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Independent Study Semester
How do habitat restorations affect plants and pollinators in Metro Vancouver Parks?
Hannah Gehrels
For Elizabeth Elle and David Green
December 9, 2013
Abstract
Anthropogenic 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
Introduction
Anthropogenic 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 Area
We 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 sampling
Only 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 sampling
We 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 analysis
We 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 diversity
Plant 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 diversity
We 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 metrics
Nestedness 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 Pollinators
Restorations 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 networks
Asymmetry 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.
Acknowledgements
Angela 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.
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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 time
Figure 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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Late
August
Averagefloralspeciesrichnesspersite
Time
0
50
100
150
200
250
300
350
Averagenumberofflowerspersite
Restored
Control
0
5
10
15
20
25
30
35
40
Averagenumberofpollinatorspersiteovertime
Restored
Control
0
2
4
6
8
10
12
Late April Early
May
Late May Early
June
Late June Early July Late July Early
August
Late
August
Averagepollinatorrichnesspersiteovertime
Time
0
5
10
15
20
25
30
35
AverageNestedness
0
0.05
0.1
0.15
0.2
0.25
AverageAsymmetry
0
0.1
0.2
0.3
0.4
0.5
0.6
AverageSpecializationIndex
(H2')
Restored Control Restored Control Restored Control
* **
Table 1: List of Sites
Site Site Code Plot Shape UTM
Year of
restoration
Distance
between
plots
Delta Heritage Air
Park
DP
Hedgerow
49°04’44.15”N
122°56’16.16”W
2005 120m
Centennial Beach BB-1 Polygon
49°00’57.15”N
123°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”N
123°07’34.34”W
2013 70m
Aldergrove Regional
Park
AG
Hedgerow
49°00’34.21”N
122°27’03.72”W
2002-2003 100m
Brae Island Regional
Park
BI
Hedgerow
49°10’30.90”N
122°34’48.55”W
2007 190m
Campbell Valley
Regional Park
CV
Hedgerow
49°01’03.15”N
122°39’48.44”W
2002-2004 60m
Colony Farm
Regional Park-2
CF-2
Hedgerow
49°14’21.46”N
122°47’49.64”W
2007 300m
Colony Farm
Regional Park-1
CF-1
Hedgerow
49°14’27.41”N
122°48’30.74”W
1999 120m
Tynehead Regional
Park
TH
Polygon
49°11’02.30”N
122°44’59.36”W
2012 260m
Appendix A: Floral unit designations by species.
Latin Name Common Name Floral Unit Designation
Achilliea sp. Inflorescence
Achillea millefolium Yarrow Inflorescence
Agoseris aurantiaca Mountain dandelion Inflorescence
Allium sativum Garlic Inflorescence
Amelanchier alnifolia Saskatoon Individual
Anaphalis margaritacea Pearly everlasting Inflorescence
Anthemis sp. Inflorescence
Artemisia sp. Inflorescence
Arctostaphylos uva-ursi Common bearberry Individual
Barbarea orthoceras American winter cress Inflorescence
Bellis perennis Lawn daisy Individual
Borago officinalis Borage Individual
Brassica campestris Field mustard Inflorescence
Buddleja davidii Butterfly bush Inflorescence
Capsella bursa-pastoris Shepherd's purse Inflorescence
Campanula Individual
Cakile maritima Sea rocket Individual
Cardamine oligosperma Little western bittercress Inflorescence
Cerastium arvense Field chickweed Individual
Cerastium glomeratum Sticky mouse-ear chickweed Individual
Cerastium semidecandrum Small mouse-ear chickweed Individual
Chamerion angustifolium Fireweed Inflorescence
Cichorium intybus Chicory Individual
Clarkia unguiculata Clarkia Individual
Cleome serrulata Rocky Mountain Beeplant Inflorescence
Claytonia perfoliata Miner`s lettuce Inflorescence
