Polar Biol (2015) 38:967–974
DOI 10.1007/s00300-015-1655-6
ORIGINAL PAPER
Abrupt changes in invertebrate herbivory on woody plants
at the forest–tundra ecotone
Mikhail V. Kozlov • Boris Yu. Filippov
Natalia A. Zubrij • Vitali Zverev
•
Received: 20 September 2014 / Revised: 26 January 2015 / Accepted: 27 January 2015 / Published online: 4 February 2015
! Springer-Verlag Berlin Heidelberg 2015
Abstract Invertebrate herbivores, insects in particular,
play important functional roles in terrestrial ecosystems. At
background (non-outbreak) densities, they consume
5–15 % of woody plant foliage in forests across the planet.
At the same time, almost nothing is known about the levels
of insect herbivory in Arctic tundra. To test the hypothesis
that the amount of plant biomass lost to insects in tundra is
substantially less than in subarctic forests, in 2013, we
explored foliar herbivory in woody plants at three sites in
the Arctic tundra and four sites in the subarctic forests of
European Russia. A vast majority of foliar damage was
imposed by externally feeding defoliators. In forests,
defoliators damaged three times more leaves and consumed
eight times more leaf area than in the tundra. No miners
were found in the tundra, and gallers affected five times
less leaf area in the tundra compared with forests. An
abrupt decrease in loss of woody plant foliage to insects
between subarctic forests and tundra (from 4.34 to 0.56 %)
supports the existence of a latitudinal gradient in herbivory
in terrestrial ecosystems. More studies are needed to predict how tundra plants, which have been historically
exposed to low levels of insect herbivory, will cope with
the increased levels of damage that are expected to occur
M. V. Kozlov (&) ! V. Zverev
Section of Ecology, University of Turku, 20014 Turku, Finland
e-mail: [email protected]
B. Yu. Filippov
Department of Zoology and Ecology, Northern (Arctic) Federal
University, Severnaya Dvina Emb. 17, 163000 Arkhangelsk,
Russia
N. A. Zubrij
Institute of Ecological Problems of the North, Ural Branch of the
Russian Academy of Sciences, Severnaya Dvina Emb. 23,
163000 Arkhangelsk, Russia
due to climate-driven range expansion and increased
abundances of plant-feeding insects.
Keywords Background herbivory ! Climatic changes !
Defoliators ! Gallers ! Miners ! Northern Europe
Introduction
Exploration of species-poor and fragile Arctic ecosystems
is crucial for understanding the general principles of ecosystem functioning (Post et al. 2009; Wookey et al. 2009;
Link et al. 2013). These studies have recently become
particularly important because climate change appears
disproportionately rapid towards the poles (Walther et al.
2002; Doney et al. 2012), and we are in serious danger of
losing knowledge of the present state of biotic interactions
in the Arctic. On the other hand, ongoing climatic change
motivates the need to rapidly assess the consequences of
the warming process on the functioning of ecosystems at
polar latitudes (Link et al. 2013). Rapid assessment may be
critical for processes mediated by arthropods, a group that
is expected to exhibit a particularly strong response to
climatic changes in the high Arctic (Hodkinson and Bird
1998; Strathdee and Bale 1998).
Insect herbivores play important functional roles in
terrestrial ecosystems, from direct effects on plant growth,
survival and reproduction to indirect regulation of evapotranspiration and nutrient cycling processes (Mattson and
Addy 1975; Seastedt and Crossley 1984; Hunter et al.
2012). At background (non-outbreak) densities, insect
herbivores consume 5–15 % of woody plant foliage in
forests across the planet (Coley and Aide 1991; Coley and
Barone 1996). At the same time, almost nothing is known
about the levels of plant damage by insects in tundra. A
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vast majority of studies addressing herbivory in the Arctic
(e.g. Olofsson et al. 2009; Wookey et al. 2009; Legagneux
et al. 2012; Stien et al. 2012) focus on vertebrate herbivores, implicitly assuming a negligible role of insect herbivory in high-latitude ecosystems. Moreover, researchers
exploring plant-feeding insects in Arctic ecosystems (e.g.
