Do alien plant invasions really affect pollination success in native plant species?

B I O L O G I C A L C O N S E RVAT I O N

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available at www.sciencedirect.com

journal homepage: www.elsevier.com/locate/biocon

Review

Do alien plant invasions really affect pollination success in native plant species? Anne-Line Bjerknes*, Ørjan Totland, Stein Joar Hegland, Anders Nielsen ˚ s, Norway Norwegian University of Life Sciences, Department of Ecology and Natural Resource Management, P.O. Box 5003, N-1432 A

A R T I C L E I N F O

A B S T R A C T

Article history:

A growing number of studies on naturally occurring plant species have shown that plant-

Received 27 September 2006

plant interactions for pollination vary from competitive to facilitative. In reviewing the

Received in revised form

seven published studies on how alien species can affect the pollination success in natives,

21 March 2007

we found that all authors suggest competitive effects to dominate, either through reduced

Accepted 6 April 2007

pollinator visitation rates or through increased heterospecific pollination of native flowers.

Available online 31 May 2007

Although certain pollinator interactions were competitive, the reproductive output in the native species was not always reduced. This implies that natives are not pollen limited,

Keywords:

and/or that they compensate for the loss of pollinators by other animals. However, the

Competition

few studies on pollination interactions between alien and native plant species show differ-

Exotic plants

ing results. We therefore discuss other properties that can cause aliens to be strong inter-

Facilitation

actors for pollination, and can modify how alien species affect the reproductive success in

Invasive plants

natives. We also emphasize the spatial scales addressed in the reviewed studies, as alien

Pollinators

plant species may represent valuable food resources for many pollinators. Such plant species tend to be interpreted as competitive plants for pollination, whereas we stress their facilitative ability that may occur on a landscape scale by increasing pollinator densities. Additionally, while most studies tend to work within a shorter temporal scale, the impacts of the alien plant introductions may differ depending on the year or seasonal time leading to the differing results reported. Ó 2007 Elsevier Ltd. All rights reserved.

Contents 1. 2.

3. 4. 5.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Alien species may influence the pollination of natives through effects on pollinators . . . . . . . . . 2.1. Effects on pollinator populations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2. Effects on pollinator behavior . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Studies on pollination interactions between alien and native species . . . . . . . . . . . . . . . . . . . . . . Which properties make aliens strong interactors for pollination? . . . . . . . . . . . . . . . . . . . . . . . . . Which properties make the pollination of natives susceptible to alien invasion? . . . . . . . . . . . . .

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* Corresponding author: Tel.: +47 64 96 53 47; fax: +47 64 96 58 01. E-mail addresses: [email protected] (A.-L. Bjerknes), [email protected] (Ø. Totland), [email protected] (S.J. Hegland), [email protected] (A. Nielsen). 0006-3207/$ - see front matter Ó 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.biocon.2007.04.015

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6. 7. 8.

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Impacts of network structure on alien invasion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Evolution of floral traits in native plants, a consequence of pollination interactions with Knowledge gaps and research priorities . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

Introduction

Invasions of alien plant species (plants that have escaped their native range due to unintentional or intentional human involvement, or without help of people (Pysek et al., 2004)) into various habitats are considered a global threat to biodiversity and ecosystem functioning (Mack et al., 2000; Pimentel et al., 2001; Gurevitch and Padilla, 2004), and have attracted considerable attention. Although most alien species are not successful in colonizing new areas, some manage to reproduce and persist in these habitats at high population densities (invasive species). Given the great attention alien plants have received from ecologists, few studies have focused on how aliens may affect an essential part of the life-cycle of most native flowering plant species, namely, their pollination, and subsequent reproductive success. Many flowering plant species are either facultative or obligatorily dependent on interactions with animal pollinators for seed production (Burd, 1994). Alien species invading native habitats may disrupt these interactions. For example, by attracting pollinators previously monopolized by the native flora, alien plants reduced the pollinator service received by native plants (competitive effects) (Chittka and Schu¨rkens, 2001; Brown et al., 2002). For most flowering plants, sufficient pollen availability through animal pollination is an essential process for the long-term persistence of populations because it affects seed production and genetic variability (Stanton et al., 1986; Burd, 1994; Corbet, 1998; Larson and Barrett, 2000; Ashman et al., 2004). Thus, any reduction in pollinator visitation rates, or change in pollinator type or behavior, caused by alien invasion can affect the seed production of native species and potentially their population dynamics through impacts on conspecific pollen transfer. Most reviews on threats to plant–pollinator interactions have focused on agricultural practices such as fragmentation, grazing, pesticides, herbicides and introductions of non-native pollinators (Kearns and Inouye, 1997; Kearns et al., 1998; Spira, 2001). However, two recent reviews (Richardson et al., 2000; Traveset and Richardson, 2006) have included plant–pollinator interactions in relation to introductions of alien plants and their effects on native plants more thoroughly. Richardson et al. (2000) suggested that parts of the limitation on the spread of aliens are caused by a lack of suitable pollinators. Later, Traveset and Richardson (2006) confirmed these suggestions by reviewing studies that have found that alien plants become invasive by competing for pollinators and through hybridization processes. The main objective of this paper is to illustrate how alien plants may directly affect the pollination of natives by reviewing the recent experimental and observational studies. Based on the spatial scale used in these studies, we discuss whether or not the effects of alien invasions may be competitive, neutral, and facilitative or a combination of these effects. We also

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discuss the properties that make the aliens strong interactors for pollination and natives susceptible to alien invasion, and how pollination interactions with alien plants possibly cause evolutionary changes in floral traits of native species. Finally, we suggest new research scopes to better understand alien impacts on the pollination of native plant species.

