Download Plants & Ecology Range margins and refugia Johan Dahlberg

Range margins and refugia
by
Johan Dahlberg
Plants & Ecology
The Department of Ecology,
2013/1
Environment and Plant Sciences
Stockholm University
Range margins and refugia
by
Johan Dahlberg
Supervisors: Kristoffer Hylander &
Johan Ehrlén
Plants & Ecology
The Department of Ecology,
Environment and Plant Sciences
Stockholm University
2013/1
Plants & Ecology
The Department of Ecology, Environment and Plant Sciences
Stockholm University
S-106 91 Stockholm
Sweden
© The Department of Ecology, Environment and Plant Sciences
ISSN 1651-9248
Printed by FMV Printcenter
Cover: Lathyrus vernus at a south facing slope, a refugium in the middle of Sweden (the
county of Ångermanland), north of its main distribution range. Photo: Johan Dahlberg, 2012.
Sammanfattning
Arters utbredningsområden är begränsade av fysiska barriärer, arters spridningsförmåga,
abiotiska faktorer såsom klimat samt interaktioner mellan arter. Hur en art reagerar på
miljöfaktorer och biotiska faktorer bestämmer dess abundans, utbredning och avgränsning av
utbredning. Det finns fyra olika typer av respons på globala klimatförändringar. En population
kan acklimatiseras, anpassas, migrera eller dö ut. Under ogynnsamma förhållanden kan
populationer migrera och överleva i refugier med gynnsamma miljöförhållanden. Därefter kan
de återvända till deras förra utbredningsområden när förhållandena återigen har blivit
gynnsamma. Begreppet refugium har använts för storskaliga refugier såsom interglaciala och
glaciala refugier (makrorefugier) samt för småskaliga refugier såsom mikrorefugier.
Mikrorefugiers existens gynnas av att det lokala klimatet frikopplas från det regionala
klimatet eftersom detta buffrar mot klimatförändringar. Sådan frikoppling sker mest sannolikt
i heterogena landskap. När en art flyttar sitt utbredningsområde så kan nya refugier bildas vid
den
retirerande
utbredningsgränsen.
Makrorefugier
kan
bildas
från
artens
huvudutbredningsområde om det minskar.
Summary
Species ranges are restricted in distribution by physical barriers, dispersal ability, abiotic
factors such as climate and interspecific interactions. The responses of a species to
environmental conditions and biotic factors determine its abundance, distribution and range
limits. There are four possible responses for populations facing global climate change. They
can acclimate, adapt, shift their ranges or go extinct. During unfavorable conditions
populations may shift their ranges and survive in refugia with favorable environmental
features. Thereafter they might be able to return to their former distribution when the
conditions get favorable again. The term refugium has been used for large scale refugia such
as interglacial and glacial refugia (macrorefugia), and for small scale refugia such as
microrefugia. The existence of microrefugia is promoted by decoupling of the local climate
from the regional climate because this buffers against climate change. Such decoupling is
most likely to occur in heterogeneous landscapes. At a range shift, new microrefugia may
arise at the eroding edge, while macrorefugia may form from a contracting main (continuous)
range.
3
Introduction
An evolutionary perspective
In earth’s history there has been several periods with large species turnover, old species has
died out and new species has replaced the former (Willis & McElwain 2002). In fact, five
mass extinction events for the marine faunal record over the last 600 million years are clearly
defined (Raup & Sepkoski 1982), accompanied by high extinction numbers in the terrestrial
faunal record (Willis & McElwain 2002). Gould (1985) even proposes that mass extinction is
the punctuating events leading to speciation and so drives macroevolution in the animal
kingdom. Among plants, Willis and McElwain (2002) recognizes five major periods of
evolution and species turnover where the fossil records indicates more originations over
extinctions. They further suggest that increased atmospheric CO2 associated with each of five
pulses of global plate spreading might be the underlying cause behind these main events of
plant evolution.
The periods of great species turnover may have extraterrestrial causes or earth-bound causes.
The former includes large impacts from meteorites, comet storms, radiation from supernovae
and large solar flares, while the latter includes geomagnetical reversals, continental drift,
massive volcanism, sea-level change, global cooling and glaciation, and decreasing levels of
oxygen and/or salinity in the oceans. In excess of change in climate due to positional changes
of the land masses, continental drift may lead to increased CO2 levels. This is due to increased
mantle outgassing caused by increased volcanism and faster seafloor spreading (Willis &
McElwain 2002).
These extreme events caused large numbers of extinctions through large scale disturbance,
and subsequent, high rates of speciation has been observed. Extinctions may occur when
populations cannot migrate or disperse due to the rate or magnitude of the disturbance
(Dimichele et al. 1987). In contrast, populations exposed to smaller scale disturbance often
can avoid extinction through migration, survival in refugia, or adaption (Willis & McElwain
2002). During such exposure to smaller scale disturbances species may shift their ranges
during unfavorable conditions and return to their former distribution when the condition gets
favorable again (Willis & McElwain 2002).
4
Species ranges and refugia
The causes and consequences of species exposure to disturbances, in particular the one that
Willis and McElwain (2002) regard as small scale, will be further dealt with in this essay. It
covers the characteristics of species ranges and its special case, refugia, where populations can
survive during range contraction. To understand the characteristics of refugia it is necessary to
have knowledge of the wider concept of species ranges. In the context of climate change and
refugia it is especially interesting to further investigate the properties of range shifts. How can
species cope with climate change by shifting their ranges, adapt or acclimate? How and where
may refugia arise through range shifts?
Geographic ranges
Climate and other limiting factors
Species ranges are restricted in distribution by physical barriers, dispersal ability, abiotic
factors such as climate and interspecific interactions (Gaston 2003). Physical barriers may be
rivers, particularly large and fast-floating rivers, mountain chains (Gaston 2003), oceans,
human development (Mott 2010), topographic features in the sea (McClain & Hardy 2010),
transitions between freshwater and saltwater (Mott 2010), ocean currents (Won et al. 2003),
land masses (Vinogradova 1997) and large distances (Wright 1943). Physical barriers may
also be of periodical character, for example volcanic eruptions, flooding or fires (Mott 2010).
Physical barriers may influence the limitation of species ranges either directly or, more
commonly, indirectly through the spatial, climate gradients that accompany them (Mott
2010). These gradients may limit the ranges due to constraints in the environmental tolerances
or dispersal abilities of the species. The either direct or indirect effect of physical barriers on
dispersal can be range limiting for species with different dispersal capacities. For species with
poor dispersal ability, both small and large barriers may be limiting while species with an
effective dispersal may be restricted by large barriers (Gaston 2003; Mott 2010).
According to Gaston (2003) evidence for climate limiting of distribution can be divided in
two major parts. First, species ranges often coincide with specific climate conditions and
second, temporal range shifts often track changes in environmental conditions.
5
There have been many observations of how distributions are limited by climatic factors
(Gaston 2003). The first work that elucidated the role of climatic factors in restricting species
ranges was written by Grinnell in 1917. Often several climatic variables are significantly
related to the distribution pattern of a species. There are hundreds of possible combinations of
climatic variables; for example minimum, maximum and mean temperature (Gaston 2003).
For example the distribution of Ilex aquifolium is limited by the combination of mean
temperature in the coldest and warmest months. Additionally, this species is only present if
mean temperature of the coldest month exceeds -1 degrees Celsius (Iversen 1944). Other
evidence for climate as a range limiting factor are the observations of species that are
restricted to refugia with locally favorable microclimate, outside their continuous distribution
range, and species that decreases with depth or elevation towards higher latitudes. Also, there
are species that increasingly favors north or south facing slopes with changing latitude and
thereby maintains the experienced climatic regime (Gaston 2003).
There has been reliance in the climate as an important factor for species distribution. Several
studies have tried to reconstruct past patterns in climate by use of historical plant distributions
(Gaston 2003). Plant distributions have also been used to correct climate maps of recent years
(Boyko 1947).
The reliance of climate as a factor determining species ranges is coupled with several
problems. First, many climate variables covary. Second, the microclimate experienced by a
species may not be the same as the climate measured by weather stations. Third, there may be
indirect effects of climate on the distribution of species. This is explained by the fact that
climate factors may influence the distribution of resources, competitors, predators or parasites
which in turn affect the distribution of the studied species (Gaston 2003).
To assess the climate as a range limiting factor and exclude the possibility of a merely
coincidence between the climate and range limits of species, it can be appropriate to
demonstrate that the climate is unsuitable beyond the range limits of the species (Gaston
2003). Hutchins (1947) described two ways in which the climate may be unsuitable. Due to
environmental tolerance, it may directly kill individuals outside the range limit. Even though
many species tolerates larger range of climate conditions then encompassed by their normal
ranges, range limited by lethal climate factors has been observed (Gaston 2003). Additionally,
the climate could be unsuitable for the reproduction of the species or for stages in their life
6
cycle. Range limiting by climate unsuitable for reproduction or stages in the life cycle are
more common than limiting by mortality of adults due to climate (Gaston 2003). For example,
minimum temperature during the growing season is an important determinant of seed
mortality of forest trees in Sweden (Blennow & Lindkvist 2000). Plant species that at their
range limits fails to reproduce sexually, may survive by vegetative reproduction or since they
are long-lived (Gaston 2003). Therefore, the geographical difference between the
reproductive and distributional limit is likely to be bigger for long-lived than for short-lived
species. This can be demonstrated by the long-lived, broadleaved tree Tilia cordata, for which
the reproductive limit in UK is about 200 km south of its distributional limit. In contrast, in an
annual species with a short-lived seed bank, it is probable that the distributional and
reproductive limits are more evenly matched. For the long-lived species, the current northern
distributional limit probably reflects a previously warmer climatic period (Woodward 1997).
Following this, the probability that past events reflect the current range of a species increase
with longevity (Gaston 2003).
Hutchins (1947) especially considered temperature as the limiting climate factor. This is
generally seen as the most important climatic factor limiting species ranges (Gaston 2003).
For example, frost damage may have both short- and longterm effects on plants, as well as
evolutionary effects (Inouye 2000). Even though climate is an important range limiting factor
it is not obvious whether it is a primary or secondary cause of the range limits. It may be that
another factor than the climate has been crucial for determining the range limits of a species.
