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American Journal of Botany 96(8): 1544–1550. 2009.

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 ; M ü ller-Sch ä rer 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 fi tness in their in-troduced range relative to their native range (or relative to na-tive species in their introduced range) as a result of release from their natural enemies such as herbivores and pathogens. How-ever, when introduced species leave their native habitats, they are not only escaping enemies, which inhibit their fi tness, but they may also leave behind their natural mutualists (e.g., polli-nators), which can be vital to their reproduction and establish-ment. 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

can provide accurate pollen transfer in their new range. Under-standing 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 ab-sence of pollinators (autonomous self-fertilization), (2) attract resident pollinators, and (3) have suffi cient pollen transferred by pollinators to maximize seed set and prevent pollen limita-tion. 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 favor-able because a single individual is suffi cient 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 intro-duced woody species in South Africa and found that all of them were capable of self-pollination and 72% were capable of au-togamy (see also van Kleunen and Johnson, 2007 ; van Kleunen et al., 2008).

Although capacity for autonomous self-fertilization ( “ autog-amy ” throughout) could be benefi cial to introduced species colonizing new areas, autogamy is not necessary for successful introductions. Introduced plant species that are not autogamous need to be suffi ciently pollinated by resident pollinator species in their introduced range to successfully establish or their spe-cialist 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.,

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 identifi cation 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: aharmont@nature.berkeley.edu); present address: UC Berkeley, Dept of Environmental Science, Policy & Management,137 Mulford Hall #3114, Berkeley, CA 94720 USA

doi:10.3732/ajb.0800369

BREEDING SYSTEM AND POLLINATION ECOLOGY OF INTRODUCED PLANTS COMPARED TO THEIR NATIVE RELATIVES 1

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 quantifi es 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 signifi cant 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.

1545August 2009] Harmon-Threatt et al. — Pollination ecology of introduced plants

duced species were all introduced from Eurasia and were classifi ed 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 popu-lation sizes and fl oral densities.

Breeding system experiments — To determine whether introduced and na-tive species differed in their ability to autonomously self-fertilize, we conducted pollinator exclusion experiments. We determined the degree to which each spe-cies could reproduce in the absence of visits from animal pollinators because autogamy might be relevant for colonization success ( Baker, 1955 , 1974 ). Flowers (or infl orescences, 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 fl owers were paired with nearby fl owers 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 fl owers inside the bag differed among the species pairs in this study because fl ower size and the spatial clustering of fl owers within a plant differed among these pairs. For most species, we bagged and hand pollinated one fl ower. However, for some pairs, such as the Brassicaceae, a raceme of fl owers was bagged, but only one fl ower, which was marked on the pedicel, was included in the experiment. For the Asteraceae, the whole infl orescence was manipulated. Bags were large enough to give fl owers 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 fl ower, inadvertently pol-linating the fl ower(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 fl ower formed a fruit, and if a fruit formed, we counted the number of seeds per fl ower when possible. For species pairs for which we had data on number of seeds per fl ower, the degree of au-togamy is the ratio of the bagged to hand-pollinated seed set per fl ower. For species pairs for which we did not count seeds per fl ower (i.e., because of the diffi culty of accurately counting seeds for some species pairs), fruit set (number of fruits/number of fl owers) was used as a measure of autogamy. We chose to measure the ratio of bagged to hand-pollinated rather than bagged to open-pollinated so that we would not overestimate the degree of autogamy for spe-cies 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% confi dence intervals around each estimate of autogamy to determine whether each species exhibited signifi -cant (different from zero) autogamy.

Pollinator observations — To determine whether introduced and native spe-cies differed in pollinator visitation rates, we conducted observations of polli-nator visits to each species. Each species was observed at least fi ve 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 visi-tor was observed on the fl ower ’ s sexual organs. Observations were shifted to accommodate the blooming time of Potentilla recta , which only blooms in the afternoon, and Commelina and C onvolvulus 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 there-fore pollinator visitation rates might be underestimated for this species.

