Overview Articles
The Role of Vertebrate Herbivores
in Regulating Shrub Expansion
in the Arctic: A Synthesis
KATIE S. CHRISTIE, JOHN P. BRYANT, LAURA GOUGH, VIRVE T. RAVOLAINEN, ROGER W. RUESS,
AND KEN D. TAPE
Shrubs are expanding in Arctic ecosystems, and herbivores may be influencing this expansion by reducing the growth of preferred forage species.
We synthesized new and published data to evaluate the relative influence of climate and vertebrate herbivory on different shrub species and
groups. Variation in chemistry across shrub species translates to a strong preference for (and damage to) palatable deciduous shrubs compared
with evergreen shrubs when herbivores are at low densities, but differences in palatability matter less when herbivores are at high densities and/
or food limited. Long-term observational and experimental studies indicate that herbivores moderate the expansion of fast-growing deciduous
shrubs such as willows (Salix spp.), although more research is needed to address the relative strength of climate and herbivory at larger scales.
Well-defended shrubs such as Siberian alder (Alnus viridis) and resinous dwarf birch (Betula nana exilis) are generally not preferred by
herbivores and may therefore outpace the expansion of more palatable species.
Keywords: shrub expansion, climate change, Arctic, secondary compounds, wildlife
C
limate warming in the Arctic has caused the rapid expansion of woody shrubs over the past half-century
(Tape et al. 2006, Elmendorf et al. 2012), and herbivory
has been recognized as a key factor influencing this expansion (Myers-Smith et al. 2011). Vertebrate herbivores are
capable of strongly regulating the rates of vegetation change
in tundra ecosystems, and the number of studies on the
topic has increased in recent years. The need to understand
plant–animal interactions in a warming Arctic has prompted
exclosure experiments and observational studies, and these
have demonstrated that herbivores can curtail the expansion
of their preferred forage species (Post and Pedersen 2008,
Olofsson et al. 2009, Rinnan et al. 2009, Ravolainen et al.
2014). For example, the aboveground biomass responses of
nonresinous dwarf birch (Betula nana ssp. nana) and grayleaf willow (Salix glauca) to increased temperature were
reduced substantially when plants were browsed by caribou
and muskoxen (Post and Pedersen 2008).
Despite the documentation that herbivores are capable of
regulating the response of tundra shrubs to climate change,
the degree to which different shrub species and assemblages
are influenced by climate and herbivory is unclear. Erect
shrubs cover a large portion (26%) of the unglaciated Arctic
(Walker et al. 2005) and are expected to expand to cover
a greater area in the future. Variation in the response of
different shrubs to climate change seems to be a function
of their capacity to respond to improved conditions (such
as longer growing seasons, greater nutrient availability, and
soil disturbance, which creates microsites for seedling establishment; Myers-Smith et al. 2011, Elmendorf et al. 2012).
The counteracting effect of herbivory on shrub growth has
been suggested to vary according to browsing pressure, plant
palatability, and plant tolerance to herbivory (Mulder 1999,
Myers-Smith et al. 2011). Understanding how herbivory
facilitates or moderates the expansion of different shrub species in a warming Arctic is important because the resulting
species composition will affect surface-energy exchange, soil
temperatures, decomposition, nitrogen cycling, and carbon
storage (Myers-Smith et al. 2011).
An initial step in understanding how shrub species are
differentially affected by herbivores is to document rates
of herbivory across functional groups, or groups that share
morphological, physiological, or phenological traits (Diaz
et al. 2004). Arctic shrubs can be divided most simply into
two distinct functional groups, deciduous and evergreen
shrubs, which have different traits that control their response
to environmental change and herbivory (Chapin et al. 1996).
Size, relative growth rate, patterns of resource partitioning,
and the ability to persist following disturbance are traits
that influence how a plant will respond to environmental
BioScience 65: 1123–1133. © The Author(s) 2015. Published by Oxford University Press on behalf of the American Institute of Biological Sciences. All
rights reserved. For Permissions, please e-mail: [email protected].
doi:10.1093/biosci/biv137
Advance Access publication 10 October 2015
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December 2015 / Vol. 65 No. 12 • BioScience 1123
Overview Articles
change. Deciduous plants tend to have high rates of growth,
photosynthesis, and nutrient absorption and typically partition a large proportion of growth to leaf area (Chapin et al.
1996). This group invests in the acquisition rather than the
conservation of resources (Díaz et al. 2004) and tends to
contain fewer defensive compounds than do evergreen species (Mulder 1999, Cornelissen et al. 2004).