Claytonia siberica Siberian miner`s lettuce Inflorescence
Cornus nuttallii Western dogwood Individual
Collinsia parviflora Blue-eyed mary Inflorescence
Convolvulus sepium Hedge bindweed Individual
Cornus stolonifera Red-osier dogwood Inflorescence
Craetaegus douglasii Black hawthorn Inflorescence
Crataegus monogyna Common hawthorn Inflorescence
Cytisus scoparius Scotch broom Inflorescence (branch)
Digitalis purpurea Foxglove Inflorescence
Doronicum sp. Yellow daisy Individual
Epilobium ciliatum Fringed willowherb Individual
Erysimum cheiranthoides Wormseed mustard Inflorescence
Erodium cicutarium Common stork's bill Individual
Eryngium sp. Sea holly Inflorescence
Eschscholzia californica California poppy Individual
Fragaria chiloensis Coastal strawberry Individual
Galium aparine Cleavers Individual
Gaultheria shallon Salal Inflorescence
Galeopsis tetrahit Common hemp-nettle Individual
Geum aleppicum Yellow avens Individual
Geum macrophyllum Large-leaved avens Individual
Geranium robertianum Robert Geranium Individual
Glechomo hederacea Ground ivy Individual
Grindelia integrifolia Entire-leaved gumweed Individual
Hesperis matronalis Dame's rocket Inflorescence
Hieracium aurantiacum European hawkweed Inflorescence
Holodiscus discolor Ocean spray Inflorescence
Hyacinthoides Bluebells Inflorescence
Hypericum anagalloides Bog St. John's wort Individual
Hypochaeris radicata Hairy cats ear Individual
Impatiens parviflora Small flowered touch me not Individual
Lactuca muralis Wall lettuce Inflorescence
Lathyrus palustris Marsh peavine Individual
Lamium purpureum Deadnettle Inflorescence
Lepidium densiflorum Pepperweed Inflorescence
Leucanthemum vulgare English daisy Individual
Linaria vulgaris Butter-and-eggs Inflorescence
Lotus corniculatus Bird's foot trefoil Inflorescence
Lonicera unvolucrata Black twinberry Inflorescence
Lupinus arcticus Artic Lupin Inflorescence
Lysimachia punctata PSC tall yellow Individual
Mahonia aquifolium Tall oregon grape Inflorescence
Machaeranthera bigelovii Bigelow's aster Inflorescence
Matricaria discoidea Pineappleweed Individual
Malus sp. Apple Inflorescence
Mahonia nervosa Dull oregon grape Inflorescence
Melilotus alba White sweet clover Inflorescence
Mentha arvensis Field mint Inflorescence
Medicago lupulina Black medic Inflorescence
Monarda didyma Bee balm Individual
Montia linearis Narrow-leaved montia Inflorescence
Myosotis discolour Common forget-me-not Inflorescence
Oemleria cerasiformis Indian plum Inflorescence
Ornithogalum sp. Star of Bethlehem Individual
Parentucellia viscosa Yellow parentucellia Inflorescence
Phacelia campanularia California bluebell Individual
Physocarpus capitatus Pacific ninebark Inflorescence
Phuopsis stylosa Caucasian crosswort Inflorescence
Phacelia tanacetifolia Lacy phacelia Inflorescence
Plantago lanceolata English plantain Inflorescence
Potentilla anserina Silverweed Individual
Polygonum cuspidatum Japanese knotweed Inflorescence
Polygonum douglassi Douglas' Knotweed Inflorescence
Polygonum lapathifolium Curlytop knotweed Inflorescence
Polygonum persicaria Spotted ladysthumb Inflorescence
Prunus emarginata Bitter cherry Inflorescence
Prunus laurocerasus Cherry laurel Inflorescence
Prunella vulgaris Self-heal Inflorescence
Ranunculus acris Meadow buttercup Individual
Ranunculus repens Creeping buttercup Individual
Ribes sanguineum Red-flowering currant Inflorescence
Rosa gymnocarpa Dwarf rose Individual
Rosa nutkana Nootkarose Individual
Rosa rugosa Garden rose Individual
Rubus discolor Himalayan blackberry Individual
Rudbeckia fulgida Black eyed susan Individual
Rubus laciniatus Evergreen blackberry Individual
Rubus parviflora Thimbleberry Individual
Rubus spectabilis Salmonberry Individual
Rubus ursinus Trailing blackberry Individual
Sambucus racemosa Red elderberry Inflorescence
Stellaria graminea Common stickwort Individual
Senecio sylvaticus Wood groundsel Inflorescence
