Forestry An International Journal of Forest Research

Forestry, Vol. 84, No. 1, 2011. doi:10.1093/forestry/cpq044

Advance Access publication date: 10 January 2011

Life history strategies of aspen (Populus

tremula L.) and browsing effects: a
literature review
TOR MYKING1*, FREDRIK BHLER2, GUNNAR AUSTRHEIM3 AND
ERLING J. SOLBERG4

1
Norwegian Forest and Landscape Institute, Fanaaten 4, NO-5244 Fana, Norway

2
Norwegian Forest and Landscape Institute, PO Box 115, NO-1431 s, Norway
3
Museum of Natural History and Archaeology, Norwegian University of Science and Technology, NO-7491 Trondheim, Norway
4
Norwegian Institute for Nature Research, PO Box 5685 Sluppen, NO-7485 Trondheim, Norway

*Corresponding author. E-mail: tor.myking@skogoglandskap.no

Summary
Aspen (Populus tremula L.) is associated with high biodiversity and provides high-quality forage for wild browsing
herbivores in boreal and temperate ecosystems. The long-term persistence of aspen in many regions in Scandinavia
has been questioned due to the historically high browsing levels. We here review the basic ecology, genetics and life
histories of aspen in a browsing context. Browsers can suppress the regeneration of aspen and the relatively short
lifespan of the trees result in frequent regeneration cycles and concurrent exposure to browsers. In the long term,
browsing may reduce recruitment and delay maturation, increase mortality and ultimately cause a decline of aspen.
Norwegian forest inventory data indicate a reduced recruitment rate of young aspen (diameter at breast height; 6079
mm) during the last 25 years, but it is unclear whether this is all due to browsing. Regeneration may also be hampered
by lack of disturbance. Recent genetic studies have shown that aspen may have substantial regeneration by seeds, which
allows for effective migration. The main conclusion of this review is that although browsing may affect demography
and local abundance of aspen, it is very unlikely to lead to the eradication of the species in Fennoscandia.