Climate change in the Arctic is predicted to improve growing conditions for plants. Such conditions include longer
growing seasons, increased soil temperature and nutrient availability, increased solar radiation, altered soil moisture regimes,
increased soil disturbance, and earlier timing of snow melt
(Myers-Smith et al. 2011). Deciduous shrubs are expected to
respond most rapidly to these changes (Chapin et al. 1996) and
have indeed expanded in tundra regions via increased height
and annual growth (Forbes et al. 2010, Myers-Smith et al. 2011,
Macias-Fauria et al. 2012, Frost and Epstein 2014). Evidence
suggests that deciduous shrubs respond more readily to warming or fertilization than evergreen shrubs do (Elmendorf et al.
2012, Gough et al. 2012, DeMarco et al. 2014—but see Zamin
et al. 2014). Evergreen shrubs have thick, well-defended leaves
and tend to occupy nutrient-poor sites with minimal disturbance (Chapin et al. 1996). Their slower growth response may
put them at a disadvantage compared with deciduous shrubs
when warmed or fertilized (DeMarco et al. 2014), although in
areas where they are dominant, evergreens respond rapidly to
warming (Kaarlejarvi et al. 2012, Zamin et al. 2014).
This article synthesizes new and existing information to
clarify our understanding of the role played by vertebrate herbivores in either limiting or indirectly promoting the expansion of different shrub species in tundra ecosystems. First, we
summarize what is known about the chemistry and palatability
of different Arctic shrubs to herbivores and integrate this information with original data on the variation in susceptibility of
shrub species to herbivory in riparian communities across
a large area in Arctic Alaska. We focus on widespread erect
shrub species that are mentioned in multiple studies instead
of presenting an exhaustive review on all species of shrubs in
the Arctic. We limit our investigation to erect shrub species
whose maximum growth potential is more than or equal to 15
centimeters in height (Elmendorf et al. 2012), and we focus on
the consumption of woody tissues and leaves rather than berries. Second, we use data from published exclosure studies to
evaluate which species and functional groups are most strongly
inhibited by herbivores. We combine this information with
studies documenting the expansion of different shrub species
to make inferences about the regulation of shrubs by both climate and herbivory. Third, we discuss how climate change is
expected to influence herbivore populations in the Arctic and
the consequences for shrub communities. Finally, we discuss
the broader implications of our findings for Arctic ecosystems
and suggest future research directions.
Variation in the palatability of Arctic shrubs
The degree to which herbivores are expected to limit the
growth of different shrub species will likely be strongly
1124 BioScience • December 2015 / Vol. 65 No. 12
linked to their individual palatability, which is dependent
on the amounts of carbon-based defensive compounds,
nutrients, lignin, and cellulose in plant tissues, as well as
the relative palatability of other available plants (Bryant and
Kuropat 1980). Secondary compounds can take the form
of toxins, protein-precipitating compounds, and oxidative
compounds that cause stress to herbivores or inhibit digestion (Forbey et al. 2011, Salminen and Karonin 2011). Some
herbivores have behavioral and physiological adaptations
that allow them to consume chemically defended shrubs
(Iason and Palo 1991, DeAngelis et al. 2015). Nevertheless,
broad generalizations about plant groups can be made, representing a continuum of growth–defense tradeoffs (Bryant
et al. 1983, Cornelissen et al. 2004). In general, fast-growing
species such as willows are the least chemically defended
group of shrubs, whereas evergreen shrubs have the highest
concentrations of secondary compounds.
Evergreen ericoids such as Empetrum hermaphroditum
and Vaccinium vitis-idaea typically accumulate high concentrations of tannins and other types of phenolics, which can
inhibit the digestion of protein and cause oxidative stress
to herbivores (Iason and Palo 1991, Salminen and Karonin
2011). Their leaves have low nitrogen content and also contain toxic triterpenes (table 1; Jensen and Doncaster 1999).
In addition to secondary compounds, leaves of evergreen
ericoid shrubs contain other unpalatable components, such
as support structures and thick, waxy cuticles (Dahlgren
et al. 2009). As a result, these shrubs are generally avoided
by herbivores (White and Trudell 1980, Rammul et al. 2007).
Alnus viridis fruticosa (Siberian alder) is a tall (with a
maximum height of 12 meters) deciduous nitrogen-fixing
shrub that defends its twigs and buds with resins containing the highly toxic stilbenes pinosylvin (PE) and pinosylvin methyl ether (PME; table 1; Clausen et al. 1986). Most
northern browsing vertebrates avoid browsing Siberian
alder (Bryant and Kuropat 1980, Hjalten and Palo 1992),
although moose have been observed to consume alder in
Eurasia (Bruce Forbes, Arctic Center, University of Lapland,
personal communication, 16 May 2015). Alder is unique on
the tolerance-defense spectrum, with its ability to simultaneously invest in moderately rapid growth and in highly
effective antibrowsing defenses, which is a consequence of
its capacity to fix nitrogen (Hendrickson et al. 1991).
