Independent Study Semester

How do habitat restorations affect plants and pollinators in Metro Vancouver Parks?

Hannah GehrelsFor Elizabeth Elle and David Green

December 9, 2013

AbstractAnthropogenic disturbance associated with urban growth facilitates the spread of invasive

plant species which compete with native species for access to mutualists such as pollinators. Habitat restorations are often purposed to prevent native species loss and restore mutualistic interactions. We used 12 semi-urban parks (each with a restored and control plot) located throughout the Greater Vancouver area to investigate how habitat restorations via native plantings and invasive plant removals impact plant and pollinator communities. We found that plant richness and Simpson’s diversity were higher in restored plots, but that abundance was similar with restoration treatment. We also found that pollinator richness was higher in restored plots when we controlled for time, and that abundance and Simpson’s diversity tended to follow this same trend. Finally, we found that nestedness and asymmetry were higher in control (invaded) plots due to a higher abundance of generalist invasive plants, suggesting that invasive plants become highly integrated into plant-pollinator networks and may increase network resilience. We suggest that when invasive plants are removed, managers should ensure that alternative forage is available by planting generalist native species that have radially symmetrical flowers and that together provide floral resources across the appropriate phenological and spatial scales.

Key words: invasive species, restorations, floral resources, plant-pollinator networks

IntroductionAnthropogenic disturbance associated with urban growth facilitates the spread of invasive

species which modify the structure and stability of communities (Hierro et al. 2006, Kneitel and Perrault 2006). In particular, invasive plants alter the composition of native plant communities by outcompeting native species for nutrients, water and light (Abraham et al. 2009). Invasive plant species can also compete with native species for access to mutualists such as pollinators or seed dispersers (Traveset and Richardson 2006), and generally will affect animals that depend on plants for food and habitat (Litt and Steidl 2010).

Ecological restorations are increasingly used in attempts to prevent native species loss and reestablish ecosystem function. Restorations return the species composition and physical structure of disturbed habitat to a goal state (often based on historic conditions; SER Working Group 2004). Restorations of anthropogenically altered terrestrial habitats often involve planting native species, sometimes coupled with removal of invasive species. Increased species richness or abundance is frequently used as a measure of restoration success, but species richness does not always capture ecosystem function (Elle et al. 2012). Pollinators play an important role in providing ecosystem services and may serve as a good indicator of ecosystem recovery (Montoya et al. 2012), but a consideration of plant-pollinator interactions as well as changes in richness or abundance is required (Elle et al. 2012).

Plant-pollinator interaction networks are useful because they focus on the functional role of species in a community rather than simple presence/absence (Elle et al. 2012). Since pollinators are essential for the reproduction of the vast majority of flowering plants (Ollerton et al. 2011), evaluating plant-pollinator interactions can provide information about the resilience of communities. Plant-pollinator networks have a nested structure whereby interactions are organized around a core group of generalist plant and pollinator species (Kaiser-Bunbury et al. 2011). Some specialized pollinators visit generalist plants and vice versa resulting in asymmetrical dependence (Elle et al. 2012). More nested, asymmetrical and generalized interaction networks tend to be more resilient in the face of further disturbance (Thébault and Fontaine 2010, Elle et al. 2012).

Mixed results have been found in studies that investigated impacts of restoration on pollinators in urban and semi-urban environments. Some studies have shown that habitat restorations can increase pollinator abundance, richness and diversity (Carvell et al. 2007, Hopwood 2008), whereas others have found no effect (Forup and Memmott 2005, Bartomeus et al. 2008, Matteson and Langellotto 2011, Williams 2011, Ferrero et al. 2013). Most studies agree that invasive plants can be can become high integrated into plant-pollinator interaction networks (Memmott and Waser 2002, Morales and Aizen 2006, Lopezaraiza-Mikel et al. 2007, Valdovinos et al. 2009, McKinney and Goodell 2010), which serve to increase nestedness and asymmetry (Aizen et al. 2008, Bartomeus et al. 2008). Given this variation in results, the utility of restoration efforts should be considered in different ecosystem types. In addition, none of these studies explicitly investigated how pollinators change over the season. The phenology of flowering plants (available forage) in a community is important because many solitary bee species are only actively foraging for a few weeks (O’Toole and Raw 2004, Godoy et al. 2009). The timing of native plant availability may be crucial when restoring plant communities to support pollinators, and when assessing restoration success.

Here we aim to investigate the effects of native plant restorations coupled with the removal of invasive species on the abundance, richness and diversity of pollinators and the resilience of plant-pollinator interactions in urban parks in the Greater Vancouver Regional

District. We hypothesize that in comparison to the control areas, the restored areas will have (1) higher pollinator abundance, richness and diversity, (2) higher floral abundance, richness and diversity, (3) more temporally uniform flower and pollinator abundance and richness, and (4) lower nestedness and asymmetry, and a higher specialization index.

