The effect of floral composition on bees of Meadville, PA

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1 Allegheny College Allegheny College DSpace Repository Projects by Department or Interdivisional Program Academic Year The effect of floral composition on bees of Meadville, PA Hickman, Paige All materials in the Allegheny College DSpace Repository are subject to college policies and Title 17 of the U.S. Code.

2 The effect of floral composition on bees of Meadville, PA y Paige L. Hickman Department of Environmental Science Allegheny College Meadville, Pennsylvania April, 2017

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4 TALE OF CONTENTS Acknowledgements iii Abstract iv Introduction ackground and importance of bees as pollinators Declines in wild bees Angiosperm-bee interactions and pollen specificity \ Materials & Methods ee sampling Floral composition assessment and identification ee processing and identification Data analysis Results ee fauna General relationships between flora and bee fauna Native vs exotic bees Polylectic vs oligolectic bees Oligolege occurrence within range of host plants Tables Figures Discussion Assessment of bee abundance and diversity The effect of floral composition on bee fauna Increasing bee fauna in an urban environment References 28 Appendix A: Sampling site information 32 Appendix : Floral species list 33 Appendix C: Oligolege occurrence and their host plants 38 ii

5 ACKNOWLEDGEMENTS This project would not have been possible without the assistance and support of several people. First, I would like to thank Dr. eth Choate for being my advisor and for providing valuable insight, critiques, and encouragement throughout this project and my time at Allegheny. I would also like to thank her for giving me the wonderful opportunity to participate in the summer research that was used for this project. Many thanks to Erica Moretti ( 17) and Kaye Moyer ( 19) for being such wonderful and supportive research partners. I want to thank Sam Droege of the USGS ee Inventory and Monitoring Lab for assistance in bee species identification and for providing very helpful information and resources. Lastly, I would like to thank my friends and family for keeping me relatively sane in times of stress during the course of this project. Also, special thanks to my squad for always being there for me. iii

6 Name: Paige L. Hickman Date: April, 2017 Major: Environmental Science Thesis Committee: Dr. eth Choate, Dr. Casey radshaw-wilson Title: The effect of floral composition on bees of Meadville, PA ASTRACT The world is currently experiencing a global pollinator decline due to climate change, habitat fragmentation, and pesticide use. The full extent of bee declines is not well-known because many parts of the country lack consistent bee species surveys. The United States alone is home to over 4,000 species of native bees, which are more efficient at pollinating native plants than the European honeybee due to coevolution. ees can be generalists that collect pollen from a wide variety of angiosperms or specialists that obtain pollen from a specific host-plant group. The aim of this study is to assess bee species diversity in northwestern PA and evaluate how floral composition influences bee fauna. Using bee species data from the summers of 2015 and 2016, the relationship between bee diversity and blooming angiosperms present at sites of bee sampling will be evaluated. It is hypothesized that sites with more natural flora will promote more native bee and specialist species in comparison to sites dominated by unnatural ornamental plant varieties. The study resulted in a comprehensive record of bee species present in the area. ee richness and abundance was found to be greater at Robertson sites than downtown. This study also demonstrated that native and specialist bees are more common in areas with predominantly naturally-occurring floral species in comparison to urban areas where floral diversity is restricted and hybridized ornamentals are much more abundant. iv

7 INTRODUCTION ackground and importance of bees as pollinators Approximately 90% of all flowering plant species rely on animal pollination services, including most agricultural crops (Marks, 2005). ees comprise a very abundant and diverse group of animal pollinators; there are over 4,000 species native to the United States and more than 20,000 currently known world-wide (Marks, 2005; Moisset & uchmann, 2010; Wilson & Carril, 2015). New bee species are still being discovered and it is likely that many more remain unknown (Wilson & Carril, 2015). Although most public attention is focused on the European honey bee, Apis mellifera (Linnaeus, 1758) and its decline due to colony collapse disorder, it is not native to the United States. The European honeybee was originally brought over from Europe for its economic value as a transportable pollinator of agricultural fields (Wilson-Rich et al., 2014). Thousands of bee species occur naturally in the environment. Most of these bee species are solitary, in contrast to the social A. mellifera and ombus spp. (Latreille). The vast majority of the bee species in the United States are native and have been pollinating indigenous plants preceding the arrival of the honey bee, often more efficiently due to adaptations specific to certain flower structures (Moisset & uchmann, 2010). Additionally, there are wild bees that are not native but have become established in the United States (Cane, 2003). Pollination is not the goal of bees but an incidental occurrence when females collect pollen as an essential protein source for egg-production and their larvae (Michener, 2007; Potts et al., 2003; Minckley & Roulston, 2006). ee species vary greatly in size and morphology, which affects their ability to access floral resources and thereby pollinate plants (Wilson & Carril, 2015). Native bees are known to be more efficient at pollinating native plants than exotic bees as a result of coevolution (Moisset & uchmann, 2010). The bee s access to pollen may be hindered if plants are unnatural ornamentals with a modified flower structure (Wilson & Carril, 2015). Ultimately, floral species composition is a major factor in the preservation of bee diversity because the flowers present determine what bee species can thrive in the environment. Declines in wild bees The world is currently experiencing a global pollinator decline (Ingram et al., 2002). Native bees are at risk due to climate change, pesticide use, and habitat fragmentation due to urbanization and agricultural intensification (Marks, 2005; Wilson-Rich et al., 2014). Climate change may cause early emergence of bees due to warmer temperatures and irregular weather If the flowers they rely on for nectar and pollen are not yet in bloom, bee populations may be 1

