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
in
BIOLOGICAL SCIENCES
(Biological Conservation)
at
CALIFORNIA STATE UNIVERSITY, SACRAMENTO
SUMMER
2010
© 2010
Byron Love
ALL RIGHTS RESERVED
ii
THE BEES OF THE AMERICAN AND COSUMNES RIVERS IN
SACRAMENTO COUNTY, CALIFORNIA: EFFECTS OF LAND USE ON
NATIVE BEE DIVERSITY
A Thesis
by
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
Department of Biological Sciences
iv
_________________
Date
Abstract
of
THE BEES OF THE AMERICAN AND COSUMNES RIVERS IN
SACRAMENTO COUNTY, CALIFORNIA: EFFECTS OF LAND USE ON
NATIVE BEE DIVERSITY
by
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,
v
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
vi
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
vii
encouragement, push, and opportunity to explore my curiosity of the natural world.
I am forever grateful.
viii
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
ix
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
x
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
xi
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
xii
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
xiii
1
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.
2
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).
3
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
7
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).
8
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.
10
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
11
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.
12
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 seminatural 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).
13
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
American / Discovery Park
Site Code
ARDP
Lat./Long.
N38.6044°
W121.4935°
Elevation
7
American / California State
University, Sacramento
ARSS
N38.5674°
W121.4216°
7
American / Rossmoor Rd.
ARRD
N38.6218°
W121.3000°
21
American / Sunrise Blvd.
ARLS
N38.6273°
W121.2736°
25
Cosumnes / Twin Cities Rd.
CRTC
N38.2993°
W121.3799°
6
Cosumnes / Costello Forest
CRCF
N38.3586°
W121.3393°
12
Cosumnes / Freeman Rd.
CRDD
N38.3892°
W121.2973°
14
Cosumnes / Rancho Murieta
CRRM
N38.4835°
W121.1045°
40
14
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.
15
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 6ounce 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
16
U
A
N
W
W
W
A
W
A
N
U
ARDP
CRTC
U
A
U
W
W
U
U
N N
ARSS
A
N
N
A
A
A
CRCF
A
U
A
W
N
N
ARRD
N
CRDD
U
W
W
N
N
U
ARLS
N
W
A
N
CRRM
U
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.
17
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.
20
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).
21
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
22
Proportion
1.0
River
Agriculture
0.5
Urban
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.
23
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.
Abundance (A)
Mean Abundance per
Site
Richness (S)(Gamma
Diversity)
Mean Richness per
Site
Unique Bee Species
Mean Simpson’s
Diversity Index (D)
Mean Simpson’s
Diversity (1-D)
Mean Simpson’s
Reciprocal (1/D)
per site
Mean Shannon-Wiener
Diversity Index (H)
Mean Evenness
((1/D)/S) per site
Alpha Diversity
Beta Diversity
American River Cosumnes River
2972
4938
148.6 ± 18.4
246.9 ± 44.8
P-value
Total
7910
P = 0.653 -
105
97
122
25.4 ± 2.0
25.3 ± 1.5
35
0.19 ± 0.02
27
0.22 ± 0.16
-
0.81 ± 0.02
0.78 ± 0.16
-
6.17 ± 0.61
5.11 ± 0.37
2.1 ± 0.08
2.0 ± 0.06
0.39 ± 0.03
0.31 ± 0.03
60.25
1.74
56.25
1.72
P = 0.845
P = 0.424
-
-
P = 0.012
-
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
25
Both Rivers
American River
Cosumnes River
a) Genera
11.8%
10.3%
12.9%
24.1%
25.8%
26.5%
41.2%
14.7%
16.1%
41.9%
41.4%
17.2%
3.2%
5.9%
6.9%
b) Species
9.8%
5.2%
10.5%
25.7%
26.3%
29.9%
40.2%
36.2%
40.6%
19.5%
23.8%
3.8%
20.6%
3.8%
4.1%
c) Individuals
16.2%
0.9%
12.8%
19.4%
1.3%
18.3%
0.6%
16.2%
24.7%
3.8%
2.8%
1.3%
60.0%
60.7%
Andrenidae
Apidae
Colletidae
61.1%
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.
26
0
Abundance
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.
28
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
Halictidae
Agapostemon texanus
Halictus ligatus
Halictus tripartitus
Lasioglossum incompletus
Megachilidae
Ashmeadiella aridula astragali
Megachile apicalis
Osmia nemoris
Osmia regulina
Apidae
Apis mellifera
Ceratina acantha
Melissodes lupina
Melissodes robustior
Melissodes tepida timberlakei
Abundance
Nesting/Social Behavior
191
1150
764
1119
Ground/Solitary
Ground/Social
Ground/Social
Ground/Social?
