Abstract
Wild bees are vital for maintaining biodiversity and food security. However, bees are currently threatened by the conversion of their natural habitat into urban areas, among many other factors. Here, we examine how five wild bee species respond to increasing urbanization according to their functional traits across the most populous city in Canada, which is also the fourth largest in North America. We investigate the effect of urbanization on bee demography and morphology as measured by abundance, sex ratio, body size, and foraging efforts. We found more bees in medium-urbanized sites and larger bees in medium and high-urbanized sites for two species (Eucera pruinosa and Ceratina calcarata). We found higher wing wear in low and medium-urbanization sites. Our data suggests that urbanization potentially affects these wild bee species’ abundance, body size, and foraging efficiency. We further discuss these findings according to the ecology of urbanization and the biology of each species.
Implications for insect conservation Human activity can significantly alter natural habitats, causing adverse effects on wild bees and ultimately affecting their survival. Considering the crucial role bees play in pollinating numerous crop and wild plant species, which, in turn, sustains biodiversity and food security, it is crucial to assess their response to the increasing levels of urbanization.
Similar content being viewed by others
Data Availability
All data are available from the corresponding author upon reasonable request.
References
Abrams J, Eickwort GC (1980) Biology of the communal sweat bee Agapostemon virescens (Hymenoptera: Halictidae) in New York State. Search Agric 1:1
Alcock J, Barrows EM, Gordh G et al (1978) The ecology and evolution of male reproductive behaviour in the bees and wasps. Zool J Linn Soc 64:293–326. https://doi.org/10.1111/j.1096-3642.1978.tb01075.x
Ayers AC, Rehan SM (2021) Supporting bees in cities: how bees are influenced by local and landscape features. Insects 12:128. https://doi.org/10.3390/insects12020128
Ayers AC, Rehan SM (2023) Bee–plant interaction and community response along an urbanization gradient. J Urban Ecol 9(1):juad006. https://doi.org/10.1093/jue/juad006
Banaszak-Cibicka W, Żmihorski M (2012) Wild bees along an urban gradient: winners and losers. J Insect Conserv 16:331–343. https://doi.org/10.1007/s10841-011-9419-2
Banaszak-Cibicka W, Twerd L, Fliszkiewicz M, Giejdasz K, Langowska A (2018) City parks vs natural areas-is it possible to preserve a natural level of bee richness and abundance in a city park? Urban Ecosyst 21:599–613. https://doi.org/10.1007/s11252-018-0756-8
Bendix J, Wiley JJ Jr, Commons MG (2017) Intermediate disturbance and patterns of species richness. Phys Geogr 38(5):393–403. https://doi.org/10.1080/02723646.2017.1327269
Birdshire KR, Carper AL, Briles CE (2020) Bee Community Response to Local and Landscape factors along an urban-rural gradient. Urban Ecosyst 23:689–702. https://doi.org/10.1007/s11252-020-00956-w
Blair RB, Launer AE (1997) Butterfly diversity and human land use: species assemblages along an urban grandient. Biol Conserv 80(1):113–125. https://doi.org/10.1016/S0006-3207(96)00056-0
Brasil SN, Ayers AC, Rehan SM (2023a) The effect of urbanisation and seasonality on wild bee abundance, body size and foraging efforts. Ecol Entomol 48(4):499–507. https://doi.org/10.1111/een.13243
Brasil SN, Khair MM, Ayers AC, Huisken JL, Rehan SM (2023b) Urban landscapes affect wild bee maternal investment and body size. Urban Ecosyst May 30:1–1. https://doi.org/10.1007/s11252-023-01378-0
Brown AM, Warton DI, Andrew NR, Binns M, Cassis G, Gibb H (2014) The fourth-corner solution–using predictive models to understand how species traits interact with the environment. Methods Ecol Evol 5:344–352. https://doi.org/10.1111/2041-210X.12163
Buchholz S, Egerer MH (2020) Functional ecology of wild bees in cities: towards a better understanding of trait-urbanization relationships. Biodivers Conserv 29:2779–2801. https://doi.org/10.1007/s10531-020-02003-8