Introduction
Aspen (Populus tremula) is a common species with a wide
distribution in boreal and temperate ecosystems in Eurasia.
Although its commercial importance is limited, aspen
is often found to be a keystone species due to its funda-
mental importance for other species. Large trees host hun-
dreds of herbivorous and saprophytic invertebrates, fungi
and epiphytic lichens (Kouki et al., 2004). Dead trees go
through a succession in decay in which each step is char-
acterized by specic beetles and fungi species (cf. Siitonen
and Martikainen, 1994; Kouki et al., 2004; Vehmas et al.,
2009 and references therein), and large aspen trees are im-
portant for maintaining populations of hole nesting birds,
such as woodpeckers (e.g. Gjerde et al., 2005). Aspen is
also a highly preferred winter forage species for large her-
bivores (Bergstrm and Hjeljord, 1987). During the last
six decades, the populations of large wild herbivores,
Institute of Chartered Foresters, 2011. All rights reserved. For Permissions, please email: journals.permissions@oup.com
such as moose Alces alces, red deer Cervus elaphus and
roe deer Capreolus capreolus, have increased substantially
in Norway (Austrheim et al., 2008), as well as in Sweden
and Finland (Kouki et al., 2004) and the browsing pressure
on aspen, as well as goat willow (Salix caprea) and rowan
(Sorbus aucuparia), has increased accordingly (Mnsson
et al., 2007). Thus, by inuencing the demography and
stand dynamics of aspen, large herbivores may also impact
the fate of the numerous amounts of associated species.
Worrell (1995a, 1995b) has previously reviewed the
ecology, genetics, silviculture and utilization of aspen with
particular reference to Scottish conditions, and more re-
cently, Cooke and Rood (2007 ) have given an overview
on developments in, e.g. physiology, population genetics
and ecology of poplars, but without considering the inu-
ence of browsers on the population dynamics of aspen. The
indisputable effect that large wild herbivores such as moose,
roe deer and red deer may have on the growth and survival
62 FORESTRY
of individuals of the main forage species in Scandinavia
raises a question of the consequences for aspen distribution
if the present high browsing pressure is maintained. In this
paper, we will review the basic biology of aspen including
its genetic variation and assess how basic stages in the life
history are affected by ecological interactions. Specically,
we will address how extensive browsing interacts with life
histories such as seed recruitment, seedling establishment,
vegetative reproduction, growth rate, morphology and size
of the sapling, chemical defence, seed dispersal and longevity
of aspen and how this may affect demography, local abun-
dance and regional distribution. Our focal herbivores are
large wild herbivores with a browsing (moose and roe deer)
or intermediate feeding strategy (red deer). Other disturb-
ance factors which are important for population dynamics
of aspen, such as res and forestry and more general changes
in land use and land cover, will also be considered.
Aspen biology and ecological interactions
Distribution, abundance and habitat requirements
Aspen was quick to colonize Scandinavia after the ice age, ap-
pearing already 1200011000 BP (Huntley and Birks, 1983).
Tracing glacial refugia and colonization routes is constrained
by the limited persistence of aspen pollen (Birks, 1970), but
recent genetic approaches suggest several connected refugia
close to the ice shield during the Quaternary glacial cycles
(Fussi et al., 2010). The present geographic distribution of
aspen includes most of the boreal and temperate deciduous
part of the Eurasian continent. In the east, it extends to
northern Asia and Japan, and the latitudinal range extends
from northern part of Norway at 71 N through all of
Figure 1. Geographical distribution and density of aspen (d.b.h. 50mm) in Norway (except Finnmark county in the very
north). Green indicates forested areas. Data from 13
500 sample plots (250 m2) systematically distributed below the coniferous
tree line (from the National Forest Inventory, http://www.skogoglandskap.no). Plots with no aspen are omitted.
Europe to northern Africa. The altitudinal span is also wide,
from sea level and up to 1500 m in Norway (Lid and Lid,
2005) and 1900 m in the Pyrenees (Hultn and Fries, 1986;
Worrell, 1995a). Although aspen occurs in all forested parts
of Norway, it is most abundant in coastal parts of eastern
and southern Norway (Frivold, 1994) (Figure 1).
Old aspen trees occur scattered in old-growth forests,
but aspen is primarily a pioneer species characterized
by rapid establishment on disturbed sites, rapid juvenile
growth, high light demand and relatively short lifespan
(Brset, 1960). Aspen may be a successful species in sec-
ondary successions in former disturbed habitats, such
as abandoned arable land, and may rapidly invade from
the eld edges by means of root suckers (Frivold, 1998).
It constitutes ~8 per cent of the deciduous forests in
Norway, similar to 11 million m3 which is ~9 per cent
of the biomass of B. pubescens (Kucera and Nss, 1999).
Thus, aspen occurs in the landscape as scattered individu-
als and small stands (Kouki et al., 2004). Aspen has mo-
dest requirements for summer warmth, similar to downy
birch, and is very frost hardy and drought resistant. It
occurs within a wide range of soil types, although growth
and performance is best on fertile and well-drained min-
eral soils (Worrell, 1995a). These characteristics con-
form to the general pronounced phenotypic plasticity
of the Populus genus (Cooke and Rood, 2007) and reect
exceptional wide ecological amplitude, being important
prerequisites for the extensive geographical range and early
post-glacial appearance of the species.
Regeneration
Aspen regenerates both vegetatively and by seeds, although
sexual reproduction has been stated to be of minor importance
 LIFE HISTORY STRATEGIES OF ASPEN AND BROWSING EFFECTS
(Worrell, 1995a; Latva-Karjanmaa et al., 2003). Young in-
dividuals of up to 56 years may produce coppice shoots
from stumps, but sucker shoots from shallow roots is the
most important means of vegetative reproduction, and hun-
dreds of ramets may develop from the roots of a single tree
(Worrell, 1995a). Aspen has an extensive root system, and
root suckers may arise up to 40 m from the parent trees
(Jobling, 1990). On former arable land, root suckers may
spread at a rate of 1 m per year (Frivold, 1998).
Seed production usually takes place annually in Norway
(Brset, 1960). It is dioecious, and the sex ratio reects
an excess of males in most of the distribution (male: fe-
male ratios of 2:1 in Norway, 1.81.3:1 in Scotland, to 1:1
in southern and central Italy) (Powell, 1957; Gramuglio,
1962; Worrell et al., 1999). The trees ower in spring be-
fore leaf emergence, and seeds mature 45 weeks after
owering. Both pollen and seeds are dispersed by wind
(Latva-Karjanmaa et al., 2003). Solitary trees may produce
seeds from the age of 1015 years, whereas stands rarely
produce seeds before 2030 years of age (Brset, 1985b).
Seed production capacity is pronounced. One catkin can
contain 10002000 seeds, and one tree may have as many
as 40,000 catkins (Johnson, 1942). The seeds are very
small and light, and the thousand grainmass of aspen
seeds varies from ~0.06 to 0.17 g (Fystro, 1962), which is
~2 per cent of the seed weight of Norway spruce (Fystro,
1962). As the seeds have tiny hairs, they can be transported
by wind over long distances. It has been shown that arti-
cial pollination has increased the seed production ~12-fold
over natural pollination, suggesting that pollen may be de-
cient under natural conditions (Worrell et al., 1999). The
germinability after maturation is usually high, 7095 per
cent (Fystro, 1962; Worrell et al., 1999), but even if it can
be maintained articially for several months (Worrell et al.,
1999), the viability decreases rapidly after dispersal under
natural conditions (Brset, 1954; Worrell et al., 1999).
This corresponds to the transient seed banks of aspen,
persisting in the soil for less than 1 year (Thompson et al.,
1997). The germination itself is very rapid, and could start
after lless than 24 h, with no requirement for stratication
(Brset, 1960). Another obstacle for establishment is the
lack of endosperm (Brset, 1960) which implies that the
seeds rely heavily on appropriate moisture conditions for
germination (Latva-Karjanmaa et al., 2003; de Chantal
and Granstrm, 2007). This is usually best met by mineral
soil, but scaried ground and burnt organic substrate also
provide good conditions for germination and establish-
ment (Worrell, 1995a; de Chantal and Granstrm, 2007 ).
It should be noted that the post-re reproduction may also
be facilitated by reduced allelopathic inhibition by, e.g.
Empetrum hermaphroditum which otherwise may prevent
germination in aspen (Zackrisson and Nilsson, 1992).
Stand growth and longevity
Aspen rapidly occupies available space, and studies on
trembling aspen (P. tremuluoides) have shown that max-
imum leaf area and minimum light transmission to the
63
forest oor is reached already after 1025 years (Lieffers
et al., 2002; Pinno et al., 2009). The maximum net biomass
