Plants on the move: The role of seed dispersal and initial population
establishment for climate-driven range expansions
Arndt Hampe*,1, 2
Department of Integrative Ecology, Estación Biológica de Doñana (EBD-CSIC), Consejo Superior de Investigaciones Científicas, Av. Américo Vespucio s/n, 41092 Sevilla, Spain
a b s t r a c t
Keywords:
Biotic interactions
Dispersal pathways
Leading edge
Long-distance seed dispersal
Range dynamics
Tree recruitment
Recent climate change will presumably allow many plant species to expand their geographical range up
to several hundred kilometres towards the poles within a few decades. Much uncertainty exists however
to which extent species will actually be able to keep pace with a rapidly changing climate. A suite of
direct and indirect research approaches have explored the phenomenon of range expansions, and the
existing evidence is scattered across the literature of diverse research subdisciplines. Here I attempt to
synthesise the available information within a population ecological framework in order to evaluate
implications of patterns of seed dispersal and initial population establishment for range expansions.
After introducing different study approaches and their respective contributions, I review the empirical
evidence for the role of long-distance seed dispersal in past and ongoing expansions. Then I examine
how some major ecological determinants of seed dispersal and colonisation processes - population
fecundity, dispersal pathways, arrival site conditions, and biotic interactions during recruitment - could
be altered by a rapidly changing climate. While there is broad consensus that long-distance dispersal is
likely to be critical for rapid range expansions, it remains challenging to relate dispersal processes and
pathways with the establishment of pioneer populations ahead of the continuous species range. Further
transdisciplinary efforts are clearly needed to address this link, key for understanding how plant populations ’move’ across changing landscapes.
.
1. Introduction
The 20th century experienced the strongest global warming of
the last millennium, and future temperature rises are likely to
exceed this trend with a predicted increase between 1.8 c C and 4 c C
until 2100 (Solomon et al., 2007). The potential impact of modern
rapid climate change on the distribution and conservation of
biodiversity is the object of great concern. One major consequence
is that plant and animal species worldwide are moving to higher
latitudes and elevations in response to shifts of the environmental
conditions to which they are adapted (Parmesan, 2006). Modelbased projections suggest that the expected climatic conditions
would permit many species to expand their current distribution
range several hundred kilometres towards the poles within only
a few decades (e.g. Skov and Svenning, 2004; Jump et al., 2009).
* Tel.: þ34 954 466700; fax: þ34 954 621125.
E-mail address: arndt@pierroton.inra.fr.
1
Present address: INRA, UMR 1202 Biodiversité, Gènes & Communautés, 69
Route d’Arcachon, F-33610 Cestas, France.
2
Present address: University of Bordeaux, UMR 1202 Biodiversité, Gènes &
Communautés, F-33400 Talence, France.
Much uncertainty exists however to which extent species will
actually be able to achieve such large-scale range expansions in
pace with a rapidly changing climate. The answer to this question
has
wide-ranging ecological and evolutionary consequences
spanning from the population to the biome level. Thus, the
expansion process can strongly affect the range-wide genetic
structure of species and the adaptive potential of their populations
(Excoffier et al., 2009). The differential migration capacity of species
should result in considerable reshufflings of local communities and
regional species pools (Ackerly, 2003; Jackson et al., 2009). And the
expansion of biomes such as the boreal forests will directly influence future climate, be it as a mitigating (e.g. by sequestering CO2)
or an exacerbating (e.g. reducing albedo) force (Bonan, 2008).
It is broadly accepted that range expansions depend on the
populations residing at the colonisation front, or ’leading edge’
(Thuiller et al., 2008; Murphy et al., 2010). Hence, predicting the
expansion potential of a species requires a sound understanding of
the ecological and micro-evolutionary key processes that occur in
these populations (Hampe and Petit, 2005). Two processes are
necessarily involved in a range expansion: 1) the dispersal of
individuals (propagules in the case of plants) beyond the current
range limit and 2) the establishment and growth of resulting
pioneer populations. Both processes contain a strong stochastic
component, usually escape direct observation and therefore are
extremely difficult to measure in nature (Nathan et al., 2003;
Nathan, 2006; Simberloff, 2009). A suite of direct and indirect
research approaches have been used to explore the phenomenon of
range expansions, and the existing evidence is scattered across the
literature of various research disciplines spanning dispersal
ecology, palaeoecology, landscape genetics, phylogeography, invasion biology, climate change research and different branches of
dispersal and distribution modelling.
Great progress has been made in combining some of the above
disciplines, and these interdisciplinary efforts have considerably
helped refine our understanding of species range dynamics (Petit
et al., 2004; Botkin et al., 2007; Hu et al., 2009). For instance,
a rapidly growing number of phylogeographical studies combines
molecular surveys with palaeoecological data and/or species
distribution modelling exercises (e.g., Cheddadi et al., 2006; Alsos
et al., 2009; Liepelt et al., 2009). Other examples are the rapidly
growing field of ’invasion genetics’ (Estoup and Guillemaud, 2010),
studies at the interface between dispersal ecology and invasion
research (Gosper et al., 2005) or those that merge invasion and
climate change biology (e.g., Gallien et al., 2010). A greater gap
appears however to persist between disciplines that focus on past
range dynamics and those that investigate primarily ongoing
expansions. And little interdisciplinary research has to date been
specifically dedicated to populations at the leading edge of
expanding species ranges. Hence, we are lacking a general framework that integrates the many intrinsic and extrinsic factors that
can determine the success or failure of a species to keep pace with
a rapidly changing climate.
The aim of this essay review is to synthesise some of the scattered information upon range expansions within a population
ecological and micro-evolutionary framework, in an attempt to
examine the role of seed dispersal and initial population establishment for this process. After introducing different study
approaches and their respective contributions, I will review the
empirical evidence for the role of (long-distance) dispersal in past
and ongoing range expansions. Then I examine how some major
ecological determinants of dispersal and colonisation processes population fecundity, dispersal pathways, arrival site conditions,
and biotic interactions during recruitment - could be altered by
a rapidly changing climate.
This paper draws largely on knowledge derived from extratropical woody plants, since these organisms count with the most
detailed empirical records and have served as models for important
paradigms related with the topic of this paper (e.g., Rejmanek and
Richardson, 1996; Petit et al., 2004; Svenning and Skov, 2004; Hu
et al., 2009). Moreover, the importance of trees for sustaining life
in general and biodiversity in particular can hardly be overstated.
Forests cover w30% of the land surface (w42 million km2),
store w45% of terrestrial carbon, and contribute w50% of terrestrial
net primary production (Bonan, 2008). Hence, the impact of future
climate changes on the distribution and conservation of biodiversity will depend to a great extent on the reaction of trees and the
ecosystems they sustain.
2. Contributions from different research fields
Linking patterns of seed dispersal and plant recruitment with
colonisation events at a landscape to continental level requires
integrating processes that occur at very different spatial and
temporal scales (Kollmann, 2000; Nathan, 2006). Therefore
complementary research approaches are needed to shed light on
the diverse processes and conditions involved in a successful range
expansion (Fig. 1). And while the capacity of species to experience
Fig. 1. The complementary empirical research approaches treated in this review that
are contributing to extend our understanding of climate-driven range expansions.
rapid large-scale range expansions is likely to be ultimately determined by mechanisms acting at the landscape to regional level
(such as habitat availability and connectivity), these cannot be
understood without a sound knowledge of local-scale biological
phenomena (such as patterns of plant fecundity or disperser
abundance).
