Plant Dispersal and Migration
James S Clark, B Beckage, J HilleRisLambers, I Ibanez, S LaDeau, J McLachlan, J Mohan, and
M Rocca
Volume 2, The Earth system: biological and ecological dimensions of global environmental
change, pp 81–93
Edited by
Professor Harold A Mooney and Dr Josep G Canadell
in
Encyclopedia of Global Environmental Change
(ISBN 0-471-97796-9)
Editor-in-Chief
Ted Munn
 John Wiley & Sons, Ltd, Chichester, 2002
Plant Dispersal and Migration
JAMES S CLARK, B BECKAGE, J HILLERISLAMBERS, I IBANEZ, S LADEAU,
J MCLACHLAN, J MOHAN, AND M ROCCA
Duke University, Durham, NC, USA
Although Americans may have first seen kudzu (Pueraria lobata) on US soil at the Philadelphia Centennial
Exposition of 1876, broad distribution throughout the Southeast did not come until decades later. Kudzu is
known for its rapid growth, a potential to bury forest canopies in dense foliage in the course of a single growing
season. It is natural to attribute its success as an alien invader to an aggressive habit that co-opts the light supply
of native vegetation. But kudzu’s inherent invasive potential may be overrated. The modern distribution is the
result of a determined campaign to broadly disseminate the species (reproduction is almost entirely vegetative).
Even retail (including mail order) sales of the curious ornamental during the early decades of this century might
not have been enough to establish it as the dominant alien it has become. That dominance dates from the 1930s,
when the Soil Conservation Service paid farmers $8.00 an acre to stabilize their fallow fields, and the Civilian
Conservation Corps distributed kudzu widely to control erosion (Miller and Edwards, 1982). In the absence
of detailed records of planting during the Depression and additional establishment since, history provides few
insights regarding its potential for spread in the absence of intentional propagation by humans.
Worldwide invasions of exotic plants, together with environmental changes that threaten native species,
challenge ecologists to understand population spread in the context of dispersal potential. Many countries
now support resident populations of hundreds to thousands of invasive exotic plant species. Exotics represent
greater than 50% of the flora on many remote islands (Vitousek et al., 1996). Biological invasions by exotic
species change the composition and community structure of invaded areas. In addition to the obvious effects
of competitive exclusion, such as occurred with yellow star thistle’s (Centaurea solstitalis) invasion of northern
California grasslands, there are less direct effects. Some of the more devastating consequences of cheatgrass’
(Bromus tectorum) invasion of the intermountain West came from increased fire frequency, which results in
a loss of shrubs (Whisenant, 1989). Introduced cordgrasses (Spartina spp) on tidal flats around the globe
have devastated shorebird populations that depend on tidal flats for food (Daehler and Strong, 1996). There
is increasing evidence that alien invaders can alter properties of whole ecosystems, including productivity,
nutrient cycling, and hydrology (Vitousek, 1990).
INTRODUCTION
The globe’s 250 000 extant species of seed plants have
unique distributions and migration histories. Plant migration is defined here as a change in the distribution of mature
plants that spans more than a generation. Distributions can
be continuous or discontinuous. Changes in distributions
include both expansions and contractions, but we focus here
on expansions. Geographic distributions represent a balance
between seed dispersal and vegetative spread, both of which
tend to extend the range, and environmental constraints
on survival that keep it in check. Population frontiers are
static when dispersal does not bring propagules to areas
outside the range where they currently survive. Migration
occurs when there is a change in dispersal, the environment,
or both.
Dispersal and the potential for population spread have
dual implications for populations confronted by global
change. On the one hand, migration potential, typically
aided by human transport, has brought epidemics of exotic
aliens with attendant costs in biodiversity loss, restructuring of ecosystems, and the burdens of control measures.
Potential forage species, such as alien grasses introduced
in the American West (Mack, 1986) and prickly pear
(Opuntia stricta) in Australia (Parker, 1977) have had
severe economic consequences. Aquatic ornamentals, such
as water hyacinth (Eichhornia crassipes), clog waterways
in the southeastern US. Pimentel et al. (2000) estimate that
35 billion dollars are spent annually on control of invasive plants in the US. Eradicating or delaying the spread
produces unintended consequences, and success rate is low
(Daehler and Strong, 1996). Educational activities aimed at
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THE EARTH SYSTEM: BIOLOGICAL AND ECOLOGICAL DIMENSIONS OF GLOBAL ENVIRONMENTAL CHANGE
alerting the public to potentially dangerous exotics date to
the 19th century, and include bulletins that would aid identifications of seed contaminants by farmers (Mack, 1986).
Efforts to increase public awareness might help stiffen
existing laws and policies aimed at reducing invasions
(Vitousek et al., 1996), but effective legislation requires an
understanding of how migrations occur.
On the other hand, a potential to migrate has saved
species from extinction during repeated climate changes
of the past. The legacy of prehistoric and contemporary
plant migrations includes many examples of environmental
change, both natural and human-caused, that have led
to continental-scale changes in species distributions. The
migration potential required to survive past environmental
change will be needed again as global change accelerates.
Recognition of species threatened by rapid climate change
requires an understanding of migration potential.
