower elevations. Overall, expansion of
the forest and shrub zones has decreased the size of this open alpine
zone by ~30% since 1918, consistent with other systems showing
that mountain species can become increasingly habitat limited as
southern species sweep uphill (e.g. Alexander et al., 2015; Pauchard
 |
5080
et al., 2009, 2016). Furthermore, our work suggests that this trend
is likely to continue, if not accelerate. We observed birch tree seed-
lings recruiting in every plot above the shrubline, indicating that
environmental conditions are sufficient for tree establishment and
short-­term persistence, even if they are currently too extreme for
survival to adulthood. Given that recent and projected future trends
show ongoing warming for the arctic; however, the survival odds of
these upward invaders may increase.
Migration is a longer-­term response to climate involving new col-
onization. Given the dramatic inter-­annual and interdecadal swings
in climate seen in our region, shifts in phenological timing would
presumably be a more immediate mechanism of resilience. Indeed,
such shifts have been seen widely in arctic flora, including both
earlier emergence and contraction of flowering seasons (Prevey
et al., 2019). Other studies have shown the importance of warmed
autumns, for extending growing seasons and invasion (e.g. Fridley,
2012), which are less tested in arctic systems (Gallinat et al., 2015).
Here, we possess an unprecedented measure of plant leaf and flow-
ering phenology. In short, we see dramatic inter-­annual variability in
phenology that was similar within both eras, but no overall change
in phenological duration—­unexpectedly, the length of time between
emergence and senescence in the early 1900s and now is similar.
The reasons for this lack of change in duration appear to be two-
fold. Foremost is the timing of snow melt—­we found that phenolog-
ical emergence each year is regulated by snow cover, not warming
per se (e.g. Assmann et al., 2019; Bjorkman et al., 2015), and that the
average timing of snow melt has not shifted substantially, by eleva-
tion or by timing in spring. Our data for local long-­term weather and
plot-­level snow melt clearly illustrate the well-­established positive
connection between winter temperature and precipitation: our re-
gion is warmer overall, and as a result warm winters receive higher
snowfall that presumably takes longer to melt in the spring. The net
effect is a similar pattern of plant emergence relative to snow melt
between 1918 and 2017–­2018, with high inter-­annual variability de-
pending on winter temperatures, but no overall difference in snow
melt starting time on May 25th or by elevation over the growing
season.
The second factor preserving phenological performance was
the tight connection between emergence and senescence—­species
that started earlier also ended earlier, for both leafing and flowering.
The net effect was that the duration of growing season, defined as
emergence to senescence, was largely unchanged. Reports of lack of
change in phenological duration have been made elsewhere in the
Arctic (Myers-­Smith et al., 2019; Semenchuk et al., 2016). Our work
indicates this could be a consistent trend, at least between the two
time periods of our study.
The reasons for tight linkages of emergence and senescence are
difficult to determine. One possibility relates to growing conditions
in 2018, with a considerably warmer summer potentially triggering
early senescence—­mean temperatures in May 2018 were six times
warmer than the previous year, and never went below zero. July
2018 was three times warmer than July 2017, with highs of 23°C.
These spring and summer temperatures for 2018 are well above
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MACDOUGALL et al.
both century-­long and 30-­year averages for our region. An alterna-
tive explanation is the presence of some level of adaptive canaliza-
tion in arctic plants, where the duration of phenological periods is
fixed relative to emergence, although growing conditions into the
summer could remain favourable (Semenchuk et al., 2016). Several
Arctic studies have alluded to this possibly of phenological ‘hard-­
wiring’ (Semenchuk et al., 2016; Sorensen, 1941; Starr et al., 2000;
Wookey et al., 2009), possibly due to evolved physiological time
constraints on reproductive completion to avoid late-­summer cold
or drought. They may also be adaptive connections that maintain
synchrony with pollinators, which also emerge at snow melt and
can have short foraging seasons at high latitudes (Semenchuk et al.,
2016). Regardless, the net effect was no detectable net change in
duration despite significant climate changes. It is critical to note that
this does not necessarily mean there are no adaptations to arctic
warming at our study area. However, if they have occurred, they
would be difficult to detect because inter-­annual changes in climate
and snow melt are so large as to mask any adaptive changes during
the last 100 years. As well, most of the 83 species were examined
are long-­lived perennials such that 100 years of warming may still
only span one or several generations at most.