Betula nana is a deciduous shrub distributed throughout
the circumpolar Arctic, consisting of two subspecies that differ in their concentrations of secondary metabolites (table 1;
Graglia et al. 2001, Bryant et al. 2014). The nonresinous
subspecies, B. nana nana, occurs in Fennoscandia, Iceland,
Greenland, and eastern Canada, whereas the resinous B.
nana exilis occurs in Siberia and western North America
(Graglia et al. 2001, Bryant et al. 2014). B. nana exilis twigs
are lined with resin glands, which produce toxic triterpenes
such as 3-0-malyonylebetulafolientriol oxide I papyriferic
acid (Forbey et al. 2011, Bryant et al. 2014, DeAngelis et al.
2015). Therefore, this subspecies is browsed less frequently
than its European counterpart (see supplemental table S1 for
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Overview Articles
Table 1. Defensive compounds, nitrogen, and relative palatability of northern shrubs.
Group
Species
Defensive compounda
Evergreen
Vaccinium vitis-idaea (lingonberry)
Deciduous
% N leavesb
Palatabilityc
Tannins, phenols, triterpenes
0.9
Low
Empetrum ssp. (crowberry)
Tannins, phenols, triterpenes, cycloalkenes,
flavonoids
0.9
Low
Alnus viridis (Siberian alder)
Pinosylvin methyl ether, pinosylvin, phenols
2.3
Low
Betula nana exilis (dwarf resin birch)
Phenolic glycosides, condensed tannins,
triterpenes, flavonoids
2.5
Moderate
Betula nana nana (dwarf nonresin birch)
Phenolic glycosides, condensed tannins,
flavonoids
1.8
Moderate
Betula glandulosa (tall resin birch)
Phenolic glycosides, condensed tannins,
triterpenes
2.3
Moderate
Vaccinium uliginosum (bog bilberry)
Tannins, phenols
1.8
Moderate
Vaccinium myrtillus (bilberry)
Tannins, phenols
2.1
High
Salix spp. (willows)
Phenolic glycosides, condensed tannins
3.0
High
aThe
types of defensive compounds were obtained from Bryant and colleagues 1983, Jensen and colleagues 1999, Graglia and colleagues
2001, Hansen and colleagues 2006, Kaarlejarvi and colleagues 2012, Szakiel and colleagues 2012, Bryant and colleagues 2014.
bPercentage nitrogen from Michelsen and colleagues 1996, Graglia and colleagues 2001, Kaarlejarvi and colleagues 2012, Hansen and
colleagues 2006, Thompson and Barboza 2014, Chapin 1983, and Gessner and colleagues 1998.
cThe estimate of relative palatability was derived from Batzli and Lesieutre 1991 and Dahlgren and colleagues 2009.
shrub species, their principal herbivores, and their response
to climate drivers and herbivory). Similar to B. nana exilis,
the resinous B. glandulosa (shrub birch) is defended by
toxic triterpenes (Bryant et al. 2014, DeAngelis et al. 2015).
However, B. glandulosa is frequently consumed by caribou
and snowshoe hares (table S1; Crête and Doucet 1998,
DeAngelis et al. 2015).
In contrast to evergreen ericoids, the leaves of the deciduous ericoid shrub Vaccinium myrtillus are preferred foods
for hares, voles, and ptarmigan (table S1; Stokkan and Steen
1980, Dahlgren et al. 2009). Furthermore, Vaccinium uliginosum is an important component of the diet of caribou in
northern Canada (Crête et al. 1990). The leaves of these
deciduous ericoids contain fewer secondary metabolites
such as phenolics, lower lignin content, and/or higher
nitrogen concentrations compared with evergreen shrubs
(table 1; Cornelissen et al. 2004, Dahlgren et al. 2009,
Kaarlejärvi et al. 2012).
Willows are not well defended in comparison with alder,
birch, and evergreen shrubs, but they are a highly diverse
group, containing varying concentrations of phenolic glycosides, flavonoids, and polyphenols (table 1; Hansen et al.
2006). Willows are browsed by many species of Arctic
herbivores (figure 1, table S1), and certain willows exhibit
remarkable tolerance to herbivory through strong compensatory growth responses (Danell et al. 1994).
Defensive compounds and climate change
When exposed to increased soil fertility, as could occur with
warming in tundra (Nadelhoffer et al. 1991), concentrations
of carbon-based defensive substances such as terpenes and
phenolics may decrease because of the increasing investment
of carbon in the production of new growth (Bryant et al.
