American Journal of Botany 96(8): 1544–1550. 2009.
BREEDING SYSTEM AND POLLINATION ECOLOGY OF INTRODUCED
PLANTS COMPARED TO THEIR NATIVE RELATIVES1
Alexandra N. Harmon-Threatt,2 Jean H. Burns, Lyudmila A. Shemyakina, and
Tiffany M. Knight
Department of Biology, Washington University in St. Louis, 1 Brookings Drive, Campus Box 1137,
St. Louis, Missouri 63130 USA
Identifying how plant–enemy interactions contribute to the success of introduced species has been a subject of much research,
while the role of plant–pollinator interactions has received less attention. The ability to reproduce in new environments is essential
for the successful establishment and spread of introduced species. Introduced plant species that are not capable of autonomous
self-fertilization and are unable to attract resident pollinators may suffer from pollen limitation. Our study quantifies the degree of
autogamy and pollination ecology of 10 closely related pairs of native and introduced plant species at a single site near St. Louis,
Missouri, USA. Most of these species pairs had similar capacities for autogamy; however, of those that differed, the introduced
species were more autogamous than their native congeners. Most introduced plants have pollinator visitation rates similar to those
of their native congeners. Of the 20 species studied, only three had significant pollen limitation. We suggest that the success of
most introduced plant species is because they are highly autogamous or because their pollinator visitation rates are similar to those
of their native relatives. Understanding and identifying traits related to pollination success that are key in successful introductions
may allow better understanding and prediction of biological invasions.
Key words: autogamy; invasive species; introduced plants; mutualism; plant–pollinator interactions; plant mating systems;
pollen supplementation; pollinator visitation rates.
Understanding the mechanisms that allow introduced plant
species to successfully establish and persist is a primary focus
of research in invasion biology (Alpert et al., 2000; Shea and
Chesson, 2002; Lambrinos, 2004; Müller-Schärer et al., 2004;
Torchin and Mitchell, 2004). One prominent hypothesis is the
enemy release hypothesis (Keane and Crawley, 2002), which
posits that introduced species have increased fitness in their introduced range relative to their native range (or relative to native species in their introduced range) as a result of release from
their natural enemies such as herbivores and pathogens. However, when introduced species leave their native habitats, they
are not only escaping enemies, which inhibit their fitness, but
they may also leave behind their natural mutualists (e.g., pollinators), which can be vital to their reproduction and establishment. Buchmann and Nabhan (1996) estimated that 90% of
angiosperms are biotically pollinated. For introduced plants
that require pollinators, their reproductive success depends on
their ability to attract the services of resident pollinators that
1
Manuscript received 31 October 2008; revision accepted 12 March 2009.
The authors thank J. Chase, K. Olsen, members of the Knight laboratory
at Washington University in St. Louis and the Kremen laboratory at the
University of California, Berkeley, Ø. Totland, and one anonymous
reviewer for comments that improved the manuscript. K. Moriuchi, S.
Zang, and A. Chung helped with pollinator observations and experiments.
They also thank T. Morhman for plant identification and location
information and J. Chase for logistical support. Funding for this project
was provided by Tyson Research Center, Washington University in St.
Louis, Howard Hughes Medical Institute, American Association of
University Women, Missouri Native Plant Society, and National Research
Initiative of the USDA Cooperative State Research, Education and
Extension Service, grant no. 05–2290.
2 Author for correspondence (e-mail: [email protected]);
present address: UC Berkeley, Dept of Environmental Science, Policy &
Management,137 Mulford Hall #3114, Berkeley, CA 94720 USA
doi:10.3732/ajb.0800369
can provide accurate pollen transfer in their new range. Understanding how plants succeed despite being decoupled from their
native pollinators is critical if we are to understand and predict
biological invasions and will provide insight into the ecology
and evolution of plant–pollinator interactions.
