Comparing Abundance of Flower Visiting to bakeri, vinculans, and burkei in Natural and Constructed Vernal Pools

By Kandis Gilmore

A thesis submitted to Sonoma State University in partial fulfillment of the requirements for the degree of MASTER OF SCIENCE in Biology

Committee Members:

Dr. Nathan Rank, Chair

Dr. Christina Sloop

Dr. Caroline Christian

January 19, 2018

i

Copyright 2018 By Kandis Gilmore

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Authorization for Reproduction of Master’s Thesis

I grant permission for the print or digital reproduction of parts of this thesis without further authorization from me, on the condition that the person or agency requesting reproduction absorb the cost and provide proper acknowledgment of authorship.

Date: January 19, 2018 Kandis Gilmore

iii Comparing Abundance of Flower Visiting Insects to , , and in Natural and Constructed Vernal Pools

Thesis by Kandis Gilmore

ABSTRACT

Purpose of the Study: The purpose of this study was to investigate whether artificially constructed habitats provide adequate pollination services to the three federally endangered vernal pool endemic : Sonoma sunshine (Blennosperma bakeri), Sebastopol meadowfoam (Limnanthes vinculans), and Burke’s goldfields (Lasthenia burkei). I compared visitation rates by insects to flowers in natural vernal pools to visitation rates to flowers in constructed pools on the Santa Rosa Plain.

Procedure: To assess flower visitation by insects, I conducted timed observations in the field at natural and constructed vernal pool sites. I collected specimens directly from flowers using nets and I sampled local flower visiting insects using pan traps. I identified bees and flies to the species level and compared abundance across sites and habitat types. I calculated the map distance from each population to its nearest neighboring populations and compared visitation rates according to degree of geographic isolation.

Findings: Solitary ground nesting bee species were found to be associated with each plant species, and Conophorus cristatus, a bombyliid fly, was strongly associated with Burke’s goldfields. The rate of visitation to Sonoma sunshine was significantly higher in natural pools and gradually increased across the season in constructed pools. Sebastopol meadowfoam was visited predominately by its specialist bee, pulverea, in both habitat types. Visitation rates to Burke’s goldfields were driven mainly by the C. cristatus. Overall, plants in constructed pools located near natural populations received more insect visits than those farther away.

Conclusions: Sonoma sunshine (B. bakeri) is visited by the most diverse group of insects, which could protect against loss of one pollinator species. However, it is also the most vulnerable due to seasonal variation in insect visitation and its early blooming time. Pollinators of Sebastopol meadowfoam (L. vinculans) are abundant and widespread. While there were relatively few specialist bees found associated with Burke’s goldfields, bombyliid flies may act as a suitable pollinator for this species. Overall, constructed vernal pools are not devoid of flower visiting insects, yet the difference between natural and constructed sites suggests that planning for insect pollinators and proximity to natural sites is critical when constructing new habitat for vernal pool plants.

MS Program: Biology Sonoma State University Date: January 19, 2018

iv Acknowledgments

First and foremost, I acknowledge Dr. Christina Sloop as the originator of the larger research project under which this work is included. Without her pioneering spirit and commitment to conservation science, this project would not have gotten started. I would like to thank Hattie Brown for logistical guidance and camaraderie in the field. Dr. Caroline Christian’s comments greatly improved my methods and writing. Many thanks to Dr. Nathan Rank for his invaluable assistance with project planning, statistics, feedback on writing, and moral support. I would like to thank the staff of the Foundation for their logistical support. I acknowledge the Entomology service learning students who spent time performing insect observations, and undergraduate interns who assisted with pinning insects. I thank the California Department of Fish and Wildlife for access to their vernal pool preserves as well as numerous private landowners who welcomed me and my team. Dr. Robbin Thorp and Dr. Martin Hauser generously assisted with making final species determinations on numerous insect specimens. I am grateful to Sarah Gordon and Michelle (Jensen) Halbur for providing information on plant population locations. Gratitude to Bob Holland, Carol Witham, Matt Guilliams, and Joe Silveira for welcoming me into the larger circle of vernal pool researchers across the state. Thank you to my lab mates Frederique Lavoipierre, Sarah Heidl, Christine Colijn, and Kevin Roberts, and to the many undergraduates who assisted in the field and in the lab. Most importantly, I acknowledge my family for their undying love and support.

This work was funded by a grant from the US Fish and Wildlife Service, and I received additional support from the California Native Plant Society, Milo Baker Chapter, and Sonoma State University’s Graduate Equity Fellowship.

v Table of Contents

Page List of Tables vii

List of Figures viii

Introduction 1

Methods 5

Results 12

Discussion 14

Conclusion 19

Literature Cited 20

Tables 24

Figures 34

Appendix 1: List of species collected 46

vi List of Tables

Table 1: List of study sites …………………………………………………………..p. 24

Table 2: The results from a permutational analysis of covariance testing the effects of insect category, pool type, and site on visitation rates to Blennosperma bakeri with day of year as a covariate………………………………………………………………..……p. 25

Table 3: Results from a permutational analysis of covariance testing the effects of insect category, pool type, and site on visitation rates to Limnanthes vinculans with day of year as a covariate. …………………………………………………………………..……..p. 26

Table 4: Results from a permutational analysis of covariance testing the effects of insect category, pool type, site, and year on visitation rates to Lasthenia burkei with day of year as a covariate. ………………………………………………………………..………..p. 27

Table 5: Results from an analysis of covariance testing the effects of pool type, plant species, and distance to nearest neighbor on visitation rates to the three plant species, with distance to nearest neighbor as a covariate………………………………..….….p. 28

Table 6. Mean number of specimens of the major pollinator taxa collected in constructed and natural pools……………………………………………………………….….….p. 29

Table 7. Results from a permutational analysis of variance testing the effects of insect category, pool type, site, and pool on the abundance of insect specimens collected by net sweeps over flowering patches of B. bakeri, and pan trapped insects collected near the same flowering patch………………………………………………..………….…..…p. 30

Table 8: Results from a permutational analysis of variance testing the effects of insect category, pool type, site, and pool on the abundance of insect specimens collected by net sweeps over flowering patches of L. vinculans, and of pan trapped insects collected near the same flowering patch.………………………………………………..……….…...p. 31

Table 9: Results from a permutational analysis of variance testing the effects of insect category, pool type, site, pool, and year on the abundance of insect specimens collected by net sweeps over flowering patches of La. burkei……….………………………….p. 32

Table 10: Results from a permutational analysis of variance testing the effects of insect category, pool type, site, and pool on the abundance of insect specimens collected from pan traps set out near flowering patches of La. burkei in 2010………………...……..p. 33

vii List of Figures

Figure 1. Map of study site locations…………………………………………………p. 34

Figure 2. Date ranges of sampling efforts for this study. …………………………….p. 35

Figure 3. Visitation rates across constructed and natural sites for B. bakeri…………p. 36

Figure 4. Plot showing the effect of day of year on visitation rates to B. bakeri by different insect categories………………………………………………………...…...p. 37