67
440
283
197
Stem?/Solitary
Stem/Solitary
Ground & Stem/Solitary
?/Solitary
371
146
79
60
167
Ground & External/Social
Stem/Solitary
Ground/Solitary
Ground/Solitary
Ground/Solitary
29
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. SS= sum of squares;
MS = mean square; df = degrees of freedom.
Abundance
Source
River
Month
River*Month
Error
Total
Richness
Source
River
Month
River*Month
Error
Total
Diversity
Source
River
Month
River*Month
Error
Total
Community Evenness
Source
River
Month
River*Month
Error
Total
SS
966289.9
159959.8
46932.3
683252.5.0
1856435.0
SS
0.1
451.3
5
678.1
1134.5
SS
11.1
47.6
2.9
142.7
204.3
SS
0.08
0.08
0.02
0.62
0.81
df
1
4
4
30
39
MS
966289.9
39990.0
11733.1
22775.1
F
0.224
7.287
5.641
P
0.653
< 0.01
< 0.01
df
1
1
1
36
39
MS
0.1
451.3
5
18.8
F
0.041
13.733
0.152
P
0.845
< 0.01
0.699
df
1
4
4
30
39
MS
11.1
11.9
0.7
4.8
F
0.737
5.687
0.716
P
0.424
< 0.01
0.589
df
1
4
4
30
39
MS
0.08
0.02
0.01
0.02
F
12.656
1.804
0.216
P
0.012
0.161
0.927
30
700
Abundance
600
500
400
300
200
100
0
May
Jun
American River
Jul
Aug
Sep
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.
31
40
Richness
30
20
10
0
May
Jun
American River
Jul
Aug
Sep
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.
Diversity
32
10.0
9.0
8.0
7.0
6.0
5.0
4.0
3.0
2.0
1.0
0.0
May
Jun
American River
Jul
Aug
Sep
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.
33
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
34
Evenness
0.6
0.4
0.2
0.0
May
Jun
American River
Jul
Aug
Sep
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.
35
ARD
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.
36
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
Amsinckia menziesii
Anthemis cotula
Asclepias fascicularis
Centaurea solstitialis
Chamaesyce serpyllifolia
Cichorium intybus
Cirsium vulgare
Conium maculatum
Convolvulus arvensis
Datura wrightii
Daucus carota
Eremocarpus setigerus
Eriogonum gracile
Erodium botrys
Erodium cicutarium
Eschscholzia californica
Euthamia californica
Foeniculum vulgare
Geranium carolinianum
Ghaphalium californicum
Grindelia camporum
Hieracium argutum
Helianthus annuus
Hemizonia pungens
Heterotheca grandiflora
Heterotheca oregona
Hirschfeldia incana
Holocarpha virgata
Hypericum perforatum
Lactuca serriola
Lathyrus jepsonii
Leontodon taraxacoides
Lepidium latifolium
Lotus corniculatus
Lotus purshianus
Lotus scoparius
Family
Boraginaceae
Asteraceae
Asclepiadaceae
Asteraceae
Euphorbiaceae
Asteraceae
Asteraceae
Apiaceae
Convolvulaceae
Solanaceae
Apiaceae
Euphorbiaceae
Polygonaceae
Geraniaceae
Geraniaceae
Papaveraceae
Asteraceae
Apiaceae
Geraniaceae
Asteraceae
Asteraceae
Asteraceae
Asteraceae
Asteraceae
Asteraceae
Asteraceae
Brassicaceae
Asteraceae
Hypericaceae
Asteraceae
Fabaceae
Asteraceae
Brassicaceae
Fabaceae
Fabaceae
Fabaceae
Native/Non-native
Native
Nonnative
Native
Nonnative
Native
Nonnative
Nonnative
Nonnative
Nonnative
Native
Nonnative
Native
Native
Nonnative
Nonnative
Native
Native
Nonnative
Native
Native
Native
Native
Native
Native
Native
Native
Nonnative
Native
Nonnative
Nonnative
Native
Nonnative
Nonnative
Nonnative
Native
Native
American
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
Cosumnes
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
37
Table 5 (continued)
Plant Species
Lupinus benthamii
Lupinus bicolor
Lupinus spp.