By evolution the species may have lost the physiological requirements to exist in the climate
outside its range limits, especially if the maintenance of these requirements is costly. This
leads to a tendency of coincidence between tolerated and experienced conditions (Gaston
2003).
Beside temperature there may be a range of other abiotic factors that could determine the
distribution of a species. For example, fire and other disturbances, trace metals, pH, salinity,
water availability, soils, geology, content of carbon dioxide and light (Gaston 2003). Water
balance is seen as critical for the distribution of vegetation, both at larger and smaller scales
(Gaston 2003). Furthermore, limitation by interspecific interactions may occur.
First, there is limitation of consumers by resources. For example a specialist consumer that is
restricted in distribution to the range of its host. Mostly, the range of the consumer is smaller
7
than the range of its host. This may be due to limitation by environmental factors (Gaston
2003) or low abundance and small size of host populations close to range margins (Kawecki
2008).
Second, already Darwin (1859) noticed that competitors may limit the range of species.
Connor and Bowers (1987) stated that interspecific competition plays an important role in
species distribution across different spatial scales. In fruitfly experiments it has been shown
that interspecific competition alters the distribution and abundance of the species (Davis et al.
1998). Bullock et al. (2000) showed that co-occurrence of two species of Ulex disappeared
when studied at finer scales. This shows that the scale of the analysis is important when
determining the cause of range limitation (Gaston 2003). Additionally, MacArthur (1972)
argued that many northern species are restricted to spread towards the south because of
competition. Hampe and Jump (2011) summarizes that interspecific competition often is
stressed to be the most important biotic factor influencing retraction of species low-latitudinal
range margins. However Gaston (2003) doubts that interactions (competitors or consumers) in
general are sufficient for determining range limits. Studies of palaearctic mammals reveals
that temperature range and habitat size (e.g. biomes) may be the most important range
limiting factors (Letcher & Harvey 1994). The combination of climatic factors and
competition might be a common cause of range limits. The role of competition cannot be
excluded even if the range limits coincide with specific climate conditions (Gaston 2003).
Third, limiting of the consumed by predation or parasitism is often unlikely because the
existence of the predator or parasite relies on their prey or host. It is unlikely that the host or
prey goes extinct before the predator or parasite goes extinct or switches resource (Gaston
2003). However, Hochberg and Ives (1999) showed with a mathematical model that a natural
enemy can enforce a range limit. They also observed that a predator may limit its prey by
strong influence on its reproductive rate. Further on, the density of one of two prey species
can depend on the rate of predation. During a high rate of predation, species a can be a
stronger competitor for resources and therefore outcompete species b. Conversely, during a
low rate of predation, species b may be dominant over species a (Holt & Barfield 2009).
Additionally, the struggle to avoid the predator can be regarded as interspecific competition
(Williamson 1957). Because predators/parasites may be lacking at range edges (Hodkinson
1999) it is more likely that the prey or host can avoid being consumed in these areas (Gaston
2003). Total exclusion by predator/parasites is more likely if the prey or host has limited
8
dispersal abilities (Gaston 2003). Lastly herbivores may influence the distribution of their
resources (Gaston 2003).
There has been much debate over the relative importance of abiotic factors and biotic factors
for range limits (Gaston 2003). On one hand, abiotic factors may lead to stress at range edges,
reduced competitive ability and thereby increased vulnerability to biotic factors such as
competition or pathogens. On the other hand, individuals often are scarce at range edges
which render small effects from biotic factors. Additionally, facilitation, i.e. positive
interactions between organisms, may enlarge the realized niche of a species, sometimes even
to a potentially larger size than the fundamental niche (Bruno et al. 2003).
According to Salisbury (1926) many factors limit species ranges in contrast to the ideas of
Twomey (1936) that only very few factors limit species ranges. Gaston (2003) expand upon
Salisburys statement. First, range limits may be determined by interactions of many factors.
Second, there may be a temporal variation of factors limiting a range. Third, it is almost
certainly a norm that the range limiting factors may be different from one area to another.
Fourth, the species characteristics may vary over space because the range size may be larger
than the dispersal distances. In conclusion, both abiotic and biotic factors are important for
setting the range borders of species.
Austin et al. (1984) describes three kind of environmental gradients: a. indirect or complex
gradients (e.g. altitude) – other factors that covary with these have the direct influence on
growth. b. direct gradients (e.g. pH) – factors with direct effect on growth. c. resource
gradients – factors that are used as resources. The response of species abundance to
environmental gradients is known as response curves. Abundance of species tends to peak at
intermediate, favorable levels of these gradients (Gaston 2003). In other words, they have
hump-shaped response curves. More realistic, the response curve consists of several
abundance peaks which declines towards the range margins.
The spatial distribution of abundance is determined by the species optimum response surfaces
and their local population dynamics. The optimum response surface can be regarded as the
abundance structure of a species range that reflects the environmental gradients in all
directions from the point of highest abundance (Hengeveld 1990). Where the environment is
favorable the abundance is high and vice versa. The abundance structure will change with
9
spatial and temporal variations in the environmental conditions. Therefore, many different
shapes of the abundance structure may occur due to the sensitivity of species to specific
environmental conditions. The optimum response surface model has several assumptions
which may be violated. For example they assume that the population density is coupled with
favorable habitat conditions. In fact, there may be a decoupling between some habitat
conditions and abundance, especially if the environment is strongly seasonal, temporally
unpredictable or spatially patchy, and for generalists, long-lived species or species with high
reproductive capacity (Gaston 2003). Also, the source-sink dynamics can lead to high
abundance in the low quality sinks (Pulliam 1988). Another assumption is that species
response to environmental factors is constant in space. It has been shown that there may be
adaption and selection as a consequence of abiotic and biotic conditions, especially during
range expansion (Hewitt 2000). In addition, the assumption that ecological conditions become
less favorable towards range edges may not be true. According to Soulé (1973) not all
peripheral populations experience less favorable conditions and not all populations with less
favorable conditions are located at range margins.
In conclusion, the responses of a species to environmental conditions and biotic factors
determine its realized niche. They also set the species abundance, distribution and range
limits. Additionally, these structures are influenced by source-sink dynamics and spatial
variation in the influence of these conditions on individuals with different genetics (Gaston
2003).
Edge processes
At range edges species often resides in specific habitats or microhabitats. This might be due to
a declining number of individuals towards the range edges and therefore by chance in a
smaller number of habitats, frequently in the most widely distributed habitats where the
species can exist. Sometimes, these habitats are atypical for the species compared to the
habitats occupied elsewhere. For, example Picea rubens occurs in bogs and adjacent upland
slopes at its lower elevational range margin, although bogs is an unusual habitat in its main
range (Webb et al. 1993). This might reflect changing conditions at the range margin, either in
the typical or in the atypical habitats of a species, or it might reflect the absence of typical
habitats at the range margin. Further on, there are many observations that habitat shifts at
range edges are systematic. For example, on the northern hemisphere there can be a shift in
distribution to south facing slopes with favorable microhabitats at the northern range limit of a
10
species. Microhabitats are maybe most apparent in transitions zones, areas where several
range margins meet. Therefore they possess many microhabitats and high species richness
(Gaston 2003).
However, local abundance of species may not decrease towards the range edge, instead they
might be more patchily distributed. Also, it is unlikely for the abundance to decline towards
range edge for expanding populations, for populations where individuals move unidirectional
and for populations disrupted by physical barriers (Gaston 2003).
The limiting factors at range edges affect the vital rates of the populations such that for most
of the time the criterion below isn’t met, i.e. the result of b – d + i – e is smaller than zero
instead of larger than or equivalent to zero. b is the number of births in the population, d is the
number of deaths, i is the number of immigrants and e is the number of emigrants. Small
changes in these variables may determine range edges (Gaston 2003).
b–d+i–e≥0
According to several papers, the population dynamics towards range edges are dependent on
abiotic factors and less density-dependent (Gaston 2003). Gaston (2003) concludes that less
density-dependent populations at range margins might possess greater temporal variation in
population size. This in turn could lead to greater extinction risk for margin populations, a
circumstance that has been commonly observed (Gaston 2003).
Multiple populations or metapopulation structure are more likely at range edges because of
more fragmented abundance structures. Further on, the number of establishments minus the
number of extinctions is less than zero at and beyond the range edge (Gaston 2003). This
relationship has been further analyzed by Carter and Prince (1981) as follows. For the species
to spread, the rate of colonizable sites that becomes colonized must be positive (for the
species to survive, the rate must be equal to or greater than zero). This can be written as
do / dt > 0
where o is the number of colonizable sites that are occupied.
11
Further on, this requires that
a≥δ/β
if
do / dt = βao – δo
where a is the number of unoccupied colonizable sites available, β is the rate at which
colonizable sites become occupied and δ is the rate at which colonized sites cease to be
occupied.
Building on Levins metapopulation model (Levins 1969), Holt & Keitt (2000) shows that a
species will be absent from all points along a smooth environmental gradient x if
k(x) < e(x)/c(x)
where k is the fraction of potentially colonizable sites, e is the extinction rate (per colonized
site) and c is the colonization rate of empty, colonizable sites (per colonized site). Even if the
conditions are held constant a range limit could be reached if the number of colonizable sites
declines (Holt & Keitt 2000). Furthermore, species with relatively lower extinction rate may
survive closer to unfavorable climate where there are relatively fewer potentially colonizable
sites (Gaston 2003). A range limit will arise if the colonization rate declines while k and e are
held constant (Holt & Keitt 2000). Declining colonization rate may be due to reduced
population size with fewer potential colonists and reduced successful dispersal by less
favorable environmental conditions (Holt & Keitt 2000). Gaston (2003) concludes that
changes in whichever of these three variables (k, e and c) may result in a range limit and that
all three variables need to be studied to reveal the cause of range limitation.