8 negatively impacted (Wilson-Rich et al., 2014). Pesticide use may kill bees directly along with pest insects or indirectly by eliminating flowering plants that provide their nectar and pollen supplies (Ingram et al., 2002; Marks, 2005; Wilson-Rich et al., 2014). Habitat fragmentation alters the landscape, thus destroying nesting sites and decreasing sufficient availability of flowering plants within foraging range (Wilson-Rich et al., 2014; Wilson & Carril, 2015). Human manipulation of the environment ultimately impacts floral diversity, an essential factor for the diversity of wild bees (Wilson & Carril, 2015). The extent of wild bee species loss is largely unknown because populations have not been consistently surveyed in many parts of the world (Wilson & Carril, 2015). The Xerces Society has published a Red List including over fifty native species known to be vulnerable, imperiled, or possibly extinct ( It is estimated that the number of imperiled and possibly extinct bee species is actually much higher than is currently realized due to the lack of species surveys (Wilson & Carril, 2015). It is critical that researchers continue to study native bee populations to obtain a better understanding of wild bee biodiversity decline and methods of mitigation. Angiosperm-bee interactions and pollen specificity ees evolved from wasps in the Cretaceous Period (Moisset & uchmann, 2010; Wilson-Rich et al., 2014). Paleontological evidence shows that during this time they adapted to feed and gather resources from plants, which spurred the co-evolution between species of bees and angiosperms by the Middle Eocene (Crepet, 1984; Wilson-Rich et al., 2014). Historical observations suggest that flower selection is not random and bees develop a search image, thus causing them to visit the same species of flower (Christy, 1883; Heinrich, 1975). Plants develop a pollination syndrome, which encompasses floral attributes adapted to attract a certain pollinator (Waser et al., 1996; Fenster et al., 2004). Groups of pollinators specific to a certain plant may include one or more species that do not necessarily have to share close taxonomic relationships, although they likely share similar traits that allow them to access the pollen more easily (Fenster et al., 2004). Pollen specificity of a bee species increases the likelihood of flower fidelity or constancy, which helps to ensure that proper pollination occurs as a bee visits the same species (Linsley & MacSwain, 1958; Heinrich, 1975; Cane & Sipes, 2006). True specialization is predetermined and the bee remains faithful to the same species or related species of angiosperm during each foraging trip (Cane & Sipes, 2006). This phenomenon is dependent upon blooming period 2

9 coinciding with a bee s flight time, and also the correspondence of flower structure and bee morphology (Linsley & MacSwain, 1958). The principal groupings of pollen specificity for bees are oligolectic and polylectic (Michener, 2007). Robertson (1925) defines oligolectic as having preference for pollen from a host-plant group usually consisting of angiosperms of the same species, genus, or family. He defines polylectic being generalized in pollen collection and ability to access pollen from a wide range of flowering plants not necessarily related (Robertson, 1925). Oligoleges only resort to other sources of pollen in the absence or scarcity of their preferred flowers, although in some cases this does not happen and may result in a local loss of the bee species (Linsley & MacSwain, 1958). There are varying degrees of oligolecty that indicate specialization being more or less strict (Michener, 2007; Cane & Sipes, 2006). Throughout this study, pollen specialist bees will be referred to under the umbrella term oligolectic. Oligolectic specialization is essential to certain plants that rely on only one type of pollinator and may have flower structures too complex for most species of bees to access (Minckley & Roulston, 2006). If the specializing bee species were to become imperiled or extinct, the angiosperm would likely suffer (Waser et al., 1996; Wilson-Rich et al., 2014). In essence, maintaining biodiversity of wild bees is vital to preserving biodiversity of angiosperms due to the plant-pollinator relationships they share. The objectives of this study were to assess abundance and diversity of bees in Meadville, PA and to investigate the effect of floral composition on local bee fauna. Ultimately, the study seeks to gain a better understanding of how bee species diversity is influenced by the flora of the immediate environment and make recommendations for increasing diversity in urban environments. MATERIALS & METHODS ee sampling ee sampling was conducted over a two-year period ( ) at 17 sites spaced 200 m apart throughout Meadville of Crawford County, PA (Fig.1). Sites were sampled monthly June 2015 through August 2015 and May 2016 through September 2016 (see Appendix A for specific sampling dates and site descriptions). Dates were selected to coincide with bee emergence and flight time (Potts et al., 2003; Wilson & Carril, 2015; Wilson-Rich et al., 2014). Sites included locations at Allegheny College s Robertson fields and athletic complex, backyards of privately owned houses above Allegheny College campus, Allegheny College campus, and in downtown Meadville, essentially creating a rural to urban gradient (Fig.1). The 3

10 MH site location changed slightly beginning with the July 2016 sample, however it was only moved approximately 15 m and this had little impact on angiosperm composition. Sampling occurred on days when there was no precipitation. Figure 1. Map of the 17 site locations within Meadville, PA ( N, W). Sites range from Allegheny College Robertson Fields and Athletic Complex ( R1, R2, R3, R4 ) to backyards of privately owned houses ( KM, EP, C, RO ) to Allegheny College campus ( C1, C2, C3, C4 ) to downtown sites ( OC, IC, Lib, UU, MH ). Exact locations with GPS coordinates and site details can be found in Appendix A. Scale in kilometers. Trapping was entirely passive and included one vane trap and four bee bowls per site. The vane trap (OakStump Farms blue vane trap, SpringStar Inc., Woodinville, WA) was placed on a garden hook 1.2 m in height at the center of the site and ¼ of the trap was filled with 70% EtOH. The bee bowls consisted of two white bee bowls and two yellow bee bowls (Leong & Thorp, 1999; Roulston et al., 2007; Westphal et al., 2008). Translucent soufflé cups (SOLO Cup Company, Lake Forest, IL, 3.25-oz) were painted with acrylic paint (Sargent Art Inc., Hazleton, PA) and sealed with a coat of clear acrylic sealer (Mod Podge, Plaid Enterprises Inc., Norcross, GA). owl traps were placed on the ground or at bloom height attached to wooden stakes by use of a staple gun (Cane et al., 2000; Roulston et al., 2007). ee bowls were filled ¾ with water mixed with a drop of dishwashing liquid (Dawn Ultra original scent, Procter & Gamble Company, Cincinnati, OH) as a surfactant. Dishwashing liquid with prevalent scents was avoided to prevent sampling bias (Stephen & Rao, 2005). Placement of the bee bowls was kept within the 5-m radius from the vane trap at the center of the site and within close proximity to angiosperms in bloom when possible. All traps remained in the field 48 4