Figure 5. Visitation rates across constructed and natural sites for L. vinculans.……..p. 38

Figure 6. Plot showing the effect of day of year on visitation rates to L. vinculans by different insect categories……………………………………….………………….…p. 39

Figure 7. Visitation rates across constructed and natural sites for La. burkei………....p. 40

Figure 8. Plot showing the effect of day of year on visitation rates to La. burkei by different insect categories..……………………………………………………………p. 41

Figure 9. Figure showing results of an ANCOVA testing the visitation rates of solitary bees to the three plant species with distance to nearest neighboring population as a covariate. 9A: Visitation rates across constructed and natural sites for B. bakeri, L. vinculans, and L. burkei. 9B: Plot showing relationship between visitation rate and distance to neighbor……………………………………………………...……………p. 43

Figure 10. Mean of number of individual specimens collected by net and pan trapping across constructed and natural sites for B. bakeri. ……………………………………p. 44

Figure 11. Mean of number of individual specimens collected by net and pan trapping across constructed and natural sites for L. vinculans..……………………………...…p. 45

Figure 12. Mean of number of individual specimens collected by net and pan trapping across constructed and natural sites for L. burkei..…………………….…………..….p. 46

viii Introduction As human impacts on the planet have increased, natural habitats have been altered or destroyed, which has affected many plant and species. In the United States, the

Endangered Species Act of 1973 provides for conservation of species that are endangered or threatened with , and the conservation of the ecosystems on which they depend (Department of the Interior, 1973). Since the inception of the Endangered Species

Act, there have been numerous projects to restore or create new habitat for endangered species. In the case of flowering plants, once the new populations start flowering in transplanted populations, the hope is they will attract insect pollinators to help them reproduce in their new location. In the case of endangered plants, one strategy is transplanting populations to new locations near where their habitat has been degraded or destroyed. There are a number of issues and risks associated with this, including not being able to fully recreate all of the abiotic and biotic factors required for the new plant population to succeed in the long term (Howald, 1996).

Flowering plants have long benefitted from attracting insect pollinators to distribute their pollen. It is estimated that 48% of flowering plants are outcrossing species, being either self-incompatible or having higher fecundity with outcrossed pollen (Igic and Kohn, 2006). Many species of insects from multiple insect orders visit flowers and in principle pollen can be transferred from one plant to another whenever any insect visits a receptive flower after visiting a conspecific one with viable pollen (Fenster et al., 2004).

Bees (Order ) are considered the most important pollinator taxon as they have morphological features that gather pollen to provision their nests or colonies

(Greenleaf, 2007). While some bees forage for pollen on diverse species,

1 other bees specialize on gathering pollen from species within a family or genus (Cruden,

1971). These specialist bees rely on pollen and nectar from their host plants to provision their nests for the following generation.

Vernal pools are a type of seasonal characterized by depressions in the landscape underlain by an impermeable sub-soil, and a seasonally dry or wet

Mediterranean climate (Holland and Jain, 1977). Winter rains create a perched water table that fills the pool, which slowly empties by evaporation through late spring. This yearly cycle of flooding and drought creates a physiologically challenging environment in which many uniquely adapted plant species germinate underwater and grow through the winter, until drying of the pools triggers flowering throughout spring. Vernal pools are called islands of endemism, since their physical environment protects against invasion by most introduced plant species (Stone, 1990).

The Santa Rosa Plain is an 81,000-acre complex of , streams, and oak- savannah grasslands located in Sonoma County, in the North San Francisco Bay region of

California. Urbanization and agricultural expansion have destroyed 85% of the vernal pools that historically filled the landscape, resulting in a highly fragmented habitat

(CH2M Hill, 1995). Sonoma Sunshine (Blennosperma bakeri), Sebastopol Meadowfoam

(Limnanthes vinculans), and Burke’s Goldfields (Lasthenia burkei) are three Santa Rosa

Plain vernal pool endemic plants that are state and federally listed as endangered (Federal

Register, 1992). Each has an annual life cycle with a blooming period of six to eight weeks.

Mitigation requirements related to the “no net loss” wetland policy and the

Endangered Species Act have led to the creation of many vernal pools on mitigation sites

2 throughout the Santa Rosa Plain since 1989 (Robertson, 2000; CH2M Hill, 1995). As part of the conservation strategy for the three endangered vernal pool plant species, seeds were planted in constructed vernal pools to increase the number of plant populations.

Generally, conservation practitioners consider these constructed pools to be successful if the relocated seeds germinate for three growing seasons. However, this short-term monitoring may not be enough to ensure long-term sustainability of these new populations (CH2M Hill, 1995; FWS, 2005.)

I propose that a component for long-term reproductive success in annual plants is the ecological relationship with their associated pollinators (Davis 1998; Fontaine, et. al,

2006; Kearns, et. al. 1998). All three species are predominately outcrossing, with seeds set in enclosed producing mostly non-viable seeds (Sloop et al., 2012). In all three species, flowers produced more seeds when available to insect visitors, generating between 2.5 and five times more seeds compared to inflorescences that had pollinators excluded. Given that insect visitation plays an important role in the reproductive success of these endangered plant species, it is important to investigate and discern the identity, abundance, and distribution of their insect visitors and main pollinators.

Prior studies in the Central Valley of California, showed that other Lasthenia,

Limnanthes and Blennosperma species rely on pollination from specialized bee pollinators (Thorp and Leong, 1998). Thorp (1969) described two species of solitary bees

Andrena submoesta, and A. puthua that appear to collect pollen exclusively from flowers of the genus Lasthenia. Predominant pollination for the genus Limnanthes is carried out by the specialist solitary bee A. pulverea. Known pollinators of B. bakeri are also in the

3 genus Andrena with A. blennospermatis as the specialist pollinator (Leong, et. al., 1995).

Other insects such as sweat bees (Family ), syrphid flies (Family Syrphidae), and numerous other insects also visit B. bakeri, and may contribute to its pollination

(Fontaine, et. al, 2006).

Because specialist bees have only one generation per year to gather nest provisions for the following generation, access to host plants is critical for the bees’ persistence

(Thorp and Leong, 1998). These specialist pollinators can therefore be particularly vulnerable to habitat loss and fragmentation. It remains uncertain whether specialist solitary bee pollinator populations are waning, given their main pollen source plants are endangered and their occurrences are in decline. If either plant or pollinator populations keep declining, an extinction vortex could ensue, taking with it both specialized species

(Gilpin and Soulé, 1986). Particularly, with ground nesting bees as central-place foragers, needing to return to their nest between foraging trips and therefore optimizing their foraging to reduce travel distance, the question remains whether isolation of a plant population negatively affects the frequency of bees visiting and pollinating endangered vernal pool plants.

