EFFECTS of LAND USE on NATIVE BEE DIVERSITY Byron

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THE BEES OF THE AMERICAN AND COSUMNES RIVERS IN SACRAMENTO COUNTY, CALIFORNIA: EFFECTS OF LAND USE ON NATIVE BEE DIVERSITY

Byron Love B.S., California State University, Humboldt, 2003

THESIS

Submitted in partial satisfaction of the requirements for the degree of

MASTER OF SCIENCE

BIOLOGICAL SCIENCES (Biological Conservation)

CALIFORNIA STATE UNIVERSITY, SACRAMENTO

SUMMER 2010

THE BEES OF THE AMERICAN AND COSUMNES RIVERS IN SACRAMENTO COUNTY, CALIFORNIA: EFFECTS OF LAND USE ON NATIVE BEE DIVERSITY

A Thesis

Byron Love

Approved by:

______, Committee Chair Dr. Shannon Datwyler

______, Second Reader Dr. Patrick Foley

______, Third Reader Dr. Jamie Kneitel

______, Fourth Reader Dr. James W. Baxter

Date:______iii

Student: Byron Love

I certify that this student has met the requirements for format contained in the University format manual, and that this thesis is suitable for shelving in the Library and credit is to be awarded for the thesis.

______,Graduate Coordinator ______Dr. James W. Baxter Date

Department of Biological Sciences

Abstract

THE BEES OF THE AMERICAN AND COSUMNES RIVERS IN SACRAMENTO COUNTY, CALIFORNIA: EFFECTS OF LAND USE ON NATIVE BEE DIVERSITY

Byron Love

A survey of the bees in semi-natural habitat along the American and Cosumnes rivers in Sacramento County, California, was conducted during the flower season of 2007. Although the highly modified landscapes surrounding the two rivers is distinctly different, with urban and suburban development dominant along the

American River, and agriculture along the Cosumnes River, there is no difference in the proportion of modified landscape between the two rivers. The proportion of semi-natural habitat is also similar between rivers. Sixty four species of plants provided floral resources for bees, dominated by nonnative species. Over half of the bee diversity were associated with 3 nonnative plants—Hirschfeldia incana,

Centaurea solstitialis, and Cichorium intybus—indicating the importance of nonnative plants in providing floral resources

A total of 122 bee species were identified in five families from 7910 specimens collected or observed. Bee abundance was dominated by the Halictidae family,

with 50% coming from 4 species. Apidae was the most specious family, and

Andrenidae and Colletidae accounted for less than 5% of bee abundance. A surprising 17% of bee diversity included specialist bees, with the Cosumnes river accounting for higher richness, abundance, and number of unique species. Five species of nonnative bee species were identified, but there were no indications of nonnative bees exhibiting preferences for nonnative plants. Similarity measurements reveal that bee communities are generally associated by river, with the exception of one site on the American river at the confluence with the

Sacramento river, indicating the possibility of river systems providing uniquely similar bee communities.

______, Committee Chair Dr. Shannon Datwyler

______Date

ACKNOWLEDGEMENTS

Whether or not my path would have ultimately led to bees without their introduction by my undergraduate advisor Mick Mesler is beside the point; your passion is now mine. I have been lucky to meet so many kind and helpful people during my time at Sac State, and have made many lifelong friends. I am forever indebted for the guidance, advice, and most of all patience, of Patrick Foley, but

I’m still not certain if I should thank or curse you for introducing me to R. My advisor Shannon Datwyler provided much more than academic support. Your help and advice in navigating academia has made me a better scholar and teacher. Jamie

Kneitel and Jim Baxter provided much needed assistance in working out the bugs

(or should I say bees?) in the design, analysis, and manuscript. The resolution of bee identification could not have been possible without the infinite patience of

Robbin Thorp; and Mike Baad and Jim Alford assisted with plant identification.

So many people blurred the line between cohorts, staff, and friends. Many thanks to Larry Cabral, Carrie Lessin-Cabral, Sulie Harney, Melissa Schlenker, and

Erika Holland.

Finally, a special thanks to my family who have put up with that crazy son, brother, uncle. Your love and support has provided almost as much solice as your unwaivering belief. And to Ida, a most special thanks for giving me the

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encouragement, push, and opportunity to explore my curiosity of the natural world.

I am forever grateful.

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TABLE OF CONTENTS

Page Acknowledgements ...... vii

List of Tables ...... xi

List of Figures ...... xii

Introduction ...... 1

Pollinator Declines ...... 2

Land Conversion in the Sacramento Valley ...... 4

Bee Diversity ...... 7

Goals and Objectives ...... 8

Materials and Methods ...... 10

Study Area...... 10

Experimental Design ...... 12

Landscape Analysis ...... 14

Sampling Bee Richness, Abundance, and Floral Preferences ...... 15

Sampling Floral Resources ...... 18

Data Analysis ...... 19

Results ...... 21

Landscape Analysis ...... 21

Bee Communities ...... 21

Bee Abundance, Richness, and Diversity ...... 27

Floral Resources ...... 33

The Influence of Plants on Bees ...... 41

Non-native Bees and Plants ...... 41

Comparison of Hand Netting and Pan Trapping ...... 48

Discussion ...... 50

Urban and Agricultural Habitats as Bee Refugia ...... 52

Implications of Nonnative Bees ...... 56

Bee Sampling Considerations ...... 58

Conclusion ...... 61

Appendix A: Species list of bees and numbers of individuals collected in semi-natural habitat along the American and Cosumnes Rivers in Sacramento County, California in 2007...... 63

Appendix B: Bee-visited plant list in semi-natural habitat along the American and Cosumnes Rivers in Sacramento County, California in 2007...... 68

Literature Cited ...... 76

LIST OF TABLES

Table 1. Sampling Site description, code, latitude and longitude, and elevation (in meters) of sampling locations along the American and Cosumnes Rivers in Sacramento, California ...... 13

Table 2. Comparison of bee abundance (# of individuals), richness (# of species), diversity, and several community measures between each river ...... 23

Table 3. Abundance (number of individuals), nesting and social habits of the most widespread bee species (occurring at all 8 sites) ...... 28

Table 4. ANOVA summary for the comparison of bee abundance (# of individuals), bee species richness, diversity (Simpson’s reciprocal index), and community evenness (Simpson’s reiciprocal index/richness) between the American and Cosumnes Rivers during May through September 2007 ...... 29

Table 5. List of plant species, family, native/non-native status, and occurence, observed at study sites along the American and/or Cosumnes Rivers in Sacramento County, California ...... 36

Table 6. Abundance (% cover) and richness (# of species) of plants in flower along each river between May and September 2007 ...... 40

Table 7. List of bee species collected either by hand netting or pan trapping ...... 49

LIST OF FIGURES

Figure 1. Vicinity map and study site locations along the American River and Cosumnes River in Sacramento County, California...... 11

Figure 2. Composition of land cover types ...... 16

Figure 3. Proportion of land-cover types at each study site along the Cosumnes and American Rivers ...... 22

Figure 4. A comparison of bee family diversity for bees collected at all study sites along the American and Cosumnes rivers in Sacramento County, California...... 25

Figure 5. Ranked abundance (# of individuals) of the top twenty most abundant bee species collected along the American and Cosumnes Rivers ...... 26

Figure 6. Comparison of bee abundance (# of individuals) along the American and Cosumnes Rivers between May and September 2007 ...... 30

Figure 7. Comparison of bee species richness along the American and Cosumnes Rivers between May and September 2007 ...... 31

Figure 8. Comparison of bee diversity (Simpson’s Reciprocal Index) along the American and Cosumnes Rivers between May and September 2007 ...... 32

Figure 9. Comparison of bee community evenness along the American and Cosumnes Rivers between May and September 2007 ...... 34

Figure 10. Jaccard Index of Similarity Dendrogram ...... 35

Figure 11. Comparison species richness of plants in flower along the American and Cosumnes Rivers ...... 38

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Figure 12. Comparison of the abundance (% cover) of plants in flower along the American and Cosumnes Rivers ...... 39

Figure 13. Regression of bee species richness on plant species richness ...... 42

Figure 14. Regression of bee abundance on plant species richness ...... 43

Figure 15. Regression of bee species richness on floral resource abundance ...... 44

Figure 16. Regression of bee abundance on floral resource abundance ...... 45

Figure 17. Distribution of the total numbers of nonnative bees (excluding Apis) collected between May and September 2007 ...... 47

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INTRODUCTION

When California was wild, it was one sweet bee-garden throughout its entire length…Wherever a bee might fly within the bounds of this virgin wilderness…bee-flowers bloomed in lavish abundance. -John Muir, 1894

Urban and agricultural development have converted approximately 11% of the Earth’s land surface (Ricketts et al., 1999). These highly modified landscapes disrupt native biodiversity in a number of ways, including the loss and fragmentation of habitat, and the replacement of native plant communities. The negative impacts of urban and agricultural land conversion are well documented

(McDonnell and Pickett, 1990; Blair, 1999; Benton et al., 2002; McKinney, 2002;

Bengtsson et al., 2005; Ockinger and Smith 2007). California’s Central Valley has undergone the most intense transformation of any of the state’s terrestrial ecosystems (Schoenherr, 1992). In Sacramento County, the historic landscape of delta marshes and sloughs, riparian forests, oak woodlands, grasslands and vernal pools have largely been replaced by an agricultural and urban matrix (Schoenherr,

1992; Ricketts et al., 1999). Crops, roads and parking lots, residential, commercial, and industrial buildings, as well as manicured lawns and nonnative landscaping, have all but replaced the expansive wildflower habitat that so inspired John Muir

(Muir, 1894). The influence of these landscape changes on local native bee communities is of concern due to the importance of bees in providing pollination services.

Bees provide an essential ecosystem service in the pollination of both crop and wild plants. Not only have bees played an important role in angiosperm evolution (Proctor et al., 1996), but it has been estimated that 67% of angiosperms are pollinated by bees (Axelrod, 1960). Critical for the majority of human food production, over half of the world’s 1,500 food crops depend on animal (primarily bee) pollination; these include coffee, almonds, berries, melons, and alfalfa

(Buchmann and Nabhan, 1996; Kremen et al., 2002; Ricketts, 2004; Ricketts et al.,

2004). Although the imported honey bee (Apis mellifera) has been the most important managed pollinator (Kremen et al., 2002), the use of native bees in pollinating agricultural crops can also be effective (Kremen et al., 2002; Kremen et al., 2004; Ricketts 2004; Ricketts et al., 2004; Morandin and Winston 2005;

Greenleaf and Kremen, 2006a; 2006b), and are now actively incorporated into agricultural systems. Bees also contribute indirectly to other trophic level interactions by maintaining plant populations and increasing seed set—an important food source for insects, birds, and mammals (Cane, 2005a; Danforth,

2007).

Pollinator Declines. Detecting declines in bee populations is difficult due to a lack of baseline information on population and community dynamics. Multi-year monitoring programs are necessary to capture the variation inherent in insect populations before long-term trends can be explained (Williams et al., 2001).

Nonetheless, evidence of worldwide declines in pollinator populations is growing at an alarming rate (Buchmann and Nabhan, 1996; Kearns et al., 1998). Domestic honey bee production has dropped 50-70% since the 1940s (Allen-Wardell et al.,

1998; Kearns et al., 1998; Kremen et al., 2004) due to parasitic mites, fungal and bacterial infections, and improper pesticide use. In 2006, Colony Collapse Disorder

(CCD) was identified as an important threat to honey bee populations. This poorly understood phenomenon is characterized by the disappearance of adults, leaving behind what appears to be otherwise healthy colonies that include intact brood cells and food stores (pollen and honey). Bee keepers have reported losses of up to 90% of their colonies, presumably as a result of CCD (Johnson, 2008).