Field studies are indispensable for monitoring spatio-temporal
patterns of colonisation and related population dynamics. Moreover, ecological field studies help understand the scenario in which
seed dispersal and plant recruitment occur. This includes biotic and
abiotic determinants of key parameters such as plant fecundity, the
behaviour of dispersal vectors, the fates of dispersed propagules,
habitat conditions supporting plant establishment, etc. In brief,
field studies provide baseline information for understanding why
some few dispersal events result in the successful colonisation of
new territories while the vast majority does not.
Population genetic studies help identify actual patterns of
propagule dispersal that cannot be measured by field-based
methods. Moreover, they inform about ecological and microevolutionary processes that accompany the establishment and
growth of pioneer populations (Excoffier et al., 2009). A common
denominator of all genetic approaches considered here is their
explicit consideration of space. Analytical methods are as diverse as
the spatio-temporal scales of interest (Hamrick and Trapnell, 2011).
Studies that directly assess contemporary patterns of seed dispersal
by means of parentage analyses usually operate at the level of local
populations. Larger scales require indirect methods that infer
historical patterns of dispersal from the spatial genetic structure of
extant populations; this is the case with landscape genetics (Sork
and Waits, 2010), phylogeography (Knowles, 2009) and invasion
genetics (Estoup and Guillemaud, 2010).
Palaeoecology was the first field to highlight the dynamic nature
of species ranges. The fossil record continues to play an important
role, as it provides the time frame for reconstructions of past range
expansions and serves as descriptor of past environments, critical
information for disciplines such as phylogeography or the modelling of past species distributions (Nogués-Bravo, 2009). Moreover,
palaeoecological data sometimes provide the only means to test
hypotheses about range expansions (and to reveal their limitations
in a stochastic world; see Jackson et al., 2009).
Invasion biology asks very similar questions to those addressed
here, as climate-driven ’natural’ range expansions are basically
a special case of biological invasions (Petit et al., 2004; Estoup and
Guillemaud, 2010): What makes a successful coloniser? Which
species are particularly efficient? Which environments favour
range expansions? How do pioneer populations perform? Which
evolutionary processes do they experience? The discipline builds
on more than two decades of empirical and theoretical research,
providing a great (and still little exploited) reservoir of knowledge
for ecological research on climate-driven range expansions.
Experimental climate change research contributes a further
relevant component by investigating how populations, species, and
communities will perform under future environmental conditions.
Increased CO2 levels, higher temperatures or changing precipitation regimes will influence key factors such as plant fecundity,
competitive interactions or regimes of landscape disturbance (e.g.,
fires or windbreaks), thereby directly affecting the colonisation
potential of species.
The empirical knowledge obtained by the above disciplines is
now routinely transferred into modelling and simulation exercises,
whose implementation in ecological research has been greatly
enhanced by computing power and novel analytical approaches.
Several groups of models appear relevant within the context of
range expansions (see also Thuiller et al., 2008): 1) mechanistic
models of seed dispersal help improve our predictive ability concerning long-distance dispersal events, their determinants and
consequences (Nathan, 2006; Schurr et al., 2008; Thompson and
Katul, 2008; Nathan et al., 2011); 2) genetic simulations help
derive patterns of expansions from the spatial genetic structure of
species (Petit et al., 2004; Excoffier et al., 2009; Ray and Excoffier,
2010); 3) niche-based species distribution models allow to
predict the spaces and environments available for future (or past)
expansions (e.g. Skov and Svenning, 2004; Nogués-Bravo, 2009); 4)
process-based species distribution models help achieve a better
understanding of the particular biological mechanisms involved in
expansions and how they may be affected by changing environments (Gallien et al., 2010; Meier et al., 2011); 5) (meta-)population
models allow to explore demographic determinants of and population dynamics during expansions (e.g. Anderson et al., 2009;
Cabral and Schurr, 2010); and 6) spatially explicit simulations of
plant movement allow to investigate how intrinsic (such as
dispersal evolution) and extrinsic (such as fragmentation) factors
can affects species’ expansion capacity (e.g. Pearson and Dawson,
2005; Burton et al., 2010). The latter two groups can also be
viewed as special types of process-based distribution models
(Thuiller et al., 2008).
Albeit current models are continuously improved, each type can
only inform about certain aspects of range expansions; therefore
a major current challenge resides in the development of hybrid
models that allow considering different components at a time
(Franklin, 2010; Gallien et al., 2010; Huntley et al., 2010). Promising
progresses have recently been made in this field (e.g. Dullinger
et al., 2004; Lischke et al., 2006; Engler and Guisan, 2009;
Midgley et al., 2010; Meier et al., 2011; Nathan et al., 2011).
3. Relevance of long-distance propagule dispersal for range
expansions: empirical evidence
Several lines of evidence indicate that the arrival of propagules
ahead of the current range is likely to be a - if not the - major
constraint for rapid range expansions of many plant species. For
instance, a major contribution of early plant phylogeography consisted in establishing that very rare long-distance seed dispersal
events played a central role in postglacial range expansions (e.g.,
Le Corre et al., 1997; Petit and Hampe, 2006; Davies et al., 2004).
Simulations corroborate the emphasis on the expression “very
rare” in this context (Bialozyt et al., 2006; Ray and Excoffier, 2010).
The role of long-distance seed dispersal has also been outlined in
genetic studies of ongoing range expansions (e.g., Ramakrishnan
et al., 2010; Lachmuth et al., 2010). On the other hand, phylogeographical evidence is increasingly suggesting that previous fossilbased estimates of postglacial expansion rates have probably
been overly optimistic (McLachlan et al., 2005; Provan and Bennett,
2008; Hu et al., 2009). It appears instead that most expansions
occurred at rates far below what would be necessary to track future
climatic warming (3000e5000 m/year; Petit et al., 2008).
This pessimistic notion is further backed by the influential study
of Svenning and Skov (2004), who used bioclimatic niche models to
compare the actual ranges of 55 European tree species with those
ranges that these species could potentially inhabit under current
climatic conditions. The authors estimated that species are on
average occupying as little as 38% of their potential distribution
range and concluded that the current geographic distributions of
European trees appear strongly controlled by dispersal constraints
on postglacial expansion. Even though the reported value probably
somewhat underestimates the real extent of range filling (Denk and
Bruelheide, 2006), the study of Svenning and Skov (2004) provides
compelling evidence for the role of dispersal limitation during past
range expansions. A similar albeit less striking effect was subsequently also observed in a set of 47 widespread European forest
plant species (Svenning et al., 2008).
On the other hand, an emerging paradigm in invasion biology
assigns ’propagule pressure’ a central role for the success of plant
invasions (Colautti et al., 2006; Simberloff, 2009). Note that the
term ’propagule’ refers in this context to a group of individuals that
found a new population, not to a dispersal unit. (Accordingly, the
terms ’propagule size’ and ’propagule rate’ refer to the group size
and to the frequency of arrivals through time, respectively.)
Although there are some anecdotal cases of viable populations that
have established from very few individuals, meta-analyses indicate
a consistent relationship between the number and frequency of
founders and the success of population establishment (Simberloff,
2009). Consequently, range expansions should be favoured if
plant populations are able to disperse their seeds i) over long
distances and ii) along similar pathways, thereby ensuring that new
areas receive colonisers with sufficient abundance and frequency
(see also Lachmuth et al., 2010). This ’double-sided’ dispersal ability
should in turn be determined by ecological interactions between
propagules and their dispersal agents (e.g., Gosper et al., 2005 for
bird-dispersed species) as well as by the landscape context through
which dispersal occurs (e.g., Levey et al., 2008).