production, which in theory coincides with the reaching of
maximum leaf area, is reported to occur after 1832 years
(Rytter and Stener, 2005). This reects the very active
juvenile growth during which the volume production per
unit area may exceed that of Norway spruce (Picea abies)
(Brset, 1985a). When averaged over the entire rotation,
however, the more shade-tolerant Norway spruce allows
for higher density and volume at similar site productivity
indices (Brset, 1985a). Under favourable conditions, tree
heights up to 25 and 34 m have been recorded for aspen
in Scotland and Norway, respectively (Oppdahl, 1992;
Worrell, 1995a).
Self-thinning in dense stands starts early and continues
at a high rate during the rst 20 years after establishment
(Langhammer and Oppdahl, 1990; Bokalo et al., 2007).
Thus, after an early peak in volume production, aspen
stands gradually reach a state of decline when mortality
exceeds growth. In trembling aspen, the timing of the
decline is unaffected by site productivity and may begin at
~60 years of age (Pothier et al., 2004). High mortality of
large aspen trees on poor sites is usually due to the high
incidence of root rot (Langhammer and Oppdahl, 1990 ;
Johansson and Lundh, 2005).
The competitive ability of aspen is highest on fertile soils
with fresh moisture conditions (Johansson 1996). Some in-
ferences about the interspecic competition of aspen can be
drawn from experiments with trembling aspen in mixture
with white spruce (Picea glauca) (Kabzems and Garcia,
2004; Tatarinov et al., 2005). The light demanding aspen
and shade-tolerant spruce may supplement each other if
they constitute separate overstorey and understorey, re-
spectively (Langhammer, 1982). Although the spruce will
eventually penetrate into the aspen canopy (Langhammer,
1982), more time is required for spruce to catch up with
aspen on high productive sites due to the exceptional
juvenile growth rate of aspen as compared to spruce
(Kabzems and Garcia, 2004).
The notion that aspen trees rarely reach more than 100
years old (Oppdahl, 1992) has recently been challenged
by comprehensive studies in Finland showing that the age
of mature aspen trees varied between 100 and 200 years
(Kuusinen, 1994; Latva-Karjanmaa et al., 2007). It has
been speculated whether certain clones of aspen can reach
ages of 60008000 years (L. Ericsson, personal communi-
cation), with the dynamic root system connecting different
ramets across time (Brring, 1988).
Genetic variation
Genetic variation can be split in adaptive variation and se-
lectively neutral variation (Ennos et al., 1998). Adaptive
variation is modied by selection, leading to phenotypic
variation. Usually adaptive variation is studied in metric
traits such as budburst, bud set and growth. By contrast,
selectively neutral variation has limited or no effect on the
phenotype and is usually studied by means of different
64 FORESTRY
DNA markers or isoenzymes (Ennos et al., 1998). These
markers can give useful information about the evolutionary
history of a species, glacial refugia, exchange of pollen and
seeds between populations and inbreeding (Young et al.,
2000). Neutral genetic markers are also indispensible for
discerning individual clones. Both types of genetic varia-
tions are needed to give a satisfactory picture of the genetic
variation of a species.
Day length is a decisive environmental cue for initi-
ation of important phenological events such as ower-
ing and growth cessation in many plant species. Aspen
was the rst tree species for which it was demonstrated
that different latitudinal populations have different crit-
ical daylengths for bud set in summer (Sylvn, 1940), and
latitudinal clines in critical daylength for growth cessation
were subsequently shown in a number of other tree spe-
cies (Hbjrg, 1978). Due to this genetically controlled
adaptation, populations at different latitudes are able to
cease growth well in advance of killing frost. Also timing
of leaf abscission, seasonal height and diameter increase
have strong adaptive divergence across latitudinal and alti-
tudinal gradients in aspen (Hall et al., 2007; Fracheboud
et al., 2009). In addition, there is usually a pronounced
variation in these traits within populations (Fracheboud
et al., 2009). Taken together, the variation among clones
and populations reported for, e.g. ushing date, tree form
and diameter growth (see Worrell, 1995a and references
therein) suggests that aspen is characterized by high adap-
tive genetic variation at the species and population levels,
typical for forest trees (e.g. Knig, 2005).
Whereas the phenotypic variability among populations
in, e.g. bud set may explain about 60 per cent of the total
variation (Hall et al., 2007), only ~1 per cent of the vari-
ation in selectively neutral genetic markers of aspen (i.e.
single-sequence repeats (SSRs), single-nucleotide polymor-
phisms ) resides between populations (Lexer et al., 2005;
Hall et al., 2007). Thus, aspen displays a high level of
gene ow, which wipes out spatial genetic structures be-
tween populations (Hamrick and Nason, 1996; Lexer
et al., 2005). Although seed dispersal is far less efcient
than pollen dispersal for overall gene ow in aspen (Lexer
et al., 2005), the lack of phylogeographic structure in
genetic markers transmitted exclusively by the seeds (e.g.
chloroplast DNA markers in angiosperms) suggests that
seed ow connected several refugia during the Quaternary
glaciations cycles in Central Europe (Fussi et al., 2010).
This phenomenon has also been observed for other boreal
tree species with extensive seed dispersal, such as Betula
pendula (Maliouchenko et al., 2007).
Although aspen regenerates both by root suckers and
seeds, it has been stated that root suckers is by far most
important on a stand scale, i.e. that many individuals may
be represented by one or relatively few clones (Worrell,
1995a; Suvanto and Latva-Karjanmaa, 2005). However,
isoenzyme studies have shown that the intrapopulation
genetic variation was relatively high (Lopez-de-Heredia
et al., 2004), implying that the inuence of individuals aris-
ing from seeds is higher than previously assumed. This con-
clusion was reinforced by Suvanto and Latva-Karjanmaa
(2005). Using high-resolution SSR markers, they showed
that the majority (70 per cent) of clones at two Finish sites
consisted of just one ramet, whereas the average clone size
was 2.1 ramets/clone, with no difference between old-
growth and managed forests. Secondly, the number of
clones identied by the SSR markers was greater than the
number estimated by morphological characters (Lopez-de-
Heredia et al., 2004; Suvanto and Latva-Karjanmaa,
2005). Similarly, most clones of trembling aspen in North
America consist of just one ramet, indicating that sexual re-
production is an important contributor to genetic variation
at the population level (Namroud et al., 2005; Mock et al.,
2008). The novel results on genetic variation and prolic
seed production in aspen (Worrell et al., 1999; Suvanto
and Latva-Karjanmaa, 2005) are in contradiction with
recent literature which state that sexual reproduction in
aspen is rare (e.g. Latva-Karjanmaa et al., 2003). Predom-
inant vegetative spread by root suckers is also incompatible
with the early post-glacial appearance of aspen (Huntley
and Birks, 1983), the lack of geographic clustering in gen-
etic markers transmitted by seeds (Fussi et al., 2010) and
the many aspen sites that necessitate colonization by seeds,
such as isolated, remote areas and islands.
Browsing in the context of life history traits
Life history traits are signicant features in the life cycle
of an organism which affect fecundity, mortality and
migration (Danell et al., 2003). Herbivores are found to
have specic effects on different traits in the life histories of
forage plants which affect their demography, local abun-
dance and regional distribution (Hester et al., 2006). We
will here use life history traits as an entry to evaluate the
impact of browsing on the long-term viability of aspen.
The life history traits, species-specic characteristics for
aspen and the predicted effect of browsing on aspen are
summarized in Table 1.
Recruitment and seedling establishment
Regeneration is a critical stage of a species life cycle, but
the actual effect of browsing on regeneration of aspen in
Scandinavia is not consistent across studies. Contrary to
expectations, a short-term experimental exclosure study
in northern Sweden revealed no effect of moose browsing
(0.85 moose km2) on recruitment and mortality of aspen
(Zakrisson et al., 2007), and 4 years was suggested to be
too short to detect effects of the exclosures. In the same
area and with similar moose densities, which caused signi-
cant browsing damages, the size distribution of aspen did
still t to a reversed J-shaped distribution which ensures
recruitment of future seed trees (Ericsson et al., 2001).
There is little doubt, however, that a high density of
browsers restricts and in some places totally hinders re-
cruitment of aspen trees in typical winter ranges of moose
in Fennoscandia (Table 1) (Andrn and Angelstam, 1993;
Shipley et al., 1998; de Chantal and Granstrm, 2007;
Edenius and Ericsson, 2007; Van Bogaert et al., 2009).
 LIFE HISTORY STRATEGIES OF ASPEN AND BROWSING EFFECTS 65