In order to shed light on endangered vernal pool plant-pollinator interactions, pollinator status, and restoration efficacy on the Santa Rosa Plain vernal pool landscape, this study identifies the main pollinator(s) and pollinator communities of B. bakeri, L. vinculans and La. burkei, and compares insect visitation at natural versus constructed vernal pools. This study addresses the following questions:

1. Which types of pollinating insects visit the flowers of B. bakeri, L. vinculans, and La.

burkei in natural vs. constructed environments?

4 2. How does distance to neighboring conspecific plant occurrences affect pollinator

visitation rate at a given pool?

3. How does the community composition of flower visitors collected directly from each

plant species vary between natural and constructed vernal pools?

4. How does the community composition of visitors collected from pan traps placed

near vernal pools vary between natural and constructed pools?

Methods

Study System and Sampling Design

The three endangered plant species are endemic to the Santa Rosa Plain (Ornduff

1964, 1969a, and 1969b; CH2M Hill, 1995). Throughout the Santa Rosa Plain, there are a number of naturally occurring plant populations as well as populations planted in constructed vernal pools that were created for mitigation or conservation purposes

(CH2M Hill, 1995; FWS, 2005). Study sites cover the extent of the Santa Rosa Plain within the Laguna de Santa Rosa watershed and represent as many sites as possible given access permissions. Study sites vary with respect to proximity to urban environments, number of pools per site, proximity to other sites, and history of land management

(Figure 1). Some natural sites contained only one pool per site (See Table 1). Particularly constructed sites contained many pools on the same parcel. In order to capture variability within constructed sites, I chose pools for my study that were separated by at least 500 meters.

During 2010, I conducted timed observations, net collections, and pan trapping at six natural and six constructed pools for B. bakeri, and at five natural and five constructed pools for both L. vinculans and La. burkei. Each of these plant species has its

5 own peak bloom time, with B. bakeri blooming first, followed by L. vinculans and then L. burkei (See Figure 2 for date ranges of sampling). In 2011, I conducted timed observations and net collections at an additional three natural and four constructed sites containing La. burkei, and set out pan traps at sites that I did not sample in 2010.

Prior to conducting the work described in this thesis, I did a pilot study in the spring of 2009 where I conducted flower visitor observations to the three plant species over five-minute intervals at a variety of times during the day. I found that it took several minutes for the insects to start visiting flowers after habituating to the observer sitting nearby, so the following year I increased the observation interval to 10 minutes. I also found that if it was too cold (below 18oC), too early (before 9:30 am), or too windy (wind speed above 8 kph), insect visitation dropped drastically. I used this information to optimize my methods the following year, both for observations and for net collection of specimens. During the pilot study, I observed an array of insect visitors and created pollinator type categories for field identification. Most bees that visited the three focal plant species were two-thirds the size of a honeybee and resembled known pollen specialist Andrenid bees (Thorp, 1969). I called this category “solitary bee.” I was curious whether the generalist pollinator Apis mellifera would be a substitute in the absence of solitary bees, so I tracked honey bees as their own category, and identified syrphid flies as another category. I noticed that a small grey bombyliid fly was a frequent visitor to La. burkei flower heads and described this category of visitor for that plant species. There were occasional flower visits by hemipterans and small beetles, but those insects were predominately foraging on single flower heads and not moving from flower to flower.

6

Observations of floral visitation rate

I observed patches of flowering B. bakeri, L. vinculans, and La. burkei within a

0.5 m2 quadrat for 10-minute intervals. A California Native Plant Society chart, with cover categories of 5%, 10%, 25%, 35%, 50%, 75%, served to determine cover class of the target plant within the sampling quadrat. To avoid bias in selecting a quadrat location,

I haphazardly threw a pin flag backward over my shoulder, using its landing spot as the corner of the quadrat. For each observation, I focused on one particular plant species.

During the observations, I counted the number of times each type of insect made contact with the reproductive parts of a flower. In 2010, I conducted a minimum of 10 observation sessions per pool. In 2011, my efforts focused on La. burkei, and I conducted a minimum of 12 observation sessions per pool. The second year, I sampled eight pools at constructed sites and four pools at natural sites. I recorded the air temperature and wind speed at the beginning and end of each observation period.

I averaged the number of insect visits per visitor category during a 10-minute observation period for each day. The categories of insect visitors for B. bakeri and L. vinculans are solitary bee, syrphid fly, and honey bee. For La. burkei, there are four insect categories: solitary bee, syrphid fly, honey bee, and bombyliid fly.

The results showed a high proportion of zeros, causing an extremely skewed data distribution. In order to address this, I used Primer-Permanova, a statistical package robust to non-normal distributions. (Clarke and Gorley, 2006). Primer-Permanova measures distances between each data point and creates a resemblance matrix used to run permutations, resampling the data repeatedly until the results converge on a normal

7 distribution. However, Permanova requires the homogeneity of variance assumption to be valid, and therefore it is appropriate to transform the visitation rates before analysis with Permanova. Box-Cox transformations are used to find the ‘best transformation’ without an a-priori reason for choosing a particular transformation (Sokol and Rohlf,

1981). I used JMP v.12 to find the best transformation, adding 1 to each data point to make them non-zero, as typically done for log transformation. Using the Fit Model platform in JMP with expected mean squares (EMS) option, I ran a model testing the effects of the categorical variables. Using the factor profiling menu, I asked JMP to find the best transformation using the Box-Cox method. I applied this transformation to my y- variable and used those values in subsequent analyses.

I performed preliminary analyses to test for the effects of day of year, temperature, and wind speed on visitation rate. I found that day of year accounted for most of the variation and so included that in the final model. I then analyzed the data for observations using Primer-Permanova. I first created a resemblance matrix using Euclidian distances between data points, and then used the resemblance matrix to run a permutational analysis of covariance with day of year as the environmental covariate. I set the program to run 5000 permutations per analysis.

Effect of distance from a natural pool on visitation rate

I determined the location of neighboring populations of each plant species nearest to my study sites by consulting with local experts, the literature and the ‘Adopt a Vernal

Pool’ website (Sloop and Ayres, 2006; Sloop et al 2012, Halbur, et. al. 2014;

AVP 2017; Christina Sloop, Sarah Gordon, personal communication). For Blennosperma bakeri, I identified 14 occurrences, and including seven from my field work (Table 1).

8 For Limnanthes vinculans, I found 13 occurrences, including six from my field work

(Table 1). For Lasthenia burkei, I included 15 occurrences, seven of which were in my study (Table 1). I found that the distance from each pool in my study to its nearest neighbor ranged from 30 meters to 3.7 kilometers, with one outlier, Windsor Christian

Academy at 8 kilometers (Table 1). I excluded the Windsor site from further analysis.

