Abstract
Bumble bees (Bombus) play key roles as pollinators in temperate ecosystems. Some North American species have declined due to factors that include habitat loss, parasites, pesticides, and climate change. In many regions conservation is hampered by lack of quantitative data on historical abundance and distribution, making status assessments difficult. From 2012 to 2014, with help from 53 citizen scientists, we conducted surveys to determine the status of bumble bees throughout Vermont, USA. For historical comparison, we identified and digitized bumble bee specimens from 13 public and private collections. Our dataset contained 12,319 records, which we separated into historic (1915–1999; n = 1669) and modern (2000–2014; n = 10,650) periods, with our survey contributing 94% of modern data. Of 17 species, four were not detected and four showed significant declines. Rarefaction indicated that both modern and historic datasets slightly underestimated known species richness, diversity, and abundance, but confirmed a strong decline for all three parameters. Declining species broadly accorded with those reported elsewhere in eastern North America, and included those in subgenera Bombus, Fervidobombus, and Psithyrus. Four species in the subgenus Pyrobombus (B. bimaculatus, B. impatiens, B. ternarius, and B. vagans) greatly increased in relative abundance in the modern period. Landscape factors such as road density, elevation, and land use strongly predicted distribution of some species. Species diversity was correlated positively with grasslands, and negatively with deciduous and mixed forest cover, while abundance was correlated positively with evergreen forest cover, yet negatively with deciduous forest.
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References
Alford DV (1969) A study of the hibernation of bumblebees (Hymenoptera: Bombidae) in southern England. J Anim Ecol 38:149–170. https://doi.org/10.2307/2743
Alger SA (2018) Evidence of RNA virus spillover from managed honeybees to wild bumblebees. Burlington, Vermont. https://www.eaglehill.us/NENHC_2019/archives/NENHC2018-program-guide.pdf
Andersson P, Koffman A, Sjödin NE, Johansson V (2017) Roads may act as barriers to flying insects: species composition of bees and wasps differs on two sides of a large highway. Nat Conserv 18:47–59. https://doi.org/10.3897/natureconservation.18.12314
Arbetman M, Meeus I, Morales C et al (2012) Alien parasite hitchhikes to Patagonia on invasive bumblebee. Biol Invasions 1–6. https://doi.org/10.1007/s10530-012-0311-0
Arbetman MP, Gleiser G, Morales CL et al (2017) Global decline of bumblebees is phylogenetically structured and inversely related to species range size and pathogen incidence. Proc R Soc B 284:20170204. https://doi.org/10.1098/rspb.2017.0204
Austen GE, Bindemann M, Griffiths RA, Roberts DL (2016) Species identification by experts and non-experts: comparing images from field guides. Sci Rep 6:33634. https://doi.org/10.1038/srep33634
Banaszak J, Ratyńska H (2014) Local changes in communities of wild bees (Hymenoptera: Apoidea, Apiformes): 30 years later. Pol J Entomol 83:325–351. https://doi.org/10.2478/pjen-2014-0025
Bartomeus I, Ascher JS, Gibbs J et al (2013) Historical changes in northeastern US bee pollinators related to shared ecological traits. Proc Natl Acad Sci 110:4656–4660. https://doi.org/10.1073/pnas.1218503110
Bates D, Maechler M, Bolker B et al (2016) lme4: linear mixed-effects models using Eigen and S4. R package version 1.1–12. http://www.CRAN.R-project.org/package=lme4
Bhattacharya M, Primack RB, Gerwein J (2003) Are roads and railroads barriers to bumblebee movement in a temperate suburban conservation area? Biol Conserv 109:37–45. https://doi.org/10.1016/S0006-3207(02)00130-1
Blacquière T, Smagghe G, Gestel CAM van, Mommaerts V (2012) Neonicotinoids in bees: a review on concentrations, side-effects and risk assessment. Ecotoxicology 21:973–992. https://doi.org/10.1007/s10646-012-0863-x