Evolutionary adaptions that allow for range expansion without changes in the environmental
conditions seem to be rare (Eldredge 1997). There may be several reasons why a species
doesn’t expand its range beyond the limits set by abiotic and biotic factors (Hoffmann &
Blows 1994; Hoffmann & Parsons 1997). First, there may be low heritabilities of the traits
that determine range boundaries. In marginal populations this might be explained by low
12
genetic variation due to small population size, directional selection or large environmental
variability. Second, this may be explained by genetic interactions as follows. Evolution of
multiple traits is required for range expansion due to covariance in limiting environmental
factors. Also, there can be genetic trade-offs between fitness in stressful and favorable
environments. The possession of genes that favors species in stressful conditions can be costly
in the more frequent favorable conditions. Third, the effect of deleterious mutation may be
enhanced under stressful conditions (Gordo & Campos 2008), although the opposite has been
showed by Kishony & Leibler (2003). In addition, genotypes favored at range margins may
be replaced by gene flow from central range populations (Kirkpatrick & Barton 1997).
However, Gaston (2003) claims that this gene flow seems too small for such a replacement of
genes.
Climate change and range shifts
There are four possible responses for any species facing global climate change. They can
acclimate by phenotypic plasticity (Pfennig et al. 2010), adapt through genetic evolution
(Davis & Shaw 2001), shift their ranges (migrate) to follow the shift in favorable climate
conditions (Parmesan 2006) or go extinct. The term range shift has been used for expansions,
contractions and movement of species ranges (Parmesan et al. 2005; Sorte et al. 2010).
The earth has faced frequent climate change during its history. During the Pleistocene there
has been a time of constant change in climate with glacials and interglacials shaping the
landscape and species ranges (Beatty & Provan 2010). According to fossil pollen data and
macrofossil records there has been major range shifts during the glacials and interglacials of
the Quaternary period (Petit et al. 2008). Climate change between glacials and interglacials
has resulted in both latitudinal and altitudinal range shifts (Hewitt 2004). Many species have
migrated during glacials, survived in refugia, and later recolonized previous occupied areas
during subsequent interglacials. In fact, migration has been the usual response to climate
change during the Quaternary (Mott 2010).
Also, the recent anthropogenic climate change has leaded to observed range shifts in both
animal and plants (Parmesan 2006). Many species preferring cooler climate have shifted their
distributions towards higher latidudes or altitudes (Parmesan 2006). Already in the 1940s,
Ford (1945) observed northwards range shifts in butterflies in England due to warmer summer
13
temperatures. During anthropogenic climate change the range shifts are expected to occur
towards the poles or towards higher altitudes (Parmesan 2006).
Models of future scenarios predict distribution shifts during the decades to come (Parmesan &
Yohe 2003; Thuiller et al. 2008; Pereira et al. 2010). However, caution is needed because
there is an individualistic response to climate change among species (Gaston 2003). Because
of climate change, but maybe not only for this reason, species assemblages vary over time
(Gaston 2003). Also, range shifts with other causes than temperature has been observed. For
example, tracking of water balance may be the reason for range shifts among Californian
mountain plants (Crimmins et al. 2011).
The colonization process during climate change can be described by the leading edge model
of colonization. In this model the expansion of the species range is mostly controlled by longdistance dispersal from the range front. The subsequent population growth is exponential
(Hampe & Petit 2005).
Refugia
Different types of refugia, what do we mean?
The concept of refugia was originally used for glacial refugia, locations where species
survived the glacial periods during the Quaternary (Blytt 1876; Warming 1888; Sernander
1896; Lindroth 1931; Dahl 1946; Heusser 1955; Rundgren & Ingólfsson 1999; Brochmann et
al. 2003; Marko 2004; Schönswetter et al. 2004; Bennett & Provan 2008). Heusser (1955)
was first in using the latinized form of the word refugia (Bennett & Provan 2008) when he
searched pollen profiles in peat for plants surviving the last glacial on the Queen Charlotte
islands in Kanada. Later on the usage of the term refugia has been widened. Billings (1974)
and Mac-Vean and Schuster (1981) used the term interglacial refugia. At around the same
time the term was introduced for areas that escape fire and to which species later can recolonize (Zackrisson 1977; DeLong & Kessler 2000; Clarke 2002; Hylander & Johnson 2010)
and for habitats in streams protected from disturbances such as fast flowing water, dry periods
and ice cores (Williams & Hynes 1974; Sedell et al. 1990; DoleOlivier et al. 1997; Matthaei
et al. 2000; Taylor et al. 2006). In later years, the term has also been used for refugia from
current climate change, areas where conservation should be prioritized to limit the effects of
14
climate change (Ashcroft 2010), and for refugia from other forms of stress and disturbances
(Schmalholz 2007). Further on, different locations of refugia can be addressed as in situ or ex
situ refugia (Fig. 1). An in situ refugium constitute a part of the previous, wider distribution
range of a population. An ex situ refugium on the other hand, is located outside the previous,
wider distribution of a population, i.e. a place where the species didn’t occur before. Both of
these expressions has been used for glacial refugia and for potential, future refugia
(Holderegger and Thiel-Egenter 2009; Ashcroft 2010).
Figure 1.
An in situ refugium is located in the
former distribution range of the species,
while an ex situ refugium is located
outside the former distribution range.
This broadening of the term refugia and the inconsistency in its definition has potentially
decreased its usefulness (Bennett & Provan 2008). Therefore, this essay describes different
contexts in which the term refugia have been used. This information can be valuable when
using the term in specific studies.
It is clear that refugia may arise when species ranges contracts. Often this is associated with
the expansions and contractions of species ranges during Quaternary glacial and interglacial
periods (Stewart et al. 2010). Refugia may also arise during even longer time periods of
climate change caused by for example plate tectonics (Ledru et al. 2007), or as a consequence
of range contraction during the ongoing climate change (Ashcroft 2010). The reason for the
contraction is most likely to be some sort of disturbance at varying scales (Schmalholz 2007)
which makes the environment, except for the refugia, unsuitable for occupancy.
15
In other words, the definition of refugia/refugium mostly aims at the area where the species
remains after contraction (Sedell et al. 1990; Camp et al. 1997; Schmalholz 2007; Rull 2009).
In addition, the definitions of Sedell (1990) and Schmalholz (2007) includes that refugia
house populations that are important for re-colonization of the earlier occupied habitats.
Lancaster and Belyea (1997) have a broader view by stating that a refugium is a place or time
where the negative effects of disturbance are lower than in the surrounding area or time.. In
contrast, Bennett and Provan (2008) suggests that the term refugia should be replaced by the
term bottleneck when aiming at the abundance of species. The authors think that this term
better describes the continuing process that species goes through when contracting to a
refugium before later re-colonization of the previous occupied area. Stewart et. al. (2010)
excludes bottlenecks from their definition. They mean that bottlenecks don’t entail range
contraction but may result from it. Stewart et. al. (2010) points out Quaternary refugia and
defines these as “the geographical region or regions that a species inhabits during the period
of a glacial/interglacial cycle that represents the species’ maximum contraction in
geographical range”. In this definition it is added that refugia should be the area under
maximum contraction. Hampe and Jump (2011) defines refugium as an area with a climate
relict population, a population that persists in an area with suitable climate space surrounded
by unsuitable climatic conditions. He points out microrefugia as a small area with local
favorable environmental features, in which small populations can survive unfavorable periods
outside their main distribution range, protected from the unfavorable regional environmental
conditions.
It seems for me that a suitable definition for the term refugia could be: refugium is an area
with favorable environmental features, in which a population can survive after contraction of
its range due to unfavorable environmental conditions in the surroundings. This definition
resembles Rulls (2009) definition of microrefugia which is presented below (see
Microrefugia). The differences are that all sorts of refugia is included in the presented
definition. Also, it is clarified that a refugium should originate from a contracting phase. This
follows both Rull (2010) and Stewart et al. (2010). In contrast to them, I suggest that refugia
also can be expanding by migration or dispersal of the populations. ‘Population’ is used in the
definition to exclude individual shelters from for example predation which instead might be
called refuges (Ashcroft 2010). It is also clarified that the unfavorable, environmental
conditions are the cause of the isolation. This excludes populations that have been isolated
due to other factors than unfavorable conditions, for example due to recent dispersal.
16
Due to the various meanings of the term refugia in different studies, Bennet & Provan (2008)
thinks that we need to use more descriptive terms and clearly defined contexts. For example
terms such as interglacial microrefugia (Rull 2009) or microclimatic refugia (Trivedi et al.
2008) might be used. I agree with clarifying the context but it could be contra productive to
use more terms. A solution proposed by Rull (2010) is to, instead of terms such as
microrefugia and relicts, always use the term refugia (either glacial or interglacial) to avoid
confusion.
In short, the term refugia and its different forms have been used at many different spatial
scales. Descriptions of some large and small scale refugia follow. Also the climatic
prerequisites of microrefugia and their role at range shifts are discussed. Only terrestrial
refugia are considered.
Large scale refugia
The Milankovitch cycles:
For at least 200 million years (Jurassic) and probably throughout geological time there have
been regular intervals with changes in the amount and distribution of incoming solar radiation
(Willis & McElwain 2002). These cyclic intervals are called Milankovitch cycles
(Milankovitch 1930) and occurs at intervals of around 413, 100, 41, and 24-19 thousand years
(Hays et al. 1976; Berger 1977; Fischer 1986; Imbrie et al. 1993). The reduction in solar
radiation at these intervals leads to global climatic change, at some intervals with cooling and
formation of ice caps by the poles (Bradley 1999). There are different climatic/geological
phenomena that regulate the impact of the Milankovitch cycles, and during some periods
there were no buildup of ice caps (Frakes et al. 1992; Willis & McElwain 2002). These
different impacts may be related to much larger intervals of approximately 300 million years
characterized by ‘icehouse’ or ‘greenhouse’ mode (Fischer 1981, 1982; Frakes et al. 1992)
within which the Milankovitch cycles are nested (Willis & McElwain 2002). During the last 2
million years (the Quaternary) the Milankovitch cycles have been expressed as
glacial/interglacial cycles (Bennett 1990).
Glacial refugia
Glacial refugia are places where species survived the ice ages. Mostly the term has been used
for the most recent glaciation (Holderegger & Thiel-Egenter 2009). Originally, glacial refugia
17
were identified with palaeoecological evidence (Huntley & Birks 1983; Bennett et al. 1991),
but since around 1990 also phylogeographic studies has been used in the identification
(Hewitt 1996, 1999; Hewitt 2000; Bennett & Provan 2008). Together with the fossil record
they have showed that many extant populations of primarily temperate taxa are derived from
southern refugia (Hewitt 1996; Taberlet et al. 1998; Hewitt 1999; Hewitt 2000; Jackson et al.