Using Google Earth and the Laguna Foundation’s information (AVP, 2017), I obtained the geographic coordinates of each site. The Geographic Distance Matrix Generator helped me attain pairwise distances between each site (Ersts, 2017). Because of my focus on specialist pollinators, I measured distances between sites with the same plant species. I made a list of the distances between my study sites and neighboring populations within four kilometers. I calculated the mean visitation rate for solitary bees from each site and gathered data across all three plant species. After transforming the visitation rate and distance data using the Box-Cox method to meet the assumptions of normality and homogeneity of variance, I tested the effects of plant species, pool type, and distance to neighbor using an analysis of covariance (ANCOVA) in JMP Pro version 13. Since there was variability in the degree of isolation of sites, I ran a weighted regression. It could be that isolated sites attracted more insect visitors because local insects remained close to the concentrated floral resources, or conversely, sites surrounded by conspecific plant populations could attract a larger number of insects due to larger combined numbers of floral resources. To account for this variation between my study sites, I used the number of surrounding populations within a four-kilometer radius to each study site as a weighting factor.

9 Pollinator community visiting each focal plant

I collected insects visiting B. bakeri, L. vinculans, and La. burkei flowers with net sweeps during a timed 30-minute period at each pool where I conducted observations.

Based on the findings of my pilot study, I conducted net collecting when the temperature was above 18oC and wind speed less than 8 kph. Captured specimens were killed with ethyl acetate vapor or by freezing, and were pinned for identification and labeled with locality information.

I set out pan trap arrays at each site in 2010 and at the new sites in 2011. The pan trap arrays consisted of a 3x3 Latin square pattern of yellow, blue, and white plastic bowls with a bit of soapy water in the bottom, following the methods described in Leong and Thorp, 1999. I added soap to break the surface tension of the water, so that insects entering the bowl would not be able to climb out. The arrays were set out on dry ground directly adjacent to each sampling site. I collected contents of traps after 24 hours and stored specimens in alcohol for later processing where they were cleaned, dried, pinned, and labeled.

All collected specimens are kept in the research collections at the Sonoma State

University museum. Dr. Robbin Thorp at UC Davis made final species determinations of the bee specimens, and Dr. Martin Hauser at the California Department of Food and

Agriculture made final species determinations of the syrphid and bombyliid flies. I added the identified insect specimens to a database and created lists of total number of each species found at each sampling event. The comprehensive list of species collected can be found in Appendix 1.

10 I chose categories of insects for each plant species based on scientific literature and from observations in the field. There are several criteria bee researchers have used to create functional groups, choosing grouping factors such as nesting method, tongue length, or body size. A study by Kremen, et al. (2010) evaluated the effectiveness of citizen scientist observations by comparing records of observations with professional researchers’ specimen collection. They found that visual categorization of flower visitors in larger taxonomic groups accurately detected similar results when compared with specimens collected and identified by professionals. My categories are “solitary bees,”

“other bees,” honey bees, syrphid flies, and in the case of La. burkei, bombyliid flies.

“Solitary bees” consisted of the oligolectic pollen specialist for each respective plant species, plus four species of bees that resemble the specialist: A. angustitarsata, A. pensilis, Halictus tripartitus, and Lasioglossum titusi. This category was created to parallel the “solitary bee” category from my observations in the field. The “other bee” category included all other bees of various shapes and sizes. I took the sum of individuals found for each of these categories for each collecting event.

Data from net collections and pan traps were analyzed separately, as I found that a wider array of bees were attracted to the pan traps than I ever observed or collected from the focal plant species. Thus, the net collected specimens are more closely connected to the observational data, while the pan trap specimens are an indicator of the bees flying through the area using various available floral resources.

Using the number of species collected per category as a weighting factor, I generated Box-Cox best fit transformations using a simple statistical model for each flower species and collecting method. Using Primer-Permanova, I generated a

11 resemblance matrix using Euclidian distances between points for each dataset. Using this matrix, I tested the effect of pool type, site, insect category, pool, and day of year on the abundance of specimens collected. Since the collections were done in a condensed time span, it did not make sense to include day of year as a factor in the model. For net collected specimens from La. burkei, I included year as a factor in the model, as I collected in both years, 2010 and 2011.

Results

Observations of floral visitation rate

For B. bakeri, solitary bees visited the flowers in the greatest numbers (Table 2,

Figure 3). There was a difference in flower visitor rate between natural and constructed vernal pool habitats, and there was also significant variation between sites overall (Table

2). I saw visitors at a relatively high rate at natural pools early in the season, and saw fewer at constructed pools until later in the season when visitation rates increased (Figure

4). Differences in the timing of when the insects frequently visited the flowers is shown by the significant interaction of day and pool type (Table 2, Figure 4).

For L. vinculans, solitary bees were the most frequent visitor in both natural and constructed sites (Table 3, Figure 5). Day of year had a strong effect on visitation rate; as the season progressed, the solitary bee visitation rate increased in both pool types (Table

3, Figure 6).

For La. burkei, there were marginally higher rates of visitation in natural pools, and overall there were slightly more bombyllid flies visiting than other types of insects

(Table 4, Figure 7). There was a strong pattern with respect to the seasonality of insect visitations between natural and constructed sites, and between the types of insects

12 observed (Table 4, Figure 8). On early dates there is high visitation in natural sites that declined as the season progressed, while the rate stays relatively level in constructed sites, shown by an interaction between day and pool type (Table 4, Figure 8). Both bombyliid flies and solitary bees were observed more during earlier dates, while syrphid flies were observed consistently throughout the season, as shown by the interaction between day and insect category (Table 4, Figure 8).

Effect of distance from a natural pool on visitation rate

Having combined data from the three plant species together, I saw that there were large differences in visitation rates by solitary bees between each plant species (Table 5) and the overall pattern shows that there were fewer solitary bee visits in constructed pools

(Figure 9). Additionally, pools in my study that were closer to neighboring plant populations received more solitary bee visits (Table 5, Figure 9).

Pollinator community composition in natural versus constructed pools

Table 6 shows the mean number of specimens collected either via net or in pan traps organized by insect category and pool type. For B. bakeri, solitary bees comprise the largest category collected via net, and the numbers are about equal between natural and constructed sites (Table 7). The oligolectic bee A. blennospermatis, visited

Blennosperma plants in both natural and constructed sites, along with several of its look- alikes, such as A. angustitarsata, A. pensilis, H. tripartitus, and L. titusi. Notably, I collected no honeybees with nets at natural sites, which was consistent with my observational results (Figure 3), and I collected syrphid flies more frequently from B. bakeri than the L. vinculans or La. burkei (Table 6, Figure 10).

13 For L. vinculans, solitary bees were the most numerous category collected by both net and pan trap (Figure 11). Remarkably, all the solitary bees collected by net off the flowers were A. pulverea, the oligolectic specialist bee for Limnanthes sp. There were no significant differences between pool types in solitary bee visitation (Table 8).

For La. burkei, bombyllid flies were net collected in high numbers, mirroring the data obtained from flower visit observations, but they were not collected by the pan traps, which instead collected mostly solitary and other bees (Table 10, Figure 12). I collected no honeybees by net from any site with La. burkei, mirroring the low visitation rate observed (Figures 7 and 8).