2. Alien species may influence the pollination of natives through effects on pollinators Alien plant populations that alleviate resource limitations on pollinators (nectar, pollen, brood sites, etc.) (e.g., Chittka and Schu¨rkens, 2001; Shapiro, 2002; Graves and Shapiro, 2003) and share pollinators with native plants possibly influence the native plant–pollinator interaction in two ways, through effects on pollinator populations and through pollinator behavior.

2.1.

Effects on pollinator populations

Just as highly rewarding flowering crops can have strong positive effects on bumblebee densities (Westphal et al., 2003), and alien plant species may increase the geographic range of pollinators and duration of their flight season (Graves and Shapiro, 2003), it is possible that alien plant species, on a large scale (i.e., landscape), increase pollinator population size by increasing their resource availability. In turn, increased population sizes of pollinators can sustain or increase native plant population sizes through increased flower visitation. Setting aside many documented negative effects that aliens have on the population persistence of natives through vegetative interactions (Gurevitch and Padilla, 2004), aliens could mitigate the current worldwide decrease in population densities of wild pollinators by providing more floral resources to flower visitors (Graves and Shapiro, 2003; Williams et al., 2006). As shown for native species (e.g., Waser and Real, 1979), positive effects of alien invasions may also occur when aliens have different seasonal flowering times than natives, and indirectly act as facilitators by maintaining larger pollinator populations throughout the flowering season. For example, highly rewarding alien species flowering early in the season promote pollinator population growth later in the season, resulting in higher pollinator densities available for flowering native species. Similarly, a highly rewarding alien species flowering late in the season increase the number of pollinators emerging early in the following season. Such resourceeffects may indirectly be important for native plants by maintaining pollinator densities at high levels. To our knowledge, no study has examined whether alien invaders have positive effects on local pollinator population densities, or whether such effects secondarily affect the pollination and reproduction of native species. Some studies have suggested that alien plants have indirect negative impacts on pollinator populations, as they

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may reduce native plant population density and plant diversity on which pollinator populations rely exclusively. Especially on islands, Cox and Elmqvist (2000) showed that alien plant invasions have reduced native plant richness, and subsequently pollinator diversity and pollinator population size, possibly due to reduced resource availability for pollinators. Alien species can also have a direct negative effect on pollinator populations. Graves and Shapiro (2003) found that at least three California butterfly species, acting as pollinators for native plant species, currently lay eggs on introduced taxa that are toxic to the larvae. Currently, our knowledge is limited by how and to what extent alien invasions affect the population density of pollinator species, and less is known about how it affects the species and functional composition of pollinator communities at different spatial and temporal scales.

2.2.

Effects on pollinator behavior

While few studies have examined how alien invasions affect pollinator population densities, impacts on pollinator behavior have received more attention. These studies have been conducted on small spatial scales, focusing on a single plant community, and have emphasized how the presence of an alien affects pollination in natives through impacts on pollinator behavior (e.g., Chittka and Schu¨rkens, 2001; Brown et al., 2002; Aigner, 2004; Totland et al., 2006). On such small spatial scales, the presence of alien plant species may directly affect the pollination of natives in two ways (Fig. 1).

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First the total resource availability may attract more pollinators, also increasing the visitation to the natives, which subsequently also may increase pollen deposition and seed set (facilitation) (Moragues and Traveset, 2005; see also Thomson, 1978; Brown and Kodric-Brown, 1979; Campbell and Motten, 1985 for studies on native species). Second, the pollinators may prefer the aliens over the natives, and the aliens may function as competitors for pollinator service by decreasing conspecific pollen deposition through reduced visitation rate or through increased heterospecific pollen deposition, with a subsequent potential reduction in seed set (Grabas and Laverty, 1999; Chittka and Schu¨rkens, 2001; Brown et al., 2002). If plant species do not share pollinators, they will not compete for pollinator attraction or through heterospecific pollination. However, this is unlikely because pollinator sharing is common within plant communities (Waser et al., 1996; Richardson et al., 2000). Competition for pollination may also occur as an indirect effect of competition for other resources (Fig. 1), such as space, light, and soil nutrients, where many invasive alien plants are known to be superior (Davis et al., 2000). In such cases, reduced resource allocation to flowers in the natives, may reduce their attractiveness and lead to reduced pollinator visitation (also a consequence of direct competition for pollination) but not to increased heterospecific pollen deposition (Burd, 1994). Even if alien plant species interact with natives for pollinators, they may not affect the reproductive success of the

Pollination effects in native plants when alien is present

Direct pollination effects

No pollinator sharing

Pollinator sharing

No pollination effect

Pollinator visitation

Facilitation

Increased visitation rate

Decrease of heterospecific pollen cause increased seed prod.