MacLean and Jensen 1985; Kukal and Dawson 1989; Roininen et al. 2002; Lundbye et al. 2012; Roslin et al. 2013)
usually do not collect information on the level of plant
damage by insect herbivores. We are aware of only two
quantitative studies of leaf area lost by woody plants from
insect herbivory in the tundra biome (Olofsson et al. 2007;
Torp et al. 2010), and these data originated from the relatively southern shrubby tundra of Fennoscandia.
This shortage of information is especially critical
because of the current debate on the existence of latitudinal
patterns in insect herbivory. A recent meta-analysis (Moles
et al. 2011a) did not find the support for the hypothesis
(Coley and Barone 1996; Grime 2001) that herbivory
decreases with latitude (or the associated increase in
environmental harshness with latitude). However, Kozlov
et al. (2013) argued that conclusions by Moles et al.
(2011a) may be valid only for regions with temperate climate and relatively smooth environmental gradients,
between the 30th and 50th parallels in both hemispheres,
whereas at high latitudes, herbivory decreases substantially
towards the poles. Latitudinal changes in herbivory may be
especially pronounced within the transition zone between
forest and tundra, which is one of the world’s most
prominent ecotones and is associated with a strong climatic
gradient and an abrupt change in the structure and composition of plant communities (Sveinbjörnsson et al. 2002).
Along with climate, the differences in herbivory between
these biomes may be caused by latitudinal changes in leaf
mechanical properties (Onoda et al. 2011), in plant
defensive chemistry (Moles et al. 2011a, b) and in predator
pressure (Björkman et al. 2011).
In the present study, we explored foliar herbivory in
common species of woody plants at several sites in Arctic
tundra, forest–tundra and north taiga forests of European
Russia. We aimed at quantifying community-wide losses in
foliar biomass of woody plants to insects from three major
feeding guilds (defoliators, miners and gallers) to test the
hypothesis that invertebrate herbivory in tundra is substantially lower than in subarctic forests.
Polar Biol (2015) 38:967–974
Fig. 1 Study area and sampling sites
Materials and methods
(Fig. 1; Table 1). All sites were selected in natural habitats
with negligible levels of human-induced disturbance. The
selection of sampling localities and of the time of sampling
was driven by factors other than the goals of the present
study. In particular, all tundra sites were visited during the
expedition of research vessel ‘Professor Molchanov’;
therefore, our selection was presumed to be random in
relation to the existing level of herbivory which is variable
in both space and time.
All tundra sites were located relatively close to the
seashore. The maximum height of woody plants within
20–50 km from the sampling sites in the tundra was less
than 1 m (Walker et al. 2005, and pers. obs.). The sampled
communities on Kolguev Island and on Belyi Nos Peninsula were classified as low-shrub tundra and on Vaygach
Island as graminoid prostrate dwarf-shrub tundra (after
Walker et al. 2005). In surroundings of Murmansk, samples
were collected in sparse low-stature woodland (5–7 m in
height) formed by mountain birch (Betula pubescens ssp.
czerepanovii (Orlova) Hämet-Ahti). This locality lies
beyond the northern distribution limit of Norway spruce
(Picea abies (L.) Karst.) and forms a transition from north
taiga forest to low-shrub tundra. In Naryan-Mar, samples
were collected from a patch of sparse Norway spruce forest
(12–15 m) within the forest–tundra zone. Study sites near
Lovozero and Arkhangelsk were selected in dense north
taiga forests formed by Norway spruce (14–18 m), birches
(mountain birch in Lovozero and white birch, Betula
pendula Roth in Arkhangelsk) and European aspen (Populus tremula L.).
The summer of 2013 was significantly warmer relative
to long-term records (Table 1). However, the climatic
gradient between tundra and forest sites was not affected,
as can be concluded from significant correlations between
long-term averages and actual temperatures of July across
our study sites (r = 0.92, n = 7, P = 0.0038).