Methods

Study AreaWe conducted this study in 12 urban to semi-urban parks throughout the Greater

Vancouver area from April 24-August 22, 2013 (Fig. 1). Each site included a pair of plots, one restored and one control with plots matched in shape and area. Plots were an average of 176m apart from each other (range: 50-440m, Table 1). We also sampled at a 13th site (Lower Seymour Conservation Reserve), and a third plot at CF-2, but did not include these plots in our analysis because the paired plots were not similar enough for an accurate comparison between restored and control plots.

Vegetation samplingOnly potentially pollinator-attractive plants with open flowers were sampled for this

research, and so grasses, ferns, etc were not included. Flower abundance, richness and diversity for each plot were sampled on the same days pollinators were assessed. For the seven sites that had plots with linear hedgerows, vegetation was sampled along a 50 m transect along the hedgerow edge, with samples taken at 1-m intervals. The line intercept method was used such that the number of open flowers intersecting a 1m line perpendicular to the transect (into the hedgerow) was counted by species. For the five sites that had plots with approximately rectangular areas, the vegetation was sampled using the same line intercept method, but at regular intervals along 5 parallel transects placed in a stratified random manner. Length of transect varied with the size of the plot. Densely clustered floral heads (e.g. in families Asteraceae, Brassicaea, Plantaginaceae) were considered a single “flower” for the purposes of this study (see Appendix A for floral unit designations by species).

Pollinator samplingWe caught floral visitors (hereafter pollinators) with hand-nets directly from flowers. We

sampled each site approximately every two weeks on warm, sunny days (temperature ≥ 14, low wind, and sunny to partly cloudy). Pollinators were collected for 15 minutes by each of two people (= 30 minutes per plot per sample date), in the morning (1000 – 1200h), midday (1200 – 1400h) or late afternoon (1400 – 1600h). Paired plots were sampled on the same day, and most sites were sampled three times in each of the three times of day, for a total of 9 sample episodes (4.5 hours) per site. Three of the sites (BB-1, BB-2, and OM) were not restored or accessible until after we had started sampling, so were sampled for 7 sample episodes only (3.5 hours). Flower species identity was noted for each pollinator collected. All bees were identified to species except those for which revised keys were not available. Flies and wasps were identified at least to family, but to genus or species where possible.

Statistical analysisWe compared abundance, species richness, and evenness of plants and pollinators in

restored and control plots. To examine species evenness, we calculated Simpson’s diversity

index for each plot within a site: D=1−(∑ ni

N )2

, where ni is the number of individuals of species

i, and N is the total number of individuals. To investigate differences in plant and pollinator abundance, richness, and Simpson’s diversity between restored and control plots, we performed a mixed effects ANOVA with treatment as the main effect and site as a random effect. To compare pollinator and floral abundance and richness over time between the restored and control plots, we performed a repeated measures ANOVA with time, treatment, and their interaction in the model, again including site as a random effect. We could not compare Simpson’s diversity over time because on some date/site combinations, no pollinators were caught, resulting in undefined values. To examine the functional shifts in plant and pollinator communities and to identify interactions that may be vulnerable to disturbance, we created a plant-pollinator network for each plot. Using the bipartite package in R (Dormann et al. 2008), we calculated nestedness, asymmetry, and the specialization index (H2’; Blüthgen et al. 2006), for each network and compared between restored and control plots using a mixed effects ANOVA with site as a random variable.

Results

Plant abundance, richness and diversityPlant abundance did not differ with restoration treatment (F1,11=0.06, P =0.81, Fig. 2).

Richness and Simpson’s diversity were significantly higher in restored plots compared to control plots (richness: F1,11=5.62, P =0.04, Simpson’s diversity: F1,11=5.97, P =0.03). Repeated measures analysis indicated that abundance and richness changed over time with abundance peaking in early July and richness peaking in late July (abundance: F8,174=5.37, P<0.0001, richness: F8,174=4.78, P<0.0001), although the interaction term was once again not significant (abundance: F8,173=0.70, P=0.69, richness: F8,171=1.21, P=0.30). Richness was significantly higher in the restored plots in this analysis, whereas the difference in abundance remained non-significant (richness: F1,173=17.30, P<0.001, abundance F1,173=0.09, P=0.77). However, the restored plots tended to have higher flower abundance early and late in the season, whereas the control plots tended to have higher abundance in the middle of the season driven by a high abundance of invasive Rubus discolor in several of the control plots (Fig. 3).

