Landscape Context Influences Bumble Bee
Communities in Oak Woodland Habitats1
Gretchen LeBuhn2 and Cynthia Fenter3
Abstract
Oak woodlands in Northern California are becoming increasingly fragmented due to
increasing urban and agricultural development. Much of the change in land use in Napa and
Sonoma counties has been from oak woodland to vineyards. Because bees do not use grape
flower pollen, a change in landscape use from oak woodland to vineyard may have an impact
on native bee communities. We examine how bumblebee, Bombus (Apidae), abundance and
species richness are affected by oak woodland fragmentation. Adaptations such as polylectic
foraging (utilizing multiple floral resources) and long flight distances may decrease the
impact of fragmentation on bumblebees. The study sites, six in Napa and six in Sonoma
counties, were determined to have varying percentages of vineyard in the area surrounding the
sites. Collections were made at each site twice per month between March and September 2002
to 2004. Bumblebees were collected in two ways: netting and using pan traps. We found no
significant difference between high and low vineyards in bumblebee abundance or richness.
However, bumblebees use more exotic plants in oak woodland surrounded by vineyard.
Keywords: Bumblebee, exotic plant, fragmentation, native plant, vineyard.
Introduction
In the wine country of California, natural areas are being converted to farmland and
pasturelands at a staggering rate. Between 1995 and 2000, more than 100,000 acres
of land in California were converted to wine-grape agriculture (Merenlender 2000).
These landscape changes in what are primarily oak woodland habitats may affect the
ecological integrity of the remaining oak woodland.
When a landscape is converted to agricultural use, the remaining habitats
become fragmented and with this fragmentation there can be an increase in edge
habitat and, often, there is an increase in invasive plant species (With 2002). Previous
work suggests that fragmentation may also cause declines in overall pollinator
abundance (Jennersten 1988, Goverde and others 2002) and native bee species
richness (Steffen-Dewenter 2002). Because bees do not use grape flower pollen,
change in landscape use from oak woodland to vineyard may have an impact on
native bee communities, either by changing the resources available to bees or by
changing the ability of bees to move through the landscape. Changes in the matrix
surrounding core habitats have been shown to influence the ability of other
invertebrates to traverse from one site to the next (Ricketts 2001).
The majority of previous investigations regarding landscape change in oak
woodlands focus on vertebrates and plants (e.g., Knapp and others 2001, Block and
Morrison 1998, Hilty and Merenlender 2004). Very little is known about the possible
1
An abbreviated version of this paper was presented at the Sixth California Oak Symposium, Today’s
Challenges, Tomorrow’s Opportunities, October 9-12, 2006, Rohnert Park, California.
2
Assistant Professor, San Francisco State University, Department of Biology. 1600 Holloway Avenue,
San Francisco, 94132.
3
Graduate Student, San Francisco State University, Department of Biology. 1600 Holloway Avenue,
San Francisco, 94132.
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GENERAL TECHNICAL REPORT PSW-GTR-217
effects that vineyards have on invertebrate populations. Recent work on solitary bees
in oak woodlands suggests that there is a decrease in species diversity and number of
species in habitats dominated by vineyards (LeBuhn, in prep).
Bumblebees (Bombus Latreille: Hymenoptera) have adaptations that may allow
them to persist in areas of fragmentation. Bumblebee body mass can range
(depending on species and hive duty) from 0.05g to 0.6g (Heinrich 1979). Being
relatively large, bumblebees can carry more nectar and pollen longer distances that
other bee genera. Bumblebees are able to warm and cool themselves using their flight
muscles, consequently enabling them to fly as well as forage within a greater range of
temperatures than bees that do not thermoregulate (Heinrich 1979). Bumble-bees are
polylectic foragers, and therefore may make use of exotic invasive plants species that
are a result of increased edges in fragmented habitats.
As part of a larger study on the impact of landscape change on the flora and
fauna of Napa and Sonoma counties, we examined population abundance and species
richness in oak woodland wild areas surrounded by different percentages of vineyard
to determine to what extent bumblebees are impacted by the surrounding vineyard
matrix. We also examined whether bumblebees utilize native plants and exotic plants
differentially.