Indirect pollination effects Vegetative effects cause competition for other resources than pollinators

Increase of conspecific pollen cause increased seed prod.

Neutral No pollination effect

No change of heterospecific pollen Seed production remains the same

Increase of heterospecific pollen cause reduced seed prod.

No change of conspecific pollen Seed production remains the same

Competition

Reduced visitation rate

Decrease of conspecific pollen cause reduced seed prod.

Fig. 1 – Changes in pollinator behavior (visitation rate and quality of visits) and direct pollination effects in native plants caused by alien plant introductions on a local scale. Positive effects are in boxes with full borders, negative effects are in boxes with dashed borders.

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natives. First, the changed visitation rate in natives after an alien invasion may be so small that the effect in seed set might be negligible (Fig. 1). Second, if the main pollinator of the native species switches to alien flowers, other pollinator species may start to visit the native plant and, thus, compensate for the reduced pollination by the original pollinator species (Ghazoul, 2004). Finally, other factors, such as nutrient availability may constrain seed production to such an extent that any change in the visitation to native plants due to alien invasion, may not affect the seed set in the native plants (Ashman et al., 2004). While vegetative interactions occur in the immediate vicinity of the alien plants, interactions for pollination may occur outside the local distribution area of the alien, because

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mobile pollinators mediate such interactions. Hence, alien plant species may affect reproductive success in native plants that are spatially and temporally separated from them. We know of no study addressing whether aliens also affect the pollination and reproductive success of native plant individuals that are situated at a distance from the aliens, although Larson et al. (2006) have shown that alien pollen occasionally was transported at least 100 m.

3. Studies on pollination interactions between alien and native species Although interspecific interactions for pollination among native plant species are extensively studied, our literature

Table 1 – Alien plants and their effect on fitness in native plant species, through alterations in pollination Native species

Eupatorium maculatum Eupatorium perfoliatum Impatiens capensis Stachys palustris

Alien species

Lythrum salicaria

Type of study

Introducing and translocating alien Lythrum salicaria Introducing and translocating alien Lythrum salicaria Introducing and translocating alien Impatiens glandulifera Introducing alien Observations in pure vs. mixed stands Lythrum alatum Lythrum salicaria Introducing alien Dithyrea Cakile maritima Removing alien maritima Dithyrea Carpobrotus ssp. Removing alien maritima Cistus Carpobrotus spp. Observations in pure monspeliensis vs. mixed stands Cistus Carpobrotus spp. Observations in pure salviifolius vs. mixed stands Anthyllis Carpobrotus spp. Observations in pure cytisoides vs. mixed stands Lotus cytisoides Carpobrotus spp. Observations in pure vs. mixed stands Melampyrum Phacelia tanacetifolia Introducing alien pratense Campanula Euphorbia esula Observations in rotundifolia infested and noninfested plots Linum lewisii Euphorbia esula Observations in ssp. lewisii infested and noninfested plots Oxytropis Euphorbia esula Observations in lambertii ssp. infested and nonlambertii infested plots

Fitness related effects in native

References

Visitation rate

Seed (s) and/or Alien (a) or native (n) fruit (f) set pollen deposition

Increased

Reduced (s)

No effect

Reduceda

No effect Reduced

No effect (s) Reduced (f) Reduced (s)

Reduced No effect

Reduced (s) No effectb

Brown et al. (2002) Aigner (2004)

No effect

No effectb

Aigner (2004)

No effect

No effect (s)

Increased

No effect (s)

Moragues and Traveset (2005) Moragues and Traveset (2005) Moragues and Traveset (2005) Moragues and Traveset (2005) Totland et al. (2006) Larson et al. (2006)

Increased (a)

Increased Reduced Reduced

No effect (s)

Increased, 2000 Reduced, 2001

Grabas and Laverty (1999) Grabas and Laverty (1999) Grabas and Laverty (1999) Chittka and Schu¨rkens (2001)

No effect, 2000 Reduced, 2001d

Reduced (n)c

Larson et al. (2006)

No effect

Reduced (n)c

Larson et al. (2006)

Effects and comparisons are extracted from the seven studies found addressing questions on how alien plant species directly might affect the pollination of natives. Fitness related effects in natives are summarized as either visitation rate, seed and/or fruit set, or alien or native pollen deposition. a Seed production. b Fruit production. c Larson et al. (2006) found significantly increased conspecific pollen in non-infested plots. This indicates that it is less conspecific pollen in infested plots. d Larson et al. (2006) found significantly increased visitation rates in Linum lewisii ssp. lewisii, in non-infested plots, 2001. This indicates a reduced visitation rate in infested plots compared to non-infested plots.