Experimental evidence for the hypothesis that range expansions
could be constrained by dispersal limitation comes from numerous
translocations of plant recruits outside the current range (e.g.,
Kellmann, 2004; Ibáñez et al., 2008; Marsico and Hellmann, 2009).
High rates of recruit survival are commonly observed in these
experiments and interpreted as a sign that the local absence of the
target species could be primarily due to the lack of propagule
arrival. However, other potential factors such as plant mortality
through climatic extreme events cannot be ruled out by this
approach (Slatyer and Noble, 1992; Jalili et al., 2010), and no
experiment on woody plants has to date monitored whether
translocations have actually resulted in self-sustaining populations
(Simberloff, 2009).
There are still few species distribution models that incorporate
more or less realistic estimates of dispersal (Thuiller et al., 2008;
but see e.g. Dullinger et al., 2004; Iverson et al., 2004; Lischke et al.,
2006; Engler and Guisan, 2009; Meier et al., 2011). Fully in line
with the empirical evidence, simulations typically show that the
spread rate tends to exert a strong influence on predicted distribution ranges. On the other hand, mechanistic models of
propagule dispersal by wind underpin that spread rate estimates
can be strongly affected by even small differences in the production, release conditions or survival of seeds if these aspects alter
the frequency of effective long-distance dispersal (e.g., Bohrer
et al., 2008; Jongejans et al., 2008; Soons and Bullock, 2008;
Nathan et al., 2011). Differences in the behaviour of animal seed
dispersers are likely to have a similar impact (cf Will and
Tackenberg, 2008).
In conclusion, rapidly accumulating evidence suggests that
range expansions under future rapid climate change could be
rather severely constrained by the availability of founders ahead of
the current distribution range. In plants, constraints would largely
arise from the rarity of long-distance propagule dispersal towards
suitable establishment sites (Nathan, 2006). This hypothesis
remains however untested, as not a single of the described
approaches has achieved to identify the actual role of propagule
dispersal per se (as opposed to other demographic processes
involved in colonisation processes).
4. How are ecological determinants of dispersal
affected by climate change?
The ability of species to place colonists in suitable areas ahead of
the range is likely to be governed by ecological determinants that
affect propagule departure, transport and arrival, respectively. In
the following, I will discuss three aspects that are related with each
of these three dispersal stages: plant fecundity, dispersal pathways,
and propagule delivery sites. Finally, I will discuss some possible
climate-driven changes in the biotic interactions that colonising
plants are experiencing.
4.1. Fecundity
While there is broad consensus that any invasion by leptokurtic
dispersal is highly sensitive to the shape of the tail of the dispersal
kernel (Nathan, 2006), less attention has historically been paid to
the influence of fecundity on large-scale geographical spread rates
(but see e.g. Boulant et al., 2008; Martin and Canham, 2010 for
local-scale expansions; Burton et al., 2010; Nathan et al., 2011 for
modelling exercises). This aspect should be particularly relevant
for long-distance dispersal, however, because the abundance of
propagules at a given distance tends to scale directly with fecundity
of the source population as the tail of the dispersal kernel flattens
(Clark et al., 2001). In other words, the frequency of long-distance
dispersal events to establishment sites ahead of an expanding
range is likely to be more or less tightly related with the availability
of propagules in the hinterland (see also Murphy et al., 2010).
Many models of invasion spread have incorporated fecundity more precisely: net reproductive rate - since the seminal paper of
Skellam (1951). Yet half a century had to elapse before Clark et al.
(2001) demonstrated on theoretical grounds that variation in this
key parameter can exert strong effects on invasion rates. While
these authors emphasised the fact that considering fecundity as
a variable parameter considerably reduces model-based estimates
of past expansion rates, their result serves likewise to highlight that
climate-driven changes in population fecundity could play a key
role in future range expansions (see also Clark et al., 2003). In fact,
Nathan et al. (2011) found that future changes in the spread of
several North American wind-dispersed trees might be largely
determined by earlier maturation and higher fecundity that could
result from rising CO2 levels.
Numerous experimental studies have shown that elevated CO2
levels can significantly increase the flower, pollen and seed output
of individual plants (LaDeau and Clark, 2001, 2006a; Jablonski et al.,
2002; Stiling et al., 2004; Way et al., 2010), although this increase
may sometimes go along with decreasing seed quality (most
notably in terms of nitrogen content; Jablonski et al., 2002; but see
Stiling et al., 2004; Way et al., 2010). In addition, trees in CO2enriched environments have been shown to start reproducing at
a younger age (LaDeau and Clark, 2006b). Experimental evidence
for warming effects on tree fecundity is much more scant than that
considering CO2. In fact, Nakamura et al. (2010) claimed to be
reporting on the first temperature manipulation experiment that
warmed canopy strata in natural tall tree forests. They found that
branch warming by 5 c C extended the length of the growing season
of canopy leaves and roughly doubled the acorn production of
fruiting Quercus crispula trees.
A number of field studies have monitored multi-year patterns of
fecundity in populations near the (climate-governed) leading edge
of species ranges (Pigott and Huntley, 1981; Hofgaard, 1993; Holm,
1994; Despland and Houle, 1997; Meunier et al., 2007). Unsurprisingly, both fruit production and seed quality are typically linked
with favourable climatic conditions. In fact, reproduction is often
virtually limited to particularly warm years. Consequently, future
warming may be expected to result in higher long-term average
fecundity, a less irregular seed production and improved seed
quality in such populations.
The direct positive effects of CO2 increase and climate warming
on the fecundity of leading edge populations should be further
exacerbated by the relaxation of Allee effects as these populations
grow larger and denser (Taylor and Hastings, 2005). Allee effects
are generally widespread in plant populations and likely to be
particularly present in small pioneer stands ahead of the continuous expansion front. Given that such populations have moreover
passed through a recent strong genetic bottleneck, an increasing
availability of mates should not only have direct effects on seed set
but also be particularly effective in restoring genetic diversity and
favouring selection against inbred genotypes (e.g. Lachmuth et al.,
2010; see also Estoup and Guillemaud, 2010). While numerous
theoretical studies have shown that Allee effects can considerably
slow down spread rates of invasive species (reviewed in Taylor and
Hastings, 2005), the genetic-evolutionary component of this
process clearly deserves further investigation.
4.2. Dispersal pathways
The trajectories of migrating propagules are largely determined
by the landscape context through which they move (Damschen
et al., 2008; Nathan et al., 2008). The strong context-dependence
of long-distance dispersal and resulting colonisation events is
possibly a major reason for the eminently idiosyncratic nature of
past range expansions (Hu et al., 2009; Jackson et al., 2009).
A better understanding of how dispersal pathways and expansion
routes are triggered by the abiotic and biotic environment is
therefore critical for improving predictions of future range shifts. It
also is a major challenge for research, however, as the complexity of
natural landscapes and the spatio-temporal scales involved in their
investigation push both empirical and modelling studies of
dispersal processes quickly to their limits (Nathan, 2006; Nathan
et al., 2008; Thompson and Katul, 2008).