Overall, I found 40 different species of bees, and two species of syrphid flies in pan traps near B. bakeri, 26 species of bees, and five species of syrphid flies in pan traps near L. vinculans, and 35 species of bees and six species of syrphid flies in pan traps near

La. burkei (Appendix 1.) For all pan-trap analyses, there were no significant effects except for the category of insect collected (Tables 7, 8, and 10). For B. bakeri and La. burkei, pan traps contained many species of bees other than the solitary bees seen visiting the flowers (Figures 10 and 12). However, for L. vinculans, the most abundant species collected in pan traps was the specialist solitary bee, A. pulverea (Figure 11).

Discussion

Prior to this research, it was unknown whether specialist andrenid bees described from congeners in the Central Valley of California visited remaining natural populations of endangered vernal pool plants on the Santa Rosa Plain. Moreover, it was undetermined whether specialist pollinators had also colonized ‘newer’ populations of endangered plants established within constructed vernal pools, or if generalist pollinators visited and

14 pollinated them. This research shows that solitary bees play a leading role in the reproductive ecology of these plants, and that they, and other important insect pollinators occur in both natural and constructed vernal pools. While constructed pools received fewer insect visits overall (Tables 2-5; Figure 9), they were not devoid of pollinators.

Constructed sites where I collected the most specialist bees were situated in the vicinity of natural sites, which is consistent with the finding that constructed pools closer to natural habitats receive more bee visits (Table 5, Figure 9). Based on this, I would recommend that future constructed vernal pools be located within 2 kilometers of another pool with the target plant species.

My study primarily focused on discerning differences in the plant-pollinator interactions between natural and constructed vernal pool habitats. I also learned that each plant species is unique regarding frequency and type of insects visiting inflorescences among pool types. For example, while there were more insects visiting B. bakeri in natural habitats earlier in the season, as compared to constructed pools, both pool types had a similar rate of insect visitation later in the season (Table 2, Figure 4). The lower rate of visitation according to pool type reflects this delay in visitation to constructed pools, and also supported by an earlier study of insect visitors to B. bakeri (Leong, 2000).

Also, while I collected the specialist bee A. blennospermatis from B. bakeri, there were four other bee species of a similar shape and size co-occurring and using the same floral resources during this study (Table 6). This could mean the B. bakeri system may have resiliency to the loss of one pollinator species. Further study into the efficacy of pollination and frequency at which these generalist species visit B. bakeri would be useful to know the relative importance of each of the pollinator species found. The

15 occurrence and reliability of these generalist species may not be enough to sustain the plant population. One concern raised by these results is that, with the lower observed rates of visitation at the constructed sites, the plants may not produce as many seeds, which could result in the population size reducing over time (Davis, 1998).

Solitary bees played an important role for L. vinculans in both the flower visitor observations and the abundance of collected specimens. Furthermore, given the number of specialist solitary bees, A. pulverea were far more abundant on L. vinculans than the other two focal plants (Table 6.) This could mean that L. vinculans is the most dependent on its specialist bee pollinator. From a conservation perspective, it is encouraging that I found this pollinator with its host plant at all locations sampled. One factor contributing to high abundance of A. pulverea on the Santa Rosa Plain may be that the upland plant species L. douglasii (Common meadowfoam) provides additional forage for these bee populations, perhaps boosting their numbers. I observed A. mellifera, the European honeybee, also foraging on L. vinculans. Its abundance was higher in created sites (Figure

11), which may suggest that honeybees could substitute if specialist bees are missing. A study of pollen limitation and pollination in agricultural fields of L. alba showed that a plot with 60 Osmia bees produced similar seed set as plots with 4000 honey bees (Jahns,

2000). If the pollination efficiency for L. vinculans of A. mellifera relative to A. pulvera is similar to that found in Jahns’ study comparing native bees to honey bees, we would need a much higher amount of honey bees than what I observed to achieve similar levels of seed set when A. pulvera is present.

I was surprised to find that the bombyliid fly was the main visitor to La. burkei.

Burke’s goldfields’ specialist bee, A. submoesta, and its look-alike species were much

16 less abundant compared to bees found on the other two focal plant species (Table 6.) I also did not observe bees visiting flowers of La. burkei very often relative to the amount of bombyliid fly visits (Figures 7 and 8). This could mean that the bombyliid fly

Conophorus cristatus is acting as the main pollinator for La. burkei. While the specialist bee may rely on its host plant for food, the plant may not solely rely on it for pollination.

The results of the ANCOVA testing effects on visitation to La. burkei showed that although there was not a measureable difference in overall insect visitation rates between years, the prominence of the various insect groups changed in visitation rate across years, with bombyliid fly visits increasing and syrphid fly visits decreasing in 2011 (Table 4).

Although I found C. cristatus to be less abundant in constructed pools, it was still the most numerous insect visitor observed on La. burkei. The C. cristatus flies may act as a suitable pollinator due to their hairy body and nectar-probing proboscis (Thorp, R., personal communication). A study of Contra Costa goldfields (La. conjugans) showed that gnats were an effective pollinator in restored vernal pools where bee numbers were low (Faist, et al, 2015).

Bombyliid fly larvae are ectoparasitoids on other insects, and some are known to lay their eggs in burrows of ground-nesting bees (Boesi et al., 2009). However, the larval host of the genus Conophorus has not yet been discovered (Evenhuis, N., personal communication). Perhaps there is a tritrophic interaction between the host plant, ground nesting bees that gather its pollen, and bombyliid flies that lay their eggs in the nests of these bees while also drinking nectar from the host plant. More research should occur on this topic to inform the conservation of La. burkei further.

17 One criticism of constructed vernal pool sites is that the high ratio of wetland to upland, having been designed to maximize wetland acreage, might not provide adequate upland acreage for solitary flower visiting bees to nest (Leong, et. al., 1995; Faist, et. al.,

2005). Despite extensive searching, I was not able to locate any bee nests in all sampling locations, so I cannot comment directly on the size of upland needed to provide habitat.

However, I found the greatest number of A. submoesta (the specialist on La. burkei) at a created site, Woodbridge Mitigation Bank. I hypothesize the numbers were highest there because of 17 pools at that site with La. burkei, providing more forage for the bees to support a larger population of specialists, despite a relatively smaller amount of upland habitat compared to other sites.

However, I am concerned about the potential consequences of a breakdown in the close mutualism between B. bakeri and its pollinators, given the reduced visitation rates early in the season at constructed pools. With increased variability in weather and rainfall patterns due to climate change, there is greater potential for a phenological mismatch between these plants and their pollinators (Memmot, et. al., 2007; Kearns, et. al. 1998).

Furthermore, results from the pollinator exclusion experiment showed B. bakeri produced five times fewer seeds when pollinators were excluded (Sloop et al., 2012). If B. bakeri’s reproductive success declines due to lack of pollinators, floral displays could grow smaller and become less attractive to foraging bees, resulting in Allee effects and a negative feedback loop of rapid population decline (Davis, 1998).

I speculate that, given the higher incidence of bombyliid flies visiting La. burkei compared to bees, and higher seed set in open-pollinated flowers (Sloop, et. al., 2012), the bombyliid flies are playing a part in increasing pollination rates for La. burkei.

