Abstract
The role of urban expansion on bee diversity is poorly understood, but it may play an important role in restructuring pollinator diversity observed in rural regions at the urban perimeter. We studied bee communities in two habitats essential for pollinators (residential gardens and semi-natural areas) at 42 sites situated at the edge of greater Montreal, Canada. Bee species richness, abundance and functional diversity all increased with urbanization in both habitat types, but gardens and semi-natural areas supported distinct bee communities with unique responses to urbanization in terms of species turnover. Compared to semi-natural sites, residential gardens supported bees that foraged from a greater number but a lower proportion of available plant species. Bees did not discriminate between exotic and indigenous plant species in either gardens or semi-natural sites and were attracted to flowers in either habitat irrespective of their origins. Protecting semi-natural ruderal areas and providing residential garden habitats for pollinators are both effective means of promoting regional bee diversity in urbanizing regions.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Ahrne K, Bengtsson J, Elmqvist T (2009) Bumble bees (Bombus spp) along a gradient of increasing urbanization. PLoS One 4:e5574. doi:10.1371/journal.pone.0005574
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 282:20142849. doi:10.1098/rspb.2014.2849
Banaszak-Cibicka W (2014) Are urban areas suitable for thermophilic and xerothermic bee species (Hymenoptera: Apoidea: Apiformes)? Apidologie 45:145–155. doi:10.1007/s13592-013-0232-7
Banaszak-Cibicka W, Żmihorski M (2012) Wild bees along an urban gradient: winners and losers. J Insect Conserv 16:331–343. doi:10.1007/s10841-011-9419-2
Banaszak-Cibicka W, Ratyńska H, Dylewski Ł (2016) Features of urban green space favourable for large and diverse bee populations (Hymenoptera: Apoidea: Apiformes). Urban For Urban Green 20:448–452. doi:10.1016/j.ufug.2016.10.015
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. P Natl A Sci 110:4656–4660. doi:10.1073/pnas.1218503110
Bartoń K (2014) MuMIn: multi-model inference. R package version 1.10.5. http://CRAN.R-project.org/package=MuMIn
Bascompte J, Jordano P, Olesen JM (2006) Asymmetric coevolutionary networks facilitate biodiversity maintenance. Science 312:431–433. doi:10.1126/science.1123412
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:e23459. doi:10.1371/journal.pone.0023459
Bates D, Mächler M, Bolker B, Walker S (2014) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. doi:10.18637/jss.v067.i01
Blüthgen N, Menzel F, Blüthgen N (2006) Measuring specialization in species interaction networks. BMC Ecol 6:9. doi:10.1186/1472-6785-6-9
Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, White J-SS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135. doi:10.1016/j.tree.2008.10.008
Borcard D, Legendre P (2002) All-scale spatial analysis of ecological data by means of principal coordinates of neighbour matrices. Ecol Model 153:51–68. doi:10.1016/S0304-3800(01)00501-4
Botías C, David A, Hill EM, Goulson D (2017) Quantifying exposure of wild bumblebees to mixtures of agrochemicals in agricultural and urban landscapes. Environ Pollut 222:73–82. doi:10.1016/j.envpol.2017.01.001
Cane JH, Minckley RL, Kervin LJ, Williams NM (2006) Complex responses within a desert bee guild (Hymenoptera: Apiformes) to urban habitat fragmentation. Ecol Appl 16:632–644. doi:10.1890/1051-0761(2006)016[0632:CRWADB]2.0.CO;2