Methods
Study Organisms
Bumblebees are eusocial insects that live in colonies founded by a single overwintering queen. The queen forages for nectar and pollen in early spring to provide
for her early brood members. Once the nest is established, workers take over the task
of foraging for the colony through the season. In mid- to late summer, new queens
and males are produced. The new males and reproductive queens leave the nest to
mate, and the new queens search for appropriate quarters for hibernation. The six
bumblebee species (B. vosnesneskii, B. californicus, B, sitkensis, B. melanopygus, B.
bifarius, and B. flavifrons) that we observed in Napa and Sonoma counties are
ground-nesting, generalist foragers that use a variety of floral resources; Bombus spp.
were observed using both native and non-native plants at all sites.
Sites
To evaluate the abundance and species richness of bumblebees, and to determine
whether there is a significant difference between native or exotic floral resource use
in fragmented oak woodlands, we chose sites using aerial photographs and GIS maps
of the Napa and Sonoma valleys. Potential study sites all met certain criteria for low
elevation (100 to 200m) and slope (5 to 15○) to reduce variance between sites. We
analyzed the percent of land that is vineyard within 1,000 m of each potential site.
Surrounding areas composed of greater than 35 percent vineyard were defined as
‘high’ vineyard and areas with less than 10 percent vineyard were defined as ‘low.’
We visited each potential sampling site and included all sites that had at least 1 ha of
oak woodland and that we were able to get permission to sample.
Sampling
We followed standard bee sampling techniques (protocols can be found at
http://online.sfsu.edu/~beeplot). Within each site a 100 m2 sample plot was
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Landscape Context Influences Bumble Bee Communities in Oak Woodland Habitats—LeBuhn
established. Collections were made at each site twice per month between March and
September in 2002, and between April and September 2003. Bumblebees were
sampled using nets and pan traps. Preliminary data and previous monitoring studies
show different colored pan traps attract different species of bee (Leong and Thorp
1999). Therefore, we used 30 plastic Solo Brand® bowls that were 5-in., 6-oz.—10
bowls each of white, blue, and yellow for each transect. The blue and yellow bowls
were painted with Krylon® fluorescent paint. The bowls were divided into sets of 30
(10 of each color) and numbered so that we could randomize the order of the colors.
Each bowl was placed 5m apart along two transects in each plot. The bowls were
filled with a stock solution of one teaspoon of Dawn® dish detergent per gallon of
water to reduce water surface tension in the pan traps. Bowls were set out between
09:00 and 15:00h. Bees caught in pan traps were pinned and identified to species.
We netted bumblebees for 1 hour in the morning and 1 hour in the afternoon per
sampling day. We divided each sampling plot into quadrants and netted within each
quadrant for 15 minutes. The host plant type being utilized by the bee at the time of
sampling was identified to species. At least one voucher specimen was taken of each
bumblebee and plant to verify identification. In 2002, to assess the availability of
floral resources, we identified to species (where possible) and measured the number
of open flowers per sampling event to the greatest order of magnitude (1, 10, 100, 1k,
10k, 100k, 1m, 10m).
Analysis
To determine if there is a significant difference between ‘high’ and ‘low’ vineyard
sites in bumblebee abundance and species richness, net data and pan trap data were
pooled and analyzed using a two-way ANOVA using SPSS (ver. 11.5). To examine
the relationship between host plant type and vineyard effect across both sampling
years, we created contingency tables using Statview (ver. 5.01)
Results
We found 6 species of the 12 distinct species of bumblebees reported in Napa and
Sonoma counties. They were from highest to lowest frequency (2002 sample / 2003
sample): B. vosnesenskii (604/210), B. californicus (49/80), B. melanopygus
edwardsii (16/64), B. flavifrons (1/5), B. bifarius (0/4), and B. sitkensis 0/1). B.
vosnesenskii was the most abundant species across all sites and years. There were
three species on average in both high and low vineyard sites in 2002 and 2003. We
had significantly higher numbers of bumblebee observations overall in 2002 (670)
relative to 2003 (389).
We found no difference in the richness or abundance (table 1) of bumblebees
between sites surrounded primarily by vineyard and sites embedded in a natural
landscape in either year.
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GENERAL TECHNICAL REPORT PSW-GTR-217
Table 1—Two-way analysis of variance of natural log of species richness and natural log of
abundance.
Source
Type III
Sum of
Squares
Mean
Square
df
F
Sig.