Often several fl owers on different plants were observed during a single ob-servation. In these cases, we pooled the visitation rate across these fl owers to get a single data point for visitation rate. We calculated visitation rate as the number of visits per fl ower per 20-min observation. Visitation rate was continu-ously distributed and was treated as a continuous variable. For each plant fam-ily, we used one-way ANOVA to determine whether native and introduced fl owers 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 supplementa-tion experiments to quantify pollen limitation for each species. Approximately 20 pairs of fl owering individuals (40 individuals total) of each species were marked with neutrally colored (brown or black) yarn and randomly divided into

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, how-ever, does not guarantee suffi cient quantity and quality of pol-len 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 breed-ing systems of introduced plant species will help identify the role of pollination in invasions; however, few pollen supple-mentation experiments testing for pollen limitation have been conducted on introduced species. Of over 1000 pollen supple-mentation experiments synthesized in a recent review, only 10 were of introduced plant species ( Knight et al., 2005 ), and thus, there was insuffi cient power to detect difference in the magni-tude 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 sig-nal 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, un-published data), and thus we might expect that it would be necessary to control for relatedness in breeding system com-parisons. This study is the fi rst experimental manipulation of the pollination ecology of multiple pairs of closely related in-troduced and native congeners (or confamilials if congeners were not available).

To assess the role of pollination ecology on the reproductive fi tness of introduced plants, we evaluated three possible factors affecting reproductive success: autogamy, attraction to pollina-tors, and pollen limitation. We expected that (1) breeding sys-tem would be conserved within a family (null hypothesis), but, when it was not, the introduced plant would have a higher de-gree of autonomous self-fertilization, (2) introduced species that were not autogamous would have similar pollinator visita-tion rates as their native relatives (because of similarity in fl oral traits across plants within a family), and (3) plants that are not autogamous and attract fewer pollinators would show signifi -cant pollen limitation. We found support for autogamy, high pollinator visitation, and signifi cant 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 fi eld 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 fi elds and open areas with plants.

We compared species pairs, all of which are biotically pollinated, from 10 plant families that occur at the fi eld 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 classifi cations as native or introduced were determined using USDA categorization ( USDA, 2007 ). Intro-

1546 American Journal of Botany [Vol. 96

and Liliaceae pairs failed to set any seed in the bagged treat-ment (i.e., no autogamy; Appendix S1). The Asteraceae species were both fully autogamous. The introduced Commelinaceae, Caryophyllaceae, Convolvulaceae, and Rosaceae had signifi -cantly higher fruit set when bagged than did their native relative ( F 1,25 = 11.68, P < 0.001; F 1,7 = 52.76, P < 0.001; F 1,22 = 44.11, P < 0.001; F 1,13 = 9.66, P < 0.01, respectively).

Pollinator visitation rates of introduced species did not differ signifi cantly from or were greater than their native species pair in eight of nine cases ( Fig. 2B ). In the Rosaceae pair, the intro-duced species had a signifi cantly higher visitation rate than its native counterpart ( F 1,8 = 20.9, P < 0.002). However, fl owers of the introduced Caprifoliaceae were visited less frequently by pollinators than flowers of the native species ( F 1,8 = 8.46, P < 0.02).

Three species (the introduced Fabaceae, the introduced Caprifo-liaceae, and the native Convolvulaceae) had signifi cant pollen limitation (i.e., different from zero) (Appendix S2, see Supplemen-tal 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 ± 0.206, while the na-tive had a pollen limitation magnitude of − 0.128 ± 0.163. The in-troduced Caprifoliaceae received signifi cantly fewer visits than its native congener and had signifi cantly higher pollen limitation ( Fig. 2B and 2C ). The native Convolvulus sepium was signifi cantly pollen limited, in spite of relatively high visitation rates ( Fig. 2B ). Pollen limitation differed between the native and introduced spe-cies in the Brassicaceae, Fabaceae, Convolvulaceae, and Caprifo-liaceae families ( F 1,35 = 5.608, P = 0.02, F 1,26 = 11.96, P = 0.001; F 1,18 = 5.652, P = 0.03; and F 1,62 = 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

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 fl ower chosen for the experiment was on a separate plant. The fl ower-level, as opposed to whole-plant-level, manipulation was chosen to maximize the amount of effort spent in quantifying pollen limitation for multiple pairs, maximizing the power to gen-eralize. Flower-level manipulations may result in overestimation of pollen limi-tation if plants reallocate resources to fl owers with supplemented pollen within a plant ( Knight et al., 2006 ).

