Results
Description of
biodiversity
Our final dataset included 26,716 individual bees representing 5 bee
families, 30 genera, and 144 species. See [CITATION FOR DRYAD
SUBMISSION] for the complete dataset and list of species. We collected
33% of the total number of bee species that have been found in
Pennsylvania (Kilpatrick et al., 2020). The species accumulation curve
for these data shows a leveling off pattern but did not reach an
asymptote (Figure 2A). The abundances among species show a typical rank
abundance curve with a small number of very abundant species and many
rare species (Figure 2B). Ten species had over 1,000 individuals while
over half of the species had 5 or fewer individuals. We captured by far
the most individuals and species from the family Apidae (19,870
individuals and 47 species) followed by Halictidae (5,942 and 33),
Andrenidae (477 and 28), Megachilidae (383 and 30), and Colletidae (44
and 6).
Biodiversity changes within years
We found very strong evidence for seasonal changes in all measures of
biodiversity and on average month explained an average of 74% of the
variation in our models (Figure 3, Table 1). Abundance and richness
showed a hump-shaped pattern peaking in July. In our models, month
explained nearly 90% of variation in abundance and richness. The number
of bees captured per site increased by 193% between April and August,
which were the lowest and highest values we observed (Figure 3A).
Similarly, average richness increased by 89% between April and July
(Figure 3B). Diversity also increased and decreased across the seasons,
but less sharply than in richness, and peaked in August instead of July
(Figure 3C). Diversity increased by 41% between May and August and
decreased by 60% from August to October (Figure 3C). Because diversity
incorporates both richness and evenness, the weaker pattern in diversity
compared to richness is a consequence of evenness having a pattern
nearly opposite that seen in richness (P < 0.0001, R2 = 0.68),
highest in spring and fall and lowest in July.
Phylogenetic structure also varied between months. Mean pairwise
distance dropped (becoming more clustered) by 1.9 standard deviations
between May and July and then increased (becoming more even) by 1.1
standard deviations between July and October. The months of April, June,
August, and September had intermediate values (Figure 3D). We observed
limited variation in phylogenetic structure between sites resulting in
our model explaining 87% of the total variation (Table 1). Community
composition varied substantially among months with our multivariate
model explaining 64% of the variation in bee communities (Figure 4A,
Table 1). Spring months (April-June) all had distinct bee communities.
July through September had similar compositions which were themselves
distinct from spring months and October (Figure 4A).
Biodiversity change across
years
We found very strong evidence for biodiversity change over time between
2014 and 2019 with year explaining an average of 42% of variation
across all biodiversity metrics (Figure 3, Table 1). Abundance of bees
captured declined by 48% between 2014 and 2019 (Figure 3E). Richness
declined by 41% between the peak in 2016 and the lowest point in 2019
(Figure 3F). Similar to richness, diversity also declined after 2016,
dropping by 59% between 2016 and 2019 (Figure 3G), though the model for
diversity explained about half as much variation as the model for
richness (Table 1).
Phylogenetic structure increased and decreased over time with the most
clustered communities in 2014 and 2019, and the most even communities in
2016 (Figure 3H). Mean pairwise distance increased (became more even) by
1.8 standard deviations between 2014 and 2016, and then decreased
(becoming more clustered) by 1.6 standard deviations between 2016 and
2019. Bee communities were quite stable across the first three years
though they shifted slightly over time in the last three years (Figure
4B). Year explained about 36% of the variation in community
composition.
Species patterns in seasonality, phenological breadth, and
change over
time
Looking across the 40 species for which we collected 30 or more
individuals (Table A1), bee families varied significantly in seasonality
(Figure 5, Figure 6, F3,36 = 10.91, P <
0.001). Species in the families Megachilidae and Andrenidae were
collected an average of 54 days earlier than species in the families
Apidae and Halictidae (Tukey tests, P < 0.006). In the family
Megachilidae, Osmia species and Hoplitis pilosifrons were
among the earliest emerging species, but Megachile mendica was
most active in July and August (Figure 5). In the Andrenidae, allAndrena species are most active in April and May, butCalliopsis andreniformis was most abundant in July. Among species
in the family Apidae, Eucera hamata was the only species with
peak abundance in May. Species in the genera Anthophora,
Ceratina, and Bombus were most active in June, though there is
some variation among species within those genera. Other species in the
family Apidae, including Ptilothrix , Melitoma, andMelissodes, as well as Eucera (Peponapis )pruinosa, peaked in July and August (Figure 5). Most species in
the family Halictidae were most abundant in July and August, though twoAgapostemon species were active earlier (Figure 5, Figure 6).
Phenological breadth varied among families (Figure 5, Figure 6,
F3,36 = 3.896 , P = 0.02) with two families that were
significantly different. Species in the family Andrenidae had the
narrowest breadth at 35 days on average, and species in the Halictidae
were active the longest at 89 days on average (Tukey test, P = 0.02).
The families Megachilidae (49 days) and Apidae (66 days) showed
intermediate breadth. In the Andrenidae, all Andrena species had
a breadth of less than 42 days, but Calliopsis andreniformis had
a breadth of 79 days. In the Megachilidae, Osmia species’
breadths range from 21 to 58 days while Megachile mendica had a
breadth of 71 days. Species in the Halictidae consistently had a wide
phenological breadth, greater than 75 days, though Halictus
ligatus had a relatively narrow window of 55 days. We split species in
the Apidae into two groups, each consisting of related clades, that
varied significantly in phenological breadth (t-test, t = -3.7, df =
18.3, P = 0.002). Species in the genera Bombus, Apis, Ceratina,and Xylocopa had an average breadth of 85 days, while species in
the genera Eucera, Mellisodes, Ptilothrix, Melitoma, andAnthophora had an average breadth of 44 days (Figure 5, Figure
6).
We observed substantial species-level variation in the changes in
abundance across years (Figure 5, Table A1). We detected no little-to no
change in abundance for 26 species (P>0.1), 8 species
showed moderate to strong evidence for decline (P<0.05), 5
more showed weak evidence for decline (P<0.1), and we found
strong evidence for increase in 1 species (P<0.01). While bee
family was not a significant predictor of changes in abundance
(F3,36 = 1.813, P = 0.16), we observed some patterns
among families and genera. Species in the families Megachilidae and
Andrenidae were all stable. Other families showed mixed trends. For
example, among species in the family Apidae, all carpenter bee species
in the genera Xylocopa and Ceratina were stable except forCeratina mikmaqi which declined by 1 standard deviation unit (SD)
between 2014 and 2019. Six out of eight species in the Halictidae showed
evidence for declines, most species by about 1 SD, but Agapostemon
virescens declined by 1.7 SD. Four species in the genus Bombusshowed pronounced declines ranging between 1.2 and 1.8 SD while twoBombus species were stable. Similarly, Melitoma taureadeclined by 1.3 SD. We saw radical variation among species in tribe
Eucerini (Apidae): some species stable over time (Eucera and someMelissodes ), Melissodes desponsa had the biggest decline
we observed (1.8 SD), and Melissodes bimaculatus increased by 2.2
SD, which was the only significant increase and also the largest
magnitude of change we found.