11 hours each month and were checked 24 hours after placement outside to ensure they had not been disturbed. Floral composition assessment and identification During each sample, angiosperms currently in bloom were identified to species at each site within a 5-m radius of the vane trap using the Peterson Field Guide to Wild Flowers of Northeastern/North-central North America (Peterson & McKenny, 1968). The count of open blooms for each species was estimated for those with over 100 blooms. Flower species were identified, either in the field or based on samples taken. Recorded angiosperms were later categorized as being native, alien, or unnatural based on Peterson & McKenny (1968) and the USDA Plants Database ( Native and established alien species are considered naturally occurring in that they can exist in nature without anthropogenic involvement. Unnatural species refer to those planted or spread anthropogenically that otherwise would not be present in the environment; such species include ornamental hybrid plant varieties and garden herb cultivars. A full list of angiosperms identified with both scientific and common names, categorization, and bloom count can be found in Appendix. ee processing and identification Once collected, bees were washed, dried, and pinned. Any hymenopterans 2 mm or less in length were disregarded because this length is less than that of known bee species. The key to families of Apoidea of the U.S. and Canada from American insects: a handbook of the insects of America north of Mexico (Arnett, 2000) was utilized to first identify bees to family. The Discover Life bee genera key ( was used to then take bee identifications to the genus level. ees from the months of May and June 2016 were identified to species by Sam Droege, MA (S. Droege, personal communication, July 2016). The Discover Life bee species keys for each genus ( was used to identify the remainder of the bees to species. All bees were then taken to Sam Droege, MA (S. Droege, personal communication, November 2016) for verification of those identified and for identification of those unable to be identified. Data analysis ee fauna ee fauna was assessed by abundance and species richness. Abundance is total count of individual bees of all species. Species richness is the count of different species represented. 5

12 ee species were also classified as native or exotic and polylectic or oligolectic. Percentages of individuals and species by bee family and ecological grouping were calculated. ee abundance analyses include individuals of unknown identification for total bee abundance, however unknown individuals were excluded from analyses of abundance by ecological grouping. ecause females of Hylaeus modestus (Say, 1837) and Hylaeus affinis (Smith, 1853) cannot be distinguished from one another, they have been grouped as Hylaeus affinis/modestus. For bee species richness analyses, H. affinis/modestus and H. modestus were considered to be one species. ee species richness only includes bees of known species. Qualitative analysis for oligolectic bees was performed to determine whether floral species of their host-plant group were present at their respective sites when these bee species were found. ee fauna at each site type was assessed by means of overall bee abundance and richness for each of the four site types. One-way ANOVA was conducted for each analysis to compare variation in the bee fauna as affected by site type (JMP , SAS Institute Inc.). Tukey s Honest Significant Difference (HSD) was then used to compare the means of bee abundance and diversity for the site types. General relationships between flora and bee fauna General relationships among flora and bee fauna were evaluated by linear regressions using floral species richness, the count of different plant species identified within the 5-m radius at a site during the sample date. Unknown plant species were not included in analyses using floral species richness or bloom abundance. Linear regressions were performed for both bee species richness and bee abundance as a function of floral species richness for both sampling years and then also for individual sampling years. A linear regression was also performed to investigate a relationship between 2016 bee fauna and 2015 flora. Strength of a linear correlation was accessed by r 2 values. Open bloom abundance, the total of all estimated bloom counts for floral species present in the 5-m radius at each site for each sampling date, was grouped into three categories: <100 (little to no blooms), 100 to 1000 (average amount of blooms), and >1000 (plentiful blooms). Mean bee abundance and mean bee species richness were calculated for each bloom grouping. One-way ANOVA was conducted to compare variation in both bee abundance and bee species richness as affected by grouped bloom abundance (JMP , SAS Institute Inc.). Tukey s HSD was conducted, post hoc, to compare means of bee abundance and richness for grouped bloom abundances. 6

13 Native vs exotic bees Native and exotic bee fauna at each site type were assessed by means of bee abundance and richness for each of the four site types. One-way ANOVA was conducted for each analysis to compare variation in the native and exotic bee richness and abundance as affected by site type. Tukey s HSD was then used to compare the means for the site types. Percentages of distinct native and exotic bee species collected across all sampling dates were calculated for each site type. The effect of floral composition on native and exotic bee fauna was evaluated by categorizing sites as being predominantly natural, predominantly unnatural, or having no blooms. Predominantly natural indicates that the percentage of naturally-occurring native and alien angiosperm species was greater than that of the unnatural angiosperm species. Conversely, if the percentage of unnatural angiosperm species was greater, the site was categorized as predominantly unnatural. Sites categorized as no blooms had no angiosperm species in bloom within the 5-m radius assessed. Specific sites included in the floral site categories vary depending on sampling date as floral composition of sites changed throughout the two-year sampling period. ee fauna in relation to floral composition was then analyzed using means of bee abundance and richness for the sites. Means of bee abundance and richness for floral site groupings were calculated for native bees and exotic bees. One-way ANOVA was performed to compare variation in the bee fauna as affected by floral site category. Post hoc, Tukey s HSD was conducted to compare bee abundance and richness means for the floral site groupings. Polylectic vs oligolectic bees Polylectic and oligolectic bee fauna at each site type were assessed by means of bee abundance and richness for each of the four site types. One-way ANOVA was conducted for each analysis to compare variation in the polylectic and oligolectic bee richness and abundance as affected by site type. Tukey s HSD was then used to compare the means for the site types. Percentages of distinct polylectic and oligolectic bee species collected across all sampling dates were calculated for each site type. 7