Declines have also been documented for native bees. The Xerces Society for Invertebrate Conservation (Xerces.org) lists over 50 North American species of concern. For example, the distribution and frequency of three North American bumble bees (Bombus occidentalis, B. affinis, and B. tericola) have been dramatically reduced over the past decade. Bombus franklini, an endemic species once common in its restricted range in southwest Oregon and northwest California, is thought to be extinct. In Central America, stingless bees in the genus Melipona and Trigona (important pollinators of neotropcial forest trees and crops) are also reported to be in decline (NRA, 2007). Causes of native bee declines continue to be investigated, but evidence suggests that habitat fragmentation and exposure to

4 nonnative pathogens from commercially reared bees may be important contributing factors (R. Thorp, personal communication).

Land Conversion in the Sacramento Valley. Habitat loss is considered a primary cause of pollinator declines (Allen-Wardell et al., 1998; Kearns et al.,

1998; Winfree et al., 2007a). The Central Valley has been altered by human activities more than any other region in the state, losing almost 90% of its grasslands, freshwater marshes, and riparian woodlands, since the early 1800s

(Schoenherr, 1992). Vernal pools have also experienced similar declines and are critical for a number of specialized plant-bee relationships endemic to vernal pools

(Thorp and Leong, 1996). Human activities have modified the landscape in

Sacramento Valley into a mosaic of urban and agricultural development. Both of these types of land conversions can influence bee communities in complex ways that are not always clear (Cane et al., 2006; Winfree et al., 2007a).

The conversion of natural habitat to agricultural production can positively or negatively influence bee diversity. A number of mechanisms including changes in the availability of natural habitat, access to floral rewards (pollen and nectar), and exposure to pesticides (Kremen et al., 2002; Kremen et al., 2004). Bee diversity can be negatively influenced by agricultural intensification, which is exemplified by a reduction in habitat heterogeneity. A study of pollinator-obligate watermelon crops in Central Valley California found that larger fields further from

5 natural habitat, received fewer bee visitors than did smaller fields closer to natural habitat (Kremen et al.,2002 ). Regardless of their proximity to natural habitat, crops that do not offer floral rewards, such as wheat, rice, and corn, or crops that require intensive pesticide treatments, are also known to have negative effects on bee diversity (Cane and Tepedino, 2001).

Conversely, agricultural production can enhance bee diversity by creating islands of floral resources where before there were none. For instance, the clearing of forests for agricultural production opens previously shaded habitats, providing opportunities for shade-intolerant plant species (Cane and Tepedino, 2001). In addition, pulses of floral resources (pollen and nectar) associated with certain crops, such as alfalfa and sunflowers, have been shown to increase bee diversity

(Kremen, 2008). However, a short-lived burst of floral resources may only benefit species capable of completing their life cycles during the ephemeral bloom period

(Cane and Tepedino, 2001).

The conversion from natural habitat to urban developments can also have varied results on bee diversity. As with agricultural development, urbanization reduces the natural habitat and resources necessary for the persistence of native bee communities.Consequently, bee diversity is often negatively correlated with urban development (McIntyre and Hostetler, 2001; Cane et al., 2006; Matteson et al.,

2008; Kearns and Oliveras, 2009). As with agricultural development, urban habitats

6 can be enhanced to favor bee diversity. Due to post WWII policies, which created semi-natural habitats in disused railroad beds, abandoned airports and roadsides, half of Germany’s bee species are found in the city of Berlin (Saure, 1996). Indeed, bee habitats in urban landscapes do not have to be expansive to be effective. For example, in Berkely and Albany California, two one-acre community gardens each provide the resources necessary to maintain between 20-50% of the local bee fauna

(Frankie et al., 2005). Likewise, tiny park in downtown Curitiba (Brazil; population

1.3 million) contains half the bee diversity of a 200-hectare semi-natural habitat outside the city (Cane, 2005a).

Today the Sacramento Valley Landscape is dominated by urban and agricultural developments. Intensive land conversion over the past 150 years has reduced natural habitat by over 90% (Schoenherr, 1992). Fragmented and isolated remnants of natural habitat can be found in public lands, land trusts, and municipal parks. Two of these fragments are adjacent to two of the major rivers running through Sacramento County, the American and Cosumnes Rivers. The remnant fragments of natural habitat along these rivers are not pristine, but can be considered semi-natural habitat. While they still retain many of their natural features (e.g., grassland, oak woodland, riparian forest), they are subject to human modification and use (Brown et al., 2003). For instance, the semi-natural habitat along the American River includes golf courses and bike trails, and the Cosumnes

River offers hunting opportunities and a nature preserve. Whether they retain their native bee communities is the subject of this study.

Bee Diversity. World bee diversity is currently estimated at 20,000 species

(Michener, 2000). In North America, over half of the continent’s 3,500 to 4,000 species can be found in California, making the state a hotspot of bee diversity.

There are a number of reasons why California is home to such a large bee fauna. In addition to the multitude and variability of potential bee habitats, due in part to the state’s large size and varied climate and topography, bees exhibit a unique biogeographic characteristic. In contrast to most taxa, which exhibit an increase in species richness closer to the tropics, bee diversity is highest in warm-temperate xeric regions (Michener 1979; 2000). One explanation is the perpetual supply of pollen and nectar produced in tropical environments. The continuous production of floral resources tends to favor generalist social species (Roubik, 1989). Social bees can occur as large numbers of individual bees occupying a given habitat. As a result, even though abundance may be high, the overall species richness declines, resulting in a decrease in bee diversity (Roubik, 1989). In contrast, the seasonal production of floral resources favor solitary, and often specialist, bee species, increasing the number of species which can occupy a given niche (Buchmann and

Nabhan, 1996).

Despite California’s status as a global bee hotspot, the only catalog of

California bees is an unpublished 30 year old report by Moldenke and Neff (1974).

While Moldenke’s California work went far to illuminate the scope of the state’s bee diversity, there is still much work required to determine the identities, ranges, and natural histories of the estimated 1,500 to 2,000 bee species in this California

(Moldenke and Neff, 1974; Moldenke, 1975; Michener, 1979). As an example, 15 new species were discovered during a recent survey of the bees in California’s

Pinnacles National Monument, south of San Francsisco (Messenger and Griswold,

2002).

The intrinsically rich bee diversity of this region, an ever-increasing demand for continued land conversion and development, and a less than adequate understanding of the local bee fauna, make bee research here in Sacramento an important priority for conservation biologists and land managers alike.

Goals and Objectives. This study describes and compares the bee communities in semi-natural habitat along both the American River and the

Cosumnes River in Sacramento County, California. Given that both urban and agricultural development can influence bee communities in similar ways, I tested the hypothesis that bee richness and abundance will be similar in the semi-natural habitat along the two rivers. This hypothesis was tested by comparing the proportions of modified (urban and agriculture) and semi-natural habitat to

9 determine whether any differences in land-cover type existed between the two rivers. Second, the plant communities were compared to determine whether there were any differences in the availability of floral resources (pollen and nectar). The third objective was the comparison of the bee communities—both native and nonnative—between the two river systems to determine whether there were any differences in bee abundance, diversity, community similarity, and floral preferences.

In addition to providing insights into the influence of agriculture and urban habitats on bee communities, this work contributes to the compilation of local bee faunas. By providing baseline data that can aid in the detection of future trends, identifying and monitoring populations of extinction-prone specialists as well as nonnative bee species, and identifying range expansions and contractions that may occur as a result of global climate change, bee surveys are valuable sources of information in the development of conservation strategies. As far as is known, this is the first survey of native bees along the American River in Sacramento. While bee surveys have been conducted along the lower Cosumnes River (R. Thorp unpublished), this work adds to that body of knowledge.

MATERIALS AND METHODS

Study Area. This study was conducted along the American and Cosumnes

Rivers in Sacramento County, California (Figure 1). Sacramento County is located in the Central Valley of California, and its Mediterranean climate is typified by hot dry summers and cool damp winters. The headwaters of both rivers originate east of Sacramento County in the Sierra Nevada Mountains, and empty into the

Sacramento River, along the western edge of the county.

Adjacent to each river is a variable strip of semi-natural habitat, which includes remnants of native plant communities that consist of delta marshes and sloughs, riparian forests, oak woodlands, grasslands, and vernal pools (Schoenherr,

1992; Ricketts et al., 1999). Native vegetation along this semi-natural corridor has bee largely replaced with non-native plant species. The landscape surrounding the semi-natural habitat has been transformed into a matrix of industrial, urban, and suburban development along the American River, and intensive agricultural operations along the Cosumnes River (with the exception of the 3,500 acre gated community of Rancho Murieta located at the eastern end of the study area).

The semi-natural corridor along the American River—from its confluence with the Sacramento River, upstream to the Folsom Lake State Recreation area— includes a recreational parkway, which is managed by the Sacramento County

Parks Department. Recreational facilities include an asphalt bike trail, grass picnic

Figure 1. Vicinity map and study site locations along the American River and Cosumnes River in Sacramento County, California. Site codes along the American River: ARDP=Discovery Park; ARSS=California State University, Sacramento; ARRD=Rossmoor Road; ARLS=Sunrise Blvd. Site codes along the Cosumnes River: CRTC=Twin Cities Road; CRCF=Costello Forest; CRDD=Freeman Road; CRRM=Rancho Murieta. See Table 1 for site latitude and longitude coordinates.

and recreational areas, and parking lots. Parkway management activities include turf mowing and watering, weed control, and limited habitat restoration

(e.g., oak tree plantings, and the removal of invasive plant species, such as Yellow

Star Thistle, Red Sesbania, and Scotch Broom).

The semi-natural corridor along the Cosumnes River through Sacramento

County is largly undeveloped and is managed by a consortium of public, private, and non-profit agencies, including The Nature Conservancy, Ducks Unlimited,

California Department of Fish and Game, Sacramento County Department of

Regional Parks, California Department of Water Resources, and private landowners. A 46,000 acre preserve has been established along the lower portion of the study site, with the objective of conserving and restoring native habitat.

Management activities include periodic flooding, invasive plant removal, and agricultural and livestock operations.

Experimental Design. Four sites were selected within each of the semi- natural corridors surrounding both the American and Cosumnes Rivers (8 total)

(Table 1, Figure 1). At the center of each site, a 1 hectare plot was defined in open herbaceous habitat (primarily forbs and grasses). Spatial independence was preserved by maintaining a minimum distance of 3 kilometers between sites

(LeBuhn et al., 2003; Windree et al., 2007a).

Table 1. Site description, code, latitude and longitude, and elevation (in meters) of sampling locations along the American and Cosumnes Rivers in Sacramento, California.

River / Site Description Site Code Lat./Long. Elevation American / Discovery Park ARDP N38.6044° 7 W121.4935°

American / California State ARSS N38.5674° 7 University, Sacramento W121.4216°

American / Rossmoor Rd. ARRD N38.6218° 21 W121.3000°

American / Sunrise Blvd. ARLS N38.6273° 25 W121.2736°

Cosumnes / Twin Cities Rd. CRTC N38.2993° 6 W121.3799°

Cosumnes / Costello Forest CRCF N38.3586° 12 W121.3393°

Cosumnes / Freeman Rd. CRDD N38.3892° 14 W121.2973°

Cosumnes / Rancho Murieta CRRM N38.4835° 40 W121.1045°

Each site was sampled for bee richness, abundance, and floral preference; floral resources were sampled by measuring blooming plant richness and abundance (specific sampling methods follow below). Sampling occurred 5 times at approximately one-month intervals between April and September 2007. Because bee activity is tightly correlated with environmental conditions (LeBuhn et al.,

2003; Michener, 2000), variation due to changes in weather was minimized by sampling pairs of sites on each river (e.g., ARDP and CRTC) on consectutive days

(with one exception when there was a four day interval between sampling).

Landscape Analysis. Prior to sampling, the landscape surrounding each site was compared to detect differences in the major land-cover types between rivers.

The proportion of three land-cover types was determined within a 1.5 kilometer diameter around each site. The categories of interest in this study are: semi-natural, agricultural, and urban/suburban as described below.