The reproductive success of introduced species will depend
on the ability of the plant to (1) produce offspring in the absence of pollinators (autonomous self-fertilization), (2) attract
resident pollinators, and (3) have sufficient pollen transferred
by pollinators to maximize seed set and prevent pollen limitation. The establishment of introduced species is often initiated
from a small founding population. When populations are small,
autogamous or vegetative reproduction is expected to be favorable because a single individual is sufficient for colonization
(e.g., Baker, 1955). This theory leads to the hypothesis that
introduced plant species are more likely to have autogamous
breeding systems compared to native plant species. Consistent
with this hypothesis, Daehler (1998) found that plant families
that only contain biotically pollinated species are less likely to
contain species that invade natural areas than those that contain
at least some abiotically pollinated species. Also, Rambuda
and Johnson (2004) studied the breeding systems of 17 introduced woody species in South Africa and found that all of them
were capable of self-pollination and 72% were capable of autogamy (see also van Kleunen and Johnson, 2007; van Kleunen
et al., 2008).
Although capacity for autonomous self-fertilization (“autogamy” throughout) could be beneficial to introduced species
colonizing new areas, autogamy is not necessary for successful
introductions. Introduced plant species that are not autogamous
need to be sufficiently pollinated by resident pollinator species
in their introduced range to successfully establish or their specialist pollinator needs to have been introduced (Richardson
et al., 2000). Several studies have shown that introduced plant
species that require pollinators can successfully attract resident
generalist pollinators (Richardson et al., 2000; Brown et al.,
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Harmon-Threatt et al.—Pollination ecology of introduced plants
2002; Memmott and Waser, 2002; Olesen et al., 2002; Goulson,
2003; Goulson and Hanley, 2004; Morales and Aizen, 2006;
Bjerknes et al., 2007). The ability to attract pollinators, however, does not guarantee sufficient quantity and quality of pollen transfer (Fishbein and Venable, 1996; Irwin et al., 2001;
Richardson, 2004; Aizen and Harder, 2007). This information
leads to the additional hypothesis that introduced plant species
that are not autogamous must have pollinator visitation rates
equal to or greater than their native relative or they will suffer
from pollen limitation.
Understanding the degree of pollen limitation and the breeding systems of introduced plant species will help identify the
role of pollination in invasions; however, few pollen supplementation experiments testing for pollen limitation have been
conducted on introduced species. Of over 1000 pollen supplementation experiments synthesized in a recent review, only 10
were of introduced plant species (Knight et al., 2005), and thus,
there was insufficient power to detect difference in the magnitude of pollen limitation between native and introduced plant
species.
Relatively few studies of pollination ecology have compared
introduced species to closely related native species (Brown
et al., 2002); however, such contrasts might increase the power
of comparative tests (Martins and Garland, 1991) if some of the
variation in breeding system and pollination success is due to
phylogeny (Felsenstein, 1985). In some systems, there is a signal of phylogeny on breeding system traits (Kelly and Woodward,
1996; J. H. Burns, University of California–Davis; R. B. Faden,
Smithsonian; and S. J. Steppan, Florida State University, unpublished data), and thus we might expect that it would be
necessary to control for relatedness in breeding system comparisons. This study is the first experimental manipulation of
the pollination ecology of multiple pairs of closely related introduced and native congeners (or confamilials if congeners
were not available).
To assess the role of pollination ecology on the reproductive
fitness of introduced plants, we evaluated three possible factors
affecting reproductive success: autogamy, attraction to pollinators, and pollen limitation. We expected that (1) breeding system would be conserved within a family (null hypothesis), but,
when it was not, the introduced plant would have a higher degree of autonomous self-fertilization, (2) introduced species
that were not autogamous would have similar pollinator visitation rates as their native relatives (because of similarity in floral
traits across plants within a family), and (3) plants that are not
autogamous and attract fewer pollinators would show significant pollen limitation. We found support for autogamy, high
pollinator visitation, and significant pollen limitation in some of
our introduced plant species.