14 RESULTS ee fauna Over two sampling seasons, 1603 bees were collected including representatives of 5 families, 24 genera, and 106 distinct species. The most frequently collected species throughout all sample dates were of the genus Lasioglossum (Curtis), primarily consisting of pollen generalists (Table 1). Lasioglossum ephialtum (Gibbs, 2010), a polylectic native species was the most abundant species representing 18% of all individuals (Table 1). The majority of bees were polylectic pollen generalists, while oligolectic pollen specialists comprised a small percentage (Table 2). The majority of the bees collected were native with 11% of species and 15% of individuals being exotic (Table 2). The most common exotic bee species were Lasioglossum zonulum (Smith, 1848, Apis mellifera, and Hylaeus hyalinatus (Smith, 1842) (Table 1). Chelostoma rapunculi (Lepeletier, 1841), was the only species both exotic and oligolectic (Table 1). The most abundant oligolege was the species Peponapis pruinosa (Say, 1837), a pollen specialist for the plant genus Cucurbita (Table 3; Table 1). Three out of the ten oligolectic species specialize on the Asteraceae family (Table 3). Yellow bee bowls collected the greatest percentage of bees and most of the bees caught in these traps belonged to Halictidae. The vane traps primarily caught larger species of bees like those of the genus ombus. The collection of Chelostoma rapunculi and Hylaeus pictipes (Nylander, 1852) were state records as these species had never been recorded in Pennsylvania prior to this study. Chelostoma rapunculi was collected at sites on Allegheny College campus in June of 2015 and Hylaeus pictipes was collected at various sites in July and August of Additionally, an undescribed species of the genus Lasioglossum was found at site R3 in May Records and the undescribed species were confirmed by Sam Droege, MA and Jason Gibbs, PhD (S. Droege & J. Gibbs, personal communication, November 2016). The undescribed species cannot be described until more specimens are collected. Overall mean bee abundance was greatest at Robertson and varied significantly based on a one-way ANOVA, although Tukey s HSD was not significant because it is more conservative, controlling for the overall alpha level (Fig.2A: F = 2.90, df = 3, P = 0.037). Overall mean bee richness by site type was significantly greater at Robertson (Fig.2: F = 5.38, df = 3, P = 0.002). General relationships between flora and bee fauna Total bee species richness as a function of floral species richness (Fig. 3A, R 2 = 0.031) and total bee abundance as a function of floral species richness (Fig. 3, R 2 = 0.020) were not 8

15 strong linear relationships, but they were positive. Overall an increase in bee fauna with increasing floral species richness was seen (Fig. 3). ee abundance and species richness for 2016 as functions of floral species richness of the previous year reveal slightly stronger positive linear relationships (Fig.4A, R 2 = 0.063; Fig.4, R 2 = 0.042). Mean bee abundance did not significantly vary by bloom abundance (Fig.5A: F = 1.73, df = 2, P = 0.181), but showed more bees at sites with more blooms. Mean bee species richness was significantly less for <100 blooms than for 100 to 1000 and >1000 blooms (Fig. 5: F = 5.80, df = 2, P = 0.004). Native vs exotic bees Mean native bee abundance did not vary significantly by site type (Fig.6A: F = 2.25, df = 3, P = 0.086), but mean exotic bee abundance varied significantly. Robertson had significantly greater mean abundance than downtown (Fig.6: F = 3.38, df = 3, P = 0.020). Mean native bee species richness was significantly greater at Robertson compared to campus and downtown (Fig. 7A: F = 4.87, df = 3, P = 0.003). Mean exotic bee species richness was significantly greater at Robertson than downtown sites (Fig.7: F = 3.04, df = 3, P = 0.031). Of all different bee species collected at the site type for all sample dates, Robertson had 8.5% exotic species, while downtown had 13% exotic species (Table 4). Mean native and exotic bee abundance and richness did not vary significantly by based on categorization of sites by floral composition as predominantly natural, predominantly unnatural, and no blooms (Fig.8A: F native = 0.908, df native = 2, P native =.406, F exotic = 1.13, df exotic = 2, P exotic = 0.327; Fig.8: F native = 0.554, df native = 2, P native = 0.576, F exotic = 0.647, df exotic = 2, P exotic = 0.525). ees were collected at sites where there were no recorded blooms within the 5-m radius. The no blooms category had the lowest richness and abundance means for both native and exotic bees. (Fig. 8). Polylectic vs oligolectic bees Mean polylege abundance varied significantly with Robertson having greater numbers than campus (Fig.9A: F = 2.99, df = 3, P = 0.033). Mean oligolege abundances at campus was significantly greater than abundance at downtown sites (Fig.9: F = 2.86, df = 3, P = 0.039). Mean polylectic species richness varied significantly and was greatest Robertson compared to the other site types (Fig.10A: F = 4.94, df = 3, P = 0.003). Mean oligolectic species richness was significantly greater at Robertson than at downtown sites (Fig.10: F = 3.42, df = 3, P = 0.019). Of all different bee species collected at the site type for all sample dates, Robertson had 11% oligolectic species, while downtown had 1.6% oligolectic (Table 5). 9