The history of kudzu spread in the southeastern US captures many of the frustrations of determining how dispersal
figures in plant migration potential. Differential ability to
invade new environments begs the question of just how
important is dispersal. Of the 25 000 alien plant species
in Florida, an impressive 900 have become established in
native vegetation (Pimentel et al., 2000). The flip side of
this calculation is the >24 000 species that can grow there
but have not escaped to become components of unmanaged
vegetation. Seed dispersal does not appear to contribute
importantly to contemporary spread of kudzu. We do know
that the modern dominance of this perennial vine began
with a widespread planting campaign. Clearly, dispersal
potential is only one of many factors that might ultimately
predict the potential for and rate of spread.
Although we focus here on how dispersal affects the
potential for migration, most of the examples we consider
involve widespread changes in the environment, including
climate, land cover, or trophic structure (e.g., introductions
of other aliens or absence of natural enemies in novel
environments). We begin with a brief summary of what we
have learned from models of migration, all of which have
dispersal at their core. We then summarize the state of our
knowledge on dispersal biology, with special emphasis on
long-distance events and how well we can estimate them.
We then turn to past plant migrations, both prehistoric and
contemporary, for the light they can shed on migration
potential. Finally, we synthesize the overriding themes that
emerge from theory, dispersal biology, and the prehistoric
and historic record as a basis for some general guidelines
that may help us forecast future migrations and areas
needing further research.
THE ELEMENTS OF PLANT MIGRATION
The Dispersal Vectors that Account for Spread
Analyses of factors that might control migration potential
identify as key variables total seed production and extreme
dispersal events. These two variables go hand in hand,
because extreme events become increasingly probable with
increased seed production.
The scatter of seed about the parent plant is termed the
seed shadow. The shape of the seed shadow is determined
by the dispersal kernel, which describes the probability that
a seed released from the parent plant will travel a given
distance. The density of seed expected to settle a given
distance from the parent is found by multiplying the dispersal kernel by total seed production, or fecundity. Dispersal
kernels for seeds are termed fat-tailed, the tail referring
to the few long-distance dispersal events. Although these
long-distance events are rare, they can still dominate the
rate of spread (Figure 1). One rare long-distance event can
Initial expansion from a population frontier ...
h
(a) −XNh
...
−X2h −Xh 0
... and spread by extremes
(b)
Distance (X )
Figure 1 A plant migration includes both diffusive spread that results from local dispersal as well as rare, extreme
events that can result in fast and erratic invasion. Spread from a coherent population frontier can proceed rapidly due
to combined seed production of large numbers of adults (a), whereas total seed availability diminishes far from the
population frontier (b). (Reproduced with permission of the University of Chicago Press from Clark et al., 2001)
PLANT DISPERSAL AND MIGRATION
overshadow the contributions of the bulk of seeds that land
near the parent.
To gain a rough idea of how fecundity interacts with
the shape of the seed shadow, compare the velocities
of spread predicted by simple models of diffusion and
fat-tailed spread. Diffusion refers to a traveling wave of
advance that results in the absence of rare, long-distance
events. The velocity of this traveling wave is proportional
to the square root of the log of lifetime seed production
R0 , or net reproduction rate (Kolmogorov et al., 1937;
Skellam, 1951). Thus, the rate of spread is only weakly
affected by total seed production. By contrast, the velocity
of spread expected from dispersal kernels fitted to trees is
proportional to the square root of lifetime seed production
(Clark et al., 2001).
These two results diverge as R0 becomes large, because
the tail of the dispersal kernel translates at least some of
the increased seed production into long-distance events.
Diffusive spread occurs when such events cannot occur,
regardless of fecundity.
Despite a large dispersal biology literature, seed production and dispersal are poorly quantified for most species
in most settings. In general, dispersal data tell us that
plants tend to have fat-tailed dispersal kernels (Portnoy and
Willson, 1993; Clark et al., 1999a) and dispersal distance
depends on aerodynamic properties of seed (Figure 2).
Models tell us that when the kernel is fat-tailed, extreme
dispersal events control the rate of spread (Kot et al., 1996;
Lewis, 1997; Clark, 1998), and total seed production has
strong impact on the extremes (Clark et al., 2001a,b). Especially high fecundity is a clue that extreme events can be
particularly important. Thus, predicting migration potential
by any dispersal mechanism depends on our ability to estimate extreme events and seed production.
Dispersal by Wind
Long-distance dispersal by wind is poorly quantified, but
seed trap studies combined with observational data suggest
that it can range over many kilometers. Wind dispersal
depends on aerodynamic properties of seed, which vary
among species, and on wind fields, which vary in space
and time. Many species have seeds that are highly specialized for wind dispersal. Plumed fruits and the parachutes
of Taraxacum and other Liguliflorae (Compositae) provide
for broad dissemination in wind velocities of less than
1 m sec!1 (Weaver and Clements, 1938). The spread of tumbleweed (including Salsola kali) through the Dakotas near
the turn of the century was facilitated by saltation of dead
plants that scatter seed in transit. Larger seeds have shorter
extremes. The well-developed samaras of Acer rubrum
(Figure 2) increase drag and, thus, reduce fall velocity. The
few studies that have measured wind dispersal for multiple
years at a single site report significant interannual (Houle,
1998; Clark et al., 1999b) and stand (Clark et al., 1999b)
3
Figure 2 The samaras of Acer rubrum seed are an
example of specialized structures for wind dispersal
variability in seed production, but shape of the seed shadow
is relatively consistent (Clark et al., 1999a). Dispersal distances for temperate deciduous, mixed conifer, and lowland
tropical forest species average less than 40 m, with highest mean values for species that produce especially small
seeds (e.g., Betula) (Gladstone, 1979; Ribbens et al., 1994;
Clark et al., 1998, 1999a). Wind-dispersal is more efficient
in areas of limited vegetation cover, which reduces wind
velocity near the ground.