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review revealed only five experimental studies that have assessed how alien species influence pollination and/or subsequently reproductive success in native species (Table 1). In these five studies, four found either reduced visitation rates or reduced seed production due to the presence of an alien plant species, while one did not find any effect. In addition, we found three observational studies on pollination interactions between native and alien species (Table 1). Although such observational studies cannot detect causal effects of alien invasion on the pollination and reproduction of natives, they provide important information on the possible outcomes of such interactions. Chittka and Schu¨rkens (2001) found, through observations and experiments that the invasive alien Impatiens glandulifera significantly affected both pollinator visitation and subsequent seed set of the native Stachys palustris. The large and showy flowers of I. glandulifera are highly attractive to important bumblebee pollinators of S. palustris, and because the alien produced much more nectar and had more showy flowers than the native, pollinators were drawn away from S. palustris. Thus, the presence of the alien plant species caused a reduction in visitation rates and subsequent seed set in the native species. Brown et al. (2002) obtained similar results when they experimentally manipulated the presence of the alien plant Lythrum salicaria that occur together with the native Lythrum alatum. Seed set in L. alatum decreased when it occurred together with the alien species. As in the Impatiens–Stachys interaction, the alien L. salicaria had larger and more numerous flowers, and greater nectar and pollen rewards, than the native L. alatum. Visitation rate of L. alatum was reduced by 14–54% when it co-occurred with L. salicaria. In addition, interspecific movements between flowers of the two species constituted a large part (33–65%) of the total number of movements between flowers, suggesting a reduction in visitation quality, due to heterospecific pollination and pollen wastage, in addition to the reduced visitation quantity, caused a decrease in seed set when the alien was present. Grabas and Laverty (1999) investigated density effects when studying how different densities of the alien L. salicaria affected the pollination and reproduction of native co-flowering, Eupatorium maculatum, Eupatorium perfoliatum, Impatiens capensis. When the alien was present they found increased visitation rate to E. maculatum, and more than 58% increase in the amount of L. salicaria pollen on E. macultaum stigmas. Furthermore they found a 19% reduction in seed production in E. perfoliatum in medium-density plots. Moreover, fruit set in I. capensis decreased by 30% in high-density plots of L. salicaria at one site. Hence, studies of both Brown et al. (2002) and Grabas and Laverty (1999) indicate that L. salicaria negatively affect the reproductive success of native species. Totland et al. (2006) experimentally introduced Phacelia tanacetifolia in old and young forest sites where the native Melampyrum pratense naturally occurred. During periods with bee activity, the alien had a strong negative effect on the visitation rate by bumblebees to the native species, although the presence of the alien species increased the number of bees entering the study plots. Despite reduced visitation due to alien presence, the seed production of the native was unaffected.

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Aigner (2004) removed two alien species (Cakile maritima and Carpobrotus spp.) from plots where the native species Dithyrea maritima occurred. This treatment increased total visitation rate in the native plants, on average, by 2.18 times, although the effect was not statistically significant. Although these data suggest a negative effect of the alien presence on pollinator visitation in the native, the alien removal treatment did not affect fruit production in the native species. In an observational study in Mallorca, Moragues and Traveset (2005) investigated the effects of the alien Carpobrotus spp. on the native species Cistus monspeliensis, Cistus salviifolius, Anthyllis cytisoides and Lotus cytisoides. They measured flower visitation rates in the native species, the presence of alien pollen on the stigmas of native flowers, and also the effect of heterospecific pollination (experimentally) on native seed set (growing in pure- and mixed stands with the alien Carpobrotus spp.). They detected competition for pollinator visitation only in L. cytisoides, a facilitative effect in C. salvifolius and A. cytisoides, and no effect in C. monspeliensis. These effects were not consistent over time. Moreover, the presence of Carpobrotus pollen on stigmas was almost negligible, and supplemental pollination experiments showed that alien pollen did not interfere significantly with native pollen, and, thus, did not affect seed set in the natives. Their results indicate that the alien Carpobrotus influence visitation rates in native species positively, negatively, or not at all. Since the impacts of the alien differed between years, it is possible that the influence of alien on natives depends upon ecological circumstances, such as pollinator abundance, or flower abundance of other native species. Larson et al. (2006) examined, in an observational study, how the alien Euphorbia esula may affect pollination in several native species. Visitation rates in two native species (Campanula rotundifolia and Linum lewisii ssp. lewisii) were higher in non-invaded than in invaded sites, whereas visitation to the native Oxytropis lambertii ssp. lambertii was unaffected by alien presence. Overall, 65 of the 653 native flowers examined had Euphorbia pollen on their stigmas; and 13 of these were collected in non-invaded sites. The presence of Euphorbia pollen in non-invaded sites implied that pollinators transported it more than 100 m, indicating that alien plants may negatively affect reproduction in native plants growing outside invaded sites. We examined the above studies in more detail, separating the effects of each alien species on each native species for each of the studies and separating the effects per year when possible. Of these, 5 out of 22 (22%) found reduced visitation rates, 7 out of 22 (32%) found increased visitation rates, and 10 out of 22 (46%) found no effect in visitation rates. For seed/fruit set, 4 out of 10 (40%) found reduced seed/fruit set while 0 out of 10 (0%) found increased seed/fruit set, and 6 out of 10 (60%) found no effect. In 12 out of 17 (71%) cases, alien pollen grains were found on native stigmas, though in highly variable quantities. Studying the visitation rates, the most prevalent outcome is the absence of effect, however, as none of the studies found increased reproduction (seedand/or fruit set), competitive effects are more prevalent than facilitative effects. In studies that only involve native species, all types of interspecific interactions for pollination, both in visitation and reproduction, have been found (competitive,