Pollinator abundance, richness and diversityWe netted 3247 individuals in total, representing 150 species (bees: 24 Halictidae, 21

Megachilidae, 17 Andrenidae, 10 Bombus, 10 other bees, as well as the highly managed Apis mellifera; flies: 41 Syrphidae, 9 other flies; 17 wasps; and 8 other floral visitors (hummingbird, butterflies, beetle, etc)). Although all tended to be higher in the restored plots (Fig. 2), pollinator abundance, richness, and Simpson’s diversity did not significantly differ with restoration treatment (abundance: F1,11=1.74, P=0.21, richness: F1,11=1.53, P=0.24, and Simpson’s diversity: F1,11=0.88, P=0.37). The repeated measures analysis indicated that abundance and richness changed over time (abundance: F8,173=2.10, P=0.04, richness: F8,173=3.41, P=0.001). Abundance in the restored plots peaked in the third sampling period (late May), which seems to

be driven by 2 species: the solitary Andrena miserabilis which was only found at one plot (PS-2) on one day, and the highly managed Apis melifera at another plot (AG) where managed hives were kept nearby. Abundance in the control plots and richness for both treatments peaked in late July (Fig. 4). There was no difference in how control vs. restored plots responded to time (interaction term was not significant; abundance: F8,171=0.34, P=0.95, richness: F8,171=0.61, P=0.77). Both abundance and richness were higher in the restored plots in this analysis, but only richness achieved significance (abundance: F1,171=2.92, P=0.089, richness: F1,171=7.10, P=0.008).

Network metricsNestedness tended to be higher in the control plots, but did not achieve statistical

significance (F1,11=4.05, P =0.07, Fig. 5). Asymmetry was significantly higher in the control plots compared to the restored plots (F1,11=11.45, P =0.01). The specialization index (H2’) did not differ with restoration treatment (F1,11=0.39, P =0.54).

Discussion

Plants and PollinatorsRestorations increased floral species richness and Simpson’s diversity as we predicted,

but these improved floral resources did not translate into higher abundance, richness or diversity of pollinators in the restored plots. In general, pollinator communities are expected to track plant communities that provide food resources (Potts et al. 2004, Hennig and Ghazoul 2011). Some previous studies found that restoration increased pollinator richness (Carvell et al. 2007, Hopwood 2008). Of those studies that did not find increased richness with restoration (Forup and Memmott 2005, Bartomeus et al. 2008, Matteson and Langellotto 2011, Williams 2011, Ferrero et al. 2013), there were three main interpretations that apply to our study which we discuss below.

First, native plant additions may have been insufficient numerically to produce a measureable increase in pollinator species richness (Matteson and Langellotto 2011). In our study, restorations improved floral richness and Simpson’s diversity, but floral abundance was similar with restoration treatment. The most common invasive plant species, Himalayan Blackberry (Rubus discolor), produces large numbers of flowers per unit area. It seems that the native plant additions in the restored plots were insufficient in number to produce a measurable increase in floral abundance relative to the floral resources in the control plots from abundant invasive species like Rubus discolor. This similarity in floral abundance with restoration treatment may have, in turn, affected our lack of significant improvement in pollinator species richness. A model by Matteson and Langellotto (2011) suggested that it would take approximately 200-250 flowers to increase bee richness by one species. If the assumptions of this model apply to our system, the similarity in flower abundance with restoration treatment that we found in our experiment would be predicted to be associated with no difference in pollinator richness, as we found.

Second, pollinator community composition may be different even though abundance, richness and diversity are similar (Williams 2011, Ferrero et al. 2013, Wray et al. in press). In our study, pollinators could have flown between plots (plots were on average 176m apart whereas the typical flight distance of solitary bees is 200-400m, Greenleaf et al. 2007), which may have dampened the observed differences in pollinator communities between restored and

control plots. However, the ‘floral market’ hypothesis suggests that pollinators choose between plant species on the basis of the quality of their resources (nectar and pollen, Chittka and Schürkens 2001). This hypothesis indicates that even if pollinators were flying between plots, they were making choices about which flowers to visit, so we could still expect a difference in pollinator communities if the plant communities are different. For instance, we might expect more generalist pollinator species to be present in the control plots that have more generalist invasive plants (Cane et al. 2006). In future analyses of our data, we will pursue community-scale analyses (e.g. ordination) to assess differences in the plant and pollinator communities, rather than just evaluating differences in richness and diversity (Wray et al. in press).

Thirdly, flowering plants do not provide all the resources needed for pollinators. Nesting sites for soil-nesting bees may be particularly limited in urbanized landscapes due to soil compaction and pavement (Cane et al. 2006, Matteson et al. 2008). In contrast to floral resources, however, nesting resource availability is difficult to assess, and further studies on bee nest site use in urban areas are required. If nest sites are a major limiting factor for some pollinators, simple additions of floral resources may not be enough to increase overall pollinator abundance, richness and diversity (Potts et al. 2005).