Long distance dispersal is erratic and hard to predict.
Extreme dispersal is not quantified, but fitted dispersal
models are fat-tailed at distances of <100 m (Clark et al.,
1999a), and there are examples of population spread due to
seed movement in open environments that exceed 103 m.
For example, colonization of Glacier Bay at rates of
300 –400 m year!1 (Fastie, 1995) is comparable with rates
inferred from fossil pollen data in the early Holocene
(Ritchie and MacDonald, 1986). Storms can transport
objects larger than seeds >100 km (Snow et al., 1995).
The importance of long distance dispersal for spread is
evident on isolated islands, which cannot be reached by
diffusive spread. For example, 30% of the seed-bearing
plants on Krakatau (¾30 km from Java and 12 km from the
4
THE EARTH SYSTEM: BIOLOGICAL AND ECOLOGICAL DIMENSIONS OF GLOBAL ENVIRONMENTAL CHANGE
nearest small island) 15 years after the 1883 eruption were
brought by wind (Ernst, 1908). Although long-distance
dispersal by wind was important, wind-dispersed taxa were
underrepresented.
Extreme dispersal by wind is poorly quantified, but there
is sufficient evidence to conclude that it is a plausible mechanism for rapid spread of relatively small-seeded species
that release seeds in the canopy. It is a less plausible mechanism for especially large seed and for seeds released in
dense understories.
Dispersal by Water
Seed transport by water (hydrochory) permits spread to
islands, along coastlines, across large water bodies, and
along river systems. Potential for long-distance dispersal by
water is more readily estimated than for wind, because the
direction of transport is more predictable, as are advection
rates (flow velocities in rivers or ocean currents) and
residence times in the water column, which depend on
seed properties. For example, the tropical Atlantic shores of
South America and Africa are linked by equatorial currents,
and they share a common mangrove flora. This flora is
distinct from the East Africa, India, and Malaya mangrove
flora (Guppy, 1917). Lack of a connection between east and
west African coasts, despite their proximity, explains their
lack of common species. The efficacy of water transport
is apparent from observational studies (e.g., Weaver and
Clements, 1938; Craddock and Huenneke, 1997), and it is
the only explanation for the presence of some species in
remote sites (Godley, 1967).
Colonization of remote islands and spread along coastlines requires adaptations for flotation and salt tolerance.
Transport is governed by ocean circulation and by local
tidal currents (Huiskes et al., 1995). Cocos nucifera (Arecaceae) with its corky husk withstands some exposure to
salt water (Schimper, 1891). Small hairs on the seeds
of Salicornia, a salt marsh chenopod, trap air and facilitate dispersal with tides (Dalby, 1963). Other adaptations
involve enlargement of the diaspore surface (e.g., Matricaria maritima, Ridley, 1930) and buoyant structures that
remain attached to seed, including carpels (Guppy, 1917),
perianth bracts (König, 1960), and fragments of the inflorescence (Dalby, 1963). Many mangrove species (involving several angiosperm families) are viviparous, whereby
seedlings develop while still attached to the parent plant.
Seedlings photosynthesize and obtain nutrients and water
while borne on ocean currents and can remain viable for
a year or more (Davis, 1940). Seedlings of red mangrove
(Rhizophora mangle) have a buoyant hypocotyl, whereas
other species have buoyant pericarps, cotyledons, or entire
embryos (Rabinowitz, 1978).
Extended viability in ocean currents can result in extreme
long-distance colonization. The isolated estuaries of the
Pacific coast represent islands of suitable habitat for introduced cordgrasses (Spartina) that are invaded by propagules
borne on tidal currents (Daehler and Strong, 1996). Some
mangrove species are capable of voyages spanning the
largest oceans (including the Indian, western Pacific, and
Atlantic, Sauer, 1988). Accumulation of species on remote
oceanic islands is probably limited, in part, by water dispersal (Ernst, 1908).
Rivers can provide corridors for rapid migration. In riparian zones, some trees time fruiting to coincide with seasonal
floods (Schneider and Sharitz, 1988; Kubitzki and Ziburski,
1994). Thebaud and Debussche (1991) suggest that water
transport during autumn floods facilitates the spread of the
typically wind-dispersed species Fraxinus ornus. Seeds dispersed by water first colonize littoral (Murray, 1986) or
riparian zones, but a spread to upland areas can follow.
North-flowing rivers of Eurasia might have accelerated
plant migrations following the last ice age (Huntley and
Birks, 1983).
Water dispersal can result in rapid spread, but it is limited
by the distribution and velocity of water currents. For
example, Eurasia contains many northward flowing rivers
that might facilitate post-Glacial spread to high latitudes,
whereas eastern North America does not.
