COMMUNITY AND ECOSYSTEM ECOLOGY

Effects of Suburbanization on Forest Bee Communities

ADRIAN L. CARPER,1,2,3 LYNN S. ADLER,4 PAIGE S. WARREN,5 AND REBECCA E. IRWIN1

Environ. Entomol. 43(2): 253Ð262 (2014); DOI: http://dx.doi.org/10.1603/EN13078

ABSTRACT Urbanization is a dominant form of land-use change driving species distributions,
abundances, and diversity. Previous research has documented the negative impacts of urbanization
on the abundance and diversity of many groups of organisms. However, some organisms, such as bees,
may beneÞt from moderate levels of development, depending on how development alters the

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availability of foraging and nesting resources. To determine how one type of low-intensity human
development, suburbanization, affects bee abundance and diversity and the mechanisms involved, we
surveyed bees across suburban and natural forests in the Raleigh-Durham area of North Carolina. We
sampled for bees using a combination of bee bowls and hand-netting from March through July of 2008
and 2009. We found higher bee abundance in suburban than natural forests, and although observed
species richness was greater in suburban than natural forests, there were no signiÞcant differences in
rareÞed richness or evenness estimates in either year. In addition, the effects of suburbanization were
similar across bee species of varying ecological and life-history characteristics. At the local scale, bee
abundance and species richness were both positively related to the abundance and richness of
ßowering species within forests, while the proportion of surrounding developed open areas, such as
yards and roadsides, was a strong positive predictor of both bee abundance and richness at the
landscape scale. These results suggest that open habitats and the availability of ßoral resources in
suburban sites can support abundant and diverse bee communities and underscore the potential for
native bee conservation in urban habitats.

KEY WORDS bee, land use, pollinator, suburban, urban

Land-use change is a leading component of human-
induced environmental change (Kalnay and Cai 2003)
that has ecological consequences at both local and
global scales (Foley et al. 2005). Urbanization (the
expansion of developed residential, municipal, and
industrial areas) is a dominant form of land-use change
that has drastically expanded in recent history (Irwin
and Bockstael 2007), reducing biodiversity through
habitat loss, fragmentation, and competition with in-
troduced, competitively dominant, and often synan-
thropic species (Shochat et al. 2010). Declines in spe-
cies richness (Burkle et al. 2013) also raise concern
over the stability of natural communities and the eco-
system services they provide (Eigenbrod et al. 2011).
Bees are an important group of organisms in urban
and natural areas, given their importance as pollina-
tors. Approximately 87% of ßowering plants rely on
pollinators, especially bees, to reproduce (Ollerton et
al. 2011). A growing body of evidence points to a
1 Department of Biological Sciences, Dartmouth College, 78 Col-
lege St., Hanover, NH 03755.
2 Present address: Department of Ecology and Evolutionary Biol-
ogy, University of Colorado, Ramaley N122, Boulder, CO 80309.
3 Corresponding author, e-mail: adrian.l.carper@colorado.edu.
4 Biology Department, 221 Morrill Science Center South, 611 N.
Pleasant St., University of Massachusetts, Amherst, MA 01003.
5 Department of Environmental Conservation, University of Mas-
sachusetts, 216 Holdsworth, Amherst, MA 01003.
decline in bee populations (Biesmeijer et al. 2006,
Cameron et al. 2011, Bartomeus et al. 2013, Burkle et
al. 2013), and habitat loss because of land-use changes
is hypothesized as a major factor (Winfree et al. 2009).
For example, bee abundance and diversity often de-
cline with increasing metrics of urbanization, such as
built landscape (Bates et al. 2011), a pattern suggested
as a general trend (Hernandez et al. 2009). However,
the effects of urbanization likely vary with the degree
or type of anthropogenic disturbance (Winfree et al.
2009), with the potential costs and beneÞts likely de-
pendent on a variety of factors, including the type of
development, the surrounding natural habitat, and the
availability of foraging and nesting resources. For ex-
ample, urban gardens can promote diverse bee assem-
blages (Fetridge et al. 2008), and the number of gar-
dens in the surrounding landscape has been shown
to positively inßuence bumblebee colony survival
(Goulson et al. 2010). Moderate levels of human dis-
turbance, such as rural and suburban development,
could represent intermediate levels of disturbance
that promote species coexistence (Connell 1978) and
therefore could hold potential for bee conservation.
However, more studies are needed to document pat-
terns and identify mechanisms driving bee abundance
and species richness.
To understand how one type of human develop-
ment, suburbanization, affects bee abundance and