Table 1: Life history traits of aspen and the predicted effects of browsing

Trait Characteristic Predicted effects of browsing Reference

Vegetative recruitment Strong Poor recruitment of (Andrn and Angelstam, 1993;
young aspen cohorts Baker et al., 1997; Ericsson et al.,
2001; Kouki et al., 2004; Wooley
et al., 2008)
Seedling recruitment Variable Trampling positive for (Hester et al., 2000; Danell et al.,
germination, but may 2003)
increase seedling mortality
Growth rate High Reduced growth rate due (Stevens et al., 2007; Halofsky et al.,
to browsing, and indirectly 2008)
due to cost of chemical
defence (see below)
Morphology Apical dominance Suspension of apical (Andrn and Angelstam, 1993;
dominance, reduced Baker et al., 1997; Danell et al.,
leader growth 2003)
Tree size Small large Accumulation of small (Ericsson et al., 2001; Kouki et al.,
(30 m height) trees (<34 m) within 2004)
the reach of browsers
Seed production High production, Less recruitment results (Johnson, 1942; Ericsson et al., 2001)
and dispersal efcient dispersal in less seed production
and migration
Chemical defence Inducible defence, Rapidly induced resistance, (Hwang and Lindroth, 1997; Glynn
genetic variation long-term selection of et al., 2003; Stevens and Lindroth,
in chemical resistance resistant clones, reduced growth 2005; Bailey et al., 2007)
Longevity Short lived (i.e. usually Reduced longevity of ramets (Baker et al., 1997; Ericsson et al.,
less than 100 years) 2001)

According to Andrn and Angelstam (1993), moose
densities of 24 individuals km2 will totally prevent
aspen saplings from growing into a tree (cf. Abaturov
and Smirnov, 2002). It is not surprising, therefore, that sur-
veys of aspen demography in heavily browsed conservation
areas in Finland have shown an almost absence of young
aspen cohorts (5 cm < diameter at breast height (d.b.h.) < 15
cm), despite the more common presence of saplings (d.b.h.
<5 cm) (Kouki et al., 2004). Similarly, in a winter foraging
area in southern Finland regeneration of aspen was abun-
dant in height classes up to 100 cm, but there were no trees
taller than 2 m (de Chantall et al., 2009). Data from the
National forest inventory in Norway indicate a similar de-
cline in the overall number of young aspen (e.g. d.b.h. =
6079 mm, Figure 2).
Aspen in these diameter classes are typically between
5 and 10 m tall, i.e. above reach of moose and deer, but
are likely to have been within browsing height some 1025
years earlier (Solberg et al., 2010). This corresponds with
the period of peak population density of moose in Norway
(Lavsund et al., 2003), indicating that the younger cohorts
recorded in the survey have been exposed to substantially
higher browsing pressure when saplings than the older co-
horts. However, because aspen may be browsed at even
the smallest height classes (<1 m), more survey cycles are
needed before we observe the full extent of ungulate brows-
ing on aspen recruitment in Norway. In this context, also
the potential interaction between forestry and browsing
should be considered, i.e. because of increasing browsing
pressure the level of mechanical cleaning (or spraying) of
deciduous trees may have been reduced. Since the introduc-
tion of clear cutting in Norway in the 1950s (e.g. Rolstad
et al., 2002), much effort has been invested in providing
young coniferous stands with optimal growth condition
(see below). Hence, aspen may for long have experienced
poor recruitment conditions in managed forests. A posi-
tive side effect of browsing for establishment is that the
trampling scaries the soil and creates germination sites for
seeds (Persson et al., 2000). However, the same trampling
can be negative for established seedlings and may increase
seedling mortality (Hester et al., 2000; Danell et al., 2003).
Growth rate, size and morphology
Browsing may affect growth in different ways. Firstly,
moose may directly suppress the growth of aspen trees
up to at least 34 m of height (Ericsson et al., 2001; den
Herder et al., 2009), and the rapid growth which may ini-
tially surpass a metre per year (Brset, 1956; Worrell
et al., 1999), is crucial to escape quickly from the brows-
ers (Table 1). Suckers are supplied with nutrients from the
parents root system and may thus exceed the critical brows-
ing height in just 23 years under good growing conditions
(Brset, 1956). Secondly, browsing may suspend the apical
dominance which leads to excessive branching, and at least
temporarily, arrested height growth (Andrn and Angelstam,
1993; Baker et al., 1997). The implication of this physio-
logical response could be that once browsed, a ramet will have
a lower probability of developing into a mature tree (Baker
et al., 1997). On average, there is a loss of growth equivalent to
66 FORESTRY

