SIGNIFICANCE OF VOLE BROWSING IN PLANT-HERBIVORE INTERACTIONS IN THE BOREAL ECOSYSTEM
PROJECT DESCRIPTION PHD-PROJECT - MARCEL SCHRIJVERS-GONLAG
Høgskolen i Hedmark
Avdeling for anvendt økologi og landbruksfag
FINAL VERSION MSG080812
Introduction
In natural ecosystems around the world herbivores play an important role in ecosystem processes. Herbivores
affect plant community structure and dynamics in many ways. Although herbivory may kill small plants (and
also seedlings) instantly (direct effects of herbivory), the more common effect is a reduction in growth and
resource uptake and changes in plant chemistry and morphology. This affects future herbivory, and possibly
population dynamics of herbivores, as well as competitive hierarchies between plants and thus vegetation
composition and dynamics as well as nutrient cycling (Hester et al. 2006a; Hobbs 1996; Skarpe & Hester 2008).
Herbivory by large herbivores
Much research has been conducted on large herbivores. Large herbivores are major drivers of the shape and
function of many terrestrial ecosystems (Danell et al. 2006; Hester et al. 2006a; Olff et al. 1999a; Olff et al.
1999b). Grazing and browsing by large herbivores have, apart from direct effects on the vegetation, also
indirect effects that influence the plant community level. The huge impact of large herbivores on plant
populations, forest structure and ecosystem processes is clearly demonstrated by published data on the
activities of moose (Alces alces) from Europe, Asia and North America, collected by Persson et al. (2000). The
estimates they collected suggest, that an average moose eats about 8000 kg fresh plant material annually,
tramples an area of about a hectare, and produces about 5000 pellet groups (Persson et al. 2000).
Grazing and browsing by large herbivores affects soils and soil biological properties such as litter
decomposition, soil nitrogen availability, nutrient cycling, soil microarthropod communities and soil microbial
activity. This can be done in several ways: by enhancing availability of nutrients, speeding up processes (urine
and faeces deposition, increased soil temperature etc) as well as by decreasing availability of nutrients, slowing
down processes etc as a result of, for instance, enhanced production of defense compounds (Bakker et al. 2004;
Harrison & Bardgett 2003, 2004, 2008; Lessard et al. 2012; Pastor et al. 2006; Stritar et al. 2010; Van der Wal et
al. 2004). These factors have effect on vegetation structure, composition and dynamics and on the interaction
with browsing and grazing by large herbivores (Goheen et al. 2004; Goheen et al. 2010; Hester et al. 2006a;
Hester et al. 2006b; Mathisen et al. 2010; Peinetti et al. 2001; Skarpe & Hester 2008; Speed et al. 2010; Van de
Koppel & Prins 1998; Zeigenfuss et al. 2011).
Small herbivores
Small mammalian and insect herbivores may be affected by large herbivores through changes in plant species
composition, nutrient content, chemical and morphological defenses and through vegetation structure (Bakker
et al. 2009; Keesing 1998; Saetnan & Skarpe 2006; Schrijvers & Schot-Opschoor 1997; Smit et al. 2001;
Suominen & Danell 2006; Vesterlund et al. 2012). Herbivory and related behavior (winter food hoarding,
disturbance etc) by small herbivores itself might be of importance for vegetation dynamics, interactions
between herbivores and soil nutrient cycling processes (Bakker et al. 2004; Gervais et al. 2010; Hansson 2002;
Roth & Vander Wall 2005; Sherrod et al. 2005; Vander Wall et al. 2006). For instance: voles can consume a
comparable amount of biomass as moose do in the boreal forest. In peak years voles consume more than 10
times as much biomass per area as moose (at a moose density of one per square kilometer), and their influence
on forage plants and soil processes is likely to impact vegetation composition and structure and to influence
foraging of other herbivores, from moose to insects (Andreassen et al. in Skarpe 2011).
PhD project description MSG
Page 1 of 21
Herbivory in the boreal forest
This project (as being part of the overall BEcoDyn project, see Andreassen & Dietrichs (2011)) focuses on the
boral forest, a major forest type in the northern hemisphere which is known to be a nitrogen-limited system
(Persson et al. 2005b). Moose is a common large herbivore in the boreal forest in most parts of the northern
hemisphere (Baskin 2009; Henttonen et al. 2008; Kays & Wilson 2009). In the boreal forest, moose browsing is
recognised as ecologically very important because moose can affect the quality and quantity of forage for other
large and small herbivores, vegetation structure and species composition as well as material and energy flows
and other soil dynamics in the ecosystem through their selective feeding, defecation, urination and trampling
(Beest et al. 2010; Harrison & Bardgett 2008; Mathisen et al. 2010; Mathisen & Skarpe 2011; Persson et al.
2005a; Persson et al. 2005b; Suominen et al. 1999; Suominen et al. 2008). For example, Persson et al. (2005b)
found that litter quantity decreased with increasing level of simulated moose density. They also found that,
contradictory to studies from North America, litter quality (C:N ratio and N contribution per mass unit of litter)
was not affected by level of simulated moose density (Persson et al. 2005b).
Less recognised, but presumably also very important for ecological processes in the boreal forest is herbivory by
small mammals, which has been studied in several reseach projects in Scandinavia and Canada (Dahlgren et al.
2007; Krebs et al. 2001).
In the boreal forest several vole and mouse species are present. Small rodents (both voles and mice) play an
important role in many ecosystems, including the boreal forest, for several reasons:
1. small rodents are important prey species for a large number of mammalian and avian predators and a
lot of reptile species (Eccard et al. 2008; Forsman & Lindell 1997; Graham & Lambin 2002; Hughes et al.
2010; Korpimaki et al. 1991; Mappes et al. 1993; Panzacchi et al. 2010; Sundell et al. 2004).
2. they are primary consumers of a wide range of species, including plants, mosses, lichens, fungi and
invertebrates (Bangs 1984; Hjalten et al. 1996; Ure & Maser 1982).
3. the vegetation is directly influenced by small rodents, not just because of 2) (which may influence
forage quality and avilability for other herbivores as well) but also because voles can affect tree
seedlings. Inflicted damage to silviculture by debarking or severing tree seedlings by small rodents can
cause severe economic losses (Hansson 1991, 1992, 1994, 2002; Huitu et al. 2009; Pusenius et al. 2000;
Pusenius et al. 2002; Vehvilainen & Koricheva 2006).
4. small rodents can both inhibit and facilitate seed dispersal (Roth & Vander Wall 2005; Scheper & Smit
2011; Schrijvers & Schot-Opschoor 1997; Smit et al. 2001; Vander Wall 2002, 2003; Vander Wall et al.
2006).
5. small rodents can, just like for instance ungulates do, influence (both acceleration and deceleration) soil
processes like nitrogen and carbon cycling and therefore influence plant and litter production (Menezes
et al. 2001; Pastor & Cohen 1997; Pastor et al. 1996; Peinetti et al. 2001; Persson et al. 2009; Ritchie et
al. 1998; Singer & Schoenecker 2003).
6. populations of small rodents in the boreal ecosystem tend to fluctuate more or less regularly in a 4-year
cycle, adding a temporal variation to all the above mentioned conditions (Andreassen & Dietrichs 2011;
Kjellander & Nordström 2003; Selås 2006).
The most abundant vole/mouse species in the boreal forest (so-called forest-dwelling species) belong to the
genus Myodes (formerly known as Clethrionomys): in America it’s red-backed voles, Myodes sp. (several
species) and in Europe it’s mainly grey-sided vole, Myodes rufocanus and bank vole, Myodes glareolus (Boonstra
& Krebs 2012; Ecke et al. 2002; Panzacchi et al. 2010). Field vole, Microtus agrestis is also abundant in the
Scandinavian landscape but prefers grass-dominated meadows over dense shrubland and forested areas
(Hanski et al. 2001; Panzacchi et al. 2010).
Bilberry (Vaccinium myrtillus) is an abundant plant species in the understory of many forest types in the boreal
forest region in Scandinavia (Fremstad 1997) and grows also in the northern parts of Asia (figure 1. in Nestby et
al. (2011)). Bilberry is also present in the western part of the United States, where it used to be considered a
PhD project description MSG
Page 2 of 21
subspecies or variety of bilberry (Vaccinium myrtillus ssp. oreophilum or V. myrtillus var. oreophilum) or even a
different species: V. oreophilum that’s nowadays often called whortleberry or ‘low bilberry’ (Canadensys 2012;
USDA 2012). This dwarf shrub is used as forage by a lot of browsers: for instance red deer (Cervus elaphus),
moose, roe deer (Capreolus capreolus), mountain hare (Lepus timidus), several vole species and insect species.
Indirectly it is important for insect feeding forest grouse chicks. Grey-sided vole uses bilberry primarily as a
winter forage, whereas bank vole feeds on bilberry also in summertime (Dahlgren et al. 2007). Several research
projects show a positive association between bank vole abundance and bilberry availability (see f.ex. Gorini et
al. 2011). For these reasons we use bilberry and bank vole in our experiments (see Methods).