Cariveau DP, Winfree R (2015) Causes of variation in wild bee responses to anthropogenic drivers. Curr Opin Insect Sci 10:104–109. doi:10.1016/j.cois.2015.05.004
Carper AL, Adler LS, Warren PS, Irwin RE (2014) Effects of suburbanization on forest bee communities. Environ Entomol 43:253–262. doi:10.1603/EN13078
Carré G et al (2009) Landscape context and habitat type as drivers of bee diversity in European annual crops. Agric Ecosyst Environ 133:40–47. doi:10.1016/j.agee.2009.05.001
Carvalheiro LG et al (2013) Species richness declines and biotic homogenisation have slowed down for NW-European pollinators and plants. Ecol Lett 16:870–878. doi:10.1111/ele.12121
Chao A, Gotelli NJ, Hsieh T, Sander EL, Ma K, Colwell RK, Ellison AM (2014) Rarefaction and extrapolation with hill numbers: a framework for sampling and estimation in species diversity studies. Ecol Monogr 84:45–67. doi:10.1890/13-0133.1
Chrobock T, Winiger P, Fischer M, van Kleunen M (2013) The cobblers stick to their lasts: pollinators prefer native over alien plant species in a multi-species experiment. Biol Invasions 15:2577–2588. doi:10.1007/s10530-013-0474-3
Dicks L, Corbet S, Pywell R (2002) Compartmentalization in plant–insect flower visitor webs. J Anim Ecol 71:32–43. doi:10.1046/j.0021-8790.2001.00572.x
Dormann CF, Fründ J, Blüthgen N, Gruber B (2009) Indices, graphs and null models: analyzing bipartite ecological networks. Open Ecol J 2:7–24. doi:10.2174/1874213000902010007
Fetridge ED, Ascher JS, Langellotto GA (2008) The bee fauna of residential gardens in a suburb of new York City (Hymenoptera: Apoidea). Ann Entomol Soc Am 101:1067–1077. doi:10.1603/0013-8746-101.6.1067
Fortel L 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. doi:10.1371/journal.pone.0104679
Frankie GW, Thorp RW, Schindler M, Hernandez J, Ertter B, Rizzardi M (2005) Ecological patterns of bees and their host ornamental flowers in two northern California cities. J Kansas Entomol Soc 78:227–246. doi:10.2317/0407.08.1
Fründ J, Linsenmair KE, Blüthgen N (2010) Pollinator diversity and specialization in relation to flower diversity. Oikos 119:1581–1590. doi:10.1111/j.1600-0706.2010.18450.x
Fukase J, Simons A (2016) Increased pollinator activity in urban gardens with more native flora. Appl Ecol Env Res 14:297–310. doi:10.15666/aeer/1401_297310
Garbuzov M, Schürch R, Ratnieks FLW (2015) Eating locally: dance decoding demonstrates that urban honey bees in Brighton, UK, forage mainly in the surrounding urban area. Urban Ecosyst 18:411–418. doi:10.1007/s11252-014-0403-y
Gardiner MM, Burkman CE, Prajzner SP (2013) The value of urban vacant land to support arthropod biodiversity and ecosystem services. Environ Entomol 42:1123–1136. doi:10.1603/EN12275
Geroff RK, Gibbs J, McCravy KW (2014) Assessing bee (Hymenoptera: Apoidea) diversity of an Illinois restored tallgrass prairie: methodology and conservation considerations. J Insect Conserv 18:951–964. doi:10.1007/s10841-014-9703-z
Geslin B, Gauzens B, Thébault E, Dajoz I (2013) Plant pollinator networks along a gradient of urbanisation. PLoS One 8:e63421. doi:10.1371/journal.pone.0063421
Geslin B 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. doi:10.1002/ece3.2374
Gibbs J (2010) Revision of the metallic species of Lasioglossum (Dialictus) in Canada (Hymenoptera, Halictidae, Halictini). Zootaxa 2591:1–382
Gittleman JL, Kot M (1990) Adaptation: statistics and a null model for estimating phylogenetic effects. Syst Biol 39:227–241. doi:10.2307/2992183