We documented whether the fl ower 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 fl owers, we calculated the magnitude of pollen limitation as ln(number of seeds per fl ower in supplement treatment + 1) − ln(number of seeds per fl ower 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 signifi es pollen limita-tion. For each plant family, we used one-way ANOVA to determine if the na-tive and introduced species differed in their magnitude of pollen limitation. We also calculated 95% confi dence intervals around each estimate of pollen limita-tion to determine whether each species had signifi cant (different from zero) pollen limitation.

RESULTS

Breeding system was not signifi cantly different in six of 10 species pairs ( Fig. 2A ). Autogamy levels for fi ve of 10 intro-duced species and four of the 10 native species differed signifi -cantly from zero (Appendix S1, see Supplemental Data with online version of this article). The Fabaceae, Scrophulariaceae,

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 classifi ed as forbs by the USDA PLANTS Database (USDA, NRCS, 2007) except Lonicera japonica, L. fl ava , and Vicia villosa , which are vine, vine/shrub, and vine/forb, respectively. Introduced species were all introduced from Eurasia and classifi ed 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 con-ducted on the Asteraceae or Lilliaceae pairs. A hyphen (-) indicates no data were recorded for this species.

1547August 2009] Harmon-Threatt et al. — Pollination ecology of introduced plants

DISCUSSION

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 fi t-ness. We present the fi rst study to contrast autogamy, pollinator visitation, and pollen limitation of multiple pairs of related in-troduced 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 pollina-tors, (2) be able to attract resident pollinators, or (3) be signifi -cantly 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 au-togamous breeding system, some are able to successfully attract resident pollinations, and others manage to establish and spread despite signifi cant pollen limitation.

We expected that the degree of autonomous self-fertilization would be conserved for most species pairs, and when it dif-fered, the introduced species should have greater autogamy. The similar breeding system of most of our species pairs sug-gests that there is a strong signal of phylogeny on breeding sys-tem 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 signifi cantly in their degree of autogamy, and in three of these cases, the introduced species was more autogamous than its na-tive relative. Our results may indicate that autogamy is an im-portant 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 fl ora (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 establish-ment phase are necessary to conclude if Baker ’ s (1974) mecha-nism 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 signifi -cantly in their pollinator visitation rate. There were signifi cant differences in visitation rate for the Caprifoliaceae and Rosa-ceae pairs: the Caprifoliaceae had greater visitation for the na-tive species and the Rosaceae had lower pollinator visitation for the native species. It is unclear why the introduced Caprifoli-aceae, Lonicera japonica , which has a white fl ower that is simi-lar in size and morphology to its native congener, L. fl ava (a yellow-fl owered species), is less attractive to pollinators. We note that the native L. fl ava was primarily pollinated by carpen-ter 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

than the introduced Convolvulus . Note that in the case of Convol-vulus , 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.

Fig. 2. The degree of autogamy (ratio of reproductive success [seeds per fl ower or fruit set] in the bagged : pollen supplement treatment) (A), pollinator visitation rate (visits/fl ower/20 min) (B) and magnitude of pol-len limitation (ln [supplement reproductive success] – ln [control reproduc-tive success]) (C) for introduced and native species pairs. Introduced species and native species that differ for these response variables are indi-cated by *** P < 0.001, ** P < 0.01 and * P < 0.05.

1548 American Journal of Botany [Vol. 96

thus less likely to suffer from pollen limitation. Indeed, ecolo-gists choose to study native plants that have interesting pollina-tion 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 can-not 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 fi tness conse-quences 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 outcross-ing might be favored after establishment). Second, Allee ef-fects, a positive relationship between fi tness and either numbers or density of conspecifi cs ( Allee, 1931 , 1938 ; Stephens and Sutherland, 1999 ), may decrease the probability that an intro-duced species will establish and/or slow its spread (e.g., Å gren, 1996 , but see Davis et al., 2004 ; Cappuccino, 2004 ; van Kleunen and Johnson, 2005, 2007 ). Third, self-compatibility could also play a signifi cant role in the establishment of introduced spe-cies. Self-compatible species might be less restricted by propagule supply in the early stages of an introduction if geito-nogamy 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 spe-cies is often discussed in the context of the enemy release hy-pothesis (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 interac-tions to include mutualists might provide a greater understand-ing 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 fi rst empirical examinations of the role of pollination ecology for multiple pairs of related in-troduced and native species.