Figure 2. Abundance of aspen distributed on diameter at breast height, d.b.h. (e.g. d.b.h. 60 = 6079 mm, d.b.h. 320 = 320500 mm)
in four inventory cycles (6: 19861993, 7: 19941998, 8: 20002004, 9: 20052009). Data from 14 605 permanent sample
plots (n = 11
293 tree observations) surveyed in all cycles. Abundance is the sum of trees per hectare per plot. Number per plot
was scaled to trees per hectare to adjust for varying plot size (100250 m2) in different cycles. Trees of d.b.h. 6079 mm are
typically 510 m high (mean = 7.5 m) and thus with most twigs above reach of ungulates. Data from the National Forest
Inventory (http://www.skogoglandskap.no).

29 years for aspen after exposure to intense moose brows-
ing (Nslund, 1986). Finally, chemical resistance induced by
herbivory (see below) comes at a cost to growth (Osier and
Lindroth, 2006; Stevens et al., 2007). Thus, growth responses
to herbivory go far beyond the metric loss of biomass and
exemplify the trade-off between rapid growth out of reach of
browsers and induced chemical defence.
Seed production and dispersal
Browsing may delay and constrain recruitment of new
cohorts of parent trees (Linder et al., 1997; Ericsson et al.,
2001) with the consequence that the overall pollen and seed
production is reduced (Table 1). As articial pollination ex-
periments have shown that seed production in aspen is sen-
sitive to pollen abundance (Worrell et al., 1999), a side effect
of lower density of mature male trees could be low pollen
concentration, which might limit seed production addition-
ally. Reduced seed dispersal at the local and regional level
could affect the capability of colonizing new habitats.
Chemical defence
Trembling aspen (P. tremuloides) has served as a useful
model species for herbivore plant defence interaction
studies (Table 1). The European aspen (P. tremula) and
trembling aspen readily hybridize (Frivold, 1994), and
the defence responses found in trembling aspen could
also be present in European aspen. In response to arti-
cial defoliation, trembling aspen shows increased levels
of anti-herbivore chemicals such as tannins and phenolic
glycosides, and there are also estimates of high heritability
and genetic variation among clones both for induced and
constitutive levels for these allochemicals (Hwang and
Lindroth, 1997; Stevens et al., 2007). Along with these
experimental results, it has been shown that the North
American elk prefers to feed on some clones over others
and that the preferred clones have relatively low phen-
olic glycoside concentrations (Bailey et al., 2007; Wooley
et al., 2008). Although chemical defence does not seem
to give protection from herbivory at high elk densities
(Wooley et al., 2008), it has been speculated whether
browsing can shape the genetic structure of future aspen
populations owing to the substantial genetic component
in the concentrations of the anti-herbivore chemicals
(Bailey et al., 2007). Recognition of the widespread sexual
reproduction in aspen (Worrell et al., 1999; Suvanto and
Latva-Karjanmaa, 2005) is certainly a prerequisite for the
genetic variation at small spatial scales and for effective
selection of possible resistant clones.
Longevity
The rather short life span of aspen ramets (Worrell, 1995a)
necessitates frequent regeneration cycles and establishments
 LIFE HISTORY STRATEGIES OF ASPEN AND BROWSING EFFECTS
per time unit, during which recurrent browsing may pro-
hibit or delay the development and eventually increase
mortality of the recruits (Baker et al., 1997; Danell et al.,
2003). Thus, longevity of ramets <34 m may be reduced
with high moose densities (Ericsson et al., 2001). Browsing
may also reduce longevity of mature trees following bark
stripping and wounding (Baker et al., 1997; Kay, 1997).
Despite the indisputable effect of browsing on ramets
(Table 1), the effect on individual clones is less obvious.
Clones which can consist of hundreds of widely spaced
ramets (Jobling, 1990; Worrell, 1995a), have the potential
of getting very old (Brring, 1988; L. Ericsson, personal
communication) and be an important source of re-sprouts
far beyond the normal lifespan of a ramet. Thus, although
the abundance of aspen is inuenced by browsers, prolic
vegetative regeneration implies that longevity per se is not
a straightforward term in the case of this tree species.
Other disturbance factors
Fire
As a pioneer species, establishment of aspen depends on
disturbance that scaries the soil and thereby improves
the water availability during germination, conditions
which are often met after forest res (Worrell, 1995a;
Latva-Karjanmaa et al., 2003). Fires also greatly enhance
sucker regeneration (Baker et al., 1997). Thus, forest res
are regarded as a crucial component for maintaining the
dynamics of boreal forests. When res are suppressed,
recruitment of pioneer species such as Scots pine and aspen
declines, whereas the age distribution of competitors in the
long term (i.e. climax species) such as Norway spruce may
have abundant seedling regeneration (Linder et al., 1997).
Lack of natural disturbance may therefore change the tree
composition towards dominance of spruce (Zackrisson,
1977; Kouki et al., 2004). The highest re frequencies
recorded in Sweden had a re interval of ~30 years, and
the forests were dominated by birch and aspen (Essen
et al., 1997). During the last two centuries, however,
efcient re suppression has almost eliminated res as a
rejuvenating factor in the forests of Sweden and Finland
(Zackrisson, 1977; de Chantal et al., 2005). The situ-
ation in Norway appears similar. During the last 120130
years, forest res have been a minor contributor to disturb-
ance, and although the documentation is limited, res ap-
peared to be more common prior to the mid-19th century
(yen, 1998). An important implication is that old-growth
forests in which res are suppressed may be incapable
of sustaining viable populations of aspen. In such forests,
existing groups and individual aspen trees are usually
a legacy of previous res or other disturbance episodes,
such as windthrow (de Chantal and Granstrm, 2007;
Latva-Karjanmaa et al., 2007).
Forestry
Because of low economic value and tendency of aspen suck-
ers to prevent regeneration of more valuable tree species,
67
the forestry in much of Fennoscandia has been combating
aspen mechanically (Latva-Karjanmaa et al., 2007) and by
herbicides during 19501980 (stlund et al., 1997; Latva-
Karjanmaa et al., 2007). For disease prevention, it has also
been removed as a host of Melamsora pinitorqua, a rust
disease of young pine stands (stlund et al., 1997). More-
over, a clear-cutting regime where old-growth forests are
replaced by young, even aged conifers is often incapable of
maintaining large seed trees of aspen (Essen et al., 1997;
Latva-Karjanmaa et al., 2006), but may be an important
source of disturbance. Thus, a strict hands-off regime
maintains the big trees, but provides limited disturbance for
regeneration, whereas managed forests may provide com-
parably good conditions for regeneration by scarication
of the soil, but implies often removal of the mature trees.
Clear cuts provide enhanced biomass of herbaceous and de-
ciduous vegetation, which is attractive fodder for ungulates
and therefore signicantly affects the foraging behaviour
(Kuijper et al., 2009). The indirect effects of forestry may
be decisive for the browsing ecology of ungulates, which in
turn affect distribution and abundance of aspen. In Norway,
certain standards for forest management (Levende skog;
http://www.levendeskog.no) were approved by forestry
stakeholders and environmental organisations in 1998 to
secure a sustainable forestry, including a signicant pro-
portion of deciduous trees, maintenance of old big trees
and conservation of forest genetic resources. According to
the Forest inventory, there is an increasing number of large
aspen trees in Norwegian forests (Figure 2), but it is not clear
to what extent this can be attributed to the management
standards. Nonetheless, the standards will probably be
important for maintaining aspen trees in the future, once
they are sufciently large to escape from browsing.
Windthrow
Windthrown trees may offer both scaried ground which
facilitates germination and establishment (Brset, 1960;
Worrell, 1995a) and physical protection against browsers (de
Chantal and Granstrm, 2007). Under the shelter provided by