Plant strategies related to herbivory
As browsing and grazing by herbivores have effects on plants and vegetation processes, plants can deal with
herbivory in different ways. Various strategies which minimise negative effects of herbivory on plant fitness are
shown in figure 1. These strategies are all called resistance strategies and within that concept different
avoidance and tolerance strategies (the two principal plant strategies against damaging effects of herbivory) can
be distinguised (Mauricio 2000; Rosenthal & Kotanen 1994; Strauss & Agrawal 1999), see figure 1. Plants that
avoid or deter herbivores are fed upon less than susceptible plants. Tolerant plants are not eaten less than
plants with little tolerance, but the effects of herbivore damage are not so detrimental to a tolerant plant as
they are to a less tolerant plant (Mauricio 2000).
Internal escape mechanisms encompass morphological traits, as short stature (maintaining a large proportion of
the biomass below herbivory level) or keeping most edible biomass above reach for terrestrial mammalian
herbivores (this concerns huge shrubs and tree species, primarily). Other examples of internal escape are
deciduousness, the reduction of the whole plant to underground organs and survival as seed in unfavorable
conditions (Skarpe & Hester 2008). These temporal internal escape mechanisms make the plant less apparent,
sensu Feeny (1976). Another example is the storage of resources in woody stems or below ground surface.
Figure 1. Plant resistance to herbivores: conceptual strategies (derived from Kotanen & Rosenthal 2000; Milchunas & Noy-Meir 2002;
Rosenthal & Kotanen 1994; Strauss & Agrawal 1999). Modified by Skarpe & Hester (2008) from Hester et al. (2006a).
External escape mechanisms include growing in inaccessible places such as rock outcrops or steep slopes
(Skarpe & Hester 2008). Plants may also escape herbivory by association with either less palatable or more
palatable species, depending upon what scale the herbivore makes forage-decisions (selective herbivory on a
fine scale or relatively rough herbivory on stand level): neighbours are important (Hjalten et al. 1993; Olff et al.
1999b; Skarpe & Hester 2008). This includes the establisment of saplings in unpalatable patches (Smit & Ruifrok
2011).
Plant defense strategies can be devided in physical (structural) and chemical defenses. Physical defenses as
spines, prickles and thorns reduce plant losses to herbivores, even when they do not prevent browsing (Skarpe
& Hester 2008; Smit et al. 2010). A large number of chemical compounds in plants have been shown to have
deterrent effects on herbivore foraging.
PhD project description MSG
Page 3 of 21
Chemical defense strategies
The research on plant defense has been guided by a series of hypotheses that initially seemed to hold great
promise for developing a general theory of plant defense, in particular one that would explain why most plants
seem to be so well defended (Stamp 2003). By the mid-1970s, the Optimal Defense Hypothesis was taking
shape. Data gathered to test this hypothesis suggested the need for another one. Among other less cited and
used ones, another three main hypotheses on plant defenses have been developed during the next two
decennia. These four hypotheses are briefly outlined below.
The Optimal Defense Hypothesis (OD)
This hypothesis assumes that defenses are costly because they divert resources from growth, and that
herbivory is the primary selective force shaping quantitative patterns of secondary metabolism (Fagerstrom et
al. 1987; McKey 1974; Stamp 2003). The hypothesis predicts that because defenses are costly, resources are
allocated to defense in ways that optimize that investment. Plants will defend tissues in direct proportion to the
cost of their loss. Easily replaced, less critical tissues and organs will be less defended than hard-to-replace,
indispensable ones (Mattson et al. 1988). Plant parts with high fitness value will therefore be highly defended.
Furthermore, patterns of defensive investment will reflect the frequency and severity of herbivory experienced
by populations over evolutionary time (Chew & Courtney 1991).
Growth Rate Hypothesis (=Resource Availability Hypothesis) (GRH)
Published in the mid-1980s, this plant defense hypothesis states that the optimal level of defense will vary with
the potential growth rate of the plant (Coley et al. 1985). The level of defense investment increases as the
plant’s potential growth rate decreases. Because growth rate is correlated with nutrient availability, higher
defenses are expected in ‘slower growers’ (plant species evolved in resource-limited environments) resulting in
relatively low herbivore damage. On the other hand, lower levels of defense are expected in ‘fast-growers’
(plant species evolved in resource-rich environments), resulting in relatively high herbivore damage. The
optimal defense level is achieved with intermediate levels of defense causing maximum growth rates. Below
this level growth is reduced because of high losses to herbivores, above this level growth is reduces because of
an excessively high cost of defense (Coley et al. 1985). In the Growth Rate Hypothesis, herbivory and
competition are complementary to the selective pressure of resources (Stamp 2003).
Two conceptually similar hypotheses have been advanced to predict environmental effects on the phenotypic
expression of secondary metabolism (Herms & Mattson 1992):
(1) the Carbon-Nutrient Balance Hypothesis
(2) the Growth-Differentiation Balance Hypothesis
Carbon-Nutrient Balance Hypothesis (=Environmental Constraint Hypothesis) (CNBH)
This hypothesis, developed around the same time as the Growth Rate Hypothesis, predicts that concentrations
of carbon-based secondary metabolites will be positively correlated with the carbon/nutrient (C/N) ratio of the
plant. Conversely, concentrations of nitrogen-based secondary metabolites are predicted to be inversely
correlated with the C/N ratio of the plant (Bryant et al. 1983). In other words: in nutrient-limited environments
chemical defenses are largely carbon-based. In high-nutrient or low-carbon environments carbon-based
defenses decline, and nitrogen-based defenses become more important.
The Carbon-Nutrient Balance Hypothesis focuses on the effects of shade and fertilization on allocation to
secondary metabolism versus growth (Bryant et al. 1983; Stamp 2003).
Growth-Differentiation Balance Hypothesis (GDBH)
Already being published in the first half of the twentieth century by Loomis (1932), this hypothesis regained
attention in the late 1980s (Lorio 1986) and was expanded in the early 1990s (Herms & Mattson 1992). The
Growth-Differentiation Balance Hypothesis states that there is a physiological trade-off between growth and
secondary metabolism and predicts a parabolic effect of resource availability (such as water or nutrients) on
secondary metabolite production. This hypothesis subsumes the Carbon-Nutrient Balance Hypothesis,
predicting that any environmental factor that slows growth more than it slows photosynthesis can increase the
carbon pool available for allocation to secondary metabolism.
PhD project description MSG
Page 4 of 21
The expanded Growth-Differentiation Balance Hypothesis (Herms & Mattson 1992) predicts how over
evolutionary time the relative importance of herbivory and competition have shaped plant allocation patterns.
So, selective pressures of herbivory and competiton have been added to the original hypothesis, having it
expanded with an ‘ecological side’ and an ‘evolutionary side’ (Stamp 2003). Regrowth of plant tissue, after
herbivory, is integrated in the mathematical model of the expanded Growth-Differentiation Balance Hypothesis
(Herms & Mattson 1992).
As pointed out by Stamp (2003), the Carbon-Nutrient Balance Hypothesis needs the Growth Rate Hypothesis,
and vice versa, to explain certain observations. And both these hypotheses need the Growth-Differentiation
Balance Hypothesis to account for trade-off complexities between growth and differentiation. The several
hypotheses can serve complementary to explain observed findings. It is appropriate to integrate these different
hypotheses on plant defense (Stamp 2003). When doing so, several observed phenomena can be explained,
what otherwise would seem like a contradiction. For instance, when considering a light gap in a shaded forest,
observed differences in defense compounds can be explained by using the Growth Rate Hypothesis for
interspecific differences and the Carbon-Nutrient Balance Hypothesis for intraspecific differences (Bryant et al.
1983; Coley 1987). As concluded by Stamp (2003, 2004) the expanded Growth-Differentiation Balance
Hypothesis is the most theoretically mature of the hypotheses of plant defense.
Plant tolerance might be a more advantageous strategy than avoidance when plant defense is ineffective in
preventing loss of biomass (this can occur when plants are growing in resource-rich environments but also
when, for instance, trampling or bark stripping is an important source of damage) (Hester et al. 2006a; Jokela et
al. 2000; Strauss & Agrawal 1999). Tolerance can be described as the capacity of a plant to maintain its fitness
through growth and reproduction after sustaining herbivore damage. Intrinsic tolerance is about plant tolerance
mechanisms that are governed by intrinsic factors (determined genetically). Extrinsic tolerance deals with
external factors such as environmental resources available for growth (Rosenthal & Kotanen 1994).
Intrinsic morphological features promoting plant tolerance of herbivory by large herbivores include protected
and/ or numerous meristems, wide distribution of leaves and buds, branching or tillering responses, stolons,
rhizomes, seed numbers, viability, longevity and size (Hester et al. 2006a). The presence of active meristems
after damage is a crucial trait conferring tolerance (Richards 1993). Important for herbivory impact is the
difference between dicotyledons (woody plants and forbs) and monocotyledons (grasses, sedges etc) with
respect to meristem position: dicotyledons have their apical meristems at the tip of their branches, vulnerable
to browsing, whereas most or all meristems on monocotyledons are basal (much less likely to be grazed)
(Hester et al. 2006a; Skarpe & Hester 2008).