16 Oligolege occurrence within range of host plants Records of plant species within the 5-m radius assessed at each site rarely included host-plant species of oligoleges collected at those sites. Peponapis pruinosa, the cucurbit specialist was collected at sites without record of its host plant much more frequently than the other oligoleges. Peponapis pruinosa was the most common oligolege collected at campus sites within range of gardens where cucurbits were likely to be found (Fig.8; Appendix C). Oligolectic species such as L. oenotherae more frequently coincides with sites at which its hostplant was recorded. Throughout all sites and sampling dates, there was no record of Campanula, the host-plant genus for the oligolectic C. rapunculi. C. rapunculi represented 0.26% of individuals collected (Table 1). Oligoleges and their respective host plants belonging to the goldenrod genus, the aster genus, and the daisy family were most common at Robertson sites. See Appendix C for records of sites at which oligolege occurrence was coincidental with the presence of their host-plants within the 5-m radius assessed. Tables Table 1. ee species list of all collected and identified in Meadville, PA area during the two-year sampling period with the ecological groupings of native vs exotic and pollen specificity, abundance, and % individuals. Family Species a Native vs Exotic b Pollen Specificity c Abund d % Indiv e (n = 1551) Andrenidae Andrena alleghaniensis (Viereck, 1907) N P Andrena asteris (Robertson, 1891) N O Andrena bisalicis (Viereck, 1908) N O Andrena carlini (Cockerell, 1901) N P Andrena cornelli (Viereck, 1907) N O Andrena crataegi (Robertson, 1893) N P Andrena cressonii (Robertson, 1891) N P Andrena illini (ouseman and Laerge, 1979) N P Andrena imitatrix (Cresson, 1872)/morrisonella (Viereck, 1917) N P Andrena miserabilis (Cresson, 1872) N P Andrena nasonii (Robertson, 1895) N P Andrena perplexa (Smith, 1853) N P Andrena placata (Mitchell, 1960) N O Andrena rugosa (Robertson, 1891) N P Andrena tridens (Robertson, 1902) N P Andrena vicina (Smith, 1853) N P Calliopsis andreniformis (Smith, 1853) N P Apidae Anthophora terminalis (Cresson, 1869) N P Apis mellifera (Linnaeus, 1758) E P ombus bimaculatus (Cresson, 1863) N P ombus fernaldae (Franklin, 1911) N P ombus impatiens (Cresson, 1863) N P ombus perplexus (Cresson, 1863) N P ombus vagans (Smith 1854) N P Ceratina calcarata (Robertson, 1900) N P

17 Ceratina dupla (Say, 1837) N P Ceratina mikmaqi (Rehan and Sheffield, 2011) N P Ceratina strenua (Smith, 1879) N P Melissodes bimaculatus (Lepeletier, 1825) N P Melissodes denticulatus (Smith, 1854) N O Melissodes desponsus (Smith, 1854) N O Melissodes illatus (Lovell and Cockerell, 1906) N O Nomada articulata (Smith, 1854) N P Nomada (Scopoli) bidentate grp. N P Nomada cressonii (Robertson, 1893) N P Nomada denticulata (Robertson, 1902) N P Nomada imbricata (Smith, 1854) N P Nomada maculata (Cresson, 1863) N P Nomada pygmaea (Cresson, 1863) N P Nomada sayi (Robertson, 1893)/illinoensis (Robertson, 1900) N P Peponapis pruinosa (Say, 1837) N O Xylocopa virginica (Linnaeus, 1771) N P Colletidae Hylaeus affinis (Smith, 1853)/modestus (Say, 1837) N P Hylaeus annulatus (Linnaeus, 1758) N P Hylaeus hyalinatus (Smith, 1842) E P Hylaeus leptocephalus (Morawitz, 1871) E P Hylaeus mesillae (Cockerell, 1896) N P Hylaeus modestus (Say, 1837) N P Hylaeus pictipes (Nylander, 1852) E P Halictidae Agapostemon virescens (Fabricius, 1775) N P Augochlora pura (Say, 1837) N P Augochlorella aurata (Smith, 1853) N P Augochloropsis metallica-fulgida (Fabricius, 1793) N P Halictus confusus (Smith, 1853) N P Halictus ligatus (Say, 1837) N P Halictus rubicundus (Christ, 1791) N P Lasioglossum admirandum (Sandhouse, 1924) N P Lasioglossum bruneri (Crawford, 1902) N P Lasioglossum cinctipes (Provancher, 1888) N P Lasioglossum coeruleum (Robertson, 1893) N P Lasioglossum coriaceum (Smith, 1853) N P Lasioglossum cressonii (Robertson, 1890) N P Lasioglossum ellisiae (Sandhouse, 1924) N P Lasioglossum ephialtum (Gibbs, 2010) N P Lasioglossum gotham (Gibbs, 2011) N P Lasioglossum hitchensi (Gibbs, 2012) N P Lasioglossum illinoense (Robertson, 1892) N P Lasioglossum imitatum (Smith, 1853) N P Lasioglossum leucozonium (Schrank, 1781) E P Lasioglossum lineatulum (Crawford, 1906) N P Lasioglossum michiganense (Mitchell, 1960) N P Lasioglossum nymphaearum (Cockerell, 1916) N P Lasioglossum obscurum (Robertson, 1892) N P Lasioglossum oenotherae (Stevens, 1920) N O Lasioglossum pectorale (Smith, 1853) N P Lasioglossum perpunctatum (Ellis, 1913) N P Lasioglossum pilosum (Smith, 1853) N P Lasioglossum quebecense (Crawford, 1907) N P Lasioglossum smilacinae (Robertson, 1897) N P Lasioglossum subviridatum (Cockerell, 1938) N P Lasioglossum tegulare (Robertson, 1890) N P Lasioglossum trigeminum (Gibbs, 2011) N P Lasioglossum versans (Lovell, 1905) N P Lasioglossum versatum (Robertson, 1902) N P