Cadotte MW, Carscadden K, Mirotchnick N (2011) Beyond species: functional diversity and the maintenance of ecological processes and services. J Appl Ecol 48:1079–1087. https://doi.org/10.1111/j.1365-2664.2011.02048.x
Cameron SA, Lozier JD, Strange JP, Koch JB, Cordes N, Solter LF, Griswold TL (2011) Patterns of widespread decline in North American bumble bees. Proc Natl Acad Sci 108:662–667. https://doi.org/10.1073/pnas.1014743108
Cane JH (1987) Estimation of bee size using intertegular span (Apoidea). J Kansas Entomol Soc 145–147. https://www.jstor.org/stable/25084877
Cane JH, Minckley RL, Kervin LJ, Roulston TAH, Williams NM (2006) Complex responses within a desert bee guild (Hymenoptera: Apiformes) to urban habitat fragmentation. Ecol Appl 16:632–644. https://doi.org/10.1890/1051-0761
Cartar RV (1992) Morphological senescence and longevity: an experiment relating wing wear and life span in foraging wild bumble bees. J Anim Ecol 225–231. https://doi.org/10.2307/5525
Castilla AR, Pope NS, O’Connell M, Rodriguez MF, Treviño L, Santos A, Jha S (2017) Adding landscape genetics and individual traits to the ecosystem function paradigm reveals the importance of species functional breadth. Proceedings of the National Academy of Sciences, 114(48), 12761–12766. https://doi.org/10.1073/pnas.161927111
City of Toronto (2017) Parks plan: 2013–2017 Available at: https://www.torontoca/wp-content/uploads/2017/08/9645-parks-plan-2013-17pdf (Accessed on January 10, 2023)
Cullen N, Xia J, Wei N, Kaczorowski R, Arceo-Gómez G, O’Neill E, Hayes R, Ashman TL (2021) Diversity and composition of pollen loads carried by pollinators are primarily driven by insect traits, not floral community characteristics. Oecologia May 196:131–143. https://doi.org/10.1007/s00442-021-04911-0
Dry S, Legendre P (2008) Testing the species traits–environment relationships: the fourth-corner problem revisited. Ecology 89:400–3412. https://doi.org/10.1890/08-0349.1
Eickwort GC (1981) Aspects of the nesting biology of five nearctic species of Agapostemon (Hymenoptera: Halictidae). J Kansas Entomol Soc 337–351. https://www.jstor.org/stable/25084166
Eickwort GC, Ginsberg HS (1980) Foraging and mating behavior in Apoidea. Ann Rev Entomol 25:21–446. https://doi.org/10.1146/annurev.en.25.010180.002225
Ferrari A, Polidori C (2022) How city traits affect taxonomic and functional diversity of urban wild bee communities: insights from a worldwide analysis. Apidologie 53:46. https://doi.org/10.1007/s13592-022-00950-5
Fisher RA (1930) The genetical theory of natural selection: a complete variorum edition. Oxford University Press
Forrest JR, Thorp RW, Kremen C, Williams NM (2015) Contrasting patterns in species and functional-trait diversity of bees in an agricultural landscape. J Appl Ecol 52:706–715. https://doi.org/10.1111/1365-2664.12433
Fortel L, Henry M, Guilbaud L, Guirao AL et al (2014) Decreasing abundance, increasing diversity and changing structure of the wild bee community (Hymenoptera: Anthophila) along an urbanization gradient. PLoS ONE 9:e104679. https://doi.org/10.1371/journal.pone.0104679
Fortuin CC, Gandhi KJ (2021) Functional traits and nesting habitats distinguish the structure of bee communities in clearcut and managed hardwood & pine forests in Southeastern USA Forest. Ecol Manage 496:119351. https://doi.org/10.1016/j.foreco.2021.119351
Foster DJ, Cartar RV (2011) What causes wing wear in foraging bumble bees? J Exp Biol 214:1896–1901. https://doi.org/10.1242/jeb.051730
Frankie G, Thorp R, Hernandez J et al (2009) Native bees are a rich natural resource in urban California gardens. Calif Agric 63:113–120. https://doi.org/10.3733/ca.v063n03p113
Geslin B, Le Féon V, Folschweiller M et al (2016) The proportion of impervious surfaces at the landscape scale structures wild bee assemblages in a densely populated region. Ecol Evol 6:6599–6615. https://doi.org/10.1002/ece3.2374
Gonsamo A, Chen JM, Wu C (2013) Citizen Science: linking the recent rapid advances of plant flowering in Canada with climate variability. Sci Rep 3:2239. https://doi.org/10.1038/srep02239
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.125595
