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Experimental Warming Alters
Productivity and Isotopic Signatures
of Tundra Mosses
Kirsten K. Deane-Coe,
1,3
* Marguerite Mauritz,
2,3
Gerardo Celis,
3
Verity Salmon,
3
Kathryn G. Crummer,
3,4
Susan M. Natali,
5
and Edward A. G. Schuur
2,3
1
School of Integrative Plant Sciences, Cornell University, Ithaca, New York 14853, USA;
2
Department of Biological Sciences, Northern
Arizona University, Flagstaff, Arizona 86011, USA;
3
Department of Biology, University of Florida, Gainesville, Florida 32601, USA;
4
School of Forest Resources and Conservation, University of Florida, Gainesville, Florida 32601, USA;
5
Woods Hole Research Center,
Falmouth, Massachusetts 02540, USA
ABSTRACT
In the tundra, mosses play an important functional
role regulating belowground and ecosystem pro-
cesses, but there is still considerable uncertainty
about how tundra moss communities will respond to
climate change. We examined the effects of 5 years of
in situ air and soil warming on net primary produc-
tivity (NPP), carbon (C) and nitrogen (N) isotope
signatures (d
13
Candd
15
N), and C:N in dominant
Alaskan tundra mosses. Air warming increased mean
air temperatures by up to 0.5C and resulted in an 80–
90% reduction in NPP in the feather moss Pleurozium
and the peat moss Sphagnum. Soil warming increased
permafrost thaw depth by 12–18%, upper soil water
content by 23–27%, and resulted in a threefold in-
crease in Sphagnum NPP. d
13
C was positively corre-
lated with moss NPP, and increased by 0.5–1& in all
mosses under soil warming. C:N was reduced in
Sphagnum and Pleurozium, due to increases in tissue
%N in the soil warming treatment, suggesting that
moss N availability could increase as temperatures
increases. Higher N availability in warmer conditions,
however, may be offset by unfavorable moisture
conditions for moss growth. Similar to responses in
tundra vascular plant communities, our results fore-
cast interspecific differences in productivity among
tundra mosses. Specifically, air warming may reduce
productivity in Sphagnum and Pleurozium,butsoil
warming could offset this response in Sphagnum.
Such responses may lead to changes in tundra moss
community structure and function as temperatures
increase that have the potential to alter tundra C and
N cycling in a future climate.
Key words: global change; permafrost; bryo-
phytes; Sphagnum; Pleurozium; Dicranum; NPP; d
13
C;
d
15
N.
INTRODUCTION
Climate change is projected to be the greatest and
most rapid in the high latitudes (Houghton and
others 1996; IPCC 2013). Temperature increases in
the tundra are projected to be twice that of the
global mean (ACIA 2004), and tundra plant com-
munities and ecosystems often display directional
responses to warming (Epstein and others 2004;
Received 3 February 2015; accepted 30 March 2015;
published online 20 May 2015
Author contribut ions KKDC conceived and designed the study,
performed research, analyzed data, and wrote the manuscript. MM and
GC analyzed data and contributed to manuscript revisions. VS performed
field research, developed models, and contributed to manuscript revi-
sions. KGC performed isotopic analyses. SMN implemented the original
field experiment and contributed to manuscript revisions. EAGS designed
and supervised the field experiment and contributed to manuscript re-
visions.
*Corresponding author; e-mail: kkc32@cornell.edu
Ecosystems (2015) 18: 1070–1082
DOI: 10.1007/s10021-015-9884-7
2015 Springer Science+Business Media New York
1070
Hudson and Henry 2009; Elmendorf and others
2012a). There is now substantial evidence from
passive warming experiments in the tundra that
vascular plant biomass and growth are affected by
increased temperatures (Chapin and others 1995;
Chapin and Shaver 1996; Hobbie and Chapin 1998;
Borner and others 2008). In particular, warming is
resulting in an increase in cover of graminoids and
deciduous shrubs (Arft and others 1999; Brooker
and van derWal 2003; Walker and others 2006;
Elmendorf and others 2012b; Natali and others
2012), as well as woody shrub expansion into
novel habitats (Tape and others 2006; Forbes and
others 2010).
In the tundra, deep soils are frozen year-round as
permafrost, and a shallow annual thaw (<1m)
creates a seasonally variable active layer. Processes
occurring just above the active layer at the soil
surface exert strong regulatory control on feed-
backs and exchange between tundra soils and the
atmosphere. Soil surfaces in the tundra are nearly
always covered by a thick and diverse photosyn-
thetic layer dominated by mosses. This moss layer
regulates soil temperature and moisture (Beringer
and others 2001; Gornall and others 2007;
Soudzilovskaia and others 2013), and in doing so
controls water availability to plant and soil organ-
isms as well as evaporative losses to the atmo-
sphere. Mosses living in this layer also can
dominate ecosystem carbon (C) inputs during
spring and fall (Campioli and others 2009), when
vascular plants are the least active, which influ-
ences ecosystem C balance (Beringer and others
2001; Gornall and others 2007; Rydin and Jeglum
2013; Lindo and others 2013; Street and others
2013). In addition to contributing to C cycling,
mosses can alter nitrogen (N) cycling of tundra
ecosystems. Two of the dominant functional types,
feather mosses and peat mosses, commonly asso-
ciate with N
2
-fixing cyanobacteria, which repre-
sents a substantial N source of tundra ecosystems
(Solheim and others 1996; DeLuca and others
2002, 2007; Markham 2009). Given their known
importance as an intrinsic ecological component of
high latitude ecosystems, changes in productivity
and species composition of tundra mosses are likely
have a profound impact on regional biogeochem-
istry and feedbacks to global climate.