0046-225X/14/0253Ð0262$04.00/0 䉷 2014 Entomological Society of America

254 ENVIRONMENTAL ENTOMOLOGY
richness and the mechanisms involved, we surveyed
bees across paired suburban and natural forests in a
metropolitan area of the southeastern United States.
We deÞned suburban development as single-family,
residential neighborhoods encompassed within or on
the edge of more intensively incorporated metropol-
itan areas. We asked the following questions: 1) How
does suburbanization affect forest bee abundance,
richness, and composition? We predicted that subur-
ban sites would have higher bee abundance and rich-
ness given that suburbs typically have gardens and
green spaces and are often esthetically managed to
provide ßowers throughout the growing season, which
could beneÞt bees. However, the response of individ-
ual bee species to suburbanization may vary with eco-
logical or life-history characteristics (Williams et al.
2010). Therefore, we predicted that suburban forests
would have more polylectic bees because of increased
availability of exotic ßowers in suburban gardens on
which generalist bees could forage, and more soil and
hive-nesting bees because of increased availability of
open areas, such as yards and roadsides, and bare
ground from human activities, such as gardening and
erosion. Conversely, we expected natural forests to
have greater abundances of oligolectic, pith, and stem-
nesting bees because larger forests likely retain more
native ßowers and Þne woody nesting substrates. 2)
What local and landscape factors affect bee commu-
nities? Bee abundance and richness can be driven by
both the abundance and richness of ßoral resources
(Potts et al. 2003) and the availability of suitable nest-
ing substrates in the landscape (Cane et al. 2006). We
predicted bee abundance and richness would increase
with local ßoral abundance and richness. However,
bees can forage widely, and some patterns of abun-
dance or richness may not be evident at local scales.
At the landscape scale, we predicted open and low-
intensity developed land covers would be strong pos-
itive predictors of bee abundance and species richness
because open surroundings likely provide superior
foraging and nesting resources (McFrederick and
LeBuhn 2006).
Materials and Methods
Study Area. We conducted this study in Raleigh-
Durham, NC (hereafter RDU). RDU is one of the
fastest growing urban areas in the United States (U.S.
Census Bureau 2009) and is located in a region un-
dergoing some of the fastest rates of land-cover
change in the eastern United States (Brown et al.
2005). The two counties surrounding RDU (Durham
and Wake) include ⬇737,000 single-family detached
homes (62.5% of residences; NC OfÞce of State Budget
and Management), creating a matrix of suburban de-
velopments in proximity to large tracts of naturally
occurring forest. Using a paired approach, we identi-
Þed Þve sites within suburban forests and Þve sites in
managed natural areas (hereafter, suburban forests
and natural forests, respectively). We paired sites and
located each pair at least 5 km apart. Natural forests
consisted of contiguous tracts of mixed pine and hard-
Vol. 43, no. 2
wood forest that were ⬎10 ha and primarily managed
for the conservation of their natural resources, such as
county and state parks. Suburban forests consisted of
persistent wooded patches in single-family housing
developments located ⬍5 km from each correspond-
ing forested site (Supp. Table 1 [online only]). We
established equal-sized sampling plots within each site
pair ranging from 0.22 to 0.57 ha (Supp. Table 1 [online
only]). The paired approach allowed us to control for
landscape-scale differences in site characteristics
while minimizing potential overlap in bee foraging
within pairs.
Bee Abundance, Richness, and Composition. We
sampled bees over two ßowering seasons: May
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through July of 2008 and April through July of 2009.
Sampling occurred approximately once per month in
2008 (three sampling dates) and twice per month in
2009 (six sampling dates). Bees were sampled using
pan traps and hand-netting following a standard pro-
tocol (LeBuhn et al. 2003). Pan traps were made from
9-cm diameter plastic bowls (Fisherbrand Hexagonal
Polystyrene Weighing Dishes, Pittsburgh, PA) that
were left white or painted ßuorescent blue or yellow.
In each site, we arranged 15 pan traps (5 of each color)
Þlled with soapy water along a single 70-m transect,
with 5 m between each trap. Transects were laid hap-
hazardly within contiguous sampling plots except in
two of the suburban sites, where two smaller forest
patches were bisected by roads or driveways (RV and
SC; Supp. Table 1 [online only]). We randomly as-
signed the color of pan traps to their positions along
each transect and left the traps on the forest ßoor from
0800 to 1800 hours EDT. Captured bees were strained,
rinsed, and dried before sorting. Hand-netting was
conducted for 1 h per plot per sampling period to
capture bees not attracted to pan traps. We conducted
netting between 1000 and 1400 hours, during peak bee
activity, and euthanized bees in ethyl acetate collect-
ing jars. Suburban and natural forests were consecu-
tively sampled within each site pair, with the order
(suburban or natural forest Þrst) randomly chosen. In
2008, hand-netting corresponded to pan-trapping ses-
sions by sampling one site pair per day. In 2009, pan
trapping was done simultaneously across all sites, and
hand-netting was conducted in each site pair within
24 Ð 48 h of pan-trapping events. All bees were pinned,
labeled, identiÞed to either species or morphospecies,
and housed in a collection at Dartmouth College.
We compiled ecological and life-history informa-
tion for each bee species from the primary literature,
historical accounts, Discover Life (Ascher and Pick-
ering 2012), and consultation with experts (J. Ascher,
personal communication). For each bee species, we
characterized nesting substrate (soil, wood, pithy