Semi-natural habitats: included open herbaceous fields and levees typical of the

habitat along the American river corridor (also known as the American River

Parkway), riparian forests, and restored natural habitats (e.g. Effie Yeaw Nature

Center, and the Cosumnes River Preserve). Excluded from this category are

highly managed land types, such as golf courses, lawns and gardens.

Agricultural habitats: included dry crops of grains, irrigated row crops (e.g.

grapes, corn, legumes, and clovers), hedgerows, and irrigation canals, roads and

highways, and outbuildings.

Urban habitats: included residential, commercial, and industrial areas, parks

with highly managed land types (e.g., golf courses, lawns, and gardens that are

regularly mowed, fertilized, and watered), roads and highways, airports, and

empty lots (paved and unpaved).

Distinguishing among land-cover types was accomplished visually using aerial photographs supplied by Google Earth Pro © (Figure 2). The area (square kilometers) was measured by describing polygons around specific land-cover types within each circular area. In areas where the land-cover type was not readily distinguishable through aerial photographs, ground-truthing (by driving or walking through the questionable area) was used to make the final categorization.

Sampling Bee Richness, Abundance, and Floral Preferences. Bee richness and abundance in each site was estimated using a combination of pan trapping and sweep netting following LeBuhn et al., (2003). Passive pan traps were made of 6- ounce plastic bowls (Solo brand) of three colors, two of which were painted with florescent blue and yellow spray paint, and the other stock white. Two transects were laid out in the form of an ‘X’ in each plot (each transect was approximately 75 meters in length). Five bowls of each color were placed at 5 meter intervals along each transect (for a total of 15 pan traps per transect, and 30 pan traps per plot) and

U A W A N W W W A U N ARDP CRTC U A U A W N W U U N N A N A A ARSS CRCF

A U A W N N N W

ARRD CRDD

W U N N W N A U N U ARLS CRRM

Figure 2. Composition of land-cover types. Study sites along the American River (left panel) and Cosumnes River (right panel) from west (top) to east (bottom). U=Urban/Suburban; A=Agriculture; N=Semi-natural; W=Water.

filled with a non-scented soap water solution (one small “squirt” of Seventh

Generation brand liquid detergent per gallon). Pan traps were set out between 700 and 1700 hours, for a total of 8 hours per sampling event. Specimens were pooled at the end of each day by trap color, and stored in ethyl alcohol.

Active sweep netting was conducted to collect floral association data, as well as bees that do not typically visit pan traps (LeBuhn et al., 2003). Hand netting occurred for two 1-hour periods during the day—before and after noon—during which I randomly walked through the plot searching floral patches and along open patches of ground (for searching males and nesting females, and cleptoparasites), such that the entire plot was sampled twice daily. Specimens were separated according to the bloom on which they were collected, or based on their behavior

(e.g., flying, nest searching). Because of the difficulty accurately identifying bee species and sex, collecting floral association data by observation is generally not feasible. Three species, however, were considered distinct enough to collect data by observation: the sexually dimorphic and distinct species, Xylocopa veripuncta and

Agapostemon texanus, and the common Apis mellifera. The identification of bumblebees (Bombus species) by in-flight observation was attempted early on in the study; however, these data were not considered in the analysis due to subtleties in identification traits not discovered until later in the project.

Specimens were currated, pinned, and labeled following standard entomological practices (Borror and White, 1970; Borror et al., 1989), and

18 identified to species or morphospecies following Michener (2000). Males of morphospecies were not considered in the analyses of richness to minimize overestimating species due to gender dimorphism.

Sampling Floral Resources. Standard vegetation sampling methods typically do not consider the needs of bees in terms of the availability of pollen and nectar. Instead, they focus on the abundance or cover of individual plants, regardless of whether or not they are producing pollen or nectar at the time of sampling. Sampling methods that measure pollen and nectar are time and labor intensive, and thus do not easily lend themselves to the characterization of large areas. To quantify the floral resources available to bees in a quick and efficient way, this study only collected data on the richness and relative abundance

(described below) of plants in bloom during sampling. Richness data was sampled by recording plants in bloom during a sampling event. Identification, and native or non-native status, were determined using Hickman (1993). Voucher specimens were stored in the CSUS herbarium.

The relative abundance of flowering plants was determined using a modified Braun-Blanquet cover abundance scale (Barbour et al., 1987). Only plant species with open flowers were sampled, with the relative proportion of flowers in a site ranked into one of the following six percent cover classes: rare < 1% (mean

0.1), 1 = 1-5% (mean 2.5), 2 = 5-25% (mean 15.0), 3 = 25050% (mean 37.5), 4 =

50-75% (mean 62.5), and 5 = 75-100% (mean 87.5). Floral resource abundance

19 was calculated as the sum of means for all cover classes in flower at a sampling event. To minimize the bias inherent in this method, the same individual (B. Love) ranked all samples in this study.

Data Analysis. Because study sites were sampled repeatedly over time, the independence among replicates is in question, and this study design may be considered pseudoreplication (Hurlbert, 1984). However, this assumption may be minimized with bees because of their short adult lifespan, generally between 2 and

6 weeks (Stephen et al., 1969), and their ephemeral nature (Roubik, 1989). The idea that bees collected during a sampling event can bias subsequent sampling events was tested in a similar study which sampled bees bi-weekly (Messinger,

2006). By calculating similarity values between consecutive sampling events, it was determined that each event sampled an entirely new bee fauna.

Dependant variables tested for the bee communities included abundance, richness, diversity, and species eveneness. A repeated measures ANOVA was used to determine whether there were any differences in the dependant variables between the two rivers, between months, and between the two rivers within months. Dependant variables tested for the floral resources available to bees included species richness and abundance. A t-test was used to determine differences between rivers in total richness and abundance, as well as a comparison of native and nonnative richness and abundance.

Linear regression was used to test the relationship between floral resources

(richness and abundance) and the dependant variables, bee richness and abundance.

Contingency tests were used to investigate foraging preferences between native and nonnative bees. A bee community similarity dendrogram was calculated using a coefficient of Jaccard (Krebs, 1999).

A comparison of the different land-cover types (semi-natural, agriculture, and urban/suburban) was made between rivers using plots as replicates. The proportion of each land-cover type was tested using the nonparametric Wilcoxon test.

Statistical analyses were performed using R (version 2.8.0), and figures were plotted using Microsoft Excel (version 2007).

RESULTS

Landscape Analysis. Overall, sites along the American River had a greater proportion of urban land-cover than those on the Cosumnes River (89% versus

11%) (W = 15.5, P = 0.041) (Figures 2 and 3). In contrast, all of the agricultural land-cover was found along the Cosumnes River (W = 0, P = 0.021). Furthermore, there was no statistical difference in the proportion of this landscape matrix (89% urban on the American River, and 100% agriculture on the Cosumnes River) (W =

8.5, P = 1). There was no difference in the proportion of semi-natural habitat adjacent to either river (W = 6, P = 0.686).

Bee Communities. A total of 7910 bees were collected across all study sites during the 40 days of sampling between April and September 2007 (Table 2).

Overall, the sampling effort included 80 hours of hand netting and 320 hours of pan trapping. A total of 122 species in 34 genera were identified, representing four of the five bee families: Colletidae, Andrenidae, Halictidae, Megachilidae, and Apidae

(See Appendix A for species list). Each sampling event yielded a mean of 25.4 species (range: 15 – 38) and 197.7 individuals (range: 44 – 926). The bee community identified in this study represents 3% of the extant bee fauna in the contiguous United States.

For both rivers combined, bees in the family Halictidae accounted for the majority of individuals collected (61%), but only 20% of the species and 15% of

1.0

River 0.5 Agriculture Urban Proportion Semi-natural

0.0 CRTC CRCF CRDD CRRM ARDP ARSS ARRD ARLS

Cosumnes River American River

Figure 3. Proportion of land-cover types at each study site along the Cosumnes and American Rivers. Semi-natural habitat is found adjacent to each river, and the surrounding matrix is comprised of urban and agricultural development.

Table 2. Comparison of bee abundance (# of individuals), richness (# of species), diversity, and several community measures between each river. Diversity measures were calculated using pan trap data only. Standard error reported as ±1SE. P-values are for differences between rivers. No P-value indicates no statistical tests were performed.

American River Cosumnes River P-value Total Abundance (A) 2972 4938 7910 Mean Abundance per 148.6 ± 18.4 246.9 ± 44.8 P = 0.653 - Site Richness (S)(Gamma 105 97 122 Diversity) Mean Richness per 25.4 ± 2.0 25.3 ± 1.5 P = 0.845 - Site Unique Bee Species 35 27 - Mean Simpson’s 0.19 ± 0.02 0.22 ± 0.16 - Diversity Index (D) Mean Simpson’s 0.81 ± 0.02 0.78 ± 0.16 - Diversity (1-D) Mean Simpson’s 6.17 ± 0.61 5.11 ± 0.37 P = 0.424 - Reciprocal (1/D) per site Mean Shannon-Wiener 2.1 ± 0.08 2.0 ± 0.06 - Diversity Index (H) Mean Evenness 0.39 ± 0.03 0.31 ± 0.03 P = 0.012 - ((1/D)/S) per site Alpha Diversity 60.25 56.25 - Beta Diversity 1.74 1.72 -

24 the genera (Figure 4). Conversely, bees in the family Apidae accounted for the majority of species and genera (41% each), but only 19% of the individuals. Two genera accounted for over 50% of Apidae abundance: Melissodes (39.3%) and

Ceratina (17.4%). This diverse family also includes the non-native honeybee Apis mellifera, which accounted for 5% of total bee abundance and 24.3% of family level abundance. Megachilidae was dominated by 2 genera, Osmia and Megachile, which accounted for over 90% of Megachilidae abundance. Andrenidae species accounted for 12% of bee diversity, but less than 1% of abundance, while

Colletidae bees were both uncommon and localized.

Over half of all bee species sampled (55%) were represented by 10 or fewer individuals and 35% were singletons or doubletons (species represented by only one or two individuals, respectively). In contrast, four species, Halictus ligatus,

Lasioglossum incompletes, H. tripartitus, and L. morphospecies 1, accounted for

50% of the total number of individuals (Figure 5). These bee species are all from the family Halictidae, and the three identified species are known to exhibit social behavior. Although they were widespread, their abundances were typically skewed to one river or the other—with the exception of H. tripartitus, which was common on both rivers. The majority of species (65%) occurred at 4 or fewer study sites, with 31% occurring at only one site. Ten percent of bee species occurred at all 8

Both Rivers American River Cosumnes River a) Genera 11.8% 12.9% 10.3% 26.5% 25.8% 24.1%

41.4% 14.7% 41.2% 16.1% 41.9% 17.2%

3.2% 5.9% 6.9% b) Species 9.8% 10.5% 5.2% 26.3% 25.7% 29.9%

40.2% 40.6% 36.2% 19.5% 23.8% 20.6% 3.8% 3.8% 4.1% c) Individuals 0.9% 12.8% 1.3% 0.6% 16.2% 19.4% 18.3% 16.2% 24.7% 3.8% 2.8% 1.3%

60.0% 60.7% 61.1%

Andrenidae Apidae Colletidae Halictidae Megachilidae

Figure 4. A comparison of bee family diversity for bees collected at all study sites along the American and Cosumnes rivers in Sacramento County, California.

Abundance 0 200 400 600 800 1000 1200

Halictus ligatus Lasioglossum incompletus Halictus tripartitus Lasioglossum morphospecies 1 Megachile apicalis Apis mellifera Osmia nemoris Osmia regulina Lasioglossum morphospecies 5 Agapostemon texanus Halictus farinosus Melissodes stearnsi Melissodes tepida timberlakei Ceratina acantha Lasioglossum morphospecies 3 Hylaeus conspicuus Melissodes communis alopex Lasioglossum titusi Lasioglossum tegulariformis Melissodes lupina

American River Cosumnes River

Figure 5. Ranked abundance (# of individuals) of the top twenty most abundant bee species collected along the American and Cosumnes Rivers.