Sisyrinchium idahoense Blue eyed grass Individual
Sisymbrium officinale Hedge mustard Inflorescence
Sorbus aucuparia European mountain ash Inflorescence
Sonchus arvensis Smooth asper Individual
Solanum dulcamara European bittersweet Individual
Sonchus oleraceus Pale asper Inflorescence
Spiraea douglasii Hardhack Inflorescence
Spiraea sp. Inflorescence
Stachys Cooleyae Colley's hedge-nettle Inflorescence
Stachys mexicana Mexican hedge-nettle Inflorescence
Symphoricarpos albus Common snowberry Inflorescence
Symphytum sp. Comfrey Inflorescence
Taraxacum officinale Common Dandelion Inflorescence
Tanacetum vulgare Common tansy Inflorescence
Tellima grandiflora Fringecup Inflorescence
Thlaspi arvense Field penny cress Inflorescence
Tiarella trifoliata Foamflower Inflorescence
Trifolium incarnatum Crimson clover Inflorescence
Trifolium pratense Red clover Inflorescence
Trifolium repens White clover Inflorescence
Vaccinium parvifolium Red huckleberry Inflorescence
Veronica beccabunga spp.
Americana
American brooklime
Inflorescence
Veronica serpyllifolia Speedwell Inflorescence
Vicia americanum American vetch Inflorescence
Vicia cracca Tufted vetch Inflorescence
Vicia hirsuta Tiny vetch Inflorescence
Viguiera multiflora Showy goldeneye Inflorescence
Vicia sativa Common vetch Inflorescence
Viburnum 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 metrics
Abundance Richness Diversity Abundance Richness Diversity Nestedness Asymmetry H2'
Aldergrove Regional Park
Control 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 0.59
Restored 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 Park
Control 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 0.33
Restored 871 15 0.5856 80 17 0.80 26.10 -0.04 0.55
Campbell Valley Regional Park
Control 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 Park
Control 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 Park
Control 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 0.55
Restored 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 Park
Control 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 0.36
Control 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

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Hannah's ISS

  • 1. Independent Study Semester How do habitat restorations affect plants and pollinators in Metro Vancouver Parks? Hannah Gehrels For Elizabeth Elle and David Green December 9, 2013 Abstract Anthropogenic 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
  • 2. Introduction Anthropogenic 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
  • 3. 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 Area We 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 sampling Only 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 sampling We 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.
  • 4. Statistical analysis We 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 diversity Plant 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 diversity We 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)
  • 5. 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 metrics Nestedness 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 Pollinators Restorations 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
  • 6. 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 networks Asymmetry 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.
  • 7. 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. Acknowledgements Angela 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.
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  • 10. Williams, N. M. 2011. Restoration of Nontarget Species: Bee Communities and Pollination Function in Riparian Forests. Restoration Ecology 19:450–459.
  • 11. 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 time Figure 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).
  • 12.