Bommarco R, Lundin O, Smith HG, Rundlöf M (2012) Drastic historic shifts in bumble-bee community composition in Sweden. Proc R Soc Lond B Biol Sci 279:309–315. https://doi.org/10.1098/rspb.2011.0647
Bowers MA (1985) Bumble bee colonization, extinction, and reproduction in subalpine meadows in northeastern Utah. Ecology 66:914–927
Cameron SA, Lozier JD, Strange JP et al (2011) Patterns of widespread decline in North American bumble bees. Proc Natl Acad Sci 108:662–667. https://doi.org/10.1073/pnas.1014743108
Cameron SA, Lim HC, Lozier JD et al (2016) Test of the invasive pathogen hypothesis of bumble bee decline in North America. Proc Natl Acad Sci 201525266. https://doi.org/10.1073/pnas.1525266113
Campbell Grant EH (2015) Please don’t misuse the museum: ‘declines’ may be statistical. Glob Change Biol 21:1018–1024. https://doi.org/10.1111/gcb.12702
Carper AL, Adler LS, Warren PS, Irwin RE (2014) Effects of suburbanization on forest bee communities. Environ Entomol 43:253–262. https://doi.org/10.1603/EN13078
Chao A, Gotelli NJ, Hsieh TC et al (2014) Rarefaction and extrapolation with Hill numbers: a framework for sampling and estimation in species diversity studies. Ecol Monogr 84:45–67. https://doi.org/10.1890/13-0133.1
Cohn JP (2008) Citizen science: can volunteers do real research? Bioscience 58:192–197. https://doi.org/10.1641/B580303
Colla SR (2016) Status, threats and conservation recommendations for wild bumble bees (Bombus spp.) in Ontario, Canada: a review for policymakers and practitioners. Nat Areas J 36:412–426. https://doi.org/10.3375/043.036.0408
Colla S, Packer L (2008) Evidence for decline in eastern North American bumblebees (Hymenoptera: Apidae), with special focus on Bombus affinis Cresson. Biodivers Conserv 17:1379–1391. https://doi.org/10.1007/s10531-008-9340-5
Colla SR, Richardson LL (2015) COSEWIC status report on the yellow-banded bumble bee Bombus terricola. Committee on the Status of Endangered Wildlife in Canada, Ottawa. http://www.registrelep-sararegistry.gc.ca/default_e.cfm
Colla SR, Otterstatter MC, Gegear RJ, Thomson JD (2006) Plight of the bumble bee: pathogen spillover from commercial to wild populations. Biol Conserv 129:461–467. https://doi.org/10.1016/j.biocon.2005.11.013
Colla SR, Gadallah F, Richardson L et al (2012) Assessing declines of North American bumble bees (Bombus spp.) using museum specimens. Biodivers Conserv 21:3585–3595. https://doi.org/10.1007/s10531-012-0383-2
Connelly H, Poveda K, Loeb G (2015) Landscape simplification decreases wild bee pollination services to strawberry. Agric Ecosyst Environ 211:51–56. https://doi.org/10.1016/j.agee.2015.05.004
Cusser S, Neff JL, Jha S (2016) Natural land cover drives pollinator abundance and richness, leading to reductions in pollen limitation in cotton agroecosystems. Agric Ecosyst Environ 226:33–42. https://doi.org/10.1016/j.agee.2016.04.020
Daly C, Neilson RP, Phillips DL (1994) A statistical-topographic model for mapping climatological precipitation over mountainous terrain. J Appl Meteorol 33:140–158
David A, Botías C, Abdul-Sada A et al (2016) Widespread contamination of wildflower and bee-collected pollen with complex mixtures of neonicotinoids and fungicides commonly applied to crops. Environ Int 88:169–178. https://doi.org/10.1016/j.envint.2015.12.011
Dickinson JL, Zuckerberg B, Bonter DN (2010) Citizen science as an ecological research tool: challenges and benefits. Annu Rev Ecol Evol Syst 41:149–172. https://doi.org/10.1146/annurev-ecolsys-102209-144636
Dickinson JL, Shirk J, Bonter D et al (2012) The current state of citizen science as a tool for ecological research and public engagement. Front Ecol Environ 10:291–297. https://doi.org/10.1890/110236
