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The Wild of New York: Our Insurance Policy Against Honey Decline Bryan N. Danforth and Maria van Dyke Department of Entomology, Cornell University, Ithaca, NY

ollination is a valuable service provided by both managed bees (pri- marily honey bees, Apis mellifera) and wild, native bees. Bee pollina- tion is essential for the production of fruits, nuts, vegetables, spices, P stimulants (such as coffee), and edible oils (such as sun- “We are lucky to have a diverse native flower and canola). Estimates bee fauna that can fill the gap if of the economic contribution honeybees become more expensive or of vary widely, are simply unavailable to New York crop but two recent studies give producers.”” us a sense of the magnitude of the contribution pollina- tors make to the global and national economy. Gallai et al. (2009) estimated that the contribution of pollination to the global economy was approximately $170 billion annually, and Calderone (2012), based on data for the US alone, estimated that pollination contributes over $15 bil- lion/year to the US economy. In New York, important pollinator- dependent crops include apple ($250 million/year), squash and pumpkin ($74 million/ year), tomatoes ($47 million/year), strawberries ($7 million/year), cherries ($3 million/year), and pears ($2.5 million/year) (economic data from New York State Department of Agriculture and Markets; www.agriculture.ny.gov). Many of New York’s most high value fruits are entirely dependent on pol- linators for successful production. Based on our research on apples over the past seven years, there is a Figure 1. Histogram showing the distribution of the number surprisingly diverse fauna of wild bees that contribute to apple pollination in of species across the 42 bee genera known from NY. We have documented over 118 wild bee species visiting apple blossoms New York. Our largest genera are and in surveys of NY apple orchards from Lake Ontario to the Hudson Valley , followed by , Megachile, (Russo et al. 2015). We have shown that wild bees are numerically abundant Osmia, and Bombus. New York hosts a total of 416 wild bee species. across orchards varying in size and management (Russo et al. 2015), that wild bees are highly effective pollinators on a per-visit basis (Park et al. 2015), and that wild bee diversity and abundance are correlated with apple fruit and seed set (Blitzer et al., in prep.). Apples are not the only crop that benefits from wild pollinators. Strawberries, pears, cherries, tomatoes and cucurbit crops are benefitting from a diverse wild pollinator fauna as well. In April, 2015, Governor Cuomo announced that New York State will establish a taskforce to develop a Pollinator Protection Plan to promote the health and stability of pollinator populations in New York State. A first step toward developing a comprehensive Pollinator Protection Plan is to accurately document the diversity of wild bees in New York. To that end, we have been developing a complete list of New York’s wild bees. Our goal is to accurately document what species occur in New York, which bee species are native and which are non-native, and as much information about the natural history, nesting biology, floral preferences, social behaviors as possible. This is essential baseline data for developing a comprehensive Pollinator Protection Plan for NY. We assembled our list of New York bee species using the American Museum of Natural History’s “ Easy Capture” database (Schuh Figure 2. Andrena (Melandrena) female on a dandelion (Taraxacum). Andrena are ground-nesting bees et al. 2010, Schuh 2012). These data were originally gathered as part that are important early spring pollinators of of an NSF-funded research grant to John Ascher, Jerome Rozen, Jr., and apples, cherries, strawberries and many other Douglas Yanega entitled “Collaborative Databasing of North American Bee flowering trees. Photo credit: Bryan Danforth NEW YORK FRUIT QUARTERLY . VOLUME 23 . NUMBER 4 . WINTER 2015 17 Collections within a global informatics network.” Specimen and not externally, records come from major eastern North American as do most - collections, including American Museum of Natural History, collecting bees. Cornell University, University of Connecticut, and Rutgers A n o t h e r University. We supplemented the list with regional (e.g., Giles & important group Ascher 2006, Matteson et al. 2008, Feteridge et al. 2008, Ascher of bees are the et al. 2014) and crop-based (e.g., Gardner & Ascher 2006, Russo carpenter bees. et al. 2015) surveys of bee diversity in New York. Note that this In North America is likely an incomplete list of New York bees because no state we have both small survey has ever been conducted on the wild bees of New York (Ceratina) and