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Ecology |
Department of Ecology and Natural Resource Management, The Norwegian University of Life Sciences, P.O. Box 5003, NO-1432 Ås, Norway
Received for publication December 1, 2005. Accepted for publication March 23, 2006.
ABSTRACT
The invasion of exotic species into natural habitats is considered to be a major threat to biodiversity, and many studies have examined how exotic plants directly affect native plant species through competitive interactions for abiotic resources. However, although exotics can have potentially great ecological and evolutionary consequences, very few researchers have studied the effect of exotics on the interactions between plants and their mutualistic partners, such as pollinators, and none have reported on such impacts in logged and undisturbed boreal forest ecosystems. Here we show how experimental introductions of an exotic plant species (Phacelia tanacetifolia Bentham) affect pollinator visitation and female reproductive success of a native plant (Melampyrum pratense L.) in recently disturbed (i.e., logged) and in undisturbed boreal forest habitats. The presence of Phacelia significantly increased the number of bumble bees entering plots in both habitat types. However, the exotic species had a strong negative impact on the visitation rate to the native species in both habitat types. Despite this negative impact on pollinator visitation, the exotic had no effect on female reproductive success of the native species in any habitat. Our results show that seed production may be more robust than pollinator visitation to exotic invasion, irrespective of habitat disturbance history.
Key Words: Bombus • boreal forest ecosystems • competition for pollination • disturbance • exotic species • forestry • invasion • Melampyrum pratense • Phacelia tanacetifolia
The invasion of natural habitats by exotic species is recognized as one of the biggest threats to biodiversity (Mooney, 1999
). Exotic invasions are particularly likely in habitats disturbed by human activities (Burke and Grime, 1996
; Davis et al., 2000
), and several studies show that alien invasions reduce the local diversity of plant communities (Meiners et al., 2001
; Levine et al., 2003
). Studies on the specific mechanisms leading to reduced diversity after alien invasion have focused primarily on how alien species competitively displace native species through direct competition for abiotic resources (e.g., Crawley et al., 1999
; Levine et al., 2003
). However, exotic species may affect native species indirectly in several ways, including how natives interact with mutualist partners, such as pollinators, an interaction that has large consequences for the ecology and evolution of plant species (Ashman et al., 2004
). Unfortunately, not many researchers have examined the effect of alien invasion on the interactions between native plant species and their pollinators (Grabas and Laverty, 1999
; Chittka and Schürkens, 2001
; Brown and Mitchell, 2001
; Brown et al., 2002
; Memmott and Waser, 2002
; Morales and Aizen, 2002
; Aigner, 2004
; Gazoul, 2004; Moragues and Traveset, 2005
). Plant–pollinator interactions are essential for the long-term maintenance of ecosystem species diversity and composition, because they ensure plant reproduction and maintain genetic diversity of plant populations and result in novel combinations of traits that may contribute to species survival (Kearns et al., 1998
; Ashman et al., 2004
). In addition, flowering plants provide essential nutrition to the animals involved. Despite the potentially great importance, we only know of four previous empirical studies that have experimentally examined how alien invasion affect both pollinator visitation and reproductive success of native species (Grabas and Laverty, 1999
; Chittka and Schürkens, 2001
; Brown et al., 2002
; Aigner, 2004
), and we know of no studies that have examined if alien invasion impact on plant–pollinator interactions varies among habitats of contrasting human disturbance, as we do here (but see Morales and Aizen, 2002
).
Plants of different species may affect each other's pollinator visitation positively or negatively. Positive interactions may occur when the presence of one species (e.g., an alien) enhances pollinator visitation to another species (e.g., a native) because the presence of one species attracts so many pollinators to a heterospecific patch that the visitation rate to the other species (e.g., native) is increased compared to a monospecific patch. Such facilitative interaction is often referred to as the magnet species effect (Waser, 1983
; Laverty, 1992
; Johnson et al., 2003
; Feldman et al., 2004
; Moeller, 2004
). Negative competitive interactions for pollinator service may occur when the presence of one species (e.g., an alien) reduces the pollinator visitation to another (e.g., a native) because the former species dominate the available pool of potential pollinators, resulting in a reduction in visitation quantity to the latter (Waser, 1983
; Caruso, 1999
; Brown et al., 2002
). Moreover, plants of different species may reduce each other's pollination success through heterospecific pollination, resulting in reduced pollination quality (Waser, 1983
; Brown and Mitchell, 2001
). Because seed production of most animal-pollinated species appears to be affected by the amount of conspecific pollen grains deposited on their stigmas (Burd, 1994
; Ashman et al., 2004
), it is plausible that interactions for pollinator attraction and heterospecific pollination that alter pollination quantity and/or quality could influence plant reproductive success.