Two important intrinsic physiological features promoting plant tolerance to herbivory are growth rate (slower
growing plants are in general less tolerant to herbivory because it takes longer to replace lost tissue, particularly
in resource-limited environments) and growth plasticity (the capacity to ‘release’ previously dormant buds,
modify nutrient uptake and allocation, increase photosynthetic activity, carbon uptake, growth rate etc)
(Bradshaw 1965; Coley et al. 1985; Hester et al. 2006a; Rosenthal & Kotanen 1994).
Extrinsic tolerance factors affecting plant tolerance may allow increased plant growth, nutrient uptake and/or
light acquisition following trampling or grazing damage. The most obvious extrinsic tolerance factor is soil
nutrient status (Hester et al. 2006a).
Plant responses to herbivory
Following the plant strategies described above, in which plants ‘prepare’ themselves for herbivory attacks that
might possibly occur, plants can respond to herbivory that actually has occurred in several ways, both
morphologically as well as chemically. Plants growing in seasonal environments do not generally respond at
once to herbivory occurring during the dormant season, unless the impact is severe enough to cause
desiccation and death, but generally respond to this herbivory in the following growing season. But plants
growing in seasonal environments may respond immediately to grazing/browsing taken place during the
growing season (Gill 2006; Hester et al. 2004; Senn & Haukioja 1994). Considering plant responses to herbivory,
PhD project description MSG
Page 5 of 21
it is important to take precipitation and history of herbivory into account: Diaz et al. (2007) showed that climatic
and historical contexts are essential for understanding plant trait responses to grazing, as some response
patterns are modified by particular combinations of precipitation and history of herbivory.
Morphological responses
Resprouting follows herbivory when (stored) resources are available and some buds are present that have
escaped herbivory and can be ‘activated’ for new growth (Skarpe & Hester 2008). Resprouting of shoots is
generally most intense following herbivory early in the growing season or during dormancy, as plants have more
time to compensate before the end of the growing season (Bergstrom & Danell 1995; Hrabar et al. 2009; Skarpe
& Hester 2008). When apical dominance is eliminated by removal of apical meristems in leading shoots as a
result of herbivory, many lateral shoots may develop, resulting in a plant with less height and with often more
lateral spreading branches than unbrowsed fellow specimens (Hester et al. 2004; Makhabu et al. 2006). High or
medium intensity twig browsing in woody species generally removes significant proportions of meristems
present, in many species resulting in fewer shoots in the following growing season. As a result there is less
competition for resources among individual shoots, and shoots can become larger and have higher nutrient
concentrations than unbrowsed ramets (Bergstrom et al. 2000; Danell et al. 1994; du Toit et al. 1990; Hester et
al. 2004; Hrabar et al. 2009; Peinetti et al. 2001; Rooke et al. 2004). This may also be influenced by increased
root:shoot ratio following the browsing of shoots (Danell & Bergstrom 1989; McNaughton 1984). Increased
browsing on bilberry has been reported to increased relative light availability in the boreal forest field layer
vegetation (probably because of reduced competiton by bilberry). This increased relative light availability
resulted in an increased cover of less palatable species. These effects of browsing were modified by the
productivity gradient, leading to a higher relative increase in light availability in highly productive areas than in
low productive areas (Mathisen et al. 2010).
As a result of very intense browsing, some species respond by sprouting basal shoots from the lower part of the
stem (Bond & Midgley 2001). Removal of flowering stems prevents flowering and seed production, thus
favouring unpalatable species and species that reproduce vegetatively over those that do not, and favouring
perennials over annuals. Removal of other parts of the plant can also lead to reduced flowering or size/number
of seeds as a result of reduced resources available (Hartley & Jones 2009; Mathisen et al. 2010). Browsing is
reported to induce development of bigger leaves (increased leaf area) (Bergstrom et al. 2000; Peinetti et al.
2001). Specific leaf area (leaf area per unit dry weight) is increased because of the production of thinner leaves.
This increase might be less in nitrogen-rich soils, as specific leaf area is reported to be highest when soil
nitrogen content is low (Bouriaud et al. 2003).
Browsing removing little biomass (as small-scale, low-intensity defoliation by insects) might have no significant
impact on plant morphology (leaf and shoot size and shoot density) or result in decreased shoot and leaf size
(Ferwerda et al. 2005; Hrabar et al. 2009). For small-scale, low-intensity browsing (removal of little biomass) the
effect of natural browsing on leaves and experimental defoliation by a researcher might be different (Ferwerda
2005; Hrabar et al. 2009).
Also, we must be aware of the limitation of short-term studies with respect to morphological responses of
plants to herbivory: compensatory responses in woody plants may take several years to develop, and that
consequences of herbivore damage to individual modules may profoundly differ from whole-plant responses.
Therefore, short-term studies using branches or ramets as experimental units are likely to underestimate the
tolerance of woody plants to herbivory (Haukioja & Koricheva 2000).
Nevertheless, net primary production can be influenced by herbivory, following changes in morphological
characteristics of the plant as number and size of annual shoots, leaves, specific leaf area and changes in
generative reproductive effort (number of flowers/ berries), dependant on browsing intensity.
Chemical responses
Following the plant defense strategies described above, several chemical responses to herbivory might occur.
Plants that are adapted to resource-limited environments are expected to be highly defended (Growth Rate
Hypothesis) with carbon-based secondary metabolites (Carbon-Nutrient Balance Hypothesis) and, when
attacked by herbivores, these plants might respond by an increase in defense compounds (‘induced defense’:
PhD project description MSG
Page 6 of 21
following the Optimal Defense Hypothesis) when the remaining photosynthetic tissue allows for this (so, when
the amount of biomass removed is relatively small as is the case with, for instance, little browsing by insects or
voles), according to the Growth-Differentiation Balance Hypothesis. When these plants suffer great biomass
losses, however, there is no possibility to use resources for defense purposes and the plant needs to use all
available resources for enhancing (restoring) photosynthetic capacity: growth is prioritised over defense. So, in
shoots on browsed plants the amount of defense compounds might be reduced as a result of resources being
allocated for fast growth at the expense of defense, and/or as a result of the breakdown of existing defense
compounds and their components subsequently used for growth (Coley et al. 1985).
Plants (as, for instance, bilberry) that are adapted to relatively resource-limited conditions but within these
conditions grow at relatively productive sites, are expected to be less defended (Growth Rate Hypothesis) and
contain less carbon-based and more nitrogen-based secondary metabolites (Carbon-Nutrient Balance
Hypothesis) than plants that grow at relatively unproductive sites at resource-limited conditions. If herbivory
causes only a relatively small amount of biomass loss, these plants might respond by enhancing production of
plant defense compounds (Optimal Defense Hypothesis) (Ferwerda 2005) and/or enhancing growth (GrowthDifferentiation Balance Hypothesis). Experiments do, however, not always correspond with theory (Ferwerda et
al. 2005; Hrabar et al. 2009). When a huge amount of biomass (a large portion of the canopy) is removed by
herbivores, the root/shoot ratio of the plant is highly modified. This might lead to carbon allocation to growth
and a decrease in production of defense compounds (following the Growth-Differentiation Balance Hypothesis),
resulting in a higher nutrient content of newly grown leaves (following the Carbon-Nutrient Balance Hypothesis)
which enhances palatability (du Toit et al. 1990; Scogings et al. 2011; Skarpe & van der Wal 2002). Enhanced
palatability might be detectable by herbivores even years after a single browsing event (Makhabu & Skarpe
2006). This might result in a positive feed-back loop, possibly enhancing the development of a so-called
browsing lawn (Cromsigt & Kuijper 2011; du Toit et al. 1990; Makhabu et al. 2006; Skarpe & Hester 2008).
Vegetation composition and ecosystem effects
The responses of plants following herbivory might give rise to huge impacts on herbivores, and have been
suggested to drive small mammal cycles, and also influence vegetation composition and dynamics, by altering
competitive hierarchies between plants (interspecific competition) (Hester et al. 2006a; Hobbs 1996; Selås
2006; Skarpe & Hester 2008). The two main possible outcomes: an increase in a tolerant, highly browsed
species, or an increase in a nutrient-poor and/or highly defended (thus: unpalatable to most herbivores)
species, will not be subject of study in this PhD-project. The response time (experiments lasts for less than two
years, see further) is way too short to see any shifts in species composition.