1983). In support of this hypothesis, B. nana nana, B. nana
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exilis, and S. herbacea x polaris decreased condensed tannin
concentrations after fertilization (Graglia et al. 2001, Hansen
et al. 2006). However, in the same experiment, V. vitis-idaea
increased concentrations of tannins after warming and
nutrient addition. In a separate study, warming had little or
no effect on tannin concentrations in E. hermaphroditum,
V. vitis-idaea, V.myrtillus, or B. nana nana (Kaarlejärvi
et al. 2012). In a study of E. hermaphroditum in Norway,
the effect of experimental warming on phenolics depended
on the individual phenolic compound, the nutrient regime,
and the grazing intensity at the site (Väisänen et al. 2013).
Clearly, the response of Arctic shrub secondary chemistry is
complex and varies significantly among and within species.
Variation in susceptibility to herbivory in Arctic
shrubs: A case study
To assess whether the continuum of tolerance versus defense
in Arctic shrubs in northern Alaska explains patterns of herbivory, we surveyed six Arctic shrub species (Alnus viridis
fruticosa, Betula nana exilis, S. lanata, S. glauca/niphoclada,
S. pulchra, and Salix alaxensis) occurring near major river
floodplains for signs of browsing. Because of the timing of
sampling (early June), we were able to quantify stem and
bud browsing but not leaf browsing. Supplemental text S1
describes the methods of data collection and analysis. We
used generalized linear mixed models to determine whether
the probability that a plant was browsed could be explained
by plant species or possible confounding effects such as
distance to the river and shrub height. Shrub species was
an important predictor of browsing for all herbivores except
snowshoe hares (figure 2; see supplemental tables S2 and S3
for model output). Willows were browsed more frequently
than birch and alder by all herbivores except snowshoe
hares (figure 2, figure 3). Ptarmigan browsed S. alaxensis
December 2015 / Vol. 65 No. 12 • BioScience 1125
Overview Articles
Figure 1. Arctic herbivores include the willow ptarmigan (a), muskox (b), and caribou (c). Also pictured are willows
recently browsed by moose and ptarmigan (d), willows with a stunted growth form due to browsing by ptarmigan (e), and
a healthy alder growing in an Arctic riparian floodplain with browsed willows in the foreground (f). Willow ptarmigan
photograph: Neil Paprocki; caribou photograph: Sophie Gilbert; other photographs: Katie Christie.
most frequently, followed by the other willow species, and
finally, B. nana exilis (figure 2). Ptarmigan did not browse
A. viridis. Moose followed a similar pattern, except they
appeared to avoid both B. nana exilis and A. viridis stems
(figure 2). The probability of browsing by small mammals
(Microtus oeconomus, Microtus miurus, Myodes rutilus, and
Spermophilus parryii) was greatest for S. lanata and S. glauca
and declined with shrub height and distance from the river
(table S3). Snowshoe hare browsing did not vary predictably
with any of the variables tested. The intensity of browsing by
all herbivores (proportion of stems browsed) was greatest for
S. alaxensis (46% of stems browsed), followed by S. pulchra
(37%), S. glauca/niphoclada (26%), S. lanata (24%), A. viridis
(19%), and B. nana exilis (17%; figure 3; see supplemental
table S4 for parameter estimates).
This case study represents browsing over the course of
one year and therefore may not be representative of longterm patterns of herbivory, nor does it show patterns of
leaf browsing by herbivores. Nevertheless, the results show
1126 BioScience • December 2015 / Vol. 65 No. 12
striking patterns of herbivory by ptarmigan, moose and
small mammals that largely adhered to the continuum of
tolerance versus defense, with willows experiencing the
­
greatest levels of herbivory and alder and birch experiencing
the least. Snowshoe hares appeared to have a more general
diet than other species, potentially because of b
­ ehavioral
mechanisms that enable them to consume chemically
defended plants (DeAngelis et al. 2015). Evidence from this
study suggests that herbivores have specific foraging strategies, which will in turn dictate their role in shaping Arctic
shrub communities. These results have strong ramifications
for expanding shrub communities, such that B. nana exilis
and A. viridis fruticosa may have an advantage over the more
heavily browsed willows.
Evidence for shrub expansion and regulation by
herbivores
A meta-analysis of 61 warming experiments in various Arctic
locations showed that evergreen shrubs are less responsive to
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Overview Articles
continue to dominate relatively cool sites
with poor soils. Models incorporating
both herbivory and climate change predict that in a warming climate, evergreen
shrubs will have an advantage over more
palatable and widely consumed deciduous shrubs, such as willows, where vertebrate herbivores are abundant (Yu et al.
2011). To evaluate this hypothesis, we
summarize results from nine different
exclosure studies that tested the effect of
herbivores on various Arctic shrubs in
figure 4 (data from these studies can be
found in supplemental table S5). Studies
were chosen on the basis of the following criteria: (a) the study was conducted
in an Arctic or tundra environment;
(b) results were presented in such a way
Figure 2. Results from browsing surveys near the Noatak and Sagavanirktok
that the proportional reduction in the
Rivers, Alaska, showing the probability of browsing (the number of plants
plant could be calculated; (c) the study
browsed/number of plants surveyed) by different vertebrate herbivores. The
was an exclosure study, not a browsing
sample size is shown beneath the axis labels. The error bars denote positive
simulation; and (d) results were reported
standard errors and represent variation among sites. No error bars are shown
for species, not groups of species.
for A. viridis because this species was found at only one site.