In spite of their ecological role, it is still unclear
how mosses in high latitude ecosystems will re-
spond to projected change. Abundance of tundra
peat mosses (for example, Sphagnum) and feather
mosses (for example, Pleurozium) has been shown
to increase as a function of temperature along
natural gradients (Gunnarsson 2005; Hudson and
Henry 2009; Lang and others 2012). But abun-
dance and cover of these mosses remains un-
changed, or, more commonly, decreases as a
function of temperature in experimental warming
studies (Press and others 1998; Wahren and others
2005; Walker and others 2006; Lang and others
2012). These contrasting results may arise because
moss functioning is seldom directly addressed in
most tundra warming experiments that are pri-
marily designed to assess vascular plant or soil re-
sponses to increased temperatures.
Productivity in many mosses is governed by en-
vironmental water availability because tissue water
content varies passively with the surrounding en-
vironment, and physiological performance and
growth can be limited at both high and low ends of
the spectrum (Dilks and Proctor 1979; Rice and
Giles 1996; Williams and Flanagan 1996; Toet and
others 2006; Coe and others 2012). Mosses also
typically display the majority of their annual
growth during the shoulder seasons (just before
and just after the growing season), where they are
often photosynthetically active under snowpack
and can account for up to 25% of net aboveground
carbon accumulation (Campioli and others 2009).
Although long-term temperature manipulation
experiments in the northern latitudes over the last
30 years have been ecologically extremely infor-
mative (van Wijk and others 2004; Elmendorf and
others 2012b), most experimental warming in the
tundra has taken place during the growing season
only (for example, Chapin and Shaver 1985; Press
and others 1998; Hobbie and others 1999). The few
designs that have successfully increased winter
temperatures do so using increased snow depth (for
example, Wahren and others 2005), but the spring
melt-out from the larger snowpack simultaneously
delays the start of the growing season and increases
ecosystem moisture inputs. Temperature increases
are very likely to influence water availability to,
and hence productivity of, tundra mosses, espe-
cially in areas undergoing permafrost thaw and
subsidence (Camill and others 2001), but tem-
perature manipulations confounded by unintended
moisture alterations make it difficult to discern
causation of plant responses.
Tundra mosses also have very different growth
forms relative to their vascular neighbors: they
grow as loose lateral mats, dense turfs, or deep
hummocks, and most do not possess annual growth
markers. Changes in moss biomass and produc-
tivity under warming conditions, therefore, may
not be reflected in traditional sampling techniques
for vascular plants (Henry and Molau 1997; van
Wijk and others 2004; Elmendorf and others
Tundra Moss Productivity Under Global Change 1071
2012b). Analyses of stable C and N isotopes in moss
tissues have the potential to provide information
on moss nutrient status and productivity, par-
ticularly if combined with moss-specific net pri-
mary productivity (NPP) measurements.
Because of the confounding influences of increased
temperature and increased water availability in pre-
vious warming studies, and the limitations of tradi-
tional plant sampling techniques, it has thus far been
extremely challenging to draw conclusions for moss
response to warming in the tundra. Here, we exam-
ined the influence of warming temperatures on three
dominant Alaskan tundra moss genera, Sphagnum,
Pleurozium,andDicranum, using a long-term field
experiment that increased temperatures on an an-
nual basis using soil warming (during the winter, via
passive insulation with snow) combined with air
warming (during the growing season) without ma-
nipulating ecosystem moisture inputs (see Natali and
others 2011). We examined changes in moss NPP, C
and N isotopic signatures, and C:N after 4 and 5 years
of warming. Based on the relationship between tissue
water content and productivity in mosses, we hy-
pothesized that (1) air warming would result in re-
ductions in moss productivity, because higher air
temperatures that may increase potential
evapotranspiration could function to reduce water
availability to mosses; but (2) soil warming would
result in increased moss productivity, because in the
absence of air warming mosses would not be limited
by temperature or water availability and might also
benefit from increased soil N. Further, because
Sphagnum, Pleurozium,andDicranum differ in relative
growth rates and tolerance to altered hydrologic en-
vironment, we predicted that the relative magnitude
of responses to warming would differ across moss taxa
and would be reflected in C and N isotopic signatures.
METHODS
Site Description
The Carbon in Permafrost Experimental Heating
Research (CiPEHR) project, established in 2008, is
located at the Eight Mile Lake study site in the
Northern foothills of the Alaska Range (6352¢59¢N,
14913¢32¢W, c. 700 m elevation). Mean monthly
temperatures range from -16C in December to
+15C in July, with a historic mean annual tem-
perature (1976–2013) of -1.0C and more recent
(2004–2013) mean annual temperature of -2.7C.
The site is positioned on moist acidic tundra with
Gelisol soils composed of a 0.45–0.64 m thick or-
ganic horizon above a cryoturbated mineral soil.
The active layer (c. 50–60 cm thick) thaws annu-
ally during the growing season, and is situated
above a perennially frozen layer of permafrost. For
additional site details please refer to Schuur and
others (2007, 2009) and Natali and others (2011).
Dominant vascular plants at the site are the
tussock-forming sedge Eriophorum vaginatum, the
deciduous shrubs Betula nana and Vaccinium uligi-
nosum, and the evergreen groundcovers V. vitis
idaea and Rhododendron subarcticum. Common li-
chen genera include Cladonia, Cetraria, Flavocetraria,
and Peltigera. The three dominant mosses at the site
are Sphagnum fuscum, Pleurozium schreberi, and Di-
cranum spp. Other common mosses include Aula-
comnium turgidum, A. pallustre, Hylocomium
splendens, Polytrichum commune, P. strictum, S.
squarrosum, S. magellanicum, S. girghonsonii, S. cus-
pidatum, and S. compactum.
Experimental Design
Soil warming was achieved using snow fences
(1.5 m tall 9 8 m long, n = 6) placed perpendicular
to the prevailing wind direction that trapped insu-
lating layers of snow during the winter. To control
water input during snowmelt in warming plots,
and to enable us to isolate warming effects from
moisture effects or delayed phenology, excess
snowpack was removed from warming plots before
spring thaw. All plots were snow-free by 1 May in
2009–2012 and by 1 June in 2013.