There are several prognoses for the future of our high-­latitude
mountain plant community. Ongoing upward expansion from south-
ern species threatens to increasingly restrict the extent of non-­
forested habitat (e.g. Arft et al., 1999; Van Bogaert et al., 2011). We
also detected migration shifts by most species, which we interpret as
direct or indirect responses to warming temperatures but also mois-
ture availability controlled by snow melt. Clearly, arctic montane
plants face challenges in time and space. Temporally, the easiest
responses are immediate within-­season adjustment in phenology,
which we observed for most species. Spatially, however, the risk
of not moving is to be over-­run by boreal species sweeping uphill.
Temporal responses may be necessary to withstand the immediate
effects of warming, but insufficient longer term. Finally, the largely
concordant trends in leafing and flowering phenology indicate capa-
bilities of both phenophases to rapidly adjust to inter-­annual varia-
tion in conditions but also suggests their responses may be tightly
coupled (e.g. Kochmer & Handel, 1986). Any form of tight coupling
where flowering is dependent on vegetative development may be
expected on Arctic Mountains, given their narrow and sometimes
unpredictable growing seasons. However, any coupling of pheno-
phases, especially a limited flexibility in flower time, could become
problematic with more extreme arctic climates. The strength of phe-
nological coupling between leafing and flowering in arctic flora re-
quires further testing.
There are several caveats to our results. The first is the clear
difficulty in accurately quantifying trends in early emergence, given
that the key driver of emergence—­snow melt—­can fluctuate inter-­
annually by weeks or even months. Relatedly, the same quantifica-
tion challenges exist with the influence of elevation—­inter-­annual
fluctuations in phenological performance including emergence and
senescence interacted strongly with elevation. Many of our species
are distributed across at least two of the three broad vegetation

MACDOUGALL et al.
zones (e.g. forest, open alpine, summit) such that ‘early emergence’
will likely unfold differently for species by location. Finally, our long-­
term historical comparisons have potential challenges, in that the
year of comparison with contemporary trends profoundly shapes
analytical outcome. For example, we would have observed signifi-
cantly different comparative outcomes in phenology if our historical
data derived from the 1960s, when conditions were the coldest in
the last 110 years.
There are numerous reports of large and rapid transformation
in the diversity and distribution of the high-­latitude montane flora,
with suggestions that this system may be a bell-­weather for wide-
spread species loss in ecosystems globally. These projections have
been modelled (e.g. Niskanen et al., 2019) or based on data that
are often lacking in spatial or temporal precision because of histor-
ical limitations. Here, we have data for dozens of species, pulling
back the curtain on plant responses over a century. Species have
adjusted their distributions profoundly, providing possible tempo-
rary refuge especially against invading southern plant communi-
ties. However, with potential limits on phenological duration, the
downwards contraction of some arctic flora towards areas with the
most persistent snowbeds, and non-­arctic invaders at every point
along the gradient including the summit, our work demonstrates
that Arctic Mountain species are being increasingly squeezed from
all sides.
DATA AVA I L A B I L I T Y S TAT E M E N T
Data available on request due to privacy/ethical restrictions.
ORCID
Andrew S. MacDougall https://orcid.org/0000-0002-1869-7868
Paul Caplat https://orcid.org/0000-0002-2449-3079
Johan Olofsson https://orcid.org/0000-0002-6943-1218
Matthias B. Siewert https://orcid.org/0000-0003-2890-8873
Ellen Esch https://orcid.org/0000-0002-4253-0910
Keith Larson https://orcid.org/0000-0001-7089-524X
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J., Siewert, M. B., Bonner, C., Esch, E., Lessard-­Therrien, M.,
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K., Fries, T. C. E., & Larson, K. (2021). Comparison of the
distribution and phenology of Arctic Mountain plants between
the early 20th and 21st centuries. Global Change Biology, 27,
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