Exclosure studies showed that herbivores can have positive, neutral, or
negative effects on evergreen shrubs
­(figure 4). As was predicted, herbivores
reduced the height and cover of V. vitisidaea to a lesser extent (3%) than of
willows (3%–10%; figure 4; den Herder
et al. 2008, Pajunen et al. 2008, Kitti
et al. 2009). However, multiple studies
in Norway indicated that high densities of lemmings can reduce the cover
of unpalatable E. hermaphroditum and
V. vitis-idaea (figure 4; Olofsson et al.
2009, Hoset et al. 2014, Olofsson et al.
2014). Contrasting results were found in
another study in Norway, in which herbivory by voles and lemmings increased
the abundance of E. hermaphroditum (figure 4; Grellmann et al. 2002).
Observational studies also reveal contrasting effects of herbivory on evergreen shrubs. Evergreen ericoids were
Figure 3. The browsing intensity (mean proportion of stems browsed per
decimated on a Scandinavian island
plant) by all herbivores on different species of shrubs near the Noatak and
with high densities of voles but thrived
Sagavanirktok Rivers, Alaska. The herbivores included moose, ptarmigan,
when voles were at moderate densities
hares, and small mammals. The sample size is shown beneath the axis labels.
(Dahlgren et al. 2009). However, no
The error bars denote positive standard errors and represent variation within
effect of reindeer density was observed
and among sites.
on the abundance of E. hermaphroditum
warming than deciduous shrubs (Elmendorf et al. 2012).
in Finnmark (Bräthen et al. 2007). An
However, evergreen shrubs in experimentally warmed
explanation for the variable effect of herbivores on unpalatchambers have been shown to rapidly increase their biomass
able evergreen shrubs is that voles and lemmings feed on
in low-productivity areas where they are already dominant
these shrubs when at population peaks (e.g., when released
(Zamin et al. 2014). Therefore, evergreen shrubs will likely
from predator pressure) when preferred foods are limited
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December 2015 / Vol. 65 No. 12 • BioScience 1127
Overview Articles
Figure 4. The mean proportional change in height, cover, biomass, and abundance caused by herbivory; the error bars
represent the standard error. The data were compiled from herbivore exclosure studies in the Arctic, and were averaged
across sites (see supplemental table S5 for values from individual sites). Because the studies were conducted over different
time periods, the values have been standardized so that they reflect changes over a single year. Negative and positive
values indicate a decrease and increase, respectively, in the plant characteristic relative to plants that were protected from
herbivores. Only studies in which exclosures were used and in which effect size was reported were included, and data from
exclosures that excluded both small mammals (voles, lemmings, ground squirrels) and large mammals (reindeer, caribou,
moose) were used whenever possible. All reported values are from plots experiencing ambient conditions (not fertilized
or warmed). The height and cover data were obtained from Pajunen and colleagues (2008), den Herder and colleagues
(2008), and Kitti and colleagues (2009); the biomass data were obtained from Olofsson and colleagues (2009; change
in biomass; black), Post and Pedersen (2008; biomass index; red squares), Zamin and Grogan (2013; new stem biomass
only; green triangles), and Gough and colleagues (personal communication; total aboveground biomass, blue crosses). The
abundance data were obtained from Grellmann and colleagues (2002). The standard errors were calculated on the basis of
the variability among sites reported in each published study. When only one data point was reported, we used the formula
SE = p(1–p) , where p was the proportional reduction and n was the sample size. Color image can be viewed on the
n
BioScience website.

(Dahlgren et al. 2009, Hoset et al. 2014), whereas at lower
densities, herbivores ignore unpalatable shrubs and focus on
preferred deciduous shrubs. Furthermore, trampling or light
browsing can cause shoot mortality, and damage to even a
small amount of tissue can be detrimental to ericoid shrubs
because they are unable to replenish stored reserves in an
environment where resources are often limited (Pajunen
et al. 2008, Dahlgren et al. 2009).
