Urban Ecosystems

, Volume 21, Issue 3, pp 419–428 | Cite as

Wild bee abundance declines with urban warming, regardless of floral density

  • April L. Hamblin
  • Elsa YoungsteadtEmail author
  • Steven D. Frank


As cities expand, conservation of beneficial insects is essential to maintaining robust urban ecosystem services such as pollination. Urban warming alters insect physiology, fitness, and abundance, but the effect of urban warming on pollinator communities has not been investigated. We sampled bees at 18 sites encompassing an urban warming mosaic within Raleigh, NC, USA. We quantified habitat variables at all sites by measuring air temperature, percent impervious surface (on local and landscape scales), floral density, and floral diversity. We tested the hypothesis that urban bee community structure depends on temperature. We also conducted model selection to determine whether temperature was among the most important predictors of urban bee community structure. Finally, we asked whether bee responses to temperature or impervious surface depended on bee functional traits. Bee abundance declined by about 41% per °C urban warming, and temperature was among the best predictors of bee abundance and community composition. Local impervious surface and floral density were also important predictors of bee abundance, although only large bees appeared to benefit from high floral density. Bee species richness increased with floral density regardless of bee size, and bee responses to urban habitat variables were independent of other life-history traits. Although we document benefits of high floral density, simply adding flowers to otherwise hot, impervious sites is unlikely to restore the entire urban pollinator community since floral resources benefit large bees more than small bees.


Bee Impervious surface Pollinator decline Pollinator Urban heat island Urban warming 



We thank Holly Menninger; Sally Thigpen; the City of Raleigh Department of Parks, Recreation, and Cultural Resources; and volunteer homeowners who helped us find study sites and let us conduct research on their property. John Ascher, Adrian Carper, Sheila Colla, Sam Droege, Joel Gardner, Jason Gibbs, and Leif Richardson shared their knowledge of bee life history and nesting. Sam Droege and Jason Gibbs identified bee specimens. Nicole Bissonnette, Bobby Chanthammavong, Catherine Croft, Laura Daly, Samantha Dietz, Karly Dugan, Morgan Duncan, Anna Holmquist, and Danielle Schmidt assisted with specimen collection, bee measurements, and database management. Laura Daly identified plants. This study was funded by an Agriculture and Food Research Initiative Competitive Grant (2013-02476) from the USDA National Institute of Food and Agriculture to SDF and EY. This work was also funded by Cooperative Agreement No. G11 AC20471, G13 AC00405, and G15AP00153 from the United States Geological Survey to SDF. Its contents are solely the responsibility of the authors and do not necessarily represent the views of the Department of the Interior Southeast Climate Science Center or the USGS. This manuscript is submitted for publication with the understanding that the United States Government is authorized to reproduce and distribute reprints for Governmental purposes. North Carolina State University Department of Entomology also contributed support for this research.

Authors’ contributions

ALH and SDF conceived the ideas and designed methodology; ALH collected the data; ALH and EY analyzed the data; ALH and EY led the writing of the manuscript. All authors contributed critically to the drafts and gave final approval for publication.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

11252_2018_731_MOESM1_ESM.docx (1.6 mb)
ESM 1 (DOCX 1612 kb)