Herbivory by small rodents can, as mentioned earlier, influence soil processes like nitrogen and carbon cycling
by changing productivity and plant species composition, which in turn can ultimately alter litter production,
nutrient cycling, and the partitioning between aboveground and belowground allocation of carbon (Persson et
al. 2009). Voles can, on the short term, increase nitrogen mineralization by depositing faeces and urine, but
they also may decrease nitrogen mobility by decreasing the biomass of high-nitrogen species (Sirotnak & Huntly
2000). Ritchie et al. (1998) term these two scenarios of herbivore-ecosystem interactions the nutrient
accelerating and nutrient decelerating scenarios, respectively. The concentrations of nitrogen in plant species
might be of crucial importance: a low nitrogen content (less than 1,5%) is postulated to result in decrease rates
of nitrogen cycling whereas nitrogen concentrations that exceed 1,5% give rise to positive feedbacks between
plants, herbivores and soil nitrogen availability that increase rates of nitrogen cycling (Pastor et al. 2006). But,
not everything is fully clear in this respect. For instance: some studies give reason to belief that nitrification
might be enhanced by vole activity, and that this effect continues after vole populations crash. More research is
needed: ‘The effects voles have on soil processes that influence carbon and nutrient cycle requires further
investigation’ (Gervais et al. 2010).
Interactions between herbivores
All these herbivory-induced responses by plants, vegetation and ecosystems imply interactions between
herbivores that are mediated by modification of habitat (e.g., cover for small mammals) and/or food
availability/quantity and/or quality, facilitation or inhibition (Bakker et al. 2009; Saetnan & Skarpe 2006; Smit et
PhD project description MSG
Page 7 of 21
al. 2001; Van de Koppel & Prins 1998). Such interactions may be related to different influences on plant
chemistry (see before) and to different nutritive requirements by small- (e.g. voles) and large-bodied (e.g.
moose) herbivores and by ruminants (e.g. moose) and non-ruminants (hind-gut fermenters, e.g. voles) (this is
not subject of this PhD-project) (Duncan & Poppi 2008; Sneddon & Argenzio 1998; Vispo & Hume 1995).
Questions and hypotheses
In this project we are mainly focusing on the following four research questions (Q) and corresponding
hypotheses (H):
1. Q1:
What are the effects of different intensities of vole browsing on bilberry, at different levels of
resource availability?
This research question is split up into three subquestions:
Q1a: what is the chemical response of bilberry to different intensities of vole browsing, at
different levels of resource availability?
Q1b: what is the morphological response of bilberry to different intensities of vole browsing, at
different levels of resource availability?
Q1c: what is the effect of different intensities of vole browsing on bilberry litter production and
soil mineralization, at different levels of resource availability?
Corresponding hypotheses:
H1.0: The null hypothesis is that there is no chemical nor morphological response of bilberry to
different intensities of vole browsing. Also there is no effect on bilberry litter production nor on
soil mineralization.
H1a: At low browsing intensities, the concentration of defense compounds and nutritive
compounds is increased.
At high browsing intensities, nutrient concentrations of new shoots and leaves are high, and
concentration of secondary carbon based metabolites is low.
At a low resource availability level, concentration of defense compounds will be low.
At an intermediate resource availability level, concentration of defense compounds will be
high (unless browsing intensity is high enough to prohibit the remaining photosynthetic
tissue to allow for production of defense compounds: in this situation, resources are
allocated for growth at the expense of defense).
When resource availability is high concentration of defense compounds will be low.
H1b:
H1c:
At high browsing intensities, length of new shoots, area of leaves and specific leaf area are
large and number of shoots and of flowers/seeds is low. Total shoot biomass decreases with
browsing intensities. When browsing occurs at the top of the stem plant height is reduced
and plant cover (as a result of an increase in number of lateral branches) is high.
Litter mass per total aboveground plant mass decreases with increasing level of browsing.
Litter nutritive quality is not affected by browsing, or litter nutritive quality decreases with
increasing level of browsing. Soil mineralization rate follows the same patterns.
PhD project description MSG
Page 8 of 21
2. Q2:
What are the differences in morphological and chemical (both defense and nutritive
compounds) responses in bilberry to simulated browsing by insects, voles and moose?
H2.0: The null hypothesis is that there are no differences in morphological and chemical (both
defense and nutritive compounds) responses in bilberry to simulated browsing by insects, voles
and moose.
H2a: There are differences in response which are a result of two differences between browsing
bilberry by insects, voles and moose:
1. the amount of biomass these herbivores consume: when a small amount of biomass
is lost to the plant, the concentration of defense compounds and nutritive
compounds is increased. When a huge amount of biomass is lost to the plant (great
disturbance of root-shoot ratio), the production of carbon based secondary
metabolites (including defense compounds) is low and nutrient concentration is high
(promoting growth).
2. the way these different herbivores browse on bilberry. Defoliation by insects leads to
loss of just a relatively small portion of aboveground biomass of the plant, resulting
in an increase in the concentration of defense compounds and nutritive compounds.
Annual shoot browsing and shoot/stem browsing by voles and moose, respectively,
can result in a much greater loss of tissue and subsequently a greater change in the
root/shoot ratio of the plant. This results in a low concentration of carbon based
secondary metabolites (including defense compounds) and a high concentration of
nutrients.
See H1b for morphological responses (and note that browsing of the top of the stem is
unlikely to happen with insect browsing).
3. Q3:
Is there a difference in morphological and/or chemical response to browsing between
bilberry plants originating from relatively nutrient poor sites and plants originating from
relatively nutrient rich sites? If such a difference exists, does adding of nutrients affect this
difference?
H3.0: The null hypothesis is that there is no difference in morphological and/or chemical response to
browsing between bilberry plants originating from relatively nutrient poor sites and plants
originating from relatively nutrient rich sites.
H3a: Plants that originate from relatively nutrient-rich sites will have lower levels of defense
compounds and higher levels of nutrients than plants from less productive habitats. This
higher level of nutrients results in a stronger/faster morphological response on browsing. We
expect bilberry plants originating from relatively nutrient rich sites to have a higher possible
resource uptake rate compared to populations evolved under low resource availability.
Adding nutrients will therefore result in a stronger response on browsing in these plants than
in plants originating from less productive habitats.
PhD project description MSG
Page 9 of 21
4. Q4:
Is there an effect of previous browsing on vole preference for bilberry?
H4.0: The null hypothesis is that there is no effect of previous browsing on vole preference for
bilberry.
H4a: Vole browsing is negatively related to previous little browsing (small amount of biomass lost
to the plant: high concentration of defense compounds, see H2) and positively related to
previous medium/heavy browsing (medium/high amount of biomass lost to the plant:
medium/low concentration of defense compounds whereas nutrient concentration is
medium/high, see H2).
There is more vole browsing on bilberry plants that have evolved on a location with
‘skogbonitet’ 17 than on bilberry plants that have evolved on a location with ‘skogbonitet’
8. There is more vole browsing on bilberry plants that grew on soil with added nutrients at
the time of previous browsing than on bilberry plants that grew on soil without added
nutrients at the time of previous browsing.
Methods
To answer the research questions that are outlined before, two different kinds of experiments are conducted in
this project: a field experiment with bank voles and browsing effects on the vegetation (particularly bilberry)
and an experiment under controlled conditions where bilberry is subject to different modes and different
intensities of simulated browsing: a clipping experiment. Besides these experiments, a baseline study at the
Skytefeltet area is continued (started in 2010 as part of the BEcoDyn project). This study gives information
about the relation between mammal browsing (shoot browsing, mainly in wintertime) and subsequent insect
herbivory (leaf browsing in spring/summertime) for different plant species in the boreal forest (particularly
bilberry), and their relation with soil mineralization (related to reseach questions 1. and 4.).
Experiments:
1. Bank vole browsing on bilberry.
2. Simulated insect-vole-moose browsing on bilberry.
3. Cafeteria test with bank vole and bilberry.
Observations:
4. Mammal-insect browsing on boreal forest vegetation (mainly bilberry) at Skytefeltet.
Ad 1. Bank vole browsing on bilberry.
This field experiment is about bank vole browsing on boreal forest vegetation with at least 40 procent cover of
bilberry. This experiment is conducted at Vinjevegen and Gålavegen, in the boreal forest west of the river Glåma
between Evenstad and Koppang at an altitude between 350 and 700 meter.
At eight sites along a productivity gradient (based on forestry ‘bonitet’, later refined by soil analyses) four plots
(each with an area of circa 18 square meter) are established: a control plot with naturally fluctuating vole
densities, a plot with no voles, a plot with a constant low vole density and a plot with a constant high vole
density. Except for the control plot, all plots are made by erecting round enclosures with metal sheets that are
circa 40-50 cm up from ground level and stick 10-20 cm into the ground. Low vole density and high vole density
is simulated by introduction of voles into the enclosed plots, on a regular basis (every 24 days) and each time
for just a short period (5 days). Data analyses on the vegetation and soil is done inside the plots, in a circular
area with an area of circa 7 square meter to avoid edge effects. Response variables (effects of browsing) include
soil mineralization, plant species composition, height and signs of previous browsing of all plant species. For
bilberry, several other response variables are also measured: morphological variables such as number and size
PhD project description MSG
Page 10 of 21
of annual shoots and specific leaf area, leaf litter and also reproduction (number of flowers/berries) and
secondary metabolites (defense compounds) and nutritive compounds. Some of these response variables are
measured at the start of the experiment and all of them are measured at the end of the experiment. After each
period of grazing by bank vole(s) in some of the enclosures, in all plots the following response variables are
measured on bilberry: signs of recent (new) browsing, the length of the shoot that is left at newly browsed
shoots (as an indication of the amount of biomass that is consumed) and leaf chemistry (‘fast response’; only
small samples are taken for chemical analyses in order not to disturb the plot).