Plant and pollinator abundance and richness varied with time, peaking in mid-season. The variation over time did not vary with restoration treatment, however, indicating that floral resource availability (and the abundance and richness of pollinators requiring those resources) was similar in control and restoration plots. This is important because pollinators rely on the overlap between their flight periods and the flowering periods of each plant species in a particular area (Bosch et al. 1997, Basilio et al. 2006). One interesting finding was that when seasonality was controlled in the repeated measures analysis, pollinator richness was significantly higher in restored plots. That is, controlling for the variability among sample periods allowed us to detect that pollinator richness was improved with restoration. The increase in richness is most pronounced in the late season, which may have been caused by the similar increase in plant richness at this time. It may be useful to consider floral availability at other times of the season and whether restoration planning could be improved by considering plant flowering time.

Plant-pollinator networksAsymmetry and nestedness were higher (asymmetry significantly so) in control plots.

This finding suggests that control (invaded) plots are more resilient to disturbance than restored plots. Many studies agree that invasive plant species can become highly integrated into plant-pollinator interaction networks (Memmott and Waser 2002, Morales and Aizen 2006, Lopezaraiza-Mikel et al. 2007, Valdovinos et al. 2009, McKinney and Goodell 2010). Aizen et al. (2008) found that more invaded sites had higher asymmetry than their less invaded counterparts resulting from a transfer in the plant-pollinator interactions from generalist native plant species to super-generalist invasive plant species. These generalist invasive plants reduce the average interaction strength in the network and increase nestedness and asymmetry (Aizen et al. 2008, Bartomeus et al. 2008, Valdovinos et al. 2009). Since most of the nonnative plants in our study area were generalist plants with radially symmetrical flowers that allow any insect to interact with them (e.g. Rubus discolor, Hypochaeris radicata, and Ranunculus repens), this reason seems to fit for our study as well. In contrast, several native plant species used in the restorations had limited pollinator access (e.g. Lonicera involucrata, Ribes sanguineum and Lupinus arcticus), and as such, were not available to all pollinators.

High asymmetry and nestedness are generally thought to confer higher network stability in the face of disturbance due to more redundant plant-pollinator interactions (Elle et al. 2012). However, a focus on these metrics may overlook other subtle changes in network structure. For example, Aizen et al. (2008) found that invasive plant species decreased the amount of native-native interactions, some of which may be ecologically and evolutionarily important. For this reason, it is important to investigate how plant-pollinator interactions change with habitat restorations, in addition to calculating these network parameters.

Since native plants coevolved with native pollinators, specialized interactions may have formed over evolutionary time, increasing the amount of specializations in a network composed of primarily native species compared to an area with invasive plants (Gotlieb et al. 2011). In our study, however, the specialization index (H2’) did not differ with restoration treatment even though restored sites had fewer invasive species than control sites (20.25% of the flowers in restored plots were invasive compared to 47.92% in control plots). It is possible that the differences in the amount of invasive species between plots may not have been large enough to have a measureable impact on the change in specialization index. Additionally, our analyses were created using cumulative networks which groups all of the plant and pollinators together, including species that are not active at the same time(Basilio et al. 2006). This method exaggerates generalization scores and could overlook possible changes in the degree of specialization over the season (Basilio et al. 2006, Burkle and Alarcón 2011). We suggest that further analyses of plant-pollinator networks include intra-annual variation.

Conclusions Invasive plants are considered to be the third major cause of pollinator diversity loss

(Kearns et al. 1998). Our study suggests that invasive plants do have a negative impact, but that the effect may not be as negative as previously thought. Specifically, our data show that pollinator richness increased with restorations via native plantings when controlling for time, and that pollinator abundance and Simpson’s diversity tended to be higher in the restored plots as well. However, the integration of invasive plant species into native networks may actually serve to make the native network more robust and resilient to changes in species composition (Memmott et al. 2004, Ferrero et al. 2013).

Our study shows that invasive plants become highly integrated into plant-pollinator networks, which has implications for managers. Specifically, we suggest that when removing invasive flowering plants, care should be taken to ensure that alternative forage is available for the pollinators that rely on those invasive plants within the appropriate phenological and spatial scales. Habitat restorations that involve planting native species should incorporate combinations of flowering plants that together provide a continuous source of floral resources for pollinators over the course of the season. Additionally, we suggest that flower morphology should also be considered in habitat restoration plans. Generalist native plants that have flowers with radial symmetry (e.g. Symphoricarpos albus, Rosa nutkana, and Rubus spectabilis in our study area) may serve to increase pollinator richness and overall network resilience.

AcknowledgementsAngela Fortune assisted with field and lab work, and Jennifer Avery assisted with the

plant analysis. Elizabeth Elle and David Green provided comments and supervision. Funding was provided by Metro Vancouver, the Environmental Youth Alliance, Simon Fraser University Biology department, and the Natural Sciences and Engineering Council (NSERC) of Canada.