We suggest that future work examining the pollination ecol-ogy of native and introduced species should consider: (1) the interactive effects of enemies (herbivores, fl orivores) and pol-linators (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 fl oral 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 pol-linators prefer, such as greater nectar production or larger fl oral 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

other fl oral traits that pollinators are known to respond to, such as fl oral scent and nectar quantity and quality. In general, our results are consistent with observations in other studies that in-troduced plants can successfully attract resident generalist pol-linators (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 signifi -cant 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 signifi cantly 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 intro-duced 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 corre-sponded well with signifi cance, but in a few cases we did not detect signifi cant autogamy or pollen limitation in some species where the magnitudes of the effects were fairly high (e.g., Ver-bascum blattaria has pollen limitation of 1.23 but does not have statistically signifi cant pollen limitation) but power was low (online Appendix S2). Therefore, the lack of signifi cant autog-amy 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 Agricul-ture ( USDA, 2007 ). One possible reason for their success in spite of signifi cant 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 fl owers, so, while individual fl owers 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 fi x nitrogen and may be able to readily establish on disturbed, nitrogen-poor soils. Signifi cant 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 signifi cant 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 fl oral traits are often conserved in lin-eages, we may have preferentially chosen native species that are highly generalized in their pollination or autogamous and

1549August 2009] Harmon-Threatt et al. — Pollination ecology of introduced plants

Irwin , R. E. , A. K. Brody , and N. M. Waser . 2001 . The impact of fl oral larceny on individuals, populations, and communities. Oecologia 129 : 161 – 168 .

Keane , R. M. , and M. J. Crawley . 2002 . Exotic plant invasions and the en-emy release hypothesis. Trends in Ecology & Evolution 17 : 164 – 170 .

Kelly , C. K. , and F. I. Woodward . 1996 . Ecological correlates of plant range size: Taxonomies and phylogenies in the study of plant com-monness and rarity in Great Britain. Philosophical Transactions of the Royal Society of London, B, Biological Sciences 351 : 1261 – 1269 .

Knight , T. M. , J. A. Steets , and T.-L. Ashman . 2006 . A quantitative synthesis of pollen supplementation experiments highlights the con-tribution of resource reallocation to estimates of pollen limitation. American Journal of Botany 93 : 271 – 277 .

Knight , T. M. , J. A. Steets , J. C. Vamosi , S. J. Mazer , M. Burd , D. R. Campbell , M. R. Dudash , et al . 2005 . Pollen limitation of plant re-production: Pattern and process. Annual Review of Ecology Evolution and Systematics 36 : 467 – 497 .

Lambrinos , J. G. 2004 . How interactions between ecology and evolution infl uence contemporary invasion dynamics. Ecology 85 : 2061 – 2070 .

Martins , E. P. , and T. Garland . 1991 . Phylogenetic analyses of the corre-lated evolution of continuous characters: A simulation study. Evolution 45 : 534 – 557 .

Memmott , J. , and N. M. Waser . 2002 . Integration of alien plants into a native fl ower – pollinator visitation web. Proceedings of the Royal Society of London, B, Biological Sciences 269 : 2395 – 2399 .

Missouri Botanical Garden . 2007 . Missouri exotic pest plant list. Website http://www.mobot.org/mobot/research/mepp/ratings.shtml [accessed 15 November 2007] .

Mitchell , C. E. , A. A. Agrawal , J. D. Bever , G. S. Gilbert , R. A. Hufbauer , J. N. Klironomos , J. L. Maron , et al . 2006 . Biotic interactions and plant invasions. Ecology Letters 9 : 726 – 740 .

Mitchell , C. E. , and A. G. Power . 2003 . Release of invasive plants from fungal and viral pathogens. Nature 421 : 625 – 627 .

Morales , C. L. , and M. A. Aizen . 2006 . Invasive mutualisms and the structure of plant – pollinator interactions in the temperate forests of north-west Patagonia, Argentina. Journal of Ecology 94 : 171 – 180 .