Douglas MR, Tooker JF (2015) Large-scale deployment of seed treatments has driven rapid increase in use of neonicotinoid insecticides and preemptive pest management in U.S. field crops. Environ Sci Technol. https://doi.org/10.1021/es506141g
Droege S, Kolski S, Ascher JS, Pickering J (2018) Apoidea: Identification keys to the bees of North America. In: Discov. Life. http://www.discoverlife.org/mp/20q?search=Apoidea#Identification. Accessed 22 Jan 2018
Dupont YL, Damgaard C, Simonsen V (2011) Quantitative historical change in bumblebee (Bombus spp.) assemblages of red clover fields. PLoS ONE 6:e25172. https://doi.org/10.1371/journal.pone.0025172
Féon VL, Henry M, Guilbaud L et al (2016) An expert-assisted citizen science program involving agricultural high schools provides national patterns on bee species assemblages. J Insect Conserv 1–14. https://doi.org/10.1007/s10841-016-9927-1
Fowler J (2016) Specialist bees of the Northeast: Host plants and habitat conservation. Northeast Nat 23:305–320
Franklin HJ (1912) The bombidae of the new world. Trans Am Entomol Soc 38:177–486
Garibaldi LA, Steffan-Dewenter I, Winfree R et al (2013) Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science 339:1608–1611. https://doi.org/10.1126/science.1230200
Geib JC, Strange JP, Galen C (2015) Bumble bee nest abundance, foraging distance, and host-plant reproduction: implications for management and conservation. Ecol Appl 25:768–778. https://doi.org/10.1890/14-0151.1
Gezon ZJ, Wyman ES, Ascher JS et al (2015) The effect of repeated, lethal sampling on wild bee abundance and diversity. Methods Ecol Evol 6:1044–1054. https://doi.org/10.1111/2041-210X.12375
Giles V, Ascher JS (2006) A survey of the bees of the Black Rock Forest Preserve, New York. J Hymenopt Res 15:208–231
Goulson D (2003) Effects of introduced bees on native ecosystems. Annu Rev Ecol Evol Syst 34:1–26
Goulson D, Nicholls E, Botías C, Rotheray EL (2015) Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 347:1255957. https://doi.org/10.1126/science.1255957
Graystock P, Yates K, Evison SEF et al (2013) The Trojan hives: pollinator pathogens, imported and distributed in bumblebee colonies. J Appl Ecol 50:1207–1215. https://doi.org/10.1111/1365-2664.12134
Graystock P, Goulson D, Hughes WOH (2015) Parasites in bloom: flowers aid dispersal and transmission of pollinator parasites within and between bee species. Proc R Soc Lond B Biol Sci 282:20151371. https://doi.org/10.1098/rspb.2015.1371
Graystock P, Blane EJ, McFrederick QS et al (2016) Do managed bees drive parasite spread and emergence in wild bees? Int J Parasitol Parasites Wildl 5:64–75. https://doi.org/10.1016/j.ijppaw.2015.10.001
Greenleaf SS, Williams NM, Winfree R, Kremen C (2007) Bee foraging ranges and their relationship to body size. Oecologia 153:589–596. https://doi.org/10.1007/s00442-007-0752-9
Grixti JC, Wong LT, Cameron SA, Favret C (2009) Decline of bumble bees (Bombus) in the North American Midwest. Biol Conserv 142:75–84. https://doi.org/10.1016/j.biocon.2008.09.027
Hatfield R, Jepsen S, Thorp RW et al (2014) Bombus citrinus: The IUCN Red List of threatened species. Int. Union Conserv. Nathttp://www.iucnredlist.org/details/44937676/0
Hatfield R, Jepsen S, Colla SR (2017) Bumble Bee Watch. In: Xerces Soc. Invertebr. Conserv. http://www.bumblebeewatch.org. Accessed 8 Nov 2017
Heinrich B (2004) Bumblebee economics, Revised edition. Harvard University Press, Cambridge
Homer CG, Dewitz JA, Yang L et al (2015) Completion of the 2011 National Land Cover Database for the conterminous United States-representing a decade of land cover change information. Photogramm Eng Remote Sens 81:345–354
Hsieh TC, Ma KH, Chao A (2016) iNEXT: an R package for rarefaction and extrapolation of species diversity (Hill numbers). Methods Ecol Evol 7:1451–1456
Inouye D, Droege S, Mawdsley J (2017) Words alone will not protect pollinators. Science 355:357–357. https://doi.org/10.1126/science.aam6132
IUCN (2017) The IUCN Red List of threatened species. Version 2017-2. http://www.iucnredlist.org. Accessed 8 Nov 2017