27 sites (Table 3). All but two of these species, Ashmeadiella aridula astragali and

Melissodes robustior) were in the top 20 most abundant species (Figure 5). Each study site had at least one unique bee species found in no other site, but more unique species were collected on the American River (34) than on the Cosumnes

River (27) (see Appendix A).

Bee Abundance, Richness, and Diversity. Overall, the mean number of bees

(± SE) on the American River (148 ± 18.4) was similar to the Cosumnes River

(246.9 ± 44.8) (Tables 2 and 4). Bee abundance for both rivers combined differed significantly across months and there was a river*month interaction (Figure 6 and

Table 4). Bee abundance peaked in June with a mean number (± SE) of 313 ± 96 bees and dropping to a low of 144 ± 23 bees in September. Bee species richness for both rivers combined declined monthly from a mean (± SE) high of 30 ± 2 in May, to 21 ± 2 in September (Figure 7 and Table 4). However there was no significant difference in the mean number of species between rivers, and no river*month interaction (Tables 2 and 4).

As measured by Simpson’s Reciprocal Diversity Index, bee diversity did not differ significantly between rivers (Table 2) nor was there a river*month interaction (Figure 8 and Table 4). Bee diversity for both rivers combined did change significantly across months, dropping from a mean ( ± SE) high of 7.6 ± 0.8 in May, to a low of 4.2 ± 0.5 in July, and increasing to 5.8 ± 0.9 in September.

Table 3. Abundance (number of individuals), nesting and social habits of the most widespread bee species (occurring at all 8 sites). Question marks indicate uncertainty in the natural history of the species.

Family/Species Abundance Nesting/Social Behavior Halictidae Agapostemon texanus 191 Ground/Solitary Halictus ligatus 1150 Ground/Social Halictus tripartitus 764 Ground/Social Lasioglossum incompletus 1119 Ground/Social? Megachilidae Ashmeadiella aridula astragali 67 Stem?/Solitary Megachile apicalis 440 Stem/Solitary Osmia nemoris 283 Ground & Stem/Solitary Osmia regulina 197 ?/Solitary Apidae Apis mellifera 371 Ground & External/Social Ceratina acantha 146 Stem/Solitary Melissodes lupina 79 Ground/Solitary Melissodes robustior 60 Ground/Solitary Melissodes tepida timberlakei 167 Ground/Solitary

Abundance Source SS df MS F P River 966289.9 1 966289.9 0.224 0.653 Month 159959.8 4 39990.0 7.287 < 0.01 River*Month 46932.3 4 11733.1 5.641 < 0.01 Error 683252.5.0 30 22775.1 Total 1856435.0 39

Richness Source SS df MS F P River 0.1 1 0.1 0.041 0.845 Month 451.3 1 451.3 13.733 < 0.01 River*Month 5 1 5 0.152 0.699 Error 678.1 36 18.8 Total 1134.5 39

Diversity Source SS df MS F P River 11.1 1 11.1 0.737 0.424 Month 47.6 4 11.9 5.687 < 0.01 River*Month 2.9 4 0.7 0.716 0.589 Error 142.7 30 4.8 Total 204.3 39

Community Evenness Source SS df MS F P River 0.08 1 0.08 12.656 0.012 Month 0.08 4 0.02 1.804 0.161 River*Month 0.02 4 0.01 0.216 0.927 Error 0.62 30 0.02 Total 0.81 39

700 600 500 400 300 Abundance 200 100 0 May Jun Jul Aug Sep

American River Cosumnes River

Figure 6. Comparison of bee abundance (# of individuals) along the American and Cosumnes Rivers between May and September 2007. Differences are significant across months with both rivers combined (p < 0.001), and there is a river*month interaction (p < 0.002). Error bars are ±1SE.

20 Richness 10

0 May Jun Jul Aug Sep

American River Cosumnes River

Figure 7. Comparison of bee species richness along the American and Cosumnes Rivers between May and September 2007. Differences are significant across months with both rivers combined (p < 0.001), but there is no river*month interaction (P = 0.699). Error bars are ±1SE.

10.0 9.0 8.0 7.0 6.0 5.0

Diversity 4.0 3.0 2.0 1.0 0.0 May Jun Jul Aug Sep

American River Cosumnes River

Figure 8. Comparison of bee diversity (Simpson’s Reciprocal Index) along the American and Cosumnes Rivers between May and September 2007. Differences are significant across months with both rivers combined (p < 0.002), but there is no river*month interaction (P = 0.589). Error bars are ±1SE.

Species evenness was significantly higher on the American River than on the Cosumnes River (Tables 2 and 4), but did not differ across months (with both rivers combined) nor was there a river*month interaction (Figure 9). A cluster analysis using Jaccard’s similarity index (Krebs, 1999) shows that the sites within each river system group together—with the exception of ARDP (Figure 10), which is located on the confluence with the American River and the Sacramento River.

Floral Resources. A total of 64 species of plants flowered during the study

(Table 5). Plant species richness was significantly higher on the Cosumnes River

(15.5 ± 0.7) than on the American River (10.6 ± 1.1) (t (33.9) = 3.762, p < 0.01)

(Figure 11). In contrast, there was no difference in floral resource abundance

(percent cover) between rivers (t (34.9) = 1.876, P = 0.069), with a mean abundance of 85.9 ± 7.0 along the American River and 108.2 ± 9.5 along the Cosumnes River

(Figure 12).

Non native plants were dominant in both species richness and abundance.

Of the forty seven plant species observed along the American River, 19 were native and 28 were non-native. Of the fifty eight plant species observed along the

Cosumnes River, 27 were native and 31 were non-native (Table 6). The pooled non-native plant species richness (8.6 ± 0.6) was significantly higher than the pooled native plant species richness (4.4 ± 0.3) (t (55.5) = 6.118, p < 0.01) (Figure

11). Similarly, pooled plant abundance data found that non-native plants were

0.6

0.4

Evenness 0.2

0.0 May Jun Jul Aug Sep

American River Cosumnes River

Figure 9. Comparison of bee community evenness along the American and Cosumnes Rivers between May and September 2007. Differences are not significant between months with both rivers combined (P = 0.161), and there is no river*month interaction (P = 0.927). Error bars are ±1SE.

ARDP

ARSS CRDD ARRD ARLS CRCF

CRTC CRRM

Figure 10. Jaccard Index of Similarity Dendrogram. Sites along each river share a higher level of similarity except for the site on the American (ARDP) closest to the Sacramento River confluence.

Table 5. List of plant species, family, native/non-native status, and occurence, observed at study sites along the American and/or Cosumnes Rivers in Sacramento County, California. Plants listed were in flower at some point during the study period between May and September 2007.

Plant Species Family Native/Non-native American Cosumnes Amsinckia menziesii Boraginaceae Native X X Anthemis cotula Asteraceae Nonnative X X Asclepias fascicularis Asclepiadaceae Native X Centaurea solstitialis Asteraceae Nonnative X X Chamaesyce serpyllifolia Euphorbiaceae Native X Cichorium intybus Asteraceae Nonnative X X Cirsium vulgare Asteraceae Nonnative X X Conium maculatum Apiaceae Nonnative X X Convolvulus arvensis Convolvulaceae Nonnative X X Datura wrightii Solanaceae Native X X Daucus carota Apiaceae Nonnative X Eremocarpus setigerus Euphorbiaceae Native X X Eriogonum gracile Polygonaceae Native X X Erodium botrys Geraniaceae Nonnative X X Erodium cicutarium Geraniaceae Nonnative X X Eschscholzia californica Papaveraceae Native X X Euthamia californica Asteraceae Native X X Foeniculum vulgare Apiaceae Nonnative X X Geranium carolinianum Geraniaceae Native X X Ghaphalium californicum Asteraceae Native X Grindelia camporum Asteraceae Native X Hieracium argutum Asteraceae Native X X Helianthus annuus Asteraceae Native X X Hemizonia pungens Asteraceae Native X X Heterotheca grandiflora Asteraceae Native X Heterotheca oregona Asteraceae Native X Hirschfeldia incana Brassicaceae Nonnative X X Holocarpha virgata Asteraceae Native X Hypericum perforatum Hypericaceae Nonnative X X Lactuca serriola Asteraceae Nonnative X X Lathyrus jepsonii Fabaceae Native X Leontodon taraxacoides Asteraceae Nonnative X Lepidium latifolium Brassicaceae Nonnative X X Lotus corniculatus Fabaceae Nonnative X Lotus purshianus Fabaceae Native X X Lotus scoparius Fabaceae Native X X

Table 5 (continued) Plant Species Family Native/Non-native American Cosumnes Lupinus benthamii Fabaceae Native X Lupinus bicolor Fabaceae Native X Lupinus spp. Fabaceae Native (?) X X Marrubium vulgare Lamiaceae Nonnative X X Medicago polymorpha Fabaceae Nonnative X X Melilotus alba Fabaceae Nonnative X X Melilotus indicus Fabaceae Nonnative X Mentha pulegium Lamiaceae Nonnative X Mentzelia laevicaulis Loasaceae Native X Nicotiana attenuate Solanaceae Native X X Nicotiana quadrivalvis Solanaceae Native X Oenothera elata Onagraceae Native X X Oxalis corniculata Oxalidaceae Nonnative X X Phyla nodiflora Verbenaceae Native X X Plagiobothrys nothofulvus Boraginaceae Native X Plantago species Plantaginaceae Nonnative (?) X Raphanus sativus Brassicaceae Nonnative X X Rosa californica Rosaceae Native X X Rubus concolor Rosaceae Nonnative X X Sambucus mexicana Caprifoliaceae Native X X Silybum marianum Asteraceae Nonnative X X Sisymbrium altissimum Brassicaceae Nonnative X Solanum elaeagnifolium Solanaceae Nonnative X Sonchus spp Asteraceae Nonnative (?) X X Spergularia rubra Caryophyllaceae Nonnative X X Trifolium hirtum Fabaceae Nonnative X X Verbascum blattaria Scrophulariaceae Nonnative X X Verbascum Thapsus Scrophulariaceae Nonnative X Verbena bonariensis Verbenaceae Nonnative X X Verbena lasiostachys Verbenaceae Native X Vicia villosa Fabaceae Nonnative X X

18 16 14 12 10 Total 8 Native Richness 6 Non-native 4 2 0 American River Cosumnes River

Figure 11. Comparison species richness of plants in flower along the American and Cosumnes Rivers. Total richness was higher on the Cosumnes River (p < 0.01). Non-native richness of both rivers combined was higher than native richness (p < 0.01). Error bars are ±1SE.

120

100

Total 60 Native Abundance 40 Non-native

0 American River Cosumnes River

Figure 12. Comparison of the abundance (% cover) of plants in flower along the American and Cosumnes Rivers. Total abundance between rivers was not significant (P = 0.07). Non-native abundance between both rivers combined was higher than native abundance (p < 0,01). Error bars are ±1SE.

Table 6 . Abundance (% cover) and richness (# of species) of plants in flower along each river between May and September 2007. Standard error reported as ±1SE. P- values are for differences between rivers. No P-value indicates no statistical tests were performed.

American Cosumnes River River P-value Total Mean Abundance (A) 85.9 ± 7.0 108.2 ± 9.5 P = 0.069 n/a Mean Abundance 20.8 ± 3.3 34.3 ± 8.3 27.7 ± 4.5 Native Mean Abundance Non- 65.2 ± 6.5 74.0 ± 5.7 69.8 ± 4.3 native Richness (S) 47 58 64 Richness Native 19 27 31 Richness Non-native 28 31 33 Mean Total Richness 10.6 ± 1.1 15.5 ± 0.7 P < 0.001 n/a Mean Native Richness 3.9 ± 0.4 4.8 ± 0.4 4.4 ± 0.3 Mean Non-native 6.7 ± 0.9 10.5 ± 0.7 8.6 ± 0.3 Richness

41 significantly more abundant than nonnative plants (69.8 ± 4.3 and 27.7 ± 4.5, respectively) (t (77.9) = 6.751, p < 0.01) (Figure 12).