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facilitative and neutral) (see, e.g., Waser, 1978; Feinsinger and Tiebout, 1991; Laverty, 1992; Fishman and Wyatt, 1999; Caruso, 2000; Moeller, 2004; Larson et al., 2006). Thus, it is possible that interactions between aliens and natives differ ecologically from those between natives, due to unique properties of the alien species that make them strong interactors for pollination with native species. On the other hand, little is known about how much visitation frequency in natives must change to result in detectable effects on their reproduction, or how many heterospecific pollen grains a stigma should receive before it affects the performance of the conspecific pollen. There are indications that this will be both species- and site specific (e.g., Grabas and Laverty, 1999). Since the number of studies on interactions between natives is greater than the number of studies involving alien species, the potential for observing more types of interactions is greater. It also seems likely that researchers are drawn to the obvious. They are more likely to investigate something that looks like it will have a large effect, and with the alien plants, there is likely a subconscious bias to look for negative effects. Thus, studies so far have involved highly invasive species that form dense infestations, the most likely to harbor negative effects for native species. Grabas and Laverty (1999) and Moragues and Traveset (2005) used a large spatial scale in their studies, where sites were separated by several kilometers. By focusing on within site comparisons, these authors were in fact doing effect comparisons on a small scale, like the other studies (Chittka and Schu¨rkens, 2001; Brown et al., 2002; Aigner, 2004; Larson et al., 2006; Totland et al., 2006). In reviewing the studies, the distance between the sites where alien and native plants were together and sites only containing native plants varied among the studies, from about 1 m to 500 m. All these studies examined insect pollination (mainly by honeybees, bumblebees and flies). The size of large-scale studies will depend on the taxa of the pollinators. However, as an example of a wellstudied taxon, honeybees rarely forage within 500 m (Seeley, 1985), and they may exploit forage sources lying within an area of 100 km2 (Waddington et al., 1994). The studies compared sites within communities, and effects measured on pollinator behavior rather than pollinator population dynamics. However, as it is also conceivable that alien invasions have facilitative and/or competitive effects by affecting pollinator population sizes through effects on floral resource availability of both alien and native plants. Comparisons should also be done on a larger spatial scale, comparing invaded and noninvaded sites between different plant populations and/or landscapes. Although most studies suggested that competition for pollinator service prevailed between aliens and natives, there is a possibility that facilitation is revealed when invaded and non-invaded native populations of different population sizes are compared, including those alien–native species pairs hitherto studied. As frequently suggested in ecological studies, the temporal scale is often too short (e.g., Roubik, 2001; Price et al., 2005). All the above studies observed alien effects on pollination on natives in the peak flowering time of their study species or even a shorter timeline. In many places, pollen reception in flowers may vary greatly due to strong seasonal shifts in the composition of the pollinator assemblages and

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floral resources (Ashman and Stanton, 1991), and may not be detected if plant–pollinator interactions only are studied in a limited time period. All studies included observations from two successive years, except Chittka and Schu¨rkens (2001) and Totland et al. (2006) who researched only one year. The year-to-year variation in the effects of alien invasion revealed in these studies, suggest that larger temporal scales (several years) are needed to see if there are any effects of alien invasion on the pollination of native species.

4. Which properties make aliens strong interactors for pollination? Alien plant species may have unique properties that make them strong interactors for pollination in competition with native plant species: 1. Flower attractiveness. Many alien plants are primarily introduced as crops or ornamentals. Such plants, particularly the ornamentals, often have a sweet scent and showy flowers, features that make them highly attractive to pollinators. When interacting for pollination with such species, natives potentially suffer through competition for pollinator visitation due to lower attractiveness (Chittka and Schu¨rkens, 2001; Brown et al., 2002). 2. Flower morphology. Memmott and Waser (2002) found that alien plants with a taxonomic affinity to natives performed best as invaders into plant–pollinator networks, presumably because their similarity in floral morphologies with the natives enabled them to conquer their pollinators. In such cases, it is conceivable that aliens with similar morphologies as the natives, and/or that are more attractive than the natives have a competitive advantage in pollinator attraction. 3. Population size and density. Alien species may occur, as invasive plants, in denser and larger populations than many native species, presumably because they have escaped their natural enemies, such as herbivores and parasites (Keane and Crawley, 2002; Wolfe, 2002), or because of their life-history (producing large number of offspring, dispersing over great distances) (Meiners et al., 2002). Pollinators ˚ gren, are often attracted to such dense populations (A 1996; Mustajarvi et al., 2001; Thompson, 2001), and in many cases dense and/or large populations/communities have been found to increase visitation rates, reproductive success, and plant fitness (Kunin, 1997; Jacquemyn et al., 2002; Johnson et al., 2003). Visitation frequency and heterospecific pollen deposition in natives may not necessarily depend on the presence of the alien plant, but also its population size and/or density. Many studies on competition between plant species via pollination have not found significant reductions in plant fitness, even when visitation frequencies have significantly declined, or heterospecific pollen deposition significantly increased (e.g., Caruso, 1999, 2002; Totland et al., 2006). This implies there is no pollen limitation in these systems, but it is also conceivable that the relation between the population size and/or density between the alien and native plant species is too small. Studies of both population-density and -size show