stems, cavity, or hive), ßoral specialization (oligolec-
tic vs. polylectic), and sociality (solitary, subsocial,
eusocial, or parasitic). Only those species that foraged
on a single plant family or a subset of ßowering genera
were considered oligolectic. We separated bees that
nest in existing cavities in wood as cavity instead of
wood nesters. Lumping cavity and wood-nesting spe-
cies had no effect on the interpretation of results. We
April 2014 CARPER ET AL.: EFFECTS OF SUBURBANIZATION ON FOREST BEE COMMUNITIES
also classiÞed bee species according to body size by
measuring intertegular span for up to three females
per species and calculating body mass through a
known relationship between intertegular span and dry
body mass (Cane 1987). We classiÞed species as small
(⬍4 mg), medium (4 Ð16 mg), or large (⬎16 mg; Win-
free et al. 2007), reßecting the quantiles of the size
distribution.
Data Analysis. All statistical analyses (throughout
the study) were conducted using SAS version 9.2 (SAS
Institute 2009) unless otherwise noted. The number of
bees captured using pan traps and hand-netting was
combined within each site for each sampling date. To
estimate bee abundance, we calculated the mean
number of bees per sampling event per site for each
year. Analyzing total bees across sampling events per
site yielded similar results (data not shown). To esti-
mate bee diversity, we used species richness (the
combined number of species captured across all sam-
pling events at each site across both years) and Simp-
sonÕs Evenness index. To account for differences in
bee abundance on estimates of species richness, we
rareÞed samples to the lowest common abundance
using ECOSIM software (Gotelli and Entsminger
2001). To account for the paired approach, we used
one-tailed paired t-tests (JMP version 8.0.2, SAS In-
stitute) to test whether suburban forests had higher
bee abundance and species richness than natural for-
ests. We had no a priori prediction about the effects
of suburbanization on species evenness, so we used a
two-tailed paired t-test to assess whether suburban-
ization affected evenness.
To compare species composition between suburban
and natural forests, we used a series of approaches.
First, we calculated MorisitaÕs C and percentage sim-
ilarity for each site pair and for pooled captures across
the Þve suburban and Þve natural sites. We used
MorisitaÕs C because it is less inßuenced by sample size
and species richness than other similarity indices
(Wolda 1981). Second, we tested for spatial autocor-
relation in bee abundance and species richness be-
tween sites by computing MoranÕs I. Third, we used
nonmetric multidimensional scaling (NMDS), via the
“vegan” package (Oksanen et al. 2012) in R version
2.14, to visualize any dissimilarity in bee community
composition between suburban and forested sites. We
conducted the NMDS using the Bray-Curtis dissimi-
larity measure, which takes into account the number
of unique species between two sites relative to the
total number of species sampled. The relative Þt of the
NMDS was evaluated by computing the Þnal stress of
the ordination. Stress is a measure of mismatch be-
tween the rankÐ order dissimilarities and the ordina-
tion distance, often referred to as a badness-of-Þt test,
with values ⬍0.05 indicating strong support for the
ordination distances.
To determine whether the effects of suburbaniza-
tion varied with bee ecology or life-history, we used
generalized linear models (PROC GLIMMIX). We
included forest type (suburban or natural forest)
along with nesting habit, lecty, sociality, and body size
as Þxed factors in four separate analyses, including
255
interactions, and site as a random effect. We used the
combined bee abundance across both years as re-
sponse variables, specifying a negative binomial dis-
tribution to reduce overdispersion. A signiÞcant in-
teraction between forest type and nesting habit, lecty,
sociality, or body size would suggest that the effects of
suburbanization on bee abundance are driven by
groups of species with particular ecological or life-
history characteristics.
Factors Driving Bee Abundance and Composition.
At the local scale we estimated both foraging and
nesting resources. We conducted ßower censuses
over the entire area sampled for bees in each site,
corresponding to each bee sampling event, in 2008 and
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2009. We recorded the total number of individuals of
each ßowering species and counted the number of
ßowers on a subset of 10 haphazardly chosen individ-
uals per species. For plants in the Asteraceae, we
recorded the number of ßowering heads containing
open disc ßowers on each plant. On large shrubs and
trees with ⬎500 ßowers, we counted the number of
ßowers on three separate branches and multiplied the
average number of ßowers per branch by the total
number of ßowering branches to estimate the total
number of ßowers per plant. We then multiplied the
mean number of ßowers per plant by the total number
of individuals to estimate the total number of ßowers
per species per plot, and calculated ßower density by
dividing by the area of each plot.
Nesting resources may also be important in driving
bee abundance and diversity (Cane et al. 2006). To
estimate wood-nesting resources, we used three 20-m
line-intercept transects in each site to quantify coarse
woody debris (CWD) in 2009. We recorded the length
and width of dead wood ⱖ7.5 cm in diameter inter-
secting each transect (Woodall and Monleon 2008).
We then calculated the volume of CWD per square
meter using a standard formula, V ⫽ ␲2兺d2/8L, where
V is the volume of woody debris per unit area, d is the
diameter of each piece of wood, and L is the length of
the transect (Harmon et al. 2004). We observed no
bare ground along any transect and thus were unable
to quantify it as substrate for soil nesting.
Lastly, we incorporated measures of other abiotic
factors that could directly or indirectly affect bee
activity or abundance. Changes in climate associated