18 Lasioglossum weemsi (Mitchell, 1960) N P Lasioglossum zephyrum (Smith, 1853) N P Lasioglossum zonulum (Smith, 1848) E P Sphecodes sp. (Latreille) Megachilidae Anthidium manicatum (Linnaeus, 1758) E P Anthidium oblongatum (Illiger, 1806) E P Chelostoma philadelphi (Robertson, 1891) N P Chelostoma rapunculi (Lepeletier, 1841) E O Hoplitis sp. (Klug) Megachile addenda (Cresson, 1878) N P Megachile brevis (Say, 1837) N P Megachile campanulae (Robertson, 1903) N P Megachile centuncularis (Linnaeus, 1758) N P Megachile latimanus (Say, 1823) N P Megachile mendica (Cresson, 1878) N P Megachile montivaga (Cresson, 1878) N P Megachile relativa (Cresson, 1878) N P Megachile rotundata (Fabricius, 1787) E P Megachile texana (Cresson, 1878) N P Osmia bucephala (Cresson, 1864) N P Osmia cornifrons (Radoszkowski, 1887) E P Osmia georgica (Cresson, 1878) N P Osmia pumila (Cresson, 1864) N P Osmia taurus (Smith, 1873) E P Stelis lateralis (Cresson, 1864) N P a Species: Sam Droege, MA of the USGS ee Inventory and Monitoring Lab confirmed species identifications (S. Droege, personal communication, November 2016). H. pictipes is newly introduced to North America and this identification was confirmed by Jason Gibbs, PhD and Sam Droege, MA (S. Droege & J. Gibbs, personal communication, November 2016). b Native vs exotic: Species classified as native (N) or exotic (E) to North America based on Sheffield et al. (2011), Giles & Ascher (2006), and Cane (2003). L. leucozonium and L. zonulum, although previously considered Holarctic, are speculated to be non-native (Giles & Ascher 2006; Sheffield et al. 2011). c Pollen specificity: Species classified as polylectic (P) or oligolectic (O) based on Fowler & Droege (2016). Polylectic assumed if species was not described explicitly as being oligolectic. d Abundance: Total specimens collected for both years across all sites. e % Individuals: percentage of total collection identified the species (n = 1551). Individuals of unknown species within genera of species identified excluded. 12

19 Table 2. Percentages of total individual bees and species richness for family and the ecological groupings (native vs exotic and pollen specificity). Taxonomic/Ecological Grouping Family % Individuals a % Species b Andrenidae Apidae Colletidae Halictidae Megachilidae Native vs Exotic Native Exotic Pollen Specificity Polylectic Oligolectic a % Individuals: n = 1603 for family, individuals of unknown species included. n = 1549 for native vs exotic and pollen specificity, individuals of unknown species excluded. Calculated from total individuals for both years across all sites. b % Species: n = 106, accounting for H. affinis/modestus and H. modestus as one species. Calculated from total species identified for both years across all sites. Table 3. Host plant groups of all oligolectic bee species collected during the two-year sampling period. Total bees collected also included. Oligolectic ee Species Host-Plant Group Host-Plant Group Total ees (scientific name) a (common name) b Collected c Andrena asteris* Solidago L., Goldenrod genus, Symphyotrichum Nees Aster genus 2 Andrena bisalicis Salix L. Willow 1 Andrena cornelli Rhododendron L. Rhododendron/azalea genus 4 Andrena placata* Solidago L., Goldenrod genus, Symphyotrichum Nees Aster genus 1 Melissodes denticulatus Asteraceae Daisy family 5 Melissodes desponsus Asteraceae Daisy family 7 Melissodes illatus Asteraceae Daisy family 1 Peponapis pruinosa Cucurbita L. Cucurbit/squash genus 37 Lasioglossum oenotherae Oenothera L. Evening primrose genus 7 Chelostoma rapunculi Campanula ellflower genus 4 *Note that A. asteris and A. placata have two host-plant groups. a Host plants based on Fowler & Droege (2016). b Common names from USDA Plant Database ( c Total specimens collected for both years across all sites. 13

20 Table 4. Percentages of native bee species and exotic bee species collected at each site type. Site Type Total Species (n) a Native Species b Exotic Species c Robertson 71 92% 8.5% Houses 51 82% 18% Campus 62 84% 16% Downtown 62 87% 13% a Total different species (n) collected at the sites within the site type for both years. b Native species: percentage of native bee species for the total species collected at the site type. c Exotic species: percentage of exotic bee species for the total species collected at the site type. Table 5. Percentages of polylectic and oligolectic bee species collected at each site type. Site Type Total Species (n) a Polylectic Species b Oligolectic Species c Robertson 71 89% 11% Houses 51 94% 5.9% Campus 62 90% 9.7% Downtown 62 98% 1.6% a Total different species (n) collected at the sites within the site type for both years. b Polylectic species: percentage of polylectic bee species for total species collected at the site type. c Oligolectic species: percentage of oligolectic bee species for the total species collected at the site type. 14

21 Mean bee abundance Mean bee species richness Figures Figure 2. (A-) Overall bee abundance and richness means for the four site types. A P = 0.037* 10 8 A P = R H C D 0 R H C D Site type Site type Site types: Robertson (R), Houses (H), Campus (C), Downtown (D). [5A] Mean bee abundance for each site type, bee abundance includes individuals of unknown species. [5] Mean bee richness for each site type, bee species richness excludes bees of unknown species. Means calculated with bee abundances and bee richness recorded for both years across all sites. *One-way ANOVA revealed a significant difference, but Tukey's HSD was not significant. 15