Jha S, Kremen C (2013) Resource diversity and landscape-level homogeneity drive native bee foraging. Proc Natl Acad Sci 110:555–558. https://doi.org/10.1073/pnas.1208682110
Kalm P (1770) Travels into North America: containing its natural history, and a circumstantial account of its plantations and agriculture in general, with the civil, ecclesiastical and commercial state of the country, the manners of the inhabitants, and several curious and important remarks on various subjects. Printed for T. Lowndes, London
Kerr JT, Pindar A, Galpern P et al (2015) Climate change impacts on bumblebees converge across continents. Science 349:177–180. https://doi.org/10.1126/science.aaa7031
Kevan PG (1975) Forest application of the insecticide fenitrothion and its effect on wild bee pollinators (Hymenoptera: Apoidea) of lowbush blueberries (Vaccinium spp.) in southern New Brunswick, Canada. Biol Conserv 7:301–309. https://doi.org/10.1016/0006-3207(75)90045-2
Kim KC, Byrne LB (2006) Biodiversity loss and the taxonomic bottleneck: emerging biodiversity science. Ecol Res 21:794. https://doi.org/10.1007/s11284-006-0035-7
Kleijn D, Winfree R, Bartomeus I et al (2015) Delivery of crop pollination services is an insufficient argument for wild pollinator conservation. Nat Commun 6:7414. https://doi.org/10.1038/ncomms8414
Klein A-M, Vaissière BE, Cane JH et al (2007) Importance of pollinators in changing landscapes for world crops. Proc R Soc Lond B Biol Sci 274:303–313. https://doi.org/10.1098/rspb.2006.3721
Klyza CM, Trombulak SC (1999) The story of Vermont: a natural and cultural history. UPNE, Hanover
Kudo G, Ida TY (2013) Early onset of spring increases the phenological mismatch between plants and pollinators. Ecology 94:2311–2320. https://doi.org/10.1890/12-2003.1
Larson JL, Kesheimer AJ, Potter DA (2014) Pollinator assemblages on dandelions and white clover in urban and suburban lawns. J Insect Conserv 1–11. https://doi.org/10.1007/s10841-014-9694-9
Laverty TM, Harder LD (1988) The bumble bees of eastern Canada. Can Entomol 120:965–987. https://doi.org/10.4039/Ent12097-2
Lebuhn G, Droege S, Connor EF et al (2013) Detecting insect pollinator declines on regional and global scales. Conserv Biol 27:113–120
Lukyanenko R, Parsons J, Wiersma YF (2016) Emerging problems of data quality in citizen science. Conserv Biol 30:447–449. https://doi.org/10.1111/cobi.12706
Lye GC, Osborne JL, Park KJ, Goulson D (2011) Using citizen science to monitor Bombus populations in the UK: nesting ecology and relative abundance in the urban environment. J Insect Conserv 16:697–707. https://doi.org/10.1007/s10841-011-9450-3
Mac Nally R, Walsh CJ (2004) Hierarchical partitioning public-domain software. Biodivers Conserv 13:659–660. https://doi.org/10.1023/B:BIOC.0000009515.11717.0b
MacFarlane RP (1974) Ecology of Bombinae (Hymenoptera: Apidae) of Southern Ontario, with emphasis on their natural enemies and relationships with flowers. Thesis (Ph. D.)–University of Guelph
Mackenzie KE, Averill AL (1995) Bee (Hymenoptera: Apoidea) diversity and abundance on cranberry in southeastern Massachusetts. Ann Entomol Soc Am 88:334–341. https://doi.org/10.1093/aesa/88.3.334
Marshall L, Biesmeijer JC, Rasmont P et al (2017) The interplay of climate and land use change affects the distribution of EU bumblebees. Glob Change Biol. https://doi.org/10.1111/gcb.13867
MassGIS (2014) MassDOT Roads. Massachusetts Department of Transportation. In: Mass. Dep. Transp. http://www.mass.gov/anf/research-and-tech/it-serv-and-support/application-serv/office-of-geographic-information-massgis/datalayers/eotroads.html
Matteson KC, Ascher JS, Langellotto GA (2008) Bee richness and abundance in New York City urban gardens. Ann Entomol Soc Am 101:140–150. https://doi.org/10.1603/0013-8746(2008)101%5B140:BRAAIN%5D2.0.CO;2