Works Cited

Abraham, J. K., J. D. Corbin, and C. M. D. Antonio. 2009. California native and exotic perennial grasses differ in their response to soil nitrogen, exotic annual grass density, and order of emergence. Plant Ecology 201:445–456.

Aizen, M. A., C. L. Morales, and J. M. Morales. 2008. Invasive mutualists erode native pollination webs. Plos Biology 6:396–403.

Bartomeus, I., M. Vilà, and L. Santamaría. 2008. Contrasting effects of invasive plants in plant-pollinator networks. Oecologia 155:761–70.

Basilio, A. M., D. Medan, J. P. Torretta, and N. J. Bartoloni. 2006. A year-long plant-pollinator network. Austral Ecology 31:975–983.

Bosch, J., J. Retana, X. Cerdá, and S. Url. 1997. International Association for Ecology Flowering Phenology, Floral Traits and Pollinator Composition in a Herbaceous Mediterranean Plant Community. Pecologia 109:583–591.

Burkle, L. a, and R. Alarcón. 2011. The future of plant-pollinator diversity: understanding interaction networks across time, space, and global change. American Journal of Botany 98:528–38.

Cane, J. H., R. L. Minckley, L. J. Kervin, T. H. Roulston, and N. M. Williams. 2006. Complex responses within a desert bee guild (Hymenoptera: Apiformes) to urban habitat fragmentation. Ecological applications : a publication of the Ecological Society of America 16:632–44.

Carvell, C., W. R. Meek, R. F. Pywell, D. Goulson, and M. Nowakowski. 2007. Comparing the efficacy of agri-environment schemes to enhance bumble bee abundance and diversity on arable field margins. Journal of Applied Ecology 44:29–40.

Chittka, L., and S. Schürkens. 2001. Successful invasion of a floral market. Nature 411:653.Dormann, C. F., G. B, and F. J. 2008. Introducing the bipartite Package: Analysing Ecological

Networks. R news 8:8–11.Elle, E., S. L. Elwell, and G. A. Gielens. 2012. The use of pollination networks in conservation.

Botany 90:525–534.Ferrero, V., S. Castro, J. Costa, P. Acuña, L. Navarro, and J. Loureiro. 2013. Effect of invader

removal: pollinators stay but some native plants miss their new friend. Biological Invasions 15:2347–2358.

Forup, M. L., and J. Memmott. 2005. The Restoration of Plant-Pollinator Interactions in Hay Meadows. Restoration Ecology 13:265–274.

Godoy, O., D. M. Richardson, F. Valladares, and P. Castro-Díez. 2009. Flowering phenology of invasive alien plant species compared with native species in three Mediterranean-type ecosystems. Annals of Botany 103:485–94.

Gotlieb, A., Y. Hollender, and Y. Mandelik. 2011. Gardening in the desert changes bee communities and pollination network characteristics. Basic and Applied Ecology 12:310–320.

Greenleaf, S. S., N. M. Williams, R. Winfree, and C. Kremen. 2007. Bee foraging ranges and their relationship to body size. Oecologia 153:589–96.

Hennig, E. I., and J. Ghazoul. 2011. Pollinating animals in the urban environment. Urban Ecosystems 15:149–166.

Hierro, J. L., D. Villarreal, Ö. Eren, J. M. Graham, and R. M. Callaway. 2006. Disturbance Facilitates Invasion: The effects are stronger abroad than at home. The American Naturalist 168:144–156.

Hopwood, J. L. 2008. The contribution of roadside grassland restorations to native bee conservation. Biological Conservation 141:2632–2640.

Kaiser-Bunbury, C. N., T. Valentin, J. Mougal, D. Matatiken, and J. Ghazoul. 2011. The tolerance of island plant-pollinator networks to alien plants. Journal of Ecology 99:202–213.

Kneitel, J. M., and D. Perrault. 2006. Disturbance-induced changes in community composition increase species invasion success. Community Ecology 7:245–252.

Litt, A. R., and R. J. Steidl. 2010. Insect assemblages change along a gradient of invasion by a nonnative grass. Biological Invasions 12:3449–3463.

Lopezaraiza-Mikel, M. E., R. B. Hayes, M. R. Whalley, and J. Memmott. 2007. The impact of an alien plant on a native plant-pollinator network: an experimental approach. Ecology letters 10:539–50.

Matteson, K. C., J. S. Ascher, and G. A. Langellotto. 2008. Bee Richness and Abundance in New York City Urban Gardens Bee Richness and Abundance in New York City Urban Gardens. Conservation Biology and Biodiversity 101:140–150.

Matteson, K. C., and G. A. Langellotto. 2011. Small scale additions of native plants fail to increase beneficial insect richness in urban gardens. Insect Conservation and Diversity 4:89–98.