Study sites
Sampling and processing
Leaves of woody plants were collected in 2013 from three
localities in tundra and four localities in forested habitats
In forests, we selected 3–6 species of woody plants that
were most common at our study sites (except for conifers),
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Polar Biol (2015) 38:967–974
969
Table 1 Characteristics of study sites
Locality
Latitude, N
Longitude, E
Altitude, m a.s.l.
Temperature of July, "C
Long-term average
2013
Vegetation zone and
community type
Sampling date
Vaygach Island
70"250 1600
59"030 3400
7
5.0
8.9
Low-shrub tundra
15–20 August 2013
Belyi Nos Peninsula
69"360 1400
60"120 4100
5
7.3
11.8
Low-shrub tundra
6 July 2013
Kolguev Island
68"470 0600
49"190 4600
7
7.5
12.5
Dwarf-shrub tundra
4 July 2013
00
18 August 2013
0
00
0
Murmansk
68"53 59
33"40 11
195
12.6
14.8
Forest–tundra
Naryan-Mar
67"380 1200
53"030 3700
10
13.3
17.5
Forest–tundra
11 July 2013
Lovozero
67"530 1400
34"250 1700
305
13.6
14.4
North taiga forest
15 August 2013
Arkhangelsk
64"250 4900
40"580 2700
20
16.3
16.6
North taiga forest
28 September 2013
while in tundra, we sampled all available woody species.
To avoid a bias, plant species to be sampled in forested
habitats were selected before visiting our sites, i.e. without
a knowledge on their current levels of damage by insects.
This protocol allowed for comparison of community-wide
levels of herbivory between two biomes, forest and tundra,
on the basis of site-specific values. We collected one
branch (with 100–200 leaves) from each of 2–5 individuals
(depending on plant abundance and the available time for
sampling) of each species (for sample sizes, consult
Table 2). Plant individuals were selected by pointing at
them from the distance of 10–15 m, from which the level
of herbivory cannot be evaluated; this protocol minimized
the possibility of confirmation bias, i.e. the tendency of
humans to seek out evidence and interpret it in a manner
that confirms their existing ideas and hypotheses (Wilgenburg and Elgar 2013). For both Vaccinium vitis-idaea L.
and Salix rotundifolia Trautv., we chose individual stems
that had 10–40 leaves and aggregated several stems
growing next to each other. All leaves from these branches/
stems (including petioles of completely consumed leaves)
were collected and preserved between the sheets of paper
as ordinary herbarium specimens.
Following widely used methodology (Southwood et al.
1982; Fox and Morrow 1983; Alliende 1989), each leaf
was attributed to one of the following damage classes
according to the proportion of the leaf area that was consumed or damaged (galled, mined or skeletonized): intact
leaves, 0.01–1, 1.1–5, 6–25, 26–50, 51–75 and 76–100 %.
The numbers of leaves in each damage class were recorded
separately for each feeding guild. All samples were processed by the same person (MVK).
number of leaves in the sample (including undamaged
leaves). Then the number of leaves in each damage class
was multiplied by the median value of the damaged leaf
area (i.e. 0.5 % for the damage class 0.01–1 %), and the
obtained values were summed for all damage classes
within a sample separately for each feeding guild. The
second response variable, average proportion of leaf area
lost to (or damaged by) insects from each of these feeding
guilds, was calculated by dividing the obtained values by
the total number of leaves in the sample (including
undamaged leaves). For defoliators, we also calculated the
third response variable, proportion of leaf area lost from
the damaged leaf, by dividing the obtained value by the
number of damaged leaves.
The proportion of leaves damaged by external defoliators
and the leaf area consumed by these insects (both total loss
and loss per damaged leaf) were log-transformed prior to the
analysis to meet the normality assumption. Because each
site was sampled only once, it was impossible to include the
sampling period (mid- or late summer/autumn) and the
study site in the same statistical model. Therefore, we used
two different models of ANOVA (SAS GLM procedure,
SAS Institute 2009) to test the hypotheses that (1) foliar
damage does not differ between two sampling periods and
(2) foliar damage differs between tundra and forest biomes.