It is well known from phylogeographical studies that major
geographic barriers have influenced past population and range
dynamics. For instance, mountain ranges have blocked certain
lineages from further expansion; a paradigmatic example is the
retention of Italian populations of many plant and animal species
by the Alps (Hewitt, 2000). Conversely, the postglacial expansion of
European beech (Fagus sylvatica) across much of Europe occurred
largely along major mountain ranges (Magri et al., 2006). However
fascinating, large-scale phylogeographical surveys provide insights
of limited utility for predicting future expansion patterns because
of their coarse spatial resolution. Moreover, many present-day
landscapes are completely different from those through which
postglacial range expansions occurred. Hence, great uncertainty
exists regarding the question to what extent studying past range
dynamics can help predict future developments (Midgley et al.,
2007; Petit et al., 2008).
More specific information about ongoing climate-driven range
expansions can soon be expected from the burgeoning field of
landscape genetics (Sork and Waits, 2010; Storfer et al., 2010). To
date, only a handful of molecular studies have investigated localscale population expansions at altitudinal range limits (e.g.,
Truong et al., 2008; Piotti et al., 2009; but see e.g. Ramakrishnan
et al., 2010 for a lowland range expansion not driven by climate).
Yet the advent of powerful sequencing techniques and novel
analytical approaches implemented on strong conceptual grounds
(Anderson et al., 2010; Estoup and Guillemaud, 2010) should soon
permit to reveal latitudinal range shifts almost in real time that are
too subtle to be detected by more traditional approaches. At least if
investigations can draw on an efficient detection and thorough
sampling of individuals from the colonisation front; this will
require a detailed knowledge of species distributions at local to
regional scale.
The development of mechanistic models of long-distance seed
dispersal is another active research area that produces important
insights into patterns and determinants of seed movement at
a landscape scale. Based on observational or experimental data,
such exercises indicate that dispersal pathways are to some extent
predictable from the landscape context even for long-distance
dispersal events (Tackenberg, 2003; Soons et al., 2004; Levey
et al., 2008; Schurr et al., 2008). However, dispersal patterns can
also be considerably modified by relatively minute changes in seed
production, departure or survival (e.g., Bohrer et al., 2008;
Jongejans et al., 2008; Soons and Bullock, 2008), suggesting that
models need to take explicit account of both plant-related and
landscape-related determinants of dispersal (Schurr et al., 2008).
Despite important advances in this field, a diversity of aspects
still remain very poorly understood. Just to name a few: Mechanistic models of long-distance seed dispersal remain largely limited
to wind-dispersed species (but see Cousens et al., 2010). Even
within this research field, it remains little known how well current
models can actually be up-scaled to a regional scale, and how the
respective importance of different determinants of dispersal (e.g.,
uplift mode, landscape structure, macro-meteorology) changes as
one moves from one scale to another (Thompson and Katul, 2008).
Moreover, it has been speculated that (especially extreme) longdistance dispersal events could often actually be performed by
non-standard dispersal vectors (Higgins et al., 2003; Nathan, 2006).
Finally, the role of landscape-scale patterns of seed dispersal for
range expansions remains very difficult to evaluate as long as the
existence of particular pathways of long-distance dispersal cannot
be related with the actual establishment and growth of pioneer
populations ahead of species ranges. Further transdisciplinary
efforts are needed to address this link, key for understanding how
plant populations ’move’ across changing landscapes.
Given the scant empirical evidence available, it is unsurprising
that very few investigations have explicitly addressed how
dispersal pathways might be affected by future climate changes.
Two notable exceptions are Kuparinen et al. (2009) and Nathan
et al. (2011) who used an elegant combination of microclimatic
data, species traits and mechanistic modelling. Whereas the former
study found that increasing air temperatures can indeed favour the
frequency of long-distance propagule dispersal by wind, the latter
study concluded that their effect on species expansion rates seems
to be rather small compared with expectable changes in maturation
and fecundity following higher CO2 levels. On the other hand,
observed increases in the frequency and strength of storms
(Trenberth et al., 2007) should contribute to increase the frequency
of long-distance dispersal events in wind-dispersed species. The
effect of future climate change on the behaviour of biotic dispersal
agents is even more difficult to predict. Changes in plant density
and landscape-scale aggregation should affect dispersal distances
via the behaviour of frugivorous bird populations and communities
(Carlo and Morales, 2008). At a regional scale, climate-driven
changes of migration routes and wintering grounds (Berthold
et al., 1992; Rivalan et al., 2007) could result in substantial
changes in the abundance of avian seed dispersers.
4.3. Sites of propagule delivery
Climate-driven range expansions occur because leading edge
populations experience successful establishment and growth
thanks to the relaxation of environmental constraints. In most
places, such expansions will not be apparent as a moving front;
isolated, low-density populations will initially establish in particularly favourable sites followed by increases in abundance and
occupancy (Murphy et al., 2010). In a landscape perspective, the
relaxation of climatic constraints on plant recruitment should go
along with a growing area available for colonisation as well as an
increasing connectivity of available patches. As both seed sources
and suitable establishment sites become more abundant and
widespread across the landscape, the propagule pressure required
for establishing self-sustaining populations should rapidly decrease
(Simberloff, 2009).
On the other hand, recent climate change goes along with
changes in the frequency and impact of physical disturbances (e.g.
storms or fires; Turner, 2010). Such disturbances can catalyse very
rapid increases in local recruitment and, if widespread enough,
even promote range expansions. For instance, Johnstone and
Chapin (2003) observed that forest stands along the northern
distribution limit of lodgepole pine (Pinus contorta) showed
consistent increases in pine dominance following fire and they
concluded that fires can speed up the species’ range expansion by
offering suitable regeneration niches. Fire can also be effective in
promoting transitions from black spruce (Picea mariana) to white
spruce (P. glauca) forest under a warmer climate (Wirth et al.,
2008). Landhäusser et al. (2010) observed similarly that aspen
(Populus tremuloides) is rapidly expanding its range upslope in the
Canadian Rocky Mountain region as a result of forest management
practices favouring widespread recruit establishment in conjunction with a warming climate.
4.4. Biotic interactions during dispersal and initial establishment
Climate change directly influences the movements and establishment of recruiting colonisers, but it also exerts indirect effects
through its mediation of biotic interactions that interfere at
different stages of the recruitment process. The inherent
complexity and context-dependence of such biotic interactions
burdens predictions upon future changes in biotic interactions and
their consequences with great uncertainty (Mitchell et al., 2006;
Parmesan, 2006).
The arrival of seeds at establishment sites should be affected by
climate-driven modifications in the distribution and movements of
animal seed dispersers. A paradigmatic example for such a modification is the blackcap (Sylvia atricapilla), a major disperser of many
European fleshy-fruited plants. Central European populations of
this bird species show a rapidly increasing tendency to migrate
northwest and winter in southern Britain instead of the Mediterranean Basin (Berthold et al., 1992). This phenomenon could
enhance the expansion of several plant species that are currently
rare or absent from north-western central Europe and the British
Isles.
On the other hand, the expansion potential of some species
might be constrained by the lack of mutualists in the new area if
these expand more slowly or along other routes (Van der Putten
et al., 2010). Species relying on specific mycorrhizas or pollinators
would be potential candidates (Richardson et al., 2000). To date no
studies have to my knowledge documented this phenomenon in
the context of climate-driven range expansions. Evidence from
invasion biology suggests however that such limitations would
probably be rather rare due to the generalist character of many
mutualistic interactions (Richardson et al., 2000).