MATERIALS AND METHODS
Study site and species—These studies were conducted over four summers
(2004, 2005, 2007, 2008) at Tyson Research Center, an 80-ha field station
owned and managed by Washington University in St. Louis and located 40 km
southwest of St. Louis, Missouri, USA. Most of the site (85%) consists of oak–
hickory forest, and the remainder consists of old fields and open areas with
plants.
We compared species pairs, all of which are biotically pollinated, from 10
plant families that occur at the field site (Fig. 1). Species were paired by family,
and when possible by genus, to control for differences in traits across lineages.
To limit noise caused by temporal differences, all data for both species in each
pair were recorded within the same year. Species classifications as native or
introduced were determined using USDA categorization (USDA, 2007). Intro-
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duced species were all introduced from Eurasia and were classified as either
invasive or naturalized based on the USDA Plants Database (USDA, 2007) and
Missouri Exotic Pest Plant (Missouri Botanical Garden, 2007) list (Fig. 1). For
most of our native and introduced plant species, multiple populations were
present within our study site. In these cases, we choose study populations for
which the native and introduced species within a pair occurred at similar population sizes and floral densities.
Breeding system experiments—To determine whether introduced and native species differed in their ability to autonomously self-fertilize, we conducted
pollinator exclusion experiments. We determined the degree to which each species could reproduce in the absence of visits from animal pollinators because
autogamy might be relevant for colonization success (Baker, 1955, 1974).
Flowers (or inflorescences, racemes) of each species (see Fig. 1 for sample
sizes) were individually bagged with thin, small-mesh (<1 mm) netting prior to
blooming to prevent pollinator access but allow wind access. These flowers
were paired with nearby flowers on different plants that were hand pollinated
with outcross pollen (see pollen supplementation experiment methods below)
and left unbagged. The size of the bags used and the number of flowers inside
the bag differed among the species pairs in this study because flower size and
the spatial clustering of flowers within a plant differed among these pairs. For
most species, we bagged and hand pollinated one flower. However, for some
pairs, such as the Brassicaceae, a raceme of flowers was bagged, but only one
flower, which was marked on the pedicel, was included in the experiment. For
the Asteraceae, the whole inflorescence was manipulated. Bags were large
enough to give flowers space to open but not so large that they weighed down
the plant. Further, care was taken to ensure that the bags were large enough that
they did not rub against the stigma and anthers of the flower, inadvertently pollinating the flower(s) within the bag. Flowers were chosen for this experiment
when they were in the bud phase, and plants in the hand-pollinated treatment
were hand pollinated as they opened (see pollen supplementation experiment
methods later). We documented whether the flower formed a fruit, and if a fruit
formed, we counted the number of seeds per flower when possible. For species
pairs for which we had data on number of seeds per flower, the degree of autogamy is the ratio of the bagged to hand-pollinated seed set per flower. For
species pairs for which we did not count seeds per flower (i.e., because of the
difficulty of accurately counting seeds for some species pairs), fruit set (number
of fruits/number of flowers) was used as a measure of autogamy. We chose to
measure the ratio of bagged to hand-pollinated rather than bagged to openpollinated so that we would not overestimate the degree of autogamy for species with high pollen limitation. For each plant family, we used a one-way
ANOVA to determine whether the native and introduced species differed in
their degree of autogamy. We also calculated 95% confidence intervals around
each estimate of autogamy to determine whether each species exhibited significant (different from zero) autogamy.
Pollinator observations—To determine whether introduced and native species differed in pollinator visitation rates, we conducted observations of pollinator visits to each species. Each species was observed at least five times for
20 min, and observations were spaced evenly throughout the day, excluding the
hottest portions when pollinators are not active. A visit was counted if the visitor was observed on the flower’s sexual organs. Observations were shifted to
accommodate the blooming time of Potentilla recta, which only blooms in the
afternoon, and Commelina and Convolvulus species, which only bloom in the
morning. No pollinator observations were conducted at night, although there is
some evidence that Silene stellata is partially nocturnally pollinated, and therefore pollinator visitation rates might be underestimated for this species.