with urban development have been shown to alter
animal distributions (Parris and Hazell 2005). Differ-
ences in temperature or relative humidity (RH) could
affect bee activity and the likelihood of capture, or the
distribution or phenology of suitable host plants. To
characterize temperature and RH, two iButton data
loggers (Embedded Data Systems LLC, Lawrence-
burg, KY) were haphazardly placed in each site to
record temperature and RH hourly over the ßowering
season in 2009. iButtons were mounted beneath low-
lying branches and shielded with a small plastic rain
guard.
At the landscape scale, we used data from the 2006
National Land Cover Database (Fry et al. 2011) to
explore how land-use cover affected bee abundance.
The National Land Cover Database uses satellite im-
256 ENVIRONMENTAL ENTOMOLOGY
Fig. 1. Suburban forests exhibited greater bee abundance (a) and observed species richness (b) than natural forests in
2008 and 2009, but no difference in rareÞed species richness (c). Bars are means ⫾ SE. Asterisks indicate signiÞcant differences
(P ⬍ 0.05).
agery to characterize land cover at a 30-m resolution.
We calculated the proportions of surrounding land
covers within a 1-km radius of the center of each site
using ArcGis (version 9.3.1, ESRI, Redlands, CA) and
identiÞed the four most dominant land covers: ever-
green (pine) forest, deciduous forest, developed open
space (⬍20% impervious surface), and low-intensity
developed (20 Ð 49% impervious surface). We chose 1
km because it likely encompasses the foraging dis-
tance of most of the species sampled while leaving
little overlap within site pairs.
Data Analyses. At the local scale, we compared
ßower species richness, ßoral density, and CWD be-
tween forest types in each year using one-tailed paired
t-tests to test the hypothesis that suburban forests have
greater ßoral resources but fewer nesting resources
compared with natural forests. We also used linear
regression to determine whether ßoral density and
richness predicted bee abundance and richness. We
calculated mean, minimum, and maximum daily tem-
perature, as well as RH, averaging values from the two
iButtons in each site. We compared each metric of
temperature and RH between forest types using sep-
arate repeated measures analyses of variance.
At the landscape scale, we compared land cover
types between suburban and natural forests using mul-
tivariate analysis of variance, with site pair and forest
type as Þxed factors and the proportions of the four
dominant land covers as responses. We used multiple
regressions (JMP version 8.0.2, SAS Institute) to de-
termine whether land cover predicted bee abundance
and species richness. Each proportion of land cover
was log-transformed to meet the assumptions of ho-
moscedasticity, and multicollinearity was assessed
from the variance inßation factors.
Results
In 2008, we captured 258 bees (mean: 86 bees per
sampling event, pooled across sites) and in 2009, 365
bees (mean: 61 bees per sampling event), belonging to
six families, 26 genera, and 71 species or morphospe-
cies. All but Þve individuals were identiÞed to species.
One Lasioglossum sp. male, one Ceratina sp., and three
Nomada sp. males were identiÞed as morphospecies.
In addition, we combined individuals in two taxo-
nomic groupings currently being revised: 11 Hylaeus
affinis Smith/modestus Say and 19 Halictus ligatus Say/
Vol. 43, no. 2
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poeyi Lepeletier. Each of these two groupings was
treated as a single species in subsequent analyses. The
two most dominant bee species, Augochlorella aurata
Smith (Halictidae) and Lasioglossum bruneri Craw-
ford (Halictidae), represented 17 and 14% of all bees
collected, respectively. Exotic bee species were rare
and made up ⬍3% of the total number of captures. We
captured eight honeybees (Apis mellifera L.) in sub-
urban forests and two in natural forests. We also cap-
tured two giant resin bees (Megachile sculpturalis
Smith) and Þve alfalfa leafcutting bees (Megachile
rotundata F.) in suburban forests. In addition, we
captured 38 species that were each represented by a
single specimen, including 28 from suburban and 10
from natural forests (Supp. Table 2 [online only]).
Bee Abundance, Richness, and Composition. Sub-
urban forests had 2.2 times more bees captured per
sampling event than natural forests in 2008 (t4 ⫽ 1.99,
P ⫽ 0.059) and 1.8 times more bees in 2009 (t4 ⫽ 2.88,
P ⫽ 0.022, Fig. 1a). In suburban forests, bee richness
ranged from 7 to 19 species compared with natural
forests, where bee richness ranged from 6 to 16 spe-
cies. Although observed species richness was signiÞ-
cantly higher in suburban forests in both years (2008:
t4 ⫽ 2.87, P ⫽ 0.027; 2009: t4 ⫽ 4.78, P ⫽ 0.004; Fig. 1b),
rarefaction yielded no signiÞcant difference in species
richness between suburban and natural forests in ei-
ther year (2008: t4 ⫽ ⫺1.45, P ⫽ 0.09; 2009: t4 ⫽ ⫺0.52,
P ⫽ 0.31; Fig. 1c). We also detected no spatial auto-
correlation in either year (MoranÕs I ⫽ ⫺0.11, P ⫽
0.808, MoranÕs I ⫽ ⫺0.12, P ⫽ 0.420, respectively).
Percentage similarity between paired suburban and
natural forests ranged from 21.8 to 45.2%. Pooled
across site pairs and years, suburban and natural for-
ests were characterized by 59.3% similarity (MorisitaÕs
C ⫽ 0.85). The most abundant genus sampled was
Lasioglossum, with 19 total species, 7 of which were
unique to suburban forests, compared with only 3
species unique to natural forests. Suburban forests also
yielded nearly three times as many singletons (species
represented by a single captured individual) as natural
forests (28 vs. 10 species, respectively). However,
there was no signiÞcant difference in SimpsonÕs Even-
ness between suburban and natural forests (t4 ⫽ 1.32,
P ⫽ 0.258). NMDS indicated overlap in bee compo-
sition between suburban and natural forests, driven
mainly by one natural forest site (Fig. 2). The Þnal
April 2014 CARPER ET AL.: EFFECTS OF SUBURBANIZATION ON FOREST BEE COMMUNITIES 257