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higher reproductive success in large and dense populations (e.g., Feinsinger et al., 1986; Feinsinger and Tiebout, ˚ gren, 1991; Menges, 1991; Aizen and Feinsinger, 1994; A 1996; Kunin, 1997; Bosch and Waser, 2001; but see Campbell and Motten, 1985; Sowig, 1989; Klinkhamer and de Jong, 1990). Hence, the ability of alien species to establish large populations may be an indirect competitive advantage when interacting for pollinator attraction with native species. 4. Generalization/specialization. It has been suggested that alien plants with a generalized pollination strategy (plants attracting many visitor species) more easily invade existing plant–pollinator networks than pollination specialists (plants attracting one or a few visitor species) (Johnson and Steiner, 2000; Richardson et al., 2000, but see Morales and Aizen, 2002; Va´zquez, 2005). Some studies suggested that alien plants established a lower number of interactions with flower visitors than native plants (Memmott and Waser, 2002; Olesen et al., 2002). While most studies only included the effect of alien plants that occur at a high population density, Memmott and Waser (2002) also studied alien plant species with a low population density. Such alien species do not have this high-density advantage in the attraction of pollinators and may interact with fewer pollinator species. Nevertheless, pollination-generalists alien species are more likely to alter pollinator interactions of more native plant species than a specialist that attract fewer pollinator species (Memmott and Waser, 2002; Rejmanek et al., 2005). For example, Memmott and Waser (2002) found that pollination-generalist alien plant species were most frequently visited by pollinator generalists, and that their visitors also visited a much broader floral spectrum than pollinators that only visited native plants. This might exert competitive effects on native plants by increasing heterospecific pollination and/or reducing pollinator visitation to the native plants. On the other hand, increased floral resources may have facilitative effects on native plant species, through increased pollinator population sizes resulting in increased visitation rates to native plant species.

5. Which properties make the pollination of natives susceptible to alien invasion? Several properties of the native species may affect how pollination and reproductive success of native species are influenced by alien invasion: 1. Pollinator dependence. Plant species whose seed production is highly dependent on cross-pollination are more likely to be affected by reduced pollinator visitation (Wilcock and Neiland, 2002), positively or negatively, by alien invasion than plant species with autogamous pollination. Nevertheless, seed production in highly autogamous species may still be negatively affected by heterospecifc pollination and reduced pollinator interactions (Brown and Mitchell, 2001; Bell et al., 2005). Based on the reviewed studies (Table 1), we were not able to draw the conclusion that highly pollinator dependent species are the ones that endure in the presence of aliens. In four of seven studies,

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the pollinator dependence was not reported (Grabas and Laverty, 1999; Chittka and Schu¨rkens, 2001; Aigner, 2004 , Larson et al., 2006). The remaining three studies (Brown et al., 2002; Moragues and Traveset, 2005; Totland et al., 2006) and other studies (Kwak and Jennersten, 1991; Kearns and Inouye, 1994; Bingham and Ranker, 2000; Huber et al., 2004) suggest that eight of the 14 present native species are self-compatible. The last six species remain unknown (E. maculatum, E. perfoliatum, S. palustris, L. alatum, Dithyrea maririma, and Oxytropis lambertii ssp. lambertii). Of the eight self-compatible species, only four reported seed/fruit set/production (I. capensis, C. monspeliensis, C. salviifolius, and M. pratense). I. capensis was the most self-compatible of these species, although this was the only species of these four that experienced a reduced fruit set. Hence, due to lack of self-incompatible species included in the studies, we are not able to conclude whether or not pollinator dependence may buffer the effect alien plants may have upon the reproductive success in the natives. 2. Pollinator specialization. Among plants that are either facultatively or obligatorily dependent on pollinators for reproduction, the degree of pollination specialization may determine the response of plant reproduction to altered pollination service, e.g., due to disturbance (e.g., introduction of alien plant species) (Aizen and Feinsinger, 1994; Aizen et al., 2002). If an alien plant species is able to monopolize few or many pollinator species, specialist plants are expected to be more vulnerable than generalist plants because any decrease in abundance, or loss of single pollinator species, could lead to reproductive failure (Bond, 1994; Waser et al., 1996; Aizen et al., 2002). The generalist plants are on the other hand, better able to compensate for the loss of one pollinator species, because it is more unlikely that the alien plants monopolize its entire pollinator assemblage (Ghazoul, 2004). In the reviewed studies, reproductive success was measured in nine of the 14 generalist species, where five species did not experience any reproductive effect, as we would have predicted for a generalist plant. On the other hand, four species experienced reduced seed/fruit set/production, which is what we would expect for a specialist plant. Because the seven reviewed studies only included generalist species, we were not able to compare specialist and generalist plants, or to conclude whether generalization is an advantage for natives with alien presence. 3. Flower morphology. Native plant species that deposit pollen on the same place on pollinator bodies as aliens are more likely to experience competitive effects due to heterospecific pollination (sensu Waser and Price, 1983) than native species with different pollen placement. Pollen deposition on the flower visitors was not described in the reviewed studies, but visual inspections suggest heterospecific pollination to occur in all the species combinations reported. Only three alien–native combinations were studied for heterospecific pollen depositions (Grabas and Laverty, 1999; Larson et al., 2006), and alien pollen was more abundant on native stigmas in the presence of aliens. Reproductive success was however measured