Animals
Many of the hypotheses that concern rapid plant migration involve vertebrate vectors (Reid, 1899; Johnson and
Adkisson, 1985). Vertebrates disperse seed by ingesting
fruits and passing or regurgitating seeds intact (endozoochory), by caching (dyszoochory), and by carrying seeds
that adhere to fur or feathers (epizoochory) (Howe and
Westley, 1997). The most important vertebrate dispersal
vectors are: (i) hoarding mammals and birds; (ii) arboreal
frugivorous mammals that consume fruits with arils or pulps
containing protein, sugar, or starch; (iii) bats that feed on
pulps rich in lipids or proteins; and (iv) frugivorous birds
(Howe and Westley, 1997). Birds and mammals are the
most common vertebrate dispersal agents, but other vertebrate vectors include fish (Goulding, 1980), turtles (Moll
and Janzen, 1995), and lizards (Nogales et al., 1998). Ants
disperse large quantities of seed, but dispersal distances are
typically small, averaging perhaps one meter and ranging
to 10 m (Hughes and Westoby, 1992). Vertebrates can process a large portion (e.g., >70%) of a plant’s seed or fruit
production (Herrera et al., 1994; Vander Wall, 1994) and,
therefore, may have a large impact on dispersal. Dispersal
is further influenced by birds that prey on other vertebrates
that have consumed seed (Reid, 1899; Nogales et al., 1998).
Plant adaptations that facilitate spread by vertebrates
have probably contributed to past invasions. Darwin (1859)
reports >80 seeds of several species in dried mud taken
from a partridge leg. Elaborate adaptations to attract frugivores include thickened seed coats surrounded by brilliant,
multicolored fleshy pericarp (Howe and Westley, 1997).
Reproductive structures that adhere to animal fur may have
PLANT DISPERSAL AND MIGRATION
facilitated 20th century invasion of the intermountain West
by cheatgrass. Barbs of Xanthium and Bidens fruits allow
for similar mobility. Remote sites may be especially dependent on vertebrate vectors. Birds may have brought >75%
of the flora to the Galapagos (Porter, 1976) and smaller
fractions of total floras to islands that are less remote
(Ernst, 1908). Vertebrates as large as elephants are important dispersers for some plant species today (Chapman
et al., 1992), and loss of Pleistocene megafauna may have
subsequently limited spread of these species (Janzen and
Martin, 1982).
The benefits of animal dispersal can be overemphasized,
because losses are typically large (Schupp, 1993). Spread
is facilitated not only by transport (Janzen, 1971; Harper,
1977) but also by scarification (pregerminative influences
that make seed coats permeable to water and gases) (Fenner,
1985; Chapman et al., 1992) and provision of concentrated
resources, such as in animal dung high in nitrogen and
phosphorus (Bazzaz, 1991; Chapman et al., 1992). But
most vertebrate vectors are seed predators. As little as
1% of seed handled by vertebrate seed predators may
escape eventual consumption (Cahalane, 1942), although
it can range as high as 15 to 75% (Forget, 1990; Steele
and Smallwood, 1994), particularly in years of high seed
production. Even frugivores, which pass seed through the
intestinal tract intact, can lower viability (Murray, 1988).
Vertebrate dispersal can be more directed than wind dispersal in ways that might have particular significance for
migration. Seeds are moved to microsites or habitats that
may be especially suited to seedling survival (Hulme, 1997;
Hoshizaki et al., 1997; Vander Wall, 1994). Seed burial
within specific habitats (Yasunda et al., 2000) can promote
establishment success (Forget, 1990, 1991). In one study,
common ravens dispersed numerous seeds and placed 75%
in habitats favorable for germination (Nogales et al., 1999).
Blue jays preferentially cache seeds in regenerating woodland and edge habitats, which may have facilitated spread
in the past (Johnson et al., 1997; Kollmann and Pirl, 1995).
Herrera et al. (1994) found that birds tend to disperse seeds
to forest–gap interfaces. Transport to favorable habitats not
only increases establishment success, but can also affect
dispersal distance, depending on the distribution of land
cover.
Dispersal distances vary greatly among vertebrate vectors. Rodents move seeds 100 to 101 m (Forget, 1990;
Kollmann and Schill, 1996) with maximum recorded distances ranging from 20–70 m (Forget, 1990; Tamura and
Shibasaki, 1996; Yasunda et al., 2000). Rodent seed caches
are repeatedly moved and sometimes robbed by other
rodents, potentially increasing the distance seeds are dispersed beyond a single individual’s home range (Tamura
and Shibasaki, 1996; Vander Wall, 1994). Foxes and bears,
which consume fruits, may travel 10 km in a day (Storm and
Montgomery, 1975) suggesting potential for long-distance
5
dispersal. Old World frugivorous bats have the potential to
disperse small seeds hundreds of kilometers (Shilton et al.,
1999). Primate seed dispersal in a Columbian forest ranged
from 218 š 82 to 354 š 199 m (depending on species) with
maximum values exceeding 600 m (Yumoto et al., 1999).
Birds commonly move seeds 102 to 104 m (Kollmann and
Schill, 1996; Webb, 1986; Murray, 1988; Johnson and
Adkisson, 1985; Vander Wall and Balda, 1977).
Despite obvious potential for long distance dispersal
by large vertebrates, there are few quantitative data on
extremes. As with other vectors, the most important dispersal events, i.e., the long distance ones, are most likely
to be missed. Most of reported extreme distances by birds
and large vertebrates are less than 10 km. But storms can
disperse birds over large areas resulting in extremes that
are difficult to quantify.