Each soil warming and control treatment area
within a treatment pair (on either side of a snow
fence) contained four plots: two air warming plots
and two control plots (n = 24 each, across 6 fen-
ces). Air warming was applied during the growing
season using plexiglass open top chambers
(0.36 m
2
9 0.5 m tall) placed over plots from May
through September. Treatments will be referred to
in figures and analyses as follows: Control, air
warming only (Air), soil warming only (Soil), and
combined annual soil and air warming (Air + Soil).
Additional information on the experimental design
can be found in Natali and others (2011, 2012),
although note in previous publications that treat-
ments were referred to as follows: Ambient (Con-
trol), Summer Warming (Air), Winter Warming
(Soil), and Annual Warming (Air + Soil).
Environmental Monitoring
Constantan-copper thermocouples were used to
measure soil temperature at 5 and 10 cm depths,
and in each plot, and air temperature 10 cm above
the tundra surface was monitored with thermistors.
Surface soil moisture (gravimetric water content)
1072 Deane-Coe and others
was measured at 5-cm depth in each plot using DC-
half-bridge resistance measurements. Depth-inte-
grated (0–20 cm) soil moisture (volumetric water
content) was measured using CS-616 water con-
tent reflectometer probes (Campbell Scientific Inc.,
Logan, Utah, USA). Air temperature, soil tem-
perature, and soil moisture were measured half-
hourly and recorded to a Campbell Scientific CS-
1000 datalogger.
Percent Cover, Biomass, and NPP
Moss percent cover in each plot was measured
using a 60 9 60 cm grid placed over each plot. The
percent cover within each 8 9 8 cm grid square
was recorded for each of three dominant moss
types: Pleurozium spp. (primarily P. schreberi), Di-
cranum spp., and Sphagnum spp. (primarily S. fus-
cum, and also including S. girgensohnii, S.
magellanicum, and S. compactum). Cumulative per-
cent cover for each moss type and total moss per-
cent cover was recorded for each plot.
Moss biomass was determined using a non-de-
structive point-frame method using a 60 9 60 cm
point frame with a grid size of 8 9 8 cm (Walker
1996). At each of the 49 intersecting grid points, a
3-mm-diameter metal rod was inserted vertically
through the tundra plant canopy. Species (or
genus) identity and number of ‘hits’ were recorded
for every moss shoot that touched the rod. If the
bottom end of the rod became inserted into a dense
tuft or mat of Dicranum spp. (the growth form this
genus typically exhibits in this habitat), where it
was difficult to count the number of touching
shoots in the field, the number of Dicranum ‘hits’
was recorded as four. This was previously deter-
mined experimentally by removing a 20 9 20 cm
section of Dicranum from the field, and manually
counting the number of shoots touched by the rod
inserted into the mat (n = 50, mean hits = 4 ± 0.2;
data not shown). We determined moss biomass per
plot using allometric relationships describing the
relationship between moss ‘hits’ per point and
biomass (g m
-2
) from six 60 9 60 cm destructive
harvest plots adjacent to the site (Table 1).
To estimate NPP for the acrocarpous Sphagnum
spp. and Dicranum spp., we used the cranked wire
method, which measures vertical growth of moss
using a stainless steel reference wire inserted at the
moss surface (Clymo 1970). We placed 3–5 cranked
wires in each treatment at all fences and measured
growth from May to September. Vertical growth for
these two species was converted to biomass incre-
ment using allometric equations developed for an
adjacent site (Schuur and others 2007), and point
estimates were multiplied by percent cover in each
plot. To estimate NPP for the pleurocarpous P.
schreberi, we used the product of linear growth per
stem (measured using the change in distance from
the shoot tip to the ‘‘branch’’ above a small refer-
ence wire twisted around a portion of the stem),
stem density, biomass per unit stem growth, and
percent cover (Benscoter and Vitt 2007).
Tissue Carbon and Nitrogen Analyses
In plants, d
15
N(
15
N:
14
N compared to the atmo-
spheric air standard) represents the relative tissue
nitrogen composition from different sources (Evans
2001), and d
13
C [((
13
C:
12
C
sample
/
13
C:
12
C
standard
) -
1)*1000&] represents discrimination against
13
CO
2
during the processes of CO
2
diffusion into leaves
and subsequent fixation by the enzyme Rubisco. In
C3 vascular plants, d
13
C is directly linked to the
ratio of partial pressures of CO
2
inside the leaf (c
i
)
compared to outside the leaf (c
a
), and reflects the
balance between net C assimilation and stomatal
conductance, thus providing information about
plant water status. Mosses are also C3 plants, and
possess the same photosynthetic machinery (in-
cluding the discriminating enzyme Rubisco) but do
not possess stomata or other active means for
regulating water status, and water content is con-
trolled by that of the surrounding environment.
Carbon uptake in mosses is impeded at very high
water contents due to diffusion limitation of CO
2
through films of surface water, and at low water
contents due to an overall decrease in metabolic
processes. Net C assimilation in mosses therefore
represents a balance between conductance and
photosynthetic capacity (both of which relate to
water content) and is typically maximized at in-
termediate water contents (Dilks and Proctor 1979;
Rice and Giles 1996; Williams and Flanagan 1996;
Coe and others 2012). Similar to C3 vascular
plants, d
13
C in mosses reflects biochemical dis-
crimination against the heavier isotope during
photosynthesis, yet in contrast to vascular plants,
d
13
C varies with water status imposed by the sur-
rounding environment rather than active regula-
tion via stomata. Overall, moss d
13
C provides
information about photosynthetic performance and
relative growth rates, integrates moss photosyn-
thetic activity throughout a growth period, and
typically increases as a function of water avail-
ability (Rice and Giles 1996; Rice 2000).