18 Further research is needed on the relationship between Burke’s goldfields, the Lasthenia specialist bee, and the bombyliid flies to determine if the bombyliid is effectively pollinating the plant and/or parasitizing bee nests.

Conclusion

This study shows that each of these plant species has its unique situation with regard to insect pollinators. L. vinculans has a strong relationship with its specialist A. pulverea, also found foraging on Common meadowfoam (L. douglasii). The wider distribution of L. douglasii makes it more likely for the oligolectic bees, which rely on

Limnanthes pollen, to find new patches of host plants. I am therefore not concerned about meadowfoam pollinators going extinct locally.

The results from this study indicate that the constructed pools on the Santa Rosa

Plain have had some success with regard to supporting both endangered plants and their associated pollinators. While the flower visiting insects are found less frequently in constructed sites (Figure 9), my results show constructed vernal pools provide additional habitat utilized by varied and abundant pollinator of the three focal endangered plant species addressed.

19 Bibliography

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Kearns, CA, DW Inouye, and NM Waser. 1998. Endangered mutualisms: The conservation of plant-pollinator interactions. Annual Review Of Ecology & Systematics, 29

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22 Sloop CM and DR Ayres. 2010. Conservation genetics of two endangered vernal pool plants of the Santa Rosa Plain, Sonoma County, California. Proceedings of the 2009 CNPS conference, Sacramento, CA.

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23 Table 1: List of study sites used to compare insect visitation on three flower species.

Distance to Total Sampled nearest Blennosperma bakeri Pools Pools Pool type neighbor (m) Alton Lane 38 2 Constructed 30 Maggi 1 1 Natural 1299 Slippery Rock 27 1 Constructed 1461 Todd Carinalli Mitigation Bank 52 2 Constructed 1466 Windsor Christian Academy 1 1 Natural 8072 Youth Community Park 2 2 Natural 426 Limnanthes vinculans Alton Lane 38 1 Constructed 30 Hazel Mitigation Bank 60 1 Constructed 798 Mariposa 1 1 Natural 2573 Sam Jones Air Center 1 1 Natural 1877 Todd Carinalli Mitigation Bank 52 2 Constructed 512 Wright Preserve 40 3 Natural 1525 Lasthenia burkei Alton Lane 38 2 Constructed 183 Piner Marlow 3 2 Natural 2074 Slippery Rock 27 2 Constructed 740 Wilkinson 11 2 Natural 2569 Woodbridge Mitigation Bank 17 2 Constructed 183 Wood Fulton 10 1 Natural 789 Wright Conservation Bank 7 3 Constructed 193

24 Table 2: Results from a permutational analysis of covariance testing the effects of insect category, pool type, and site on visitation rates to B. bakeri with day of year as a covariate. Visitation rate was Box-Cox transformed prior to analysis.

Source df SS Pseudo-F P(perm)

Insect category 2 0.023 6.73 0.154

Type of pool 1 0.009 8.18 0.034

Site 5 0.511 5.50 0.014

Insect category x Type of pool 1 0.007 2.22 0.308

Insect category x Site 10 0.080 1.84 0.082

Day 1 0.001 0.81 0.38

Day x Type of pool 1 0.007 6.18 0.018

Residual 46 0.049

Total 68 0.0007

25 Table 3: Results from a permutational analysis of covariance testing the effects of insect category, pool type, and site on visitation rates to L. vinculans with day of year as a covariate. Visitation rate was box cox transformed prior to analysis.

Source df SS Pseudo- F P(perm)

Insect category 2 0.109 37.48 0.0002

Type of pool 1 0.021 1.51 0.2539

Site 5 0.006 0.81 0.54

Insect category x Type of pool 2 0.008 2.84 0.068

Insect category x Site 10 0.080 1.84 0.082

Day 1 0.007 4.5 0.040

Day x Type of pool 1 0.001 0.28 0.599

Day x Site 5 0.008 1.20 0.31

Residual 36 0.053

Total 53 0.1946

26 Table 4: Results from a permutational analysis of covariance testing the effects of insect category, pool type, site, and year on visitation rates to L. burkei with day of year as a covariate. Visitation rate was Box-Cox transformed prior to analysis.

Source df SS Pseudo- F P(perm)

Day 1 0.005 2.83 0.094

Insect category 3 0.013 2.53 0.064

Type of pool 1 0.009 5.21 0.058

Year 1 0.001 0.05 0.82

Site 6 0.002 1.17 0.33

Day x Insect Category 3 0.016 2.97 0.037

Day x Type of pool 1 0.008 5.01 0.032

Insect category x Type of pool 3 0.027 5.01 0.003

Insect category x Year 3 0.029 5.45 0.001

Residual 125 0.223

Total 147 0.406

27 Table 5: Results from an analysis of covariance testing the effects of pool type, plant species, and distance to nearest neighbor on visitation rates of solitary bees to the three plant species, with distance to nearest neighbor as a covariate. Visitation rate and distance were Box-Cox transformed prior to analysis.

Source df SS F P

Site type 2 250.6 15.68 0.0016

Plant species 1 321.0 10.04 0.0023

Site type x Plant species 2 84.26 2.64 0.1095

Distance to neighbor 1 117.3 7.34 0.0179

Residual 13 207.8

Total 19 984.0

28 Table 6. Mean (+ 1 standard deviation) number of specimens of the major pollinator taxa

collected in constructed and natural pools.

Constructed Natural Net Pan Net Pan Blennosperma bakeri n = 5 n = 7 n = 6 n = 6 Mean sd Mean sd Mean sd Mean sd Solitary Bees1 3.2 (4.1) 6.0 (6.2) 3.2 (2.3) 8.0 (10.3) Apis mellifera 0.6 (1.3) 1 (1.2) -- -- 0.8 (1.0) Other bees 1.4 (2.6) 11.2 (8.7) 6.8 (7.5) 18.3 (10) Syrphid flies 1.0 (2.2) 0.8 (1.3) 1.7 (1.2) 2.0 (2.2)

Limnanthes vinculans n = 3 n = 5 n = 5 n = 5 Solitary Bees2 7.3 (6.8) 17 (38.1) 14.4 (7.6) 74 (55.7) Apis mellifera 2.0 (3.5) 1.0 (1.3) 0.4 (0.9) 1.2 (2.2) Other bees 0.2 (0.4) 0.5 (1.4) 0.1 (0.3) 0.5 (1.7) Syrphid flies 0.1 (0.4) 0.32 (0.7) 0.1 (0.3) 0.1 (0.3)

Lasthenia burkei n = 9 n = 9 n = 4 n = 5 Solitary bees3 0.7 (2.8) 0.1 (0.4) 0.25 (0.7) 0.3 (0.6) Apis mellifera -- -- 0.5 (0.8) -- -- 0.7 (1.2) Other bees 0.1 (0.3) 0.2 (0.02) 0.1 (0.3) 0.5 (1.3) Bombylliid Flies 9 (8.1) 0.3 (0.5) 16.3 (8.7) 2.0 (2.6) Syrphid flies 0.4 (0.9) 0.1 (0.3) 0.3 (0.9) 0.1 (0.4)