cant. Bee abundance varied by sociality, with eusocial

bees representing 65% of bees sampled, followed by
solitary bees (21%), subsocial (9%), and parasitic bees
(5%). Suburban forests had more bees in each sociality
category compared with natural forests (Fig. 3b). Me-
dium-sized bees were the most common bees cap-
tured, representing 51% of individuals, followed by
small and large bees making up 36 and 13%, respec-
tively. Suburban forests had more bees in each size
class compared with natural forests (Fig. 3c). Finally,
soil-nesting bees were the most abundant, comprising
⬇70% of individuals, with cavity nesters making up
11%, hive and stem nesters each making up ⬇9%, and
wood nesters making up ⬍1% (Fig. 3d).

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Factors Driving Bee Abundance and Composition.
Bee communities were affected by both local and
landscape scale factors. At the local scale, ßoral re-
sources were the strongest factor affecting bees. Flow-
ering tree species were the dominant ßoral resource in
suburban and natural forests. Oxydendrum arboreum
Fig. 2. NMDS indicated overlap in bee communities be- (L.) (Ericaceae) was the most abundant ßower re-
tween suburban and natural forests driven primarily by one source within sampling plots, constituting 47% of all
natural forest, Lake Crabtree County Park, overlapping with ßowers surveyed, followed by Ilex opaca (Alton)
suburban forests. (Aquifoliaceae) at 9% of ßowers. Aside from trees, the
three most abundant ßowering species were Erigeron
stress of the NMDS with two dimensions was 0.11, annuus (L.) (Asteraceae), Lonicera japonica (Thunb.)
indicating fair conÞdence in the ordination distances. (Caprifoliaceae), and Rubus argutus (Link) (Rosa-
Bee abundance varied as a function of ecological ceae), making up 8, 4, and 3% of surveyed ßowers,
and life-history traits and suburbanization; however, respectively. The remaining 68 species recorded made
there were no signiÞcant interactions between any of up ⬍2% of total ßower abundance each. Suburban
the ecological traits considered and suburbanization forests averaged 3.4 ⫾ 2.8 (mean ⫾ SE) and 6.2 ⫾ 3.3
(Table 1), suggesting that higher bee abundance in more ßowering species than natural forests in 2008 and
suburban sites was not driven by bees with particular 2009, respectively, but these differences were not sta-
ecological or life-history characters. Generalist bees tistically signiÞcant in 2008 (t4 ⫽ ⫺1.22, P ⫽ 0.143) or
were more abundant than specialist bees, with 2009 (t4 ⫽ ⫺1.87, P ⫽ 0.067). Suburban forests also had
polylectic species making up ⬎98% of bees captured, 14.3% greater density of ßowers than natural forests in
compared with ⬍2% that were oligolectic. Although 2008 (1.09 ⫾ 0.57 vs. 1.25 ⫾ 0.46 ßowers per square
suburban forests had 2.3 times more polylectic bees meter). However, the opposite pattern occurred in 2009
and 1.98 times more oligolectic bees (Fig. 3a), the when natural forests had 13.8% more ßowers per square
effect of suburbanization was not statistically signiÞ- meter than suburban sites (0.95 ⫾ 0.61 vs. 0.83 ⫾ 0.16
ßowers per square meter), but in neither year were these
differences in ßoral density statistically signiÞcant (2008:
Table 1. Generalized linear models of bee abundance by four t4 ⫽ ⫺0.26, P ⫽ 0.403; 2009: t4 ⫽ 0.17, P ⫽ 0.436). There
ecological characteristics (lecty, sociality, body size, and nesting was no relationship between the total number of ßowers
substrate) and forest type (suburban vs. natural)
and total bee abundance in either year (2008: r2 ⫽ 0.23,
Ecological trait df F P P ⫽ 0.164; 2009: r2 ⫽ 0.002, P ⫽ 0.905). However, ob-
served bee richness and total bee abundance increased
Lecty
Lecty 1,12 122.03 ⬍0.001 signiÞcantly with ßower richness in suburban sites in
Forest type 1,12 4.15 0.0642 2008 (richness: r2 ⫽ 0.61, P ⬍ 0.005; abundance: r2 ⫽ 0.65,
Lecty*forest type 1,12 0.05 0.8281 P ⫽ 0.005; Fig. 4a and b), though neither relationship
Sociality
Sociality 3,28 33.87 ⬍0.001
remained signiÞcant in 2009 (richness: r2 ⫽ 0.091, P ⫽
Forest type 1,28 17.57 ⬍0.001 0.396; abundance: r2 ⫽ 0.07, P ⫽ 0.46).
Sociality*forest type 3,28 1.96 0.143 The total volume of CWD ranged from 0.011 to
Body size 0.041 m3/m2 in natural forests and 0.006 Ð 0.021 m3/m2
Body size 2,20 26.92 ⬍0.001
Forest type 1,20 25.03 ⬍0.001 in suburban forests; however, natural forests showed
Body size*forest type 1,20 1.7 0.208 no signiÞcant difference in the volume of CWD from
Nesting substrate suburban forests (t4 ⫽ 0.80, P ⫽ 0.24). Given the low
Nesting 4,36 57.92 ⬍0.001 representation of wood-nesting species in our samples
Forest type 1,36 8.12 0.007
Nesting*forest type 4,36 0.99 0.424 (⬍1% of total bee captures), we did not further pursue
CWD as a mechanism driving bee abundance or rich-
*
represents an interaction between the main effects. ness. Neither mean, maximum, or minimum daily tem-
258 ENVIRONMENTAL ENTOMOLOGY Vol. 43, no. 2

