Discussion
Our study is the first to demonstrate that bees occupy the aerosphere
immediately above the forest canopy; furthermore, the community above
the canopy was compositionally distinct with similar abundances compared
to lower strata (understory, midstory, canopy). These findings expand
our understanding of forest bee communities and build on earlier
research that revealed differences between understory and canopy bees
(Cunningham-Minnick & Crist, 2020; Milam et al., 2022; Ulyshen et al.,
2010; Urban-Mead et al., 2021). However, when attempting to characterize
the forest bee community, the importance of sampling the
canopy-aerosphere interface hinges upon the question of whether these
bees should be considered as part of the forest community, or if they
are transients moving among resources. The fact that the above-canopy
assemblage was generally characterized by many species that were not
observed at lower strata and were also associated with non-forested
habitats (e.g., Agapostemon texanus Cresson,Halictus parallelus Say, Peponapis pruinosa(Say); Harrison et al., 2018) suggests that while some bees may forage
on floral resources available at tree crowns in the spring, many others
may be moving over the forest to access other habitat patches or
resources throughout the season, as reported in other insect taxa
(Wainwright et al., 2017). Nevertheless, the presence of an abundant and
species rich bee assemblage at the canopy-aerosphere interface, which
had not previously been considered, suggests that more studies are
needed to address the extent to which these bees should be considered a
subset of the forest bee community.
This study also demonstrated how the vertical stratification of forest
bee communities changed throughout the flight season. Our observations
confirm the findings of previous studies that have documented a positive
relationship between day of year and bee abundance in the canopy (i.e.,
Cunningham-Minnick & Crist, 2020; Ulyshen et al., 2010; Urban-Mead et
al., 2021). However, while this pattern may reflect a response to the
depletion of floral resource availability near the ground in temperate
forests (Proesman et al., 2019; Ulyshen et al., 2010), it remains
unclear why bees moved to the canopy. It is possible that the canopy
provides alternative foraging resources (Campbell et al., 2018; Ulyshen
et al., 2010), nesting opportunities (Cunningham-Minnick & Crist,
2020), or favorable conditions associated with tree leaf phenology
(Urban-Mead et al., 2021). Our results add a layer of complexity to the
issue by demonstrating that this temporal pattern extends vertically
beyond the forest canopy and involves a compositionally distinct subset
of the bee community that may be responding to a mix of environmental
cues. For example, the highest bee abundance across sampling points in
the spring was at the canopy-aerosphere interface during the peak bloom
of A. rubrum , suggesting that this stratum may provide access to
floral resources of the forest canopy. However, it seems unlikely that
summer bees above the canopy were foraging or nesting since forest
floral resources were depleted and most were soil-nesting species.
Vegetation height has been negatively associated with bee abundance and
diversity (Roberts et al., 2017); therefore, bees may instead use the
canopy-aerosphere interface for movement or dispersal since this space
lacks the obstacles created by the vegetation structure of forest
interiors. Alternatively, bees may be physiologically driven to take
advantage of the greater light intensities and warmer temperatures above
the canopy compared to other strata to forage earlier or later in the
day (Fig. A5; Kebler et al., 2019; Roubik, 1993). It is also possible
that some species were seeking mates above the canopy. For instance,
groups of male Apis mellifera L. mate with females 10 – 40 m
above the ground (Ruttner, 1966); similarly, male groups of someBombus species will fly to higher elevations to mate with
emerging females, a behavior known as ‘hill-topping’ (Goulson et al.,
2011). Though A. mellifera and Bombus spp. comprised 56%
of the overall abundance of bees above the canopy, these behaviors are
unlikely to explain our findings because only three individuals of these
species were males. Alternatively, males of two solitary soil-nesting
species, Andrena imitatrix Cresson and A. mandibularisRobertson, comprised 57% of bee abundance above the canopy in
the spring, though we are not aware of any studies addressing
hill-topping behavior in these species or the Andrena genus.
Thus, it appears that many of the species above the canopy were flying
over the forest to unknown ends.
There were notable differences in bee assemblages among the other strata
that may be best explained through life-history traits. For instance,
bees in our study that nest in moist, decayed wood (e.g.,Augochlora pura (Say), Lasioglossum coeruleum(Robertson), L. cressoni (Robertson), L. subviridatum(Cockerell)) or pithy twigs (e.g., Hylaeus spp., Ceratinaspp.) were nearly absent above the canopy (< 1%), while 77%
were found in the canopy and midstory, and only 22% of bees from this
guild were sampled from the understory. Our findings are consistent with
other studies that demonstrated a high abundance of wood-nesting bees
within the canopy (e.g., Urban-Mead et al., 2021; Cunningham-Minnick &
Crist, 2020; Campbell et al., 2018; Ulyshen et al., 2010) and suggest
that bees that nest in wood, including species that nest in moist
decayed wood, or ‘soft’ wood, exhibit a preference for canopy strata
within forests likely due to the availability of wood nesting
substrates. Nesting substrate in the canopy has yet to be tested as a
mechanism in explaining high abundances of wood-nesting bees within the
higher strata of forests due to the known availability of dead and
rotting wood on the forest floor, despite a lack of correlation between
coarse woody debris on the ground and the abundance of this guild in the
canopy (Urban-Mead, 2021; Campbell et al., 2018; Ulyshen et al., 2010).
Therefore, studies that quantify potential nesting substrates for
wood-nesting bees within the canopy, including those that nest in ‘soft’
wood, are clearly needed to resolve these discrepancies (Harmon-Threatt,
2020).
Milam et al. (2022) found that the inclusion of canopy sampling in
addition to understory sampling did not influence their ability to
characterize the forest bee community. Our study supports their
conclusion when only considering bees below the maximum height of the
canopy (i.e., understory, midstory, and canopy strata), but further
demonstrates that the bee community above the canopy is distinct from
lower strata. The existence of bees above the forest canopy is highly
relevant to understanding pollinator ecology and may have additional
implications for their conservation vis a vis our understanding of the
effects of habitat fragmentation and isolation on bee movements and
related population processes (Proesman et al., 2019; Roberts et al.,
2017; Winfree et al., 2009). Though our study was limited in sampling
intensity, it clearly demonstrates the complexities of spatiotemporal
bee dynamics within forests, suggests a new perspective on the role of
forests in the surrounding landscape, and emphasizes caution when
drawing conclusions about forest bee communities that were sampled with
vertically or temporally restricted designs. Thus, our study supports
the growing body of literature that asserts the need for additional
baseline research of forest bee communities along the full vertical
gradient to inform forest management and bee conservation.