In this study, we experimentally simulate the invasion of an exotic plant species that is highly attractive to pollinators and examine how this invasion affects pollinator foraging behavior on a small scale and the pollination and reproductive success of a native boreal forest herb. To assess the potential effect of human disturbance on the interaction between the exotic and native species, we conducted the experiment in both young forest stands planted on areas severely disturbed by clear felling and in old forests that bear no clear signs of recent logging (see also Morales and Aizen, 2002
). The study area is located in a forest landscape with a long history of human presence (Molinari et al., 2005
). It displays a mosaic of forest stands of contrasting maturity because the boreal forest has been increasingly fragmented and disturbed by humans since the 19th century.
Insect pollinators may be sensitive to disturbance, particularly habitat fragmentation (Kearns et al., 1998
, Aizen and Feinsinger, 2002
; Ashworth et al., 2004
). Pollinator species richness and abundance has been shown to decrease after habitat fragmentation and disturbance (Aizen and Feinsinger, 2002
and references therein) because of reduced availability of nesting sites and floral resources, and restricted dispersal opportunities. On the other hand, it is conceivable that disturbance (i.e., logging) may increase resource availability of flower visitors, particularly in boreal forest ecosystems, because the abundance of nectar- and pollen-rewarding species may temporarily increase after logging (see also Morales and Aizen, 2002
). Because any changes in the pollinator community have the potential to alter the reproductive success of insect-pollinated plants and because plant–pollinator mutualisms may be disrupted in disturbed or fragmented habitats (Kunin, 1993
; Bronstein, 1995
; but see Ashworth et al., 2004
), it is possible that an exotic plant species will have contrasting effects on the pollination and reproductive success of native species in disturbed and undisturbed forest habitats. Specifically, we predict that pollinator visitation and female reproductive success of the native species (Melampyrum pratense) is affected by the experimental introduction of the exotic species (Phacelia tanacetifolia) and that native plants in disturbed habitats are particularly prone to exotic invasion.
MATERIALS AND METHODS
Study area
This study was conducted in a species-poor boreal forest landscape situated ca. 500 m above sea level in Telemark County, southern Norway (59°21' N, 9°45' E, close to Årum, ca. 35 km north of Skien Municipality). Our study area consisted of a managed forest landscape with a matrix of forest stands of contrasting maturity and disturbance history. All study sites were situated within an area of 0.5 x 2 km and in either young forest on disturbed clear-cuts (logged within the last 10 years) or in relatively old, undisturbed forest stands with no obvious signs of recent logging (average tree age >90 years). On the disturbed sites, the forests either did not start regrowing after the clear-cut or were dominated by trees <3 m tall. In the old forest, the tree layer was mature, with trees up to more than 20 m tall. Picea abies (L.) H. Karst is the dominant tree species, but scattered specimens of Pinus sylvestris L., Betula pubescence Ehrh., and Populus tremula L. also occur. The perennial dwarf shrub Vaccinium myrtillus L. dominates the understory, although V. vitis-iadea L., V. uliginosum L., Empetrum nigrum L., and Calluna vulgaris (L.) Hull are also common. The most abundant insect-pollinated species in the area are Melampyrum pratense, Cornus suecica L., Trientalis europaea L., and Maianthemum bifolium (L.) F. W. Schmidt.
Study species
We used Phacelia tanacetifolia Bentham (Hydrophyllaceae) as the experimentally introduced exotic species. This species is known to be highly attractive to flower visitors and is used as a forage plant in beekeeping (Petanidou, 2003
and references therein). Phacelia tanacetifolia is an annual herb with ca. 6–10 mm wide, open, bluish-violet flowers, and five exserted stamens. Flowers occur in coiled inflorescences that unwind as flowers open. In our study area, we observed Bombus spp. (mainly B. pratorum L. and B. lucorum L.), flies, and beetles visiting P. tanacetifolia. The herb is native to western North America, but has frequently naturalized in Europe (Tutin, 1972). Because P. tanacetifolia currently is not invasive in Norway but is frequently used as a bee plant and as an ornamental in gardens, we examined the potential initial effects of its invasion into a patchily disturbed landscape.