Marrubium vulgare
Medicago polymorpha
Melilotus alba
Melilotus indicus
Mentha pulegium
Mentzelia laevicaulis
Nicotiana attenuate
Nicotiana quadrivalvis
Oenothera elata
Oxalis corniculata
Phyla nodiflora
Plagiobothrys nothofulvus
Plantago species
Raphanus sativus
Rosa californica
Rubus concolor
Sambucus mexicana
Silybum marianum
Sisymbrium altissimum
Solanum elaeagnifolium
Sonchus spp
Spergularia rubra
Trifolium hirtum
Verbascum blattaria
Verbascum Thapsus
Verbena bonariensis
Verbena lasiostachys
Vicia villosa
Family
Fabaceae
Fabaceae
Fabaceae
Lamiaceae
Fabaceae
Fabaceae
Fabaceae
Lamiaceae
Loasaceae
Solanaceae
Solanaceae
Onagraceae
Oxalidaceae
Verbenaceae
Boraginaceae
Plantaginaceae
Brassicaceae
Rosaceae
Rosaceae
Caprifoliaceae
Asteraceae
Brassicaceae
Solanaceae
Asteraceae
Caryophyllaceae
Fabaceae
Scrophulariaceae
Scrophulariaceae
Verbenaceae
Verbenaceae
Fabaceae
Native/Non-native
Native
Native
Native (?)
Nonnative
Nonnative
Nonnative
Nonnative
Nonnative
Native
Native
Native
Native
Nonnative
Native
Native
Nonnative (?)
Nonnative
Native
Nonnative
Native
Nonnative
Nonnative
Nonnative
Nonnative (?)
Nonnative
Nonnative
Nonnative
Nonnative
Nonnative
Native
Nonnative
American
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
Cosumnes
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
38
18
16
14
Richness
12
10
Total
8
Native
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.
39
120
Abundance
100
80
Total
60
Native
Non-native
40
20
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.
40
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. Pvalues are for differences between rivers. No P-value indicates no statistical tests
were performed.
Mean Abundance (A)
Mean Abundance
Native
Mean Abundance Nonnative
Richness (S)
Richness Native
Richness Non-native
Mean Total Richness
Mean Native Richness
Mean Non-native
Richness
American
River
85.9 ± 7.0
20.8 ± 3.3
Cosumnes
River
108.2 ± 9.5
34.3 ± 8.3
65.2 ± 6.5
74.0 ± 5.7
69.8 ± 4.3
47
19
28
10.6 ± 1.1
3.9 ± 0.4
6.7 ± 0.9
58
27
31
15.5 ± 0.7
4.8 ± 0.4
10.5 ± 0.7
64
31
33
n/a
4.4 ± 0.3
8.6 ± 0.3
P-value
P = 0.069
P < 0.001
Total
n/a
27.7 ± 4.5
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
42
50
Bee Richness
40
30
20
10
0
0
5
10
15
Plant Richness
American River
20
25
Cosumnes River
Figure 13. Regression of bees species richness on plant species richness (P =0.047,
R2 = 0.10).
43
Bee Abundance
1000
800
600
400
200
0
0
5
10
15
Plant Richness
American River
20
25
Cosumnes River
Figure 14. Regression of bee abundance on plant species richness (P = 0.456, R2 =
0.10).
44
40
Bee Species Richness
35
30
25
20
15
10
5
0
0
20
40
60
Floral Resource Abundance
80
100
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
b)
20
40
60
80
100
Bee Abundance
500
400
300
200
100
0
0
c)
20
40
60
80
1000
800
600
400
200
0
0
20
40
60
80
Floral Resource Abundance
° American River
100
 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).
46
(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
47
400
350
Abundance
300
250
Ceratina dallatorreana
Megachile apicalis
200
Megachile rotundata
150
Hylaeus bisinuatus
100
50
0
American
Cosumnes
Figure 17. Distribution of the total numbers of nonnative bees (excluding Apis)
collected between May and September 2007.
48
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%).
49
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
Andrena auricoma
Andrena candida
Andrena morphospecies 1
Andrena piperi
Anthidiellum notatum
Anthidium formosum
Bombus crotchii
Bombus edwardsii
Bombus vandykei
Calliopsis anthidius anthidius
Ceratina punctigena
Coelioxys octodentata
Colletes hyalinus
Dianthidium platyurum
Dianthidium ulkei ulkei
Dieunomia nevadensis angelesia
Hylaeus bisinuatus
Lasioglossum mellipes
Lasioglossum morphospecies 10
Lasioglossum sisymbrii
Megachile angelarum
Megachile inimica jacumbensis
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
Pan Trapped Species
Andrena subchalybea
Ceratina sequoia
Diadasia bituberculata
Diadasia consociata
Diadasia olivacea
Diadasia rinconis rinconis
Exomalopsis yoloensis
Lasioglossum morphospecies 8
Lasioglossum morphospecies 9
Melissodes pallidisignata (?)
Nomada morphospecies 1
Nomada morphospecies 3
Panurginus morphospecies 1
Peponapis pruinosa
Perdita morphospecies 3
Perdita morphospecies 4
Sphecodes morphospecies 2
Sphecodes morphospecies 3
Triepeolus heterurus
Triepeolus morphospecies 10
Triepeolus morphospecies 4
Triepeolus morphospecies 6
50
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 plantpollinator 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.,
52
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;
53
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 quality 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 seminatural 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).