Species Richness
Year
Vineyard
Year*Vineyard
0.001
0.007
0.171
1
1
1
0.001
0.007
0.171
0.011
0.064
0.159
0.917
0.803
0.221
Abundance
Year
Vineyard
Year*Vineyard
1.490
2.531
0.505
1
1
1
1.490
2.531
0.505
1.674
2.843
0.567
0.210
0.107
0.460
In addition, we found that bumblebees were using native plants less frequently
than exotic species in both the high and low vineyard sites in 2002 and 2003 (figure
1, 2002: X2=3.928, p-value = 0.0475, 2003: X2=7.871, p-value = 0.005 ). In 2002,
there were 216 observations of bumblebees on exotic species and 57 on native
species in high vineyard sites, and 294 observations of bumblebees on exotic species
and 38 on native species in low vineyard sites. In 2003, there were 123 observations
of bumblebees on exotic species and 47 on native species in high vineyard sites, and
96 observations of bumblebees on exotic species and 14 on native species in low
vineyard sites.
1
.9
.8
.7
.6
.5
.4
.3
.2
.1
0
Exotic
Native
Exotic
Native
Figure 1—Proportion of bumblebee visits to exotic or native host plant in 2002.
Striped bars are in a high vineyard environment. Solid bars are in a low vineyard
environment.
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Landscape Context Influences Bumble Bee Communities in Oak Woodland Habitats—LeBuhn
Discussion
Our results indicate that there was no difference in the richness or abundance of
bumblebees between sites surrounded primarily by vineyard and sites embedded in a
natural landscape. This is not to say that fragmentation or landscape conversion is
beneficial, it only underlines how remarkably adaptive some organisms are in the
face of abrupt modification of their surrounding landscape.
Landscape change is one cause of fragmentation, which may decrease bee
abundance and species richness (Jennersten 1988, Steffen-Dewenter and Tscharntke
2002, LeBuhn unpublished data). However, other work suggests that certain species
of native bees can thrive in a fragmented landscape depending upon foraging
behavior and nest site availability (Cane 2001, Steffen-Dewenter 2002).
We found that the most common species, of the six that we observed, at all sites
were Bombus vosnesenskii, Bombus californicus and Bombus melanopygus var.
edwardsii and that there were three species on average in both ‘high’ and ‘low’
vineyard sites. On record, there are 12 distinct species of Bombus in Napa and
Sonoma counties (R. Thorp pers. comm.). It may be that although there remains some
contiguous wild area in these valley oak woodlands, overall species richness is low
on a larger landscape scale than this study measures. McFrederick and LeBuhn
(2006) found that bumblebees in urban parks in San Francisco are experiencing low
species richness as compared to surrounding wild areas. This suggests that the loss of
certain species in fragmented areas may be due to interspecies competition. More
work on competition effects between species of bumblebees within urban parks as
well as fragmented oak woodlands may uncover the effects of interspecies
competition on species richness in fragmented landscapes.
One explanation for bumblebees showing no marked change in numbers
between sites is that they do not experience the sites as fragments. The adaptive
physical and behavioral characteristics that allow bumblebees to be unaffected by
landscape change may be due to their greater foraging abilities. Bombus spp. foraging
distances can range from 50m to 80km in extreme cases (Mikkola 1984), with
averages around 350m (Dramstad 1995, Osborne and others 1999). Davies and others
(2000) found that, species that experience isolation due to fragmentation are at
greater risk for declines in population. Their larger body size, thermoregulation and
generalist foraging habits may allow them to nest in one fragment and find suitable
host plants in a number of other fragments.
Bumblebees need two resources to persist in a given habitat: floral resources and
nesting sites. As relatively long-lived, generalist foragers, bumblebees are able to use
a wide variety of floral resources, but those resources must persist throughout the
foraging season. Interestingly, after July 1, 2002, nearly all host plants visited by
bumblebees were exotic, even though 30 percent of the plants in bloom after July 1
were native (Fenter and LeBuhn in prep.).
It is possible that the length of the foraging season for bumblebees may be
extended artificially by these non-native plants, an unexpected positive benefit of the
expansion of exotic plant species. This study does not make the claim, however, that
invasive species are utilized at an equal or greater frequency than native species due
to any preference, rather, that due to a greater likelihood of invasive plant species
later in the season, bumblebees are utilizing these available resources. These results
suggest that the biology of a particular species of Bombus will influence the response
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GENERAL TECHNICAL REPORT PSW-GTR-217
of that species to landscape change and that there may be a correlation between
foraging behavior and fitness in fragmented oak woodland.
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