González-Varo JP et al (2013) Combined effects of global change pressures on animal-mediated pollination. Trends Ecol Evol 28:524–530. doi:10.1016/j.tree.2013.05.008
Goulson D, Sparrow KR (2009) Evidence for competition between honeybees and bumblebees; effects on bumblebee worker size. J Insect Conserv 13:177–181. doi:10.1007/s10841-008-9140-y
Goulson D, Lye GC, Darvill B (2008) Decline and conservation of bumble bees. Annu Rev Entomol 53:191–208. doi:10.1146/annurev.ento.53.103106.093454
Goulson D et al (2010) Effects of land use at a landscape scale on bumblebee nest density and survival. J Appl Ecol 47:1207–1215. doi:10.1111/j.1365-2664.2010.01872.x
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. doi:10.1126/science.1255957
Greenleaf SS, Williams NM, Winfree R, Kremen C (2007) Bee foraging ranges and their relationship to body size. Oecologia 153:589–596. doi:10.1007/s00442-007-0752-9
Hall DM et al (2017) The city as a refuge for insect pollinators. Conserv Biol. doi:10.1111/cobi.12840
Hanley ME, Awbi AJ, Franco M (2014) Going native? Flower use by bumblebees in English urban gardens. Ann Bot-London 113:799–806. doi:10.1093/aob/mcu006
Hennig EI, Ghazoul J (2012) Pollinating animals in the urban environment. Urban Ecosyst 15:149–166. doi:10.1007/s11252-011-0202-7
Herbertsson L, Lindström SAM, Rundlöf M, Bommarco R, Smith HG (2016) Competition between managed honeybees and wild bumblebees depends on landscape context. Basic Appl Ecol 17:609–616. doi:10.1016/j.baae.2016.05.001
Hudewenz A, Klein AM (2015) Red mason bees cannot compete with honey bees for floral resources in a cage experiment. Ecol Evol 5:5049–5056. doi:10.1002/ece3.1762
Jha S, Kremen C (2013) Urban land use limits regional bumble bee gene flow. Mol Ecol 22:2483–2495. doi:10.1111/mec.12275
Johnson JB, Omland KS (2004) Model selection in ecology and evolution. Trends Ecol Evol 19:101–108. doi:10.1016/j.tree.2003.10.013
Jordano P, Bascompte J, Olesen JM (2003) Invariant properties in coevolutionary networks of plant–animal interactions. Ecol Lett 6:69–81. doi:10.1046/j.1461-0248.2003.00403.x
Kaluza BF, Wallace H, Heard TA, Klein AM, Leonhardt SD (2016) Urban gardens promote bee foraging over natural habitats and plantations. Ecol Evol 6:1304–1316. doi:10.1002/ece3.1941
Kennedy CM et al (2013) A global quantitative synthesis of local and landscape effects on wild bee pollinators in agroecosystems. Ecol Lett 16:584–599. doi:10.1111/ele.12082
Kwaiser KS, Hendrix SD (2008) Diversity and abundance of bees (Hymenoptera: Apiformes) in native and ruderal grasslands of agriculturally dominated landscapes. Agric Ecosyst Environ 124:200–204. doi:10.1016/j.agee.2007.09.012
Laliberté E, Legendre P (2010) A distance-based framework for measuring functional diversity from multiple traits. Ecology 91:299–305. doi:10.1890/08-2244.1
Lawrence T, Culbert E, Felsot A, Hebert V, Sheppard W (2016) Survey and risk assessment of Apis mellifera (Hymenoptera: Apidae) exposure to neonicotinoid pesticides in urban, rural, and agricultural settings. J Econ Entomol tov397. doi:10.1093/jee/tov397
Legendre P, Gallagher ED (2001) Ecologically meaningful transformations for ordination of species data. Oecologia 129:271–280. doi:10.1007/s004420100716
Legendre P, Legendre LF (2012) Numerical ecology, 3rd edn. Elsevier, Amsterdam
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 23:2857–2874. doi:10.1007/s10531-014-0752-0