59
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 kselection 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).
60
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.
61
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 seminatural 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.
63
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
Colletidae
Colletes hyalinus
Hylaeus bisinuatus* †
Hylaeus conspicuous
Hylaeus episcopalis giffardiella
Hylaeus mesillae cressoni
Andrenidae
Andrena auricoma †
Andrena candida †
Andrena morphospecies 1
Andrena piperi †
Andrena plana
Andrena subchalybea †
Calliopsis anthidius anthidius
Calliopsis obscurella †
Panurginus morphospecies 1 †
Perdita morphospecies 1 †
Perdita morphospecies 2 †
Perdita morphospecies 3 †
Perdita morphospecies 4 †
Halictidae
Agapostemon texanus
Dieunomia nevadensis angelesia
Halictus farinosus
American Cosumnes
2
2
5
18
14
5
4
5
1
1
1
17
1
138
10
36
6
1
13
1
10
2
1
1
131
4
25
61
6
147
N
G?
S
S?
S
S?
B
O
?
?
G
G
G
G
G
G
G?
G?
G?
G?
G?
G?
G?
G
G
G
F
P
O
O
PS
P
P
P
64
APPENDIX A (cont.)
Species
Halictus ligatus
Halictus rubicundus
Halictus tripartitus
Lasioglossum incompletus
Lasioglossum kincaidii
Lasioglossum mellipes †
Lasioglossum morphospecies 1
Lasioglossum morphospecies 2
Lasioglossum morphospecies 3
Lasioglossum morphospecies 4
Lasioglossum morphospecies 5
Lasioglossum morphospecies 6
Lasioglossum morphospecies 7
Lasioglossum morphospecies 8
Lasioglossum morphospecies 9 †
Lasioglossum morphospecies 10 †
Lasioglossum morphospecies 11 †
Lasioglossum sisymbrii †
Lasioglossum tegulariformis
Lasioglossum titusi
Sphecodes morphospecies 1 †
Sphecodes morphospecies 2
Sphecodes morphospecies 3 †
Megachilidae
Anthidiellum notatum
Anthidium formosum †
Ashmeadiella aridula astragali
Ashmeadiella cactorum
Ashmeadiella californica
Ashmeadiella opuntiae †
Coelioxys octodentata
Dianthidium platyurum †
American Cosumnes
186
964
18
9
331
436
153
967
3
13
1
590
16
38
21
107
37
59
1
21
176
7
15
5
15
6
1
1
2
4
2
84
16
1
113
1
1
1
2
10
3
30
1
4
1
35
4
19
3
2
5
N
G
G
G
G
G?
G?
G?
G?
G?
G?
G?
G?
G?
G?
G?
G?
G?
G
G
G?
G
G
G
E
?
S?
S?
?
S
S?
E
B
PS
?
?
?
?
?
?
?
?
?
?
?
?
?
?
F
P
P
P
P
P?
O?
P
?
C
C
C
O?
P
O
O
O
C
65
APPENDIX A (cont.)
Species
Dianthidium pudicum
Dianthidium ulkei ulkei †
Hoplitis producta gracilis
Megachile angelarum
Megachile apicalis*
Megachile brevis brevis
Megachile brevis onobrychidis
Megachile fidelis
Megachile gemula †
Megachile gentilis
Megachile inimica jacumbensis †
Megachile morphospecies 1
Megachile perhirta †
Megachile rotundata*
Megachile texana †
Osmia aglaia
Osmia albolateralis
Osmia atrocyanea
Osmia cyanella †
Osmia laeta
Osmia montana †
Osmia morphospecies 1 †
Osmia nemoris
Osmia nigrifrons †
Osmia regulina
Osmia texana
Protosmia rubifloris †
Apidae
Anthophora curta
Anthophora urbana
Apis mellifera*
Bombus californicus
American Cosumnes
N
2
3
E
1
E/G
11
3
S
8
5
S?
56
384
S
5
21
G/S?
4
11
G/S?
7
7
?
4
?
6
6
S
4
S
2
3
?
2
G
23
2
S
2
G
10
2
S
11
2
S
3
3
S
4
S?
19
4
G?
1
G
2
?
46
255
G/S
3
G/S
103
94
?
1
20
S
1
E
9
9
191
5
10
10
181
16
G
G
G/E
G
B
F
O
P
P?
P
P
P
P
P
P
O
P
P
P
O
S
S
P
P
P
66
APPENDIX A (cont.)