22 ee abundance ee species richness Figure 3. (A-) Linear regressions evaluating general trends between bee fauna and flora. A 30 R² = Floral species richness 120 R² = Floral species richness [2A] ee species richness as a function of floral species richness for both years across all sites. [2] ee abundance as a function of floral species richness for both years across all sites. ee species richness excludes unknown species. ee abundance is total number of individual bees including those of unknown species. Floral species richness excludes unknown species. 16

23 2016 bee abundance 2016 bee species richness Figure 4. (A-) 2016 bee abundance and richness as linear functions of 2015 floral species richness. A R² = floral species richness R² = floral species richness [3A] 2016 bee species richness as a function of 2015 floral species richness. [3] 2016 bee abundance as a function of 2015 floral species richness floral richness only includes data from June, July, and August sample dates in order to correspond to bee fauna from 2015 sample dates. ee species richness excludes unknown species. ee abundance is total number of individual bees including those of unknown species. Floral species richness excludes unknown species. 17

24 Mean bee species richness Mean bee abundance Figure 5. (A-) Mean bee abundance and richness by bloom count groupings. A 20 P = < to 1000 >1000 Number of blooms 10 8 A P = A < to 1000 >1000 Number of blooms loom counts grouped into three categories: <100 (little to no blooms), 100 to 1000 (average amount of blooms), >1000 (plentiful blooms). [4A] Mean bee abundance by bloom count groupings, bee abundance includes individuals of unknown species. [4] Mean bee species richness by bloom count grouping, bee richness excludes unknown species. loom counts for unknown plant species excluded. ee abundance and richness means calculated for both years across all sites. loom counts recorded for each site for each sample date. 18

25 Mean native bee species richness Mean exotic bee species richness Mean native bee abundance Mean exotic bee abundance Figure 6. (A-) Native and exotic bee abundance means for the four site types. A P = A P = A A R H C D 0 R H C D Site type Site type Site types: Robertson (R), Houses (H), Campus (C), Downtown (D). [6A] Mean native bee abundance for each site type. [6] Mean exotic bee abundance for each site type, bee abundance excludes bees of unknown species. ee abundance excludes bees of unknown species. Means calculated with bee abundances and bee richness recorded for both years across all sites. Figure 7. (A-) Native and exotic bee richness means for the four site types. A 8 A P = A A P = A 1 A R H C D 0 R H C D Site type Site type Site types: Robertson (R), Houses (H), Campus (C), Downtown (D). [7A] Mean native bee richness for each site type. [7] Mean exotic bee richness for each site type. ee species richness excludes bees of unknown species. Means calculated with bee abundances and bee richness recorded for both years across all sites. 19

26 Mean bee species richness Mean bee abundance Figure 8. (A-) ee fauna means for sites categorized by floral species composition. A P native = P exotic = Natural Unnatural No blooms Floral site categories Native bees Exotic bees 8 6 P native = P exotic = Natural Non-natural No blooms Floral site categories Native bees Exotic bees Site categories: predominantly natural, predominantly unnatural, no blooms. The sites within each category vary by sample date because they are based upon blooming angiosperms present at the time of sampling as described in the methods. [10A] Means of native bee abundances and exotic bee abundances for each floral site category, bee abundances exclude individuals of unknown species. [10] Means of native bee species richness and exotic bee species richness for each floral site category, bee richness excludes unknown species. 20

27 Mean polylectic species richness Mean oligolectic species richness Mean polylege abundance Mean oligolege abundance Figure 9. (A-) Polylectic and oligolectic bee abundance means for the four site types. A A P = A P = A A A A 0 R H C D 0 R H C D Site type Site type Site types: Robertson (R), Houses (H), Campus (C), Downtown (D). [8A] Mean polylectic bee abundance for each site type. [8] Mean oligolectic bee abundance for each site type. ee abundance excludes bees of unknown species. Means calculated with bee abundances and bee richness recorded for both years across all sites. Figure 10. (A-) Polylectic and oligolectic bee richness means for the four site types. A A P = A A A P = R H C D 0 R H C D Site type Site type Site types: Robertson (R), Houses (H), Campus (C), Downtown (D). [9A] Mean polylectic bee species richness for each site type. [9] Mean oligolectic bee species richness for each site type. ee species richness excludes bees of unknown species. Means calculated with bee abundances and bee richness recorded for both years across all sites. 21

28 DISCUSSION Assessment of bee abundance and diversity This study provided an extensive record of bee species in northwestern PA. It found many species absent in historical records of PA bee species compiled by Donovall and vanengelsdorp (2010). However, Donovall and vanengelsdorp (2010) revealed that there are some species present in the area that were not found during sampling, mostly of the genus Andrena (Fabricius). Species of Andrena are largely oligolectic (Michener, 2007), thus they are rarer to find unless in range of their host plants. Other explanations for this include factors that led to fluctuations in bee populations and potential sampling biases. Overall bee abundance and richness were drastically different between years. ee abundance during flight season is dependent upon the previous season s progeny and progeny survival during the winter (Cane & Payne, 1993). The winter prior to summer 2016 was milder than the winter before summer 2015 (wunderground.com), which may explain greater bee abundance and diversity in Potts et al. (2003) observed positive correlations between bee fauna and flora species richness; however, they found that bee abundance in one year had a stronger relationship with floral abundance of the previous year. This suggests that bee abundance of the current season may be predicted by floral abundance of the season prior (Potts et al., 2003). Similar to the findings of Potts et al. (2003), a linear regression revealed that bee fauna of this study s 2016 season was more strongly related to the floral richness of the previous season. Greater availability of floral resources in 2015 may have increased the number of larvae produced and led to more bee abundance in the following season (Tepedino & Stanton, 1981; Cane & Payne, 1993). ee abundance in general fluctuates annually, regionally, and locally (Cane & Payne, 1993). Although this study provided a comprehensive baseline of local bee species, a survey spanning additional seasons including sampling sites in other environments may be necessary to declare that all bee species in the region are documented. This survey collected a much greater number of polylectic species than oligolectic species, which mimics reports that an estimated 30% of bee species native to the northeastern United States are oligolectic (Fowler & Droege, 2016). Sampling methods also may have contributed to collecting a greater proportion of generalist bees. Oligoleges are often collected via hand netting at their host plants (Westphal et al., 2008; Stephen & Rao, 2005). Known biases of bee bowls include higher catch rate of smaller solitary generalist bees, especially Halictids (Roulston et al. 2007). Generalist Halictids were the most abundant bees collected by the bee bowls and this survey s most represented family overall. Not all bee species are as susceptible to passive trapping as others, which is another reason why hand netting is often 22