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Fig. 3. There were no signiÞcant interactions between forest type and ecological categories studied. Compared with
natural forests, suburban forests supported a signiÞcantly greater abundance of bees across all foraging habits (a), socialities
(b), body sizes (c), and nesting types (d). Bars are means ⫾ SE.

peratures nor RHs signiÞcantly differed between for-
est types in 2009 (in all cases: F1,8 ⬍ 1.6, P ⬎ 0.24).
At the landscape scale, land cover varied across sites,
with deciduous and evergreen forests, developed open
space, and hay or pasture the most dominant land covers
(Fig. 5). Suburban forests were surrounded by four
times more low intensity development and nearly Þve
times more developed open space as natural forests
(WilkÕs ␭ ⫽ 0.198, F4,5 ⫽ 5.07, P ⫽ 0.052). The proportion
of developed open space in the surrounding landscape
was signiÞcantly and positively associated with both bee
abundance and species richness (Table 2). However,
bee abundance and richness were negatively associated
with the proportion of low-intensity development in the
landscape, although the relationship was only statistically
signiÞcant for bee abundance (Table 2). All variance

Fig. 4. Flower richness within suburban forests in 2008 was a signiÞcant predictor of suburban bee abundance (a) and
species richness (b), though no relationship existed in natural forests.
April 2014 CARPER ET AL.: EFFECTS OF SUBURBANIZATION ON FOREST BEE COMMUNITIES 259

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Fig. 5. The dominant land cover types surrounding suburban and natural forests were calculated using a 1-km buffer
around each site center. Land cover types in the “Other” category include cultivated crops, developed high intensity,
shrub/scrub, barren land, emergent herbaceous, and wetlands.