  1. Angilletta MJ, Wilson RS, Niehaus AC, Sears MW, Navas CA, Ribeiro PL (2007) Urban physiology: city ants possess high heat tolerance. PLoS One 2(2):e258. CrossRefPubMedPubMedCentralGoogle Scholar
  2. Ascher JS, Pickering J (2014) discover life bee species guide and world checklist (hymenoptera: Apoidea: Anthophila) (draft 39, April 22, 2014).
  3. Baldock KC et al (2015) Where is the UK's pollinator biodiversity? The importance of urban areas for flower-visiting insects. Proc R Soc B 282(1803):20142849. CrossRefPubMedGoogle Scholar
  4. Banaszak-Cibicka W, Żmihorski M (2012) Wild bees along an urban gradient: winners and losers. J Insect Conserv 16(3):331–343. CrossRefGoogle Scholar
  5. Bartomeus I, Ascher JS, Gibbs J, Danforth BN, Wagner DL, Hedtke SM, Winfree R (2013) Historical changes in northeastern US bee pollinators related to shared ecological traits. Proc Natl Acad Sci U S A 110(12):4656–4660. CrossRefPubMedPubMedCentralGoogle Scholar
  6. Barton K (2016) MuMIn: Multi-Model Inference,
  7. Bates AJ, Sadler JP, Fairbrass AJ, Falk SJ, Hale JD, Matthews TJ (2011) Changing bee and hoverfly pollinator assemblages along an urban-rural gradient. PLoS One 6(8):e23459. CrossRefPubMedPubMedCentralGoogle Scholar
  8. Benjamin FE, Reilly JR, Winfree R (2014) Pollinator body size mediates the scale at which land use drives crop pollination services. J Appl Ecol 51(2):440–449. CrossRefGoogle Scholar
  9. Cane JH (1987) Estimation of bee size using intertegular span (Apoidea). J Kans Entomol Soc:145–147Google Scholar
  10. Cane JH, Minckley RL, Kervin LJ, Williams NM (2006) Complex responses within a desert bee guild (hymenoptera: Apiformes) to urban habitat fragmentation. Ecol Appl 16(2):632–644.Google Scholar
  11. Carper AL, Adler LS, Warren PS, Irwin RE (2014) Effects of suburbanization on forest bee communities. Environ Entomol 43(2):253–262. CrossRefPubMedGoogle Scholar
  12. Civerolo K, Hogrefe C, Lynn B, Rosenthal J, Ku JY, Solecki W, Cox J, Small C, Rosenzweig C, Goldberg R, Knowlton K, Kinney P (2007) Estimating the effects of increased urbanization on surface meteorology and ozone concentrations in the new York City metropolitan region. Atmos Environ 41(9):1803–1818. CrossRefGoogle Scholar
  13. Colinet H, Sinclair BJ, Vernon P, Renault D (2015) Insects in fluctuating thermal environments. Annu Rev Entomol 60(1):123–140. CrossRefPubMedGoogle Scholar
  14. Dale AG, Frank SD (2014) Urban warming trumps natural enemy regulation of herbivorous pests. Ecol Appl 24(7):1596–1607. CrossRefPubMedGoogle Scholar
  15. Dormann CF, Elith J, Bacher S, Buchmann C, Carl G, Carré G, Marquéz JRG, Gruber B, Lafourcade B, Leitão PJ, Münkemüller T, McClean C, Osborne PE, Reineking B, Schröder B, Skidmore AK, Zurell D, Lautenbach S (2013) Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography 36(1):27–46. CrossRefGoogle Scholar
  16. Droege S, Tepedino VJ, Lebuhn G, Link W, Minckley RL, Chen Q, Conrad C (2010) Spatial patterns of bee captures in north American bowl trapping surveys. Insect Conserv Divers 3(1):15–23. CrossRefGoogle Scholar
  17. Fortel L, Henry M, Guilbaud L, Al G, Kuhlmann M, Mouret H, Rollin O, Vaissière BE (2014) Decreasing abundance, increasing diversity and changing structure of the wild bee community (hymenoptera: Anthophila) along an urbanization gradient. PLoS One 9(8):e104679. CrossRefPubMedPubMedCentralGoogle Scholar
  18. Fründ J, Zieger SL, Tscharntke T (2013) Response diversity of wild bees to overwintering temperatures. Oecologia 173(4):1639–1648. CrossRefPubMedGoogle Scholar