Once successfully arrived, colonists can temporarily benefit
from the escape of associated antagonists as their geographical
isolation and small size renders them relatively difficult to detect
(Kawecki, 2008; Van der Putten et al., 2010). Abundant empirical
evidence for enemy release comes from studies of plant invasions
(Mitchell et al., 2006), yet it is unclear to which extent these
extreme cases of range expansions can be applied to the relatively
slow pace of climate-driven but otherwise unaided expansion
processes. Moreover, the relevance of enemy release depends on
the identity of the associated organism. Effects are probably minor
in planteherbivore interactions because invertebrate herbivores
are typically more dispersive than their host plants (Kinlan and
Gaines, 2003) and more responsive to temperature changes (Berg
et al., 2010). Interactions with specialised parasites or pathogens
could be more strongly affected (Van der Putten et al., 2010; see
also Gibson et al., 2010), resulting in a lower infection load during
early stages of population establishment (van Grunsven et al., 2007,
2010). Experimental evidence indicates moreover that the virulence of pathogens tends to decrease in small and isolated populations (Boots and Mealor, 2007), although it appears doubtful
whether such a process attains any greater relevance in pioneer
populations at rapidly expanding range margins.
Finally, interspecific competition is likely to become more
intense and render recruitment more difficult as climatic conditions improve. A well-investigated example are tundra habitats
where increased mineralisation rates following climate warming
can cause a shift from competition for soil nutrients to competition
for light (Chapin et al., 1995). There is some circumstantial evidence
that competition could have delayed past climate-driven expansions. For instance, Parshall (2002) found that hemlock (Tsuga
canadensis) invaded hardwood forests more slowly than pine
forests. However, Seppä et al. (2009) demonstrated that the
advance of the competitive Norway spruce (Picea abies) across
Scandinavia occurred very rapidly and to the expense of several
previously present woody species. Similarly, Magri (2008) argued
that competition with other tree taxa was apparently not very
influential in the postglacial increase of beech (F. sylvatica\) populations in Europe. These examples underpin that interspecific
competition is possibly “the most significant but also the least
understood biotic component determining invasion success” in
trees (Petit et al., 2004, p. 122).
5. Concluding remarks
Climate-driven changes in geographical ranges are now
observed worldwide, and already observable shifts foreshadow
more pronounced changes in the near future (Parmesan, 2006;
Petit et al., 2008). Attempts to assess and predict the impact of
recent climate change on species distributions have made considerable progress in recent years (Thuiller et al., 2008). However, we
are still very far from a mechanistic and integrative understanding
of the ecological processes involved in range expansions, especially
in long-lived species such as woody plants (Jackson et al., 2009;
Nathan et al., 2011). While ecologists have sometimes not seen
the forest for the trees, so to speak, it is also true that forests cannot
be understood without knowledge of the trees and other component species. It is the responses of individual organisms that begin
the cascade of ecological processes that manifest themselves as
changes in system properties (Hansen et al., 2001). This is why
plant population ecology and in particular dispersal research have
much to offer to the current debate on climate-driven range
dynamics.
There is now a broad consensus that long-distance dispersal is
likely to be crucial for range expansions under rapid climate
change, yet it remains extremely challenging to relate dispersal
processes and pathways with the establishment of pioneer populations ahead of the continuous species range. Addressing this link
requires integrating research perspectives and approaches from
various subdisciplines. Such transdisciplinary efforts will be key for
improving our understanding upon how plant populations ’move’
across changing landscapes.
Acknowledgments
This work was supported by the Spanish Ministerio de Ciencia e
Innovación (grants RYC-2008-02603 and CGL2010-18381) and the
European Union (grant MERG-CT-2007-208108).
References
Ackerly, D., 2003. Community assembly, niche conservatism, and adaptive evolution
in changing environments. International Journal of Plant Sciences 164,
S165eS184.
Alsos, I.G., Alm, T., Normand, S., Brochmann, C., 2009. Past and future range shifts
and loss of diversity in dwarf willow (Salix herbacea L.) inferred from genetics,
fossils and modelling. Global Ecology and Biogeography 18, 223e239.
Anderson, B.J., Akçakaya, H.R., Araújo, M.B., Fordham, D.A., Martinez-Meyer, E.,
Thuiller, W., Brook, B.W., 2009. Dynamics of range margins for metapopulations
under climate change. Proceedings of the Royal Society B 276, 1415e1420.
Anderson, C.D., Epperson, B.K., Fortin, M.J., Holderegger, R., James, P.M.A.,
Rosenberg, M.S., Scribner, K.T., Spear, S.T., 2010. Considering spatial and
temporal scale in landscape-genetic studies of gene flow. Molecular Ecology 19,
3565e3575.
Berg, M.P., Kiers, E.T., Driessen, G., van der Heijden, M., Kooi, B.W., Kuenen, F.,
Liefting, M., Verhoef, H.A., Ellers, J., 2010. Adapt or disperse: understanding
species persistence in a changing world. Global Change Biology 16, 587e598.
Berthold, P., Helbig, A.J., Mohr, G., Querner, U., 1992. Rapid microevolution of
migratory behaviour in a wild bird species. Nature 360, 668e670.
Bialozyt, R., Ziegenhagen, B., Petit, R.J., 2006. Contrasting effects of long distance
seed dispersal on genetic diversity during range expansion. Journal of Evolutionary Biology 19, 12e20.
Bohrer, G., Katul, G.G., Nathan, R., Walko, R.L., Avissar, R., 2008. Effects of canopy
heterogeneity, seed abscission and inertia on wind-driven dispersal kernels of
tree seeds. Journal of Ecology 96, 569e580.
Bonan, G.B., 2008. Forests and climate change: forcings, feedbacks, and the climate
benefits of forests. Science 320, 1444e1449.
Boots, M., Mealor, M., 2007. Local interactions select for lower pathogen infectivity.
Science 315, 1284e1286.
Botkin, D.B., Saxe, H., Araújo, M.B., Betts, R., Bradshaw, R.H.W., Cedhagen, T.,
Chesson, P., Dawson, T.P., Etterson, J.E., Faith, D.P., Ferrier, S., Guisan, A.,
Hansen, A.S., Hilbert, D.W., Loehle, C., Margules, C., New, M., Sobel, M.J.,
Stockwell, , D.R.B., 2007. Forecasting the effects of global warming on biodiversity. BioScience 57, 227e236.
Boulant, N., Kunstler, G., Rambal, S., Lepart, J., 2008. Seed supply, drought, and
grazing determine spatio-temporal patterns of recruitment for native and
introduced invasive pines in grasslands. Diversity and Distributions 14,
862e874.
Burton, O.J., Phillips, B.L., Travis, J.M.J., 2010. Trade-offs and the evolution of lifehistories during range expansion. Ecology Letters 13, 1210e1220.
Cabral, J., Schurr, F., 2010. Estimating demographic models for the range dynamics
of plant species. Global Ecology and Biogeography 19, 85e97.
Carlo, T.A., Morales, J.M., 2008. Inequalities in fruit-removal and seed dispersal:
consequences of bird behaviour, neighbourhood density and landscape aggregation. Journal of Ecology 96, 609e618.
Chapin III, F.S., Shaver, G.R., Giblin, A.E., Nadelhoffer, K.G., Laundre, J.A., 1995.
Response of Arctic tundra to experimental and observed changes in climate.
Ecology 76, 694e711.
Cheddadi, R., Vendramin, G.G., Litt, T., François, L., Kageyama, M., Lorentz, S.,
Laurent, J.M., de Beaulieu, J.L., Sadori, L., Jost, A., Lunt, D., 2006. Imprints of
glacial refugia in the modern genetic diversity of Pinus sylvestris. Global Ecology
and Biogeography 15, 271e282.