We used the annual Melampyrum pratense (Scrophulariaceae) as the targeted native species. Melampyrum pratense is an annual hemiparasitic plant, common in boreal forests throughout central and northern Europe. Two to four flowers occur together in inflorescences situated close to the stem. The corolla of M. pratense is pale yellow, zygomorphic, and ca. 15 mm long. The two anthers and single stigma are situated inside the corolla below the upper petal. The fruit is a capsule that can contain 0–4 mature seeds. Although pollinator exclusion experiments have shown that M. pratense is autogamous, seed and fruit set is considerably reduced after pollinator exclusion (Kwak and Jennersten, 1991
). Melampyrum pratense was exclusively visited by Bombus spp. during our observations. The Bombus species visiting M. pratense were the same in recently logged and disturbed sites (A. Nielsen et al., unpublished data). There were no other insect-pollinated plant species flowering inside our study plots during the experiment.
Experimental design
We set up five experimental blocks, each containing a disturbed forest stand adjacent to an undisturbed forest stand. We established one plot with an area of ca 60 x 60 m, that containing a study population of M. pratense within each disturbed and undisturbed stand. Within each of these 10 populations, we randomly positioned 10 subplots, each 2 x 2 m with M. pratense as the only species flowering during our pollinator observations. We randomly assigned half of these subplots to serve as controls and the other half to receive the exotic treatment. Thus, our experiment was a split-plot design, with disturbance as the whole-plot factor and the presence of the exotic plant as the subplot factor (described further in statistical methods). To minimize any effect of the exotic plant in the treatment plots on native plants in control plots, we separate the control and treatment plots by >5 m. Because bumble bees may forage over large areas (Goulson, 2003
), this distance may not have been sufficiently large to prevent effects from experimental plots on visitation in control plots. On the other hand, a very large distance between experimental and control plots was in practicality difficult to achieve and could also have resulted in the experimental and control plots having different environmental conditions that could affect both pollinator abundance and plant reproduction. Because our main goal was to analyze the effect of an invasive species on the small-scale foraging behavior of pollinators and the small-scale effects on native plant reproduction and because the experimental density of the invasive species that we used was relatively low (discussed later), we believe this approach is justified. Early after the establishment of the experiment, moose grazed all the P. tanacetifolia plants in all experimental subplots in one of the disturbed forest plots, forcing us to remove the block containing this plot in the split-plot analyses. In such analyses, this gave an effective sample size of four blocks with 80 study plots in total (moose did not destroy any exotic plants in any of the other blocks). The floral abundance of M. pratense in our study was higher in young (mean no. flowers/4 m2 = 128.5 ± 11.0 [SE]) compared to old forest stands (71.6 ± 8.6), but there was no difference in flower density between control (99.4 ± 10.6) and experimental plots (100.6 ± 10.3).
Early in the flowering season of M. pratense, we planted 15 plants of P. tanacetifolia at an early stage of flowering into each exotic-treatment plot. These plants were grown from seed in a greenhouse. Mortality of P. tanacetifolia was low, except in the plot where moose had grazed the plants. Dead plants were not replaced. A density of 
3.75 plants/m2 is perhaps relatively low compared to real invasions of herbaceous species, but unfortunately we did not have more plants available.
To avoid undesired establishment of P. tanacetifolia in the study area, we carefully examined the study sites the following year. No established plants were found.