LESSONS FROM THE PAST
Recent global warming does not represent the first time that
survival of plant species has depended on migration. Ice
ages saw repeated and sometimes rapid climate changes. In
regions of steep climate gradients and topographic complexity, such as the Atherton Tableland of northern Queensland,
declining aridity during the Holocene meant that rainforest species may have migrated only tens of kilometers
to replace the sclerophyll vegetation that dominated during Glacial times (Kershaw, 1993; Hopkins et al., 1990).
Mountains of southern Europe (Tzedakis, 1993), western North America (Barnosky et al., 1987), South America (Hoogheimstra, 1984), and Africa (Street-Perrott et al.,
1997) support, within a given region, most of the same
species today that they did during the last glacial maximum
(LGM) (see Last Glacial Maximum, Volume 1). Topographic complexity provides for a range of local climatic
conditions that buffer the effects of climate change.
In areas of low relief, such as eastern North America
and western Eurasia, suitable habitats for many species
shifted across continents. Populations that have survived in
these regions migrated repeatedly over successive glacial
cycles, perhaps at rates exceeding 102 m year!1 (Davis,
1986; Huntley and Birks, 1983). Ever since a rough time
scale for Pleistocene climate changes became available,
ecologists have been impressed with the seemingly impossible dispersal distances required to explain post-glacial
spread of plant populations at these continental scales (Reid,
1899; Davis, 1987; Clark et al., 1998b, Figure 8). In eastern North America and western Europe, glacial distributions
of temperate species are thought to have been well south
of modern distributions. Although the fossil evidence for
glacial distributions is spotty, the southern edge of the Laurentide ice sheet in North America represents an extreme
northern range limit for most species. Populations that now
occupy regions north of the southern ice margin must
6
THE EARTH SYSTEM: BIOLOGICAL AND ECOLOGICAL DIMENSIONS OF GLOBAL ENVIRONMENTAL CHANGE
have migrated at least that far since the LGM, and most
temperate species are thought to have come from refuges
much farther south.
Diffusive spread is too slow to account for migration of
trees (Skellam, 1951; Clark, 1998), and they are especially
inadequate for herbaceous plants. Cain et al. (1998) concluded that there is no documented mechanism by which
most woodland herbs could have reached their modern geographical ranges since the LGM. For many woodland herbs,
ant dispersal is inadequate, and seeds released only centimeters above the forest floor are not susceptible to transport at
wind speeds typical of forest understories. Occasional longdistance dispersal events appear to be the only explanation
for Holocene colonization of northern temperate forest by
woodland herbs.
The fact that dispersal data from modern plant populations do not agree with the rapid spread inferred from
the paleo record has been termed Reid’s Paradox (Clark
et al., 1998). Davis (1987) envisioned migration occurring
as a series of long-distance leaps by a few propagules that
disperse well beyond the typical seed shadow (Figure 1).
Birds (Reid, 1899; Webb, 1987; Wilkinson, 1997), wind
storms (King and Herstrom, 1997), and water transport (Firbas, 1948) are all cited as potential dispersal vectors. Clark
(1998) showed that a small amount of long-distance dispersal is consistent with actual dispersal data that might agree
with the rapid spread of some paleo-species.
There is increasing evidence for barriers to migration
that limited spread of species or genotypes. Molecular
(chloroplast DNA) data from tree populations in western
Europe suggest that east–west oriented mountain ranges
profoundly affected dispersal and, thus, migration at the end
of the last ice age. For example, during the LGM, European
beech (Fagus grandifolia) was present in both Italy and the
Carpathians. But the Italian populations do not appear to
have traversed the Alps, and northern European populations
originated in the Carpathians (Hewitt, 1999).
Some of these same geographic boundaries bolster the
argument that long-distance dispersal contributed to past
migrations. Fossil pollen data indicate that the Baltic and
North Seas (Kullman, 1996) and the Great Lakes (Webb,
1997; Woods and Davis, 1989) did not represent important
obstacles for many species, but oceans did. In contrast to
European beech, oak species in western Europe appear to
have followed several migrational pathways (Figure 3b).
A decline of genetic diversity with distance away from
Pleistocene refugia (Ibrahim et al., 1996; LeCorre et al.,
1997) and highly structured regional populations (Petit
et al., 1997) have been interpreted as consistent with longdistance dispersal events.
Although they represent one of the few plausible alternatives, extreme events, such as those described by fattailed dispersal kernels, may not be the complete solution
to Reid’s Paradox. Clark et al. (2001) demonstrate that
6 ka
8 ka
10 ka
12 ka
(a)
(b)
Figure 3 Two perspectives on Holocene oak migration
in Europe. (a) The 2% deciduous oak isopols contoured
from oak pollen recovered from sediment cores (adapted
from Huntley and Birks, 1983). (b) Migration routes reconstructed from cpDNA of modern oaks (adapted from
Dumolin-Lepegue et al., 1997)
traditional ways to estimate spread from dispersal data
overestimate the potential velocity. A reassessment of
migration potential parameterized with modern dispersal
data predicts much slower spread than has been interpreted
from the paleorecord. No model can rule out the possibility
of past long-distance events, but these new analyses suggest
that rapid migration is harder to achieve than we previously
thought.