  • 14. 0 1 2 3 4 5 6 7 8 9 10 Late AprilEarly May Late May Early June Late June Early July Late July Early August Late August Averagefloralspeciesrichnesspersite Time 0 50 100 150 200 250 300 350 Averagenumberofflowerspersite Restored Control
  • 15. 0 5 10 15 20 25 30 35 40 Averagenumberofpollinatorspersiteovertime Restored Control 0 2 4 6 8 10 12 Late April Early May Late May Early June Late June Early July Late July Early August Late August Averagepollinatorrichnesspersiteovertime Time
  • 17. Table 1: List of Sites Site Site Code Plot Shape UTM Year of restoration Distance between plots Delta Heritage Air Park DP Hedgerow 49°04’44.15”N 122°56’16.16”W 2005 120m Centennial Beach BB-1 Polygon 49°00’57.15”N 123°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”N 123°07’34.34”W 2013 70m Aldergrove Regional Park AG Hedgerow 49°00’34.21”N 122°27’03.72”W 2002-2003 100m Brae Island Regional Park BI Hedgerow 49°10’30.90”N 122°34’48.55”W 2007 190m Campbell Valley Regional Park CV Hedgerow 49°01’03.15”N 122°39’48.44”W 2002-2004 60m Colony Farm Regional Park-2 CF-2 Hedgerow 49°14’21.46”N 122°47’49.64”W 2007 300m Colony Farm Regional Park-1 CF-1 Hedgerow 49°14’27.41”N 122°48’30.74”W 1999 120m Tynehead Regional Park TH Polygon 49°11’02.30”N 122°44’59.36”W 2012 260m
  • 18. Appendix A: Floral unit designations by species. Latin Name Common Name Floral Unit Designation Achilliea sp. Inflorescence Achillea millefolium Yarrow Inflorescence Agoseris aurantiaca Mountain dandelion Inflorescence Allium sativum Garlic Inflorescence Amelanchier alnifolia Saskatoon Individual Anaphalis margaritacea Pearly everlasting Inflorescence Anthemis sp. Inflorescence Artemisia sp. Inflorescence Arctostaphylos uva-ursi Common bearberry Individual Barbarea orthoceras American winter cress Inflorescence Bellis perennis Lawn daisy Individual Borago officinalis Borage Individual Brassica campestris Field mustard Inflorescence Buddleja davidii Butterfly bush Inflorescence Capsella bursa-pastoris Shepherd's purse Inflorescence Campanula Individual Cakile maritima Sea rocket Individual Cardamine oligosperma Little western bittercress Inflorescence Cerastium arvense Field chickweed Individual Cerastium glomeratum Sticky mouse-ear chickweed Individual Cerastium semidecandrum Small mouse-ear chickweed Individual Chamerion angustifolium Fireweed Inflorescence Cichorium intybus Chicory Individual Clarkia unguiculata Clarkia Individual Cleome serrulata Rocky Mountain Beeplant Inflorescence Claytonia perfoliata Miner`s lettuce Inflorescence Claytonia siberica Siberian miner`s lettuce Inflorescence Cornus nuttallii Western dogwood Individual Collinsia parviflora Blue-eyed mary Inflorescence Convolvulus sepium Hedge bindweed Individual Cornus stolonifera Red-osier dogwood Inflorescence Craetaegus douglasii Black hawthorn Inflorescence Crataegus monogyna Common hawthorn Inflorescence Cytisus scoparius Scotch broom Inflorescence (branch) Digitalis purpurea Foxglove Inflorescence Doronicum sp. Yellow daisy Individual Epilobium ciliatum Fringed willowherb Individual Erysimum cheiranthoides Wormseed mustard Inflorescence Erodium cicutarium Common stork's bill Individual Eryngium sp. Sea holly Inflorescence Eschscholzia californica California poppy Individual Fragaria chiloensis Coastal strawberry Individual Galium aparine Cleavers Individual Gaultheria shallon Salal Inflorescence Galeopsis tetrahit Common hemp-nettle Individual Geum aleppicum Yellow avens Individual Geum macrophyllum Large-leaved avens Individual Geranium robertianum Robert Geranium Individual Glechomo hederacea Ground ivy Individual Grindelia integrifolia Entire-leaved gumweed Individual Hesperis matronalis Dame's rocket Inflorescence Hieracium aurantiacum European hawkweed Inflorescence Holodiscus discolor Ocean spray Inflorescence