Species
Bombus crotchii
Bombus edwardsii
Bombus vandykei
Bombus vosnesenskii
Ceratina acantha
Ceratina arizonensis
Ceratina dallatorreana*
Ceratina punctigena †
Ceratina sequoia †
Diadasia bituberculata
Diadasia consociate
Diadasia enavata
Diadasia olivacea
Diadasia rinconis rinconis †
Eucera actuosa
Eucera edwardsii
Eucera frater albopilosa
Exomalopsis yoloensis †
Melissodes agilis
Melissodes bimatris (?)†
Melissodes communis alopex †
Melissodes grindelia (?)
Melissodes hurdi †
Melissodes lupine
Melissodes pallidisignata (?)
Melissodes robustior
Melissodes stearnsi
Melissodes tepida timberlakei
Nomada morphospecies 1 †
Nomada morphospecies 2 †
Nomada morphospecies 3 †
Nomada morphospecies 4 †
American Cosumnes
1
1
1
3
1
4
10
87
59
55
8
6
49
1
2
1
2
4
8
67
1
2
2
14
13
3
7
9
1
4
3
2
115
1
1
3
25
54
3
1
21
35
169
101
65
1
1
1
1
N
G
G
G
G
S
S
S
S
S
G
G
G
G
G
G
G
G
G
G
G
G
G
G
G
G
G
G
G
G
G
G
G
B
S
S
S
S
F
P
P
P
P
P?
P?
P
P?
O
O
O
O
O
O
P
P
Com
O
P
O
O
O
P
C
C
C
C
67
APPENDIX A (cont.)
Species
Peponapis pruinosa
Svastra obliqua expurgate
Triepeolus concavus †
Triepeolus heterurus †
Triepeolus morphospecies 1 †
Triepeolus morphospecies 2
Triepeolus morphospecies 3 †
Triepeolus morphospecies 4 †
Triepeolus morphospecies 5 †
Triepeolus morphospecies 6 †
Triepeolus morphospecies 7 †
Triepeolus morphospecies 8 †
Triepeolus morphospecies 9 †
Triepeolus morphospecies 10 †
Xeromelecta californica †
Xylocopa tabaniformis †
Xylocopa veripuncta †
American Cosumnes
2
5
12
3
2
1
1
1
1
1
1
2
3
3
3
4
1
1
12
15
N
G
G
G
G
G
G
G
G
G
G
G
G
G
G
G
S
S
B
C
C
C
C
C
C
C
C
C
C
C
C
C
PS
PS
F
O
O
P
P
68
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
69
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
70
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
71
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
72
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
73
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
74
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
75
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
76
LITERATURE CITED
Allen-Wardell, G. P. Bernhardt, R. Bitner, A. Burquez, S. Buchmann, J. Cane, P.
A. Cox, V. Dalton, P. Feinsinger, M. Ingram, D. Inouye, C. E. Jones, K.
Kennedy, P. Kevan, H. Koopowitz, R. Medellin, S. Medellin-Morales, G. P.
Nabhan, B. Pavlik, V. Tepedino, P. Torchio, and S. Walker. 1998. The
potential consequences of pollinator declines on the conservation of
biodiversity and stability of food crop yields. Conservation Biology 12:817.
Axelrod, D. I. (1960). The evolution of flowering plants. The evolution of life. S.
Tax. Chicago, University of Chicago Press: 227-305.
Barbour, M. G., J. H. Burk and W. D. Pitts (1987). Terrestrial Plant Ecology, 2nd
Edition. Menlo Park, The Benjamin Cummings Publishing Co. Inc.
Batra, S. W. T. (2003). Bee introductions to pollinate our crops. For nonnative
crops, whence pollinators of the future? K. Strickler and J. H. Cane.
Lanham, Entomological Society of America: 85-98.
Bengtsson, J., J. Ahnstrom and A. Weibull (2005). The effects of organic
agriculture on biodiversity and abundance: a meta-analysis. Journal of
Applied Ecology 42: 261-269.
Benton, T. G., D. M. Bryant, L. Cole and H. Q. P. Crick (2002). Linking
agricultural practice to insect and bird populations: a historical study over
three decades. Journal of Applied Ecology 39: 673-687.
Blair, R. B. (1999). Birds and butterflies along an urban gradient: surrogate taxa for
assessing biodiversity? Ecological Applications 9:164-170.
Borror, D. J., C. A. Triplehorn and N. F. Johnson (1989). An introduction to the
study of insects. Fort Worth, Harcourt Brace College Publishers.
Borror, D. J. and R. E. White (1970). A field guide to insects America north of
Mexico. Boston, Houghton Mifflin Co.
77
Brooks, M. L., C. M. D'Antonio, D. M. Richardson, J. B. Grace, J. E. Keeley, J. M.
DiTomaso, R. J. Hobbs, M. Pellant and D. Pyke (2004). Effects of invasive
alien plants on fire regimes. BioScience 54(7): 677-688.