McKinney, A. M., and K. Goodell. 2010. Plant–pollinator interactions between an invasive and native plant vary between sites with different flowering phenology. Plant Ecology 212:1025–1035.

Memmott, J., and N. M. Waser. 2002. Integration of alien plants into a native flower-pollinator visitation web. Proceedings. Biological sciences / The Royal Society 269:2395–9.

Montoya, D., L. Rogers, and J. Memmott. 2012. Emerging perspectives in the restoration of biodiversity-based ecosystem services. Trends in Ecology and Evolution 27:666–672.

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.

O’Toole, C., and A. Raw. 2004. Bees of the world. Pages 1–192. Cassell Illustrated, London.Ollerton, J., R. Winfree, and S. Tarrant. 2011. How many flowering plants are pollinated by

animals? Oikos 120:321–326.Potts, S. G., B. Vulliamy, S. Roberts, C. O’Toole, a Dafni, G. Ne’Eman, and P. Willmer. 2005.

Role of nesting resources in organising diverse bee communities in a Mediterranean landscape. Ecological Entomology 30:78–85.

Potts, S. G., B. Vulliamy, S. Roberts, C. O’Toole, A. Dafni, G. Ne’eman, and P. G. Willmer. 2004. Nectar resource diversity organises flower-visitor community structure. Entomologia Experimentalis et Applicata 113:103–107.

Thébault, E., and C. Fontaine. 2010. Stability of ecological communities and the architecture of mutualistic and trophic networks. Science 329:853–6.

Traveset, A., and D. M. Richardson. 2006. Biological invasions as disruptors of plant reproductive mutualisms. Trends in ecology & evolution 21:208–16.

Valdovinos, F. S., R. Ramos-Jiliberto, J. D. Flores, C. Espinoza, and G. López. 2009. Structure and dynamics of pollination networks: the role of alien plants. Oikos 118:1190–1200.

Williams, N. M. 2011. Restoration of Nontarget Species: Bee Communities and Pollination Function in Riparian Forests. Restoration Ecology 19:450–459.

Figures and Tables

Figure captions:Figure 1: Map of study sites. Each site included a pair of plots, one restored and one non-restored. Figure 2: Plant and pollinator abundance, richness, and Simpson’s diversity index for restored and non-restored plots averaged across sites. * indicates marginally non-significant results (p<0.10), and ** indicates significant results (p<0.05).Figure 3: Average floral abundance and richness over time. Figure 4: Average pollinator abundance and richness over timeFigure 5: Nestedness, asymmetry, and the Specialization index (H2) for restored and non-restored plots averaged across sites. * indicates marginally non-significant results (p<0.10), and ** indicates significant results (p<0.05).

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Table 1: List of Sites

Site Site Code Plot Shape UTM Year of restoration

Distance between

plotsDelta Heritage Air

ParkDP Hedgerow 49°04’44.15”N

122°56’16.16”W 2005 120m

Centennial Beach BB-1 Polygon 49°00’57.15”N123°02’28.33”W 2013 165m

Boundary Bay Regional Park BB-2 Polygon 49°01’02.55”N

123°03’07.59”W Late 1990s 380m

Pacific Spirit Park-Camosun Bog PSC Polygon 49°15’13.54”N

123°11’46.24”W 2010 30m

Pacific Spirit Park (near the Museum of

Anthropology)PSM Hedgerow 49°16’14.86”N

123°15’32.20”W 2006-2007 440m

Oak Meadows Park OM Polygon 49°14’17.67”N123°07’34.34”W 2013 70m

Aldergrove Regional Park

AG Hedgerow 49°00’34.21”N122°27’03.72”W 2002-2003 100m

Brae Island Regional Park

BI Hedgerow 49°10’30.90”N122°34’48.55”W 2007 190m

Campbell Valley Regional Park

CV Hedgerow 49°01’03.15”N122°39’48.44”W 2002-2004 60m

Colony Farm Regional Park-2

CF-2 Hedgerow 49°14’21.46”N122°47’49.64”W 2007 300m

Colony Farm Regional Park-1

CF-1 Hedgerow 49°14’27.41”N122°48’30.74”W 1999 120m

Tynehead Regional Park

TH Polygon 49°11’02.30”N122°44’59.36”W 2012 260m

Appendix A: Floral unit designations by species.