2000; Lacourse et al. 2005; Soltis et al. 2006). Often these glacial refugia comprise the
southern part of the interglacial distribution of the species, in Europe mainly mountainous
regions within the Balkan, Iberian and Italian peninsulas (Bennet et al. 1991; Stewart et al.
2010) and in southeastern U.S. (Jackson et al. 2000). Compared with Iberia and Balkan, the
role of the Italian peninsula as a source for recolonization is limited due to the barrier exerted
by the Alps (Taberlet et al. 1998). Glacial refugia in European, southern regions followed by
interglacial re-colonization of northern areas are a general pattern for several species groups,
for example plants, insects and vertebrates (Hewitt 1999, 2004). The forests of the current
interglacial period became established in northern Europe due to expanding populations from
glacial refugia (Anderson et al. 2006; Cheddadi et al. 2006). In recent years, analogous
northern refugia have been recognized at the southern hemisphere (Byrne 2008).
The combining of genetic data with fossil records has also revealed glacial refugia closer to
the ice cap. Probably trees survived in glacial refugia only tens of kilometres south of the ice
sheet in North America (Cheddadi et al. 2006; Shepherd et al. 2007), while more cold-adapted
species even survived in refugia north of the ice (Stewart et al. 2001; Pruett & Winkler 2005;
Anderson et al. 2006). These higher latitude, isolated, glacial refugia are distinguished by
Stewart et al. (2010) as cryptic northern refugia (see also Microrefugia).
Holderegger and Thiel-Egenter (Holderegger & Thiel-Egenter 2009) suggests three main
types of glacial refugia for species currently living above the timber line in mountains.. These
terms are Nunatak glacial refugia, Peripheral glacial refugia and Lowland glacial refugia.
Nunataks are glacial refugia on mountain peaks above glaciers in the core of mountain ranges
(Blytt 1876; Brochmann et al. 2003; Crawford 2008; Holderegger & Thiel-Egenter 2009).
Peripheral glacial refugia are used for areas, located at the edge of mountain ranges, in which
mountain species survived (Tribsch & Schonswetter 2003; Schonswetter et al. 2005;
Holderegger & Thiel-Egenter 2009). Lowland glacial refugia were placed outside both
mountain ranges and the ice sheet (Holderegger & Thiel-Egenter 2009).
18
Interglacial refugia
Studies have showed increase in population sizes of cold-adapted species during the
beginning of the last glaciation (Stewart et al. 2010). Furtheron, several tundra and steppe
species were more widespread during the last glaciation (Bennett & Provan 2008). This is the
case for Dryas octopetala in Europe. This species was widespread throughout the lowlands of
central and parts of northern Europe towards the end of the last glaciation. Now it has a
disjunct European distribution restricted to the northernmost and alpine regions (Godwin
1975). Another example is the arctic fox Alopex lagopus that was distributed over large parts
of central and northeastern Eurasia during the last glacial maximum. Now it is confined to the
tundra regions of the northern hemisphere (Dalén et al. 2007; Bennett & Provan 2008). This
supports the hypothesis that a high proportion of cold-adapted species contracts to refugia
during interglacials. Today, many arctic species are restricted to interglacial refugia in the
high-latitude, Polar Regions, for example muskox and arctic fox (Stewart et al. 2010). These
species that are restricted to interglacial refugia during the current interglacial will be under
additional stress when temperature increases due to climate change (Ashcroft 2010). Stewart
(2010) divides interglacial refugia in polar refugia and cryptic southern refugia (see
Microrefugia)
Small scale refugia
Microrefugia
Rull (2009) distinguish the terms macrorefugia and microrefugia. He points out microrefugia
as a small area with local favorable environmental features, in which small populations can
survive unfavorable periods outside their main distribution range (the macrorefugium),
protected from the unfavorable regional environmental conditions. In this definition
macrorefugium (synonymous to refugia) is linked to glacial–interglacial alternation while
microrefugium includes several different terms such as for example ‘microrefuges’, ‘cryptic
refugia’, ‘northern refugia’, ‘isolated microhabitats’, ‘relict isolates’, ‘sparse stands’, ‘humid
microsites’ and ‘interglacial refugia’.
Cryptic refugia can be viewed as small areas with sheltered topography and stable
microclimate, mainly in montane regions, earlier considered as inhospitable (Bennett &
Provan 2008; Stewart et al. 2010). They are scattered outside their macrorefugia during
glacials or interglacials (Provan & Bennett 2008; Stewart et al. 2010). Cryptic northern
19
refugia for mainly temperate taxa are situated in glacial refugia north of their southern
macrorefugia during glacials. Analogous, southern cryptic refugia for cold-adapted species
are located in interglacial refugia at lower latitudes, presumably mountain areas, south of their
northern macrorefugia (Stewart et al. 2010). Rull (2010) summarizes that cryptic refugia
refers to our incapability of knowing the correct location of a given refugia.
Cryptic northern refugia were introduced as a possible solution to Reid’s paradox, the
discrepancy between interglacial migration rates and the dispersal capacity of trees, because
they might allow for local dispersal (Stewart & Lister 2001; McLachlan et al. 2005; Pearson
2006; Birks & Willis 2008; Provan & Bennett 2008; Dobrowski 2011). The detection of
cryptic refugia with palaeoecological methods, especially with pollen data, might be difficult
because of their local and small character (Willis et al. 2000; Birks & Willis 2008). Anyway,
cryptic refugia have been indicated through palaeoecological methods, mainly with the help
of macrofossils (Willis et al. 2000; Willis & van Andel 2004; Birks & Willis 2008), and their
existence have been further supported through the use of phylogeography (Cruzan &
Templeton 2000; Provan & Bennett 2008; Stewart et al. 2010). The rising evidence for cryptic
refugia means that the migration capacity of deciduous trees might be smaller than previous
thought. (Petit et al. 2008).
Climatic prerequisites for microrefugia
Climatic factors may limit refugia either by directly limiting the refugial population, or
indirectly by restricting antagonistic species or a biotic factor that is required for the survival
of the refugial population (Hampe & Jump 2011). In this chapter I will focus on the climatic
prerequisites for microrefugia.
Air temperature is the most important factor in mountain climate (Barry 2008; Dobrowski et
al. 2009) regarding its influence on ecosystem processes (Dobrowski et al. 2009).
Temperature is influenced by regional and local controls. Regional controls may be
circulation patterns, distance to the sea and latitude while local patterns include slope and
aspect, elevation, solar insolation, topographic convergence and others (Dobrowski et al.
2009). Often, elevation has been regarded as the most important factor controlling
temperature in areas with complex terrain. However, Vanwalleghem & Meentemeyer (2009)
showed that both topographical and ecological factors such as forest cover regulate the
temperature.
20
The finescale variation in solar heat transfer influence the temperature regimes in areas with
complex terrain (Fridley 2009). The term topoclimate, derived by Thornthwaite (1953), is the
in situ experienced climate by an organism, a sum of the regional and the local climates
(Dobrowski 2011). Topoclimate and edaphic conditions sets the physical environment
experienced by species (Dobrowski 2011), for example in microrefugia. The climatic
prerequisites of microrefugia require knowledge of present and future regional climate, how
regional climate limits species ranges, and how the terrain can modify the regional climate so
microrefugia can persist (Dobrowski 2011).
According to Dobrowski (2011) there are several factors that promote decoupling of the local
climate from the regional climate and by that also promote the existence of microrefugia.
These are cold air drainage, elevation and slope and aspect. In addition, the decoupling may
arise due to microtopography within a slope (Scherrer & Körner 2010), edaphic conditions,
water table or vegetation characters (Spitzer & Danks 2006; Suggitt et al. 2011). A discussion
of these decoupling factors follows.
Cold air drainage
Convergent environments have lower minimum temperatures than the surroundings due to
cold-air drainage and temperature inversions. Therefore, the local climate is decoupled from
the regional climate at these sites. Due to the decoupling from the regional climate with low
minimum temperatures, convergent environments are the most potential areas for
microrefugia. This is also true for mesophilous species due to the accumulation of water and
soil at the bottom of terrain depressions (Dobrowski 2011).
When the temperature cools down after sunset cold air drains into convergent environments,
especially in calm weather (Geiger 1950; Whiteman 1980; Lindkvist et al. 2000; Dobrowski
2011). The temperature then increases with altitude, a phenomenon called inversion.
Decoupling from the free atmosphere arises when the vertical mixing of air is absent (Daly et
al. 2010; Dobrowski 2011). Cold air pooling is common in sheltered positions such as valleys,
basins, sinks and other depressions in mountain areas (Dobrowski 2011). The magnitude and
persistence of an inversion is determined by the amount of incoming solar radiation and to
which extent the local climate mixes with the regional climate due to wind effects. These
factors depend on topographical characters (Whiteman 1982; Muller & Whiteman 1988;
Colette et al. 2003; Whiteman et al. 2004; Dobrowski 2011). Inversion mostly occurs in
21
nighttime, but could also last 2 to 5 hours after sunrise (Whiteman 1982; Muller & Whiteman
1988; Whiteman et al. 2004). The modeling of cold-air drainage and estimates of minimum
temperature is improved by taking surface water accumulation factors into account
(Dobrowski 2011).
Elevation
Elevation in itself is not a good predictor for minimum temperature at sites where a varying
topography affects the local climate in different ways (Lookingbill & Urban 2003; Dobrowski
et al. 2009; Dobrowski 2011). Mountain peaks are exposed to wind and drained which leads
to a climate that is more often coupled with the regional climate then at protected, wetter sites
further down the slopes (Pepin & Seidel 2005; Dobrowski 2011). Therefore, without
combining it with other topographic factors, elevation is a poor predictor of the degree of
decoupling from the regional climate and thus of the location of microrefugia (Pepin & Seidel
2005; Dobrowski 2011).
Slope and aspect
Slope and aspect exhibits varying exposure to incoming solar radiation and wind which are
factors that influence air temperature and water availability (Dobrowski 2011). For example,
south-facing slopes have often been addressed as location for microrefugia. The incoming
solar radiation in the northern hemisphere is highest on southwest-facing slopes and lowest on
northeast-facing slopes, which leads to gradients of air and soil temperatures, humidity and
soil moisture (Hutchins et al. 1976; Xu et al. 1997; Hutchinson et al. 1999). Additionally,
microtopography within a slope has very strong effects on local temperature due to varying
microexposure (incoming solar radiation), cold air flows and snow cover (Löffler et al. 2006;
Scherrer & Körner 2010).