With its high growth rate, nitrogen-fixing symbionts,
and formidable chemical arsenal against herbivores, alder
may be uniquely positioned to take advantage of a warming Arctic climate. The paleo-record indicates that alder
quickly spread in the early Holocene as temperatures
warmed and moisture increased with the retreat of the
glaciers (Kokorowski et al. 2008). Over the past century,
A. viridis fruticosa and A. incana have thrived in northern
Alaska, Canada, Siberia, and northern Sweden, and their
1128 BioScience • December 2015 / Vol. 65 No. 12
expansion appears to be linked to warming, increased
precipitation, permafrost thaw, fire frequency, and nutrient
availability (Tape et al. 2006, Lantz et al. 2010, MaciasFauria 2012, Frost and Epstein 2014). Periodic insect outbreaks (Hendrickson et al. 1991), small mammals, moose
(Bruce Forbes, Arctic Center, University of Lapland, personal communication, 16 May 2015) and snowshoe hares
may constrain the growth of alder, and further studies on
interactions with herbivores will be necessary to determine
whether they moderate its expansion. Similar to what has
occurred in boreal ecosystems (Butler and Kielland 2008),
herbivores may foster alder expansion by consuming competing shrub species (figure 1f). Alder has the potential to
substantially alter biogeochemical cycles because of its ability to fix nitrogen.
There is evidence that the height, cover, and biomass
of nonresinous dwarf birch (B. nana nana) are limited by
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Overview Articles
herbivores (figure 4; Graglia et al. 2001, Pajunen et al. 2008,
Post and Pedersen 2008, Olofsson et al. 2009—although
see Bråthen et al. 2007). Resinous dwarf birch (B. nana
exilis) in North America and Siberia may not be as strongly
limited by herbivores as its European counterpart because
of the toxic triterpenes in its bark (Bryant et al. 2014). In
northern Alaska, B. nana exilis biomass was greater outside
than inside exclosures, and this was thought to be due to
a competitive advantage over more palatable species in
the presence of herbivores (figure 4; Gough et al. 2012).
B. nana exilis responds positively to warming and nutrient
addition because of its tendency to increase the number of
active meristems and to produce long shoots under optimal
conditions (Bret-Harte et al. 2001). This subspecies’ ability to both defend itself with chemically laden resins and
respond quickly to improved conditions predisposes it to be
one of the leaders of shrub expansion where it occurs in the
Arctic, which is what happened in Beringia during the early
Holocene warming (Kokorowski et al. 2008).
Similar to B. nana exilis, B. glandulosa is a resinous birch
that is expected to be minimally influenced by herbivores
(Bryant et al. 2014). However, evidence indicates that caribou, when abundant, can reduce the biomass and prevent
the recovery of birch for several years (figure 4; Crête and
Doucet 1998, Zamin and Grogan 2012). B. glandulosa is
known to respond favorably to both warming and fertilization (Zamin and Grogan 2012, Zamin et al. 2014) and therefore is likely to exploit warmer temperatures. In Nunavik,
Canada, B. glandulosa has undergone a marked expansion
over the past half-century despite being severely damaged by
caribou in the 1980s (Tremblay et al. 2012).
Deciduous ericoid shrubs such as V. uliginosum and
V. myrtillus showed contrasting responses to herbivory.
Although V. myrtillus biomass and abundance were reduced
by herbivores in two separate exclosure studies (Grellmannn
et al. 2002, Oloffsson et al. 2009), herbivores had only a slight
positive effect on V. uliginosum, which in one study may
have benefited from being passed over by caribou in favor of
other species (figure 4; Zamin and Grogan 2013).
Willows have shown remarkable resilience to herbivory
when resources are available, and can compensate by producing longer, larger-diameter shoots (Bowyer and Neville
2003, Christie et al. 2014a). Nevertheless, evidence indicates
that herbivores regulate willow growth, architecture, reproduction, and survival (den Herder et al. 2008, Pajunen et al.
2008, Kitti et al. 2009, Ravolainen et al. 2014). In riparian
willow thickets of northern Alaska, ptarmigan browsed over
70% of individual willow shrubs (figure 2) and removed
over a third of the buds, substantially altering architecture
and reproduction (figure 1e; Christie et al. 2014a). Exclosure
studies show that on an annual basis, herbivores reduce the
height of willows by 3%–7% annually, cover by 5%–10%, and
shoot length by 32%, and they increase mortality by 14%
(figure 4; Grellmann 2002, den Herder et al. 2008, Pajunen
et al. 2008, Kitti et al. 2009, Ravolainen et al. 2014). In contrast, herbivores appeared to increase the biomass of willows
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in Greenland under ambient conditions but reduced their
biomass response by 11% under warmed conditions (Post
and Pedersen 2008).
Long-term studies of shrub expansion using aerial photography and remote sensing show that willows have expanded
over the past half-century in northern Alaska and Russia
(Tape et al. 2006, Walker et al. 2009). In the Russian Arctic,
the growth of erect willows closely tracked regional temperatures over a 60-year period despite the presence of reindeer
herds (Forbes et al. 2010). In contrast, reindeer herds in
Norway have drastically reduced the abundance of willows in
heavily browsed areas (Ravolainen et al. 2014). Collectively,
data suggest that the severe limitation of willow expansion is
likely to occur only in areas of high herbivore density.