State. large (Xylocopa) carpenter bees. These bees con- Bee Diversity in New York Figure 3. Xylocopa virginica female nectaring We estimate that there are a total of 416 bee species in struct nests in on an apple flower in the early New York state. Forty-two of the 425 genera of bees in the wood or preexisting spring. Xylocopa females nest in wood. Photo credit: Kent Loeffler world (Michener 2007) occur in New York (Figure 1). Our most cavities. Xylocopa common (and speciose) genera are Andrena, Lasioglossum, virginica is a com- Nomada, , Megachile, Colletes, Osmia, Hylaeus, mon bee in New York State (Figure 3). Nests are conspicuous Melissodes, Bombus, and Coelioxys (Figure 1). A survey of bee because males hover in front of the nests (typically located in species in Pennsylvania (Donovall and vanEngelsdorp 2010) fence posts, wooden park benches, and houses) and engage in documented a total of 371 species, comparable to the number aggressive territorial battles. we report here for New York, but likely an underestimate given Cleptoparasitic bees comprise 23 percent of the bee the size of Pennsylvania. species in New York. The two largest genera of cleptoparasitic bees in New York are Sphecodes and Nomada. Parasitic bees The majority (54%) of bees in New York State are digger are fascinating creatures. They have lost the morphological bees (ground-nesting, solitary bees, such as Andrena, Lasioglossum, Colletes, and Melissodes). Species of Andrena structures associated with nest construction and pollen (Figure 2) are typical of ground-nesting bees in their life history. collection in most other bees. Instead of constructing and At the start of the nesting season (in the spring, summer, or fall, provisioning their own brood cells, parasitic bees enter the depending on the species), female Andrena begin constructing nests of other bees (usually when the host female is away) and burrows in the soil. At the end of these subterranean burrows lay their eggs within the host nest. Once the host female has laid they construct brood cells, which are lined with waterproof her egg and closed the cell, the parasitic hatches from its secretions from the Dufour’s gland. Once a brood cell has been own egg and kills either the host egg or young larva, then feeds constructed, a female provisions it with a mixture of pollen and on the host’s pollen. Parasitic bees have devious methods for nectar collected from flowering plants in the vicinity of the nest. hiding their eggs from the host females. For example, Nomada Foraging ranges in these solitary bees are small – on the order and relatives (in the subfamily Nomadinae) put their eggs in the of 500 m maximum – so nests are typically close to the floral cell wall of the host bee’s nest. resources. Once the provisions have been collected, the pollen/ So far, the great majority of bees we have mentioned are nectar mixture is sculpted into a spherical pollen ball and an solitary (or parasitic). Important eusocial bees in New York egg is laid on top. The brood cell is then closed and the female State include both advanced eusocial taxa in which queens and begins constructing a new brood cell. Brood cells range in depth workers are morphologically distinct (such as Apis mellifera, the from just a few inches to several feet. A typical solitary female introduced ) and primitively eusocial taxa, in which might produce just 10–15 offspring over a period of two to three queens and workers are distinguishable from each other based weeks of active foraging. only on size or behavior. Important primitively eusocial taxa While the majority of bees in New York State are ground- include Bombus (; ), as well as Augochlorella, nesting, several species also make nests in preexisting cavities, Halictus, and some species of Lasioglossum (). We such as twigs, hollow stems, beetle burrows, or in sites above estimate that approximately 19 percent of the bee species in New York State are eusocial. ground. These aboveground, cavity nesters include the mason bees, the wool carder bees and various resin bees. Mason Introduced (Non-native) Bees bees in New York State include genera such as Osmia, Hoplitis, Prochelostoma, and Heriades. Mason bees comprise roughly There are known to be a total of 23 introduced bees in North 7 percent of the species of bees in New York State. Other America, and 21 of them occur in New York State (Ascher 2001, cavity- and stem-nesting bees include the leaf-cutter bees in Cane 2003, Sheffield et al. 2011a). All of the known introduced the genus Megachile (Sheffield et al. 2011b), carder bees in bees have been transported from the Old World (Eurasia) either the genus Anthidium, Pseudoanthidium, and Paranthidium, accidentally or through intentional introduction. The most and the yellow-faced bees in the genus