Distributions of data on foliar damage by miners and gallers
were greatly skewed (due to multiple zero values) and were
therefore analysed by a nonparametric Kruskal–Wallis test.
Additionally, for defoliators, we correlated response variables to mean temperatures of July, which were previously
identified as the best predictor of plant losses to defoliators,
leafminers and sap-feeders in north taiga forests (Kozlov
2008; Kozlov et al. 2013, 2015).
Data analysis
The first response variable, the proportion of leaves damaged by each of three feeding guilds (defoliators, miners,
gallers), was calculated by dividing the number of leaves
damaged by insects from the respective guild by the total
Results
The vast majority of damage recorded on leaves of woody
plants was imposed by externally feeding defoliators. Only
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970
Polar Biol (2015) 38:967–974
Table 2 Levels of foliar damage of woody plants by insect herbivores
Localitya
Plant species
Sample size
(numbers of plants/
leaves)
Foliar damage (%), mean ± SEb
Defoliators
DL
Vaygach
Island
1.41 ± 0.66
0
0
0
0
0.67 ± 0.29
0
0
0
0
Salix reticulata L.
3/414
4.6 ± 1.9
0.81 ± 0.41
0
0
1.0 ± 0.6
0.14 ± 0.10
Salix rotundifolia Trautv.
3/556
7.7 ± 0.9
0.30 ± 0.01
0
0
0.6 ± 0.5
0.09 ± 0.07
14.3
0.80
0
0
0.4
0.6
Salix lanata L.
2/222
40.2 ± 28.6
1.69 ± 0.70
0
0
0
0
Salix lapponum L.
4/516
5.0 ± 4.4
0.19 ± 0.11
0
0
0
0
Salix myrtilloides L.
2/262
4.0 ± 0.9
0.29 ± 0.08
0
0
0
0
Salix phylicifolia L.
3/339
8.5 ± 0.7
0.40 ± 0.25
0
0
0
0
14.4
0.64
0
0
0
0
Salix arctica Pall.
1/167
1.2
0.04
0
0
0
0
Salix lanata L.
4/550
2.7 ± 0.8
0.01 ± 0.00
0
0
0
0
Salix myrtilloides L.
4/551
6.3 ± 3.0
0.95 ± 0.57
0
0
0.2 ± 0.2
0.01 ± 0.01
3.4
0.33
0
0
0.07
0.003
11.33 ± 0.56
0
0
0
0
Alnus viridis ssp. fruticosa
(Ruprecht) Nyman
2/200
69.7 ± 11.7
Betula nana L.
2/200
3.5 ± 1.5
0.20 ± 0.16
0
0
0
0
Betula pubescens Ehrh.
2/200
27.5 ± 5.5
0.89 ± 0.42
0
0
0
0
Salix lanata L.
2/200
82.5 ± 15.5
9.80 ± 5.27
0
0
26.6 ± 26.6
1.22 ± 1.22
Salix phylicifolia L.
2/200
73.5 ± 10.5
11.26 ± 4.60
0
0
0
0
Vaccinium uliginosum L.
2/200
0
0
0
0
0
0
42.8
3.69
0
0
4.4
0.2
Betula nana L.
5/500
2.6 ± 1.9
0.84 ± 0.58
0
0
0
0
Betula pubescens ssp.
czerepanovii (Orlova)
Hämet-Ahti
5/505
58.6 ± 7.1
4.13 ± 1.75
0.8 ± 0.5
0.05 ± 0.03
0
0
Salix phylicifolia L.
5/500
26.2 ± 7.5
2.89 ± 0.86
0
0
0
0
Vaccinium myrtillus L.
5/500
3.1 ± 0.8
0.68 ± 0.42
0
0
0
0
22.6
2.14
0.2
0.01
0
0
Betula nana L.
3/300
11.3 ± 4.9
2.81 ± 1.85
0
0
0
0
Betula pubescens ssp.
czerepanovii (Orlova)
Hämet-Ahti
5/499
42.9 ± 9.2
3.35 ± 1.53
1.2 ± 1.0
0.06 ± 0.05
0
0
Salix phylicifolia L.