Often several flowers on different plants were observed during a single observation. In these cases, we pooled the visitation rate across these flowers to
get a single data point for visitation rate. We calculated visitation rate as the
number of visits per flower per 20-min observation. Visitation rate was continuously distributed and was treated as a continuous variable. For each plant family, we used one-way ANOVA to determine whether native and introduced
flowers differed in their visitation rate. The visitation rate was square-root
transformed for species in the Caprifoliaceae, Commelinaceae, and Liliaceae
families, and assumptions of ANOVA were checked and met for all tests
presented.
Pollen supplementation experiments—We conducted pollen supplementation experiments to quantify pollen limitation for each species. Approximately
20 pairs of flowering individuals (40 individuals total) of each species were
marked with neutrally colored (brown or black) yarn and randomly divided into
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American Journal of Botany
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Fig. 1. All species examined in this study. Descriptions are based on observations recorded during the study. Note: All species occurred at the Tyson
Research Center. All species are classified as forbs by the USDA PLANTS Database (USDA, NRCS, 2007) except Lonicera japonica, L. flava, and Vicia
villosa, which are vine, vine/shrub, and vine/forb, respectively. Introduced species were all introduced from Eurasia and classified as invasive or naturalized
based on the USDA PLANTS Database and Misssouri Exotic Pest Plant List (Missouri Botanical Garden 2007). Pollen limitation studies were not conducted on the Asteraceae or Lilliaceae pairs. A hyphen (-) indicates no data were recorded for this species.
two treatment groups: control or supplement. Pairs were similar in size and
close to each other to control for microsite variation. One of the individuals
from each pair was chosen as the control treatment, marked, and left exposed to
pollinators without manipulation. The other individual was supplemented with
pollen collected from a single donor at least 1 m outside the experimental patch
and applied using a small paint brush or tweezers. Each flower chosen for the
experiment was on a separate plant. The flower-level, as opposed to wholeplant-level, manipulation was chosen to maximize the amount of effort spent in
quantifying pollen limitation for multiple pairs, maximizing the power to generalize. Flower-level manipulations may result in overestimation of pollen limitation if plants reallocate resources to flowers with supplemented pollen within
a plant (Knight et al., 2006).
We documented whether the flower formed a fruit, and if a fruit formed, it
was collected and seeds from each fruit were counted when possible. Flowers
that were damaged were not included in the analyses. For each pair of flowers,
we calculated the magnitude of pollen limitation as ln(number of seeds per
flower in supplement treatment + 1) − ln(number of seeds per flower in control
treatment +1) using standard methods for ecological meta-analyses (e.g.,
Hedges et al., 1999). If seed set was identical in the control and supplement
treatment, then the magnitude of pollen limitation equals 0. When seed set in
the supplement treatment exceeded seed set in the control treatment, pollen
limitation was determined to be greater than zero which signifies pollen limitation. For each plant family, we used one-way ANOVA to determine if the native and introduced species differed in their magnitude of pollen limitation. We
also calculated 95% confidence intervals around each estimate of pollen limitation to determine whether each species had significant (different from zero)
pollen limitation.
RESULTS
Breeding system was not significantly different in six of 10
species pairs (Fig. 2A). Autogamy levels for five of 10 introduced species and four of the 10 native species differed significantly from zero (Appendix S1, see Supplemental Data with
online version of this article). The Fabaceae, Scrophulariaceae,
and Liliaceae pairs failed to set any seed in the bagged treatment (i.e., no autogamy; Appendix S1). The Asteraceae species
were both fully autogamous. The introduced Commelinaceae,
Caryophyllaceae, Convolvulaceae, and Rosaceae had significantly higher fruit set when bagged than did their native relative
(F1,25 = 11.68, P < 0.001; F1,7 = 52.76, P < 0.001; F1,22 = 44.11,
P < 0.001; F1,13 = 9.66, P < 0.01, respectively).