The experiment starts end of August 2012 and lasts until end of 2013 (when the snow cover is too thick to run
the experiment).
With at least five different productivity levels we meet the requirements to determine intraspecific patters of
plant response along a resource gradient (figure 2. in Stamp 2003).
Ad 2. Simulated insect-vole-moose browsing on bilberry.
From two different productivity sites (bonitet 14 and bonitet 8 at Gålavegen) bilberry plants have been
translocated to Evenstad for a clipping experiment in 2013, after they have established and survived the winter
2012-2013. A total of 800 plants (400 from each productivity site) has been planted in plant nursery bags. These
bags (12 liter) have been filled with a mixture of gravel, rhododendron-soil and sphagnum-soil to get a good
acidity and nutrient content that more or less resemble soil acidity and nutrient status in the natural habitat of
bilberry. Shade nets have been put up above the plants, to prevent too much direct sunlight from damaging the
plants. Different intensities of browsing by insects (defoliation), voles (clipping of current season’s shoots) and
moose (removal of a great portion of the canopy) are simulated under nutrient-poor and nutrient-enriched
treatments. Different intensities of browsing are simulated by clipping 10, 50 and 100 percent of all leaves
(insect browsing) and all current season’s aboveground shoots (vole browsing). For simulated moose browsing,
10 percent, 50 percent and 90 percent of the canopy is removed. Removing all the aboveground biomass would
be unnatural as moose don’t graze bilberry til ground surface. Besides this, clipping all aboveground tissue
greatly increases the risk of mortality to the plant (or, no visible or measurable response within several weeks,
which yields the same results as mortality).
Response variables (effects of clipping) include morphological variables such as height of the plant, number and
size of annual shoots (both before and after simulated browsing), internode length, specific leaf area, weight of
clipped material, weight of roots, aboveground plant biomass, reproduction (number of flowers/berries) and
secondary metabolites (defense compounds) and nutritive compounds in leaves and annual shoots. Possible
signs of natural browsing (most likely insect browsing) are recorded as well.
The plants have been transplanted at the beginning of July 2012. The fertilization experiment starts early 2013,
after the frost has left the soil. Simulated browsing experiments start May-June 2013 (after the new season’s
shoots have been growing for some weeks) and plants are harvested end of July-beginning of August 2013,
before leaves start to senesce.
Ad 3. Cafeteria test with bank vole and bilberry.
After experiment 2 has been terminated and all the measurements are done, bilberry stems/shoots (with
leaves) from all treatments and control plants are collected and stored frozen to be used in a ‘cafeteria test’
(see f.ex. Pedersen et al. 2011; Rousi et al. 1990). Preferences for bilberry tissue from the different treatments
are tested by conducting a pair-wise experiment. Bilberry stems from two different treatments are put into one
test at the same time (after they have been thawed). A total of five bank voles (as similar to each other as
possible) is used to test preferences for each pair-wise set of bilberry stems. Each vole is used for each test, one
by one. So each vole does every preference test. If the amount of plant material that’s available from
experiment 2, number of caught voles and time permits, ten bank voles are used for the cafeteria test: five
adult males and five adult females.
This experiment runs in winter 2013 and/or spring 2014.
PhD project description MSG
Page 11 of 21
Ad 4. Mammal-insect browsing on boreal forest vegetation (mainly bilberry) at Skytefeltet.
Vegetation composition (and cover) and browsing/grazing analyses are conducted in permanent quadrats in
2011, 2012 and 2013 in the Skytefeltet area. Besides these analyses, soil mineralization analyses have been
conducted in 2011 as well. This project is part of the ‘baseline study’ at Skytefeltet, being part of the BEcoDyn
project (Andreassen & Dietrichs 2011). Data from 2011 and 2012 (vegetation survey of 384 quadrats at
Skytefeltet) will be combined and analysed on the relation between mammal browsing (mainly shoot browsing)
and subsequent insect herbivory on leaves. Next to other plant species that grow in the boreal forest in
southeastern Norway, bilberry is the main plant species that is studied in this project. Preferably, data from the
field season 2013 will also be used in the data analyses.
Vegetation observations have been conducted in or are scheduled for July and August 2011, 2012 and 2013.
Sampling for soil mineralization analyses have been conducted in 2011.
Time schedule
‘rough approximate planning’
Period
Experiment (nr.)
2012
January-March
April-June
July-September
October-December
Reading/ analyzing/writing
X
1,4
1
X
X
X
Misc
start in Evenstad May 1st
IRSAE, several courses
several courses
2013
January-March
April-June
July-September
October-December
X
X
1,2
1,2,4
1,3
X
X
X
X
X
3
X
4
(X)
X
X
X
X
X
X
(X)
X
X
several courses
several courses
seminar?
submit paper nr. 1
2014
January-March
April-June
July-September
October-December
submit paper nr. 3
submit paper nr. 4;
seminar?
submit paper nr. 2
2015
January-March
April-June
July-September
October-December
X
complete
thesis/dissertation
contract ends April 30th
drink beer
find a job
All time periods and activities are indicative!
PhD project description MSG
Page 12 of 21
Publications
We expect the experiments and observations described above to yield enough data for the following five
publications (dependant on the results). In every publication, some plant defense theories and/or theory on
plant morphology in relation to browsing will be discussed. Time may allow only four out of five publications to
be written during this PhD project. If this turns out to be the case, the decision which one to delay depends on
the data gathered.
1. Insect herbivory in relation to previous mammal browsing. Results of three year vegetation survey of
384 quadrats at Skytefeltet.
This publication describes the results of the observational study at Skytefeltet, see 4. under Methods.
Main topic is browsing by insects (leaf edge nibbling, leaf mining and holes in leaves) that is influenced
by preceding browsing by mammals (stem and shoot browsing).
This publication deals mainly with research question number 4.
2. Morphological plant responses of bilberry to simulated browsing by insects, small mammals and moose.
This publication describes the results of the simulated browsing experiment, that are dealing with
morphology, see 2. under Methods. Main topic are morphological response variables (including
regrowth), as influenced by different intensities and modes of simulated herbivory (clipping
experiment).
This publication deals mainly with research question number 2. and number 3.
3. Chemical plant responses of bilberry to simulated browsing by insects, small mammals and moose:
defense compounds and nutrition levels.
This publication describes the results of the simulated browsing experiment, that are dealing with
chemistry, see 2. under Methods. Main topic are concentrations/production of both defense
compounds and nutrition compounds, as influenced by different intensities and modes of simulated
herbivory (clipping experiment).
This publication deals mainly with research question number 2. and number 3.
4. Plant responses of bilberry to browsing by bank voles: regrowth, reproduction and soil processes.
This publication deals with the results of the bank vole experiment with enclosures in the boreal forest,
see 1. under Methods. Main topics are morphological responses of bilberry, growing along a
productivity gradient, to different intensities of browsing by bank vole.
This publication deals mainly with research question number 1.
5. Influence of previous simulated herbivory by insects, small mammals and moose on palatability of
bilberry to bank vole.
This publication describes the results of the Cafeteria test, see 3. under Methods. Main topic is the
effect of previous browsing on bilberry stems and/or leaves on palatability to bank vole (if any).
This publication deals mainly with research question number 4.
PhD project description MSG
Page 13 of 21
LITERATURE
Andreassen, H. P., and P. E. Dietrichs. 2011. Project proposal: The effect of vole population cycles on the boreal forest
ecosystem dynamics. (Research institution-based strategic project - SHP). Application Number: ES493176 Project
Number: -1.
Bakker, E. S., H. Olff, M. Boekhoff, J. M. Gleichman, and F. Berendse. 2004. Impact of herbivores on nitrogen cycling:
contrasting effects of small and large species. Oecologia 138:91-101.
Bakker, E. S., H. Olff, and J. M. Gleichman. 2009. Contrasting effects of large herbivore grazing on smaller herbivores. Basic
and Applied Ecology 10:141-150.
Bangs, E. E. 1984. Summer Food-Habits of Voles, Clethrionomys-Rutilus and Microtus-Pennsylvanicus, on the Kenai
Peninsula, Alaska. Canadian Field-Naturalist 98:489-492.
Baskin, L. M. 2009. Status of regional moose populations in European and Asiatic Russia. Alces 45:1-4.
Beest, F. M. v., H. Gundersen, K. M. Mathisen, J. M. Milner, and C. Skarpe. 2010. Long-term browsing impact around
diversionary feeding stations for moose in Southern Norway. Forest Ecology and Management 259:1900-1911.
Bergstrom, R., and K. Danell. 1995. Effects of Simulated Summer Browsing by Moose on Leaf and Shoot Biomass of Birch,
Betula-Pendula. Oikos 72:132-138.
Bergstrom, R., C. Skarpe, and K. Danell. 2000. Plant responses and herbivory following simulated browsing and stem cutting
of Combretum apiculatum. Journal of Vegetation Science 11:409-414.