Lowenstein DM, Matteson KC, Minor ES (2015) Diversity of wild bees supports pollination services in an urbanized landscape. Oecologia 179:811–821. doi:10.1007/s00442-015-3389-0
Martins KT, Gonzalez A, Lechowicz MJ (2015) Pollination services are mediated by bee functional diversity and landscape context. Agric Ecosyst Environ 200:12–20. doi:10.1016/j.agee.2014.10.018
Martins KT, Normandin É, Ascher JS (2017) Hylaeus communis (Hymenoptera: Colletidae), a new exotic bee for North America with generalist foraging and habitat preferences. Can Entomol:1–14. doi:10.4039/tce.2016.62
Matteson KC, Langellotto GA (2011) Small scale additions of native plants fail to increase beneficial insect richness in urban gardens. Insect Conserv Diver 4:89–98. doi:10.1111/j.1752-4598.2010.00103.x
Matteson K, Grace JB, Minor E (2013) Direct and indirect effects of land use on floral resources and flower-visiting insects across an urban landscape. Oikos 122:682–694. doi:10.1111/j.1600-0706.2012.20229.x
McKinney ML (2008) Effects of urbanization on species richness: a review of plants and animals. Urban Ecosyst 11:161–176. doi:10.1007/s11252-007-0045-4
Mitchell T (1960) Bees of the Eastern United States, Volume 1. North Carolina Experiment Station Technical Bulletin 141. University of North Carolina Press, North Carolina
Mitchell T (1962) The Bees of Eastern North America, Vollume 2. North Carolina Experiment Station Technical Bulletin 152. University of North Carolina Press, North Carolina
Montoya JM, Yvon-Durocher G (2007) Ecological networks: information theory meets Darwin's entangled bank. Curr Biol 17:R128–R130. doi:10.1016/j.cub.2007.01.028
Newcomb, L (1977) Newcomb’s Wildflower Guide. Little Brown, Boston
Normandin É, Vereecken NJ, Buddle CM, Fournier V (2017) Taxonomic and functional trait diversity of wild bees in different urban settings. PeerJ 5:e3051. doi:10.7717/peerj.3051
Oksanen J et al. (2015) vegan: Community Ecology Package. R package version 2.3–1. https://CRAN.R-project.org/package=vegan
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. doi:10.1126/science.1257259
Osborne JL et al (2008) Quantifying and comparing bumblebee nest densities in gardens and countryside habitats. J Appl Ecol 45:784–792. doi:10.1111/j.1365-2664.2007.01359.x
Packer L, Genaro JA, Sheffield CS (2007) The bee genera of eastern Canada. Can J Arthropod Identifi 3:1–32
Paini D (2004) Impact of the introduced honey bee (Apis mellifera)(Hymenoptera: Apidae) on native bees: a review. Austral Ecol 29:399–407. doi:10.1111/j.1442-9993.2004.01376.x
Paini DR, Roberts JD (2005) Commercial honey bees (Apis mellifera) reduce the fecundity of an Australian native bee (Hylaeus alcyoneus). Biol Conserv 123:103–112. doi:10.1016/j.biocon.2004.11.001
Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290. doi:10.1093/bioinformatics/btg412
Pardee GL, Philpott SM (2014) Native plants are the bee’s knees: local and landscape predictors of bee richness and abundance in backyard gardens. Urban Ecosyst 17:641–659. doi:10.1007/s11252-014-0349-0
Patefield W (1981) Algorithm AS 159: an efficient method of generating random R× C tables with given row and column totals. J Roy Stat Soc C-App 30:91–97. doi:10.2307/2346669
Payette A, De Oliveira D (1989) Diversité et abondance des apoides (Hymenoptera: Apoidea) dans l’agroécosystème de Saint-Hyacinthe, Québec. Nat Can 116:155–165
Potts SG et al (2010) Declines of managed honey bees and beekeepers in Europe. J Apicult Res 49:15–22. doi:10.3896/IBRA.1.49.1.02
R Core Team (2015) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0. http://www.R-project.org/