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
Gunnarsson B, Federsel LM (2014) Bumblebees in the city: abundance, species richness and diversity in two urban habitats. J Insect Conserv Dec 18:1185–1191. https://doi.org/10.1007/s10841-014-9729-2
Hadley AS, Betts MG (2011) The Effects of Landscape Fragmentation on Pollination Dynamics: absence of evidence not evidence of absence. Biol Rev 87:526–544. https://doi.org/10.1111/j.1469-185X.2011.00205.x
Hamblin AL, Youngsteadt E, Frank SD (2018) Wild bee abundance declines with urban warming, regardless of floral density. Urban Ecosyst 21:419–428. https://doi.org/10.1007/s11252-018-0731-4
Hastie T, Tibshirani R, Friedman JH, Friedman JH (2009) The elements of statistical learning: data mining, inference, and prediction. Springer, New York
Hatfield R, Jepsen S, Thorp R, Richardson L, Colla S (2015) Bombus griseocollis. The IUCN Red List of Threatened Species 2015 eT44937645A46440221. https://doi.org/10.2305/IUCN.UK.2015-2.RLTS.T44937645A46440221.en
Hofmann MM, Fleischmann A, Renner SS (2020) Foraging distances in six species of solitary bees with body lengths of 6 to 15 mm, inferred from individual tagging, suggest 150 m-rule-of-thumb for flower strip distances. J Hymenoptera Res Jun 29:77:105–117. https://doi.org/10.3897/jhr.77.51182
Houston A (1985) Central-place foraging: some aspects of prey choice for multiple-prey loaders. Am Nat 125:811–826. https://doi.org/10.1086/284381
Hurd P, Linsley E (1964) The squash and gourd bees genera Peponapis Robertson and Xenoglossa Smith inhabiting America North of Mexico (Hymenoptera: Apoidea). Hilgardia 35:375–477. https://doi.org/10.3733/hilg.v35n15p375
Hurd PD Jr, Linsley EG, Michelbacher AD (1974) Ecology of the squash and gourd bee, Peponapis pruinosa, on cultivated cucurbits in California (Hymenoptera: Apoidea). Smithsonian Institution Press
Janjic J, Packer L (2003) Phylogeny of the bee genus Agapostemon (Hymenoptera: Halictidae). Syst Entomol 28:101–124. https://doi.org/10.1046/j.1365-3113.2003.00204.x
Junker RR, Blüthgen N, Brehm T, Binkenstein J et al (2013) Specialization on traits as basis for the niche-breadth of flower visitors and as structuring mechanism of ecological networks. Funct Ecol 27:329–341. https://doi.org/10.1111/1365-2435.12005
Kim JY (1999) Influence of resource level on maternal investment in a leaf-cutter bee (Hymenoptera: Megachilidae). Behav Ecol 10:552–556. https://doi.org/10.1093/beheco/10.5.552
Land Information Ontario (2019) Ontario Land Cover Compilation v20 Available at: https://www.arcgiscom/home/itemhtml?id=7aa998fdf100434da27a41f1c637382c (Accessed on December 2, 2022)
Lanner J, Kratschmer S, Petrović B, Gaulhofer F, Meimberg H, Pachinger B (2020) City dwelling wild bees: how communal gardens promote species richness. Urban Ecosyst 23:271–288. https://doi.org/10.1007/s11252-019-00902-5
Lawson SP, Ciaccio KN, Rehan SM (2016) Maternal manipulation of pollen provisions affects worker production in a small carpenter bee. Behav Ecol Sociobiol 70:1891–1900. https://doi.org/10.1007/s00265-016-2194-z
Legendre P, Galzin R, Harmelin-Vivien ML (1997) Relating behavior to habitat: solutions to the fourth-corner problem. Ecology 78:547–562. https://doi.org/10.1890/0012-9658
McDonnell MJ, Hahs AK (2008) The use of gradient analysis studies in advancing our understanding of the ecology of urbanizing landscapes: current status and future directions. Landscape Ecol 23:1143–1155. https://doi.org/10.1007/s10980-008-9253-4
McFrederick QS, LeBuhn G (2006) Are urban parks refuges for bumble bees Bombus spp (Hymenoptera: Apidae)? Biol Conserv 129:372–382. https://doi.org/10.1016/j.biocon.2005.11.004
McKinney ML (2002) Urbanization, biodiversity, and conservation: the impacts of urbanization on native species are poorly studied, but educating a highly urbanized human population about these impacts can greatly improve species conservation in all ecosystems. Bioscience 52:883–890. https://doi.org/10.1641/0006-3568
McKinney ML (2008) Effects of urbanization on species richness: a review of plants and animals Urban ecosystems. Jun;11:161 – 76. https://doi.org/10.1007/s11252-007-0045-4