Bond, W. J., and J. J. Midgley. 2001. Ecology of sprouting in woody plants: the persistence niche. Trends in Ecology &
Evolution 16:45-51.
Boonstra, R., and C. J. Krebs. 2012. Population dynamics of red-backed voles (Myodes) in North America. Oecologia
168:601-620.
Bouriaud, O., K. Soudani, and N. Breda. 2003. Leaf area index from litter collection: impact of specific leaf area variability
within a beech stand. Canadian Journal of Remote Sensing 29:371-380.
Bradshaw, A. D. 1965. Evolutionary Significance of Phenotypic Plasticity in Plants. Pages 115-155 in E. W. Caspari, and J. M.
Thoday, editors. Advances in Genetics. Academic Press.
Bryant, J. P., F. S. Chapin, and D. R. Klein. 1983. Carbon Nutrient Balance of Boreal Plants in Relation to Vertebrate
Herbivory. Oikos 40:357-368.
Canadensys. 2012. VASCAN. The database of Canadian vascular plants.
Chew, F. S., and S. P. Courtney. 1991. Plant Apparency and Evolutionary Escape from Insect Herbivory. American Naturalist
138:729-750.
Coley, P. D. 1987. Interspecific Variation in Plant Anti-Herbivore Properties - the Role of Habitat Quality and Rate of
Disturbance. New Phytologist 106:251-263.
Coley, P. D., J. P. Bryant, and F. S. Chapin. 1985. Resource Availability and Plant Antiherbivore Defense. Science 230:895899.
Cromsigt, J. P. G. M., and D. P. J. Kuijper. 2011. Revisiting the browsing lawn concept: Evolutionary Interactions or pruning
herbivores? Perspectives in Plant Ecology Evolution and Systematics 13:207-215.
PhD project description MSG
Page 14 of 21
Dahlgren, J., L. Oksanen, M. Sjodin, and J. Olofsson. 2007. Interactions between gray-sided voles (Clethrionomys rufucanus)
and bilberry (Vaccinium myrtillus), their main winter food plant. Oecologia 152:525-532.
Danell, K., and R. Bergstrom. 1989. Winter Browsing by Moose on 2 Birch Species - Impact on Food Resources. Oikos 55:1118.
Danell, K., R. Bergstrom, P. Duncan, and J. Pastor 2006. Large herbivore ecology, ecosystem dynamics and conservation.
Cambridge University Press, Cambridge, UK.
Danell, K., R. Bergstrom, and L. Iedenius. 1994. Effects of Large Mammalian Browsers on Architecture, Biomass, and
Nutrients of Woody-Plants. Journal of Mammalogy 75:833-844.
Diaz, S., S. Lavorel, S. McIntyre, V. Falczuk, F. Casanoves, D. G. Milchunas, C. Skarpe, G. Rusch, M. Sternberg, I. Noy-Meir, J.
Landsberg, W. Zhang, H. Clark, and B. D. Campbell. 2007. Plant trait responses to grazing - a global synthesis.
Global Change Biology 13:313-341.
du Toit, J. T., J. P. Bryant, and K. Frisby. 1990. Regrowth and Palatability of Acacia Shoots Following Pruning by African
Savanna Browsers. Ecology 71:149-154.
Duncan, A. J., and D. P. Poppi. 2008. Nutritional Ecology of Grazing and Browsing Ruminants. Pages 89-116 in I. J. Gordon,
and H. H. T. Prins, editors. The Ecology of Browsing and Grazing. Springer Berlin Heidelberg.
Eccard, J. A., J. Pusenius, J. Sundell, S. Halle, and H. Ylonen. 2008. Foraging patterns of voles at heterogeneous avian and
uniform mustelid predation risk. Oecologia 157:725-734.
Ecke, F., O. Lofgren, and D. Sorlin. 2002. Population dynamics of small mammals in relation to forest age and structural
habitat factors in northern Sweden. Journal of Applied Ecology 39:781-792.
Fagerstrom, T., S. Larsson, and O. Tenow. 1987. On Optimal Defence in Plants. Functional Ecology 1:73-81.
Feeny, P. 1976. Plant apparency and chemical defense. Pages 1-40 in J. W. Wallace, and R. L. Mansell, editors. Biochemical
interaction between plants and insects: proceedings of the fifteenth annual meeting of the Phytochemical Society
of North America. Plenum Press, New York.
Ferwerda, J. G. 2005. Charting the Quality of Forage. Mapping and Measuring the Variation
of Chemical Components in Foliage with Hyperspectral Remote
Sensing. PhD-thesis. Wageningen Universiteit, Wageningen.
Ferwerda, J. G., S. E. van Wieren, A. K. Skidmore, and H. H. T. Prins. 2005. Inducing condensed tannin production in
Colophospermum mopane: Absence of response to soil N and P fertility and physical damage. Plant and Soil
273:203-209.
Forsman, A., and L. E. Lindell. 1997. Responses of a predator to variation in prey abundance: Survival and emigration of
adders in relation to vole density. Canadian Journal of Zoology-Revue Canadienne De Zoologie 75:1099-1108.
Fremstad, E. 1997. Vegetasjonstyper i Norge. Instituttet, Trondheim.
Gervais, J. A., S. M. Griffith, J. H. Davis, J. R. Cassidy, and M. I. Dragila. 2010. Effects of Gray-tailed Vole Activity on Soil
Properties. Northwest Science 84:159-169.
Gill, R. M. A. 2006. The influence of large herbivores on tree recruitment and forest dynamics in K. Danell, R. Bergström, P.
Duncan, and J. Pastor, editors. Large Herbivore Ecology, Ecosystem Dynamics and Conservation. Cambridge
University Press.
Goheen, J. R., F. Keesing, B. F. Allan, D. L. Ogada, and R. S. Ostfeld. 2004. Net effects of large mammals on Acacia seedling
survival in an African savanna. Ecology 85:1555-1561.
PhD project description MSG
Page 15 of 21
Goheen, J. R., T. M. Palmer, F. Keesing, C. Riginos, and T. P. Young. 2010. Large herbivores facilitate savanna tree
establishment via diverse and indirect pathways. Journal of Animal Ecology 79:372-382.
Gorini, L., J. D. C. Linnell, L. Boitani, U. Hauptmann, M. Odden, P. Wegge, and E. B. Nilsen. 2011. Guild composition and
habitat use of voles in 2 forest landscapes in south-eastern Norway. Integrative Zoology 6:299-310.
Graham, I. M., and X. Lambin. 2002. The impact of weasel predation on cyclic field-vole survival: the specialist predator
hypothesis contradicted. Journal of Animal Ecology 71:946-956.
Hanski, I., H. Henttonen, E. Korpimaki, L. Oksanen, and P. Turchin. 2001. Small-rodent dynamics and predation. Ecology
82:1505-1520.
Hansson, L. 1991. Bark Consumption by Voles in Relation to Mineral Contents. Journal of Chemical Ecology 17:735-743.
Hansson, L. 1992. Vole Densities and Consumption of Bark in Relation to Soil Type and Bark Mineral Content. Scandinavian
Journal of Forest Research 7:229-235.
Hansson, L. 1994. Bark Consumption by Voles in Relation to Geographical Origin of Tree Species. Scandinavian Journal of
Forest Research 9:288-296.
Hansson, L. 2002. Consumption of bark and seeds by voles in relation to habitat and landscape structure. Scandinavian
Journal of Forest Research 17:28-34.
Harrison, K. A., and R. D. Bardgett. 2003. How browsing by red deer impacts on litter decomposition in a native
regenerating woodland in the Highlands of Scotland. Biology and Fertility of Soils 38:393-399.
Harrison, K. A., and R. D. Bardgett. 2004. Browsing by red deer negatively impacts on soil nitrogen availability in
regenerating native forest. Soil Biology & Biochemistry 36:115-126.
Harrison, K. A., and R. D. Bardgett. 2008. Impacts of Grazing and Browsing by Large Herbivores on Soils and Soil Biological
Properties. Pages 201-216 in I. J. Gordon, and H. H. T. Prins, editors. The Ecology of Browsing and Grazing. Springer
Berlin Heidelberg.
Hartley, S. E., and C. G. Jones. 2009. Plant Chemistry and Herbivory, or Why the World is Green. Pages 284-324 in M. J.
Crawley, editor. Plant Ecology. Blackwell Publishing Ltd.
Haukioja, E., and J. Koricheva. 2000. Tolerance to herbivory in woody vs. herbaceous plants. Evolutionary Ecology 14:551562.
Henttonen, H., M. Stubbe, T. Maran, and T. A. 2008. Alces alces. In: IUCN 2012. IUCN Red List of Threatened Species.
Version 2012.1. <www.iucnredlist.org>. Downloaded on 16 July 2012.
Herms, D. A., and W. J. Mattson. 1992. The Dilemma of Plants - to Grow or Defend. Quarterly Review of Biology 67:283335.
Hester, A. J., M. Bergman, G. R. Iason, and J. Moen. 2006a. Impacts of large herbivores on plant community structure and
dynamics in K. Danell, R. Bergström, P. Duncan, and J. Pastor, editors. Large Herbivore Ecology, Ecosystem
Dynamics and Conservation. Cambridge University Press.