8

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in only one of these species (E. maculatum), which experienced reduced seed set in the presence of the alien (Lythrum slaicaria). 4. Population size and structure. The outcome of interactions for pollination among native and alien species may depend on their population sizes (e.g., Menges, 1991; Cunningham, 2000). Fragmentation of natural habitats affect population sizes of plants and animals, and thereby their biotic interactions, including pollination (e.g., Kearns et al., 1998; Mustajarvi et al., 2001; Schulke and Waser, 2001; Steffan-Dewenter et al., 2001). For example, Aizen and Feinsinger (1994) compared pollination levels, and reproductive outputs of populations in several plant species in different-sized fragments and continuous forest. Even though the responses to fragmentation varied among species, they found a 20% decrease in pollination levels and seed output from continuous forest to fragments (see also Murren, 2002). The more fragmented a landscape is, the easier it seems to be invaded by alien plants (Kemper et al., 1999). Hence, the invasive ability of many alien plant species, and the population decline of many native plant species in heterogeneous landscapes may accelerate the effects that the alien plants may have upon the pollination of natives. Some of the reviewed studies did not report population size or structure, while others reported limited information and we are unable to extract relevant data to extrapolate the alien effects as a function of the population size and structure.

6. Impacts of network structure on alien invasion Previously, specialist plant species were considered to be more vulnerable than generalists to disturbance (e.g., the introduction of alien plants competing for pollinators) because any decrease in abundance of a single pollinator species could lead to reproductive failure (Bond, 1994; Waser et al., 1996; Aizen et al., 2002). This hypothesis assumes that specializations in plant–pollinator interactions are symmetric (i.e., that generalist plants are pollinated by generalist pollinators while specialist plants are pollinated by specialist pollinators). However, above studies addressing these questions have found no relationship between the degree of pollination specialization and the plant species’ reproductive response to disturbance (Aizen et al., 2002; Va´zquez and Simberloff, 2002). The explanation to this might be the documented asymmetry in the degree of specialization among plants and their pollinators, seen in the nested structure of plant–pollinator networks (Bascompte et al., 2003; Ashworth et al., 2004; Jordano et al., 2006). A nested network consists of a core group of generalists interacting with each other, and with extreme specialists interacting only with the generalists (Bascompte et al., 2003). It is suggested that alien plants invading new regions are more likely to establish and spread if they have a generalized pollination strategy (Johnson and Steiner, 2000; Richardson et al., 2000). The nested structure of the plant– pollinator network then propose that the alien species would interact mainly with generalist pollinators already distribut-

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ing their flower visits among numerous plant species or specialist pollinators previously specializing on a generalist plant species. This implicates that as long as the alien species is not able to monopolize a high number of pollinator species, the negative effect on the pollination of the native plant community would be buffered by the plant–pollinator network structure. If the alien plant species is a pollination specialist, attracting only a few pollinator species, these pollinators will, in most cases, be generalists giving the same buffering effect as the generalist plant. By including the number of visits conducted by each pollinator species and received by each plant species Bascompte et al. (2006) showed that also the quantitative asymmetry in the relationships among plant and animal species make the network more resistant to perturbations (e.g., the introduction of an invasive plant species). In summary, generalist alien plant species only compete for pollination with native plant species if they monopolize many pollinator species or if they monopolize specialist pollinators that are pollinating specialist plants. Both outcomes are unlikely as most networks are asymmetric.