PLANT DISPERSAL AND MIGRATION
The reanalysis that revises lower predicted rates of spread
suggests that the interpretation of the fossil record could
bear further consideration. Moreover, not all interpretations
of the paleorecord imply the high rates of spread that
seem necessary to explain migration of temperate trees
from the southern US to temperate latitudes. Bennett (1985)
argues that temperate species may have existed at temperate
latitudes (albeit, south of the Laurentide ice margin) before
the Holocene. He points out that the fossil pollen data that
have been used to interpret spread do not provide concrete
evidence for the presence of populations at low density. In
North America, two recent studies suggest the presence of
temperate hardwoods at least as far north as 35 ° N during
the LGM (Russell and Sanford, 2000; Jackson et al., 2000),
which does not imply migrations rates as high as those
needed if populations were much further south. In western
Europe the LGM climate was more extreme than in North
America, so it is likely that many populations did indeed
migrate from southern Europe.
If migration potential represented an important constraint
during past climate change, then glacial transitions might
be times of extinction. The fossil record does not provide detailed evidence for past extinctions, because fossil
pollen resolve most taxa only to family or genus level.
Thus, we could detect extinctions only of species that can
be resolved in the fossil record. Despite the limitations of
the fossil record, several extinctions near the LGM suggest that dispersal limitation during times of rapid warming
might be a contributing factor. The rainforest genus Dacrydium disappeared from northern Queensland near the LGM
when rainforest contracted due to climate change (Kershaw
et al., 2000). Fossil cones and needles suggest that Picea
critchfeldii may have been both abundant and widespread in
eastern North America during the LGM, but the fossil evidence disappears at the time of most rapid climate change
from 12 to 9 ka. Timing of the event suggests that migration
potential might have been a contributing factor (Jackson
and Weng, 1999) as may have been the case for Sequoia,
Tsuga, Carya, and Nyssa during earlier glacial cycles in
Europe (West, 1970).
Contemporary Invasions
Because contemporary invasions can be documented, they
hold promise for improving our understanding of how
dispersal contributes to migration. Most intercontinental
invasions begin with human dispersal. Countless examples
of non-native invasive species in America have attended
globalization of trade, including ornamental plantings (e.g.,
Brazilian pepper (Schinus terebinthifolius), salt cedar (Tamarix), velvet leaf (Miconia calvescens)), accidental escapes
or contaminants (e.g., leafy spurge Eupohorbia esula, cogon
grass Imperata cylindrica, cheat grass Bromus tectorum),
and erosion control (e.g., mangroves Rhizophora mangle,
7
iceplant Carpobrotus edulis, kudzu Pueraria lobata) (Plant
Conservation Alliance, 2000).
Once introduced, aliens have spread at very different
rates. The large numbers of recent alien introductions
should provide a rich data source concerning the role of
dispersal. Unfortunately, the dispersal biology of invading
species has seldom been studied in the context of the spatial pattern of spread (Parendes and Jones, 2000), and there
are few examples of migrations that can be linked to dispersal data. Most contemporary invasions are known from
anecdotal information on time and location of introduction,
mode of spread, and impacts on native communities (Mack,
1986). Studies of the invasions themselves tend to focus
on the characteristics that make ecosystems prone to invasion (Hobbs and Huenneke, 1992; Lonsdale, 1999) or on
characteristics of species that make for successful invaders
(Perrins et al., 1992). Several studies that have examined
seed dispersal after invasions (Van Wilgen and Siegfried,
1986; Malo and Suarez, 1997) focus on characteristics of
seeds rather than on the spatial aspects of spread. While
experience with contemporary invasions becomes the basis
for assessing invasive potential and for restrictions on the
import of exotic species (Ruesink et al., 1995; Ewel et al.,
1999), poor understanding of dispersal partly explains our
low predictive capability, even post hoc.
Several examples where dispersal biology has been
reconstructed post hoc illustrate the idiosyncrasies of individual invasions. Some species that are absent from suitable
habitats, upon introduction, expand rapidly. In 1902, the
American Sugar Corporation introduced Rhizophora mangle, a Florida mangrove, to Molokai, Hawaii, in an effort
to mitigate coastal erosion. The islands had not supported
mangrove species prior to this time, presumably due to
dispersal limitation. R mangle dispersal depends on ocean
currents, and those that affect Hawaii flow from the direction of Alaska. However, once introduced, the species has
spread by natural drift throughout the archipelago (Wester,
1982). The R mangle example illustrates that even a broadly
dispersed species can be dispersal-limited, depending on the
details of the dispersal process.
High fecundity can interact with novel dispersal vectors
to accelerate the spread of alien species. Purple loosestrife (Lythrum salicaria) came to American shores in the
early 1800s in contaminated ship ballast from the European coast (Stuckey, 1980). The plant thrives in marshes,
wetlands, and riparian zones, and it spreads rapidly along
waterways. The plant produces >100 000 seeds per stem
that can disperse short distances by winds and as buoyant
seeds and seedling cotyledons in flowing waters and ditches
(Balogh, 1986), and along highways in high winds created
by trucks (Wilcox, 1989). Once established, purple loosestrife propagates vegetatively and rapidly chokes out native
plants. This rapid spread illustrates the importance of high
fecundity, the effects of which are amplified by the rare,
8
THE EARTH SYSTEM: BIOLOGICAL AND ECOLOGICAL DIMENSIONS OF GLOBAL ENVIRONMENTAL CHANGE
extreme dispersal events made possible by water transport
and human vectors.
The rate and pattern of spread can be highly variable.
Cheatgrass (Bromus tectorum) migration throughout the
intermountain West represents one of the best-documented
alien invasions (Carpenter and Murray, 2000). A reconstruction by Mack (1986) suggests that cheatgrass probably
arrived in the 1880s as a seed contaminant from Europe.