dead wood aggregations following re and windthrow, aspen
seedlings may grow several times higher than in open areas
(de Chantal and Granstrm, 2007). The risk of windthrow
depends on a number of interacting factors, such as species,
soil conditions and stand-related characteristics. Increasing
age and height of a stand enhance the risk of uprooting (Ruel,
1995). The increased incidence of extreme storms which is
expected by the end of the century suggests that the frequency of
windthrow may increase in northern Europe (Venalainen et al.,
2004; Schlyter et al., 2006). The increasing age and height of
the major forest trees in Norway (Larsson and Hylen, 2007)
may enhance the windthrow frequency and improve the con-
ditions for germination and regeneration of aspen.
Changes in land use and land cover
Woody encroachment in semi-natural habitats formerly
grazed by livestock or used for haymaking or fuel-wood
68 FORESTRY
cutting is evident all over Europe (CORINE Land Cover;
http://www.eea.europa.eu/publications/COR0-landcover),
including Norway (Moen, 1998; Fjellstad and Dramstad,
2005; Fjellstad et al., 2007). At the regional scale, especially
coastal outlying land is expected to be exposed to encroach-
ment due to a 50 per cent biomass reduction of large domestic
herbivores from 1949 to 1999 (Austrheim et al., 2008). In
the inland and alpine region, the strong decrease of livestock
grazing was compensated for by an almost similar increase
in browsing and grazing by wild ungulates in the same pe-
riod. However, total herbivore pressure reached a minimum
in the 1960s at a time when also haymaking had ceased in
Norway and before the wild herbivores started to increase
in the early 1970s (Austrheim et al., 2008). These land-use
changes have opened for secondary succession that pioneer
shrubs and trees such as aspen are expected to benet from
(Frivold, 1998), which in turn may have contributed to the
density increases and range expansion of wild ungulates.
Conclusions
There is no doubt that regeneration of aspen can be strongly
hampered at high herbivore densities (Andrn and Angel-
stam, 1993; Shipley et al., 1998). The short lifespan of aspen
ramets implies that the regeneration cycle vegetative, sexual
or both has to be repeated relatively frequently, with a con-
current possibility for browsers to interfere with growth and
development. The consequence could be what we currently
observe by the decline in the smallest age classes of aspen in
Norway (Figure 2). Indeed, North-American studies suggest
that heavy and persistent browsing by elk and other ungulates
can cause substantial decline and possibly even eradication
of clones of trembling aspen (Baker et al., 1997; Kay, 1997;
White et al., 1998). These strong effects seem rst of all to
appear in areas where large predators have been extirpated or
displaced (e.g. Beschta and Ripple, 2009), which is currently
also the situation in most of Norway. Thus, unless human
harvesting can fully compensate for the lack of predation by
large carnivores in Norway, the recruitment rate and abun-
dance of aspen may decrease both at the local and regional
levels, particularly in easily accessible areas. Nonetheless, the
rapid juvenile growth of aspen (Brset, 1956) implies that
aspen can grow out of reach of browsers in 23 years, and
the possible extensive longevity of clones reduces the need for
frequent seed years and may ensure population viability des-
pite periods of heavy browsing and poor regeneration oppor-
tunities. An important message from recent research is that
the regeneration by seeds is more widespread than previously
assumed (Worrell et al., 1999; Suvanto and Latva-Karjan-
maa, 2005), which is decisive for effective migration, e.g. to
areas less attractive to browsers. Thus, the combined effect of
these traits suggests that aspen as a species is rather tolerant
to browsing and that a boost in recruitment may follow a sus-
pension of the browsing pressure since the regeneration stage
can be present despite poor survival of young aspen cohorts
(Kouki et al., 2004). After reintroducing the grey wolf in
Yellowstone National Park in 19951996, the elk population
declined and willows and aspen returned to the area (Ripple
and Beschta, 2007). The consequence of a decline of mature
aspen trees could be more harmful for associated biodiversity
(Siitonen and Martikainen, 1994; Vehmas et al., 2009) with
potentially poor spreading capability.
Forest res may improve the condition for regeneration of
aspen, but have declined in importance over the last century
due to effective re suppression. In contrast, modern man-
agement guidelines for forestry operations have facilitated
regeneration and contribute to maintenance of old-growth
trees. The positive effect of windthrow for regeneration is
yet modest, but may increase in the future. The strong de-
crease in livestock grazing and haymaking in Norwegian
outlying land during the latest decades is expected to have
caused an increase of successional trees such as aspen. Thus,
collectively, the present and predicted future disturbance re-
gime does not appear to represent important constraints for
regeneration and maintenance of aspen at the regional scale.
This review shows that there is a need for more research
on how browsing interacts with other factors in shaping the
spatiotemporal variation in recruitment rates and population
dynamics of aspen and what ungulate densities that allows
maintenance of viable aspen populations in different habitats.
An important component in this is the recent inclusion of the
sapling stage (<5 cm d.b.h.) in the regular forest monitoring
in Norway (R. Astrup, personal communication). Similar
surveys are established for other tree species (e.g. rowan
and goat willow), as well as surveys of the regional brows-
ing pressure. These data will hopefully prove important for
management of the ungulate populations. It would also be
useful to know the small-scale spatial genetic variation of iso-
lated populations in the outskirts of the distribution of aspen
as this would allow inferences about the efciency of seed
dispersal versus vegetative regeneration, as well as the level
of genetic variation in outskirt populations. As the present
knowledge about variation in chemical defence against her-
bivores in Populus is limited to studies in P. tremuloides, this
should be undertaken in P. tremula as well.
Funding
Norwegian Committee on Forest Genetic Resources,
the Norwegian Forest and Landscape Institute, and the
Research Council of Norway (Milj 2015, 184036).
Acknowledgements
We wish to thank Ivar Gjerde and James Speed for constructive
comments on a previous version of the manuscript, and also Rune
Eriksen and Rasmus Astrup for providing the forest inventory data.
Conict of Interest Statement
None declared.
References
Abaturov, B. and Smirnov, K. 2002 Effects of moose population
density on development of forest stands in central European
Russia. Alces. (Suppl. 2), 15.
 LIFE HISTORY STRATEGIES OF ASPEN AND BROWSING EFFECTS
Andrn, H. and Angelstam, P. 1993 Moose browsing on Scots
pine in relation to stand size and distance to forest edge.
J. Appl. Ecol. 30, 133142.
Austrheim, G., Solberg, E.J., Mysterud, A., Daverdin, M. and
Andersen, R. 2008 Hjortedyr og husdyr p beite i norsk utmark
i perioden 19491999. Rapport zoologisk serie 2008-2. Norges
teknisk naturvitenskapelige universitet, Vitenskapsmuseet,
Trondheim (In Norwegian, English summary).
Bailey, J.K., Schweitzer, J.A., Rehill, B.J., Irschick, D.J., Whitham,
T.G. and Lindroth, R.L. 2007 Rapid shifts in the chemical com-
position of aspen forests: an introduced herbivore as an agent
of natural selection. Biol. Inv. 9, 715722.
Baker, W.L., Munroe, J.A. and Hessl, A.E. 1997 The effects of
elk on aspen in the winter range in Rocky Mountain National
Park. Ecography. 20, 155165.
Bergstrm, R. and Hjeljord, O. 1987 Moose and vegetation in-
teractions in northwestern Europe and Poland. Swedish Wildl.
Res. Suppl. 1, 213228.
Beschta, R.L. and Ripple, W.J. 2009 Large predators and trophic
cascades in terrestrial ecosystems of the western United States.
Biol. Conserv. 142, 24012414.
Birks, H.H. 1970 Studies in the vegetational history of Scotland.
I. A pollen diagram from Abernethy forest, Inverness-shire
(Scotland). J. Ecol. 58, 827846.
Bokalo, M., Comeau, P.G. and Titus, S.J. 2007 Early development