Clark, J.S., Lewis, M., Horvath, L., 2001. Invasion by extremes: population spread
with variation in dispersal and reproduction. American Naturalist 157,
537e554.
Clark, J.S., Lewis, M., MacLachlan, J.S., HilleRisLambers, J., 2003. Estimating population spread: what can we forecast and how well? Ecology 84, 1979e1988.
Colautti, R.I., Grigorovich, I.A., MacIsaac, H.J., 2006. Propagule pressure: a null model
for biological invasions. Biological Invasions 8, 1023e1037.
Cousens, R.D., Hill, J., French, K., Bishop, I.D., 2010. Towards better prediction of seed
dispersal by animals. Functional Ecology 24, 1163e1170.
Damschen, E.I., Brudvig, L.A., Haddad, N.M., Levey, D.J., Orrock, J.L., Tewksbury, J.J.,
2008. The movement ecology and dynamics of plant communities in fragmented landscapes. Proceedings of the National Academy of Sciences of the
USA 105, 19078e19083.
Davies, S., White, A., Lowe, A., 2004. An investigation into effects of long-distance
seed dispersal on organelle population genetic structure and colonisation
rate: a model analysis. Heredity 93, 566e576.
Denk, T., Bruelheide, H., 2006. There may be bias in R/P ratios (realized vs. potential
range) calculated for European tree species e an illustrated comment on
Svenning & Skov. Journal of Biogeography 33, 2013e2018.
Despland, E., Houle, G., 1997. Climate influences on growth and reproduction of
Pinus banksiana (Pinaceae) at the limit of the species distribution in eastern
North America. American Journal of Botany 84, 928e937.
Dullinger, S., Dirnböck, T., Grabherr, G., 2004. Modelling climate change-driven
treeline shifts: relative effects of temperature increase, dispersal and invasibility. Journal of Ecology 92, 241e252.
Engler, R., Guisan, A., 2009. MIGCLIM: predicting plant distribution and dispersal in
a changing climate. Diversity and Distributions 15, 590e601.
Estoup, A., Guillemaud, T., 2010. Reconstructing routes of invasion using genetic
data: why, how and so what? Molecular Ecology 19, 4113e4130.
Excoffier, L., Foll, M., Petit, R.J., 2009. Genetic consequences of range expansions.
Annual Review of Ecology, Evolution and Systematics 40, 481e501.
Franklin, J., 2010. Moving beyond static species distribution models in support of
conservation biogeography. Diversity and Distributions 16, 321e330.
Gallien, L., Münkemüller, T., Albert, C.H., Boulangeat, I., Thuiller, W., 2010. Predicting
potential distributions of invasive species: where to go from here? Diversity
and Distributions 16, 331e342.
Gibson, A.K., Mena-Ali, J.I., Hood, M.E., 2010. Loss of pathogens in threatened plant
species. Oikos 119, 1919e1928.
Gosper, C., Stansbury, C.D., Vivian-Smith, G., 2005. Seed dispersal of fleshy-fruited
invasive plants by birds: contributing factors and management options.
Diversity and Distributions 11, 549e558.
Hampe, A., Petit, R.J., 2005. Conserving biodiversity under climate change: the rear
edge matters. Ecology Letters 8, 461e467.
Hamrick, J.L., Trapnell, D.W., 2011. Using population genetic analyses to understand
seed dispersal patterns. Acta Oecologica 37.
Hansen, A.J., Neilson, R.P., Dale, V.H., Flather, C.H., Iverson, L.R., Currie, D.J., Shafer, S.,
Cook, R., Bartlein, P.J., 2001. Global change in forests: responses of species,
communities, and biomes. BioScience 51, 765e779.
Hewitt, G.M., 2000. The genetic legacy of the Quaternary ice ages. Nature 405,
907e913.
Higgins, S.I., Nathan, R., Cain, M.L., 2003. Are long-distance dispersal events in
plants usually caused by nonstandard means of dispersal? Ecology 84,
1945e1956.
Hofgaard, A., 1993. Seed rain quantity and quality, 1984e1992, in a high altitude
old-growth spruce forest, northern Sweden. New Phytologist 125, 635e640.
Holm, S.O., 1994. Reproductive patterns of Betula pendula and B. pubescens Coll.
along a regional altitudinal gradient in northern Sweden. Ecography 17, 60e72.
Hu, F.S., Hampe, A., Petit, R.J., 2009. Paleoecology meets genetics: deciphering past
vegetational dynamics. Frontiers in Ecology and the Environment 7, 371e379.
Huntley, B., Barnard, P., Altwegg, R., Chambers, L., Coetzee, B.W.T., Gibson, L.,
Hockey, P.A.R., Hole, D.G., Midgley, G.F., Underhill, L.G., Willis, S.G., 2010. Beyond
bioclimatic envelopes: dynamic species’ range and abundance modelling in the
context of climatic change. Ecography 33, 621e626.
Ibáñez, I., Clark, J.S., Dietze, M.C., 2008. Evaluating the sources of potential migrant
species: implications under climate change. Ecological Applications 18,
1664e1678.
Iverson, L.R., Schwartz, M.W., Prasad, A.M., 2004. How fast and far might tree
species migrate in the eastern United States due to climate change? Global
Ecology and Biogeography 13, 209e219.
Jablonski, L.M., Wang, X.Z., Curtis, P.S., 2002. Plant reproduction under elevated CO2
conditions: a meta-analysis of reports on 79 crop and wild species. New Phytologist 156, 9e26.
Jackson, S.T., Betancourt, J.L., Booth, R.K., Gray, S.T., 2009. Ecology and the ratchet of
events: climate variability, niche dimensions, and species distribution.
Proceedings of the National Academy of Sciences of the USA 106,
S19685eS19692.
Jalili, A., Jamzad, Z., Thompson, K., Araghi, M.K., Ashrafi, S., Hasaninejad, M.,
Panahi, P., Hooshang, N., Azadi, R., Tavakol, M.S., Palizdar, M., Rahmanpour, A.,
Farghadan, F., Mirhossaini, M.G., Parvaneh, K., 2010. Climate change, unpredictable cold waves and possible brakes on plant migration. Global Ecology and
Biogeography 19, 642e648.
Johnstone, J.F., Chapin, F.S., 2003. Non-equilibrium succession dynamics indicate
continued northern migration of lodgepole pine. Global Change Biology 9,
1401e1409.
Jongejans, E., Shea, K., Skarpaas, O., Kelly, D., Sheppard, A.W., Woodburn, T.L., 2008.
Dispersal and demography contributions to population spread of Carduus
nutans in its native and invaded ranges. Journal of Ecology 96, 687e697.
Jump, A.S., Mátyás, C., Peñuelas, J., 2009. The altitude-for-latitude disparity in the
range retractions of woody species. Trends in Ecology and Evolution 24,
694e701.
Kawecki, T.J., 2008. Adaptation to marginal habitats. Annual Review of Ecology,
Evolution and Systematics 39, 321e342.
Kellmann, M., 2004. Sugar maple (Acer saccharum Marsh.) establishment in boreal
forest: results of a transplantation experiment. Journal of Biogeography 31,
1515e1522.
Kinlan, B.P., Gaines, S.D., 2003. Propagule dispersal in marine and terrestrial environments: a community perspective. Ecology 84, 2007e2020.
Knowles, L.L., 2009. Statistical phylogeography. Annual Review of Ecology, Evolution
and Systematics 40, 593e612.
