Wild bee abundance declines with urban warming, regardless of floral density
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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.
KeywordsBee 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.
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.
- Ascher JS, Pickering J (2014) discover life bee species guide and world checklist (hymenoptera: Apoidea: Anthophila) (draft 39, April 22, 2014). http://www.discoverlife.org/mp/20q?guide=Apoidea_species
- 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. https://doi.org/10.1073/pnas.1218503110 CrossRefPubMedPubMedCentralGoogle Scholar
- Barton K (2016) MuMIn: Multi-Model Inference, https://cran.r-project.org/package=MuMIn
- Cane JH (1987) Estimation of bee size using intertegular span (Apoidea). J Kans Entomol Soc:145–147Google Scholar
- 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
- 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. https://doi.org/10.1016/j.atmosenv.2006.10.076 CrossRefGoogle Scholar
- Colinet H, Sinclair BJ, Vernon P, Renault D (2015) Insects in fluctuating thermal environments. Annu Rev Entomol 60(1):123–140. https://doi.org/10.1146/annurev-ento-010814-021017 CrossRefPubMedGoogle Scholar
- 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. https://doi.org/10.1111/j.1600-0587.2012.07348.x CrossRefGoogle Scholar
- 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. https://doi.org/10.1371/journal.pone.0104679 CrossRefPubMedPubMedCentralGoogle Scholar
- 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. https://doi.org/10.1002/ece3.2374 CrossRefPubMedPubMedCentralGoogle Scholar
- Gibbs J (2011) Revision of the metallic Lasioglossum (Dialictus) of eastern North America (hymenoptera: Halictidae: Halictini). Zootaxa 3073:1–216Google Scholar
- Hall DM et al (2016) The city as a refuge for insect pollinators. Conserv Biol 31:4–29Google Scholar
- 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
- Hunter MR, Hunter MD (2008) Designing for conservation of insects in the built environment. Insect Conserv Divers 1:189–196Google Scholar
- 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. https://doi.org/10.1126/science.aaa7031 CrossRefPubMedGoogle Scholar
- Legendre P, Legendre L (2012) Numerical Ecology. Elsevier, AmsterdamGoogle Scholar
- 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
- McCune B, Grace JB, Urban DL (2002) Analysis of ecological communities. MjM Software Design, Gleneden BeachGoogle Scholar
- Oksanen J et al. (2016) Vegan: community ecology package. R package version 2.4–1. Available at: CRAN.R-project.org/package=vegan
- Pinheiro J, Bates D, DebRoy S, Sarkar D (2016) nlme: Linear and Nonlinear Mixed Effects Models. R package version 3.1–128. Available at: CRAN.R-project.org/package=nlme
- 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: https://doi.org/10.1371/journal.pone.0066665
- R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
- Roulston TH, Goodell K (2011) The role of resources and risks in regulating wild bee populations. Annu Rev Entomol 56(1):293–312. https://doi.org/10.1146/annurev-ento-120709-144802 CrossRefPubMedGoogle Scholar
- 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