Pollinator visitation
To assess if P. tanacetifolia affected pollinator visitation to native M. pratense, we observed control and experimental plots simultaneously for 20 min periods between 0930 and 1840 hours over several days of the flowering period and counted the total number of bumble bee visits to flowers of M. pratense and to inflorescences of P. tanacetifolia during each observation period (N = 144 periods in total for the four blocks). Before each period started, we counted the number of open flowers of M. pratense and the number of inflorescences with open flowers in P. tanacetifolia. We counted inflorescences, rather than individual flowers in P. tanacetifolia because flowers are very densely positioned inside inflorescences. We defined a flower visit to M. pratense to have occurred when a bumble bee entered the flower. A visit to P. tanacetifolia was recorded when a visitor aligned on the inflorescence. We only counted visits by bumble bees because no other visitor taxa were observed on M. pratense during the study and because this was the only pollinator taxa shared by the two plant species. In addition to bumble bees, numerous flies visited P. tanacetifolia (ca. 50% of visits was conducted by bumble bees). However, because the pollination of M. pratense was the focus of our study (and as noted, these flies did not visit M. pratense), these were not counted. We also examined how the presence of the exotic species affected aspects of the behavior of individual bumble bees. First, during the 20-min periods, we counted the total number of bumble bees entering the plots and defined an entry to have occurred when a bumble bee was first observed to visit a flower, regardless of species. Second, to assess flower constancy of individual bumble bees, we counted the number of times a bumble bee was observed to switch from flowers on one species to flowers of the other, and also noted the direction of the switch. It should be noted that because we were primarily interested in assessing how exotic introduction affected visitation and reproduction in a native plant, we did not control for total flower density in our experimental set-up by supplemental planting of the native to achieve the same total flower density as in experimental plots with the exotic species.
We used a mixed-model ANOVA (GLM, SPSS 12.0; Chicago, Illinois, USA) to assess if the presence of the exotic species affected the number of bumble bees entering plots (log + 1-transformed) and the pollinator visitation rate to the native species (arcsine square-root transformed), and whether the effect of the alien differed between young and old forest habitats. Our models included the habitat factor (young vs. old forest, fixed factor), the block factor (four blocks of young and old forest sites situated close together, random factor), the interaction between the habitat and the block factors, the experimental factor (alien vs. control, fixed), and the interaction between the experiment and the habitat factor. Due to the split-plot design of our experiment, we used the interaction between habitat and block as the error term for the habitat factor and the error of the whole model as the error term of the experimental and the experiment by habitat interaction (see Milliken and Johnson, 1984
). To examine in more detail how the exotic plant could affect the pollinator visitation rate to the native species, we used linear multiple regressions on data from plots where the exotic was introduced to assess if the visitation rate per flower to M. pratense (dependent, arcsine square-root transformed) was related to the flower density of M. pratense (log-transformed), the inflorescence density of P. tanacetifolia (log-transformed), the number of bumble bees entering the plot (log-transformed), and the visitation rate to P. tanacetifolia inflorescences (untransformed). Because the mean of many of these variables differed significantly between old and young forest habitats, we conducted separate regressions for each habitat type, instead of using ANCOVA, which assumes that covariable means do not differ between levels of the grouping variable (Sokal and Rohlf, 1995
) (forest type in our case). In these regressions, we included observations from the block where moose had destroyed several plots. We removed all observation periods lacking bumble bee entry from our analyses on visitation rates because these periods provide no information on how the two plant species interfere regarding pollination. This resulted in a total sample size of 88 periods in the analyses of visitation rates.
Female reproductive success
To assess if the experimental introduction of P. tanacetifolia affected female reproductive success of M. pratense, we randomly selected two flowering plants of M. pratense within each plot. On these plants, we randomly selected three flowers that were in anthesis when the exotic was flowering. We collected mature fruits immediately before seed dispersal and counted developed seeds. Many plants were lost, primarily due to moose grazing, before fruit maturation, and could therefore not be included in the analyses. We used a similar split-plot ANOVA as described above for pollinator visitation to test for treatment and habitat-type effects on seed set per flower and fruit set per plant in M. pratense.
RESULTS
Pollinator visitation
A two-factor ANOVA showed that there was no difference in visitation rate to exotic inflorescences between recently disturbed and undisturbed old forest habitats (F1,3 = 0.20; P = 0.68). Moreover, a nonsignificant block factor (F3,3 = 1.40; P = 0.39) showed that the visitation rate to P. tanacetifolia was spatially invariant among the four blocks of disturbed and undisturbed forest sites. Pooled across blocks and forest types, P. tanacetifolia received a mean of 0.62 ± 0.1 (SE) visits per inflorescence per 20 min.