5/500
77.8 ± 4.3
19.01 ± 3.08
0
0
0
0
Vaccinium myrtillus L.
5/500
22.2 ± 13.1
10.77 ± 7.68
0
0
0
0
Vaccinium uliginosum L.
5/500
22.4 ± 9.2
8.61 ± 5.95
0
0
0
0
Vaccinium vitis-idaea L.
4/367
2.4 ± 0.7
0.39 ± 0.21
0
0
0
0
29.8
7.49
0.2
0.01
0
0
Betula pendula Roth
3/394
71.6 ± 12.3
3.69 ± 1.54
1.2 ± 0.4
0.01 ± 0.01
17.1 ± 7.6
0.49 ± 0.30
Populus tremula L.
3/334
47.0 ± 15.2
1.03 ± 0.53
0
0
17.5 ± 4.7
0.18 ± 0.09
Vaccinium myrtillus L.
3/327
9.1 ± 2.3
0.34 ± 0.10
0
0
0
0
42.6
1.69
0.4
0.003
11.5
0.22
Mean values
a
LA
35.5 ± 10.0
Mean values
Arkhangelsk
DL
9.4 ± 3.0
Mean values
Lovozero
LA
3/372
Mean values
Murmansk
DL
3/388
Mean values
Naryan-Mar
LA
Salix myrtilloides L.
Mean values
Belyi Nos
Peninsula
Gallers
Salix lanata L.
Mean values
Kolguev
Island
Miners
For characteristics of localities, consult Table 1
b
Measures of foliar damage: DL, proportion of leaves damaged by insects from the respective feeding guild; LA, average proportion of leaf area
lost to (or damaged by) insects from the respective feeding guild. Standard errors (SE) reflect variation among plant individuals
15 of 11263 examined leaves were mined by moth larvae
(from families Stigmellidae and Gracillariidae), and only
186 leaves bore galls formed by insects or mites.
123
Neither proportion of leaves damaged by external defoliators (mean ± SE based on site-specific values: mid-summer,
23.8 ± 8.5 %; late summer/autumn: 26.7 ± 6.0 %;
Polar Biol (2015) 38:967–974
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Table 3 Sources of variation in characteristics of plant damage by defoliating insects (ANOVA, type III sum of squares). For definition of
response variables, consult text
Source
df
Proportion of damaged
leaves
Mean square
F
P
Proportion of leaf area lost from
the damaged leaf
Proportion of leaf area lost
to defoliating insects
Mean square
P
Mean square
F
F
P
Biome (tundra vs. forest)
1
6.62
4.93
0.04
2.21
6.36
0.02
12.35
7.54
0.01
Site (Biome)
5
0.74
0.55
0.74
1.05
3.01
0.03
1.09
0.66
0.65
23
1.34
Error
F1,28 = 0.91, P = 0.35) nor the total loss of leaf area caused
by these insects (mid-summer, 2.80 ± 1.27 %; late summer/
autumn: 3.51 ± 1.20 %; F1,28 = 1.81, P = 0.91) differed
between the two sampling periods. This conclusion was valid
also for miners (v2 = 2.49, df = 1, P = 0.11) and gallers
(v2 = 0.51, df = 1, P = 0.58). Therefore, samples collected
in mid-summer were combined with samples collected in late
summer or autumn for the analysis of differences in herbivory
between forest and tundra biomes.
Plant species collected from the same site generally
differed in the level of damage by defoliators at forest sites
but not at tundra sites (Table 2). Leaf damage by defoliators at forest sites significantly exceeded the damage at
tundra sites (Table 3). The proportion of leaf damage and
the total loss of leaf area were three times and eight times
higher, respectively, in the forest than in the tundra
(Fig. 2). Consistently, the average proportion of leaf area
lost to defoliators from the damaged leaf in forests
(11.64 ± 3.74 %) was twice as high as in tundra
(6.90 ± 1.58 %). The proportion of leaves damaged by
defoliators significantly (r = 0.78, n = 7 sites, P = 0.04)
increased with long-term mean temperature of July, and
average proportion of leaf area lost to these insects also
tended to increase with temperature (r = 0.71, n = 7,
P = 0.07). Although no miners were found in tundra sites
and gallers affected five times less leaf area in tundra than
in forests (Fig. 2), the difference between biomes in plant
damage by these two feeding guilds did not reach the level
of statistical significance (miners: v2 = 2.19, df = 1,
P = 0.14; gallers: v2 = 0.06, df = 1, P = 0.80).