In summary, the counterbalancing effects of herbivory
and climate on shrub growth and height seem to vary
depending on shrub species, herbivore species, and herbivore density. Although trampling and herbivory by vertebrates are likely to slow the expansion of evergreen shrubs,
we hypothesize that both the top-down effects of moderate
herbivory and the bottom-up effects of climate will be weakest on this group (figure 5), with the caveat that at high
densities (such as on predator-free islands), herbivores can
keep evergreen shrubs in check. Deciduous shrubs such as
alder, birch, and willows appear to be leading the expansion
of shrubs in Arctic tundra ecosystems (Tape et al. 2006,
Macias-Fauria et al. 2012, Frost and Epstein 2014). We
expect these species to respond favorably to increased disturbance frequency (e.g., fire, permafrost degradation, and
human activities), longer growing seasons, and enhanced
nutrient availability in the Arctic (figure 5; Myers-Smith
et al. 2011). Exclosure and observational studies demonstrate that herbivores dampen the response of willows and B.
nana nana to improved conditions in the Arctic (figure 5),
whereas herbivores only slightly moderate the response of
better-defended species such as B. nana exilis and Alnus
viridis, and these species may expand more rapidly, in part
because of higher rates of herbivory on more palatable species (figure 5). Interestingly, during the late glacial transition (approximately 16,000–11,000 calendar year Before
Present), B. nana exilis and Alnus viridis dominated the
positive response of vegetation to increased temperatures in
Beringia (Kokorowski et al. 2008).
Herbivore density will influence the response of shrubs to
improved conditions in the Arctic such that at low herbivore
densities, inherent physiological characteristics and site conditions will define shrub responses to improved conditions
(Rinnan et al. 2009, Myers-Smith et al. 2011). At medium
herbivore densities, palatable deciduous shrubs will be targeted by herbivores, encouraging unpalatable deciduous and
evergreen shrubs to flourish (Dahlgren et al. 2009). At high
herbivore densities, the expansion of all three groups may be
inhibited because herbivores will be less selective and more
likely to trample vegetation (Pajunen et al. 2008, Dahlgren
et al. 2009, Olofsson et al. 2009). Much remains to be learned
about the counterbalancing forces of climate and herbivory
December 2015 / Vol. 65 No. 12 • BioScience 1129
Overview Articles
and increased fire frequency and severity. Climate factors
such as extreme weather events cause synchronous population declines among Arctic vertebrates (Hansen et al. 2013).
Warmer winters are expected to continue to dampen rodent
population cycles, which in turn strongly influence vegetation (Hoset et al. 2007, Ims et al. 2011). Tundra specialists
may over time become replaced by species better adapted
to boreal conditions as shrubs expand and sub-Arctic vegetation becomes more prevalent (Callaghan et al. 2004).
Increased fire severity in the Arctic is expected to decrease
winter habitat for caribou by up to 30%, but increase moose
habitat by 19%–63% (Joly et al. 2012). Already, caribou have
experienced declines in many parts of their range because of
anthropogenic factors and climate change (Festa-Bianchet
et al. 2011—although see Kolpaschikov et al. 2015), whereas
for reindeer, the negative effects of climate change have
been offset by supplemental feeding, leading to population
increases in some parts of their range (Forbes 2010). Moose
(Alces alces) and hares (Lepus americanus, Lepus europaeus)
appear to be expanding northward (Jansson and Pehrson
2007, Schmidt et al. 2009). Ptarmigan, who use willows for
food and cover from predators, may benefit in the short
term from shrub expansion, because their distribution is
strongly linked to the amount of shrubs exposed above the
snow (Christie et al. 2014b). However, warm winters may
counteract this effect and have adverse effects on Arctic
ptarmigan populations by lowering the quality of subnivean
roost sites and increasing the probability of rain events
(Wang et al. 2002). As Arctic specialists retreat northward
and boreal species expand into a more hospitable Arctic,
trophic interactions are likely to change. Boreal predators
and pathogens may expand northward to exploit prey–host
populations and may subsequently regulate their densities
(Van der Putten et al. 2010) and reduce their impact on the
vegetation (Dahlgren et al. 2009).
Figure 5. An illustration of how moderate levels of
herbivory and climate change are predicted to regulate
different shrub groups. The thickness of the arrows
represents the hypothesized strength of the effect, with the
dashed line representing the weakest effect. The effect of
climate depends on the response to altered conditions and
site conditions, whereas the effect of herbivory depends on
palatability, browsing pressure, tolerance, and resource
limitation. The plus signs reflect the net effect of top-down
and bottom-up forces, and more plus signs indicate a
greater predicted shrub expansion under climate change.
in the Arctic, and future research that examines these processes across a range of herbivore densities and shrub communities is needed.