Morgan , M. T. , and W. G. Wilson . 2005 . Self-fertilization and the escape from pollen limitation in variable pollination environments. Evolution 59 : 1143 – 1148 .

M ü ller-Sch ä rer , H. , U. Schaffner , and T. Steinger . 2004 . Evolution in invasive plants: Implications for biological control. Trends in Ecology & Evolution 19 : 417 – 422 .

Olesen , J. M. , L. I. Eskildsen , and S. Venkatasamy . 2002 . Invasion of pol-lination networks on oceanic islands: Importance of invader complexes and endemic super generalists. Diversity & Distributions 8 : 181 – 192 .

Pannell , J. R. , and S. C. H. Barrett . 1998 . Baker ’ s law revisitied: Reproductive assurance in a metapopultion. Evolution 52 : 657 – 668 .

Parker , I. M. 1997 . Pollinator limitation of Cytisus scoparius , an inva-sive exotic shrub. Ecology 78 : 1457 – 1470 .

Parker , I. M. 2000 . Invasion dynamics of Cytisus scoparius : A matrix model approach. Ecological Applications 10 : 726 – 743 .

Rambuda , T. D. , and S. D. Johnson . 2004 . Breeding systems of in-vasive alien plants in South Africa: Does Baker ’ s rule apply? Diversity & Distributions 10 : 409 – 416 .

Richardson , D. M. , N. Allsopp , C. M. D ’ antonio, S. J. Milton, and M. Rejmanek . 2000 . Plant invasions — The role of mutualisms. Biological Reviews of the Cambridge Philosophical Society 75 : 65 – 93 .

Richardson , S. C. 2004 . Benefi ts and costs of fl oral visitors to Chilopsis linearis : Pollen deposition and stigma closure. Oikos 107 : 363 – 375 .

Shea , K. , and P. Chesson . 2002 . Community ecology theory as a frame-work for biological invasions. Trends in Ecology & Evolution 17 : 170 – 176 .

Stebbins , G. L. 1957 . Self fertilization and population variability in higher plants. American Naturalist 91 : 337 – 354 .

Stebbins , G. L. , and R. Singh . 1950 . Artifi cial and natural hybrids in the Gramineae, tribe Hordeae. 4. Two triploid hybrids of Agropyron and Elymus . American Journal of Botany 37 : 388 – 393 .

Steets , J. A. , and T.-L. Ashman . 2004 . Herbivory alters the expression of a mixed-mating system. American Journal of Botany 91 : 1046 – 1051 .

pollen arriving and the effectiveness by which it is deposited may be lower per pollinator visit than that of native plant spe-cies (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 introduc-tions, which may be key in understanding and predicting cur-rent and future invasions.

LITERATURE CITED

Å gren , J. 1996 . Population size, pollinator limitation and seed set in the self-incompatible herb Lythrum salicaria. Ecology 77 : 1779 – 1790 .

Aizen , M. A. , and L. D. Harder . 2007 . Expanding the limits of the pollen-limitation concept: Effects of pollen quantity and quality. Ecology 88 : 271 – 281 .

Allee , W. C. 1931 . Animal aggregations: A study in general sociology. University of Chicago Press, Chicago, Illinois, USA.

Allee , W. C. 1938 . The social life of animals. William Heinemann, London, UK.

Alpert , P. , E. Bone , and C. Holzapfel . 2000 . Invasiveness, invasibility and the role of environmental stress in the spread of non-native plants. Perspectives in Plant Ecology, Evolution and Systematics 3 : 52 – 66 .

Armbruster , W. S. 2006 . Evolutionary and ecological perspectives on spe-cialization: From the arctic to the tropics. In N. Waser and J. Ollerton [eds.], Plant – pollinator interactions: From specialization to generaliza-tion, 260-282. University of Chicago Press, Chicago, Illinois, USA.

Baker , H. G. 1955 . Self compatability and establishment after long dis-tance dispersal. Evolution 9 : 347 – 349 .

Baker , H. G. 1974 . The evolution of weeds. Annual Review of Ecology and Systematics 5 : 1 – 24 .

Bjerknes , A. L. , Ø . Totland , and S. J. Hegland . 2007 . Do alien plant invasions really affect pollination success in native plant species? Biological Conservation 138 : 1 – 12 .