Brown, J. H., C. G. Curtin and JR. W. Braithwaite (2003). Management of the
semi-natural matrix. How landscapes change: human disturbance and
ecosystem fragmentation in the Americas. G. A. Bradshaw, P. A. Marquet
and K. L. Ronnenberg. New Your, Springer.
Buchmann, S. L. and G. P. Nabhan (1996). The forgotten pollinators. Washington
D. C., Island Press.
Cane, J. H. (2003). Exotic nonsocial bees (Hymenoptera: Apiformes) in North
America: ecological implications. For nonnative crops, whence pollinators
of the future? K. Strickler and J. H. Cane. Lanham, Entomological Society
of America: 113-126.
Cane, J. H. (2005a). Bees, pollination, and the challenges of sprawl. Nature in
fragments: the legacy of sprawl. E. A. Johnson and M. W. Klemens,
Columbia University Press: 109-124.
Cane, J. H. (2005b) Pollination potential of the bee Osmia aglaia for cultivated red
respberries and blackberries (Rubus: Rosaseae). Horticultural Science.
40:1705-1708.
Cane, J. H., R. L. Minckley, L. J. Kervin, T. H. Roulston and N. M. Williams
(2006). Complex responses within a desert bee guild (Hymenoptera:
Apiformes) to urban habitat fragmentation. Ecological Applications 16(2):
632-644.
Cane, J. H. and V. J. Tepedino (2001). Causes and extent of declines among native
North American invertebrate pollinators: detection, evidence, and
consequences. Conservation Ecology 5(1): [online] URL:
http://www.consecol.org/vol5/iss1/art1/.
Danforth, B. (2007). Bees. Current Biology 117(5): R156-R161.
DeGrandi-Hoffman, G. (2003). Honey bees in U. S. agriculture: past, present, and
future. For nonnative crops, whence pollinators of the future? K. Strickler
and J. H. Cane. Lanham, Entomological Society of Ameria: 11-20.
78
Fenster, C. B., W. S. Armbruster, P. Wilson, M. R. Dudash and J. D. Thomson
(2004). Pollination syndromes and floral specialization. Annual Review of
Ecology, Evolution, and Systematics 35: 375-403.
Fetridge, E. D., J. S. Ascher and G. A. Langellotto (2008). The bee fauna of
residential gardens in a suburb of New York City (Hymenoptera: Apoidea).
Annals of the Entomoloical Society of America 101(6): 1067-1077.
Frankie, G. W., R. W. Thorp, L. E. Newstrom-Lloyd, M. Rizzardi, J. F. Barthell, T.
L. Griswold, J. Kim and S. Kappagoda (1998). Monitoring solitary bees in
modified wildland habitats: implications for bee ecology and conservation.
Community and Ecosystem Ecology 27(5): 1137-1148.
Frankie, G. W., R. W. Thorp, M. Schindler, J. L. Hernandez, B. Ertter and M.
Rizzardi (2005). Ecological patterns of bees and their host ornamental
flowers in two northern California cities. Journal of the Kansas
Entomological Society 78(3): 227-246.
Frankl, R., S. Wanning and R. Braun (2005). Quantitative floral phenology at the
landscape scale: is a comparative spatio-temporal description of "flowering
landscapes" possible? Journal for Nature Conservation 13: 219-229.
Fritts, T. H. and G. H. Rodda (1998). The role of introduced species in the
degradation of island ecosystems: a case history of Guam. Annual Review
of Ecology and Systematics 29: 113-140.
Gathmann, A. and T. Tscharntke (2002). Foraging ranges of solitary bees. Journal
of Animal Ecology 71: 757-764.
Goulson, D. (2003). Effects of introduced bees on native ecosystems. Annual
Review of Ecology, Evolution, and Systematics 34: 1-26.
Greenleaf, S. S. and C. Kremen (2006a). Wild bee species increase tomato
production and respond differently to surrounding land use in Northern
California. Biological Conservation 133: 81-87.
Greenleaf, S. S. and C. Kremen (2006b). Wild bees enhance honey bees' pollination
of hybrid sunflower. The Proceedings of the National Academy of Sciences
USA 103(37): 13890-13895.
Greenleaf, S. S., N. M. Williams, R. Winfree and C. Kremen (2007). Bee foraging
ranges and their relationship to body size. Oecologia 153: 589-596.
79
Herrera, C. M. (1988). Variation in mutualisms: the spatio-temporal mosaic of a
pollinator assemblage. Biological Journal of the Linnean Society 35: 95125.
Hickman, J. C., Ed. (1993). The Jepson Manual: Higher Plants of California.
Berkeley, University of California Press.
Hisamatsu, M. and S. Yamane (2006). Faunal makeup of wild bees and their flower
utilization in a semi-urbanized area in central Japan. Entomological Science
9: 137-145.
Hurd, P. D. J. (1955). The carpenter bees of California. Bulletin of the California
Insect Survey 4(2): 35-72.