Kollmann, J., 2000. Dispersal of fleshy-fruited species: a matter of spatial scale?
Perspectives in Plant Ecology, Evolution and Systematics 3, 29e51.
Kuparinen, A., Katul, G., Nathan, R., Schurr, F.M., 2009. Increases in air temperature
can promote wind-driven dispersal and spread of plants. Proceedings of the
Royal Society B 276, 3081e3087.
Lachmuth, S., Durka, W., Schurr, F.M., 2010. The making of a rapid plant invader:
genetic diversity and differentiation in the native and invaded range of Senecio
inaequidens. Molecular Ecology 19, 3952e3967.
LaDeau, S.L., Clark, J.S., 2001. Rising CO2 levels and the fecundity of forest trees.
Science 292, 95e98.
LaDeau, S.L., Clark, J.S., 2006a. Elevated CO2 and tree fecundity: the role of tree size,
inter-annual variability and population heterogeneity. Global Change Biology
12, 822e833.
LaDeau, S.L., Clark, J.S., 2006b. Annual pollen production in Pinus taeda grown under
elevated CO2. Functional Ecology 20, 541e547.
Landhäusser, S.M., Deshaies, D., Lieffers, V.J., 2010. Disturbance facilitates rapid
range expansion of aspen into higher elevations of the Rocky Mountains under
a warming climate. Journal of Biogeography 37, 68e76.
Le Corre, V., Machon, N., Petit, R.J., Kremer, A., 1997. Colonisation with long-distance
seed dispersal and genetic structure of maternally inherited genes in forest
trees: a simulation study. Genetical Research of the Cambridge Philosophical
Society 69, 117e125.
Levey, D.J., Tewksbury, J.J., Bolker, B.M., 2008. Modelling long-distance seed
dispersal in heterogeneous landscapes. Journal of Ecology 96, 599e608.
Liepelt, S., Cheddadi, R., de Beaulieu, J.L., Fady, B., Gömöry, D., Hussendorfer, E.,
Konnert, M., Litt, T., Longauer, R., Terhurne-Berson, R., Ziegenhagen, B., 2009.
Postglacial range expansion and its genetic imprints in Abies alba (Mill.) a synthesis from palaeobotanic and genetic data. Review of Palaeobotany and
Palynology 153, 139e149.
Lischke, H., Zimmermann, N.E., Bolliger, J., Rickebusch, S., Löffler, T.J., 2006. TreeMig:
a forest-landscape model for simulating spatio-temporal patterns from stand to
landscape scale. Ecological Modelling 199, 409e420.
Magri, D., 2008. Patterns of post-glacial spread and the extent of glacial refugia of
European beech (Fagus sylvatica). Journal of Biogeography 35, 450e463.
Marsico, T.D., Hellmann, J.J., 2009. Dispersal limitation inferred from an experimental translocation of Lomatium (Apiaceae) species outside their geographic
ranges. Oikos 118, 1783e1792.
Martin, P.H., Canham, C.D., 2010. Dispersal and recruitment limitation in native
versus exotic tree species: life-history strategies and Janzen-Connell effects.
Oikos 119, 807e824.
McLachlan, J.S., Clark, J.S., Manos, P.S., 2005. Molecular indicators of tree migration
capacity under rapid climate change. Ecology 86, 2088e2098.
Magri, D., Vendramin, G.G., Comps, B., Dupanloup, I., Geburek, T., Gömöry, D.,
Lata1owa, M., Litt, T., Paule, L., Roure, J.M., Tantau, I., Van Der Knaap, W.O.,
Petit, R.J., De Beaulieu, J.L., 2006. A new scenario for the Quaternary history of
European beech populations: palaeobotanical evidence and genetic consequences. New Phytologist 171, 199e221.
Meier, E., Zimmermann, N., Lischke, H., Schmatz, D., 2011. Global change-induced
range shifts in European trees: assessing the influence of macroclimate,
competition and habitat connectivity. Global Ecology and Biogeography 20.
doi:10.1111/j.1466-8238.2011.00669.x.
Meunier, C., Sirois, L., Bégin, Y., 2007. Climate and Picea mariana seed maturation
relationships: a multi-scale perspective. Ecological Monographs 77, 361e376.
Midgley, G.F., Davies, I.D., Albert, C.H., Altwegg, R., Hannah, L., Hughes, G.O.,
O’Halloran, L.R., Seo, C., Thorne, J.H., Thuiller, W., 2010. BioMove: an integrated
platform simulating the dynamic response of species to environmental change.
Ecography 33, 612e616.
Midgley, G.F., Thuiller, W., Higgins, S.I., 2007. Plant species migration as a key
uncertainty in predicting future impacts of climate change on ecosystems:
progress and challenges. In: Canadell, J.G., Pataki, D.E., Pitelka, L.F. (Eds.),
Terrestrial Ecosystems in a Changing World. Springer-Verlag, Berlin, pp. 149e160.
Mitchell, C.E., Agrawal, A.A., Bever, J.D., Gilbert, G.S., Hufbauer, R.A., Klironomos, J.N.,
Maron, J.L., Morris, W.F., Parker, I.M., Power, A.G., Seabloom, E.W., Torchin, M.E.,
Vázquez, D.P., 2006. Biotic interactions and plant invasions. Ecology Letters 9,
726e740.
Murphy, H.T., VanDer Wall, J., Lovett-Doust, J., 2010. Signatures of range expansions
and erosions in eastern North American trees. Ecology Letters 13, 1233e1244.
Nakamura, M., Muller, O., Tayanagi, S., Nakaji, T., Hiura, T., 2010. Experimental
branch warming alters tall tree leaf phenology and acorn production. Agricultural and Forest Meteorology 150, 1026e1029.
Nathan, R., 2006. Long-distance dispersal of plants. Science 313, 786e788.
Nathan, R., Perry, G., Cronin, J.T., Strand, A.E., Cain, M.L., 2003. Methods for estimating long-distance dispersal. Oikos 103, 261e273.
Nathan, R., Schurr, F.M., Spiegel, O., Steinitz, O., Trakhtenbrot, A., Tsoar, A., 2008.
Mechanisms of long-distance seed dispersal. Trends in Ecology and Evolution
23, 638e647.
Nathan, R., Horvitz, N., He, Y., Kuparinen, A., Schurr, F.M., Katul, G.G., 2011. Spread of
North American wind-dispersed trees in future environments. Ecology Letters
14, 211e219.
Nogués-Bravo, D., 2009. Predicting the past distribution of species’ climatic niches.
Global Ecology and Biogeography 18, 521e531.
Parmesan, C., 2006. Ecological and evolutionary responses to recent climate change.
Annual Review of Ecology, Evolution, and Systematics 37, 637e669.
Parshall, T., 2002. Late Holocene stand-scale invasion by hemlock (Tsuga canadiensis) at its western range limit. Ecology 83, 1386e1398.
Pearson, R.G., Dawson, T.P., 2005. Long-distance plant dispersal and habitat fragmentation: identifying conservation targets for spatial landscape planning
under climate change. Biological Conservation 123, 389e401.
Petit, R.J., Bialozyt, R., Garnier-Géré, P., Hampe, A., 2004. Ecology and genetics of tree
invasions: from recent introductions to Quaternary migrations. Forest Ecology
and Management 197, 117e137.
Petit, R.J., Hampe, A., 2006. Some evolutionary consequences of being a tree. Annual
Review of Ecology, Evolution and Systematics 37, 187e214.