McArt SH, Urbanowicz C, McCoshum S et al (2017) Landscape predictors of pathogen prevalence and range contractions in US bumblebees. Proc R Soc B 284:20172181. https://doi.org/10.1098/rspb.2017.2181
McFarland KP (2018) Vermont Bumble Bee Survey-manual for participants. Figshare doi: https://doi.org/10.6084/m9.figshare.6327230.v1
McFarland KP, Richardson LL (2014a) Species status report for Bombus affinis. Vermont Agency of Natural Resources, Montpelier
McFarland KP, Richardson LL (2014b) Species status report for Bombus bohemicus. Vermont Agency of Natural Resources, Montpelier
McFarland KP, Richardson LL (2014c) Species status report for Bombus terricola. Vermont Agency of Natural Resources, Montpelier
Miller-Struttmann NE, Geib JC, Franklin JD et al (2015) Functional mismatch in a bumble bee pollination mutualism under climate change. Science 349:1541–1544. https://doi.org/10.1126/science.aab0868
Minteer BA, Collins JP, Love KE et al (2014) Avoiding (re) extinction. Science 344:260–261
Mitchell TB (1960) Bees of the eastern United States. I. North Carolina Agricultural Experiment Station
Mitchell TB (1962) Bees of the eastern United States. II. North Carolina Agricultural Experiment Station
Montalva J, Sepulveda V, Vivallo F, Silva DP (2017) New records of an invasive bumble bee in northern Chile: expansion of its range or new introduction events? J Insect Conserv 21:657–666. https://doi.org/10.1007/s10841-017-0008-x
Morandin LA, Winston ML, Abbott VA, Franklin MT (2007) Can pastureland increase wild bee abundance in agriculturally intense areas? Basic Appl Ecol 8:117–124. https://doi.org/10.1016/j.baae.2006.06.003
MRNF Québec (2014) National road network Québec. Government of Canada, Natural Resources Canada, Earth Sciences Sector, Canada Centre for Mapping and Earth Observation
Murray TE, Coffey MF, Kehoe E, Horgan FG (2013) Pathogen prevalence in commercially reared bumble bees and evidence of spillover in conspecific populations. Biol Conserv 159:269–276. https://doi.org/10.1016/j.biocon.2012.10.021
NH DOT (2015) NH public roads. NH Department of Transportation, Bureau of Planning & Community Assistance. In: NH Dep. Transp. Bur. Plan. Community Assist. http://www.granit.unh.edu/data/search?dset=roads_dot/nh
Nicholson CC, Koh I, Richardson LL et al (2017) Farm and landscape factors interact to affect the supply of pollination services. Agric Ecosyst Environ 250:113–122. https://doi.org/10.1016/j.agee.2017.08.030
Nieto A, Roberts SP, Kemp J et al (2014) European red list of bees. Luxemb Publ Off Eur Union 98
NOAA (2013) Coastal Change Analysis Program (C-CAP) 1996 to 2010 regional land cover change data - coastal United States. Office for Coastal Management, National Oceanic and Atmospheric Administration
Ogilvie JE, Griffin SR, Gezon ZJ et al (2017) Interannual bumble bee abundance is driven by indirect climate effects on floral resource phenology. Ecol Lett 20:1507–1515. https://doi.org/10.1111/ele.12854
Ollerton J, Winfree R, Tarrant S (2011) How many flowering plants are pollinated by animals? Oikos 120:321–326. https://doi.org/10.1111/j.1600-0706.2010.18644.x
Ollerton J, Erenler H, Edwards M, Crockett R (2014) Extinctions of aculeate pollinators in Britain and the role of large-scale agricultural changes. Science 346:1360–1362. https://doi.org/10.1126/science.1257259
Omernik JM, Griffith GE (2014) Ecoregions of the conterminous united states: evolution of a hierarchical spatial framework. Environ Manag 54:1249–1266. https://doi.org/10.1007/s00267-014-0364-1
Osborne JL, Martin AP, Carreck NL et al (2008) Bumblebee flight distances in relation to the forage landscape. J Anim Ecol 77:406–415. https://doi.org/10.1111/j.1365-2656.2007.01333.x
Perlut NG, Strong AM, Donovan TM, Buckley NJ (2006) Grassland songbirds in a dynamic management landscape: behavioral responses and management strategies. Ecol Appl 16:2235–2247