Hurlbert, S. H. (1984). Pseudoreplication and the design of ecological field
experiments. Ecological Monographs 54(2): 187-211.
Johnson, R. (2008). Recent honey bee colony declines. S. Analyst in Agricultural
Economics Resources, and Industry Division: 19.
Kearns, C. A., D. W. Inouye and N. M. Waser (1998). Endangered mutualisms: the
conservation of plant-pollinator interactions. Annual Review of Ecology
and Systematics 29: 83-112.
Kearns, C. A. and D. M. Oliveras (2009). Environmental factors affecting bee
diversity in urban and remote grassland plots in Boulder, Colorado. Journal
of Insect Conservation. Open source online, DOI 10.1007/s10841-0099215-4.
Krebs, C. J. (1999). Ecological Methodology, 2nd Edition. Menlo Park, Addison
Wesley Longman.
Kremen, C (2008). Crop pollination services from wild bees. Bee pollination in
agricultural ecosystems. R. R. James and T. L. Pitts-Singer. New York,
Oxford University Press.
Kremen, C., N. M. Williams, R. L. Bugg, J. P. Fay and R. W. Thorp (2004). The
area requirements of an ecosystem service: crop pollination by native bee
communities in California. Ecology Letters 7: 1109-1119.
80
Kremen, C., N. M. Williams and R. W. Thorp (2002). Crop pollination from native
bees at risk from agricultural intensification. The Proceedings of the
National Academy of Sciences USA 99(26): 16812-16816.
LeBuhn, G., T. Griswold, R. Minckley, S. Droege, T. Roulston, J. Cane, F. Parker,
S. Buchmann, V. Tepedino, N. Williams, C. Kremen and O. Messenger
(2003). A standardized method for monitoring bee populations--The Bee
Inventory (BI) Plot: 11.
Linsley, E. G. (1958). The ecology of solitary bees. Hilgardia 27(19): 543-599.
MacArthur, R. H. and E. O. Wilson (1967). The theory of island biogeography.
Princeton, Princeton University Press.
Matteson, K. C., J. S. Ascher and G. A. Langellotto (2008). Bee richness and
abundance in New York City urban gardens. Annals of the Entomoloical
Society of America 101(1): 140-150.
McDonnell, M. J. and S. T. A. Pickett (1990). Ecosystem structure and function
along urban-rural gradients: an unexploited opportunity for ecology.
Ecology 71(4): 1232-1237.
McIntyre, N. E. and M. E. Hostetler (2001). Effects of urban land use on pollinator
(Hymenoptera: Apoidea) communities in a desert metropolis. Basic and
Applied Ecology 2: 209-218.
McKinney, M. L. (2002). Urbanization, biodiversity, and conservation. BioScience
52: 883-890.
Messenger, O. and T. Griswold (2002). A pinnacle of bees. Fremontia 30(3-4): 3240.
Messinger, O. (2006). A survey of the bees of Grand Staircase-Escalante National
Monument, southern Utah: Incidence, abundance, and community
dynamics. Biology. Logan, Utah State University. Master of Science: 147.
Michener, C. D. (1979). Biogeography of the bees. Annals of the Missouri
Botanical Garden 66(3): 277-347.
81
Michener, C. D. (2000). The bees of the world. Baltimore, The Johns Hopkins
University Press.
Moldenke, A. R. (1975). Niche specialization and species diversity along a
California transect. Oecologia 21(3): 219-242.
Moldenke, A. R. and J. Neff (1974). The bees of California: a catalogue with
special relevence to pollination and ecological research, technical report 743 (Part III of 3). Santa Cruz, University of California.
Mooney, H. A. and E. E. Cleland (2001). The evolutionary impact of invasive
species. The Proceedings of the National Academy of Sciences USA
98(10): 5446-5451.
Morandin, L. A. and M. L. Winston (2005). Wild bee abundance and seed
production in conventional, organic, and genetically modified canola.
Ecological Applications 15(3): 871-881.
Moritz, R. F. A., S. Hartel and P. Neumann (2005). Global invasions of the western
honeybee (Apis mellifera) and the consequences for biodiversity.
Ecoscience 12(3): 289-301.
NRA (2007). National Research Council of the National Academies. Status of
pollinators in North America. Washington, D.C., National Academies Press.
Ockinger, E. and H. Smith (2007). Semi-natural grasslands as population sources
for pollinating insects in agricultural landscapes. Journal of Applied
Ecology 44: 50-59.
Osborne, J. L., S. J. Clark, R. J. Morris, I. H. Williams, J. R. Riley, A. D. Smith, D.
R. Reynolds and A. S. Edwards (1999). A landscape-scale study of bumble
bee foraging range and constancy, using harmonic radar. Journal of Applied
Ecology 36: 519-533.