Hylaeus. Megachile common and conspicuous of our introduced European bees is females line their cells with circular pieces of leaf that they cut the honeybee, Apis mellifera, which is managed commercially for from rosebushes and other plants. Hylaeus females line their honey and pollination services. Other introduced bees include burrows (constructed in plant stems or other hollow tubes) species of Megachile, Hylaeus, Chelostoma, Hoplitis, Anthidium with a cellophane-like material produced by the Dufour’s gland. and Andrena (Ascher 2001, Miller et al. 2002, Cane 2003, Hylaeus are unusual bees because they carry pollen internally Sheffield et al. 2011a). Ascher (2001) estimated that accidentally 18 NEW YORK STATE HORTICULTURAL SOCIETY introduced bees account for 0.5 percent of the North American bee species. While they comprise a small number of species, introduced bees make up, in some cases, a large proportion One Bushel Crates of the individuals in New York State. This is especially true of the European honeybee. Most accidentally introduced bees are stem- or cavity-nesting species. These species (in theHylaeinae, Megachilidae, and Xylocopinae) are easily transported in plant materials (e.g., wood) or in man-made materials. Nonnative bee species can have a negative impact on native species for a variety of reasons. Nonnative species may compete with native species for floral and nesting resources, they may carry pathogens that can infect native species, and they can cause mating disruption when they are closely related to native species (Stout and Morales 2009). Unfortunately, we know very little about the impact of nonnative bees on native eastern North American bees. Transcontinental transport of colonies for greenhouse tomato pollination is thought to have led to the introduction of nonnative bumblebee pathogens — specifically microsporidian pathogens in the genus Nosema (Cameron et al. Well built and reliable, these boxes will 2011, Cordes et al. 2012). Introduction of nonnative pathogens is one of the leading hypotheses for the decline in several protect your produce. In bulk, $6.50 each bumblebee species in North America, including Bombus affinis, B. terricola, and B. pensylvanicus. Hamlin Sawmill Osmia cornifrons, also known as the horn-faced bee, is a 1873 Redman Rd. Hamlin, NY 14464 nonnative mason bee that was intentionally introduced into 585-964-3561 the US (along with Osmia taurus) for fruit pollination in the [email protected] 1970s (Batra 1979, 1982). Both non-native Osmia species have www.OneBushelCrate.com host-plant ranges and nesting requirements that are similar to those of our native “blue orchard bee” (Osmia lignaria). Apparent declines in Osmia lignaria in the eastern US may Díaz 2008). The bee is also a nonnative invader that is spreading be linked to the arrival of O. cornifrons and O. taurus, but a across much of western Europe from Belgium (Vereecken and careful examination of the historical data on the abundance of Barbier 2009) to Italy (Quaranta et al. 2014). This large, aggres- O. lignaria has not been conducted. A recent report by Hedtke sive resin bee has been reported to forcibly usurp active nests et al. (2015) indicates that feral populations of O. cornifrons in of our native large (Xylocopa virginica). Roulston the US host Ascosphaera pathogens originally reported from and Malfi (2012) reported an attack on an active carpenter bee Japan, suggesting that intentional introduction of O. cornifrons nest in which the giant resin bee attacked and physically re- has led to the unintentional introduction of a nonnative fungal moved adult carpenter bees guarding the nest entrance. During pathogen into North American Osmia populations. Whether the attack the resin bee grabbed the legs of the carpenter bee, bit this pathogen is present in O. lignaria populations has not yet the carpenter bee near the head, and made repeated attempts to been established. sting it. In addition, the resin bee appeared to use sticky resins Megachile sculpturalis, also known as the giant resin bee to gum up the wings of the carpenter bee—a remarkable case of (Figure 4), was introduced into the southeastern US (North what appears to be chemical warfare in the bee world. Laporte Carolina) in the ear- and Minckley (2012) reported a similar example of nest usurpa- ly 1990s (Mangum tion that included the use of sticky resin against the resident and Brooks 1997, carpenter bees in Rochester, NY. The rapid spread of the giant Mangum and Sum- resin bee throughout the eastern US (and Europe) and the re- ner 2003, Hinojosa- ports of nest usurpation suggest that this bee may have a very Díaz et al. 2005, Ma- significant impact on native carpenter bee populations across ier 2009). It has since an enormous geographic range. spread throughout