The Influence of Plants on Bees. Bee species richness was positively related to plant species richness (F (1,38) = 4.225, P = 0.047) (Figure 13). However, plant richness did not explain much of the variation in bee richness (R2 = 0.101), suggesting a weak effect. No correlation was found between bee abundance and plant species richness (F (1,6) = 0.634, P = 0.456) (Figure 14), nor between bee species richness and floral resource abundance (F (1,38) = 1.282, P = 0.265) (Figure

15). Bee abundance was not related to floral resource abundance (F (1,38) = 0.020, P

= 0.737) (Figure 16a). However, when data for each river were analyzed separately, floral resource abundance did have a positive effect on bee abundance on the

American River (F (1,18) = 4.555, P = 0.047) (Figure 16b) , but not on the Cosumnes

River (F (1,18) = 0.116, P = 0.888) (Figure 16c). Even so, floral resource abundance did not explain much of the variation in bee abundance (R2 = 0.202), suggesting a weak relationship.

Nonnative Bees and Plants. Five species of nonnative bees were collected during this study: Apis mellifera (371 individuals), Ceratina dallatorreana (55 individuals), Megachile apicalis (440 individuals, M. rotundata (21 individuals), and Hylaeus bisinuatus (2 individuals). An additional nonnative species—Hylaeus spatulariella—was collected in a nearby urban garden during the same time period

20 Bee Richness Bee 10

0 0 5 10 15 20 25 Plant Richness

American River Cosumnes River

Figure 13. Regression of bees species richness on plant species richness (P =0.047, R2 = 0.10).

1000

800

600

400

Bee Abundance 200

0 0 5 10 15 20 25 Plant Richness

American River Cosumnes River

Figure 14. Regression of bee abundance on plant species richness (P = 0.456, R2 = 0.10).

40 35 30 25 20 15 10 Bee Species Species Bee Richness 5 0 0 20 40 60 80 100 Floral Resource Abundance

Figure 15. Regression of bee species richness on floral resource abundance (P = 0.265, R2 = 0.03).

45 a)

1000 750 500 250 0 0 20 40 60 80 100 b) 500 400 300 200 100 Bee Abundance 0 0 20 40 60 80 c)

1000 800 600 400 200 0 0 20 40 60 80 100 Floral Resource Abundance

° American River • Cosumnes River

Figure 16. Regression of bee abundance on floral resource abundance. a), both rivers combined (P = 0.888, R2 = < 0.01); b), the American River (P = 0.047, R2 = 0.202); c), the Cosumnes River (P = 0.737, R2 = 0.01).

(S. Greenleaf, unpublished). The mean ( ± SE) number of nonnative bees

(excluding Apis) collected during a sampling event was 4.2 ±1.0 and 21.8 ±8.4 on the American and Cosumnes Rivers, respectively. Nonnative bee abundance (less

Apis) was slightly higher on the Cosumnes River than on the American River (t

(19.6) = 2.084, P = 0.050). The distribution of the total number of nonnative bees is shown in Figure 17.

Nonnative bees (including Apis) have a preference for nonnative plants

(Pearson’s Chi-squared test, P = 0.047). However, when Apis and non-Apis nonnative bees are analyzed separately, Apis shows a stronger preference for nonnative plants (Fisher’s Exact test, P = 0.018, odds ratio 1.48), while non-Apis nonnative bees do not (Fisher’s Exact test, P = 0.366, odds ratio 1.19). Based on the odds ratio, which is a measure of the likelihood that a bee will visit a native or nonnative plant, honeybees are 1.5 times as likely to visit nonnative plants, whereas other nonnative bees show no preference.

Nonnative plants accounted for the majority of plant richness and floral resource abundance (Figures 11 and 12, respectively). Appendix B lists the bee visitors of all plant species (natives and nonnatives). Eight of the 11 plant species most attractive to bees were nonnatives, and three nonnative plants—Hirschfeldia

400

350

300

250 Ceratina dallatorreana 200 Megachile apicalis

Abundance 150 Megachile rotundata Hylaeus bisinuatus 100

0 American Cosumnes

Figure 17. Distribution of the total numbers of nonnative bees (excluding Apis) collected between May and September 2007.

incana, Centaurea solstitialis, and Cichorium intybus, attracted 61% of bee diversity collected during this study.

Comparison of Hand Netting and Pan Trapping. Table 7 lists the bee species collected by either pan traps or hand netting. Pan trapping collected over

6,000 specimens, yet represented only 73% of total bee richness. Hand netting collected over 1,600 specimens, representing 90% of the total bee richness identified during this study. Twice as many species unique to a particular collection method were collected by hand netting compared with pan trapping (41 versus 22, respectively). Pan trapping, however, collected a larger percentage of specialist bee species than did hand netting (27.3% versus 18.6%).

Table 7. List of bee species collected either by hand netting or pan trapping. Numbers following names denote distinct morphospecies. Question marks denote unconfirmed identification.

Hand Netted Species Pan Trapped Species Andrena auricoma Andrena subchalybea Andrena candida Ceratina sequoia Andrena morphospecies 1 Diadasia bituberculata Andrena piperi Diadasia consociata Anthidiellum notatum Diadasia olivacea Anthidium formosum Diadasia rinconis rinconis Bombus crotchii Exomalopsis yoloensis Bombus edwardsii Lasioglossum morphospecies 8 Bombus vandykei Lasioglossum morphospecies 9 Calliopsis anthidius anthidius Melissodes pallidisignata (?) Ceratina punctigena Nomada morphospecies 1 Coelioxys octodentata Nomada morphospecies 3 Colletes hyalinus Panurginus morphospecies 1 Dianthidium platyurum Peponapis pruinosa Dianthidium ulkei ulkei Perdita morphospecies 3 Dieunomia nevadensis angelesia Perdita morphospecies 4 Hylaeus bisinuatus Sphecodes morphospecies 2 Lasioglossum mellipes Sphecodes morphospecies 3 Lasioglossum morphospecies 10 Triepeolus heterurus Lasioglossum sisymbrii Triepeolus morphospecies 10 Megachile angelarum Triepeolus morphospecies 4 Megachile inimica jacumbensis Triepeolus morphospecies 6 Megachile perhirta Melissodes bimatris (?) Melissodes grindelia (?) Melissodes hurdi Nomada morphospecies 2 Nomada morphospecies 4 Osmia montana Osmia morphospecies 1 Perdita morphospecies 1 Perdita morphospecies 2 Protosmia rubifloris Sphecodes morphospecies 1 Svastra obliqua expurgata Triepeolus concavus Triepeolus morphospecies 1 Triepeolus morphospecies 3 Triepeolus morphospecies 5 Triepeolus morphospecies 7 Xeromelecta californica

DISCUSSION

This study suggests that semi-natural habitat surrounded by agricultural or urban landscapes can support diverse bee communities despite the extensive land conversions experienced in the Central Valley during the past 150 years. The bee communities along each river share many similarities, including a number of common bee species and diversity patterns. Nonetheless, the bee communities in these two habitats exhibit many unique characteristics, such as a set of bees found only on one or the other river. The fact that these two habitats support diverse, and yet unique, bee communities is an indicator that both are of value in the conservation efforts of bees.

The bee communities along the American and Cosumnes Rivers include a number of common bee species, many of which are generalist foragers able to utilize floral resources from a host of different plant species—a strategy common in disturbed habitats (Cane, 2005b). Specialized bees are typically uncommon in highly disturbed habitats because of their fragile relationship with specific plants

(Michener, 2000; Vasquez and Simberloff, 2002; Fenster et al., 2004), and while this study cannot make comparisons with pristine habitat, the fact that specialized bees occur here is insightful. For instance, the sunflower specialist Diadasia enavata, and the squash specialist Peponapis pruinosa, commonly occurred on

51 both rivers, and there were a number of other specialists as well, including species from the genera: Calliopsis, Dianthidium, Megachile, Ashmeadiella, Osmia,

Melissodes, Diadasia, and Svastra. The presence of oligolectic bees is therefore promising, suggesting that not all disturbed habitats are devoid of specialized plant- pollinator relationships.

Both bee communities also support a number of unique species. For instance, the large carpenter bees Xylocopa were only found on sites along the

American River, despite the presence of woody nest substrate on the Cosumnes

River. These bees are generally common in North America (Hurd, 1955) and in

Sacramento (personal observation), making any attempt at explaining their absence on the Cosumnes sites speculative. There are also instances where closely related species are separated by river. Two common ground-nesting bees, Melissodes stearnsi, and M. communis alopex were not found to co-occur. Further investigation into the niche each species fills would clarify whether this separation has ecological significance, or whether this pattern is simply be due to rarity and sampling biases, as is often the case in surveys.

The overall bee richness identified in this study indicates that a rich and diverse bee community can persist in sub-marginal habitat. Even so, the variable spatial and temporal dynamics of bees place limits on single year surveys and support the need for long-term monitoring programs (Herrera, 1988; Frankie et al.,

1998; Williams et al., 2001; LeBuhn et al., 2003). Multi-year programs reveal the dynamic nature of bee communities, and better account for their diversity (Cane et al., 2006; Messinger, 2006). Because this study examined at bee species richness and diversity over only one year, there are likely species that were not detected.

Bee species richness and diversity can be expected to increase early in the flowering season to some peak, and then decline as the season ends, tracking floral blooms. The decline in bee richness throughout the course of this study indicates that peak bee richness occurred either at the start of the study or earlier. It appears that capturing this peak may require sampling to begin earlier in the year, most probably in late February or early March. It is not uncommon for some bees to begin emerging in late winter, especially larger bees such as Bombus, Xylocopa, and Anthophoridae species (personal observation). Nonetheless, the high level of diversity identified during the course of this study suggests that bee communities in the Sacramento Valley persist in urban and agricultural landscapes.

Urban and Agricultural Habitats as Bee Refugia. The value of urban/suburban and agricultural landscapes in providing habitat for bee diversity has not been adequately explored (Cane, 2005a). However, there is mounting evidence that these highly modified land types—often considered deleterious to diversity, or at least sub-marginal—can be beneficial for native bee communities

(Kremen et al., 2004; Hisamatsu and Yamane, 2006; Fetridge et al., 2008;

Matteson et al., 2008). Additionally, creating and enhancing quality bee habitat can be achieved with little financial investment, be easily combined with other restoration or rehabilitation efforts (for wildlife, birds, water conservation, etc.), and enhance agricultural pollination (Thorp, 2003; Torchio, 2003; Ricketts, 2004;

Greenleaf and Kremen, 2006b), while providing natural green-space in otherwise anthropogenicaly modified environments.

As this, and other studies have shown, anthropogenically modified habitats can provide bees with the necessary foraging and nesting resources, as evidenced by the diverse bee communities found in—and around—urban and agricultural environments (McIntyre and Hostetler, 2001; Cane, 2005a; Frankie et al., 2005;

Cane et al., 2006; Greenleaf and Kremen, 2006b; Winfree et al., 2007b).

Consequently, creating or enhancing habitat may be achieved by providing the two fundamental resources required by bees—flowering plants and nest substrate—in sufficient quantity and quality. Because bees are central place foragers, meaning that they repeatedly leave their nest to collect nest-building and -provisioning materials, the spatial arrangement of these resources is important. Both nesting and floral resources must be within the flight range of the bee in order to be of use. For example, large patches of resource-rich flowers alone are not enough to support bee populations in the absence of suitable nesting substrate. The range over which bees will forage is dependent on body size, with large-bodied bees capable of larger

54 ranges than small-bodied bees (Osborne et al., 1999; Gathmann and Tscharntke,

2002; Greenleaf et al., 2007; but see Cane, 2005b). As a result, the diversity and persistence of bee populations is influenced by the size and connectivity of resource islands, as suggested by island biogeography theory (MacArthur and Wilson,

1967).

