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Characterizing the Floral Resources of a North American Metropolis Using METHODS, TOOLS, AND TECHNOLOGIES Characterizing the floral resources of a North American metropolis using a honey bee foraging assay 1, 2 3 1 DOUGLAS B. SPONSLER, DON SHUMP, RODNEY T. RICHARDSON, AND CHRISTINA M. GROZINGER 1Department of Entomology, Huck Institutes of the Life Sciences, Center for Pollinator Research,Pennsylvania State University, University Park, Pennsylvania 16802 USA 2Philadelphia Bee Company, Philadelphia, Pennsylvania 19125 USA 3Department of Biology, York University, Toronto, Ontario M3J 1P3 Canada Citation: Sponsler, D. B., D. Shump, R. T. Richardson, and C. M. Grozinger. 2020. Characterizing the floral resources of a North American metropolis using a honey bee foraging assay. Ecosphere 11(4):e03102. 10.1002/ecs2.3102 Abstract. Roughly a third of described insect species visit flowers, making the flower–insect interface one of the chief pillars of global biodiversity. Studying flower–insect relationships at the scale of communi- ties and landscapes has been hindered, however, by the methodological challenges of quantifying land- scape-scale floral resources. This challenge is especially acute in urban landscapes, where traditional floral surveying techniques are ill-suited to the unique constraints of built environments. To surmount these chal- lenges, we devised a “honey bee foraging assay” approach to floral resource surveying, wherein continu- ous colony weight tracking and DNA metabarcoding of pollen samples are used to capture both the overall availability and taxonomic composition of floral resources. We deploy this methodology in the complex urban ecosystem of Philadelphia, Pennsylvania, USA. Our results reveal distinct seasonality of flo- ral resource availability, with pulses of high availability in May, June, and September, and a period of pro- longed scarcity in August. Pollen genus richness mirrored this pattern, with peak richness in May and June. The taxonomic composition of pollen samples varied seasonally, reflecting underlying floral phenol- ogy, with especially strong turnover between May and June samples and between August and September samples delineating well-defined spring, summer, and fall floral resource communities. Trait analysis also revealed seasonal structure, with spring samples characterized by trees and shrubs, summer samples including a stronger presence of herbaceous “weeds”, and fall samples dominated by woody vines. Native flora predominated in spring, giving way to a preponderance of exotic flora in summer and fall. At a basic level, this yields insight into the assembly of novel urban floral resource communities, showcasing, for example, the emergence of a woody vine-dominated fall flora. At an applied level, our data can inform urban land management, such as the design of ecologically functional ornamental plantings, while also providing practical guidance to beekeepers seeking to adapt their management activities to floral resource seasonality. Methodologically, our study demonstrates the potential of the honey bee foraging assay as a powerful technique for landscape-scale floral resource surveying, provided the inherent biases of honey bee foraging are accounted for in the interpretation of the results. Key words: biodiversity; hive scale; Internal transcribed spacer; metabarcoding; pollination; trnL; urban ecology. Received 13 November 2019; revised 23 January 2020; accepted 29 January 2020. Corresponding Editor: Mary L. Cade- nasso. Copyright: © 2020 The Authors. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. E-mail: [email protected] ❖ www.esajournals.org 1 April 2020 ❖ Volume 11(4) ❖ Article e03102 METHODS, TOOLS, AND TECHNOLOGIES SPONSLER ET AL. INTRODUCTION morphology (excluding, for example, flowers requiring sonication to release pollen from It has been estimated that roughly a third of all anthers). described insect species are either directly or Here, we present a two-year study of the floral indirectly dependent on flowers for food (Ward- resource composition and dynamics of Philadel- haugh 2015). This ecological centrality of flow- phia, Pennsylvania, USA. Founded in 1682, the ers-as-food extends to systems in which historic city of Philadelphia straddles the interface of the floral communities have been dramatically Appalachian Piedmont and Atlantic Coastal altered, such as urban landscapes characterized Plain physiographic provinces (Fenneman and by novel assemblies of native and exotic flora Johnson 1946) and hosts over 2500 plant species (Aronson 2014). Urban landscapes can host (Clemants and Moore 2003). Its patchwork diverse communities of flowers and flower visi- heterogeneity of sociological composition is both tors, sometimes even