much of eastern North America (as Rare, Threatened, and Endangered Bees far north as Ontar- We know very little about the conservation status of most bee species in New York State because there is no long-term io), as far south as Figure 4. Megachile sculpturalis mating pair. Alabama (Mangum This species is a non-native invader monitoring program for wild bees. However, one way to moni- and Sumner 2003), introduced from China in the early tor historical changes in wild bee populations is to use specimen and was recently re- 1990s. Today this bee occurs across record data from natural history museums, such as the Ameri- much of eastern North America. can Museum of Natural History and the Cornell University In- ported as far west as Photo credit: Eric Barbier and Kansas (Hinojosa- Pierre-Jean Bernard sect Collection [http://cuic.entomology.cornell.edu/]. Museum

NEW YORK FRUIT QUARTERLY . VOLUME 23 . NUMBER 4 . WINTER 2015 19 records can give us a historical perspective on the change in the absolute and relative abundance of a species over time. A re- cent study (Bartomeus et al. 2013) examined historical museum records for 438 bee species across the eastern US in order to identify evidence of significant declines over the past 140 years. Sample sizes were sufficient to examine historical trends in 187 species. Of those 187, 49 species occurring in NY were found to be in decline or rare and potentially threatened. Bumblebees, because of their large size and ease of observation, are perhaps the best known bees in terms of conservation status. A number of eastern bumblebee species are known to have experienced significant declines over the past 30 years. Bombus terricola, B. bohemicus, B. insularis, B. pensylvanicus, and B. terricola are all in decline over part or all of their ranges. Bombus affinis, a common eastern bumblebee prior to 1996, is now extremely rare and may be close to extinction. The causes of these declines are not clear but may include loss of natural habitat, exposure to pesticides, and the Figure 5. Colletes compactus males in sleeping aggregation. In some groups of solitary bees, males gather together in the evening to arrival of nonnative pathogens (especially Nosema bombi from form sleeping aggregations. These aggregations may provide Europe; Cameron et al. 2011, Cordes et al. 2012). some protection from predators but we do not know very Besides the bumblebees, which are well-studied and much about why bees form these aggregations. This species is charismatic pollinators, the list of declining bee species detected reported to be in decline based on the analysis of Bartomeus et al. 2013. Photo credit: Susan Barnett. by Bartomeus et al. (2013) includes solitary ground-nesting bees (e.g., Andrena, Melissodes, and Colletes [Figure 5]), solitary stem- and cavity-nesting bees (e.g., Osmia and Megachile), social are many records of E. pilosula prior to 1940 and the known ground-nesting bees (e.g., Lasioglossum subgenus Dialictus), range of E. pilosula includes 18 states and 4 Canadian provinces narrow host-plant specialists (e.g., Peponapis pruinosa, some (Sheffield et al. 2004, Wagner and Ascher 2008). However, in Andrena and Colletes), and cleptoparasites (e.g., Coelioxys the past 60 years, the bee has only been collected four times: and Epeolus). The study of Bartomeus et al. (2013) is likely in Montana (1958), Ontario (1960), Nova Scotia (2002), and an underestimate of the number of threatened bee species in Connecticut (2008). This bee is a prime candidate for listing as the Northeast because the rarest bees were excluded from the an endangered species in North America. analysis because of their small sample size. Bees in the family are among the rarest of New Conclusions York’s bees. Melittidae is an enigmatic, seemingly ancient group Many of the wild bees we have described above are of bees with its greatest diversity in southern Africa. Virtually contributing economically to New York agricultural production. all melittid bees are narrow host-plant specialists (Michez One can view these wild bees as New York agriculture’s 2008) and many groups seem to prefer sandy soils for nesting. insurance policy against honeybee decline. We are lucky to In New York we have just five species in two genera:Melitta and have a diverse native bee fauna that can fill the gap if honeybees . Melitta eickworti and Melitta americana are both become more expensive or are simply unavailable to New York specialists on Vaccinium (Ericaceae). Melitta americana can be crop producers. Wild bees do not seem to suffer from the same common in and around blueberry and cranberry fields (Payette diseases and parasites that are linked to declines in honey bees 2013, Cariveau et al. 2013), but Melitta eickworti is restricted to in North America. NY