It seems that the daily maximum temperatures are more controlled by incoming solar
radiation than the minimum temperatures (Dobrowski 2011). This is due to that the daily
minimum temperatures are foremost controlled by moving, cold air masses, and only
indirectly by radiation (Bergen 1968; Manins & Sawford 1979; Fridley 2009). Therefore,
populations in microrefugia on south-facing slopes are more limited by snow, ice and seasonlength then by minimum temperature (Dobrowski 2011). Furthermore, the cloud cover has a
dampening effect on solar radiation, and also the solar radiation changes from short-wave to
latent at wet sites due to high soil moisture and canopy cover (Dobrowski 2011). Therefore,
22
the slope and aspect has a bigger effect on local temperature in arid sites than in wetter areas
(Fridley 2009).
The effect of slope and aspect on water availability is higher than on local temperature. The
evapotranspiration (and the water balance) is affected by slope and aspect through varying
shortwave radiation and wind exposure (Hupet & Vanclooster 2001; Gong et al. 2006;
McVicar et al. 2007; Dobrowski 2011). Also, soil moisture and groundwater level is affected
by slope and aspect (Hutchinson et al. 1999; Zinko 2006). Soil moisture and near-ground
humidity influences transpiration and evaporation and thus the temperature. The daytime
maximum temperature is lowered by soil moisture (Dai et al. 1999) because wet surfaces are
dried out before warming (Fridley 2009). This limits the heat carrying capacity of the soil
(Geiger et al. 2003).
The dampening effect of soil moisture on nighttime minimum
temperature is less pronounced (Dai et al. 1999), but soil moisture may buffer against cold
extremes (Geiger et al. 2003). Mainly because of the large effect of slope and aspect on water
availability and the decrease of short-wave radiation in mesic regions (Dobrowski 2011),
slope and aspect are more important for the location of microrefugia in arid regions than in
temperature limited regions. For example, the use of depressions as refugia during the glacial
suggests water availability as a limiting factor instead if minimum temperature (Dobrowski
2011).
Also, the duration of the snow cover is influenced by aspect. After canopy cover, differences
in site aspect is the most important factor for duration of the snow cover. The effects of these
factors on snow cover are mainly driven by their influence on incoming solar radiadion
(Coughlan & Running 1997). The effect of aspect on snowpack is most pronounced at lower
elevations where the solar angle is lower early in the season (Coughlan & Running 1997).
Duration of the snow cover is one of the factors controlling local temperature (Löffler et al.
2006).
Vegetation cover, water table and edaphic conditions
The vegetation cover and the water content in plants can have a significant effect on
temperature regimes (Fridley 2009). A forest canopy dampens the diurnal and seasonal
temperature variation as compared to the variation in the free atmosphere (Fridley 2009).
Additionally, it has been showed that higher vegetation height in heathlands reduces
temperatures close to the ground (Thomas et al. 1999).
23
Sites with extreme water surplus (such as high elevations and protected streamsides) may
have a delayed warming in spring and dampened diurnal temperature variations (Shanks
1954; Fridley 2009), which indicates that they are less coupled to the regional temperature
than drier sites (Fridley 2009). Also, small scale water bodies, e.g. springs, ravines, lakes or
mires act as thermoregulators (Caissie 2006; Hampe & Jump 2011). On bogs, the Sphagnum
and peat layer insulates the ground habitats. Along with the dampening effect of the water
table this leads to a cooler microclimate than in the surroundings (Spitzer & Danks 2006).
The role of refugia at range shifts
The picture of a species range in figure 2 shows the continuous range (main population) of a
species distributed along an environmental gradient. When the environmental gradient
changes, the species will shift its range towards more favorable environmental conditions, in
this case towards the top of the paper which can represent either south or north. During this
shift, the leading edge refers to the expanding edge, while the eroding edge refers to the rear
edge. Both a leading and a rear edge is characterized by small, more or less isolated
populations. At the leading edge these are the result of expansion (Hampe & Jump 2005), or
Figure 2. Example of a distribution range of a
species across an environmental gradient. When
this gradient change, the range of the species will
shift its main population (continuous range) range
towards more favorable environmental conditions
(towards the top of the paper, either to the south
or to the north). Both the leading and the rear
edge are characterized by small isolated
populations. At the leading edge these are the
result of expansion, or previous refugial
populations that expand, and at the rear edge
these are refugial populations. The rear edge can
be stable or trailing (modified from Hampe &
Petit 2005).
24
they may be microrefugia from an earlier contracting phase that now expand. At a rear edge,
these populations are located in microrefugia. The rear edge can be stable with small or
altitudinal range shifts owing to a heterogenous landscape. Such landscapes might locally
buffer the climatic change due to decoupling of the local climate from the regional climate
(Dobrowski 2010). The rear edge can also be trailing with larger latitudinal range shifts
(Hampe & Jump 2005).
The picture of a shifting species range in figure 2 is simplified in several ways. A continuous
range is also limited to the west and to the east by one or several factors. This means that
there may be refugia also in these directions. Furthermore, a range shift could take place
towards other directions than north and south if there are changes in environmental gradients
in these directions. In addition to shifts of both the rear and the leading edge towards one
direction, there might be situations when there is only one edge of the shifting continuous
range. In such cases, it is more suitable to use the terms expanding or eroding edge for the
shifting range margin (see Fig. 3 for ranges with eroding edges only). Finally, if the
environmental gradient inverse, the leading edge will become the rear edge and the other way
around.
Let’s focus on the temperature as the main environmental gradient. Consider a species
adapted to specific temperature conditions and consider it has both a leading and a rear edge.
This species could be adapted to cold, warm or intermediate temperature conditions. When
the temperature changes it may shift its range towards the more favorable temperature
conditions, preferably towards one of the poles if it gets warmer or towards the equator if it
gets colder. Notably, the leading range may also shift towards higher altitudes during climate
warming or towards lower altitudes during climate cooling. Continuously, new isolated
populations will form ahead of the leading range through colonization, to a largely extent
controlled by long-distance dispersal (Hampe & Jump 2005). Whether these isolated
populations are newly formed or earlier formed microrefugia, isolated populations at the
leading range will expand into the surrounding areas, depending on where the conditions gets
favorable, until they merge with the shifting continuous range. At this moment, populations
will cease to be refugial. At the eroding rear edge, microrefugia with locally favorable
temperature conditions may arise, both at a stable and at a trailing rear edge.
25
Figure 3. Contracting species ranges with eroding edges but no expanding edges. a) This pattern
might arise during a warming scenario for a cold-adapted species distributed around one of the
poles, around a mountain-top or on a plateau. b) A similar pattern might also arise if the species
is distributed along the equator.
This range shift might lead to the contraction of the continuous range. If so, the range forms
one or several macrorefugium in addition to the microrefugia at the range edges. It is not
obvious whether a shift towards more favorable temperature conditions leads to an expansion
or a contraction of the continuous range (main range), or if its size is more or less stable. First,
this depends on the characteristics of the leading edge, which includes the dispersal capacity
of the species and to which degree the range expansion is hindered for different reasons. One
kind of expansion limiter can be physical barriers such as mountain ranges, ice sheets and
large water bodies. For example, the Mediterranean and the Sahara may hinder southward
range shifts by temperate species during climate cooling. Another option is that the range
expansion is limited due to abiotic or biotic factors (Gaston 2003; Mott 2010). Secondly, this
also depends on the properties of the rear edge, i.e. if it is stable or trailing.
At the extremes, if there is only an eroding edge or only an expanding edge, the range will
contract or expand respectively. These circumstances might prevail if the species is
distributed on a plateau, around a mountain-top, around one of the poles, or along the equator.
Two examples that comprise ranges with only eroding edges belong maybe to the most
26
obvious range shift scenarios. These are the range contraction and the subsequent arise of
refugia for cold-adapted species when the climate gets warmer and for warm-adapted species
when the climate gets colder (Fig. 3). The main reason for the former case might be that cold
habitats around the poles or at high altitudes are likely to decrease during climate warming
(Fig. 3a). Similarly, the latter case is explained by that warm habitats close to the equator are
likely to decrease during climate cooling (Fig. 3b). One example is the rainforest cover in
Africa that was reduced during the last glacial maximum due to cooler and drier climate (Leal
2004). Also bear in mind the higher species richness in the tropics compared to temperate
regions (Wallace 1878). If species migrates towards the equator during climate cooling, there
might be more biotic interactions with influence on the species ranges.
Furthermore, the rear edge characteristics of a cold-adapted species when a glacial is
approaching will largely depend on the ice cap that builds up. If it is an arctic species, an
advancing ice cap may force the continuous range of the species to shift towards the equator.
For this reason, no or few rear edge microrefugia might exist at the rear edge. It is possible
though, that there might instead be refugia beyond the ice sheet limit, at nunataks, along the
coasts or on islands in the sea (Stewart et al. 2001; Pruett & Winkler 2005; Anderson et al.
2006; Holderegger & Thiel-Egenter 2009). Other, less cold-adapted species will not be as
close to the advancing ice sheet, so the chance is bigger that microrefugia arise at their rear
edges.
Figure 4. Example of climatic oscillations during the glacial-interglacial oscillations. a) The mean
temperature decrease from the interglacial toward the glacial period. b) The mean temperature
increase from the glacial toward the interglacial period. c) The mean temperature decrease during
an interglacial period. d) The mean temperature increase during an interglacial. All these
temperature oscillations may result in range shifts and the arise of refugia.
27
A temperature change scenario, leading to range shifts, can take place at the scale of the
Milankovitch cycles, resulting in an interglacial or a glacial (Fig. 4a-b; Bennett 1990). It can
also take place as regional climatic fluctuations at a smaller temporal and spatial scale during
an interglacial or glacial (Fig. 4c-d; IPCC 2001). The persistance of climatic refugia depends
on the scale during which they were formed. If they were formed during climate cooling, they
can last until the next warming period. At stable edges they might even persist over several
glacials and interglacials (Hampe & Petit 2005). At trailing edges they are likely to be more
short-lived due to the latitudinal movements of the ranges. The persistance of climatic refugia
requires that the local climate is decoupled from the regional climate; otherwise the refugial
population will be at large risk for extinction.