Temporal variation of floral resources can also influence which species of bees can inhabit a specific habitat. The timing of floral blooms must coordinate with the emergence of bees, and must persist in sufficient quantity and quality throughout their flight season, which vary considerably between species and even sex. Male bees, for instance, typically emerge before females to prepare for their arrival, as was the case with Diadasia enavata in this study. Males emerge first, set up mating territories, and rely on the presence of any nectar-producing plant to build up their energy reserves while waiting for the females to emerge. Females of this oligolectic species, however, rely on pollen from specific plant species to provision nests; therefore, the flowering phenology is critical for bee breeding success.

Other bees, such as the generalist Agapostemon texanus—a multivoltine species—exhibit bimodal flight seasons. In this species males and females emerge together early in the season to mate; the male population subsequently decreases while females provision the first brood. Populations spike again later in the season

55 when the second generation emerges to mate and ultimately diapause during the winter (Roberts, 1969). In this example, specific plant species are not as important as having sufficient quantities of pollen and nectar at the beginning of the season and persisting long enough to raise two broods. Temporal requirements can be summarized into four basic groups: early-, middle-, and late-season bees, and those species with long flight seasons. Therefore bee diversity in a given habitat can be expected to correlate with the temporal availability of blooms in much the same way as plant diversity can provide foraging resources for generalists or specialists.

The qua lity of floral resources is also an important consideration. For example, many horticultural varieties provide few, if any, resources (J. Cane, personal communication). While these types of flowers are typically large and showy, they may in fact be deleterious to bees by consuming their efforts and energy with no return in investment. Others, such as the native California poppy

(Eschscholzia californica) provide pollen, but no nectar. This species provides an important resource for nest-provisioning females, but it must be present with nectar-producing species to provide the fuel needed for adults.

In addition, and contrary to many restoration/rehabilitation efforts, the most important decisions are not necessarily whether a plant species is native or nonnative to a particular location (as is the case with native plant conservation groups), but whether the plant provides a useful resource in sufficient quantity and

56 quality, and at the right time. Recent work in the city of Davis, California, indicate that nonnative plant species provide critical resources for native butterfly species and that removing certain nonnative plants can have a detrimental effect on butterfly populations (Shapiro, 2002). Considering the dominance of nonnative plants identified during this study, the same condition may hold true in Sacramento

County—at least to some degree. Efforts to eradicate undesirable species in semi- natural habitat along the American and Cosumnes rivers (e.g., Yellow Star thistle,

Centaurea solstitialis) should take into consideration the role nonnative plant species play for bees in these disturbed habitats. Just as increasing the spatial and temporal variation in floral resources has been shown to be positively correlated with bee diversity (Messinger, 2006), so can the reduction in resources be expected to negatively impact bee communities.

Implications of Nonnative Bees. Three of the four species of nonnative bees identified in this study, excluding the honey bee Apis mellifera, were accidentally introduced: Megachile rotundata, M. apicalis, Ceratina dallatorreana and Hylaeus bisinuatus. Two of the species (M. rotundata and M. apicalis) are now commercially managed pollinators of alfalfa crops (Goulson, 2003).

Threats to biodiversity as a result of invasive species are well recognized and account for half of the threats to imperiled species, surpassed only by habitat loss (Wilcove et al., 1998). The term “invasive” refers to the potential negative

57 ecological impacts often associated with the abrupt movement of a species into a novel habitat where there is no shared evolutionary history between indigenous and nonnative biota. The sudden introduction of species into novel habitats is a natural phenomenon, as stochastic events have historically facilitated the mixing of formerly isolated species and populations (Mooney and Cleland, 2001). However, humans have accelerated the rate of introductions over the past 500 years— often accidentally, but sometimes intentionally, as with the introduction of the honey bee,

Apis mellifera. While it is not clear whether—or to what extent—there is competition between native bees and Apis today (Goulson, 2003; Paini, 2004;

Moritz et al., 2005; Thomson, 2006), it is likely that any dramatic displacements, extirpations, or long-term effects on the native bee community took place when

Apis was first introduced in the early 1600’s (DeGrandi-Hoffman, 2003). Results from this study appear to support this position, as Apis abundance was not very high, nor could their slight preference for nonnative plants be explained by anything other than the dominance of nonnative plants in the environment.

Freed from the constraints of natural competitors, predators and pathogens, introduced species can quickly dominate a habitat. In doing so, they exploit resources to such an extent as to displace—and sometimes extirpate—local fauna, as occurred on the island of Guam with the introduction of the brown tree snake

(Fritts and Rodda, 1998). Nonnative species can also modify colonized habitats by

58 changing the frequency and intensity of natural disturbances such as fire (Brooks et al., 2004) and flood regimes (Sher et al., 2000), and generally disrupt evolutionary relationships forged over geologic time periods by natural selection (Mooney and

Cleland, 2001). We will never know the ecological impacts of the honey bee in

North America. However, we do know it is unlikely that humans will cease the introductions of nonnative species anytime soon.

Nonnative bee species from 28 genera were intercepted at U.S. ports and checkpoints between 1974 and 1985 (Batra, 2003). Fortunately, the vast majority of individuals and species do not establish viable populations (Batra, 2003). There are

21 species of nonnative bees currently inhabiting North America, 17 of which were accidental introductions (Cane, 2003). Besides the honey bee, three nonnative bee species have been intentionally introduced for use in agricultural production:

Osmia cornifrons and O. cornuta, for the pollination of spring-blooming fruit trees, and Anthophora plumipes, for blueberries (Cane, 2003). Interestingly, two of the accidental introductions have turned out to be useful in agricultural systems. The leafcutter Megachile rotundata and M. apicalis, have been found to be efficient and manageable pollinators of alfalfa crops (Stephen, 2003).

Bee Sampling Considerations. The effects of intensive sampling regimes on bee populations are not well known. Insects are generally considered r-selected organisms, with rapid reproduction and high fecundity (Borror et al., 1989).

Indeed, the richness of the global bee fauna would seem to support this claim. A closer look at the natural history of bees, however, reveals a different story. The average number of offspring produced by a single bee during her lifetime is far lower than many other insects, typically between 20 and 30 individuals. (Linsley

1958; Stephen et al., 1969). This suggests that bees may lean more towards k- selection rather than r-selection. If this is indeed the case (I have not found evidence either supporting or refuting this claim, although I have had personal communication with experts insisting that bees are r-selected) then there could be serious impacts of the common sampling efforts employed in bee conservation.

Contemporary bee community sampling designs utilizes a combination of pan trapping and net sampling to accurately and objectively estimate bee richness and abundance. Both methods have advantages and disadvantages under specific conditions. For instance, understanding the attractiveness of specific plant species requires hand netting bees directly on open flowers. Pan traps, however, collect bees indiscriminately without regard to floral preferences. Conversely, pan traps are useful for collecting the abundance and density of bees in a specific area because they standardize the collecting effort by bowl color, size, distribution, and time. In addition, pan traps are particularly useful when collecting for long periods of time, or in habitats devoid of blooms (e.g., after a fire or other disturbance, and before or after peak blooming periods).

A potential bias of pan trapping was described by Cane et al. (2000), who suggest that pan trap attractiveness (i.e., its efficiency) is inversely proportional to local floral productivity. In other words, bees are less attracted to pan traps when floral resources are abundant. I have observed similar conditions where the lack of blooms in a habitat yielded high numbers of bees collected in pan traps. It has been suggested that data collected in habitats with scarce floral resources do not represent the local bee community because bees in such habitats are more apt to increase their foraging ranges (Jack Neff, personal communication at The Bee

Course, 2006).

Using a combination of hand netting and pan trapping can increase the number of species collected during a study or survey. Of the 30 species collected in one study, 17 species were unique to hand netting, 8 species were unique to pan trappping, and 5 species were collected by both methods (Cane et al., 2000). The results of my study support this trend. Hand netting yielded 43 unique species and

22 species were unique to pan trapping. Interestingly, hand netting required 60% less specimens to yield double the number of unique species (1,657 individuals collected by hand net verses over 6,000 in pan traps). This result suggests that hand netting may be a desirable approach in describing the general bee richness of a habitat while minimizing the number of individuals removed.

Continued research into the effects of long term monitoring programs on bee community population dynamics is warranted, especially considering the potential pollinator crisis we are facing, and the conflict between our need to collect

(i.e., kill) bees in order to conserve them.

Conclusion. We will never know the bee community that serviced the carpets of wildflowers enjoyed by John Muir. That we have come to recognize the absolute necessity of bee pollinators in maintaining plant diversity in general as well as supplying us with a significant proportion of our food requirements is promising. Acting on concerns initiated by declines in honey bee populations and other high profile bee pollinator declines (i.e., bumble bees) is beneficial to humans and bees alike. Increasing and enhancing bee habitat in human dominated landscapes provide necessary refugia for bees, while insuring against the loss of pollination services essential for food production.

This study has shown that native bee communities can persist in semi- natural habitats surrounded by intensely modified landscapes. In addition, conservation efforts can be employed by individuals at the home garden level, as well as land managers and policy makers. Increasing public awareness of the essential nature of bee pollinators, their fundamentally benign nature, and the ease with which we can incorporate bee habitat into our conservation efforts, will go a

62 long way in mitigating the effects of anthropogenic land conversions on native bee diversity.

APPENDIX A

Species list of bees and numbers of individuals collected in semi-natural habitat along the American and Cosumnes Rivers in Sacramento County, California in 2007. Nonnative bee species followed by an asterisk. Bee species unique to a river are followed by a dagger (†) Column N (nesting habit): G = ground; S = above ground stem, twig, cavity, or wood; E = external nesting. Column B (social behavior): blanks are considered solitary species; S = social; PS = primitively social; C = cleptoparasite; Com = communal. Column F (floral foraging behavior): blanks are unknown, but probably generalists (polylectic); P = generalist; O = specialist. A question mark proceeded by a letter indicates unsure.

Species American Cosumnes N B F Colletidae Colletes hyalinus 2 G? Hylaeus bisinuatus* † 2 S O Hylaeus conspicuous 5 138 S? ? Hylaeus episcopalis giffardiella 18 10 S Hylaeus mesillae cressoni 14 36 S? ? Andrenidae Andrena auricoma † 5 G Andrena candida † 4 G Andrena morphospecies 1 5 6 G Andrena piperi † 1 G P Andrena plana 1 1 G Andrena subchalybea † 13 G Calliopsis anthidius anthidius 1 1 G? O Calliopsis obscurella † 17 G? O Panurginus morphospecies 1 † 1 G? Perdita morphospecies 1 † 10 G? Perdita morphospecies 2 † 2 G? Perdita morphospecies 3 † 1 G? Perdita morphospecies 4 † 1 G? Halictidae Agapostemon texanus 131 61 G P Dieunomia nevadensis angelesia 4 6 G P Halictus farinosus 25 147 G PS P

APPENDIX A (cont.)