1 Includes specialist bee Andrena blennospermatis, A. pensilis, Halictus tripartitus, and Lassioglossum titusi in nets, and for pan traps this category included A. blennospermatis, A. angustitarsata, H. tripartitus, and L. titusi 2 Only specialist bee A. pulverea was collected in nets, for pan traps this category includes A. pulverea, H. tripartitus, and L. titusi 3 For net collected, this includes specialist bee A. submoesta, A. angustitarsata, A. pensilis, and L. titusi and for pan trap, A. submoesta, A. angustitarsata, A. pensilis, H. tripartitus, and L. titusi

29 Table 7. Results from a permutational analysis of variance testing the effects of insect category, pool type, site, and pool on the abundance of insect specimens collected by net sweeps over flowering patches of B. bakeri, and pan trapped insects collected near the same flowering patch. Insect abundance was Box-Cox transformed prior to analysis.

Net Pan Trap Source df SS Pseudo-F P(perm) df SS Pseudo-F P(perm) Type of pool 1 14.638 1.08 0.393 1 25.141 1.15 0.347

Insect category 3 603.86 65.35 0.001 3 337.6 8.39 0.002

Site 5 67.083 0.8 0.539 4 80.842 1.93 0.237

Type of pool x Insect category 3 10.974 1.19 0.343 3 18.738 0.53 0.661

Pool 4 66.815 6.21 0.002 6 62.887 1.59 0.208

Site x Insect Category 15 46.538 1.15 0.399 12 141.97 1.79 0.134

Residual 12 32.288 18 119

Total 43 959.9 47 824.16

30 Table 8: Results from a permutational analysis of variance testing the effects of insect category, pool type, site, and pool on the abundance of insect specimens collected by net sweeps over flowering patches of L. vinculans, and of pan trapped insects collected near the same flowering patch. Insect abundance was Box-Cox transformed prior to analysis.

Net Pan trap

Source df SS Pseudo-F P(perm) df SS Pseudo-F P(perm) Type of pool 1 0.025 0.159 0.747 1 0.056 0.01 0.839

Insect category 3 102.49 19.17 0.001 3 2332.6 37.5 0.001

Site 4 3.968 0.175 0.971 6 29.586 0.17 0.929

Type of pool x Insect category 3 5.079 0.977 0.455 3 56.541 0.91 0.435

Pool 2 11.342 2.68 0.146 2 58.941 1.39 0.285

Site x Insect Category 12 20.914 0.824 0.621 18 372.9 0.98 0.531

Residual 6 12.691 6 127.12

Total 31 170.24 39 3247.8

31 Table 9: Results from a permutational analysis of variance testing the effects of insect category, pool type, site, pool, and year on the abundance of insect specimens collected by net sweeps over flowering patches of La. burkei. Insect abundance was Box-Cox transformed prior to analysis.

Source df SS Pseudo- F P(perm)

Year 1 0.504 0.24 0.67

Type of pool 1 0.441 0.16 0.723

Insect category 4 97.420 9.77 0.002

Site 5 15.324 1.11 0.44

Year x Type of pool 1 0.004 0.01 0.966

Year x Insect category 4 10.511 1.23 0.31

Type of pool x Insect Category 4 12.641 3.16 0.329

Pool 5 14.299 1.33 0.267

Site x Insect Category 20 53.544 1.25 0.243

Residual 39 83.34

Total 84 376

32 Table 10: Results from a permutational analysis of variance testing the effects of insect category, pool type, site, and pool on the abundance of insect specimens collected from pan traps set out near flowering patches of La. burkei in 2010. Insect abundance was

Box-Cox transformed prior to analysis.

Source df SS Pseudo- F P(perm)

Type of pool 1 7.062 5.65 0.069

Insect category 4 156.57 16.23 0.001

Site 4 4.789 0.59 0.70

Type of pool x Insect Category 4 7.973 0.83 0.522

Pool 4 8.073 1.49 0.243

Site x Insect Category 16 39.724 1.83 0.129

Residual 16 21.654

Total 84 256.76

33 Figure 1. Map of study site locationsS. B.tu bakeridy A abbreviatedrea as BLBA, La. burkei abbreviated as LABU, and L. vinculans abbreviated as LIVI.

!( (Windsor Christian Academy, 13.5 km north) Sampling Sites !( Species, Site type ¯ # * BLBA, Constructed *# !( BLBA, Natural *# *# LABU, Constructed !( !(!( !( LABU, Natural !( *# LIVI, Constructed !( LIVI, Natural Study Sites

*#!(!(

!( !( !(!( *#*#

!(

*#*# *# *# !(!(

0 1.25 2.5 5 *#*#

Kilometers Base layer from ArcGIS Online

34 Figure 2. Date ranges of sampling efforts for this study. Black bars indicate total flowering period, while clear bars show the period during which timed observations were performed. Thickly shaded bars show the timing of net collections and thin shading shows the time span of pan trapping efforts.

35 Figure 3. Least-squared means (+1 standard error) of visitation rates across constructed and natural sites for B. bakeri. Visitation rates were calculated from average counts of insect visits within a 10 minute period.

0.12 Natural Constructed

0.08 Cox transformed Cox - Visitation Rate Box 0.04

0 Honey Bee Solitary Bee Syrphid Fly

36 Figure 4. Plot showing the effect of day of year on visitation rates to B. bakeri by different insect categories.

transformed Cox Cox - Visitation Rate Box

37

Figure 5. Least-squared means (+1 standard error) of visitation rates across constructed and natural sites for L. vinculans. Visitation rates were calculated from average counts of insect visits within a 10 minute period.

0.16 Natural Constructed 0.12

0.08 Cox transformed Cox - Visitation Rate Box

0.04

0 Honey Bee Solitary Bee Syrphid Fly

38 Figure 6. Plot showing the effect of day of year on visitation rates to L. vinculans by different insect categories.

Cox transformed - Visitation Rate Box

39

Figure 7. Least-squared means (+1 standard error) of visitation rates across constructed and natural sites for L. burkei. Visitation rates were calculated from average counts of insect visits within a 10 minute period and Box-Cox transformed.

0.16 Natural Constructed

0.12

0.08 Cox tranformed Cox - Visitation Rate Box

0.04

0 Bombyliid Fly Honey Bee Solitary Bee Syrphid Fly

40 Figure 8. Plot showing the effect of day of year on visitation rates to La. burkei by different insect categories.

Cox Cox transformed - Visitation Rate Box

41

Figure 9. Results from an analysis of covariance (ANCOVA) testing the effects of pool type, plant species, and distance to nearest neighbor on visitation rates of solitary bees to the three plant species, with distance to nearest neighboring conspecific plant population as a covariate. 9A: Least-squared means (+1 standard error) of visitation rates across constructed and natural sites for B. bakeri, L. vinculans, and La. burkei. There were notable differences between plant species and habitat types (Table 5).