Hester, A. J., P. Millard, G. J. Baillie, and R. Wendler. 2004. How does timing of browsing affect above- and below-ground
growth of Betula pendula, Pinus sylvestris and Sorbus aucuparia? Oikos 105:536-550.
Hester, A. J., P. F. Scogings, and W. S. W. Trollope. 2006b. Long-term impacts of goat browsing on bush-clump dynamics in
a semi-arid subtropical savanna. Plant Ecology 183:277-290.
Hjalten, J., K. Danell, and L. Ericson. 1996. Food selection by two vole species in relation to plant growth strategies and
plant chemistry. Oikos 76:181-190.
PhD project description MSG
Page 16 of 21
Hjalten, J., K. Danell, and P. Lundberg. 1993. Herbivore Avoidance by Association - Vole and Hare Utilization of WoodyPlants. Oikos 68:125-131.
Hobbs, N. T. 1996. Modification of ecosystems by ungulates. Journal of Wildlife Management 60:695-713.
Hrabar, H., D. Hattas, and J. T. du Toit. 2009. Differential effects of defoliation by mopane caterpillars and pruning by
African elephants on the regrowth of Colophospermum mopane foliage. Journal of Tropical Ecology 25:301-309.
Hughes, N. K., E. Korpimaki, and P. B. Banks. 2010. The predation risks of interspecific eavesdropping: weasel-vole
interactions. Oikos 119:1210-1216.
Huitu, O., N. Kiljunen, E. Korpimaki, E. Koskela, T. Mappes, H. Pietiainen, H. Poysa, and H. Henttonen. 2009. Densitydependent vole damage in silviculture and associated economic losses at a nationwide scale. Forest Ecology and
Management 258:1219-1224.
Jokela, J., P. Schmid-Hempel, and M. C. Rigby. 2000. Dr. Pangloss restrained by the Red Queen - steps towards a unified
defence theory. Oikos 89:267-274.
Kays, R. W., and D. E. Wilson 2009. Mammals of North America. Second Edition. Princeton University Press.
Keesing, F. 1998. Impacts of ungulates on the demography and diversity of small mammals in central Kenya. Oecologia
116:381-389.
Kjellander, P., and J. Nordström. 2003. Cyclic voles, prey switching in red fox, and roe deer dynamics - a test of the
alternative prey hypothesis. Oikos 101:338-344.
Korpimaki, E., K. Norrdahl, and T. Rintajaskari. 1991. Responses of Stoats and Least Weasels to Fluctuating Food
Abundances - Is the Low Phase of the Vole Cycle Due to Mustelid Predation. Oecologia 88:552-561.
Kotanen, P. M., and J. P. Rosenthal. 2000. Tolerating herbivory: does the plant care if the herbivore has a backbone?
Evolutionary Ecology 14:537-549.
Krebs, C. J., S. Boutin, and R. Boonstra, editors. 2001. Ecosystem dynamics of the boreal forest: The Kluane Project.
Cambridge University Press New York, NY.
Lessard, J. P., W. N. Reynolds, W. A. Bunn, M. A. Genung, M. A. Cregger, E. Felker-Quinn, M. N. Barrios-Garcia, M. L.
Stevenson, R. M. Lawton, C. B. Brown, M. Patrick, J. H. Rock, M. A. Jenkins, J. K. Bailey, and J. A. Schweitzer. 2012.
Equivalence in the strength of deer herbivory on above and below ground communities. Basic and Applied Ecology
13:59-66.
Loomis, W. E. 1932. Growth-differentiation balance vs. carbohydrate-nitrogen ratio. Proceedings of the American Society
for Horticultural Science 29:240-245.
Lorio, P. L. 1986. Growth-Differentiation Balance - a Basis for Understanding Southern Pine-Beetle Tree Interactions. Forest
Ecology and Management 14:259-273.
Makhabu, S. W., and C. Skarpe. 2006. Rebrowsing by elephants three years after simulated browsing on five woody plant
species in northern Botswana. South African Journal of Wildlife Research 36:99-102.
Makhabu, S. W., C. Skarpe, and H. Hytteborn. 2006. Elephant impact on shoot distribution on trees and on rebrowsing by
smaller browsers. Acta Oecologica-International Journal of Ecology 30:136-146.
Mappes, T., M. Halonen, J. Suhonen, and H. Ylonen. 1993. Selective Avian Predation on a Population of the Field Vole,
Microtus-Agrestis - Greater Vulnerability of Males and Subordinates. Ethology Ecology & Evolution 5:519-527.
Mathisen, K. M., F. Buhtz, K. Danell, R. Bergstrom, C. Skarpe, O. Suominen, and I. L. Persson. 2010. Moose density and
habitat productivity affects reproduction, growth and species composition in field layer vegetation. Journal of
Vegetation Science 21:705-716.
PhD project description MSG
Page 17 of 21
Mathisen, K. M., and C. Skarpe. 2011. Cascading effects of moose (Alces alces) management on birds. Ecological Research
26:563-574.
Mattson, W. J., R. K. Lawrence, R. A. Haack, D. A. Herms, and P. J. Charles. 1988. Defensive strategies of woody plants
against different insect-feeding guilds in relation to plant ecological strategies and intimacy of association with
insects. Pages 3-38 in W. J. Mattson, J. Levieux, and C. Bernard-Dagan, editors. Mechanisms of woody plant
defences against insects: search for pattern. Springer-Verlag, New York.
Mauricio, R. 2000. Natural selection and the joint evolution of toleranceand resistance as plant defenses. Evolutionary
Ecology 14:491-507.
McKey, D. 1974. Adaptive Patterns in Alkaloid Physiology. The American Naturalist 108:305-320.
McNaughton, S. J. 1984. Grazing Lawns - Animals in Herds, Plant Form, and Coevolution. American Naturalist 124:863-886.
Menezes, R. S. C., E. T. Elliott, D. W. Valentine, and S. A. Williams. 2001. Carbon and nitrogen dynamics in elk winter ranges.
Journal of Range Management 54:400-408.
Milchunas, D. G., and I. Noy-Meir. 2002. Grazing refuges, external avoidance of herbivory and plant diversity. Oikos 99:113130.
Nestby, R., D. Percival, I. Martinussen, N. Opstad, and J. Rohloff. 2011. The European Blueberry (Vaccinium myrtillus L.) and
the Potential for Cultivation. A Review. The European Journal of Plant Science and Biotechnology 5:5-16.
Olff, H., V. K. Brown, and R. H. Drent 1999a. Herbivores Between Plants and Predators. Blackwell Science, Oxford.
Olff, H., F. W. M. Vera, J. Bokdam, E. S. Bakker, J. M. Gleichman, K. de Maeyer, and R. Smit. 1999b. Shifting mosaics in
grazed woodlands driven by the alternation of plant facilitation and competition. Plant Biology 1:127-137.
Panzacchi, M., J. D. C. Linnell, C. Melis, M. Odden, J. Odden, L. Gorini, and R. Andersen. 2010. Effect of land-use on small
mammal abundance and diversity in a forest-farmland mosaic landscape in south-eastern Norway. Forest Ecology
and Management 259:1536-1545.
Pastor, J., and Y. Cohen. 1997. Herbivores, the functional diversity of plants species, and the cycling of nutrients in
ecosystems. Theoretical Population Biology 51:165-179.
Pastor, J., Y. Cohen, N. T. Hobbs, and R. B. Kjell Danell, Patrick Duncan, John Pastor 2006. The roles of large herbivores in
ecosystem nutrient cycles
Large Herbivore Ecology, Ecosystem Dynamics and Conservation. Cambridge University Press.
Pastor, J., B. Dewey, and D. P. Christian. 1996. Carbon and nutrient mineralization and fungal spore composition of fecal
pellets from voles in Minnesota. Ecography 19:52-61.
Pedersen, S., H. P. Andreassen, I. L. Persson, R. Julkunen-Tiitto, K. Danell, and C. Skarpe. 2011. Vole preference of bilberry
along gradients of simulated moose density and site productivity. Integrative Zoology 6:341-351.
Peinetti, H. R., R. S. C. Menezes, and M. B. Coughenour. 2001. Changes induced by elk browsing in the aboveground
biomass production and distribution of willow (Salix monticola Bebb): their relationships with plant water, carbon,
and nitrogen dynamics. Oecologia 127:334-342.
Persson, I. L., K. Danell, and R. Bergstrom. 2000. Disturbance by large herbivores in boreal forests with special reference to
moose. Annales Zoologici Fennici 37:251-263.
Persson, I. L., K. Danell, and R. Bergstrom. 2005a. Different moose densities and accompanied changes in tree morphology
and browse production. Ecological Applications 15:1296-1305.
Persson, I. L., M. B. Nilsson, J. Pastor, T. Eriksson, R. Bergstrom, and K. Danell. 2009. Depression of belowground respiration
rates at simulated high moose population densities in boreal forests. Ecology 90:2724-2733.