The presence of the exotic species significantly increased the number of bumble bees entering the 2 x 2 m study plots (Fig. 1A; F1,118 = 22.82; P < 0.0001). There was no difference in the number of bumble bees entering plots in disturbed vs. undisturbed forests (Fig. 1A; F1,3 = 0.64; P = 0.48), and there was no significant treatment x habitat interaction on the number of bee entries (F1,118 = 1.17; P = 0.28). Finally, there was no significant difference among blocks in the number of bee entries per plot (F3,3 = 1.15; P = 0.46). In control plots, 48% of the periods had no bee entry, whereas only 14% of periods in experimental plots had no bee entry, a highly significant difference in frequencies (
2 = 17.6; df = 1; P < 0.0001).
|
Seventy-six and 71.4% of the periods with more than one flower visit (regardless of which species) in undisturbed and disturbed forest stands, respectively, had no pollinator switches between the two species.
Multiple linear regressions (Table 1) showed that the visitation rate to M. pratense in the undisturbed forest habitats was significantly, negatively related to the visitation rate to P. tanacetifolia inflorescences and positively related to the number of bumble bees entering the plot, while it was not related to flower density of M. pratense or P. tanacetifolia. In disturbed forest habitats, the visitation rate to M. pratense was significantly, positively related to the number of bumble bees entering plots, but was not related to the other predictors (Table 1).
|
Seed number per fruit in M. pratense did not differ significantly (F1,66 = 0.007; P = 0.93) between plants in control (mean = 1.38, SE = 0.090) and experimental plots (mean = 1.37, SE = 0.10). Moreover, there was no significant difference in seed number between undisturbed (mean = 1.40, SE = 0.11) and disturbed (mean = 1.35, SE = 0.08) forest habitats (F1,3 = 0.08; P = 0.80), and no significant treatment x habitat interaction (F1,65 = 0.30; P = 0.59).
DISCUSSION
Pollinator visitation
Pollinator foraging behavior was altered, and the resulting flower visitation rate to Melampyrum pratense was substantially reduced at a local patch scale in the presence of the experimentally introduced exotic species, Phacelia tanacetifolia. Moreover, regression analysis showed that in plots with P. tanacetifolia, visitation rate to the native species was negatively related to visitation rate to the exotic, at least in the undisturbed forest. Interestingly, these negative impacts of exotic invasion on native pollinator attraction occurred despite the fact that experimental plots had substantially more bumble bee entries than control plots. Thus, although P. tanacetifolia exerted a magnet species effect on bumble bees, at the scale we studied (Laverty, 1992
), it did not increase the visitation rate to M. pratense. Instead, bumble bees that entered experimental plots mainly visited the exotic, and individual bumble bees had a high degree of preference for, and constancy on, the exotic species, thus reducing the visitation rate to M. pratense. Our data suggests that when P. tanacetifolia is introduced, it functions as a competitor for pollinator visitation to the native species, at least at a local patch scale. This competitive effect occurred even though we introduced P. tanacetifolia at relatively low density. Note that natural invasions usually differ from our experimental invasion, particularly with regard to the density and area covered by the exotic species. Thus, our experimental simulation of an invasion event is likely most relevant to the effect of an exotic plant species on pollination and reproduction at early stages of an invasion.
Previous experimental studies on the impacts of exotic invasion on the pollination success of native species have obtained opposing results. Brown et al. (2002)
found that Lythrum salicaria significantly reduced pollinator visitation to the native congener L. alatum in USA, whereas Chittka and Schürkens (2001)
found that the alien Impatiens glandulifera reduced the pollinator visitation rate to the native Stachys palustris in Germany. In contrast to these results, Grabas and Laverty (1999)
found that the presence of L. salicaria increased (or had small effects) on pollinator visitation rate to Eupatorium maculatum in Canadian wetlands, whereas Aigner (2004)
found no significant effect of experimental removal of non-native species on the pollinator service to Dithyrea maritimea in USA. Thus, available experimental results suggest that effects of alien presence on pollinator visitation rates to native species are highly equivocal. Nevertheless, our results and those of Chittka and Schürkens (2001)
and Brown et al. (2002)
may suggest that there is a higher probability of negative than positive impacts of exotic invasion on pollinator visitation rate to flowers of native species.