We collected moss shoots of Sphagnum, Pleu-
rozium, and Dicranum in July 2012 and 2013 from
all treatment replicates for tissue N and C content
as well as d
15
N and d
13
C analyses. Samples from the
Tundra Moss Productivity Under Global Change 1073
same treatments at each snow fence were pooled to
ensure that sufficient sample material was collected
while minimizing destructive harvesting. Shoots
were dried at 60C, ground, and analyzed on a
Thermo Finnigan (Waltham, Massachusetts, USA)
continuous flow isotope radio mass spectrometer
coupled to a Costech (Valencia, California, USA)
elemental analyzer. Isotope corrections for delta
13
C
were performed with a peach leaf standard refer-
ence material (NIST 1547) relative to VPDB, and
d
15
N relative to air.
Statistical Analyses
All data processing and analyses were performed
using the R platform (R development core team
2015). Air temperature, soil temperature, soil
moisture, thaw depth, d
13
C, d
15
N, and tissue C:N
data were analyzed with a mixed linear model
analysis of variance (ANOVA) using a blocked de-
sign with soil warming and air warming as fixed
factors, and block and fence (nested in block) as
random factors. Biomass and NPP data were ana-
lyzed using the framework above, only percent
cover (PC) was added as a continuous predictor in
models because these are area-based measures of
productivity. Tukey’s HSD post hoc comparisons
were used to determine significant differences
within groups. Data were transformed when nec-
essary to meet ANOVA distribution requirements,
and all errors presented represent one standard
error of the mean.
RESULTS
When measurements were conducted, plots had
been warmed continuously for either four (2012) or
five (2013) years. Ambient conditions in 2013 were
significantly drier than 2012, in terms of 0-20 cm
depth-integrated moisture (VWC) (P < 0.05), 5 cm
depth soil surface moisture (GWC) (P < 0.05), and
total precipitation: 228 mm (2012), 138 mm (2013)
(Table 2). Air temperatures were also 2–3Cwarmer
in 2013 compared to 2012 (P < 0.05). The air
warming treatment alone did not increase mean
growing season air temperature in 2012, but
increased it by 0.4Cin2013(P < 0.01). The air +
soil warming treatment resulted in a 0.2Cincrease
in growing season air temperature in 2012, and a 0.6
increase in 2013 (P < 0.05). Soil warming increased
average 10 cm soil temperatures by 0.10–0.25Cin
2012 and did not change 10 cm temperatures in
2013. Five centimeter soil temperatures were not
altered by the warming treatments in 2012, and
were slightly reduced by air warming in 2013 (Ta-
ble 2). Air warming resulted in a 4.9% increase in
GWC and no change in VWC in 2012, and no
change in either GWC or VWC in 2013. Soil
warming resulted in a 10% increase in GWC and an
11% increase in VWC in 2012, and a 17% increase
in GWC and a 12% increase in VWC in 2013.
Air + soil warming resulted in a 27% increase in
GWC and an 22% increase in VWC in 2012, and a
23% increase in GWC and a 22% increase in VWC
in 2013 (Table 2). Growing season permafrost thaw
depth was also increased by warming in both years:
in 2012 thaw depth was 13% deeper in the soil
warming plots and 12% deeper in the air + soil
warming plots, and in 2012 thaw depth was 18%
deeper in the soil warming plots and 13% deeper in
the air + soil warming plots (P < 0.05).
Total moss percent cover in plots ranged from 1.4 to
77%, and differed among the dominant moss genera
(P = 0.01). The feather moss Pleurozium exhibited the
greatest average percent cover (11.7 ± 2.26%), fol-
lowed by Dicranum (6.48 ± 0.99%), and Sphagnum
(4.28 ± 1.63%). Moss aboveground biomass ranged
from 5 to 150 g m
-2
,andDicranum displayed the
largest mean biomass among dominant mosses (Ta-
ble 3). Sphagnum displayed the greatest range of
biomass between plots, and included both the highest
and lowest values observed. Percent cover and bio-
mass were positively correlated in Sphagnum
(r
2
=0.91), Pleurozium (r
2
=0.64), and Dicranum
(r
2
= 0.43). Although there were species-specific
trends towards increases (Pleurozium) and decreases
Table 1. Allometric Relationships Used to Calculate Moss Biomass (g m
-2
) from Average Number of
Contact Points per Pin Drop in Six 60 X 60 cm Destructive Harvest Plots Adjacent to the Field Warming
Treatments (49 drops per plot using a point frame)
Moss genus Equation coefficients Model strength
Slope Intercept r
2
P
Dicranum 130.0 4.008 0.972 <0.0001
Pleurozium 42.62 -0.738 0.973 <0.0001
Sphagnum 132.6 -3.011 0.905 0.003
All mosses 122.8 -5.172 0.865 <0.0001
1074 Deane-Coe and others
(Sphagnum, Dicranum) in biomass with either ex-
perimental warming treatment, there were no sig-
nificant treatment effects on these parameters.
Moss NPP ranged from 2 to 80 g m
-2
y
-1
, dif-
fered among dominant genera (P < 0.05), and was
significantly lower in 2013 compared to 2012
(P < 0.05). NPP was largest in Dicranum in both
2012 and 2013, and did not differ across soil
warming treatments (Figure 1). Pleurozium NPP
was the smallest in both years (Figure 1), and was
reduced by over 90% in the air warming treatment
in 2012 (P < 0.05). In both years, Sphagnum NPP
was reduced by the air warming treatment (by 80%
in 2012 and 50% in 2013) and increased in the soil
warming treatment (twofold in 2012, threefold in
2013) (P < 0.05). NPP was positively correlated
with percent cover in both 2012 (P < 0.001;
r
2
= 0.16) and 2013 (P < 0.001; r
2
= 0.17) (Fig-
ure 2).