Species American Cosumnes N B F Halictus ligatus 186 964 G P Halictus rubicundus 18 9 G PS P Halictus tripartitus 331 436 G P Lasioglossum incompletus 153 967 G ? P Lasioglossum kincaidii 3 13 G? ? P? Lasioglossum mellipes † 1 G? ? O? Lasioglossum morphospecies 1 590 16 G? ? Lasioglossum morphospecies 2 38 21 G? ? Lasioglossum morphospecies 3 107 37 G? ? Lasioglossum morphospecies 4 59 1 G? ? Lasioglossum morphospecies 5 21 176 G? ? Lasioglossum morphospecies 6 7 15 G? ? Lasioglossum morphospecies 7 5 15 G? ? Lasioglossum morphospecies 8 6 1 G? ? Lasioglossum morphospecies 9 † 1 G? ? Lasioglossum morphospecies 10 † 2 G? ? Lasioglossum morphospecies 11 † 4 G? ? Lasioglossum sisymbrii † 2 G P Lasioglossum tegulariformis 84 16 G Lasioglossum titusi 1 113 G? ? O? Sphecodes morphospecies 1 † 1 G C Sphecodes morphospecies 2 1 1 G C Sphecodes morphospecies 3 † 2 G C Megachilidae Anthidiellum notatum 10 1 E P Anthidium formosum † 3 ? O Ashmeadiella aridula astragali 30 35 S? Ashmeadiella cactorum 1 4 S? O Ashmeadiella californica 4 19 ? Ashmeadiella opuntiae † 3 S O Coelioxys octodentata 2 S? C Dianthidium platyurum † 5 E

APPENDIX A (cont.)

Species American Cosumnes N B F Dianthidium pudicum 2 3 E Dianthidium ulkei ulkei † 1 E/G O Hoplitis producta gracilis 11 3 S P Megachile angelarum 8 5 S? P? Megachile apicalis* 56 384 S P Megachile brevis brevis 5 21 G/S? P Megachile brevis onobrychidis 4 11 G/S? P Megachile fidelis 7 7 ? P Megachile gemula † 4 ? P Megachile gentilis 6 6 S P Megachile inimica jacumbensis † 4 S O Megachile morphospecies 1 2 3 ? Megachile perhirta † 2 G P Megachile rotundata* 23 2 S P Megachile texana † 2 G P Osmia aglaia 10 2 S Osmia albolateralis 11 2 S Osmia atrocyanea 3 3 S Osmia cyanella † 4 S? Osmia laeta 19 4 G? Osmia montana † 1 G O Osmia morphospecies 1 † 2 ? Osmia nemoris 46 255 G/S Osmia nigrifrons † 3 G/S Osmia regulina 103 94 ? Osmia texana 1 20 S Protosmia rubifloris † 1 E Apidae Anthophora curta 9 10 G Anthophora urbana 9 10 G P Apis mellifera* 191 181 G/E S P Bombus californicus 5 16 G S P

APPENDIX A (cont.)

Species American Cosumnes N B F Bombus crotchii 1 G S P Bombus edwardsii 1 1 G S P Bombus vandykei 3 1 G S P Bombus vosnesenskii 4 10 G S P Ceratina acantha 87 59 S P? Ceratina arizonensis 55 8 S P? Ceratina dallatorreana* 6 49 S P Ceratina punctigena † 1 S P? Ceratina sequoia † 2 S O Diadasia bituberculata 1 G O Diadasia consociate 2 4 G O Diadasia enavata 8 67 G O Diadasia olivacea 1 G O Diadasia rinconis rinconis † 2 G O Eucera actuosa 2 14 G P Eucera edwardsii 13 3 G P Eucera frater albopilosa 7 9 G Exomalopsis yoloensis † 1 G Com Melissodes agilis 4 3 G O Melissodes bimatris (?)† 2 G Melissodes communis alopex † 115 G P Melissodes grindelia (?) 1 1 G Melissodes hurdi † 3 G Melissodes lupine 25 54 G O Melissodes pallidisignata (?) 3 1 G Melissodes robustior 21 35 G O Melissodes stearnsi 169 G O Melissodes tepida timberlakei 101 65 G P Nomada morphospecies 1 † 1 G C Nomada morphospecies 2 † 1 G C Nomada morphospecies 3 † 1 G C Nomada morphospecies 4 † 1 G C

APPENDIX A (cont.)

Species American Cosumnes N B F Peponapis pruinosa 2 5 G O Svastra obliqua expurgate 12 3 G O Triepeolus concavus † 2 G C Triepeolus heterurus † 1 G C Triepeolus morphospecies 1 † 1 G C Triepeolus morphospecies 2 1 1 G C Triepeolus morphospecies 3 † 1 G C Triepeolus morphospecies 4 † 1 G C Triepeolus morphospecies 5 † 2 G C Triepeolus morphospecies 6 † 3 G C Triepeolus morphospecies 7 † 3 G C Triepeolus morphospecies 8 † 3 G C Triepeolus morphospecies 9 † 4 G C Triepeolus morphospecies 10 † 1 G C Xeromelecta californica † 1 G C Xylocopa tabaniformis † 12 S PS P Xylocopa veripuncta † 15 S PS P

APPENDIX B

Bee-visited plant list in semi-natural habitat along the American and Cosumnes Rivers in Sacramento County, California in 2007. The list includes native/nonnative plant status, bee species names, and number of occurrences in the study across all samples (denoted by non-italic numeral following species name). Different morphospecies are denoted by italicized numeral following species name.

Apiaceae Daucus carota (nonnative) Apis mellifera 4, Halictus farinosus 4, Halictus ligatus 5, Halictus rubicundus 2, Hylaeus episcopalis giffardiella 1, Hylaeus mesillae cressoni 13 Foeniculum vulgare (nonnative) Apis mellifera 1

Asteraceae Anthemis cotula (nonnative) Apis mellifera 1, Ceratina acantha 2, Halictus farinosus 3, Halictus ligatus 12, Halictus tripartitus 1, Hylaeus conspicuus 3, Lasioglossum morphospecies 6 1, Lasioglossum tegulariformis 1, Lasioglossum titusi 2, Megachile apicalis 1 Centaurea solstitialis (nonnative) Agapostemon texanus 4, Anthophora curta 4, Anthophora urbana 3, Apis mellifera 38, Bombus vosnesenskii 2, Ceratina acantha 9, Ceratina dallatorreana 3, Diadasia enavata 3, Dianthidium platyurum 1, Halictus farinosus 7, Halictus ligatus 60, Lasioglossum morphospecies 1 4, Lasioglossum morphospecies 3 3, Lasioglossum morphospecies 4 1, Megachile apicalis 63, Megachile brevis brevis 2, Megachile brevis onobrychidis 1, Megachile fidelis 3, Megachile gentilis 1, Megachile inimica jacumbensis 1, Megachile perhirta 1, Megachile rotundata 1, Melissodes bimatris (?) 1, Melissodes communis alopex 2, Melissodes grindelia (?) 1, Melissodes lupina 2, Melissodes robustior 5, Melissodes stearnsi 1, Melissodes tepida timberlakei 5, Osmia nemoris 2, Osmia texana 1, Svastra obliqua expurgata 11, Triepeolus concavus 2, Triepeolus morphospecies 5 1 Cichorium intybus (nonnative) Agapostemon texanus 4, Apis mellifera 10, Ashmeadiella californica 1, Ashmeadiella opuntia 1, Bombus sp. 4, Bombus californicus 1, Bombus crotchii 1, Bombus vosnesenskii 3, Ceratina acantha 1, Dianthidium platyurum 3, Eucera actuosa 1, Halictus farinosus 3, Halictus ligatus 5, Halictus tripartitus 1, Hylaeus conspicuus 2, Lasioglossum kincaidii 4, Lasioglossum morphospecies 5 1, Lasioglossum titusi 2, Megachile apicalis 9, Megachile brevis brevis 1, Megachile brevis onobrychidis 1, Megachile fidelis 1, Megachile gentilis 1, Melissodes lupina 2, Melissodes robustior 3, Osmia montana 1, Osmia regulina 2, Osmia texana 2, Svastra obliqua expurgata 1

APPENDIX B (cont.)

Cirsium vulgare (nonnative) Apis mellifera 5, Ceratina acantha 1, Diadasia enavata 1, Halictus ligatus 3, Lasioglossum incompletus 3, Megachile apicalis 2, Xylocopa veripuncta 1 Euthamia californica (native) Apis mellifera 1, Hylaeus mesillae cressoni 1, Lasioglossum morphospecies 3 1 Gnaphalium californicum (native) Ceratina acantha 1, Lasioglossum tegulariformis 2 Grindelia camporum (native) Ashmeadiella aridula astragali 5, Ashmeadiella californica 5, Ceratina dallatorreana 2, Diadasia enavata 24, Halictus ligatus 11, Hylaeus conspicuus 1, Megachile apicalis 10, Megachile brevis brevis 2, Megachile brevis onobrychidis 1, Melissodes lupina 3, Triepeolus morphospecies 9 1 Helianthus annuus (native) Agapostemon texanus 1, Apis mellifera 11, Bombus vandykei 1, Bombus vosnesenskii 1, Diadasia enavata 26, Halictus ligatus 20, Megachile apicalis 2, Megachile fidelis 1, Melissodes agilis 4, Melissodes communis alopex 1, Melissodes lupina 1, Melissodes robustior 9, Melissodes tepida timberlakei 1, Osmia texana 1, Svastra obliqua expurgata 3, Xylocopa veripuncta 1 Hemizonia pungens (native) Apis mellifera 1, Ashmeadiella californica 3, Colletes hyalinus 1, Diadasia enavata 3, Dianthidium sp. 1, Halictus ligatus 5, Hylaeus conspicuus 17, Hylaeus mesillae cressoni 1, Lasioglossum incompletus 1, Megachile apicalis 4, Megachile rotundata 1, Melissodes lupina 1 Heterotheca grandiflora (native) Ceratina dallatorreana 1, Halictus ligatus 7, Lasioglossum morphospecies 3 1 Heterotheca oregona (native) Anthophora curta 4, Apis mellifera 2, Dianthidium pudicum 1, Dianthidium pudicum 1, Dianthidium ulkei ulkei 1, Dieunomia nevadensis angelesia 5, Halictus ligatus 4, Hylaeus conspicuus 1, Megachile inimica jacumbensis 3, Melissodes grindelia (?) 1, Perdita morphospecies 1 10 Hieracium argutum (native) Agapostemon texanus 2, Dieunomia nevadensis angelesia 1, Halictus farinosus 1, Halictus ligatus 7, Halictus tripartitus 2, Lasioglossum incompletus 2, Lasioglossum morphospecies 11, Lasioglossum morphospecies 3 2, Megachile fidelis 1, Melissodes robustior 4 Holocarpha virgata (native) Anthidiellum notatum 1, Apis mellifera 1, Halictus ligatus 5, Halictus tripartitus 1, Lasioglossum morphospecies 5 4, Melissodes robustior 1, Melissodes stearnsi 1, Triepeolus morphospecies 8 1

APPENDIX B (cont.)

Leontodon taraxacoides (nonnative) Agapostemon texanus 1, Halictus ligatus 1, Halictus tripartitus 1, Lasioglossum morphospecies 5 1, Megachile apicalis 1, Osmia regulina 1

Silybum marianum (nonnative) Apis mellifera 2, Ceratina acantha 1, Halictus ligatus 5, Hylaeus episcopalis giffardiella 1, Lasioglossum incompletus 3, Lasioglossum morphospecies 5 2, Megachile apicalis 3, Osmia nemoris 1, Osmia regulina 1, Osmia texana 1 Sonchus sp. (nonnative) Agapostemon texanus 1, Apis mellifera 2

Boraginaceae Amsinckia menziesii (native) Ceratina dallatorreana 1, Osmia regulina 1

Brassicaceae Hirschfeldia incana (nonnative) Agapostemon texanus 5, Andrena auricoma 5, Andrena candida 1, Andrena morphospecies 1 5, Andrena piperi 1, Apis mellifera 58, Ashmeadiella aridula astragali 4, Bombus sp. 5, Calliopsis obscurella 1, Ceratina acantha 43, Ceratina dallatorreana 2, Coelioxys octodentata 1, Diadasia enavata 1, Dieunomia nevadensis angelesia 3, Halictus farinosus 17, Halictus ligatus 8, Halictus tripartitus 14, Hoplitis producta gracilis 1, Hylaeus conspicuus 13, Hylaeus episcopalis giffardiella 11, Hylaeus mesillae cressoni 10, Lasioglossum incompletus 4, Lasioglossum mellipes 1, Lasioglossum morphospecies 1 6, Lasioglossum morphospecies 2 2, Lasioglossum morphospecies 3 11, Lasioglossum 4 13, Lasioglossum morphospecies 5 7, Lasioglossum morphospecies 6 5, Lasioglossum morphospecies 7 4, Lasioglossum morphospecies 11 1, Lasioglossum sisymbrii 1, Lasioglossum tegulariformis 1, Lasioglossum titusi 3, Megachile angelarum 2, Megachile apicalis 8, Megachile brevis brevis 1, Megachile brevis onobrychidis 1, Megachile fidelis 1, Megachile gentilis 2, Megachile morphospecies 1 1, Megachile rotundata 4, Melissodes bimatris (?) 1, Melissodes hurdi 1, Melissodes lupina 11, Melissodes robustior 9, Melissodes tepida timberlakei 3, Nomada morphospecies 4 1, Osmia albolateralis 1, Osmia atrocyanea 1, Osmia regulina 5, Sphecodes morphospecies 1 1, Triepeolus morphospecies 2 1, Triepeolus morphospecies 7 1, Xylocopa veripuncta 2 Lepidium latifolium (nonnative) Apis mellifera 5, Colletes hyalinus 2, Hylaeus conspicuus 13, Hylaeus episcopalis giffardiella 3, Hylaeus mesillae cressoni 8, Lasioglossum incompletus 1

APPENDIX B (cont.)