Climate change and herbivore populations
Herbivore populations in the Arctic are likely to change with
shifting vegetation composition and phenology, increased
temperatures and precipitation, longer growing seasons,
1130 BioScience • December 2015 / Vol. 65 No. 12
Conclusions
Naito and Cairns (2015) reported that Arctic river valleys
are at a “tipping point,” shifting inexorably toward homogenous erect shrublands, with permanently altered structure
and function. Evidence from long-term observational and
experimental studies indicates that herbivores reduce but do
not prevent the expansion of fast-growing deciduous shrubs
such as willows and nonresinous dwarf birch, thereby moderating the positive effects of climate warming on shrubs.
Variation in nutritional chemistry among Arctic shrubs
translates to strong preferences for (and damage to) palatable deciduous shrubs, despite the ability of many willows
to compensate for browsing. Evergreen shrubs are generally less preferred by herbivores but can be vulnerable to
trampling and browsing where animals are at high densities.
The well-defended Siberian alder and resinous dwarf birch
are generally not preferred by herbivores and may outpace
the expansion of more palatable willows, although studies
are needed to test this hypothesis. Although it is clear that
herbivores have the capacity to influence shrub growth,
http://bioscience.oxfordjournals.org
Overview Articles
how herbivore populations will respond to altered climate
regimes and vegetation communities is unknown and warrants further investigation. Expanding populations of herbivores will consume large quantities of deciduous shrubs
and may play an increasing role in moderating their growth.
The effects of herbivory extend beyond aboveground
changes to Arctic ecosystems, and herbivores are known to
influence nitrogen and carbon cycling and net ecosystem
productivity. Herbivores can increase ecosystem productivity by creating small-scale disturbances, fertilizing soils, and
increasing microbial activity, resulting in shifts among alternative stable states (Stark et al. 2002, Olofsson et al. 2004,
van der Wal et al. 2006). Furthermore, by inhibiting shrub
expansion, herbivores can mediate the effects of climate
warming on carbon dioxide exchange in tundra ecosystems
(Cahoon et al. 2012, Väisänen et al. 2014).
To better understand how trophic interactions between
herbivores and shrubs are expected to change, we suggest
the following four research directions: (1) Changes in shrub
height, biomass, and abundance should be monitored over
the long term to determine rates of expansion for different
species. (2) Herbivore exclosures need to be maintained over
the long term across a broad range of Arctic habitat types
and climate conditions to quantify the effects of herbivores,
and they should be designed to exclude both large and small
herbivores while not altering snow conditions. These studies
also need to clearly establish the links between herbivory
and carbon and nitrogen cycling. (3) The distribution and
abundance of important Arctic herbivores needs to be
monitored over the long term to determine how climate
change is affecting their populations. (4) Studies need to
monitor the expansion of alder and the role herbivores play
in limiting its expansion. Arctic ecosystems are experiencing
unprecedented change, and we recognize top-down control
by herbivores as a crucially important process in attempting
to understand and model these changes.
Acknowledgments
We would like to thank Christa Mulder, Mark Lindberg,
Joel Schmutz, Bruce Forbes, and the anonymous reviewers
for their valuable comments on earlier drafts of this article.
We thank the Institute of Arctic Biology at the University of
Alaska, in Fairbanks, and the National Science Foundation
(Award no. 1026415) for financial support and Becky
Hewitt, Neil Paprocki, and Katie Rubin for help in the field.
With the exception of the principal author, the order of
authorship was determined alphabetically.
Supplemental material
The supplemental material is available online at http://
bioscience.oxfordjournals.org/lookup/suppl/doi:10.1093/biosci/
biv137/-/DC1.
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Katie S. Christie ([email protected]) conducted this research as a PhD student at the Institute of Arctic Biology at the University of Alaska, in Fairbanks.
She researches plant–animal interactions and wildlife population dynamics
and currently holds a postdoctoral position at the University of Alberta. John
P. Bryant ([email protected]) researches plant–animal interactions and is
a professor emeritus at the University of Alaska, in Fairbanks. Laura Gough
([email protected]) is a professor and chair of the Department of Biological
Sciences at Towson University where she studies how plant communities are
structured and influence ecosystem properties, particularly in arctic tundra.
Virve T. Ravolainen ([email protected]) researches plant ecology in
Arctic ecosystems at the Norwegian Polar Institute, in Tromsø, Norway. Roger
W Ruess ([email protected]) is a professor of biology at the University of
Alaska, in Fairbanks, where he researches herbivory and nutrient cycling in
northern ecosystems. Ken D. Tape ([email protected]) is an ecologist at the
Institute for Northern Engineering at the University of Alaska, in Fairbanks,
where he researches landscape changes in the Arctic.
December 2015 / Vol. 65 No. 12 • BioScience 1133