inßation factors were small (⬍5), suggesting multicol- port a diversity of native bees (Matteson et al. 2008,
linearity had little effect on results. Banaszak-Cibicka and Zmihorski 2012). Although we
found that observed species richness was higher in
Discussion suburban forests across both years, the lack of differ-
ence between rareÞed species richness suggests that
Suburbanization can have powerful effects on the low richness in natural forest sites could be a result of
abundance and richness of both plants and animals low bee abundance and reduced likelihood of capture.
(Shochat et al. 2006). Here, we report that forests Nonetheless, the Þnding that suburban areas harbor
within suburban development in a metropolitan area more abundant and at least as rich bee communities as
of the southeastern United States have higher bee nearby natural areas is consistent with some studies.
abundance than natural forests. Moreover, suburban For example, Winfree et al. (2007) found that both bee
forests had more bees of all ecological and life-history abundance and species richness were higher in sub-
characteristics that we sampled. At the local scale, bee urban and urban development than in extensive for-
abundance and richness were positively associated ests in New Jersey. However, other studies comparing
with ßower abundance and richness, though the re- bee richness in desert and residential areas have
lationship varied between years. At the landscape found higher richness in the natural desert habitat
level, bee abundance and richness were positively (Hostetler and McIntyre 2001, Gotlieb et al. 2011).
associated with the amount of open space, and neg- Thus, while some aspects of residential areas may
atively associated with low-intensity development. beneÞt bees, the overall landscape context is likely
Taken together, these results suggest that the combi- important in driving species richness patterns (Ahrne
nation of open habitats and availability of diverse ßoral
et al. 2009).
resources in suburban sites are capable of sustaining
Contrary to our predictions, bee community com-
abundant and diverse bee communities.
position exhibited little difference between suburban
These results add to a growing body of literature
and natural forests. We found no interactions between
demonstrating that urban and suburban areas can sup-
forest type and ecological or life-history categories on
bee abundance, implying that all types of bees in our
Table 2. Least squares multiple regressions of bee abundance study system responded similarly to suburbanization.
and observed species richness against the proportion of four dom- This result contradicts empirical work that demon-
inant land-cover types surrounding each of 10 study sites
strated guild-speciÞc responses of bees to disturbance
Land-cover type ␤ SE t P (Williams et al. 2010). Without more precise mea-
surements of characteristics, such as the distribution
Abundance
Log (deciduous forest) 11.07 12.92 0.86 0.431 and availability of nesting substrates, it is difÞcult to
Log (evergreen forest) ⫺13.59 17.27 ⫺0.79 0.467 speculate why no differences were observed. One
Log (developed, low intensity) ⫺21.33 7.85 ⫺2.72 0.042 explanation is that bees captured in the forest are
Log (developed, open space) 44.30 12.02 3.69 0.014
Species richness
primarily moving between widely distributed re-
Log (deciduous forest) 5.53 2.32 2.38 0.063 sources in the landscape, and the scale of our sampling
Log (evergreen forest) ⫺2.58 3.10 ⫺0.83 0.444 did not adequately reßect the scale at which differ-
Log (developed, low intensity) ⫺3.11 1.41 ⫺2.21 0.079 ences in community composition are evident. The 71
Log (developed, open space) 7.30 2.16 3.39 0.020
species captured are also only a subset of the regional
260 ENVIRONMENTAL ENTOMOLOGY
bee fauna, and our sampling periods may have missed
some species, such as early and late season specialists.
Regardless, suburban bee community composition ap-
pears similar to that of natural forests, only more abun-
dant. This pattern was reinforced by overlap in NMDS,
which suggests that the bee community composition
was fairly similar across forest types. However, it is
important to note that the NMDS overlap was driven
primarily by one natural forest, Crabtree County Park.
Interestingly, this was the only natural forest site that
actively planted ßowers along roadsides and park
structures (A.C., unpublished data), and thus had
much higher ßoral density than the other naturally
forested sites. If such planted resources are important
factors structuring bee communities, they could ex-
plain the potential overlap. Further work on the role
of planted ßoral resources is needed to determine
whether they can affect forest bee communities.
The abundance and diversity of ßoral resources are
dominant factors structuring bee communities (Potts
et al. 2003), and ßoral resources within urban areas can
support a variety of bee species (Tommasi et al. 2004).
The relationships between bees and ßoral resources in
our sites were highly variable between sites and years.
At the local scale, bee abundance and richness were
more strongly associated with ßower richness than
ßower abundance in 2008. Floral richness has been
experimentally demonstrated to affect bee abundance
(Ebeling et al. 2008) and can be important in struc-
turing pollinator communities in other systems
(Moeller 2005). The lack of relationship between ei-
ther bee abundance or richness and ßower richness in
2009 could be because of unmeasured factors obscur-
ing any potential relationship, or be indicative of the
stochastic nature of ßoral resources. Additionally, the
scale of ßoral sampling may not have been adequate to
accurately depict the availability of ßoral resources for
bees, which are very mobile foragers. More extensive
ßoral sampling from roadside surveys in 2011, includ-
ing yards, gardens, and other green spaces, indicated
that suburban landscapes tended to have more abun-
dant and diverse ßoral resources than forested land-
scapes, which was not evident at local scales within
forest patches (A.C., data not shown). Unfortunately,
roadside surveys did not coincide with bee sampling,
so we were unable to test for relationships between
landscape ßoral resources and local bee abundance
and diversity. One caveat is that the distribution of