Carbon isotope discrimination differed among the
three genera, with Pleurozium displaying the most
negative d
13
C signatures in both years (P < 0.05;
Figure 3). On average, d
13
C was lowest in mosses
exposed to the air warming treatment, and highest in
the soil warming treatment (Figure 3). There was an
overall significant effect of soil warming on d
13
Cfor
all mosses (P < 0.05), and a trend towards an effect
of air warming (P = 0.06) in 2013. There was a sig-
nificant air warming effect on Sphagnum and Dicra-
num d
13
Cin2012(P < 0.05), and Pleurozium d
13
Cin
2013 (P < 0.05). There was a significant soil warm-
ing effect on Dicranum d
13
Cin2013andPleurozium
d
13
Cin2012(P < 0.05). Sphagnum d
13
Cin2013was
significantly influenced by air warming, soil warm-
ing, and the interaction between them, and was
highest under soil warming and lowest under
air + soil warming (P < 0.05). There was also a sig-
nificant, positive correlation between NPP and d
13
C
in mosses collected both years: d
13
C=
0.64*Log(NPP + 1) - 30.6 (2012) and d
13
C=
0.33*Log(NPP + 1) - 30.1 (2013) (Figure 2). d
13
C
explained 31% of the variability in NPP in 2012
(P < 0.0001) but only 10% in 2013 (P < 0.05).
Nitrogen isotopic signature, d
15
N, differed among
moss genera and was, on average highest in
Sphagnum in both years (Figure 4; P < 0.0001).
Moss d
15
N was not significantly altered by treat-
ments in either year, although in 2013 d
15
N dis-
played higher variability across treatments
compared to 2012. Sphagnum d
15
N, in contrast to
Dicranum and Pleurozium, differed substantially be-
tween the 2 years with values of 2.77 ± 0.34 in
2012 and -3.30 ± 0.26 in 2013.
Percent C in Pleurozium and Sphagnum was sig-
nificantly reduced by the air warming treatment in
Table 2. Mean Air Temperature (C ± SE), Soil Temperatures (C ± SE) Measured at 5 and 10 cm, Mean ( ± SE) 0–20 cm Depth-integrated Soil
Moisture (Volumetric Water Content; VWC), Mean (±SE) Surface Soil Moisture (Gravimetric Water Content; GWC), and Mean Maximum Growing
Season Thaw Depth in Control Plots (Control) Compared to Air Warming (Air), Soil Warming (Soil), and Combined Air and Soil Warming
(Air + Soil) Treatments
Control Air Soil Air + Soil
2012 2013 2012 2013 2012 2013 2012 2013
Air temperature (10 cm above soil) 10.6
ab
± 0.07 12.7
c
± 0.13 10.8
b
± 0.06 13.1
d
± 0.11 10.3
a
± 0.03 12.8
cd
± 0.12 11.0
b
± 0.05 13.2
d
± 0.11
Soil temperature (5-cm depth) 7.50
a
± 0.26 7.51
a
± 0.25 7.34
a
± 0.39 7.19
a
± 0.43 7.36
a
± 0.18 7.23
a
± 0.17 7.25
a
± 0.19 7.19
a
± 0.25
Soil temperature (10-cm depth) 5.29
a
± 0.27 5.24
a
± 0.28 5.15
a
± 0.25 5.01
a
± 0.22 5.54
a
± 0.18 5.34
a
± 0.24 5.39
a
± 0.23 5.12
a
± 0.25
Depth-integrated soil moisture (VWC) 42.5
ab
± 2.40 37.8
a
± 3.40 42.9
ab
± 1.80 38.5
a
± 1.50 51.8
ab
± 2.00 42.5
ab
± 2.90 47.3
b
± 2.50 46.1
ab
± 2.10
Surface soil moisture (GWC) 8.1
ab
± 1.5 6.5
ab
± 0.8 8.5
ab
± 0.2 5.9
a
± 0.5 10.3
b
± 1.2 8.0
ab
± 1.1 8.9
ab
± 0.8 7.6
ab
± 0.7
Thaw depth (cm) 63.0
a
± 0.5 67.0
abc
± 1.7 62.6
a
± 0.8 64.7
ab
± 2.0 72.6
cde
± 2.6 79.1
e
± 2.8 70.4
bcd
± 1.8 75.4
de
± 2.8
Growing season means (for air temperature) were determined by day of year (124–241 in 2012, 152–241 in 2013) and standard errors are based on fence replicates (n = 6). Treatment by year interactions that differ significantly
(P < 0.05) are identified with different superscript letters. Sampling period for all environmental variables was day of year 121–273 except for air temperatures (121–264 in 2012, 154–264 in 2013).
Tundra Moss Productivity Under Global Change 1075
2012 (P < 0.05; Table 3), and percent N was sig-
nificantly increased by the soil warming treatment
(Sphagnum, 2013) and air + soil warming treat-
ment (Pleurozium, 2012) (P < 0.05; Table 3). As a
consequence, C:N was significantly reduced in
Sphagnum in the soil warming treatment (2013,
P < 0.05), and in Pleurozium in the air + soil
warming treatment (2012, P < 0.05).
DISCUSSION
Air warming caused a reduction in NPP in the
feather moss Pleurozium in 2012 and the peat moss
Sphagnum in both 2012 and 2013, in support of our
first hypothesis. Declines were most dramatic in
2012, where NPP in both of these mosses was re-
duced by over 80% on average. Dicranum NPP, on
the other hand, was not influenced by treatments
in either year, but did exhibit NPP rates on average
twice that of Pleurozium and Sphagnum, with the
greatest differences between the genera observed in
2013. Air warming also resulted in a consistent
reduction in d
13
C in all three mosses, and we found
that d
13
C was positively correlated with NPP in
both years, as has been observed in other moss
communities (Rice 2000). In contrast to vascular
plants, where low d
13
C values typically result from
greater growth rates due to high water use effi-
ciency, low d
13
C values in mosses are most com-
monly observed when growth rates are low due to
low tissue water content, when chloroplastic de-
mand and diffusional resistance of CO
2
are both
low (Rice and Giles 1996; Rice 2000). Collectively,
the reduction in NPP and d
13
C in two of the three
dominant mosses at our site points to the possibility
of drier conditions that reduced moss growth as a
result of air warming.