Before 1900, it was noted from photographs, in collections,
and by wheat growers from British Columbia to Utah. An
annual with wind dispersed seeds, cheatgrass spread was
accelerated by rail transport of livestock, as seeds adhere to
fur, and they survive in dung. Following an initial lag phase,
cheatgrass range expansion was rapid, but patchy. Centers
of abundance spread to several western states in the early
1900s and coalesced over the next few decades to form a
relatively continuous range in the Intermountain West. By
1930, cheatgrass had reached its current distribution across
the Great Basin. The initial lag has been observed for a
number of invasions (e.g., Pitelka et al., 1997). The patchy
spread is consistent with fat-tailed dispersal with infilling
being more representative of a diffusion process.
The potential to learn from contemporary invasions is
unrealized, in part, due to limited study of dispersal. When
dispersal is available, it may not be enough to predict rates
of spread, because disturbance and species interactions have
profound effects on establishment success.
WHAT TO EXPECT: GLOBAL WARMING,
MASS INTRODUCTIONS, AND HUMAN
DISTURBANCE REGIMES
Dispersal is critical for plant migration, representing the
first step in a complex process that involves establishment,
growth, and survival. We cannot yet expect to accurately
predict many new invasions. Because dispersal is too poorly
understood, especially the long-distance events that disproportionately control invasion speed, migrations will be so
variable that forecasts will be of limited use for any specific invasion that occurs. Global changes in disturbance,
land cover, dispersal vectors, and climate interact with plant
migrations, many involving scales of space and time that
are not yet well-understood: in addition biotic interactions
may play an overriding role in many migrations. These may
not be predictable from dispersal potential or from those
interactions in their places of origin.
The first two of these concerns deal directly with the
relationship between dispersal and migration and are the
focus of this review. Too few studies have attempted
to quantify dispersal and seed production at necessary
spatial and temporal scales (Clark et al., 1999b). Maximum
dispersal distances estimated by direct or inverse methods
range to several hundred meters, although indirect evidence
indicates that propagules sometimes travel much farther.
Average dispersal distances are negatively correlated with
seed size and positively correlated with fecundity, and
fecundity is highly variable. Models lead us to expect erratic
migrations with mean rates controlled by extreme dispersal
events. High propagule producers have the clear advantage
in this process, much more so than would be expected by a
process of diffusion. Although dispersal data will allow us
to develop estimates of spread potential based on dispersal
ability, those estimates will have broad variance. Thus, the
rates for any given species in any given environment will
deviate from the expectation.
The latter two concerns are not the focus of this review,
but they play such a large role in migrations that they
will ultimately determine our understanding of population
spread. We briefly summarize some of the changes in our
biotic and physical environment that will have profound
impacts on future plant dispersal and migration.
Interactions with Global Change
Changing chemistry of the atmosphere and climate present
new sources of uncertainty for plant migrations. Despite
interpretations that past migrations may have occurred
rapidly, long distance dispersal may not save many species
from the climate change associated with greenhouse warming. The rates of 21st century climate change pose unprecedented challenges to migration, perhaps requiring species
ranges to shift at rates of 1–5 km year!1 (Davis, 1986;
Dyer, 1995; Sykes and Prentice, 1996; King and Herstrom,
1997). Analyses of dispersal consequences for tree migration rates (Clark et al., 2001) suggest that a number of
species simply may not disperse far enough. The molecular evidence suggesting the importance of corridors for
migration in Europe (Figure 3) raises additional concerns
for future migrations.
A changing physical environment is complicated by
a shifting biotic one. For predicting migrations, dispersal information from extant ecosystems is not enough.
Contemporary invasions have surprised us before, due to
unexpectedly high competitive abilities of alien species
and novel dispersal vectors. Although we might have
been able to quantify dispersal reasonably well in some
of these cases, the migration potential often depends on
interactions.
Climate change may reorganize food webs in ways that
impact migration rates, as some species outrun their mutualists and natural enemies, while others become limited by
new biotic settings. Vertebrate dispersal vectors and pollinators may not respond to climate change in step with the
plants that would benefit from them (Bethke and Nudds,
1995; Bawa and Dayanandan, 1998; Bazzaz, 1998; Sorenson et al., 1998; Visser et al., 1998; Dunn and Winkler,
1999). For example, droughts that reduce wetlands and
the migratory waterfowl that depend on them (Bethke and
PLANT DISPERSAL AND MIGRATION
Nudds, 1995; Sorenson et al., 1998) will ultimately reduce
transport of seed (Ehrlich et al., 1988). Likewise, extreme
winter storms reduce passerine densities and their ranges
(Mehlman, 1997). Recent global warming in temperate
regions has already accelerated some phenological events
that affect dispersal. For example, Estonian springs have
advanced eight days over the last 80 years, with the last
40 years being particularly warm (Ahas, 1999). In seasonal
environments, avian reproduction is successful if timed to
food availability. Future increases in spring temperature
could result in a mismatch between the timing of egg
laying and the availability of food (Visser et al., 1998).
Increasing springtime temperatures from 1959 to 1991 have
caused North American tree swallows (Tachycineta bicolor)
to lay eggs nine days earlier (Dunn and Winkler, 1999).