9B: Plot showing relationship between visitation rate and distance to neighbor.

A 10 9 Constructed 8 Natural 7 6 5 4 Cox transformed Cox - 3 Mean visitation rate visitation Mean

Box 2 1 0 B. bakeri L. vinculans La. burkei

B 8 7 6 5 4 3 Cox tranformed Cox

- 2 Mean visitation rate visitation Mean

Box 1 0 10000 11000 12000 13000 14000 15000 16000 Mean distance to neighbor Box-Cox transformed

42 Figure 10. Mean (+1 standard error) of number of individual specimens collected by net and pan trapping across constructed and natural sites for B. bakeri.

Net Collected 9 Constructed 8 Natural 7

6

5

4

3

Mean number of specimens specimens of number Mean 2

1

0 Solitary bees A. mellifera Other bees Syrphid flies

Pan trapped 30

25

20

15

10 Mean number of specimens specimens of number Mean 5

0 Solitary bees A. mellifera Other bees Syrphid flies

43 Figure 11. Mean (+1 standard error) of number of individual specimens collected by net and pan trapping across constructed and natural sites for L. vinculans.

Net Collected

25 Constructed 20 Natural

15

10

5 Mean number of specimens of number Mean

0 Solitary bees A. mellifera Other bees Syrphid flies

Pan Trapped

140

120

100

80

60

40 Mean number of specimens of number Mean

20

0 Solitary bees A. mellifera Other bees Syrphid flies

44 Figure 12. Mean (+1 standard error) of number of individual specimens collected by net and pan trapping across constructed and natural sites for La. burkei.

Net Collected

30

25 Constructed Natural 20

15

10

Mean number of specimens of number Mean 5

0 Bombyllid fly Solitary bees Other bees Syrphid flies

Pan Trapped

2.5

2.0

1.5

1.0

0.5 Mean number of specimens of number Mean

0.0 Bombyllid fly Solitary bees A. mellifera Other bees Syrphid flies

45 Appendix 1. Number of specimens collected from Blennosperma bakeri, Limnanthes

vinculans and Lasthenia burkei listed by insect functional group and collecting method.

Bees were grouped as ‘Solitary Bee’ if they superficially resembled the specialists and

would have been counted in the observational data (Table 6).

B. bakeri L. vinculans L. burkei Net Pan Net Pan Net Pan Specialist Bee Andrena blennospermatis 19 9 . . . . Andrena pulverea . . 94 574 . . Andrena submoesta . . . . 16 4 Honey Bee Apis mellifera 3 11 8 11 . 7 Solitary Bee Andrena angustitarsata . 1 . . 1 4 Andrena pensilis 9 . . . 5 1 Halictus tripartitus 4 34 . 7 . 6 Lasioglossum titusi 3 40 . 10 13 8 Other Bee Agapostemon texanus . 3 . 4 . 1 Andrena caerulea 1 1 . 1 . . Andrena candida . 4 . . . . Andrena cercocarpi . . . 2 . . Andrena chalybaea . 18 . 2 . 3 Andrena cuneilabris . 23 . 18 . . Andrena cymatilis 1 . . . . . Andrena hypoleuca 1 . . 1 . . Andrena miserabilis . 1 . . . . Andrena orthocarpi 2 . . . . 1 Andrena osmiodes . 1 . . . 3 Andrena pulverea 24 36 . . . 19

46 Appendix 1, cont.

B. bakeri L. vinculans L. burkei Net Pan Net Pan Net Pan Other Bee, cont. Andrena sp large black . 2 . . . . Andrena suavis . 5 . . . . Andrena subchalybea . . . . . 6 Andrena sublayiae . . . . 1 . Andrena torulosa . 8 . 12 . . Bombus californicus . . . . . 1 Bombus melanopygus . . . . . 1 Ceratina nanula . 4 1 1 . . Eucera actuosa . . . 1 . . Eucera edwardsii . . . . . 4

Halictus farinosus . 1 . . . 1 Halictus ligatus . 2 . 2 4 4 Halictus rubicundus . . . 1 1 . Hylaeus conspicuous . . . 2 . . Lasioglossum (Dialictus) incompletum . 12 . 7 . 18 L. (Dialictus) sp. 1 . . . . . 7 L. (Dialictus) sp. D . 7 1 15 . 17 L. (Dialictus) sp. ‘KG1’ . . . . 1 1 L. (Dialictus) sp. shiny 1 11 . . . . L. (Dialictus) tegulariforme . 1 . . . . L. (Dialictus) tegularis . 1 . . . . Lasioglossum (Evylaeus) kincaidii . 1 . . 1 7 L. (Evylaeus) sp. large . 1 . . . . L. (Evylaeus) sp. medium . 8 . . . . L. (Evylaeus) sp. 1 3 . . . . . L. (Evylaeus) sp. E 10 4 1 2 . 5 L. (Evylaeus) sp. I 1 3 . 2 . 1

47 Appendix 1, cont. B. bakeri L. vinculans L. burkei Net Pan Net Pan Net Pan L. (Evylaeus) sp. ‘small sp.’ . 1 . . . . Lasioglossum incompletum . . . . 1 . Lasioglossum olympiae . . . 2 . 5 Lasioglossum pacifica 3 5 . . . . Osmia (Chenosmia) sp. ‘green’ . 1 . . . . Osmia albolateralis . . . 1 . 1 Osmia atrocyanea . . . . . 1 Osmia californica . 2 . . . . Osmia sp. ‘large blue’ . 1 . . . . Osmia sp. ‘medium’ . 2 . . . . Osmia sp. 1 1 . . . . . Osmia sp. ‘KG’ . . . 1 . 1 Osmia nemoris . 5 . 19 . 39 Osmia regulina . . . 2 . 3 Osmia trevoris . 1 . 1 . 1 Osmia ‘trevoris-like morph’ . 2 . 1 . 1 Panurginus sp. 1 . . . . 1 . Panurginus sp. 2 . . . . . 2 Panurginus nigrellus . . . 2 . 1 Panurginus sp. ‘new undescribed’ . . . . 3 2 Sphecodes sp. . 1 . . . . Syrphid Flies Eristalis arbustorum . . 2 . 5 3 Eristalis hirta 1 . . 1 . . Eupeodes volucris . . 1 . 1 . Helophilus fasciatus . . . 3 . 1 Lejops polygrammus 1 . 1 2 . 1 Parhelophilus sp. . . . 1 . . Platycheirus stegnus 3 . 1 . 3 1

48 Appendix 1, cont.

B. bakeri L. vinculans L. burkei Net Pan Net Pan Net Pan Syrphid Flies, cont. Sphaerophoria sulphuripes . . 1 . 3 . Toxomerus marginatus 9 14 2 3 22 7 Toxomerus occidentalis 1 3 . . 1 2

Bombyliid Fly Conophorus cristatus . . . . 205 8

49