Willows (Salix spp.) were the only group of woody
plants sampled in both forest and tundra biomes (although
the species composition of willows differed between forests and tundra: Table 2). Within willows, both the magnitude and statistical significance of the differences
between the biomes in the amount of chewing herbivory
were higher than in the community-wide comparisons
(average proportion of damaged leaves, forest: 60.7 ±
17.2 %, tundra: 9.5 ± 3.2 %, F1,9 = 30.2, P = 0.0004;
average proportion of leaf area lost to insects, forest:
10.81 ± 4.66 %, tundra: 0.54 ± 0.14 %, F1,9 = 74.5, P \
0.0001). The damage of two willow species that were
0.35
1.64
sampled in both biomes (S. lanata and S. phylicifolia) was
higher in forest sites than in tundra sites (Table 2), and the
average proportion of leaf area lost by these two willow
species from the damaged leaf in forests (14.98 ± 3.12 %)
was nearly five times as high as in tundra (3.29 ± 1.98 %;
F1,6 = 12.8, P = 0.01).
Discussion
Our study demonstrated that insect herbivores in tundra
ecosystems consumed only 0.56 % of the foliar biomass of
woody plants, which was much lower than in forest ecosystems close to the northern tree limit (4.34 %). This
result is in line with the conclusion by McNaughton et al.
(1989) that highly productive ecosystems sustain a larger
level of herbivory per unit of primary production than less
productive ecosystems. Furthermore, the detected differences between losses of woody plant foliage to insects in
northern forests and tundra habitats, that were separated by
(on average) 2.5" latitude (Table 1), were of the same
magnitude as the differences between northern and southern forests in Fennoscandia, separated by 10" latitude
(Kozlov 2008 and unpublished data). This result supports
the hypothesis (Kozlov et al. 2013) that gradients in
background herbivory are stronger at high latitudes than in
regions with temperate climates, in particular because the
slope of the temperature gradient increases towards the
poles (Terborgh 1973). This discovery emphasizes the need
for further study of both the levels of the background
herbivory and associated consequences for the fitness of
plants in the Arctic. In particular, systematic measurements
of invertebrate herbivory north of the Arctic circle, from
north taiga forests to polar deserts, are of special importance for revealing the general pattern in the relationship
between latitude, woody plant diversity, plant life form and
losses of foliage to insects.
The absolute levels of foliar herbivory in our tundra sites
are similar to earlier data from tundra sites in Iceland,
where defoliating insects damaged 1.0–13.1 % (mean
5.2 %) of leaves in Salix herbacea L. and 1.0–26.2 %
(mean 6.4 %) of leaves in Vaccinium uliginosum L.