Latin Name Common Name Floral Unit DesignationAchilliea sp. InflorescenceAchillea millefolium Yarrow InflorescenceAgoseris aurantiaca Mountain dandelion InflorescenceAllium sativum Garlic InflorescenceAmelanchier alnifolia Saskatoon IndividualAnaphalis margaritacea Pearly everlasting InflorescenceAnthemis sp. InflorescenceArtemisia sp. InflorescenceArctostaphylos uva-ursi Common bearberry IndividualBarbarea orthoceras American winter cress InflorescenceBellis perennis Lawn daisy IndividualBorago officinalis Borage IndividualBrassica campestris Field mustard InflorescenceBuddleja davidii Butterfly bush InflorescenceCapsella bursa-pastoris Shepherd's purse InflorescenceCampanula IndividualCakile maritima Sea rocket IndividualCardamine oligosperma Little western bittercress InflorescenceCerastium arvense Field chickweed IndividualCerastium glomeratum Sticky mouse-ear chickweed IndividualCerastium semidecandrum Small mouse-ear chickweed IndividualChamerion angustifolium Fireweed InflorescenceCichorium intybus Chicory IndividualClarkia unguiculata Clarkia IndividualCleome serrulata Rocky Mountain Beeplant InflorescenceClaytonia perfoliata Miner`s lettuce InflorescenceClaytonia siberica Siberian miner`s lettuce InflorescenceCornus nuttallii Western dogwood IndividualCollinsia parviflora Blue-eyed mary InflorescenceConvolvulus sepium Hedge bindweed IndividualCornus stolonifera Red-osier dogwood InflorescenceCraetaegus douglasii Black hawthorn InflorescenceCrataegus monogyna Common hawthorn InflorescenceCytisus scoparius Scotch broom Inflorescence (branch)Digitalis purpurea Foxglove InflorescenceDoronicum sp. Yellow daisy IndividualEpilobium ciliatum Fringed willowherb IndividualErysimum cheiranthoides Wormseed mustard InflorescenceErodium cicutarium Common stork's bill IndividualEryngium sp. Sea holly InflorescenceEschscholzia californica California poppy IndividualFragaria chiloensis Coastal strawberry IndividualGalium aparine Cleavers IndividualGaultheria shallon Salal InflorescenceGaleopsis tetrahit Common hemp-nettle IndividualGeum aleppicum Yellow avens IndividualGeum macrophyllum Large-leaved avens IndividualGeranium robertianum Robert Geranium IndividualGlechomo hederacea Ground ivy IndividualGrindelia integrifolia Entire-leaved gumweed IndividualHesperis matronalis Dame's rocket InflorescenceHieracium aurantiacum European hawkweed InflorescenceHolodiscus discolor Ocean spray Inflorescence

Hyacinthoides Bluebells InflorescenceHypericum anagalloides Bog St. John's wort IndividualHypochaeris radicata Hairy cats ear IndividualImpatiens parviflora Small flowered touch me not IndividualLactuca muralis Wall lettuce InflorescenceLathyrus palustris Marsh peavine IndividualLamium purpureum Deadnettle InflorescenceLepidium densiflorum Pepperweed InflorescenceLeucanthemum vulgare English daisy IndividualLinaria vulgaris Butter-and-eggs InflorescenceLotus corniculatus Bird's foot trefoil InflorescenceLonicera unvolucrata Black twinberry InflorescenceLupinus arcticus Artic Lupin InflorescenceLysimachia punctata PSC tall yellow IndividualMahonia aquifolium Tall oregon grape InflorescenceMachaeranthera bigelovii Bigelow's aster InflorescenceMatricaria discoidea Pineapple weed IndividualMalus sp. Apple InflorescenceMahonia nervosa Dull oregon grape InflorescenceMelilotus alba White sweet clover InflorescenceMentha arvensis Field mint InflorescenceMedicago lupulina Black medic InflorescenceMonarda didyma Bee balm IndividualMontia linearis Narrow-leaved montia InflorescenceMyosotis discolour Common forget-me-not InflorescenceOemleria cerasiformis Indian plum InflorescenceOrnithogalum sp. Star of Bethlehem IndividualParentucellia viscosa Yellow parentucellia InflorescencePhacelia campanularia California bluebell IndividualPhysocarpus capitatus Pacific ninebark InflorescencePhuopsis stylosa Caucasian crosswort InflorescencePhacelia tanacetifolia Lacy phacelia InflorescencePlantago lanceolata English plantain InflorescencePotentilla anserina Silverweed IndividualPolygonum cuspidatum Japanese knotweed InflorescencePolygonum douglassi Douglas' Knotweed InflorescencePolygonum lapathifolium Curlytop knotweed InflorescencePolygonum persicaria Spotted ladysthumb InflorescencePrunus emarginata Bitter cherry InflorescencePrunus laurocerasus Cherry laurel InflorescencePrunella vulgaris Self-heal InflorescenceRanunculus acris Meadow buttercup IndividualRanunculus repens Creeping buttercup IndividualRibes sanguineum Red-flowering currant InflorescenceRosa gymnocarpa Dwarf rose IndividualRosa nutkana Nootka rose IndividualRosa rugosa Garden rose IndividualRubus discolor Himalayan blackberry IndividualRudbeckia fulgida Black eyed susan IndividualRubus laciniatus Evergreen blackberry IndividualRubus parviflora Thimbleberry IndividualRubus spectabilis Salmonberry IndividualRubus ursinus Trailing blackberry IndividualSambucus racemosa Red elderberry InflorescenceStellaria graminea Common stickwort IndividualSenecio sylvaticus Wood groundsel InflorescenceSisyrinchium idahoense Blue eyed grass IndividualSisymbrium officinale Hedge mustard InflorescenceSorbus aucuparia European mountain ash Inflorescence