  • 19. Hyacinthoides Bluebells Inflorescence Hypericum anagalloides Bog St. John's wort Individual Hypochaeris radicata Hairy cats ear Individual Impatiens parviflora Small flowered touch me not Individual Lactuca muralis Wall lettuce Inflorescence Lathyrus palustris Marsh peavine Individual Lamium purpureum Deadnettle Inflorescence Lepidium densiflorum Pepperweed Inflorescence Leucanthemum vulgare English daisy Individual Linaria vulgaris Butter-and-eggs Inflorescence Lotus corniculatus Bird's foot trefoil Inflorescence Lonicera unvolucrata Black twinberry Inflorescence Lupinus arcticus Artic Lupin Inflorescence Lysimachia punctata PSC tall yellow Individual Mahonia aquifolium Tall oregon grape Inflorescence Machaeranthera bigelovii Bigelow's aster Inflorescence Matricaria discoidea Pineappleweed Individual Malus sp. Apple Inflorescence Mahonia nervosa Dull oregon grape Inflorescence Melilotus alba White sweet clover Inflorescence Mentha arvensis Field mint Inflorescence Medicago lupulina Black medic Inflorescence Monarda didyma Bee balm Individual Montia linearis Narrow-leaved montia Inflorescence Myosotis discolour Common forget-me-not Inflorescence Oemleria cerasiformis Indian plum Inflorescence Ornithogalum sp. Star of Bethlehem Individual Parentucellia viscosa Yellow parentucellia Inflorescence Phacelia campanularia California bluebell Individual Physocarpus capitatus Pacific ninebark Inflorescence Phuopsis stylosa Caucasian crosswort Inflorescence Phacelia tanacetifolia Lacy phacelia Inflorescence Plantago lanceolata English plantain Inflorescence Potentilla anserina Silverweed Individual Polygonum cuspidatum Japanese knotweed Inflorescence Polygonum douglassi Douglas' Knotweed Inflorescence Polygonum lapathifolium Curlytop knotweed Inflorescence Polygonum persicaria Spotted ladysthumb Inflorescence Prunus emarginata Bitter cherry Inflorescence Prunus laurocerasus Cherry laurel Inflorescence Prunella vulgaris Self-heal Inflorescence Ranunculus acris Meadow buttercup Individual Ranunculus repens Creeping buttercup Individual Ribes sanguineum Red-flowering currant Inflorescence Rosa gymnocarpa Dwarf rose Individual Rosa nutkana Nootkarose Individual Rosa rugosa Garden rose Individual Rubus discolor Himalayan blackberry Individual Rudbeckia fulgida Black eyed susan Individual Rubus laciniatus Evergreen blackberry Individual Rubus parviflora Thimbleberry Individual Rubus spectabilis Salmonberry Individual Rubus ursinus Trailing blackberry Individual Sambucus racemosa Red elderberry Inflorescence Stellaria graminea Common stickwort Individual Senecio sylvaticus Wood groundsel Inflorescence Sisyrinchium idahoense Blue eyed grass Individual Sisymbrium officinale Hedge mustard Inflorescence
  • 20. Sorbus aucuparia European mountain ash Inflorescence Sonchus arvensis Smooth asper Individual Solanum dulcamara European bittersweet Individual Sonchus oleraceus Pale asper Inflorescence Spiraea douglasii Hardhack Inflorescence Spiraea sp. Inflorescence Stachys Cooleyae Colley's hedge-nettle Inflorescence Stachys mexicana Mexican hedge-nettle Inflorescence Symphoricarpos albus Common snowberry Inflorescence Symphytum sp. Comfrey Inflorescence Taraxacum officinale Common Dandelion Inflorescence Tanacetum vulgare Common tansy Inflorescence Tellima grandiflora Fringecup Inflorescence Thlaspi arvense Field penny cress Inflorescence Tiarella trifoliata Foamflower Inflorescence Trifolium incarnatum Crimson clover Inflorescence Trifolium pratense Red clover Inflorescence Trifolium repens White clover Inflorescence Vaccinium parvifolium Red huckleberry Inflorescence Veronica beccabunga spp. Americana American brooklime Inflorescence Veronica serpyllifolia Speedwell Inflorescence Vicia americanum American vetch Inflorescence Vicia cracca Tufted vetch Inflorescence Vicia hirsuta Tiny vetch Inflorescence Viguiera multiflora Showy goldeneye Inflorescence Vicia sativa Common vetch Inflorescence Viburnum trilobum Highbush cranberry Inflorescence
  • 21. 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 metrics Abundance Richness Diversity Abundance Richness Diversity Nestedness Asymmetry H2' Aldergrove Regional Park Control 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 0.59 Restored 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 Park Control 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 0.33 Restored 871 15 0.5856 80 17 0.80 26.10 -0.04 0.55 Campbell Valley Regional Park Control 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 Park Control 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 Park Control 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 0.55 Restored 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 Park Control 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 0.36 Control 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