  19. Geslin B, le Féon V, Folschweiller M, Flacher F, Carmignac D, Motard E, Perret S, Dajoz I (2016) The proportion of impervious surfaces at the landscape scale structures wild bee assemblages in a densely populated region. Ecol Evol 6(18):6599–6615. CrossRefPubMedPubMedCentralGoogle Scholar
  20. Gibbs J (2011) Revision of the metallic Lasioglossum (Dialictus) of eastern North America (hymenoptera: Halictidae: Halictini). Zootaxa 3073:1–216Google Scholar
  21. Gotelli N, Chao A (2013) Measuring and estimating species richness, species diversity, and biotic similarity from sampling data. Enc Biodivers 5:195–211CrossRefGoogle Scholar
  22. Greenleaf SS, Williams NM, Winfree R, Kremen C (2007) Bee foraging ranges and their relationship to body size. Oecologia 153(3):589–596. CrossRefPubMedGoogle Scholar
  23. Hall DM et al (2016) The city as a refuge for insect pollinators. Conserv Biol 31:4–29Google Scholar
  24. Hsieh T, Ma K, Chao A (2016) iNEXT: an R package for rarefaction and extrapolation of species diversity (hill numbers). Methods Ecol Evol 7:1451–1456CrossRefGoogle Scholar
  25. Hubbart JA (2011) An inexpensive alternative solar radiation shield for ambient air temperature and relative humidity micro-sensors. J Nat Env Sci 2:9–14Google Scholar
  26. Hunter MR, Hunter MD (2008) Designing for conservation of insects in the built environment. Insect Conserv Divers 1:189–196Google Scholar
  27. Jin S, Yang L, Danielson P, Homer C, Fry J, Xian G (2013) A comprehensive change detection method for updating the National Land Cover Database to circa 2011. Remote Sens Environ 132:159–175. CrossRefGoogle Scholar
  28. Kaye J et al (2008) Hierarchical Bayesian scaling of soil properties across urban, agricultural, and desert ecosystems. Ecol Appl 18(1):132–145. CrossRefPubMedGoogle Scholar
  29. Kearns CA, Oliveras DM (2009) Environmental factors affecting bee diversity in urban and remote grassland plots in boulder, Colorado. J Insect Conserv 13(6):655–665. CrossRefGoogle Scholar
  30. Kerr JT, Pindar A, Galpern P, Packer L, Potts SG, Roberts SM, Rasmont P, Schweiger O, Colla SR, Richardson LL, Wagner DL, Gall LF, Sikes DS, Pantoja A (2015) Climate change impacts on bumblebees converge across continents. Science 349(6244):177–180. CrossRefPubMedGoogle Scholar
  31. Kühsel S, Blüthgen N (2015) High diversity stabilizes the thermal resilience of pollinator communities in intensively managed grasslands. Nat Commun 6:7989. CrossRefPubMedPubMedCentralGoogle Scholar
  32. Legendre P, Legendre L (2012) Numerical Ecology. Elsevier, AmsterdamGoogle Scholar
  33. Lowenstein DM, Matteson KC, Xiao I, Silva AM, Minor ES (2014) Humans, bees, and pollination services in the city: the case of Chicago, IL (USA). Biodivers Conserv 23(11):2857–2874. CrossRefGoogle Scholar
  34. Matteson KC, Ascher JS, Langellotto GA (2008) Bee richness and abundance in new York City urban gardens. Ann Entomol Soc Am 101(1):140–150.Google Scholar
  35. McCune B, Grace JB, Urban DL (2002) Analysis of ecological communities. MjM Software Design, Gleneden BeachGoogle Scholar
  36. Meineke EK, Dunn RR, Sexton JO, Frank SD (2013) Urban warming drives insect pest abundance on street trees. PLoS One 8(3):e59687. CrossRefPubMedPubMedCentralGoogle Scholar
  37. Meineke EK, Dunn RR, Frank SD (2014) Early pest development and loss of biological control are associated with urban warming. Biol Lett 10(11):20140586. CrossRefPubMedPubMedCentralGoogle Scholar
  38. Meineke E, Youngsteadt E, Dunn RR, Frank SD (2016) Urban warming reduces aboveground carbon storage. Proc R Soc B 283(1840):20161574. CrossRefPubMedGoogle Scholar
  39. Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol Evol 4(2):133–142. CrossRefGoogle Scholar
  40. New TR (2015) Insect conservation and urban environments. Springer, New York. CrossRefGoogle Scholar