29 used as a supplementary trapping method (Roulston et al. 2007). Common bee bowl colors include yellow, white, and blue. Some bees are more attracted to certain colors depending on the colors of the plants they access for resources (Leong & Thorp, 1999). Color preference may be stronger for oligolectic bees (Leong & Thorp, 1999), thus by not including blue bee bowls, some oligolectic species may have been excluded. The polylectic A. mellifera and H. hyalinatus were amongst the most common exotic polyleges. The majority of exotic species are polylectic, which allows them to become established more easily (Cane, 2003). This is true especially in the case of Apis mellifera, an extreme generalist able to obtain resources from thousands of plant species throughout the continent (Cane, 2003). There are 21 known exotic bee species present in North America, four of which are oligolectic (Cane, 2003). The sole exotic oligolege trapped in this study, C. rapunculi was more uncommon than other oligolectic species. Exotic oligoleges are very rare because they have a restricted range that must include their host plants, which are usually invasive to the U.S. and consequently usually uncommon (Cane, 2003). Ultimately, further repetitive sampling throughout the duration of bee flight season and inclusion of alternative sampling techniques are necessary to overcome sampling biases and fluctuations in bee populations that inhibit an accurate representation of bee diversity. Nevertheless, the results of this study contribute to bee-monitoring in a previously undersurveyed area of PA. Effect of floral composition on bee fauna This study demonstrates that overall bee abundance and species richness is positively related to floral species richness, and bee species richness was decreased when blooms were sparse. It was expected that the relationships between bee fauna and flora species richness would be stronger, but other factors such aforementioned sampling biases and fluctuations of bee abundance likely came into play. In general, bee abundance and richness is known to be positively related to floral abundance and richness, although there are other influential environmental components such as nesting site availability (Pardee & Philpott, 2014). Research has indicated that habitat fragmentation and urbanization contribute to local declines in pollinators by limiting floral resources (Winfree et al., 2011). Overall bee richness was significantly greatest at Robertson, where sites generally had predominantly natural floral composition with many native species. Robertson s greater proportion of naturally-occurring angiosperms including many natives may explain this result because the majority of the bees collected were native and coevolved with native plants. Pardee and Philpott (2014) investigated bee abundance and richness in suburban backyard gardens 23

30 with either non-native or native plants. They found bee abundance to be significantly greater in gardens dominated by native plants (Pardee & Philpott, 2014). Heinrich (1975) observed native bee disregard for non-native plants in preference of native plants. Additionally, Frankie et al. (2005) performed a study of bee visitation to native and non-native plants in residential areas and found that native plants attracted more native bees and honey bees. Non-native ornamental species were bred to appeal to people aesthetically and for easy cultivation in gardens with disregard to pollinator attraction (Frankie et al., 2005). Some of these ornamental varieties were actually bred to be pollenless (Frankie et al., 2005). It is possible that downtown sites had less bee fauna overall due to the presence of unnatural ornamentals. Findings from Lerman and Milam (2010) further support these results. They investigated bee fauna in relation to floral abundance in the lawns of suburban yards and determined that naturally-occurring flowering plant species, such as clover, support pollinators in an environment subject to habitat fragmentation (Lerman & Milam, 2016). Downtown Meadville may then be able to support more bee fauna even in such a fragmented environment by introducing more native angiosperms. Moreover, this study revealed that oligolectic species were generally most common at sites with native plant species that included their host plants, especially if the oligolege is strict in its specialization. Peponapis pruinosa, the cucurbit specialist may not be as strict in its oligolecty because it occurred more frequently than other oligoleges and not usually within close proximity of cucurbits. Cane and Payne (1993) assessed oligolectic bee abundance within close proximity to their host plants and found them to be more common than polylectic species. However, Minckley et al. (1999) hypothesized that oligolectic bees would occur within close range to their host plants. They found that this was not consistently the case and that there are other factors, like nesting area, influencing distributions of oligoleges (Minckley et al., 1999). When sites were categorized by percentages of natural and unnatural flora, native bee abundance and richness was not greatest at sites with a higher percentage of naturallyoccurring floral species. This unexpected outcome may be due in part to composition of the surrounding flora. ees were occasionally collected at sites where no blooming floral species recorded within the 5-m radius assessed, indicating that the radius assessed was not large enough to account for all surrounding flora impacting the bee fauna. ee foraging range is 150 m at minimum, well beyond the 5-m radius of the sites (Gathmann & Tscharntke, 2002). Therefore, examining general floral composition at the site type gave a more accurate understanding of flora within the bees foraging range and its effect on bee abundance and diversity. 24