Morales CL, Traveset A (2009) A meta-analysis of impacts of alien vs. native plants on pollinator visitation and reproductive success of co-flowering native plants. Ecol Lett 12:716–728. https://doi.org/10.1111/j.1461-0248.2009.01319.x
Moretti M, De Bello F, Roberts SP, Potts SG (2009) Taxonomical vs functional responses of bee communities to fire in two contrasting climatic regions. J Anim Ecol 98–108. https://www.jstor.org/stable/27696345
Mueller UG, Wolf-Mueller B (1993) A method for estimating the age of bees: Age dependent wing wear and coloration in the wool-carder bee Anthidium manicatum (hymenoptera: Megachilidae). J Insect Behav 6:529–537. https://doi.org/10.1007/BF01049530
Newcomb L (2011) Newcomb’s Wildflower Guide: an ingenious New Key System for Quick, positive field identification of the Wildflowers, flowering shrubs and vines of northeastern and north-central North America. Little, Brown, Boston, MA, pp 1–490
Normandin É, Vereecken NJ, Buddle CM, Fournier V (2017) Taxonomic and functional trait diversity of wild bees in different urban settings. Peer 5:e3051. https://doi.org/10.7717/peerj.3051
O’Connell M, Jordan Z, McGilvra E et al (2021) Reap what you sow: local plant composition mediates bumblebee foraging patterns within urban garden landscapes. Urban Ecosyst 24:391–404. https://doi.org/10.1007/s11252-020-01043-w
Orians GH, Pearson NE (1979) On the theory of central place foraging. In: Horn DJ et al (eds) Analysis of ecological systems, vol 2. The Ohio State University Press, Columbus, pp 154–177
Osborne JL, Martin AP, Shortall CR et al (2008) Quantifying and comparing bumblebee nest densities in gardens and countryside habitats. J Appl Ecol 45:784–792. https://doi.org/10.1111/j.1365-2664.2007.01359.x
Peterson JH, Roitberg BD (2006) Impact of resource levels on sex ratio and resource allocation in the solitary bee, Megachile rotundata. Environmental Entomology. Oct 1;35(5):1404-10. https://doi.org/10.1093/ee/35.5.1404
Pope NS, Jha S (2018) Seasonal food scarcity prompts long-distance foraging by a wild social bee. Am Nat 191:45–57. https://doi.org/10.5061/dryad.c6j8p
Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25(6):345–353. https://doi.org/10.1016/j.tree.2010.01.007
Potts S, Imperatriz-Fonseca V, Ngo H et al (2016) Safeguarding pollinators and their values to human well-being. Nature 540:220–229. https://doi.org/10.1038/nature20588
Ratnieks FL (2000) How far do bees’ forage. Bee Improv 6:10–11
Rebele F (1994) Urban ecology and special features of urban ecosystems. Glob Ecol Biogeogr Lett 4(6):173–187. https://doi.org/10.2307/2997649
Rehan SM (2020) Small carpenter bees (Ceratina). In: Stark C (ed) Encyclopedia of social insects. Springer. https://doi.org/10.1007/978-3-319-90306-4_106-1
Rehan SM, Richards MH (2010) Nesting biology and subsociality in Ceratina calcarata (Hymenoptera: Apidae). Can Entomol 142(1):65–74. https://doi.org/10.4039/n09-056
Roberts RB (1969) Biology of the bee genus Agapostemon (Hymenoptera: Halictidae). The University of Kansas Science Bulletin, 48:689. https://digitalcommons.usu.edu/bee_lab_all/22
Sarkar D, Sarkar MD, KernSmooth S (2015) Package ‘lattice’ Version 0.20, 33
Seto KC, Güneralp B, Hutyra LR (2012) Global forecasts of urban expansion to 2030 and direct impacts on biodiversity and carbon pools. Proceedings of the National Academy of Sciences 109:16083–16088. https://doi.org/10.1073/pnas.12116581
Shell WA, Rehan SM (2018) Behavioral and genetic mechanisms of social evolution: insights from incipiently and facultatively social bees. Apidologie 49:13–30. https://doi.org/10.1007/s13592-017-0527-1
Statistics Canada (2021) Toronto [Census subdivision], Ontario Census Profile 2021 Census Statistics Canada Catalogue no 98-316-X2021001 Ottawa Released February 9, 2022 https://rb.gy/ae5upv (accessed on February 4, 2023)
Steffan-Dewenter I, Münzenberg U, Bürger C, Thies C, Tscharntke T (2002) Scale-dependent effects of landscape context on three pollinator guilds. Ecology 83:1421–1432. https://doi.org/10.1890/0012-9658