One conclusion drawn from the range shift process described above is as follows. Even if
there are more or less obvious range shift scenarios, the described process infers that a species
may form refugia both at warming and cooling scenarios. This is especially true for species
adapted to intermediate temperature conditions, but it may as well be true for species adapted
to cold or warm temperature conditions. The temperatures resulting from climate change may
be too extreme even for the most cold- or warm-adapted species, possibly leading to range
shifts.
In summary, the formation of refugia from climate change depends on many factors such as
terrain and land mass characters as well as on abiotic and biotic factors. It also depends on the
species dispersal capacity, the degree of temperature change and the temperature niche of the
species.
28
References
Anderson, L. L., Hu, F. S., Nelson, D. M., Petit, R. J. & Paige, K. N. (2006) Ice-age
endurance: DNA evidence of a white spruce refugium in Alaska. – Proceedings of the
National Academy of Sciences of the United States of America 103: 12447-12450.
Ashcroft, M. B. (2010) Identifying refugia from climate change. – Journal of Biogeography
37: 1407-1413.
Ashcroft, M. B., Chisholm, L. A. & French, K. O. (2009) Climate change at the landscape
scale: predicting fine-grained spatial heterogeneity in warming and potential refugia
for vegetation. – Global Change Biology 15: 656-667.
Austin, M. P., Cunningham, R. B. & Fleming, P. M. (1984) New Approaches to direct
gradient analysis using environmental scalars and statistical curve-fitting procedures.
– Vegetatio 55: 11-27.
Barry, R. G. (2008) Mountain weather and climate. Cambridge University Press, Cambridge.
Beatty, G. E. & Provan, J. (2010) Refugial persistence and postglacial recolonization of North
America by the cold-tolerant herbaceous plant Orthilia secunda. – Molecular Ecology
19: 5009-5021.
Bennett, K. D. (1990) Milankovitch cycles and their effects on species in ecological and
evolutionary time. – Paleobiology 16: 11-21.
Bennett, K.D. Tzedakis, P. C. & Willis, K. J. (1991) Quaternary refugia of north European
trees. – Journal of Biogeography 18: 103–115
Bennett, K. D. & Provan, J. (2008) What do we mean by 'refugia? – Quaternary Science
Reviews 27: 2449-2455.
Bennett, K. D., Tzedakis, P. C. & Willis, K. J. (1991) Quaternary refugia of north european
trees. – Journal of Biogeography, 18, 103-115.
Bergen, J. D. (1968) Cold air drainage on a forested mountain slope. – Journal of Applied
Meteorology 8: 884-894.
Berger, A. (1977) Support for the astronomical theory of climatic change. – Nature 269: 4445.
Billings, W. D. (1974) Adaptations and origins of alpine plants. – Arctic and Alpine Research
6: 129-142.
Birks, H. J. B. & Willis, K. J. (2008) Alpines, trees, and refugia in Europe. – Plant Ecology &
Diversity 1: 147-160.
29
Blennow, K. & Lindkvist, L. (2000) Models of low temperature and high irradiance and their
application to explaining the risk of seedling mortality. – Forest Ecology and
Management 135: 289-301.
Blytt, A. G. (1876) Essay on the immigration of the Norwegian flora during alternating rainy
and dry periods. A. Cammermeyer, Christiania.
Boyko, H. (1947) On the role of plants as quantitative climate indicators and the geoecological law of distribution. – Journal of Ecology 35: 138-157.
Bradley, R. S. (1999) – Paleoclimatology. Reconstructing climates of the Quaternary.
Academic Press, London.
Brochmann, C., Gabrielsen, T. M., Nordal, I., Jon, Y. L. & Elven, R. (2003) Glacial survival
or tabula rasa? The history of North atlantic biota revisited. – Taxon 52: 417-450.
Bruno, J. F., Stachowicz, J. J. & Bertness, M. D. (2003) Inclusion of facilitation into
ecological theory, – Trends in Ecology & Evolution 18 (3): 119-125.
Bullock, J. M., Edwards, R. J., Carey, P. D. & Rose, R. J. (2000) Geographical Separation of
two Ulex species at three spatial scales: Does competition limit species' ranges? –
Ecography 23: 257-271.
Byrne, M. (2008) Evidence for multiple refugia at different time scales during Pleistocene
climatic oscillations in southern Australia inferred from phylogeography. –
Quaternary Science Reviews 27: 2576-2585.
Caissie, D. (2006) The thermal regime of rivers: a review. – Freshwater Biology 51: 13891406.
Camp, A., Oliver, C., Hessburg, P. & Everett, R. (1997) Predicting late-successional fire
refugia pre-dating European settlement in the Wenatchee mountains. – Forest Ecology
and Management 95: 63-77.
Carter, R. N. & Prince, S. D. (1981) Epidemic models used to explain biogeographical
distribution-limits. – Nature 293: 644-645.
Cheddadi, R., Vendramin, G. G., Litt, T., Francois, 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: 271-282.
Clarke, P. J. (2002) Habitat islands in fire-prone vegetation: do landscape features influence
community composition? – Journal of Biogeography 29: 677-684.
30
Colette, A., Chow, F. K. & Street, R. L. (2003) A numerical study of inversion-layer breakup
and the effects of topographic shading in idealized valleys. – Journal of Applied
Meteorology 42: 1255-1272.
Connor, E. F. & Bowers, M. A. (1987) The spatial consequences of interspecific competition.
– Annales Zoologici Fennici 24: 213-226.
Coughlan, J. C. & Running, S. W. (1997) Regional ecosystem simulation: A general model
for simulating snow accumulation and melt in mountainous terrain. – Landscape
Ecology 12: 119-136.
Crawford, R. M. M. (2008) Plants at the margin. Ecological limits and climate change.
Cambridge University Press, Cambridge.
Crimmins, S. M., Dobrowski, S. Z., Greenberg, J. A., Abatzoglou, J. T. & Mynsberge, A. R.
(2011) Changes in climatic water balance drive downhill shifts in plant species’
optimum elevations. – Science 331: 324-327.
Cruzan, M. B. & Templeton, A. R. (2000) Paleoecology and coalescence: phylogeographic
analysis of hypotheses from the fossil record. – Trends in Ecology & Evolution 15:
491-496.
Dahl, E. (1946) On different types of unglaciated areas during the ice ages and their
significance to phytogeography. – New Phytologist 45: 225-242.
Dai, A., Trenberth, K. E. & Karl, T. R. (1999) Effects of clouds, soil moisture, precipitation,
and water vapor on diurnal temperature range. – Journal of Climate 12: 2451-2473.
Dalén, L., Nyström, V., Valdiosera, C., Germonpré, M., Sablin, M., Turner, E., Angerbjörn,
A., Arsuaga, J.L., Götherström, A., (2007) Ancient DNA reveals lack of postglacial
habitat tracking in the arctic fox. – Proceedings of the National Academy of Sciences
of the USA 104: 6726–6729.
Daly, C., Conklin, D. R. & Unsworth, M. H. (2010) Local atmospheric decoupling in
complex topography alters climate change impacts. – International Journal of
Climatology 30: 1857-1864.
Darwin, C. (1859) On the origin of species by means of natural selection, or preservation of
favored races in the struggle for life. John Murray, London.
Davis, A. J., Jenkinson, L. S., Lawton, J. H., Shorrocks, B. & Wood, S. (1998) Making
mistakes when predicting shifts in species range in response to global warming. –
Nature 391: 783-786.
Davis, M. B. & Shaw, R. G. (2001) Range shifts and adaptive responses to Quaternary
climate change. – Science 292: 673-679.
31
DeLong, S. C. & Kessler, W. B. (2000) Ecological characteristics of mature forest remnants
left by wildfire. – Forest Ecology and Management 131: 93-106.
Dimichele, W. A., Phillips, T. L. & Olmstead, R. G. (1987) Opportunistic evolution - abiotic
environmental-stress and the fossil record of plants. – Review of Palaeobotany and
Palynology 50: 151-178.
Dobrowski, S. Z. (2011) A climatic basis for microrefugia: the influence of terrain on climate.
– Global Change Biology 17: 1022-1035.
Dobrowski, S. Z., Abatzoglou, J. T., Greenberg, J. A. & Schladow, S. G. (2009) How much
influence does landscape-scale physiography have on air temperature in a mountain
environment? – Agricultural and Forest Meteorology 149: 1751-1758.
DoleOlivier, M. J., Marmonier, P. & Beffy, J. L. (1997) Response of invertebrates to lotic
disturbance: Is the hyporheic zone a patchy refugium? – Freshwater Biology 37: 257276.
Eldredge, N. (1997) “Cretaceous meteor showers, the human ecological 'niche', and the sixth
extinction.” Humans and Other Catastrophes [Conference]. American Museum of
Natural History New York.
Fischer, A. G. (1981) Climatic oscillations in the biosphere. In Nitecki, M. (eds.) Biotic
Crises in Ecological and Evolutionary Time. New York, Academic Press, pp 103-131
Fischer, A. G. (1982) Long-term climatic oscillations recorded in stratigraphy. In Berger, W.
H. & Crowell, J. C. (eds.) Climate in Earth History. Washington, D.C., National
Academy Press, pp 97-104
Fischer, A. G. (1986) Climatic rhythms recorded in strata. – Annual Review of Earth and
Planetary Sciences 14: 351-376.
Ford, E. B. (1945) Butterflies. Collins, London.
Frakes, L. A., Francis, J. E. & Syktus, J. I. (1992) Climate modes of the Phanerozoic: the
history of Earth's climate over the past 600 million years. Cambridge University
Press, Cambridge.
Fridley, J. D. (2009) Downscaling climate over complex terrain: high finescale (< 1000 m)
spatial variation of near-ground temperatures in a montane forested landscape (Great
smoky mountains). – Journal of Applied Meteorology and Climatology 48: 10331049.
Gaston, K. J. (2003) The structure and dynamics of geographic ranges. Oxford University
Press, Oxford.