Paini, D. R. (2004). Impact of the introduced honey bee (Apis mellifera)
(Hymenoptera: Apidae) on native bees: A review. Austral Ecology 29: 399407.
Proctor, M., P. Yeo and A. Lack (1996). The Natural History of Pollination.
Portland, Timber Press.
82
Ricketts, T. H. (2004). Tropical forest fragments enhance pollinator activity in
nearby coffee crops. Conservation Biology 18(5): 1262-1271.
Ricketts, T. H., G. C. Daily, P. R. Ehrlich and C. D. Michener (2004). Economic
value of tropical forest to coffee production. The Proceedings of the
National Academy of Sciences USA 101(34): 12579-12582.
Ricketts, T. H., E. Dinerstein, D. M. Olson, C. J. Loucks, W. Eichbaum, D.
DellaSala, K. Kavanagh, P. Hedao, P. T. Hurley, K. M. Carney, R. Abell
and S. Walters (1999). Terrestrial Ecoregions of North America: A
Conservation Assessment. Washington, D. C., Idland Press.
Roberts, R. B. (1969). Biology of the bee genus Agapostemon (Hymenoptera:
Halictidae). University of Kansas Science Bulletin 48: 689-719.
Roubik, D. W. (1989) Ecology and natural history of tropical bees. Cambridge,
Cambridge University Press.
Saure, C. (1996). Urban habitats for bees: the example of the city of Berlin. The
conservation of bees. A Matheson, S. L. Buchman, C. O'Toole, P. Westrich
and I. H. Williams. San Diego, Academic Press, Inc.
Schoenherr, A. A. (1992). A Natural History of California. Berkeley and Los
Angeles, University of California Press.
Shapiro, A. M. (2002). The Californian urban butterfly fauna is dependent on alien
plants. Diversity and Distributions 8: 31-40.
Sher, A. A., D. L. Marshall and S. A. Gilbert (2000). Competition between native
Populus deltoides and invasive Tamarix ramosissima and the implications
for reestablishing flooding disturbance. Conservation Biology 14(6): 17441754.
Stephen, W. P. (2003). Solitary bees in North America agriculture: a perspective.
For nonnative crops, whence pollinators of the future? K. Strickler and J. H.
Cane. Lanham, Entomological Society of America: 41-66.
Stephen, W. P., G. E. Bohart and P. F. Torchio (1969). The biology and external
morphology of bees: with a synopsis of the genera of Northwestern
America. Corvallis, Agricultural Experiment Station, Oregon State
University.
83
Thomson, D. M. (2006). Detecting the effects of introduced species: a case study of
competition between Apis and Bombus. Oikos 114: 407-418.
Thorp, R. W. (2003). Bumble bees (Hymenoptera: Apidae): commercial use and
environmental concerns. For nonnative crops, whence pollinators of the
future? K. Strickler and J. H. Cane. Lanham, Entomological Society of
America: 21-40.
Thorp, R. W. and J. M. Leong (1996). Specialist bee pollinators of showy vernal
pool flowers. Ecology, conservation, and management of vernal pool
ecosystems--proceedings from a 1996 conference, California Native Plant
Society.
Torchio, P. F. (2003). The development of Osmia lignaria Say (Hymenoptera:
Megachilidae) as a managed pollinator of apple and almond crops: a case
history. For nonnative crops, whence pollinators of the future? K. Strickler
and J. H. Cane. Lanham, Entomological Society of America: 67-84.
Vasquez, D. P. and D. Simberloff (2002). Ecological specialization and
susceptibility to disturbance: conjectures and refutations. The American
Naturalist 159(6): 606-623.
Walther-Hellwig, K. and R. Frankl (2000). Foraging habitats and foraging
distances of bumblebees, Bombus spp. (Hymenoptera: Apidae), in
agricultural landscape. Journal of Applied Entomolgy 124: 299-306.
Wilcove, D. S., D. Rothstein, J. Dubow, A. Phillips and E. Losos (1998).
Quantifying threats to imperiled species in the United States. BioScience
48(8): 607-618.
Williams, N. M., R. L. Minckley and F. A. Silveira (2001). Variation in native bee
faunas and its implications for detecting community changes. Conservation
Ecology 5(1): [online] URL: http://www.consecol.org/vol5/iss1/art7/.
Winfree, R., T. Griswold and C. Kremen (2007a). Effect of human disturbance on
bee communities in a forested ecosystem. Conservation Biology 21(1): 213223.
Winfree, R., N. M. Williams, J. Dushoff and C. Kremen (2007b). Native bees
provide insurance against ongoing honey bee losses. Ecology Letters 10:
1105-1113.
84
Winston, M. L. (1991). The biology of the honey bee, Harvard University Press.