Pollinator visitation rates of introduced species did not differ
significantly from or were greater than their native species pair
in eight of nine cases (Fig. 2B). In the Rosaceae pair, the introduced species had a significantly higher visitation rate than its
native counterpart (F1,8 = 20.9, P < 0.002). However, flowers
of the introduced Caprifoliaceae were visited less frequently
by pollinators than flowers of the native species (F1,8 = 8.46,
P < 0.02).
Three species (the introduced Fabaceae, the introduced Caprifoliaceae, and the native Convolvulaceae) had significant pollen
limitation (i.e., different from zero) (Appendix S2, see Supplemental Data with online article). Despite having the same pollinator
visitation as its native species pair, the introduced Fabaceae species
had a pollen limitation magnitude of 0.797 r 0.206, while the native had a pollen limitation magnitude of −0.128 r 0.163. The introduced Caprifoliaceae received significantly fewer visits than
its native congener and had significantly higher pollen limitation
(Fig. 2B and 2C). The native Convolvulus sepium was significantly
pollen limited, in spite of relatively high visitation rates (Fig. 2B).
Pollen limitation differed between the native and introduced species in the Brassicaceae, Fabaceae, Convolvulaceae, and Caprifoliaceae families (F1,35 = 5.608, P = 0.02, F1,26 = 11.96, P = 0.001;
F1,18 = 5.652, P = 0.03; and F1,62 = 7.93, P = 0.01, respectively),
where the introduced species is more pollen limited for three of
these cases, and only the native Convolvulus is more pollen limited
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Harmon-Threatt et al.—Pollination ecology of introduced plants
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DISCUSSION
Fig. 2. The degree of autogamy (ratio of reproductive success [seeds
per flower or fruit set] in the bagged : pollen supplement treatment) (A),
pollinator visitation rate (visits/flower/20 min) (B) and magnitude of pollen limitation (ln [supplement reproductive success] – ln [control reproductive success]) (C) for introduced and native species pairs. Introduced
species and native species that differ for these response variables are indicated by *** P < 0.001, ** P < 0.01 and * P < 0.05.
than the introduced Convolvulus. Note that in the case of Convolvulus, the native was less autogamous than the introduced species.
Pollen limitation for the Liliaceae pair was not calculable due to
low population numbers and primarily vegetative reproduction.
The reproductive success of a plant is a complex function of
breeding system and pollination ecology (Harder and Barrett,
2006; Waser and Ollerton, 2006). Understanding reproductive
success has profound implications for species invasions and fitness. We present the first study to contrast autogamy, pollinator
visitation, and pollen limitation of multiple pairs of related introduced and native species, to examine the role of these in the
reproductive success of introduced species. We predicted that
established introduced plants will either (1) have the capacity
for autonomous self-fertilization and thus not require pollinators, (2) be able to attract resident pollinators, or (3) be significantly pollen limited. Our results show support for each of these
possible outcomes. Thus, introduced plants are diverse in their
pollination ecology: some are successful because of their autogamous breeding system, some are able to successfully attract
resident pollinations, and others manage to establish and spread
despite significant pollen limitation.
We expected that the degree of autonomous self-fertilization
would be conserved for most species pairs, and when it differed, the introduced species should have greater autogamy.
The similar breeding system of most of our species pairs suggests that there is a strong signal of phylogeny on breeding system traits, which has been shown in other studies (Kelly and
Woodward, 1996; J. H. Burns, R. B. Faden, and S. J. Steppan,
unpublished data). However, four of our species pairs differed
significantly in their degree of autogamy, and in three of these
cases, the introduced species was more autogamous than its native relative. Our results may indicate that autogamy is an important factor in the establishment of introduced plant species,
as suggested by Baker (1974), and are consistent with other
synthetic studies that show that autogamous plant lineages have
high representation in introduced flora (e.g., Rambuda and
Johnson, 2004; van Kleunen and Johnson, 2007; van Kleunen
et al., 2008). However, our study and these reviews can only
show a pattern of higher autogamy in introduced plants. A true
test of Baker’s law would consider the global invasiveness of
both native and introduced species in each pair, for which we
do not account. Further studies of plants during their establishment phase are necessary to conclude if Baker’s (1974) mechanism is correct.