Brown , B. J. , R. J. Mitchell , and S. A. Graham . 2002 . Competition for pollination between an invasive species (purple loosestrife) and a na-tive congener. Ecology 83 : 2328 – 2336 .

Buchmann , S. L. , and G. P. Nabhan . 1996 . The forgotten pollinators. Island Press, Washington D.C., USA.

Burd , M. 1994 . Bateman principle and plant reproduction — The role of pollen limitation in fruit and seed set. Botanical Review 60 : 83 – 139 .

Cappuccino , N. 2004 . Allee effect in an invasive alien plant, pale swal-low-wort Vincetoxicum rossicum (Asclepiadaceae). Oikos 106 : 3 – 8 .

Colautti , R. I. , A. Ricciardi , I. A. Grigorovich , and H. J. Macisaac . 2004 . Is invasion success explained by the enemy release hypothesis? Ecology Letters 7 : 721 – 733 .

Daehler , C. C. 1998 . The taxonomic distribution o invasive angiosperm plants: Ecological insights and comparisons to agricultural weeds. Biological Conservation 84 : 167 – 180 .

Davis , H. G. , C. M. Taylor , J. C. Civille , and D. R. Strong . 2004 . An Allee effect at the front of a plant invasion: Spartina in a Pacifi c estu-ary. Journal of Ecology 92 : 321 – 327 .

Felsenstein , J. 1985 . Phylogenies and the comparative method. American Naturalist 125 : 1 – 15 .

Fishbein , M. , and D. L. Venable . 1996 . Diversity and temporal change in the effective pollinators of Asclepias tuberosa. Ecology 77 : 1061 – 1073 .

Goulson , D. 2003 . Effects of introduced bees on native ecosystems. Annual Review of Ecology Evolution and Systematics 34 : 1 – 26 .

Goulson , D. , and M. E. Hanley . 2004 . Distribution and forage use of ex-otic bumblebees in South Island, New Zealand. New Zealand Journal of Ecology 28 : 225 – 232 .

Harder , L. D. , and S. C. H. Barrett . 2006 . Ecology and evolution of fl owers. Oxford University Press, Oxford, UK.

Hedges , L. V. , J. Gurevitch , and P. S. Curtis . 1999 . The meta-analysis of response ratios in experimental ecology. Ecology 80 : 1150 – 1156 .

Hinz , H. L. , and M. Schwarzlaender . 2004 . Comparing invasive plants from their native and exotic range: What can we learn for bio-logical Control? Weed Technology 18 : 1533 – 1541 .

1550 American Journal of Botany

Stephens , P. A. , and W. J. Sutherland . 1999 . Consequences of the Allee effect for behaviour, ecology and conservation. Trends in Ecology & Evolution 14 : 401 – 405 .

Torchin , M. E. , and C. E. Mitchell . 2004 . Parasites, pathogens, and inva-sions by plants and animals. Frontiers in Ecology and the Environment 2 : 183 – 190 .

USDA, NRCS . 2007 . United States Department of Agriculture, The PLANTS database. Website http://plants.usda.gov . National Plant Data Center, Baton Rouge, Louisiana, USA [accessed 15 November 2007] .

van Kleunen , M. , and S. D. Johnson . 2005 . Testing for ecological and ge-netic Allee effects in the invasive shrub Senna didymobotrya (Fabaceae). American Journal of Botany 92 : 1124 – 1130 .

van Kleunen , M. , and S. D. Johnson . 2007 . Effects of self-compat-ibility on the distribution range of invasive European plants in North America. Conservation Biology 21 : 1537 – 1544 .

van Kleunen , M. , J. C. Manning , V. Pasqualetto , and S. D. Johnson . 2008 . Phylogenetically independent associations between autono-mous self-fertilization and plant invasiveness. American Naturalist 171 : 195 – 201 .

Waser , N. M. , L. Chittka , M. V. Price , N. M. Williams , and J. Ollerton . 1996 . Generalization in pollination systems, and why it matters. Ecology 77 : 1043 – 1060 .

Waser , N. M. , and J. Ollerton . 2006 . Plant – pollinator interactions: From specialization to generalization. University of Chicago Press, Chicago, Illinois, USA.