  41. Nooten SS, Andrew NR, Hughes L (2014) Potential impacts of climate change on insect communities: a transplant experiment. PLoS One 9(1):e85987. CrossRefPubMedPubMedCentralGoogle Scholar
  42. Oke TR (1973) City size and urban heat island. Atmos Environ 7(8):769–779. CrossRefGoogle Scholar
  43. Oksanen J et al. (2016) Vegan: community ecology package. R package version 2.4–1. Available at:
  44. Oyen KJ, Giri S, Dillon ME (2016) Altitudinal variation in bumble bee (Bombus) critical thermal limits. J Therm Biol 59:52–57CrossRefPubMedGoogle Scholar
  45. Pinheiro J, Bates D, DebRoy S, Sarkar D (2016) nlme: Linear and Nonlinear Mixed Effects Models. R package version 3.1–128. Available at:
  46. Popic TJ, Davila YC, Wardle GM (2013) Evaluation of common methods for sampling invertebrate pollinator assemblages: net sampling out-perform pan traps. PLoS One 8:e66665, 6, DOI:
  47. Potts SG, Vulliamy B, Dafni A, Ne'eman G, Willmer P (2003) Linking bees and flowers: how do floral communities structure pollinator communities? Ecology 84(10):2628–2642. CrossRefGoogle Scholar
  48. Quistberg RD, Bichier P, Philpott SM (2016) Landscape and local correlates of bee abundance and species richness in urban gardens. Environ Entomol 45:592–601CrossRefGoogle Scholar
  49. R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  50. Rader R, Reilly J, Bartomeus I, Winfree R (2013) Native bees buffer the negative impact of climate warming on honey bee pollination of watermelon crops. Glob Chang Biol 19(10):3103–3110. CrossRefPubMedGoogle Scholar
  51. Roulston TH, Goodell K (2011) The role of resources and risks in regulating wild bee populations. Annu Rev Entomol 56(1):293–312. CrossRefPubMedGoogle Scholar
  52. Scaven VL, Rafferty NE (2013) Physiological effects of climate warming on flowering plants and insect pollinators and potential consequences for their interactions. Curr Zool 59(3):418–426. CrossRefPubMedPubMedCentralGoogle Scholar
  53. Seto KC, Guneralp B, Hutyra LR (2012) Global forecasts of urban expansion to 2030 and direct impacts on biodiversity and carbon pools. Proc Natl Acad Sci U S A 109(40):16083–16088. CrossRefPubMedPubMedCentralGoogle Scholar
  54. Sheffield CS, Pindar A, Packer L, Kevan PG (2013) The potential of cleptoparasitic bees as indicator taxa for assessing bee communities. Apidologie 44(5):501–510. CrossRefGoogle Scholar
  55. Stephen WP, Rao S (2007) Sampling native bees in proximity to a highly competitive food resource (hymenoptera: Apiformes). J Kans Entomol Soc 80(4):369–376.Google Scholar
  56. Symonds MR, Moussalli A (2011) A brief guide to model selection, multimodel inference and model averaging in behavioural ecology using Akaike's information criterion. Behav Ecol Sociobiol 65(1):13–21. CrossRefGoogle Scholar
  57. Winfree R, Bartomeus I, Cariveau DP (2011) Native pollinators in anthropogenic habitats. Annu rev Ecol. Evol Syst 42:1CrossRefGoogle Scholar
  58. Youngsteadt E, Ernst AF, Dunn RR, Frank SD (2016) Responses of arthropod populations to warming depend on latitude: evidence from urban heat islands. Glob Change Biol 23(4):1436–1447. CrossRefGoogle Scholar
  59. Yuan F, Bauer ME (2007) Comparison of impervious surface area and normalized difference vegetation index as indicators of surface urban heat island effects in Landsat imagery. Remote Sens Environ 106(3):375–386. CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • April L. Hamblin
  • Elsa Youngsteadt
    • 1
    Email author
  • Steven D. Frank
    • 1
  1. 1.Department of Entomology & Plant PathologyNorth Carolina State UniversityRaleighUSA

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