32
Geiger, R. (1950) The climate near the ground. Harvard University Press, Cambridge,
Massachusetts.
Geiger, R., Aron, R. H. & Todhunter, P. (2003) The climate near the ground. Rowman &
Littlefield Publishers, Lanham, Maryland.
Godwin, H. (1975) History of the British flora. Cambridge University Press, Cambridge.
Gong, L. B., Xu, C. Y., Chen, D. L., Halldin, S. & Chen, Y. Q. D. (2006) Sensitivity of the
Penman-Monteith reference evapotranspiration to key climatic variables in the
Changjiang (Yangtze river) basin. – Journal of Hydrology, 329, 620-629.
Gould, S. J. (1985) The paradox of the first tier: an agenda for paleobiology. – Paleobiology
11: 2-12.
Hampe, A. & Jump, A. S. (2011) Climate relicts: past, present, future. – Annual Review of
Ecology, Evolution, and Systematics 42: 313-333.
Hampe, A. & Petit, R. J. (2005) Conserving biodiversity under climate change: the rear edge
matters. – Ecology Letters 8: 461-467.
Hays, J. D., J. Imbrie & N. J. Shackleton (1976) Variations in the earth's orbit: pacemaker of
the ice ages. – Science 194: 1121-1132.
Hengeveld, R. (1990) Dynamic biogeography. Cambridge University Press, Cambridge.
Heusser, C. J. (1955) Pollen profiles from the Queen charlotte islands, British columbia. –
Canadian Journal of Botany 33: 429-449.
Hewitt, G. (2000) The genetic legacy of the Quaternary ice ages. – Nature 405: 907-913.
Hewitt, G. M. (1996) Some genetic consequences of ice ages, and their role in divergence and
speciation. – Biological Journal of the Linnean Society 58: 247-276.
Hewitt, G. M. (1999) Post-glacial re-colonization of European biota. – Biological Journal of
the Linnean Society 68: 87-112.
Hewitt, G. M. (2004) Genetic consequences of climatic oscillations in the Quaternary. –
Philosophical Transactions of the Royal Society of London B: Biological Sciences
359: 183-195.
Hochberg, M. E. & Ives, A. R. (1999) Can natural enemies enforce geographical range
Limits? – Ecography 22: 268-276.
Hodkinson, I. D. (1999) Species response to global environmental change or why
ecophysiological models are important: a reply to Davis et al. – Journal of Animal
Ecology 68: 1259-1262.
Hoffmann, A. A. & Blows, M. W. (1994) Species borders - ecological and evolutionary
perspectives. – Trends in Ecology & Evolution 9: 223-227.
33
Holderegger, R. & Thiel-Egenter, C. (2009) A discussion of different types of glacial refugia
used in mountain biogeography and phylogeography. – Journal of Biogeography 36:
476-480.
Holt, R. D. & Barfield, M. (2009). Trophic interactions and range limits: the diverse roles of
predation. – Proceedings of the Royal Society B: Biological Sciences 276: 1435–1442.
Holt, R. D. & Keitt, T. H. (2000) Alternative causes for range limits: a metapopulation
perspective. – Ecology Letters 3: 41-47.
Huntley, B. & Birks, H. J. B. (1983) An atlas of past and present pollen maps for Europe: 013000 years ago. Cambridge University Press, Cambridge.
Hupet, F. & Vanclooster, M. (2001) Effect of the sampling frequency of meteorological
variables on the estimation of the reference evapotranspiration. – Journal of
Hydrology 243: 192-204.
Hutchins, L. W. (1947) The bases for temperature zonation in geographical distribution. –
Ecological Monographs 17: 325-335.
Hutchins, R. B., Blevins, R. L., Hill, J. D. & White, E. H. (1976) Influence of soils and
microclimate on vegetation of forested slopes in eastern kentucky. – Soil Science 121:
234-241.
Hutchinson, T. F., Boerner, R. E. J., Iverson, L. R., Sutherland, S. & Sutherland, E. K. (1999)
Landscape patterns of understory composition and richness across a moisture and
nitrogen mineralization gradient in Ohio (USA) Quercus forests. – Plant Ecology 144:
177-189.
Hylander, K. & Johnson, S. (2010) In situ survival of forest bryophytes in small scale refugia
after an intense forest fire. – Journal of Vegetation Science 21: 1099-1109.
Imbrie, J., A. C. Mix & D. G. Martinson (1993) Milankovitch theory viewed from Devils
hole. – Nature 363: 531-533.
Inouye, D. W. (2000) The ecological and evolutionary significance of frost in the context of
climate change. – Ecology Letters 3: 457-463.
IPCC (2001) Climate change 2001: The scientific basis. Contribution of working group I to
the third assesment report of the Intergovermental panel on climate change.
Cambridge University Press, Cambridge.
Iversen, J. (1944) Viscum, Hedera and Ilex as climate indicators. A Contribution to the study
of the post-glacial temperature climate. – Geologiska föreningens förhandlingar 66(3):
463-483.
34
Jackson, S. T., Webb, R. S., Anderson, K. H., Overpeck, J. T., Webb, T., Williams, J. W. &
Hansen, B. C. S. (2000) Vegetation and environment in eastern North America during
the last glacial maximum. – Quaternary Science Reviews 19: 489-508.
Kawecki, T. J. (2008) Adaptation to marginal habitats. – Annual Review of Ecology Evolution
and Systematics 39: 321-342.
Kirkpatrick M. & Barton, N. H. (1997) Evolution of a species' range. – American Naturalist
150: 1-23.
Kishony, R. & S. Leibler (2003) Environmental stresses can alleviate the average deleterious
effect of mutations. – Journal of Biology 2: 14.
Lacourse, T., Mathewes, R. W. & Fedje, D. W. (2005) Late-glacial vegetation dynamics of
the Queen Charlotte islands and adjacent continental shelf, British Columbia, Canada.
– Palaeogeography Palaeoclimatology Palaeoecology 226: 36-57.
Lancaster, J. & Belyea, L. R. (1997) Nested hierarchies and scale-dependence of mechanisms
of flow refugium use. – Journal of the North American Benthological Society 16: 221238.
Leal, M. E. (2004) The African rain forest during the Last Glacial Maximum, an archipelago
of forests in a sea of grass. PhD thesis Wageningen University, Wageningen.
Ledru, M. P., Salatino, M. L. F., Ceccantini, G., Salatino, A., Pinheiro, F. & Pintaud, J. C.
(2007) Regional assessment of the impact of climatic change on the distribution of a
tropical conifer in the lowlands of South America. – Diversity and Distributions 13:
761-771.
Letcher, A. J. & Harvey, P. H. (1994) Variation in geographical range size among mammals
of the palearctic. – American Naturalist 144: 30-42.
Levins, R. (1969) Some Demographic and genetic consequences of environmental
heterogeneity for biological control. – Bulletin of the ESA 15: 237-240.
Lindkvist, L., Gustavsson, T. & Bogren, J. (2000) A frost assessment method for mountainous
areas. – Agricultural and Forest Meteorology 102: 51-67.
Lindroth, C. H. (1931) Die insektenfauna und ihrer probleme. – Bidrag från Uppsala 13: 105599.
Lookingbill, T. R. & Urban, D. L. (2003) Spatial estimation of air temperature differences for
landscape-scale studies in montane environments. – Agricultural and Forest
Meteorology 114: 141-151.
35
Löffler, J., Pape, R. & Wundram, D. 2006. The climatological significance of topography,
altitude and region in high mountains – a survey of oceanic–contintental
differentiations of the Scandes. – Erdkunde 60: 15-24.
MacArthur, R. H. (1972) Geographical ecology: patterns in the distribution of species.
Princeton University Press, Princeton, New Jersey.
Macvean, C. & Schuster, J. C. (1981) Altitudinal distribution of passalid beetles (Coleoptera,
Passalidae) and pleistocene dispersal on the volcanic chain of northern Central
America. – Biotropica 13: 29-38.
Manins, P. C. & Sawford, B. L. (1979) Katabatic winds: a field case study. – Quarterly
Journal of the Royal Meteorological Society 105: 1011-1025.
Marko, P. B. (2004) 'What's larvae got to do with it?' Disparate patterns of post-glacial
population structure in two benthic marine gastropods with identical dispersal
potential. – Molecular Ecology 13: 597-611.
Matthaei, C. D., Arbuckle, C. J. & Townsend, C. R. (2000) Stable surface stones as refugia
for invertebrates during disturbance in a New Zealand stream. – Journal of the North
American Benthological Society 19: 82-93.
McClain, C. R. & Hardy, S. M. (2010) The dynamics of biogeographic ranges in the deep sea.
– Proceedings of the Royal Society B: Biological Sciences 277: 3533-3546.
McLachlan, J. S., Clark, J. S. & Manos, P. S. (2005) Molecular indicators of tree migration
capacity under rapid climate change. – Ecology 86: 2088-2098.
McVicar, T. R., Van Niel, T. G., Li, L. T., Hutchinson, M. F., Mu, X. M. & Liu, Z. H. (2007)
Spatially distributing monthly reference evapotranspiration and pan evaporation
considering topographic influences. – Journal of Hydrology 338: 196-220.
Milankovitch, M. (1930) Mathematische klimalehre und astronomische theorie der
klimaschwankungen. In Köppen, V. & Geiger, R. (eds.) Handbuch der Klimatologie I
(A). Gebrüder Borntraeger Berlin, pp 1-176.
Mott, C. L. (2010) Environmental constraints to the geographic expansion of plant and animal
species. – Nature Education Knowledge 3(10): 72.
Muller, H. & Whiteman, C. D. (1988) Breakup of a nocturnal temperature inversion in the
Dischma valley during DISKUS. – Journal of Applied Meteorology 27: 188-194.
Parmesan, C. & Yohe, G. (2003) A globally coherent fingerprint of climate change impacts
across natural systems. – Nature 421: 37-42.
Parmesan, C. (2006) Ecological and evolutionary responses to recent climate change. –
Annual Review of Ecology Evolution and Systematics 37: 637-669.
36
Parmesan, C., Gaines, S., Gonzalez, L., Kaufman, D. M., Kingsolver, J., Townsend Peterson,
A. & Sagarin, R. (2005) Empirical perspectives on species borders: from traditional
biogeography to global change. – Oikos 108: 58-75.