Petit, R.J., Hu, F.S., Dick, C.W., 2008. Forests of the past: a window to future changes.
Science 320, 1450e1452.
Pigott, C.D., Huntley, J.P., 1981. Factors controlling the distribution of Tilia cordata at
the northern limits of its geographical range. III. Nature and cause of seed
sterility. New Phytologist 87, 817e839.
Piotti, A., Leonardi, S., Piovani, P., Scalfi, M., Menozzi, P., 2009. Spruce colonisation at
treeline: where do those seeds come from? Heredity 103, 136e145.
Provan, J., Bennett, K.D., 2008. Phylogeographic insights into cryptic glacial refugia.
Trends in Ecology and Evolution 23, 564e571.
Ramakrishnan, A.P., Musial, T., Cruzan, M.B., 2010. Shifting dispersal modes at an
expanding species’ range margin. Molecular Ecology 19, 1134e1146.
Ray, R., Excoffier, L., 2010. A first step towards inferring levels of long-distance
dispersal during past expansions. Molecular Ecology Resources 10, 902e914.
Rejmanek, M., Richardson, D.M., 1996. What attributes make some plant species
more invasive? Ecology 77, 1655e1661.
Richardson, D.M., Allsopp, N., D’Antonio, C., Milton, S.Z., Rejmanek, M., 2000. Plant
invasions - the role of mutualisms. Biological Review of the Cambridge Philosophical Society 75, 65e93.
Rivalan, P., Frederiksen, M., Loïs, G., Julliard, R., 2007. Contrasting responses of
migration strategies in two European thrushes to climate change. Global
Change Biology 13, 275e287.
Schurr, F.M., Steinitz, O., Nathan, R., 2008. Plant fecundity and seed dispersal in
spatially heterogeneous environments: models, mechanisms and estimation.
Journal of Ecology 96, 628e641.
Seppä, H., Alenius, T., Bradshaw, R.H.W., Giesecke, T., Heikkilä, M., Muukkonen, P.,
2009. Invasion of Norway spruce (Picea abies) and the rise of the boreal
ecosystem in Fennoscandia. Journal of Ecology 97, 629e640.
Simberloff, D., 2009. The role of propagule pressure in biological invasions. Annual
Review of Ecology, Evolution, and Systematics 40, 81e102.
Skellam, J.G., 1951. Random dispersal in theoretical populations. Biometrika 38,
196e218.
Skov, F., Svenning, J.C., 2004. Potential impact of climatic change on the distribution
of forest herbs in Europe. Ecography 27, 366e380.
Slatyer, R.O., Noble, I.R., 1992. Dynamics of montane treelines. In: Hansen, A.J., di
Castri, F. (Eds.), Landscape Boundaries: Consequences for Biotic Diversity and
Ecological Flows. Springer-Verlag, New York, pp. 346e359.
Solomon, S., Qin, D., Manning, M., Chen, Z., Marquis, M., Averyt, K.B., Tignor, M.,
Miller, H.L., 2007. Climate Change 2007: The Physical Science Basis. Cambridge
University Press, Cambridge, UK.
Soons, M.B., Bullock, J.M., 2008. Non-random seed abscission, long-distance wind
dispersal and plant migration rates. Journal of Ecology 96, 581e590.
Soons, M.B., Heil, G.W., Nathan, R., Katul, G.G., 2004. Determinants of long-distance
seed dispersal by wind in grasslands. Ecology 85, 3056e3068.
Sork, V.L., Waits, L.P., 2010. Contributions of landscape genetics e approaches,
insights, and future potential. Molecular Ecology 19, 3489e3495.
Stiling, P., Moon, D., Hymus, G., Drake, B., 2004. Differential effects of elevated CO2
on acorn density, weight, germination, and predation among three oak species
in a scrub-oak forest. Global Change Biology 10, 228e232.
Storfer, A., Murphy, M.A., Spear, S.F., Holderegger, R., Waits, L.P., 2010. Landscape
genetics: where are we now? Molecular Ecology 19, 3496e3514.
Svenning, J.C., Normand, S., Skov, F., 2008. Postglacial dispersal limitation of
widespread forest plant species in nemoral Europe. Ecography 31, 316e326.
Svenning, J.C., Skov, F., 2004. Limited filling of the potential range in European tree
species. Ecology Letters 7, 565e573.
Tackenberg, O., 2003. Modeling long-distance dispersal of plant diaspores by wind.
Ecological Monographs 73, 173e189.
Taylor, C.M., Hastings, A., 2005. Allee effects in biogical invasions. Ecology Letters 8,
895e908.
Thompson, S., Katul, G., 2008. Plant propagation fronts and wind dispersal: an
analytical model to upscale from seconds to decades using superstatistics.
American Naturalist 171, 468e479.
Thuiller, W., Albert, C., Araújo, M.B., Berry, P.M., Cabeza, M., Guisan, A., Hickler, T.,
Midgley, G.F., Paterson, J., Schurr, F.M., Sykes, M.T., Zimmermann, N.E., 2008.
Predicting global change impacts on plant species’ distributions: future challenges. Perspectives in Plant Ecology, Evolution and Systematics 9, 137e152.
Trenberth, K.E., Jones, P.D., Ambenje, P., Bojariu, R., Easterling, D., Klein-Tank, A.,
Parker, D., Rahimzadeh, F., Renwick, J.A., Rusticucci, M., Soden, B., Zhai, B., 2007.
Observations: surface and atmospheric climate change. Climate Change 2007:
The Physical Science Basis. Cambridge University Press, Cambridge, UK.
Truong, C., Palmé, A.E., Felber, F., 2008. Recent invasion of the mountain birch Betula
pubescens ssp. tortuosa above the treeline due to climate change: genetic and
ecological study in northern Sweden. Journal of Evolutionary Biology 20,
369e380.
Turner, M.G., 2010. Disturbance and landscape dynamics in a changing world.
Ecology 91, 2833e2849.
Van der Putten, W.H., Macel, M., Visser, M.E., 2010. Predicting species distribution
and abundance responses to climate change: why it is essential to include biotic
interactions across trophic levels. Philosophical Transactions of the Royal
Society B-Biological Sciences 365, 2025e2034.
van Grunsven, R.H.A., van der Putten, W.H., Bezemer, T.M., Berendse, F.,
Veenendaal, E.M., 2010. Plant-soil interactions in the expansion and native
range of a poleward shifting plant species. Global Change Biology 16,
380e385.
van Grunsven, R.H.A., van der Putten, W.H., Bezemer, T.M., Tamis, W.L.M.,
Berendse, F., Veenendaal, E.M., 2007. Reduced plantesoil feedback of plant
species expanding their range as compared to natives. Journal of Ecology 95,
1050e1057.
Way, D.A., LaDeau, S.L., McCarthy, H.R., Clark, J.S., Oren, R., Finzi, A.C., Jackson, R.B.,
2010. Greater seed production in elevated CO2 is not accompanied by reduced
seed quality in Pinus taeda L. Global Change Biology 16, 1046e1056.
Will, H., Tackenberg, O., 2008. A mechanistic simulation model of seed dispersal by
animals. Journal of Ecology 2008 (96), 1011e1022.
Wirth, C., Lichstein, J.C., Dushoff, J., Chen, A., Chapin III, F.S., 2008. White spruce
meets black spruce: dispersal, postfire establishment, and growth in a warming
climate. Ecological Monographs 78, 489e505.