functioning as refugia for a product and driver of concomitant ecological rare species (Baldock 2015) [though see (Geslin variation in abiotic substrate and biotic commu- et al. 2013)], but little is known about the overall nities, earning Philadelphia the apt moniker composition of urban floral resources and how “City of Neighborhoods”. To characterize the flo- they fluctuate phenologically through the grow- ral resources of this complex urban environment, ing season. we employ a “honey bee foraging assay” using a Studying floral resources at the landscape scale network of sentinel apiaries distributed through- is technically daunting in any context (Frankl out the city. Combining DNA metabarcoding of et al. 2005), but the challenge becomes especially pollen samples with continuous colony weight acute in urban landscapes where extreme land- monitoring, we characterize both the taxonomic scape heterogeneity, limited land access, and the composition and overall availability of floral physical obstacles of the built environment render resources in our study system, together with traditional approaches to floral surveying imprac- their temporal dynamics throughout the foraging ticable. Flower-visiting insects might be har- season. We conclude by comparing Philadel- nessed as efficient environmental samplers of phia’s floral resource landscape with patterns landscape-scale floral resources, provided the described in other study systems and discussing spatial and taxonomic scope of their interaction the implications of our data for understanding with the landscape is sufficiently understood and the ecological function of urban flora. the materials they collect can be analyzed infor- matively (Wood et al. 2018). While not an unbi- METHODS ased representation of local flora, such an approach would manifestly be relevant to the Sites and study years question of trophic function at the flower–insect We conducted fieldwork in 2017 and 2018. Our interface. study sites included 13 apiaries in Philadelphia, The western honey bee (Apis mellifera L.) is Pennsylvania, USA, owned and managed by the arguably the organism best suited for such a Philadelphia Bee Company (Fig. 1). Twelve api- sampling approach. As an extreme generalist, aries were used in each study year, with 11 honey bees have a diet breadth that overlaps shared across years, 1 used only in 2017 (RB), considerably with that of many other nectar- and and 1 used only in 2018 (NE). Each of our pollen-feeding insects (Butz Huryn 1997). A research apiaries included three honey bee colo- honey bee colony surveys the landscape around nies designated as research colonies for our its nest at a range routinely extending several study, resulting in a total of 36 research colonies kilometers, dynamically allocating foraging across 12 sites in each year. Some sites also effort to the most rewarding patches (Visscher included additional colonies not involved in our and Seeley 1982). Thus, the materials it collects study. Research colonies were initiated in April– are informatively biased toward the richest May of each study year from 4- or 5-frame resources within the colony’s foraging range and nucleus colonies installed in 10-frame Langstroth compatible with honey bee behavior and hives. Nucleus colonies were purchased together ❖ www.esajournals.org 2 April 2020 ❖ Volume 11(4) ❖ Article e03102 METHODS, TOOLS, AND TECHNOLOGIES SPONSLER ET AL. Fig. 1. Apiary locations (circles) plotted over land cover raster. The City of Philadelphia is demarcated by a dashed black line. Land cover data are from the Chesapeake Conservancy’s Land Cover Data Project (Chesa- peake Bay Conservancy 2017); only major cover types are shown in legend. Area east of the Delaware River in the State of New Jersey is not shown because it fell outside the scope of the land cover dataset. each year from a single supplier (Swarmbustin’ spikes (i.e., additive outliers), and persistent Honey, West Grove, Pennsylvania, USA). During weight shifts (i.e., level-shift outliers) caused by colony installation, each research hive was colony manipulations involving the addition or equipped with a Sundance I bottom-mounted removal of material from the hive. Because our pollen trap (Ross Rounds, Canandaigua, New colonies were part of a working apicultural busi- York, USA) and a Broodminder hive scale ness, it was not possible to avoid or standardize (Broodminder, Stoughton, Wisconsin, USA). these management artifacts. To address both types of artifacts, we first took Weight monitoring and pattern characterization the first-order difference of each colony weight We set our Broodminder hive scales to record time series, which turns level-shift outliers into hourly weights, beginning at colony installation additive
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