In partial support of our second hypothesis, soil
warming resulted in an increase in NPP in
Sphagnum in both 2012 and 2013, but did not
result in changes in productivity in Pleurozium or
Dicranum. Sphagnum d
13
C was also highest in soil
warming treatments in both years, and together
with higher NPP, suggests that soil warming (and
the changes in soil and permafrost dynamics that
accompany it) could alleviate negative effects of
air warming on productivity. Indeed, Sphagnum
NPP was no different from control in the air +
soil warming treatment, suggesting that increased
growth under warmed soils could offset reduc-
tions occurring as a result of increased air tem-
peratures.
Table 3. Percent C, Percent N, C:N, and Biomass (g m
-2
) for Dicranum, Pleurozium,andSphagnum Following
Four (2012) and Five (2013) Year Exposure to Air and Soil Warming Treatments
Dicranum Pleurozium Sphagnum
2012 2013 2012 2013 2012 2013
%C
Control 45.2 ± 0.20 44.3 ± 0.14 45.3 ± 0.11 44.4 ± 0.21 42.0 ± 0.23 42.7 ± 0.31
Air 44.8 ± 0.30 44.2 ± 0.40 44.9 ± 0.23 44.1 ± 0.34 41.3 ± 0.20 42.4 ± 0.23
Soil 45.2 ± 0.22
44.3 ± 0.21 44.9 ± 0.11
44.3 ± 0.21 41.9 ± 0.22 42.4 ± 0.21
Air + Soil 45.4 ± 0.12 44.0 ± 0.14 44.4 ± 0.22 44.4 ± NA 41.3 ± 0.33 42.3 ± 0.11
%N
Control 0.83 ± 0.04 0.57 ± 0.09 0.98 ± 0.04 0.71 ± 0.05 1.49 ± 0.05 0.91 ± 0.03
Air 0.91 ± 0.06 0.55 ± 0.08 0.93 ± 0.04 0.72 ± 0.06 1.56 ± 0.05 0.77 ± 0.03
Soil 0.90 ± 0.05 0.57 ± 0.03 0.89 ± 0.02 0.81 ± 0.04 1.49 ± 0.06 1.17 ± 0.14
Air + Soil 0.86 ± 0.04 0.47 ± 0.02 1.03 ± 0.04 0.68 ± NA 1.46 ± 0.06 0.98 ± 0.09
C:N
Control 55.5 ± 2.87 85.3 ± 10.7 46.8 ± 1.71 63.6 ± 3.99 28.3 ± 0.93 47.1 ± 1.94
Air 50.3 ± 3.71 85.9 ± 14.3 48.9 ± 2.10 61.5 ± 4.85 26.7 ± 0.88 55.1
± 1.85
Soil 51.4 ± 3.73 79.3 ± 4.74 50.8 ± 1.22 55.4 ± 2.51 28.4 ± 1.15 38.7 ± 4.41
Air + Soil 54.2 ± 2.47 94.0 ± 3.10 44.1 ± 1.94 65.3 ± NA 28.6 ± 0.98 43.7 ± 3.85
Biomass (g m
-2
)
Control 21.4 ± 9.27 23.1 ± 6.11 5.11 ± 2.17 8.52 ± 3.95 14.1 ± 12.3 16.4 ± 15.2
Air 19.4 ± 4.43 12.6 ± 3.26 7.80 ± 2.00
6.93 ± 2.62
8.25 ± 5.29 5.11 ± 3.41
Soil 23.2 ± 8.21 22.0 ± 5.23 5.92 ± 2.10 6.13 ± 2.07 4.61 ± 2.86 5.74 ± 2.85
Air + Soil 18.7 ± 5.28 19.5 ± 9.56 13.0 ± 3.90 9.02 ± 2.90 11.4 ± 9.44 8.30 ± 7.39
Values presented are means ± one standard error. NAs indicate instances where only one sample was available for the treatment 9 genus 9 year combination, thus standard
error could not be calculated. Bold face indicates treatment differences from control where P < 0.05;
P < 0.10.
1076 Deane-Coe and others
Water availability plays a central role in moss
productivity, and changes in soil moisture that ac-
companied warming are likely to have strongly
influenced the productivity and d
13
C of mosses. As
mosses inhabit the region at the soil-atmosphere
interface, their growth is limited by the interactive
effects of water availability at the soil surface and
rates of passive water loss from tissues to the sur-
rounding air. The relationship between warmer
and drier conditions and moss productivity was
most apparent between the sampling years: 2013
was 2–3C warmer than 2012 on average, and total
precipitation was 40% lower in 2013 compared to
2012. These conditions likely caused the low moss
NPP in 2013 compared to 2012, and the suppressed
moss C assimilation apparent in the shallower NPP
versus d
13
C relationship in 2013.
The field warming treatments similarly affected
soil moisture, which is likely to have altered
moss water availability and performance. Soil
warming increased surface moisture by 10–17%,
Figure 1. Mean net primary productivity (g m
-2
y
-1
)
± standard error for Dicranum, Pleurozium, and Sphagnum
in control, air warming (Air), soil warming (Soil), and
combined air and soil warming (Air + Soil) treatments
measured in 2012 and 2013. Mixed model effects: Air
(Pleurozium, 2012), Air and Soil (Sphagnum, 2012 and
2013). Note the difference in y-axis scales in 2012 and
2013.
A
B
Figure 2. A The relationship between percent cover and
net primary productivity (NPP, g m
-2
y
-1
) measured in
2012 (closed symbols and solid line; r
2
= 0.16, P < 0.001)
and 2013 (open symbols and dashed line;r
2
= 0.17,
P < 0.001). B The relationship between NPP (g m
-2
y
-1
)
and d
13
C(&) in all mosses combined in 2012 (closed symbols
and solid line; r
2
= 0.31, P < 0.0001) and 2013 (open symbols
and dashed line; r
2
= 0.10, P < 0.05).