Our second hypothesis was that introduced species would
have greater pollen limitation than native relatives, if they had
lower pollinator visitation. Most pairs did not differ significantly in their pollinator visitation rate. There were significant
differences in visitation rate for the Caprifoliaceae and Rosaceae pairs: the Caprifoliaceae had greater visitation for the native species and the Rosaceae had lower pollinator visitation for
the native species. It is unclear why the introduced Caprifoliaceae, Lonicera japonica, which has a white flower that is similar in size and morphology to its native congener, L. flava (a
yellow-flowered species), is less attractive to pollinators. We
note that the native L. flava was primarily pollinated by carpenter bees, which appeared to have a high rate of nectar robbing
(fruit set was only 22% for this species). The higher visitation
rate of the introduced Rosaceae might be due to its larger petal
size and taller, more erect stems. While we were careful to
choose locations in which the native and introduced pair
occurred at similar densities and population sizes, it is possible
that small differences in population size and density caused the
differences in visitation rate observed for the Caprifoliaceae
and Rosaceae species pairs. In addition, we did not measure
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American Journal of Botany
other floral traits that pollinators are known to respond to, such
as floral scent and nectar quantity and quality. In general, our
results are consistent with observations in other studies that introduced plants can successfully attract resident generalist pollinators (Richardson et al., 2000; Brown et al., 2002; Memmott
and Waser, 2002; Olesen et al., 2002; Goulson, 2003; Goulson
and Hanley, 2004; Morales and Aizen, 2006).
We predicted that those introduced species without significant autogamy or high visitation rates should be more pollen
limited than their native relatives. We found limited support for
this prediction (in the Caprifoliaceae pair): the only introduced
species that was not autogamous and had significantly lower
visitation rates than its native pair also had a higher magnitude
of pollen limitation relative to its native pair. However, while
the breeding system and pollinator visitation rates of the introduced Fabaceae were similar to those of its native relative, it
was still more pollen limited. Our native Fabaceae species is
known to be a host plant for the northern cloudywing (Thorybes
pylades), which was also the most frequent visitor, while the
introduced species was visited primarily by generalist bees.
Thus, while visitation rates are similar between these species,
the quality of each visit might be much higher for the native
species. The native Convolvulaceae was more pollen limited
than its introduced pair, which is not surprising because it was
also less autogamous. In most cases, large effect sizes corresponded well with significance, but in a few cases we did not
detect significant autogamy or pollen limitation in some species
where the magnitudes of the effects were fairly high (e.g., Verbascum blattaria has pollen limitation of 1.23 but does not have
statistically significant pollen limitation) but power was low
(online Appendix S2). Therefore, the lack of significant autogamy or pollen limitation in cases with small sample sizes should
be interpreted cautiously.
Pollen limitation does not necessarily limit a plant’s ability
to establish and spread because both Vicia villosa (introduced
Fabaceae) and Lonicera japonica (introduced Caprifoliaceae)
are pollen limited and have also been highly successful in their
introduced range. Both species are widespread in the USA and
are considered invasive by the U. S. Department of Agriculture (USDA, 2007). One possible reason for their success in
spite of significant pollen limitation is that both species are
capable of reproducing asexually, and their local population
growth may not be seed dependent. Each of these species also
produces many flowers, so, while individual flowers may be
pollen limited, the plant will still produce many seeds and thus
may not suffer demographic consequences. Further, both of
these species are successful in disturbed habitats. Vicia villosa
is able to fix nitrogen and may be able to readily establish on
disturbed, nitrogen-poor soils. Significant pollen limitation has
been shown in other successful invasive plants. For example,
Parker (1997, 2000) demonstrated that Cytisus scoparius was
highly pollen limited, and yet, its population growth rate was
still high.