R Core Team (2018) R: A language and environment for statistical computing. Version 3.5.0. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, http://www.R-project.org
Raimets R, Karise R, Mänd M et al (2018) Synergistic interactions between a variety of insecticides and an ergosterol biosynthesis inhibitor fungicide in dietary exposures of bumble bees (Bombus terrestris L.). Pest Manag Sci 74:541–546. https://doi.org/10.1002/ps.4756
Rasmont P, Iserbyt S (2012) The bumblebees scarcity syndrome: are heat waves leading to local extinctions of bumblebees (Hymenoptera: Apidae: Bombus)? Ann Soc Entomol Fr NS 48:275–280. https://doi.org/10.1080/00379271.2012.10697776
Ratti CM, Colla SR (2010) Discussion of the presence of an eastern bumble bee species (Bombus impatiens Cresson) in western Canada. Pan-Pac Entomol 86:29–31. https://doi.org/10.3956/2009-19.1
Renfrew RB (2013) The second atlas of breeding birds of Vermont, 2nd edn. University Press of New England, Lebanon
Richardson LL (2018) Fernald’s cuckoo bumble bee (Bombus fernaldae) observation. Missisquoi National Wildlife Refuge. iNaturalist.org. https://www.inaturalist.org/observations/12807025. Accessed 25 May 2018
Schmid-Hempel R, Eckhardt M, Goulson D et al (2014) The invasion of southern South America by imported bumblebees and associated parasites. J Anim Ecol 83:823–837. https://doi.org/10.1111/1365-2656.12185
Schochet AB, Hung K-LJ, Holway DA (2016) Bumble bee species exhibit divergent responses to urbanisation in a Southern California landscape. Ecol Entomol 41:685–692. https://doi.org/10.1111/een.12343
Scully CA (2010) Landscape composition and forage availability as predictors of bumblebee abundance and species richness in agricultural and forested settings in western Massachusetts. Antioch University New England, Keene
Sgolastra F, Medrzycki P, Bortolotti L et al (2016) Synergistic mortality between a neonicotinoid insecticide and an ergosterol-biosynthesis-inhibiting fungicide in three bee species. Pest Manag Sci 73:1236–1243
Sheffield CS, Rigby SM, Smith RF, Kevan PG (2004) The rare cleptoparasitic bee Epeoloides pilosula (Hymenoptera: Apoidea: Apidae) discovered in Nova Scotia, Canada, with distributional notes. J Kans Entomol Soc 77:161–164. https://doi.org/10.2317/0310.23.1
Sheffield CS, Richardson L, Cannings S et al (2016) Biogeography and designatable units of Bombus occidentalis Greene and B. terricola Kirby (Hymenoptera: Apidae) with implications for conservation status assessments. J Insect Conserv 20:189–199. https://doi.org/10.1007/s10841-016-9853-2
Stanley DA, Garratt MPD, Wickens JB et al (2015) Neonicotinoid pesticide exposure impairs crop pollination services provided by bumblebees. Nature 528:548–550. https://doi.org/10.1038/nature16167
Suzuki-Ohno Y, Yokoyama J, Nakashizuka T, Kawata M (2017) Utilization of photographs taken by citizens for estimating bumblebee distributions. Sci Rep 7:11215. https://doi.org/10.1038/s41598-017-10581-x
Szabo ND, Colla SR, Wagner DL et al (2012) Do pathogen spillover, pesticide use, or habitat loss explain recent North American bumblebee declines? Conserv Lett 5:232–239
Thomson DM (2016) Local bumble bee decline linked to recovery of honey bees, drought effects on floral resources. Ecol Lett 19:1247–1255. https://doi.org/10.1111/ele.12659
Thomson JD, Zung JL (2015) A restraining device to aid identification of bees by digital photography. J Pollinat Ecol 17:145–147
Tucker EM, Rehan SM (2016) Wild bee pollination networks in northern New England. J Insect Conserv 20:325–337
Tucker EM, Rehan SM (2017) High elevation refugia for Bombus terricola (Hymenoptera: Apidae) conservation and wild bees of the White Mountain National Forest. J Insect Sci 17:. https://doi.org/10.1093/jisesa/iew093
USDA NASS (2017) United States Department of Agriculture, National Agricultural Statistics Service 2017 Agricultural Statistics