Stenhouse RN (2004) Fragmentation and internal disturbance of native vegetation reserves in the Perth metropolitan area, western Australia. Landsc Urban Plan 68:389–401. https://doi.org/10.1016/S0169-2046(03)00151-8
Tepedino VJ (1981) The pollination efficiency of the squash bee (Peponapis pruinosa) and the honey bee (Apis mellifera) on summer squash (Cucurbita pepo). J Kansas Entomol Soc 359–377. https://www.jstor.org/stable/25084168
Tepedino VJ, Torchio PF (1982) Phenotypic variability in nesting success among Osmia lignaria propinqua females in a glasshouse environment: (Hymenoptera: Megachilidae). Ecol Entomol 7:453–462. https://doi.org/10.1111/j.1365-2311.1982.tb00688.x
Theodorou P, Radzevičiūtė R, Lentendu G et al (2020) Urban areas as hotspots for bees and pollination but not a panacea for all insects. Nat Commun 11:576. https://doi.org/10.1038/s41467-020-14496-6
Thompson K, Austin KC, Smith RM et al (2003) Urban domestic gardens (I): putting small-scale plant diversity in context. J Veg Sci 14:71–78. https://doi.org/10.1111/j.1654-1103.2003.tb02129.x
Threlfall CG, Walker K, Williams NSG, Hahs AK, Mata L, Stork N, Livesley SJ (2015) The conservation value of urban green space habitats for Australian native bee communities. Biol Conserv 187:240–248. https://doi.org/10.1016/j.biocon.2015.05.003
Vaz E, Arsanjani JJ (2015) Predicting urban growth of the greater Toronto area-coupling a Markov cellular automata with document meta-analysis. J Environ Inform 25(2):71–80. https://doi.org/10.3808/jei.201500299
Twerd L, Banaszak-Cibicka W (2019) Wastelands: their attractiveness and importance for preserving the diversity of wild bees in urban areas. J Insect Conserv 23:573–588. https://doi.org/10.1007/s10841-019-00148-8
Wang YI, Naumann U, Wright ST, Warton DI (2012) Mvabund–an R package for model-based analysis of multivariate abundance data. Methods Ecol Evol 3:471–474. https://doi.org/10.1111/j.2041-210X.2012.00190.x
Warzecha D, Diekötter T, Wolters V, Jauker F (2016) Intraspecific body size increases with habitat fragmentation in wild bee pollinators. Landsc Ecol Sep 31:1449–1455. https://doi.org/10.1007/s10980-016-0349-y
Williams PH, Thorp RW, Richardson LL, Colla SR (2014) Bumble bees of north America. Bumble Bees of North America. Princeton University Press. https://doi.org/10.1515/9781400851188
Wilson CJ, Jamieson MA (2019) The effects of urbanization on bee communities depends on floral resource availability and bee functional traits. PLoS ONE 14:e0225852. https://doi.org/10.1371/journal.pone.0225852
Yan Z, Teng M, He W, Liu A, Li Y, Wang P (2019) Impervious surface area is a key predictor for urban plant diversity in a city undergone rapid urbanization. Sci Total Environ 650:335–342. https://doi.org/10.1016/j.scitotenv.2018.09.025
Zurbuchen A, Cheesman S, Klaiber J, Müller A, Hein S, Dorn S (2010) Long foraging distances impose high costs on offspring production in solitary bees. J Anim Ecol 79:674–681. https://doi.org/10.1111/j.1365-2656.2010.01675.x
Acknowledgements
We thank members of the Rehan lab for helpful feedback on earlier versions of this work. Thanks to Anthony Ayers, Caitlin Corso, Merna Khair, and Olivia LePiane and for field collections and specimen processing. Funding for this study was provided by NSERC Discovery grants, supplements, and an E.W.R. Steacie Memorial Fellowship to SMR.
Funding
Funding for this study was provided by NSERC Discovery grants, supplements, and an E.W.R. Steacie Memorial Fellowship to SMR.
Author information
Authors and Affiliations
Contributions
SNRB, MG and SMR performed data analysis. SNRB and SMR wrote the manuscript. SMR conceived and funded the study. All authors edited and approved the final manuscript.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Ethical approval
Not applicable.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Brasil, S.N.R., George, M. & Rehan, S.M. Functional traits of wild bees in response to urbanization. J Insect Conserv 28, 127–139 (2024). https://doi.org/10.1007/s10841-023-00528-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10841-023-00528-1