In our study, we only found significant pollen limitation in
one of the native species. This result is in contrast with recent
reviews that show that >60% of plant populations are pollen
limited (Burd, 1994; Knight et al., 2005). The lack of pollen
limitation in most of our native plant species might be due to
our choice of study species. We chose native plant species that
were closely related to introduced plant species, and because
breeding systems and floral traits are often conserved in lineages, we may have preferentially chosen native species that
are highly generalized in their pollination or autogamous and
[Vol. 96
thus less likely to suffer from pollen limitation. Indeed, ecologists choose to study native plants that have interesting pollination ecology (e.g., orchid and lily species are overrepresented in
the pollination literature), and therefore the studies available for
review are a biased sample of angiosperms (Knight et al., 2005,
T. M. Knight, unpublished results). However, it could also be
argued that most plants are generalized in their pollination
(Waser et al., 1996) or to some extent autogamous, and we cannot directly compare our plant species to those reviewed in the
pollen limitation meta-analysis by Knight et al. (2005) because
most of the studies in the meta-analysis do not evaluate degree
of autogamy.
This study focuses on already established introduced plants;
a broader understanding of the role of pollination ecology in
biological invasions will require considering other phases in the
invasion process for several reasons. First, the fitness consequences of different breeding systems may shift at different
stages of invasion (e.g., autogamy may be favored at early
stages of invasion, but breeding systems that promote outcrossing might be favored after establishment). Second, Allee effects, a positive relationship between fitness and either numbers
or density of conspecifics (Allee, 1931, 1938; Stephens and
Sutherland, 1999), may decrease the probability that an introduced species will establish and/or slow its spread (e.g., Ågren,
1996, but see Davis et al., 2004; Cappuccino, 2004; van Kleunen
and Johnson, 2005, 2007). Third, self-compatibility could also
play a significant role in the establishment of introduced species. Self-compatible species might be less restricted by
propagule supply in the early stages of an introduction if geitonogamy provides reproductive assurance (Stebbins and Singh,
1950; Stebbins, 1957; Pannell and Barrett, 1998; Morgan and
Wilson, 2005), which could enhance establishment success
even in small founding populations (e.g., Baker, 1955; Rambuda
and Johnson, 2004).
The successful establishment and spread of introduced species is often discussed in the context of the enemy release hypothesis (reviewed by Mitchell and Power, 2003; Colautti et al.,
2004; Hinz and Schwarzlaender, 2004; Torchin and Mitchell,
2004). We suggest that a broader view of plant–animal interactions to include mutualists might provide a greater understanding for why some plants establish and become invasive while
others fail (see also Richardson et al., 2000; Mitchell et al.,
2006). We provide one of the first empirical examinations of
the role of pollination ecology for multiple pairs of related introduced and native species.
We suggest that future work examining the pollination ecology of native and introduced species should consider: (1) the
interactive effects of enemies (herbivores, florivores) and pollinators (e.g., Steets and Ashman, 2004). If introduced plants
receive less damage because of a release from enemies, then
they may have more resources to allocate to floral attraction,
allowing them to better attract resident pollinators. (2) Future
work should consider the pollination success of species that are
distantly related to the native community (phylogenetically
novel introduced species). Novelty may provide a pollination
advantage if the introduced plant possesses novel traits that pollinators prefer, such as greater nectar production or larger floral
displays. Alternatively, novel species may have novel traits that
the resident pollinators are unfamiliar with, resulting in fewer
pollinator visits or less accurate pollen transfer (see also Memmott
and Waser, 2002). (3) Future work should also consider pollen
quality and pollinator effectiveness. Because introduced plants
are not coevolved with the resident pollinators, the quality of
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Harmon-Threatt et al.—Pollination ecology of introduced plants
pollen arriving and the effectiveness by which it is deposited
may be lower per pollinator visit than that of native plant species (e.g., Armbruster, 2006). Future studies such as these
would help provide a more comprehensive understanding of the
role of pollination ecology and breeding system in introductions, which may be key in understanding and predicting current and future invasions.
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