Vantieghem P, Maes D, Kaiser A, Merckx T (2017) Quality of citizen science data and its consequences for the conservation of skipper butterflies (Hesperiidae) in Flanders (northern Belgium). J Insect Conserv 21:451–463. https://doi.org/10.1007/s10841-016-9924-4
VCGI (2017a) Vermont “hydrologically corrected” digital elevation model (VTHYDRODEM). In: Vt. Cent. Geogr. Inf. VCGI Memb. VT Lidar Initiat. Qual. Level 2 Lidar Hydro Enforced Digit. Elev. Model DEMHE Data 3D Elev. Program 3DEP. http://geodata.vermont.gov/
VCGI (2017b) VT TransRoad_RDS. In: Vt. Cent. Geogr. Inf. Vt. Agency Transp. http://e911.vermont.gov/
Whitehorn PR, O’Connor S, Wackers FL, Goulson D (2012) Neonicotinoid pesticide reduces bumble bee colony growth and queen production. Science 336:351–352. https://doi.org/10.1126/science.1215025
Williams PH (1986) Environmental change and the distributions of British bumble bees (Bombus Latr.). Bee World 67:50–61
Williams P, Osborne J (2009) Bumblebee vulnerability and conservation world-wide. Apidologie 40:367–387. https://doi.org/10.1051/apido/2009025
Williams P (2005) Does specialization explain rarity and decline among British bumblebees? A response to Goulson et al. Biol Conserv 122:33–43. https://doi.org/10.1016/j.biocon.2004.06.019
Williams PH, Araújo MB, Rasmont P (2007) Can vulnerability among British bumblebee (Bombus) species be explained by niche position and breadth? Biol Conserv 138:493–505
Williams P, Colla S, Zhenghua X (2009) Bumblebee vulnerability: common correlates of winners and losers across three continents. Conserv Biol 23:931–940
Williams NM, Regetz J, Kremen C (2011) Landscape-scale resources promote colony growth but not reproductive performance of bumble bees. Ecology 93:1049–1058. https://doi.org/10.1890/11-1006.1
Williams PH, Thorp RW, Richardson LL, Colla SR (2014) Bumble bees of North America: an identification guide. Princeton University Press, Princeton
Winfree R, Aguilar R, Vázquez DP et al (2009) A meta-analysis of bees’ responses to anthropogenic disturbance. Ecology 90:2068–2076. https://doi.org/10.1890/08-1245.1
Winters F (2017) NYS Streets. In: NYS GIS Program. http://gis.ny.gov/gisdata/inventories/details.cfm?DSID=932
Wulder MA, Cranny MM, Hall RJ et al (2008) Satellite land cover mapping of Canada’s forests: the EOSD land cover project
Wyatt JL, Silman MR (2010) Centuries-old logging legacy on spatial and temporal patterns in understory herb communities. For Ecol Manag 260:116–124. https://doi.org/10.1016/j.foreco.2010.04.010
Zeileis A, Wiel MA, Hornik K, Hothorn T (2008) Implementing a class of permutation tests: the coin package. J Stat Softw 28:1–23
Acknowledgements
We thank all of the citizen science volunteers who donated their valuable time that helped to make this project possible on such a large scale. We especially thank interns Larry Clarfeld and Shannon Maes, and field biologists Brendan Collins and Sarah Carline for their countless hours in field and lab. We thank Sam Droege, USGS Patuxent Wildlife Center, for his advice on designing VBBS methods and his encouragement. We are grateful to the many institutions that contributed specimen data to this project, especially the University of Vermont Zadock Thompson Zoological Collection and its curator emeritus, Dr. Ross Bell. This research benefited from the generous financial support from the Binnacle Family Foundation, the Riverledge Foundation, the Vermont Fish and Wildlife Department, and individual donors to the Vermont Center for Ecostudies. L.L. Richardson was partially supported by USDA NIFA Postdoctoral Research Fellowship 2014-01977.
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Richardson, L.L., McFarland, K.P., Zahendra, S. et al. Bumble bee (Bombus) distribution and diversity in Vermont, USA: a century of change. J Insect Conserv 23, 45–62 (2019). https://doi.org/10.1007/s10841-018-0113-5
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DOI: https://doi.org/10.1007/s10841-018-0113-5