PhD project description MSG
Page 18 of 21
Persson, I. L., J. Pastor, K. Danell, and R. Bergstrom. 2005b. Impact of moose population density on the production and
composition of litter in boreal forests. Oikos 108:297-306.
Pusenius, J., R. S. Ostfeld, and F. Keesing. 2000. Patch selection and tree-seedling predation by resident vs. immigrant
meadow voles. Ecology 81:2951-2956.
Pusenius, J., K. Prittinen, J. Heimonen, K. Koivunoro, M. Rousi, and H. Roininen. 2002. Choice of voles among genotypes of
birch seedlings: its relationship with seedling quality and preference of insects. Oecologia 130:426-432.
Richards, H. 1993. Physiology of plants recovering from defoliation. Pages 46-54 in M. Baker, editor. Grasslands for Our
World. SIR Publishing, Wellington, New Zealand.
Ritchie, M. E., D. Tilman, and J. M. H. Knops. 1998. Herbivore effects on plant and nitrogen dynamics in oak savanna.
Ecology 79:165-177.
Rooke, T., R. Bergstrom, C. Skarpe, and K. Danell. 2004. Morphological responses of woody species to simulated twigbrowsing in Botswana. Journal of Tropical Ecology 20:281-289.
Rosenthal, J. P., and P. M. Kotanen. 1994. Terrestrial Plant Tolerance to Herbivory. Trends in Ecology & Evolution 9:145148.
Roth, J. K., and S. B. Vander Wall. 2005. Primary and secondary seed dispersal of bush chinquapin (Fagaceae) by
scatterhoarding rodents. Ecology 86:2428-2439.
Rousi, M., H. Henttonen, and A. Kaikusalo. 1990. Resistance of Birch (Betula pendula and B. platyphylla) Seedlots to Vole
(Microtus agrestis) Damage. Scandinavian Journal of Forest Research 5:427-436.
Saetnan, E. R., and C. Skarpe. 2006. The effect of ungulate grazing on a small mammal community in southeastern
Botswana. African Zoology 41:9-16.
Scheper, J., and C. Smit. 2011. The role of rodents in the seed fate of a thorny shrub in an ancient wood pasture. Acta
Oecologica-International Journal of Ecology 37:133-139.
Schrijvers, M., and H. Schot-Opschoor. 1997. The effects of large mammal herbivores on small rodent density and seed
predation at National Park De Hoge Veluwe (The Netherlands). Nature Conservation and Plant Ecology Group.
Wageningen Agricultural University, Wageningen.
Scogings, P. F., J. Hjalten, and C. Skarpe. 2011. Secondary metabolites and nutrients of woody plants in relation to browsing
intensity in African savannas. Oecologia 167:1063-1073.
Selås, V. 2006. Explaining bank vole cycles in southern Norway 1980-2004 from bilberry reports 1932-1977 and climate.
Oecologia 147:625-631.
Senn, J., and E. Haukioja. 1994. Reactions of the Mountain Birch to Bud Removal - Effects of Severity and Timing, and
Implications for Herbivores. Functional Ecology 8:494-501.
Sherrod, S. K., T. R. Seastedt, and M. D. Walker. 2005. Northern pocket gopher (Thomomys talpoides) control of alpine
plant community structure. Arctic Antarctic and Alpine Research 37:585-590.
Singer, F. J., and K. A. Schoenecker. 2003. Do ungulates accelerate or decelerate nitrogen cycling? Forest Ecology and
Management 181:189-204.
Sirotnak, J. M., and N. J. Huntly. 2000. Direct and indirect effects of herbivores on nitrogen dynamics: Voles in riparian
areas. Ecology 81:78-87.
Skarpe, C. 2011. Vole Project (BEcoDyn). Field layer vegetation and browsing, how to do it. July-August 2012. Høyskolen i
Hedmark, Campus Evenstad, Evenstad.
PhD project description MSG
Page 19 of 21
Skarpe, C., and A. J. Hester. 2008. Plant traits, browsing and grazing herbivores, and vegetation dynamics. Pages 217-247 in
I. J. Gordon, and H. H. T. Prins, editors. The Ecology of browsing and grazing. Springer, Berlin.
Skarpe, C., and R. van der Wal. 2002. Effects of simulated browsing and length of growing season on leaf characteristics
and flowering in a deciduous Arctic shrub, Salix polaris. Arctic Antarctic and Alpine Research 34:282-286.
Smit, C., E. S. Bakker, M. E. F. Apol, and H. Olff. 2010. Effects of cattle and rabbit grazing on clonal expansion of spiny shrubs
in wood-pastures. Basic and Applied Ecology 11:685-692.
Smit, C., and J. L. Ruifrok. 2011. From protege to nurse plant: establishment of thorny shrubs in grazed temperate
woodlands. Journal of Vegetation Science 22:377-386.
Smit, R., J. Bokdam, J. den Ouden, H. Olff, H. Schot-Opschoor, and M. Schrijvers. 2001. Effects of introduction and exclusion
of large herbivores on small rodent communities. Plant Ecology 155:119-127.
Sneddon, J. C., and R. A. Argenzio. 1998. Feeding strategy and water homeostasis in equids: the role of the hind gut.
Journal of Arid Environments 38:493-509.
Speed, J. D. M., G. Austrheim, A. J. Hester, and A. Mysterud. 2010. Experimental evidence for herbivore limitation of the
treeline. Ecology 91:3414-3420.
Stamp, N. 2003. Out of the quagmire of plant defense hypotheses. Quarterly Review of Biology 78:23-55.
Stamp, N. 2004. Can the growth-differentiation balance hypothesis be tested rigorously? Oikos 107:439-448.
Strauss, S. Y., and A. A. Agrawal. 1999. The ecology and evolution of plant tolerance to herbivory. Trends in Ecology &
Evolution 14:179-185.
Stritar, M. L., J. A. Schweitzer, S. C. Hart, and J. K. Bailey. 2010. Introduced ungulate herbivore alters soil processes after
fire. Biological Invasions 12:313-324.
Sundell, J., O. Huitu, H. Henttonen, A. Kaikusalo, E. Korpimaki, H. Pietiainen, P. Saurola, and I. Hanski. 2004. Large-scale
spatial dynamics of vole populations in Finland revealed by the breeding success of vole-eating avian predators.
Journal of Animal Ecology 73:167-178.
Suominen, O., and K. Danell 2006. Effects of large herbivores on other fauna. Cambridge University Press.
Suominen, O., K. Danell, and J. P. Bryant. 1999. Indirect effects of mammalian browsers on vegetation and ground-dwelling
insects in an Alaskan floodplain. Ecoscience 6:505-510.
Suominen, O., I. L. Persson, K. Danell, R. Bergstrom, and J. Pastor. 2008. Impact of simulated moose densities on abundance
and richness of vegetation, herbivorous and predatory arthropods along a productivity gradient. Ecography
31:636-645.
Ure, D. C., and C. Maser. 1982. Mycophagy of Red-Backed Voles in Oregon and Washington. Canadian Journal of ZoologyRevue Canadienne De Zoologie 60:3307-3315.
USDA. 2012. Plants Database. Natural Resources Conservation Service, United States Department of Agriculture.
Van de Koppel, J., and H. H. T. Prins. 1998. The importance of herbivore interactions for the dynamics of African savanna
woodlands: an hypothesis. Journal of Tropical Ecology 14:565-576.
Van der Wal, R., R. D. Bardgett, K. A. Harrison, and A. Stien. 2004. Vertebrate herbivores and ecosystem control: cascading
effects of faeces on tundra ecosystems. Ecography 27:242-252.
Vander Wall, S. B. 2002. Masting in animal-dispersed pines facilitates seed dispersal. Ecology 83:3508-3516.
Vander Wall, S. B. 2003. Effects of seed size of wind-dispersed pines (Pinus) on secondary seed dispersal and the caching
behavior of rodents. Oikos 100:25-34.
PhD project description MSG
Page 20 of 21
Vander Wall, S. B., T. Esque, D. Haines, M. Garnett, and B. A. Waitman. 2006. Joshua tree (Yucca brevifolia) seeds are
dispersed by seed-caching rodents. Ecoscience 13:539-543.
Vehvilainen, H., and J. Koricheva. 2006. Moose and vole browsing patterns in experimentally assembled pure and mixed
forest stands. Ecography 29:497-506.
Vesterlund, S. R., O. Suominen, R. Bergstrom, K. Danell, and I. L. Persson. 2012. The impact of simulated moose densities on
conifer aphids along a productivity gradient. Ecography 35:105-112.
Vispo, C., and I. D. Hume. 1995. The Digestive-Tract and Digestive Function in the North-American Porcupine and Beaver.
Canadian Journal of Zoology-Revue Canadienne De Zoologie 73:967-974.
Zeigenfuss, L. C., K. A. Schoenecker, and L. K. Van Amburg. 2011. Ungulate Herbivory on Alpine Willow in the Sangre De
Cristo Mountains of Colorado. Western North American Naturalist 71:86-96.
PhD project description MSG
Page 21 of 21