Resources naturelles et Faune (2000) Système d’information écoforestière, carte 31H11SE. 1:20 000, Québec
Rundlöf M, Persson AS, Smith HG, Bommarco R (2014) Late-season mass-flowering red clover increases bumble bee queen and male densities. Biol Conserv 172:138–145. doi:10.1016/j.biocon.2014.02.027
Saure C (1996) Urban habitats for bees: the example of the city of berlin. In: The conservation of bees. Academic Press Limited, London, pp 47–54
Senapathi D et al (2015) The impact of over 80 years of land cover changes on bee and wasp pollinator communities in England. Proc R Soc B 282:20150294. doi:10.1098/rspb.2015.0294
Statistics Canada (2012) Focus on Geography Series, 2011 Census. Statistics Canada Catalogue no. 98–310-XWE2011004. Ottawa
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. doi:10.1890/0012-9658(2002)083[1421:SDEOLC]2.0.CO;2
Thomson D (2004) Competitive interactions between the invasive European honey bee and native bumble bees. Ecology 85:458–470. doi:10.1890/02-0626
Tommasi D, Miro A, Higo HA, Winston ML (2004) Bee diversity and abundance in an urban setting. Can Entomol 136:851–869. doi:10.4039/n04-010
Tonietto R, Fant J, Ascher J, Ellis K, Larkin D (2011) A comparison of bee communities of Chicago green roofs, parks and prairies. Landsc Urban Plan 103:102–108. doi:10.1016/j.landurbplan.2011.07.004
Tylianakis JM, Tscharntke T, Lewis OT (2007) Habitat modification alters the structure of tropical host–parasitoid food webs. Nature 445:202–205. doi:10.1038/nature05429
UN (2011) World population prospects: the 2010 revision. United Nations Publications, New York
United States Department of Agriculture, Natural Resources Conservation Service (2016) The PLANTS Database. http://plants.usda.gov. Accessed 31 October 2016
Van Rossum F, Triest L (2010) Pollen dispersal in an insect-pollinated wet meadow herb along an urban river. Landsc. Urban Plan. 95:201–208. doi:10.1016/j.landurbplan.2010.01.004
Vanbergen AJ (2013) Threats to an ecosystem service: pressures on pollinators. Front Ecol Environ 11:251–259. doi:10.1890/120126
Winfree R, Griswold T, Kremen C (2007) Effect of human disturbance on bee communities in a forested ecosystem. Conserv Biol 21:213–223. doi:10.1111/j.1523-1739.2006.00574.x
Winfree R, Bartomeus I, Cariveau DP (2011) Native pollinators in anthropogenic habitats. Annu Rev Ecol Evol Syst 42:1–22. doi:10.1146/annurev-ecolsys-102710-145042
Wojcik VA, McBride JR (2012) Common factors influence bee foraging in urban and wildland landscapes. Urban Ecosyst 15:581–598. doi:10.1007/s11252-011-0211-6
Acknowledgements
We gratefully acknowledge the Natural Science and Engineering Research Council of Canada, the Fonds de Recherche Nature et Technologies Québec, and the Quebec Centre for Biodiversity Science for funding and support. AG is supported by the Canada Research Chair program and a Killam Fellowship. We thank Julien Massé-Jodoin and Sarah Saldahna for field assistance, John Ascher, Bryan Danforth and Jason Gibbs for their help with insect identification, and the residents of Saint-Jean-Baptiste and Mont-Saint-Hilaire, as well as the Gault Nature Reserve, for allowing access to field sites.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Martins, K.T., Gonzalez, A. & Lechowicz, M.J. Patterns of pollinator turnover and increasing diversity associated with urban habitats. Urban Ecosyst 20, 1359–1371 (2017). https://doi.org/10.1007/s11252-017-0688-8
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11252-017-0688-8