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Damaged leaves (%)
40
Forest
Tundra
(a)
30
20
*
10
0
Chewers
Miners
Gallers
Consumed / damaged leaf area (%)
(b)
5
4
3
2
1
0
*
Chewers
Miners
Gallers
Fig. 2 Proportion of damaged leaves (a) and proportion of leaf area
lost to (or damaged by) insects (b) from three feeding guilds in
subarctic forests (n = 4) and tundra sites (n = 3). Bars indicate SE
based on site-specific means; an asterisk indicates significant
difference between biomes (for statistics, consult Table 3 and text)
(Kozlov et al. 2009). In contrast, all published data from
tundras of northern Fennoscandia (44.3 % of leaves damaged in S. lanata: Olofsson and Strengbom 2000; 2.56 % of
leaf area consumed in S. glauca: Olofsson et al. 2007; and
10.0 % of leaf area consumed in B. nana: Torp et al. 2010)
reported foliar damage levels in the same range as we
found in the northern forests. However, Fennoscandia is a
region that does not include ‘true’ tundra according to the
classification by Walker et al. (2005),
Low levels of foliar herbivory in the tundra are consistent with the low diversity and relatively low abundances
of herbivorous insects in this biome. According to Danks
(1986), the ratio between the number of insect species
feeding on plants and the number of plant species
decreased from 3 to 4 in temperate and northern forests to
0.1–1.2 in tundra. However, the situation is likely to
change in the near future, as many insect species have been
reported to expand their distribution towards the North
(Parmesan et al. 1999; Warren et al. 2001). Furthermore,
the abundances of many herbivorous moths have increased
123
in one of the subarctic forest sites during the last 30 years
(Hunter et al. 2014), and herbivory on birches at the
northern tree limit during the years with warmer-thanaverage summer temperatures has increased to the level
typical for habitats located 500–800 km to the south
(Kozlov et al. 2013). Thus, climate-driven range expansion
and increased abundances of species with generally more
southern distributions may add to the species pool and
abundance of herbivores in tundra ecosystems, thereby
increasing herbivory pressure on arctic plants, because
woody plants are likely to move northwards much slower
than insects.
The consequences of increased insect herbivory for
Arctic ecosystems are difficult to predict due to acute
shortage of information on insect–plant relationships in the
tundra. Although this knowledge gap was identified long
ago (Haukioja 1981; Danks 1986), little progress has been
made in this area of research (but see Lundbye et al. 2012).
In northern taiga forests, a relatively small increase in
background herbivory due to climate warming can potentially cause severe negative impacts on tree growth (Zvereva
et al. 2012). However, the question arises of whether these
predictions can be similarly applied to the tundra biome.
Moles et al. (2011a) surprisingly found that chemical
defences in plants from higher latitudes were significantly
higher than in plants from lower latitudes. Our data indirectly support this conclusion because in tundra, defoliating
insects consumed a significantly smaller part of any damaged leaf than in forests, which can indicate that they are
changing their feeding sites more frequently than in forests.
Restriction of the comparison to two willow species that
were sampled in both biomes further confirmed this conclusion. Changing of feeding sites allows herbivores to
avoid local defensive responses of their host plants
(Edwards and Wratten 1983; Bergelson et al. 1986; Zvereva and Kozlov 2000), and changing the feeding site at
lower levels of leaf damage can indicate that woody plants
in tundra have a stronger decrease in leaf palatability in
response to damage than do woody plants in forests. If our
interpretation is correct, then plant defence may hamper the
use of tundra plants by more southern herbivores, which
may need some time to adapt to the high level of plant
defences. On the other hand, the predicted increase in
herbivory is likely to be valid for shrubs that have recently
invaded the tundra (Sturm et al. 2001; Tape et al. 2006)
because most of these shrubs are growing in subarctic
forests and therefore are familiar to more southern herbivores. In this case, the increase in insect herbivory, along
with mammalian herbivory (Olofsson et al. 2009), has a
potential to slow down the rate of shrub encroachment in
tundra ecosystems.
To conclude, our findings on the sharp decrease in foliar
damage of woody plants by insects between subarctic
Polar Biol (2015) 38:967–974
forests and arctic tundra support the existence of a latitudinal gradient in herbivory in terrestrial ecosystems. More
studies are needed to predict how tundra plants, which have
been historically exposed to low levels of folivory, will
cope with increased levels of damage resulting from climate-driven range expansion and the increased abundance
of insect herbivores.
Acknowledgments We thank E. Yu. Churakova for help in identifying plants and E. L. Zvereva and three anonymous reviewers for
commenting on an earlier draft of the manuscript. Research visits by
MVK and VZ to the study sites were supported by INTERACT (Grant
agreement no. 262693 under the EC 7th Framework Programme) and
by the Otto Malḿ’s Foundation. Fieldwork by BYF and NAZ was
supported by the Ministry of Education and Science of the Russian
Federation (Grant 5.4615.2011) and the Russian Foundation for the
Basic Research (11-04-98814-north).
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