Effects of disturbance history
There was no statistically significant treatment by habitat interaction, suggesting that the magnitude of the impact of exotic invasion on native pollinator visitation was similar in recently disturbed forest compared to undisturbed forest. Thus, it does not appear that disturbance accelerated any negative effects of invasion on pollination and reproduction in our study system. There may be many reasons for this. In our system, the visitation rate to exotic inflorescences did not differ between habitats. A difference in visitation rate to the exotic species between habitats could provide a basis for a habitat-specific difference on effects of exotic invasion on visitation rate to the native species (see Grabas and Laverty, 1999
). Alternatively, it is possible that the spatial scale of our study was too small to detect any influence of disturbance on pollinators that may move across large distances (e.g., Goulson, 2003
). We established study sites only on the basis of the disturbance history of the focal forest stand. The disturbance history of adjacent forest stands was not taken into account, although that may impact pollinator foraging behavior. A different effect of exotic invasion between disturbed and undisturbed habitats could also occur if disturbance reduced the floral abundance of the native species, while the exotic species was introduced in equal density in the two habitats. Such a situation could lead to a greater negative effect in terms of pollinator visitation in the disturbed than in the intact forest habitats. However, because floral abundance of the native species was actually highest in the disturbed habitat, this situation apparently did not appear in our system. In summary, although an exotic invasion may be more likely in disturbed habitats (Burke and Grime, 1996
; Davis et al., 2000
), our results suggest that impacts on pollinator visitation rates to natives may not be exacerbated by disturbance.
Effects on reproduction
Although introduction of an exotic plant reduced pollinator visitation to M. pratense considerably at a local patch scale, it did not affect its female reproductive success. This contradicts the results of the other experimental studies we know of, where alien invasion significantly reduced the reproductive success of native species (Lammi and Kuitunen, 1995
; Grabas and Laverty, 1999
; Chittka and Schürkens, 2001
; Brown et al., 2002
). Despite a possible large difference in pollen deposition between plants growing with and without the alien, environmental constraints from other factors than pollination (e.g., resource availability or host availability) could have prevented plants in control plots with relatively higher pollen deposition to benefit from it in terms of fruit and seed production (Haig and Westoby, 1988
). On the other hand, Kwak and Jennersten (1991)
found that seed and fruit set of M. pratense were pollen limited in a south Swedish meadow. Another explanation may be that M. pratense is autogamous at our sites (see Kwak and Jennersten, 1991
). If so, its seed production may, to an unknown extent, be independent of pollinator visitation and cross-pollen deposition on stigmas (Larson and Barrett, 2000
). An analysis of its breeding system could aid us in assessing if this was the case at our study site. Moreover, our results on pollinator switching suggest that heterospecific pollination between the two species is low, because bumble bees were highly faithful to both species when foraging in heterospecific patches. Finally, based on the flower morphology of P. tanacetifolia, its pollen is likely to be deposited mainly on the lateral and ventral parts of the bumble bee body. Because stigmas of M. pratense mainly contact the dorsal part of visiting bumble bees, very little heterospecific pollination is likely, despite pollinator switching between the two species. Thus, to the extent that the exotic should have an effect on the native's reproductive success, it would most likely primarily be through pollinator attraction and visitation frequency.
Conclusions
Our results show that an experimental introduction of the exotic Phacelia tanacetifolia reduced pollinator attraction in the native Melampyrum pratense and that habitat disturbance did not modify the impact of pollinator visitation by the exotic. Reproduction in M. pratense was, however, robust to changes in visitation frequency; neither seed nor fruit set was affected by the exotic. Our results, together with the results from the few other experimental studies on the effects of exotic invasion on pollination and reproduction in natives suggest that impacts may vary among species, depending on their breeding system, pollination specialization, habitat, and other life-history properties.
FOOTNOTES
1 The authors thank the Research Council of Norway for financial support (project number 154442), Fritzöe Skoger AS for their kind and generous attitude, and A. Folstad Hagen, H. Bergsjø, L. Bach and O. W. Røstad for field and seed-sowing assistance. This manuscript was improved greatly from the comments by anonymous reviewers. 
2 Author for correspondence (orjan.totland{at}umb.no
); phone: +47 64965781; fax: +47 64965801
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