of tended mixtures of aspen and spruce in western Canadian
boreal forests. For. Ecol. Manage. 242, 175184.
Brring, U. 1988 On the reproduction of aspen (Populus tremula
L.) with emphasis on its suckering ability. Scand. J. For. Res.
3, 229240.
Brset, O. 1954 The germination power of aspen seeds. Medd.
Nor. Skogf. 13, 144. (In Norwegian, English summary).
Brset, O. 1956 Aspen suckers. Tidsskr. Skogbr. 4, 219240.
(In Norwegian, English summary).
Brset, O. 1960 Silviculture of aspen. Scottish For. 14, 6880.
Brset, O. 1985a Bjrk, osp, or. Veiledning for det praktiske skogbruk.
3rd edn. Institutt for skogskjtsel, Norges landbrukshgskole,
s. (In Norwegian).
Brset, O. 1985b Skogskjtsel I. Skogkologi. Landbruksforlaget,
Oslo, Norway. (In Norwegian).
Cooke, J.E.K. and Rood, S.B. 2007 Trees of the people: the grow-
ing science of Populus in Canada and worldwide. Can. J. Bot.
85, 11031110.
Danell, K., Bergstrm, R., Edenius, L. and Ericsson, G. 2003 Un-
gulates as drivers of tree population dynamics at module and
genet levels. For. Ecol. Manage. 181, 6776.
de Chantal, M. and Granstrm, A. 2007 Aggregations of dead
wood after wildre act as browsing refugia for seedlings of
Populus tremula and Salix caprea. For. Ecol. Manage. 250,
38.
de Chantal, M., Kuuluvainen, T., Lindberg, H. and Vanha-
Majamaa, I. 2005 Early regeneration of Populus tremula from
seed after forest restoration with re. Scand. J. For. Res. 20, 3342.
de Chantall, M., Lindberg, H. and Kallonen, S. 2009 The condi-
tion and survival of Populus tremula and other deciduous sap-
lings in a moose winter-foraging area in southern Finland. Ann.
Bot. Fenn. 46, 280290.
den Herder, M., Kouki, J. and Ruusila, V. 2009 The effects of
timber harvest, forest re, and herbivores on regeneration of
69
deciduous trees in boreal pine-dominated forests. Can. J. For.
Res. 39, 712722.
Edenius, L. and Ericsson, G. 2007 Aspen demographics in rela-
tion to spatial context and ungulate browsing: implications
for conservation and forest management. Biol. Conserv. 135,
293301.
Ennos, R.A., Worrell, R. and Malcolm, D.C. 1998 The gen-
etic management of native species in Scotland. Forestry. 71,
123.
Ericsson, G., Edenius, L. and Sundstrm, D. 2001 Factors af-
fecting browsing by moose (Alces alces L.) on European aspen
(Populus tremula L.) in a managed boreal landscape. Eco-
science. 8, 344349.
Essen, P.A., Ehnstrm, B., Ericsson, L. and Sjberg, K. 1997
Boreal forests. Ecol. Bull. 46, 1647.
Fjellstad, W. and Dramstad, W.E. 2005 3Q - Endringer i jordbrukets
kulturlandskap i stfold, Oslo/Akershus og Vestfold - Tema
Arealstruktur. NIJOS rapport 12/05. The Norwegian Institute
of Land Inventory, s, Norway. (In Norwegian).
Fjellstad, W., Dramstad, W.E. and Huso, B. 2007 3Q Jordbrukets
kulturlandskap Status og utviklingstrekk. Fylker: Hedmark
og Oppland. Dokument fra Skog og landskap. Norwegian
Forest and Landscape Institute, s, Norway. (In Norwegian).
Fracheboud, Y., Luquez, V., Bjrken, L., Sjdin, A., Tuominen, H.
and Jansson, S. 2009 The control of autumn senescence in
European aspen. Plant Physiol. 149, 19821991.
Frivold, L.H. 1994 Trr i kulturlandskapet. Landbruksforlaget,
Oslo, Norway. (In Norwegian).
Frivold, L.H. 1998 Treslag ved gjengroing av kulturlandskapet.
In Jordbrukets kulturlandskap. E. Fremstad and I.B. Lid (eds).
Universitetsforlaget, Oslo, Norway, pp. 8789. (In Norwegian).
Fussi, B., Lexer, C. and Heinze, B. 2010 Phylogeography of Popu-
lus alba (L.) and Populus tremula (L.) in Central Europe: sec-
ondary contact and hybridisation during recolonisation from
disconnected refugia. Tree Genet. Genomes. 6, 439450.
Fystro, I. 1962 Skogbrukets frforsyning. In Skogbruksboka, Vol.
2, Skogskjtsel. O. Brset (ed). Skogforlaget, Oslo, Norway,
pp. 299318. (In Norwegian).
Gjerde, I., Saetersdal, M. and Nilsen, T. 2005 Abundance of two
threatened woodpecker species in relation to the proportion of
spruce plantations in native pine forests of western Norway.
Biodiv. Conserv. 14, 377393.
Glynn, C., Herms, D.A., Egawa, M., Hansen, R. and Mattson, W.J.
2003 Effects of nutrient availability on biomass allocation as
well as constitutive and rapid induced herbivore resistance in
poplar. Oikos. 101, 385397.
Gramuglio, G.T. 1962 The sexual behaviour of Populus tremula
in Italy. Giorn. Bot. Ital. 69, 7890.
Hall, D., Luquez, V., Garcia, V.M., St Onge, K.R., Jansson, S.
and Ingvarsson, P.K. 2007 Adaptive population differentiation
in phenology across a latitudinal gradient in European aspen
(Populus tremula L.): a comparison of neutral markers, candi-
date genes and phenotypic traits. Evolution. 61, 28492860.
Halofsky, J.S., Ripple, W.J. and Beschta, R.L. 2008
Recoupling re and aspen recruitment after wolf reintroduction
in Yellowstone National Park, USA. For. Ecol. Manage. 256,
10041008.
Hamrick, J.L. and Nason, J.D. 1996 Consequences of dispersal
in plants. In Population Dynamics in Space and Time. O.E.
70 FORESTRY
Rhodes, R.K. Chesser and M.H. Smith (eds). The University of
Chicago Press, Chicago, IL, pp. 203237.
Hester, A.J., Edenius, L., Buttenschon, R.M. and Kuiters, A.T.
2000 Interactions between forests and herbivores: the role of
controlled grazing experiments. Forestry. 73, 381391.
Hester, A.J., Scogings, P.F. and Trollope, W.S.W. 2006 Long-
term impacts of goat browsing on bush-clump dynamics in a
semi-arid subtropical savanna. Plant Ecol. 183, 277290.
Hultn, E. and Fries, M. 1986 Atlas of North European Vascular
Plants North of the Tropic of Cancer. Koeltz Scientic Books,
Knigstein, Germany.
Huntley, B. and Birks, H.J.B. 1983 An Atlas of Past and Present
Pollen Maps for Europe: 0-13000 BP. Cambridge University
Press, Cambridge.
Hwang, S.Y. and Lindroth, R.L. 1997 Clonal variation in foliar
chemistry of aspen: effects on gypsy moths and forest tent cat-
erpillars. Oecologia. 111, 99108.
Hbjrg, A. 1978 Photoperiodic ecotypes in Scandinavian trees
and shrubs. Meld. Nor. Landbrukshgsk. 57, 120.
Jobling, J. 1990 Polars for Wood Production and Amenity.
Forestry Commission Bulletin No. 92. HMSO, London.
Johansson, T. 1996 Site index curves for European aspen
(Populus tremula L.) growing on forest land of different soils in
Sweden. Silva Fenn. 30, 437458.
Johansson, T. and Lundh, J.E. 2005 Alder, Aspen and Birch
Growing in Conifer Forest. Department of Bioenergy, Swedish
University of Agricultural Sciences (SLU), Uppsala, Sweden. (In
Swedish).
Johnson, H. 1942 Generativ och vegetativ frkning av Populus
tremula. Svensk Botanisk Tidsskrift. 36, 177199.
Kabzems, R. and Garcia, O. 2004 Structure and dynamics of
trembling aspen white spruce mixed stands near Fort Nelson,
BC. Can. J. For. Res. 34, 384395.
Kay, C.E. 1997 Is aspen doomed? J. For. 95, 411.
Kouki, J., Arnold, K. and Martikainen, P. 2004 Long-term
persistence of aspen - a host for many threatened species is
endangered in old-growth conservation areas in Finland. J. Nat.
Conserv. 12, 4152.
Kucera, B. and Nss, R.M. 1999 Tre. Naturens vakreste rstoff.
Landbruksforlaget, Oslo, Norway. (In Norwegian).
Kuijper, D.P.J., Cromsigt, J., Churski, M., Adam, B., Jedrzejewska,
B. and Jedrzejewski, W. 2009 Do ungulates preferentially feed
in forest gaps in European temperate forest? For. Ecol. Manage.
258, 15281535.
Kuusinen, M. 1994 Epiphytic lichen ora and diversity on Popu-
lus tremula in old-growth and managed forests of southern and
middle boreal Finland. Ann. Bot. Fenn. 31, 159163.
Knig, A. 2005 Provenance research: evaluating the spatial pat-
tern of genetic variation. In Conservation and Management of
Forest Genetic Resources in Europe. T. Geburek and J. Turok
(eds). Arbora Publishers, Zvolen, Germany, pp. 275333.
Langhammer, . 1982 Reeksjoner omkring et plantefelt med osp
og gran i Norge. Tidsskr. Skogbr. 90, 102110. (In Norwegian).
Langhammer, . and Oppdahl, H. 1990 Foryngelse og pleie av
osp (Populus tremula L.) i Norge. Rapport fra Norsk institutt
for skogforskning. 1, 122. (In Norwegian, English summary).
Larsson, J.Y. and Hylen, G. 2007 Statistics of forest conditions
and forest resources in Norway. Viten fra Skog og landskap
1/07. Norwegian Forest and Landscape Institute, s, Norway.
Latva-Karjanmaa, T., Penttila, R. and Siitonen, J. 2007 The
demographic structure of European aspen (Populus tremula)
populations in managed and old-growth boreal forests in
eastern Finland. Can. J. For. Res. 37, 10701081.
Latva-Karjanmaa, T., Suvanto, L., Leinonen, K. and Rita, H.
2003 Emergence and survival of Populus tremula seedlings