7. Evolution of floral traits in native plants, a consequence of pollination interactions with alien plants If alien invasions affect pollinator attraction to natives, and subsequently female and male reproductive success in natives, it can influence how natural selection operates on floral traits in natives, and thereby affecting the floral traits important for pollination in the native species. Most research has focused on how alien species evolve after their invasions to new habitats (Ellstrand and Schierenbeck, 2000; Lee, 2002; Hurka et al., 2003; Allendorf and Lundquist, 2003; Parker et al., 2003), but recently evolutionary responses to alien invasions in native plants have been studied (Mealor et al., 2004; Callaway et al., 2005; Lau, 2006). However, none of these studies focus on pollination-related floral traits in native species. Floral trait variation within a population has been attributed to spatial variation in resource availability, and is not necessarily genetically based (Sanchez-Lafuente, 2002). However, if these traits are heritable (Schemske and Bradshaw, 1999), and pollinator floral preference in native species is affected by the presence of alien species, floral trait evolution in native species can be modified by alien invasion. In addition, three more conditions must be met for pollinators to drive the evolution of floral traits: (1) pollinator visitation frequency or quality must be related to the floral traits; (2) certain floral phenotypes must have higher pollen removal and/or reception than others; and (3) fitness must be affected by pollinator visitation frequency or quality. If these conditions are fulfilled, several floral traits in native species may undergo character displacement in similar manner as has been shown for native species interactions (Hansen et al., 2000; Miyake and Inoue, 2003) due to alien invasion: First, autogamous or abiotic pollination may be favored in the native, such that the dependency on cross-pollination by shared floral visitors with the alien is reduced (e.g., Fishman and Wyatt, 1999; Porcher and Lande, 2005). Second,

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selection may favor a flower morphology that reduces heterospecific pollen deposition, or a reduction in pollinator sharing (e.g., Caruso, 2000). Third, a divergent flowering time in the native, away from the flowering time of the alien, may be favored to avoid competition for pollination (Waser, 1978; Lack, 1982; Rathcke, 1988a,b). Fourth, by evolving floral resemblance with the alien plant, the native may experience a facilitative effect through increased visitation rate and seed set, from pollinators unable to discriminate between the alien and the native (Johnson et al., 2003; Moeller, 2004). Thus, a convergent evolution of some floral traits, such as color, floral shape, and flowering time, may be coupled with a divergent evolution of other traits, such as stigma and anther positions to avoid heterospecific pollination. We know of no study that has investigated how aliens affect the evolution of floral traits in natives by comparing native flower traits in populations that have grown together to alien plants for a long time with those of native populations not subjected to alien invasion.

8.

Knowledge gaps and research priorities

Only two out of seven studies we found to date have detected clear competitive effects of aliens on the pollination of natives (e.g., Chittka and Schu¨rkens, 2001; Brown et al., 2002), but all seven studies suggested competition to predominate alien–native plant–pollinator interactions. It is premature to conclude that these results are applicable to all alien–native plant pollination interactions due to the paucity of empirical studies. For example, even if reduced flower visitation rates are observed in native species, their seed production is not necessarily reduced (Moragues and Traveset, 2005; Totland et al., 2006). In particular, we suggest that the breeding system, placement of pollen on pollinator bodies, and abiotic resource limitation on reproductive output in the native, may in some cases buffer negative effects of alien invasion on pollinator visitation and the subsequent reproductive output of the native. We recommend that future studies of alien effects on native pollination success consider the large spatial and temporal variability in pollination interactions. So far, most studies have only examined pollination interactions between alien and native plants on a small spatial scale and over few seasons and/or short time periods within seasons, which can only detect how alien invasion affects pollinator behavior at a local patch scale. To date, no studies have examined how alien invasion affects the population density and behavior of pollinators on a landscape scale (between communities) or over longer time periods (more than two years), but studies of how availability of floral resources affects pollinator activity on a landscape scale may suggest increased pollinator densities, abundance and diversity (Westphal et al., 2003; Ricketts, 2004; Kleijn and van Langevelde, 2006). Knowledge of these scales is important because the visitation patterns to natives are affected by both pollinator behavior and density. Although other studies suggested that the presence of an alien species reduced visitation to natives, it is still possible that the visitation to natives is higher than before the alien invasion, as a result of increased total pollinator abundance. This scenario only considers the pollination quantity

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component (the number of visits) of native–alien interactions. However, pollination quality (the number of conspecific pollen grains deposited per visit) may also change with alien invasion (through increased heterospecific pollination or changes in the pollinator assemblage of the native). How these three components (pollinator abundance, pollinator behavior, pollination quality) change with alien invasion, and how they act in concert to affect native pollination and reproductive success need further attention in the future. Studying alien–native plant–pollinator interactions on landscape scales and along gradients in alien density, over longer time periods, may detect such alien effects (pollinator abundance, pollinator behavior and pollination quality) on the pollination of natives (see, e.g., Cox and Elmqvist, 2000; Graves and Shapiro, 2003). Our knowledge of the mechanisms of interspecific pollination interactions among native species, and their consequences for plant reproduction, may to some extent be useful when assessing pollination impacts of alien species on natives. However, because many alien species are especially attractive to pollinators and since they may occur in unusually high densities, it is possible that their magnitude of impact on natives will differ compared to how natives affect each other’s pollination. In particular, we believe that studies incorporating density effects of alien species on pollinator population abundances across spatial scales, and that combine such effects with impacts on native pollination and reproduction, will create new and useful knowledge on how alien invasions have and will change the pollination and reproductive success of natives.

Acknowledgements We thank four anonymous reviewers that made excellent suggestions to improve the manuscript, and Vilma Bischof for her proof reading. The study was financed by the Norwegian University of Life Sciences and the Norwegian Research Council (project no. 154185/720 and 154442).

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