Tundra Moss Productivity Under Global Change 1077
and depth-integrated moisture by 11–12%. This
occurred because soil warming induced permafrost
degradation and surface subsidence, leading to a
13–18% increase in thaw depth and saturated soils.
Under soil warming, mosses were therefore un-
likely limited by water availability, leading to in-
creases in NPP and d
13
C. Air warming, on the other
hand, did not alter soil moisture, but did increase
mean air temperatures above the soil by up to
0.5C and maximum daily temperatures by up to
1.5C, which may have increased potential
evapotranspiration at the soil surface where the
mosses were growing. Mosses were often visibly
desiccated and brittle in the air warming plots,
which, along with reduced NPP and d
13
C, reveal
that moss performance and growth at or above the
soil surface may be adversely affected by increased
air temperatures. As soil moisture at 5 cm depth
was not influenced by air warming, but moss
growth was still sensitive to this treatment, these
data also suggest that moss performance could be-
come decoupled from soil hydrology under in-
creased air temperatures.
Changes in water availability to mosses as a re-
sult of increased air temperatures may have
negatively impacted growth and C assimilation of
Sphagnum and Pleurozium because of their sensi-
tivity to desiccation. Most tundra Sphagnum species
are extremely hydrophilic, existing as dense, moist
hummocks, or mats at or below the soil surface,
Figure 3. Carbon isotopic signatures (d
13
C; &) for Di-
cranum, Pleurozium, and Sphagnum in control, air warm-
ing (Air), soil warming (Soil), and combined air and soil
warming (Air + Soil) treatments measured in 2012 and
2013. Bold horizontal lines in box interiors represent median
values, and upper and lower edges of boxes represent in-
terquartile ranges. Mixed model effects: Soil (all genera
combined, 2012 and 2013), Air (Sphagnum and Dicranum
in 2012, Pleurozium and Sphagnum in 2013), Soil (Dicra-
num and Sphagnum in 2013, Pleurozium in 2012),
Air + Soil (Sphagnum 2013).
Figure 4. Nitrogen isotopic signatures (d
15
N; &) for Di-
cranum, Pleurozium, and Sphagnum in control, air warm-
ing (Air), soil warming (Soil), and combined air and soil
warming (Air + Soil) treatments measured in 2012 and
2013. Bold horizontal lines in box interiors represent median
values, upper and lower edges of boxes represent in-
terquartile ranges, and dots represent outliers. Note the
difference in y-axis scales in 2012 and 2013.
1078 Deane-Coe and others
commonly growing submerged in water. On aver-
age, tundra Sphagnum species display a low degree
of desiccation tolerance, and shoots will cease to
grow under conditions of low water availability
(Schipperges and Rydin 1998; McNeil and
Waddington 2003). Reductions in biomass have
been previously observed in Sphagnum under air
warming conditions in the field (Jonasson and
others 1999; Gunnarsson and others 2004), with
causes attributable to an overall drier growth en-
vironment, revealing the sensitivity of Sphagnum to
desiccation imposed by increased air temperatures.
In contrast to the thick Sphagnum mats, the feather
moss Pleurozium grows in a loose weft above the soil
surface, and although more tolerant of drying and
rewetting than Sphagnum, ceases photosynthetic
activity when dry (Williams and Flanagan 1996).
Feather mosses like Pleurozium rely on capillary
action to move water from lower to upper portions
of the shoot, and if water availability is low at the
soil surface, entire shoots and colonies can desic-
cate rapidly (Skre and others 1983). It is interesting
to note that, in contrast to Sphagnum and Pleu-
rozium (both of which might have been living closer
to their physiological limits under air warming),
Dicranum did not display reduced productivity in
the air warming treatment. This could arise from
differences in temperature tolerance due to plas-
ticity in the genus (Dicranum is diverse with a global
distribution; Bellolio-Trucco and Ireland 1990;
Hedena
¨
s and Bisang 2004), or increased tolerance
for fluctuations in water availability due to its
dense, colonial growth form.
In addition to genus-specific productivity re-
sponses, we also observed differences in d
15
N across
species and some changes in C:N in response to
warming treatments. Moss d
15
N depended pri-
marily on genus, where it was highest in Sphagnum,
and sampling year, where reductions of up to 5&
were observed in Sphagnum between 2012 and
2013. This dramatic difference in d
15
N observed in
Sphagnum may be related to altered N supply
pathways that accompany environmental changes
in hydrology (Handley and others 1999). Sphagnum
tissue d
15
N in 2012, the cooler and wetter year, was
consistent with substrate (organic and mineral soil)
d
15
N signatures (Houle and others 2006; Pries and
others 2012), whereas d
15
N signatures from 2013,
the warmer and drier year, were consistent with
what has been recorded in mosses receiving nu-
trients exclusively from atmospheric deposition
(Bragazza and others 2005). This is potentially
evidence for a shift from a terrestrial to an atmo-
spheric source of N in Sphagnum when water
availability at the soil surface is low and mosses
must rely more heavily on precipitation for hy-
dration. As this 5& change in d
15
N was not ob-
served in the other genera at our site that do not
have shoots that extend deep into the soil profile,
these results also reveal that changes in N avail-
ability that accompany changes in local hydrology
could have a disproportionate effect on mosses like
Sphagnum with significant belowground biomass. It
is also possible that d
15
N shifts in Sphagnum were
due to changing soil sources due to microbial pro-
cessing or other mechanisms that exhibited inter-
annual variability. Differences between years and
among mosses were far greater than any treatment
effects, suggesting tundra moss d
15
N is largely de-
termined by inter-annual environmental changes
that result in differences in N source composition,
or the physiological ecology and N metabolism of
individual taxa.
Macronutrient tissue composition among tundra
mosses reflected changes in productivity and N
availability that accompanied warming. C:N ex-
hibited modest declines in both Pleurozium (2012)
as a result of air + soil warming, and Sphagnum
(2013) as a result of soil warming. For both of these
mosses, declines in C:N resulted from a combina-
tion of increased %N in the soil warming treatment
and reduced %C in the air warming treatments.