The potential decoupling of plant-animal phenologies may
be particularly important in the Tropics, where the links
among plant reproductive effort, pollination, and vertebrate
seed dispersal are strong (Bawa and Dayanandan, 1998;
Bazzaz, 1998), and many plant species and their propagules are locally rare (Clark et al., 1999a). If increased
temperatures result in increased fire, then not only will fireadapted species become more abundant (e.g., Starfield and
Chapin, 1996), but animal seed dispersers may respond.
For example, Johnson et al. (1997) have observed that blue
jays (Cyanocitta cristata) cache more nuts in grasslands
following fires.
Given the importance of fecundity for dispersal when
kernels are fat-tailed, the effects of changing atmospheric
chemistry on seed production could impact on migration
potential. Elevated atmospheric carbon dioxide (CO2 ) may
cause seed production to increase (Farnsworth and Bazzaz,
1995; Schaeppi, 1996; Thomas et al., 1999; LaDeau and
Clark, 2001), to decrease (Farnsworth and Bazzaz, 1995;
Fischer et al., 1997; Thomas et al., 1999) and/or to occur
at an earlier age (Farnsworth et al., 1996; LaDeau and
Clark, 2001). Increased nitrogen deposition may have no
reproductive impact or it may increase plant fecundity (Gordon et al., 1999), whereas increased tropospheric ozone
(O3 ) may damage vegetative tissue and reduce reproductive success (Musil et al., 1999; Bergweiler and Manning,
1999). Interactions among climate, CO2 , nitrogen, O3 , and
ultraviolet-B radiation could result in surprises.
Land cover change and human disturbance have many
indirect consequences for recent migrations in ways that
facilitate spread of some and slow spread of others. Disturbance has hastened the spread of many introduced aliens,
with temperate agricultural and urban sites being among
the most invaded areas (Lonsdale, 1999). In some arid and
semiarid lands, land clearance and changes in fire regime
have facilitated the expansion of exotic grasses (D’Antonio
and Vitousek, 1992). In others, humans have promoted the
spread of woody vegetation. For example, 20th century
livestock grazing, removal of native Americans, and fire
9
suppression have promoted the spread of shrubs and trees
in pygmy woodlands of western North America (Chambers
et al., 1999). Damming of the Colorado River reduced
water table fluctuations, resulting in replacement of riparian hardwoods by the introduced saltcedar (Vitousek et al.,
1996). Eurasian aliens may have flourished in the intermountain West, in part because large, congregating mammals were absent in pre-settlement time. Lack of summer
rainfall limited productivity of the warm-season C4 grasses
and, thus, green forage for grazers in summer. The native
bunchgrasses did not respond well to introduced livestock
and were replaced by Eurasian exotics adapted to both
climate and grazers (Mack and Thompson, 1982; Mack,
1986).
On the other hand, human disturbance will hinder spread
of many native and exotic species. For many species, land
cover change will have the simple consequence of removing
much of the area needed for population spread. The alien
invader Lonicera maacki appears to spread fastest where
forest cover is connected; large expanses of agricultural
land act as a barrier to dispersal of this species (Hutchinson and Vankat, 1998). Many tree species will experience
similar effects. Models incorporating fragmentation often
predict delayed invasion due to a simple reduction in available habitat (Higgens and Richardson, 1999). Often the
effects are more complex involving alterations in animal
vector behavior (Verboom et al., 1991; Pitelka et al., 1997)
and presenting novel establishment options, both positive
and negative.
The natural dispersal kernels most often studied by ecologists are supplemented by a host of new modes of seed
dispersal. Human activities have escalated and spread far
beyond those that prevailed in the past. The occurrence of
weedy species in charred remains of Neolithic grain stores
of central Europe shows that broad, inadvertent dissemination has a history and a prehistory (Behre, 1981; Gluza,
1983). Establishment of towns and trade allowed for introductions as contaminant crop seed, fodder, or as escapes
from horticultural plantings (Parker, 1977). Many Eurasian
weeds in the western US were introduced as contaminants.
Humans disperse propagules in a number of ways, but
species producing large numbers of propagules tend to be
best represented in two of the most important dispersal
pathways in Britain, topsoil transport and cars (Hodkinson and Thompson, 1997). The number of exotic species
in nature reserves is correlated with visitation rates (Lonsdale, 1999), which supports the importance of vehicular
transport.
Improving Our Understanding
The importance of dispersal for plant migration is sufficiently uncertain that simulations involving future climate
change often contrast scenarios of no dispersal with ones
10 THE EARTH SYSTEM: BIOLOGICAL AND ECOLOGICAL DIMENSIONS OF GLOBAL ENVIRONMENTAL CHANGE
that assume global dispersal (e.g., Sykes and Prentice,
1996; Pitelka et al., 1997). By bracketing reality between
extremes, we gain insight into migration potential at scales
relevant for some of the most profound environmental challenges to plant populations since the end of the Pleistocene.
The simulations that explore these effects demonstrate the
importance of dispersal and highlight our inadequate characterization of it.
Understanding plant population spread is a realistic goal
that requires realistic expectations. The contribution of
dispersal limitation is knowable, but it will require more
analysis at the appropriate spatial and temporal scales
(Clark et al., 1999b). We know enough now to appreciate
its central role in migration potential. We should not expect
precise forecasts of spread rate, due to its highly stochastic
nature. But we can expect that a better understanding of
fecundity and dispersal biology will help us identify species
having potential for rapid spread given suitable conditions
for growth and survival.
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