Pearson, R. G. (2006) Climate change and the migration capacity of species. – Trends in
Ecology & Evolution 21: 111-113.
Pepin, N. C. & Seidel, D. J. (2005) A global comparison of surface and free-air temperatures
at high elevations. – Journal of Geophysical Research-Atmospheres 110.
Pereira, H. M., Leadley, P. W., Proenca, V., Alkemade, R., Scharlemann, J. P. W., FernandezManjarres, J. F., Araujo, M. B., Balvanera, P., Biggs, R., Cheung, W. W. L., Chini, L.,
Cooper, H. D., Gilman, E. L., Guenette, S., Hurtt, G. C., Huntington, H. P., Mace, G.
M., Oberdorff, T., Revenga, C., Rodrigues, P., Scholes, R. J., Sumaila, U. R. &
Walpole, M. (2010) Scenarios for global biodiversity in the 21st century. – Science
330: 1496-1501.
Petit, R. J., Hu, F. S. & Dick, C. W. (2008) Forests of the past: A window to future changes. –
Science 320: 1450-1452.
Pfennig, D. W., Wund, M. A., Snell-Rood, E. C., Cruickshank, T., Schlichting, C. D. &
Moczek, A. P. (2010) Phenotypic plasticity's impacts on diversification and speciation.
– Trends in Ecology & Evolution 25: 459-467.
Provan, J. & Bennett, K. D. (2008) Phylogeographic insights into cryptic glacial refugia. –
Trends in Ecology & Evolution 23: 564-571.
Pruett, C. L. & Winker, K. (2005) Biological impacts of climatic change on a Beringian
endemic: cryptic refugia in the establishment and differentiation of the rock sandpiper
(Calidris ptilocnemis). – Climatic Change 68: 219-240.
Pulliam, H. R. (1988) Sources, sinks, and population regulation. – American Naturalist 132:
652-661.
Raup, D. M. & Sepkoski, J. J. (1982) Mass extinctions in the marine fossil record. Science
215: 1501-1503.
Rull, V. (2009) Microrefugia. – Journal of Biogeography 36: 481-484.
Rull, V. (2010) On microrefugia and cryptic refugia. – Journal of Biogeography 37: 16231625.
Rundgren, M. & Ingólfsson, Ó. (1999) Plant survival in Iceland during periods of glaciation?
– Journal of Biogeography 26: 387-396.
Salisbury, E. J. (1926) The geographical distribution of plants in relation to climatic factors. –
The Geographical Journal 67: 312-335.
37
Saxon, E., Baker, B., Hargrove, W., Hoffman, F. & Zganjar, C. (2005) Mapping
environments at risk under different global climate change scenarios. – Ecology
Letters 8: 53-60.
Scherrer, D. & Körner, C. (2010) Infra-red thermometry of alpine landscapes challenges
climatic warming projections. – Global Change Biology 16: 2602-2613.
Schmalholz, M. (2007) The occurrence and ecological role of refugia at different spatial
scales in a dynamic world. – Plants & Ecology 30(2): 1-40.
Schönswetter, P., Stehlik, I., Holderegger, R. & Tribsch, A. (2005) Molecular evidence for
glacial refugia of mountain plants in the European alps. – Molecular Ecology 14:
3547-3555.
Schönswetter, P., Tribsch, A., Stehlik, I. & Niklfeld, H. (2004) Glacial history of high alpine
Ranunculus glacialis (Ranunculaceae) in the European alps in a comparative
phylogeographical context. – Biological Journal of the Linnaean Society 81: 183-195.
Sedell, J., Reeves, G., Hauer, F. R., Stanford, J. & Hawkins, C. (1990) Role of refugia in
recovery from disturbances: Modern fragmented and disconnected river systems. –
Environmental Management 14: 711-724.
Sernander, R. (1896) Några ord med anledning av Gunnar Andersson. Svenska Växtvärldens
historia. – Botaniska Notiser 114-128.
Shanks, R. E. (1954) Climates of the great Smoky mountains. – Ecology 35: 354-361.
Shepherd, L. D., Perrie, L. R. & Brownsey, P. J. (2007) Fire and ice: volcanic and glacial
impacts on the phylogeography of the New Zealand forest fern Asplenium
hookerianum. – Molecular Ecology 16: 4536-4549.
Soltis, D. E., Morris, A. B., McLachlan, J. S., Manos, P. S. & Soltis, P. S. (2006)
Comparative phylogeography of unglaciated eastern North America. – Molecular
Ecology 15: 4261-4293.
Sorte, C. J. B., Williams, S. L. & Carlton, J. T. (2010) Marine range shifts and species
introductions: comparative spread rates and community impacts. – Global Ecology
and Biogeography 19: 303-316.
Soule, M. (1973) The Epistasis cycle: a theory of marginal populations. – Annual Review of
Ecology and Systematics 4: 165-187.
Spitzer, K. & Danks, H. V. (2006) Insect biodiversity of boreal peat bogs. – Annual Review of
Entomology 51: 137-161.
Stewart, J. R. & Lister, A. M. (2001) Cryptic northern refugia and the origins of the modern
biota. – Trends in Ecology & Evolution 16: 608-613.
38
Stewart, J. R., Lister, A. M., Barnes, I. & Dalen, L. (2010) Refugia revisited: individualistic
responses of species in space and time. – Proceedings of the Royal Society B:
Biological Sciences, 277, 661-671.
Suggitt, A. J., Gillingham, P. K., Hill, J. K., Huntley, B., Kunin, W. E., Roy, D. B. & Thomas,
C. D. (2011) Habitat microclimates drive fine-scale variation in extreme temperatures.
– Oikos 120: 1-8.
Taberlet, P., Fumagalli, L., Wust-Saucy, A. G. & Cosson, J. F. (1998) Comparative
phylogeography and postglacial colonization routes in Europe. – Molecular Ecology
7: 453-464.
Taylor, R., Kelbe, B., Haldorsen, S., Botha, G. A., Wejden, B., Vaeret, L. & Simonsen, M.B.
(2006) Groundwater-dependent ecology of the shoreline of the subtropical lake St
Lucia estuary. – Environmental Geology 49: 586-600.
Thomas, J. A., Rose, R. J., Clarke, R. T., Thomas, C. D. & Webb, N. R. (1999) Intraspecific
variation in habitat availability among ectothermic animals near their climatic limits
and their centres of range. – Functional Ecology 13: 55-64.
Thornthwaite, C. W. (1953) A charter for climatology. – World Meteorological Organization
Bulletin 2.
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: 137-152.
Tribsch, A. & Schönswetter, P. (2003) Patterns of endemism and comparative
phylogeography confirm palaeoenvironmental evidence for Pleistocene refugia in the
Eastern Alps. – Taxon 52: 477-497.
Trivedi, M. R., Berry, P. M., Morecroft, M. D. & Dawson, T. P. (2008) Spatial scale affects
bioclimate model projections of climate change impacts on mountain plants. – Global
Change Biology 14: 1089-1103.
Twomey, A. C. (1936) Climographic studies of certain introduced and migratory birds. –
Ecology 17: 122-132.
Vanwalleghem, T. & Meentemeyer, R. K. (2009) Predicting forest microclimate in
heterogeneous landscapes. – Ecosystems 12: 1158-1172.
Vinogradova, N. G. (1997) Zoogeography of the abyssal and hadal zones. – Advances in
Marine Biology 32: 325-387.
Wallace, A. R. (1878) Tropical nature and other essays. Macmillan and co, London.
39
Warming, E. (1888) Om Grønlands vegetation. – Meddelelser om Grønland 12: 1-245.
Webb, S. L., Glenn, M. G., Cook, E. R., Wagner, W. S. & Thetford, R. D. (1993) Range edge
Red spruce in New Jersey, U.S.A.: bog versus upland population structure and climate
responses. – Journal of Biogeography 20 (1): 63-78.
Whiteman, C. D. (1980) Breakup of Temperature Inversions in Colorado Mountain Valleys.
Department of Atmospheric Science, Colorado state University, Fort Collins,
Colorado.
Whiteman, C. D., Pospichal, B., Eisenbach, S., Weihs, P., Clements, C. B., Steinacker, R.,
Mursch-Radlgruber, E. & Dorninger, M. (2004) Inversion breakup in small Rocky
mountain and alpine basins. – Journal of Applied Meteorology 43: 1069-1082.
Whiteman, D. (1982) Breakup of temperature inversions in deep mountain valleys: part 1.
Observations. – Journal of Applied Meteorology 21: 270-289.
Williams, D. D. & Hynes, H. B. N. (1974) The occurrence of benthos deep in the substratum
of a stream. – Freshwater Biology 4: 233-256.
Williamson, M. H. (1957) An elementary theory of interspecific competition. Nature 180:
422-425.
Willis K. J., Rudner E., Sümegi P. (2000) The full-glacial forests of central and southeastern
Europe. – Quaternary Research 53:203–213.
Willis K.J., van Andel T. H. (2004) Trees or no trees? The environments of central and
eastern Europe during the last glaciation. – Quaternary Science Reviews 23:2369–
2387.
Willis, K. J. & McElwain, J. C. (2002) The evolution of plants. Oxford University Press,
Oxford.
Won, Y., Young, C. R., Lutz, R. A. & Vrijenhoek, R. C. (2003) Dispersal barriers and
isolation among deep-sea mussel populations (Mytilidae: Bathymodiolus) from eastern
Pacific hydrothermal vents. – Molecular Ecology, 12, 169-184.
Woodward, F. I. (1997) Life at the edge: a 14-year study of a Verbena officinalis population's
interactions with climate. – Journal of Ecology 85: 899-906.
Wright, S. (1943) Isolation by distance. – Genetics 28 (2): 114-138.
Xu, M., Chen, J. Q. & Brookshire, B. L. (1997) Temperature and its variability in oak forests
in the southeastern Missouri ozarks. – Climate Research 8: 209-223.
Zackrisson, O. (1977) Influence of forest fires on north Swedish boreal forest. – Oikos 29: 2232.
40
Zinko, U., Dynesius, M., Nilsson, C. & Seibert, J. (2006) The role of soil pH in linking
groundwater flow and plant species density in boreal forest landscapes. – Ecography
29: 515-524.
41