This suggests that N availability to mosses may be
higher in warmer soils, as appears to be the case for
vascular plants in regions undergoing permafrost
thaw (Schuur and others 2007; Natali and others
2012). Yet, air warming that reduces overall NPP
appears to manifest as reductions in tissue %C in
some taxa. For mosses, ecosystem warming may
therefore increase N availability under certain
conditions, but also may create a less favorable
moisture environment for growth and C assimila-
tion.
Experimental warming at our site forecasts po-
tential changes in the tundra moss community in a
future climate. In particular, these results lend
clarity to a previously incomplete picture for
Sphagnum in tundra ecosystems. Although most
earlier work has shown declines in Sphagnum
abundance and cover in response to air tem-
perature manipulation (Jonasson and others 1999;
Gunnarsson and others 2004; Walker and others
2006; Lang and others 2012), we reveal how air
warming and soil warming can interact to create
positive conditions for Sphagnum growth. In tundra
ecosystems, soil warming can lead to positive
feedbacks involving permafrost thaw and ground
subsidence (Nelson and others 2001; Schuur and
others 2009) therefore it is possible that Sphagnum
may have an advantage in warming temperatures
Tundra Moss Productivity Under Global Change 1079
based on its tolerance of saturation. This conclusion
is supported by evidence from Northern peatlands
suggesting Sphagnum fuscum will benefit from
warming scenarios that do not reduce water
availability (Dorrepaal and others 2004). Pleu-
rozium, on the other hand, displayed high overall
sensitivity temperature increases, particularly air
warming, suggesting a potential reduction in
dominance in the long-term. Although Dicranum
displayed reduced NPP and treatment effects on
d
13
C in the warmer and drier sampling year (2013),
in general Dicranum was the one genus that did not
appear to be as responsive to warming, and there-
fore may remain a feature in tundra moss com-
munities in the future.
The moss responses observed here also have the
potential to influence C and N cycling in the tun-
dra. Because of their extensive groundcover and
activity beyond the typical constraints of the vas-
cular plant growing season, mosses can contribute
substantially to carbon inputs in northern ecosys-
tems. As Pleurozium accounted for the largest per-
cent cover of all three genera at our site, reductions
in Pleurozium NPP may influence ecosystem C in-
puts during times of year when vascular plants are
less active. Pleurozium was also the most sensitive
genus to annual warming overall, suggesting the
possibility of changes in productivity on relatively
rapid time scales. Through associations with N
2
-
fixing cyanobacteria, Pleurozium also accounts for
substantial N inputs to Northern latitude systems
(Solheim and others 1996; DeLuca and others
2002; DeLuca and others 2007; Markham 2009).
Pleurozium productivity declines accompanying in-
creased temperatures which therefore could result
in reductions in ecosystem N inputs from N fixa-
tion. In spite of the potentially large ramifications
of Pleurozium declines in this ecosystem, it is im-
portant to note that the genus with the largest
biomass and greatest overall productivity at our
site, Dicranum, and the genus comprising the ma-
jority of biomass in Northern latitude peatlands,
Sphagnum, did not display the same responses, and
may buffer altered C inputs from Pleurozium decli-
nes that accompany soil warming.
Because of their unique physiology and slow
growth rates, detection of moss responses to envi-
ronmental change in the field is often challenging.
Our results reveal that although treatment level
changes may not have been apparent from mea-
surements of biomass on this timescale, tissue ele-
mental analyses, and moss-specific measures of
productivity do suggest that mosses are sensitive to
warming. The fact that we could capture moss NPP
and d
13
C responses in response to ecosystem
warming, and observe pronounced inter-annual
differences, makes the present results especially
striking from a plant community standpoint. Ex-
amining vegetation responses across 2 years with
strikingly different abiotic conditions also revealed
the interactive effects of temperature manipulation
and local hydrology, and future work examining
how projected changes in precipitation interact
with other climate factors would strengthen our
knowledge of northern latitude response to global
change.
As a consequence of increased temperatures,
tundra plant communities are undergoing dramatic
shifts in diversity, species composition, biomass,
nutrient status, and NPP (Arft and others 1999;
Walker and others 2006;Nataliandothers2012). To
understand how warming will impact future eco-
logical relationships and ecosystem processes in the
tundra, a holistic view combining information on
non-vascular plant responses with the wealth of
research on vascular plant responses is essential. As
we have shown here, some responses may differ
between non-vascular and vascular plants, that is,
responses to altered hydrology that accompany
warming and permafrost thaw, but others may be
similar, that is, increased plant-available N. From a
moss community standpoint, our results suggest
that annual temperature increases may result in a
shift away from a feather moss-dominated com-
munity towards a peat moss-dominated community,
a result with consequences for species composition
and diversity, ecosystem N inputs, and C balance in
the tundra. Moreover, these conclusions could not
have been reached without the year-round warm-
ing experiment employed here: changing air tem-
peratures are also likely to manifest as changing soil
temperatures, soil moisture, and permafrost dy-
namics (Osterkamp and Romanovsky 1999), and
this work presents strong evidence that air warming
and soil warming treatments in combination can
offer a more complete picture of tundra plant com-
munities under global change.
ACKNOWLEDGMENTS
This material is based upon work supported by the
U.S. Department of Energy Office of Science, Office
of Biological and Environmental Sciences Division
Terrestrial Ecosystem Sciences program under
Award Number DE-SC0006982. Support was also
provided by NSF LTER #1026415 and NSF ARC
#1203777 as well as the National Parks Vital Signs
Inventory and Monitoring Program. We also wish to
thank John Krapek, Elizabeth Webb, J. Simon
McClung, and Catherine Johnston for assistance
1080 Deane-Coe and others
with field sampling and site maintenance, and
Elaine Pegoraro for compiling moss point-framing
data for biomass and NPP analyses. Sarah Stehn was
invaluable in field identification of mosses at our
site.
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