under varying moisture conditions. Can. J. For. Res. 33,
20812088.
Latva-Karjanmaa, T., Suvanto, L., Leinonen, K. and Rita, H.
2006 Sexual reproduction of European aspen (Populus tremula L.)
at prescribed burned site: the effects of moisture conditions.
New For. 31, 545558.
Lavsund, S., Nygren, T. and Solberg, E.J. 2003 Status of
moose populations and challenges to moose management in
Fennoscandia. Alces. 39, 109130.
Lexer, C., Fay, M.F., Joseph, J.A., Nica, M.S. and Heinze, B.
2005 Barrier to gene ow between two ecologically divergent
Populus species, P. alba (white poplar) and P. tremula (European
aspen): the role of ecology and life history in gene introgression.
Mol. Ecol. 14, 10451057.
Lid, J. and Lid, D.T. 2005 Norsk Flora. 7th edn. Det Norske
Samlaget, Oslo, Norway. (In Norwegian).
Lieffers, V.J., Pinno, B.D. and Stadt, K.J. 2002 Light dynamics
and free-to-grow standards in aspen-dominated mixedwood
forests. Forest. Chron. 78, 137145.
Linder, P., Elfving, B. and Zackrisson, O. 1997 Stand struc-
ture and successional trends in virgin boreal forest reserves in
Sweden. For. Ecol. Manage. 98, 1733.
Lopez-de-Heredia, U., Sierra-de-Grado, R., Cristobal, M.D.,
Martinez-Zurimendi, P., Pando, V. and Martin, M.T. 2004
A comparison of isozyme and morphological markers to
assess the within population variation in small populations of
European aspen (Populus tremula L.) in Spain. Silvae Genet.
53, 227233.
Maliouchenko, O., Palme, A.E., Buonamici, A., Vendramin,
G.G. and Lascoux, M. 2007 Comparative phylogeography
and population structure of European Betula species, with par-
ticular focus on B. pendula and B. pubescens. J. Biogeogr. 34,
16011610.
Mock, K.E., Rowe, C.A., Hooten, M.B., Dewoody, J. and
Hipkins, V.D. 2008 Clonal dynamics in western North American
aspen (Populus tremuloides). Mol. Ecol. 17, 48274844.
Moen, A. 1998 Endringer i vrt varierte kulturlandskap. In
Jordbrukets kulturlandskap. Forvaltning av miljverdier. A.
Moen, R.A. Ims and M. Jones (eds). Universitetsforlaget, Oslo,
Norway, pp. 1833. (In Norwegian).
Mnsson, J., Kalen, C., Kjellander, P., Andren, H. and Smith,
H. 2007 Quantitative estimates of tree species selectivity by
moose (Alces alces) in a forest landscape. Scand. J. For. Res.
22, 407414.
Namroud, M.C., Park, A., Tremblay, F. and Bergeron, Y. 2005
Clonal and spatial genetic structures of aspen (Populus tremu-
loides Michx.). Mol. Ecol. 14, 29692980.
Nslund, B- 1986 Simulation of Damage and Mortality in
Young Stands and Associated Stand Development Effects.
Swedish University of Agricultural Sciences, Department of
Silviculture, Ume, Sweden.
Oppdahl, H. 1992 Site-index, growth and yield in aspen (Populus
tremula) in South Norway. Medd. Skogforsk. 44, 144.
 LIFE HISTORY STRATEGIES OF ASPEN AND BROWSING EFFECTS
Osier, T.L. and Lindroth, R.L. 2006 Genotype and environment
determine allocation to and costs of resistance in quaking
aspen. Oecologia. 148, 293303.
stlund, L., Zackrisson, O. and Axelsson, A.L. 1997 The history
and transformation of a Scandinavian boreal forest landscape
since the 19th century. Can. J. For. Res. 27, 11981206.
yen, B.H. 1998 Skogbrann i Norge de siste 200 r. Oppdrag-
srapport fra Norsk institutt for skogforskning. 8, 130. (In
Norwegian).
Persson, I.-L. and Danell, K.R.B. 2000 Disturbance by large her-
bivores in boreal forests with special reference to moose. Ann.
Zool. Fenn. 37, 251263.
Pinno, B.D., Pare, D., Guindon, L. and Belanger, N. 2009 Predict-
ing productivity of trembling aspen in the Boreal Shield ecozone
of Quebec using different sources of soil and site information.
For. Ecol. Manage. 257, 782789.
Pothier, D., Raulier, F. and Riopel, M. 2004 Ageing and decline
of trembling aspen stands in Quebec. Can. J. For. Res. 34,
12511258.
Powell, G.R. 1957 The position of aspen (Populus tremula)
in British silviculture. Hon. Thesis. Edinburgh University,
Scotland.
Ripple, W.J. and Beschta, R.L. 2007 Restoring Yellowstones
aspen with wolves. Biol. Conserv. 138, 514519.
Rolstad, J.E., Fremstad, V., Gundersen, V.S. and Storaunet,
K.O. 2002 Naturskog i Norge. Denisjoner, kologiog bruk i
norsk skog- og miljforvaltning. Aktuelt fra skogforskningen
1-2002. Norwegian Forest Research Institute, s, Norway.
(In Norwegian).
Ruel, J.C. 1995 Understanding windthrow silvicultural implica-
tions. Forest. Chron. 71, 434445.
Rytter, L. and Stener, L.G. 2005 Productivity and thinning effects
in hybrid aspen (Populus tremula L. P. tremuloides Michx.)
stands in southern Sweden. Forestry. 78, 285295.
Schlyter, P., Stjernquist, I., Barring, L., Jonsson, A.M. and
Nilsson, C. 2006 Assessment of the impacts of climate change
and weather extremes on boreal forests in northern Europe, fo-
cusing on Norway spruce. Clim. Res. 31, 7584.
Shipley, L.A., Blomquist, S. and Danell, K. 1998 Diet choices
made by free-ranging moose in northern Sweden in relation to
plant distribution, chemistry, and morphology. Can. J. Zool.
76, 17221733.
Siitonen, J. and Martikainen, P. 1994 Occurrence of rare and
threatened insects living on decaying Populus tremula a com-
parison between Finnish and Russian Karelia. Scand. J. For.
Res. 9, 185191.
Solberg, E.J., Strand, O., Veiberg, V., Andersen, R., Heim, M.
Rolandsen, C.M. et al. 2010 Hjortevilt 2009-rsrapport fra
Overvkingsprogrammet for hjortevilt. NINA Rapport 584.
The Norwegian Institute for Nature Research, Trondheim,
Norway. (In Norwegian).
Stevens, M.T. and Lindroth, R.L. 2005 Induced resistance in the
indeterminate growth of aspen (Populus tremuloides). Oecolo-
gia. 145, 298306.
71
Stevens, M.T., Waller, D.M. and Lindroth, R.L. 2007 Resistance
and tolerance in Populus tremuloides: genetic variation, costs,
and environmental dependency. Evol. Ecol. 21, 829847.
Suvanto, L.I. and Latva-Karjanmaa, T.B. 2005 Clone identica-
tion and clonal structure of the European aspen (Populus trem-
ula). Mol. Ecol. 14, 28512860.
Sylvn, N. 1940 Lng- och kortdagstyper av de svenska
skogstrden. Sv. Papper. 18, 332342. (In Swedish).
Tatarinov, F., Bochkarev, Y., Oltchev, A., Nadezhdina, N. and
Cermak, J. 2005 Effect of contrasting water supply on the diam-
eter growth of Norway spruce and aspen in mixed stands: a case
study from the southern Russian taiga. Ann. For. Sci. 62, 807816.
Thompson, K., Bakker, J.P. and Bekker, R.M. 1997 The Soil Seed
Banks of North West Europe: Methodology, Density and
Longevity. Cambridge University Press, Cambridge.
Van Bogaert, R., Jonasson, C., De Dapper, M. and Callaghan,
T.V. 2009 Competitive interaction between aspen and birch
moderated by invertebrate and vertebrate herbivores and cli-
mate warming. Plant Ecol. Divers. 2, 221232.
Vehmas, M., Kouki, J. and Eerikainen, K. 2009 Long-term spatio-
temporal dynamics and historical continuity of European aspen
(Populus tremula L.) stands in the Koli National Park, eastern
Finland. Forestry. 82, 135148.
Venalainen, A., Zeng, H., Peltola, H., Talkkari, A., Strandman, H.
and Wang, K.Y. et al. 2004 Simulations of the inuence of
forest management on wind climate on a regional scale. Agr.
For. Meteor. 123, 149158.
White, C.A., Olmsted, C.E. and Kay, C.E. 1998 Aspen, elk, and
re in the Rocky Mountain national parks of North America.
Wildl. Soc. Bull. 26, 449462.
Wooley, B.C., Walker, S., Vernon, J. and Lindroth, R.L. 2008
Aspen decline, aspen chemistry, and elk herbivory: are they
linked? Rangelands. 30, 1721.
Worrell, R. 1995a European aspen (Populus tremula L.) a
review with particular reference to Scotland. 1. Distribution,
ecology and genetic variation. Forestry. 68, 93105.
Worrell, R. 1995b European aspen (Populus tremula L.) a
review with particular reference to Scotland. 2. Values, silvicul-
ture and utilization. Forestry. 68, 231243.
Worrell, R., Gordon, A.G., Lee, R.S. and McInroy, A. 1999 Flow-
ering and seed production of aspen in Scotland during a heavy
seed year. Forestry. 72, 2734.
Young, A., Boshier, D. and Boyle, T. 2000 Forest conservation
genetics. Principles and practice. CABI Publishing, Wallingford.
Zackrisson, O. 1977 Inuence of forest res on the North Swedish
boreal forest. Oikos. 29, 2232.
Zackrisson, O. and Nilsson, M.C. 1992 Allelopathic effects by
Empetrum hermaphroditum on seed germination of 2 boreal
tree species. Can. J. For. Res. 22, 13101319.
Zakrisson, C., Ericsson, G. and Edenius, L. 2007 Effects of brows-
ing on recruitment and mortality of European aspen (Populus
tremula L.). Scand. J. For. Res. 22, 324332.
Received 29 October 2010