residents and agricultural producers can shady forest understory with deerberry (Vaccinium stamineum; sleep well at night knowing that New York’s wild bees are hard Cane et al. 1985). Macropis includes highly specialized “oil bees” at work pollinating our crops – and they do it for free! that are narrow host-plant specialists on (yellow loosestrife). Female Macropis nest in humid, boggy habitats Acknowledgements (where their host-plants occur) and they use the floral oils for lining the brood cell as well as for larval nutrition (Cane et al. We are very grateful to John Ascher (University of Singapore 1983). The collection of floral oils may be an adaptation for and American Museum of Natural History), Jerome G. Rozen, nesting in saturated, marshy soils along streams, rivers and on Jr. (American Museum of Natural History), and Douglas Yanega the edge of ponds and lakes. In New York we have three Macropis (University of California Riverside) for access to the Arthropod species, all of which are rare and geographically restricted. Easy Capture dataset, which was essential to the creation of a Their narrow host-plant preferences and obligate association list of bee species currently present in New York state. We are with oil-producing host-plants (Lysimachia) contributes to also grateful to the members of my laboratory who provided both the rarity of these bees as well as their status as potentially input on this report. Finally, we are grateful to Art Agnello for endangered pollinators. editing this issue of the NY Fruit Quarterly. Epeoloides pilosula is likely the most threatened and endangered bee species in New York (and the Northeast). E. 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NEW YORK FRUIT QUARTERLY . VOLUME 23 . NUMBER 4 . WINTER 2015 21 Per-visit pollinator performance and regional importance the Entomological Society of Ontario 142: 29–43. of wild Bombus and Andrena (Melandrena) compared Sheffield, C. S., C. Ratti, L. Packer, and T. Griswold (2011b). to the managed honey bee in New York apple orchards. Leafcutter and mason bees of the genus Megachile Latreille Apidologie [published online 25 August 2015, 10.1007/ (Hymenoptera: Megachilidae) in Canada and Alaska. s13592-015-0383-9] Canadian Journal of Arthropod Identification 18: 1–107. Payette, A. (2013). First record of the bee Melitta americana Sheffield, C. S., S. M. Rigby, R. F. Smith, and P. G.Kevan (Smith) (Hymenoptera: Melittidae) for Quebec and Canada. (2004). The rare cleptoparasitic bee Epeoloides pilosula Canadian Field-Naturalist 127(1): 60–63. (Hymenoptera: Apoidea: Apidae) discovered in Nova Quaranta, M., A. Sommaruga, P. Balzarini, A. Felicioli, and Scotia, Canada, with distributional notes. Journal of the others (2014). A new species for the bee fauna of Italy: Kansas Entomological Society 77: 161–164. Megachile sculpturalis continues its colonization of Europe. Stout, J. C. and C. L. Morales (2009). Ecological impacts of Bulletin of Insectology 67: 287–293. invasive alien species on bees. Apidologie 40: 388–409. Roulston, T. and R. Malfi (2012). Aggressive eviction of the Vereecken, N. J. and E. Barbier (2009). Premières données sur la eastern carpenter bee (Xylocopa virginica (Linnaeus)) from présence de l’abeille asiatique Megachile (Callomegachile) its nest by the Giant Resin Bee (Megachile sculpturalis sculpturalis Smith (Hymenoptera, Megachilidae) en Smith) Journal of the Kansas Entomological Society, 85(4): Europe. Osmia 3: 4–6. 387–388. Wagner, D. L., and J. S. Ascher (2008). Rediscovery of Epeoloides Russo, L., M. G. Park, J. Gibbs, B. N. Danforth (2015). The pilosula (Cresson) (Hymenoptera: Apidae) in New England. challenge of accurately documenting bee species richness Journal of the Kansas Entomological Society 81: 81–83. in agroecosystems: bee diversity in eastern apple orchards. Ecology and Evolution 5(17): 3531–3540. Bryan Danforth is a professor and Director of Graduate Schuh, R. T. (2012). Integrating specimen databases and Studies in the Department of Entomology. He studies the revisionary systematics. Zookeys 209: 255–267. diversity and evolution of bees. Maria van Dyke is an Schuh, R. T., S. Hewson-Smith, and J. S. Ascher (2010). Specimen outreach support specialist studying the role of wild bees databases: a case study in entomology using web-based in apple pollination. She is currently developing training software. American Entomologist 56(4): 206–216. and educational materials for the Northeast Pollinator Sheffield, C. S. S. Dumesh, M. Cheryomina (2011a). Hylaeus Partnership (http://www.northeastpollinatorpartnership. punctatus (Hymenoptera: Colletidae), a bee species new to org/). [contact: [email protected]] Canada, with notes on other non-native species. Journal of

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