Sonchus arvensis Smooth asper IndividualSolanum dulcamara European bittersweet IndividualSonchus oleraceus Pale asper InflorescenceSpiraea douglasii Hardhack InflorescenceSpiraea sp. InflorescenceStachys Cooleyae Colley's hedge-nettle InflorescenceStachys mexicana Mexican hedge-nettle InflorescenceSymphoricarpos albus Common snowberry InflorescenceSymphytum sp. Comfrey InflorescenceTaraxacum officinale Common Dandelion InflorescenceTanacetum vulgare Common tansy InflorescenceTellima grandiflora Fringecup InflorescenceThlaspi arvense Field penny cress InflorescenceTiarella trifoliata Foamflower InflorescenceTrifolium incarnatum Crimson clover InflorescenceTrifolium pratense Red clover InflorescenceTrifolium repens White clover InflorescenceVaccinium parvifolium Red huckleberry InflorescenceVeronica beccabunga spp. Americana

American brooklimeInflorescence

Veronica serpyllifolia Speedwell InflorescenceVicia americanum American vetch InflorescenceVicia cracca Tufted vetch InflorescenceVicia hirsuta Tiny vetch InflorescenceViguiera multiflora Showy goldeneye InflorescenceVicia sativa Common vetch InflorescenceViburnum trilobum Highbush cranberry Inflorescence

Appendix B: Table of plant and pollinator abundance, richness, and Simpson’s diversity index (D), and plant-pollinator interaction metrics: nestedness, asymmetry, and the specialization index (H2’).

Site Treatment Type

Plants Pollinators Network metricsAbundance Richness Diversity Abundance Richness Diversity Nestedness Asymmetry H2'

Aldergrove Regional ParkControl 533 5 0.5031 157 13 0.17 46.82 0.02 0.29

Restored 657 18 0.8751 231 30 0.72 14.55 0.07 0.59

Boundary Bay Regional Park (Centennial Beach)

Control 1777 25 0.8326 122 30 0.71 19.37 0.12 0.59Restored 1389 31 0.8777 245 52 0.83 10.07 0.08 0.42

Boundary Bay Regional Park (old field)Control 114 10 0.7804 106 19 0.84 31.12 0.44 0.83

Restored 1349 14 0.7529 118 19 0.84 22.69 0.04 0.50

Brae Island Regional ParkControl 574 14 0.7373 85 18 0.90 19.96 0.32 0.40

Restored 373 10 0.6941 71 19 0.72 30.10 0.32 0.68

Colony Farm Regional Park (Hedgerow)Control 555 4 0.3069 128 27 0.71 9.87 0.04 0.49

Restored 608 9 0.8217 58 14 0.87 27.70 -0.01 0.53

Colony Farm Regional Park (near the Vancouver Avian Research Center)

Control 911 19 0.6917 99 15 0.79 34.28 0.30 0.33Restored 871 15 0.5856 80 17 0.80 26.10 -0.04 0.55

Campbell Valley Regional ParkControl 2139 16 0.7973 99 24 0.61 33.73 0.03 0.30

Restored 440 11 0.822 128 22 0.78 22.40 -0.07 0.34

Delta Heritage Air ParkControl 930 4 0.6709 63 8 0.86 34.18 0.06 0.38

Restored 818 16 0.7657 132 22 0.83 16.08 0.02 0.56

Oak Meadows ParkControl 1454 14 0.7771 106 34 0.88 15.43 0.08 0.45

Restored 532 30 0.9371 114 22 0.91 9.82 -0.11 0.44

Pacific Spirit Park (near the Museum of Anthropology)

Control 535 3 0.1458 55 22 0.86 24.76 0.28 0.55Restored 2940 14 0.556 291 42 0.78 15.85 0.05 0.46

Pacific Spirit Park (Camosun Bog)Control 607 14 0.7363 111 19 0.93 25.57 0.41 0.41

Restored 697 28 0.8031 134 22 0.79 8.14 0.03 0.50

Tynehead Regional ParkControl 1694 22 0.659 296 40 0.88 10.47 0.05 0.52

Restored 342 24 0.8 218 38 0.89 11.15 -0.04 0.36Control Average 985.25 12.5 0.64 118.92 22.42 0.76 25.46 0.18 0.46

Restored Average 918 18.33 0.77 151.67 26.58 0.81 17.89 0.03 0.49