Raphanus sativus (nonnative) Andrena morphospecies 1 2, Anthophora urbana 1, Apis mellifera 14, Ashmeadiella aridula astragali 1, Bombus sp. 9, Bombus californicus 1, Ceratina acantha 11, Ceratina dallatorreana 1, Eucera edwardsii 3, Halictus farinosus 6, Halictus tripartitus 7, Hylaeus conspicuus 5, Hylaeus mesillae cressoni 1, Lasioglossum incompletus 6, Lasioglossum morphospecies 3 1, Lasioglossum morphospecies 6 1, Lasioglossum morphospecies 7 1, Lasioglossum tegulariformis 3, Megachile angelarum 2, Megachile apicalis 9, Megachile gentilis 1, Megachile morphospecies 1 1, Melissodes tepida timberlakei 15, Osmia nemoris 1, Osmia regulina 5 Sisymbrium altissimum (nonnative) Halictus ligatus 1

Caryophyllaceae Spergularia rubra (native) Ashmeadiella aridula astragali 1, Ashmeadiella cactorum 1, Ashmeadiella californica 3, Ceratina acantha 5, Ceratina arizonensis 5, Halictus tripartitus 2, Hylaeus conspicuus 1, Lasioglossum incompletus 4, Lasioglossum tegulariformis 1, Osmia regulina 1

Convolvulaceae Convolvulus arvensis (nonnative) Agapostemon texanus 1, Apis mellifera 3, Ashmeadiella aridula astragali 1, Ceratina acantha 2, Ceratina dallatorreana 7, Diadasia enavata 6, Halictus farinosus 6, Halictus ligatus 7, Halictus tripartitus 7, Hylaeus conspicuus 2, Lasioglossum incompletus 6, Lasioglossum kincaidii 2, Lasioglossum morphospecies 1 1, Lasioglossum morphospecies 5 2, Lasioglossum tegulariformis 1, Megachile apicalis 1, Megachile texana 1, Melissodes lupina 1, Melissodes tepida timberlakei 1, Osmia texana 1

Euphorbiaceae Chamaesyce serpyllifolia (native) Halictus tripartitus 1 Eremocarpus setigerus (native) Agapostemon texanus 1, Apis mellifera 11, Ashmeadiella aridula astragali 1, Ceratina acantha 2, Halictus ligatus 4, Halictus tripartitus 2, Hylaeus mesillae cressoni 1, Lasioglossum incompletus 1, Lasioglossum morphospecies 1 5, Lasioglossum morphospecies 3 1, Lasioglossum morphospecies 11 1, Lasioglossum tegulariformis 4, Megachile apicalis 1, Melissodes lupina 1, Melissodes stearnsi 9, Triepeolus morphospecies 9 1

APPENDIX B (cont.)

Fabaceae Lathyrus jepsonii (native) Bombus sp. 1 Lotus corniculatus (nonnative) Agapostemon texanus 1, Apis mellifera 3, Ashmeadiella aridula astragali 3, Ceratina acantha 2, Hoplitis producta gracilis 3, Megachile angelarum 1, Megachile brevis brevis 1, Megachile rotundata 1, Osmia atrocyanea 1, Osmia cyanella 1, Osmia laeta 1, Osmia nemoris 1, Osmia regulina 5 Lotus purshianus (native) Anthidiellum notatum 1, Ashmeadiella aridula astragali 10, Ceratina acantha 1, Megachile rotundata 1 Lotus scoparius (native) Anthidiellum notatum 3, Anthidium formosum 2, Megachile angelarum 5, Megachile rotundata 1, Melissodes communis alopex 1, Melissodes tepida timberlakei 2 Lupinus benthamii (native) Bombus vosnesenskii 1 Medicago polymorpha (nonnative) Megachile brevis brevis 1 Melilotus albus (nonnative) Apis mellifera 11, Bombus sp. 1, Bombus vosnesenskii 2, Ceratina acantha 3, Halictus farinosus 5, Halictus ligatus 3, Halictus rubicundus 1, Hylaeus bisinuatus 2, Hylaeus conspicuus 4, Hylaeus episcopalis giffardiella 7, Hylaeus mesillae cressoni 4, Osmia laeta 1, Osmia regulina 1 Melilotus indicus (nonnative) Andrena candida 2, Ceratina acantha 4, Nomada morphospecies 2 1, Protosmia rubifloris 1 Trifolium hirtum (nonnative) Andrena plana 1, Apis mellifera 2, Bombus edwardsii 1, Calliopsis anthidius anthidius 1, Ceratina acantha 1, Ceratina dallatorreana 2, Eucera frater albopilosa 2, Megachile apicalis 1, Megachile morphospecies 1 1, Osmia laeta 1, Osmia nemoris 1 Vicia villosa (nonnative) Anthidium formosum 1, Anthophora urbana 3, Apis mellifera 12, Bombus sp. 14, Bombus californicus 3, Bombus edwardsii 1, Bombus vandykei 2, Bombus vosnesenskii 1, Ceratina acantha 2, Eucera edwardsii 2, Eucera frater albopilosa 7, Halictus ligatus 1, Megachile angelarum 1, Megachile gemula 3, Melissodes communis alopex 4, Melissodes tepida timberlakei 1, Osmia aglaia 1, Osmia albolateralis 5, Osmia atrocyanea 1, Osmia cyanella 1, Osmia laeta 5, Osmia nemoris 2, Osmia regulina 10, Xylocopa tabaniformis 8, Xylocopa veripuncta 7

APPENDIX B (cont.)

Geraniaceae Erodium botrys (nonnative) Agapostemon texanus 1, Calliopsis obscurella 1, Ceratina acantha 1, Halictus tripartitus 2, Lasioglossum tegulariformis 3, Lasioglossum titusi 1, Osmia cyanella 1, Xylocopa tabaniformis 1 Erodium cicutarium (nonnative) Osmia nemoris 1 Geranium carolinianum (native) Bombus vosnesenskii 1, Lasioglossum morphospecies 2 1, Megachile brevis brevis 1, Osmia albolateralis 1, Osmia laeta 1

Hypericaceae Hypericum perforatum (nonnative) Apis mellifera 3, Bombus sp. 4, Bombus californicus 2, Halictus farinosus 2, Halictus ligatus 2, Melissodes stearnsi 2, Xeromelecta californica 1, Xylocap veripuncta 1

Lamiaceae Marrubium vulgare (nonnative) Coelioxys octodentata 1, Megachile apicalis 1, Melissodes lupina 1 Mentha pulegium (nonnative) Apis mellifera 6, Bombus sp. 1, Halictus ligatus 10, Halictus tripartitus 1, Lasioglossum incompletus 1, Lasioglossum tegulariformis 1, Megachile apicalis 2, Megachile brevis brevis 6, Melissodes robustior 1, Melissodes stearnsi 1, Triepeolus morphospecies 8 1

Loasaceae Mentzelia laevicaulis (native) Apis mellifera 2

Oxalidaceae Oxalis corniculata (nonnative) Calliopsis obscurella 2, Lasioglossum morphospecies 2 1, Osmia laeta 2

APPENDIX B (cont.)

Papaveraceae Eschscholzia californica (native) Apis mellifera 5, Bombus sp. 7, Bombus californicus 1, Calliopsis obscurella 3, Ceratina acantha 2, Ceratina dallatorreana 1, Halictus farinosus 12, Halictus ligatus 8, Halictus rubicundus 6, Halictus tripartitus 3, Lasioglossum incompletus 1, Lasioglossum morphospecies 1 5, Lasioglossum morphospecies 3 1, Lasioglossum morphospecies 5 4, Lasioglossum morphospecies 7 1, Lasioglossum sisymbrii 1, Lasioglossum tegulariformis 1, Megachile brevis onobrychidis 1, Megachile rotundata 1, Melissodes stearnsi 1, Osmia nemoris 1 Polygonaceae Eriogonum gracile (native) Anthidiellum notatum 4, Apis mellifera 1, Ceratina acantha 2, Ceratina arizonensis 1, Halictus farinosus 3, Halictus ligatus 4, Hylaeus episcopalis giffardiella 1, Megachile apicalis 1, Megachile brevis onobrychidis 1, Megachile gentilis 2, Melissodes hurdi 1, Perdita morphospecies 2 2

Rosaceae Rosa californica (native) Apis mellifera 6, Bombus sp. 2, Ceratina acantha 1, Hylaeus mesillae cressoni 1 Rubus concolor (nonnative) Apis mellifera 12, Bombus sp. 6, Bombus vandykei 1, Ceratina acantha 4, Hoplitis producta gracilis 1, Hylaeus mesillae cressoni 3, Lasioglossum kincaidii 1, Lasioglossum morphospecies 2 1, Megachile angelarum 1, Megachile brevis onobrychidis 1, Megachile gentilis 1, Megachile rotundata 5, Melissodes communis alopex 8, Melissodes lupina 1, Osmia nemoris 1, Osmia nigrifrons 1, Osmia regulina 4 Scrophulariaceae Verbascum blattaria (nonnative) Lasioglossum incompletus 1

Solanaceae Datura wrightii (native) Apis mellifera 1 Solanum elaeagnifolium (nonnative) Halictus ligatus 1, Xylocopa veripuncta 2

APPENDIX B (cont.)

Verbenaceae Phyla nodiflora (native) Apis mellifera 8, Ashmeadiella aridula astragali 1, Ashmeadiella californica 1, Ceratina acantha 4, Halictus ligatus 2, Hylaeus conspicuus 4, Ashmeadiella aridula astragali 1, Ashmeadiella californica 1, Ceratina acantha 4, Halictus ligatus 2, Hylaeus conspicuus 4, Lasioglossum tegulariformis 1, Megachile apicalis 13, Megachile brevis brevis 1, Melissodes tepida timberlakei 3, Osmia morphospecies 1 1, Osmia regulina 2 Verbena bonariensis (nonnative) Agapostemon texanus 1, Anthidiellum notatum 1, Apis mellifera 13, Ashmeadiella aridula astragali 1, Ceratina acantha 12, Ceratina punctigena 1, Dianthidium platyurum 1, Halictus ligatus 4, Hylaeus mesillae cressoni 1, Megachile angelarum 1, Megachile fidelis 5, Megachile gentilis 1, Megachile rotundata 1, Melissodes paulula 1, Melissodes robustior 5, Melissodes tepida timberlakei 9, Osmia regulina 5, Triepeolus morphospecies 7 1 Verbena lasiostachys (native) Apis mellifera 2, Ashmeadiella aridula astragali 3, Bombus vosnesenskii 1

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