nectar and pollen resources may be a better predictor
of bee abundance and richness than ßoral abundance
and richness (Potts et al. 2004). Measuring nectar and
pollen resources was beyond the scope of this re-
search, but given the importance of conserving bee
communities in urban and suburban areas and recent
interest in pollinator-friendly gardens, more studies
are needed that assess community-wide nectar and
pollen resources in suburban versus natural habitats.
The abundance and distribution of nesting re-
sources also play key roles in the distribution of var-
ious nesting bees (Potts et al. 2005). Overall, suburban
areas supported more bees of all nesting categories,
suggesting that such areas either have more nesting
Vol. 43, no. 2
resources or at least a superior combination of ßower
and nesting resources. We observed no bare ground in
our surveys, which was not surprising given that sam-
pling took place under an extensive forest canopy.
Still, a greater abundance of all bees in suburban sites,
including soil-nesting species, indicates that suitable
nest sites may be more abundant in suburban areas,
despite there being more extensive impervious surface
cover in the form of low-intensity development. Win-
free et al. (2007) found a positive association between
wood-nesting species and the extent of forested hab-
itat in the landscape. Contrary to our predictions,
CWD did not differ between forest types even though
wood-nesting bees were more abundant in suburban
forests; however, these made up ⬍5% of the total bees
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sampled.
Studies considering mechanisms driving bee abun-
dance at landscape scales often Þnd that bee abun-
dance and richness are positively associated with the
amount of “natural” habitat in the surrounding land-
scape, which is assumed to reßect higher quality hab-
itat (Hines and Hendrix 2005). In urban areas, green
spaces have been shown to increase bee abundance
and diversity (Tonietto et al. 2011). At the landscape
scale in our study, land cover surrounding our sites did
predict bee abundance and diversity. The proportion
of developed open space was a strong, positive pre-
dictor of both bee abundance and diversity, indicating
that areas dominated by lawns and human structures,
such as single-family housing developments, can har-
bor bees. There were no signiÞcant effects of either
deciduous or evergreen forest on bee abundance, al-
though both represent natural land covers. One ex-
planation for these results is that open space may
reßect the distribution of ßoral and nesting resources
outside of forested patches and serve as important
foraging and nesting areas. For example, bumblebee
abundance in urban parks of San Francisco, CA was
positively associated with the openness of the sur-
rounding urban matrix, suggesting open areas either
have more resources or are more easily navigated by
foraging bees (McFrederick and LeBuhn 2006). Low-
intensity development had a negative effect on abun-
dance and diversity in our study, which was not sur-
prising given that it has up to 50% impervious surface,
and thus may provide low foraging and nesting re-
sources for bees. The differences between bee re-
sponse to developed open space and low-intensity
development suggest that any beneÞts of human de-
velopment decrease with increasing intensity of ur-
banization. In addition, the spatial scale of surveys and
landscape context likely determine the effects of ur-
banization on bee communities (Steffan-Dewenter et
al. 2002). Forested landscapes, such as in this study,
could beneÞt from moderate levels of disturbance
(Winfree et al. 2007), whereas open habitats, such as
deserts (Hostetler and McIntyre 2001, Gotlieb et al.
2011), typically lose bees to disturbance through hab-
itat loss. Historical land use could also be an important
factor effecting contemporary bee communities.
Comparative studies using museum records could pro-
vide context for temporal change in both land use and
April 2014 CARPER ET AL.: EFFECTS OF SUBURBANIZATION ON FOREST BEE COMMUNITIES
bee community composition, but was outside the
scope of this study. Therefore, more detailed knowl-
edge of the endemic bee fauna, historical land use, and
land-use practices is crucial to interpreting the effects
of urban development on bee communities.
In conclusion, this work suggests that moderate
levels of human disturbance, such as suburban devel-
opment, can support abundant and diverse bee com-
munities. With increasing concern over the status of
pollinators and the sustainability of pollination ser-
vices (Kearns et al. 1998), such Þndings underscore
the need to incorporate ecological Þndings in both
urban and conservation planning (Miller and Hobbs
2002). Given the challenges of urban and suburban
areas for bees (Cane 2005), insights from such work
could have broad implications for the conservation of
native pollinators and the sustainability of pollination
services in human-dominated environments. For ex-
ample, planned development in forested areas could
promote abundant and diverse bee communities
through the establishment of ßower-rich open areas in
concordance with the retention of natural forest hab-
itat. Ultimately, comparative studies integrating both
planned development and conservation strategies are
needed to determine how to best manage for and
conserve native pollinators.
Acknowledgments
This research was made possible by cooperation from
landowners, homeownersÕ associations, private citizens, the
North Carolina Division of Parks and Recreation, the Wake
County Department of Parks, Recreation and Open Space,
and North Carolina State University. We thank S. Droege for
assistance in bee identiÞcation; J. Ascher for help with bee
biology and life-history; and D. Bolger, Z. Gezon, R. Schaef-
fer, L. Richardson, and C. Urbanowicz for comments on the
manuscript. Funding was provided by the National Science
Foundation (DEB-0743535) and Dartmouth College (the R.
Melville Cramer Fund and a Rockefeller Center Urban Stud-
ies Research Grant). Any opinions, Þndings, and conclusions
or recommendations expressed in this material are those of
the authors and do not necessarily reßect the views of the
funding sources.
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