Biodiversity and Conservation

, Volume 23, Issue 11, pp 2857–2874 | Cite as

Humans, bees, and pollination services in the city: the case of Chicago, IL (USA)

  • David M. Lowenstein
  • Kevin C. Matteson
  • Iyan Xiao
  • Alexandra M. Silva
  • Emily S. Minor
Original Paper

Abstract

Despite the global trend in urbanization, little is known about patterns of biodiversity or provisioning of ecosystem services in urban areas. Bee communities and the pollination services they provide are important in cities, both for small-scale urban agriculture and native gardens. To better understand this important ecological issue, we examined bee communities, their response to novel floral resources, and their potential to provide pollination services in 25 neighborhoods across Chicago, IL (USA). In these neighborhoods, we evaluated how local floral resources, socioeconomic factors, and surrounding land cover affected abundance, richness, and community composition of bees active in summer. We also quantified species-specific body pollen loads and visitation frequencies to potted flowering purple coneflower plants (Echinacea purpurea) to estimate potential pollination services in each neighborhood. We documented 37 bee species and 79 flowering plant genera across all neighborhoods, with 8 bee species and 14 flowering plant genera observed on average along each neighborhood block. We found that both bee abundance and richness increased in neighborhoods with higher human population density, as did visitation to purple coneflower flower heads. In more densely populated neighborhoods, bee communities shifted to a suite of species that carry more pollen and are more active pollinators in this system, including the European honey bee (Apis mellifera) and native species such as Agapostemon virescens. More densely populated neighborhoods also had a greater diversity of flowering plants, suggesting that the positive relationship between people and bees was mediated by the effect of people on floral resources. Other environmental variables that were important for bee communities included the amount of grass/herbaceous cover and solar radiation in the surrounding area. Our results indicate that bee communities and pollination services can be maintained in dense urban neighborhoods with single-family and multi-family homes, as long as those neighborhoods contain diverse and abundant floral resources.

Keywords

Pollinators Human-environment interactions Urban Floral visitation Floral resources Ecosystem service 

References

  1. Ahrné K, Bengtsson J, Elmqvist T (2009) Bumble bees (Bombus spp.) along a gradient of increasing urbanization. PLoS ONE 4:e5574PubMedCentralPubMedCrossRefGoogle Scholar
  2. Albrecht M, Duelli P, Muller C, Kleijn D, Schmid B (2007) The Swiss agri-environment scheme enhances pollinator diversity and plant reproductive success in nearby intensively managed farmland. J Appl Ecol 44:813–822CrossRefGoogle Scholar
  3. Albrecht M, Schmid B, Hautier Y, Muller CB (2012) Diverse pollinator communities enhance plant reproductive success. Proc R Soc B 279(4845):4852Google Scholar
  4. Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA + for PRIMER: guide to software and statistical methods. Primer E, PlymouthGoogle Scholar
  5. Artz DR, Nault BA (2011) Performance of Apis mellifera, Bombus impatiens, and Peponapis pruinosa (Hymenoptera:Apidae) as pollinators of pumpkin. J Econ Entomol 104:1153–1161PubMedCrossRefGoogle Scholar
  6. Balvanera P, Pfisterer AB, Buchmann N, He J-S, Nakashizuka T, Raffaelli D, Schmid B (2006) Quantifying the evidence for biodiversity effects on ecosystem functioning and services. Ecol Lett 9:1146–1156PubMedCrossRefGoogle Scholar
  7. Banaszak-Cibicka W, Zmihorski M (2012) Wild bees along an urban gradient: winners and losers. J Insect Conserv 16:331–343CrossRefGoogle Scholar
  8. 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 8:e23459CrossRefGoogle Scholar
  9. Burnham KP, Anderson DR (1998) Model selection and inference: a practical information-theoretic approach. Springer, New YorkCrossRefGoogle Scholar
  10. Cadenasso ML, Pickett STA, Schwarz K (2007) Spatial heterogeneity in urban ecosystems: reconceptualizing land cover and a framework for classification. Front Ecol Environ 5:80–88CrossRefGoogle Scholar
  11. Cane JH (2003) Exotic nonsocial bees in North American: ecological implications. In: Strickler K, Cane JH (eds) For nonnative crops, whence pollination of the future. Thomas Say Foundation. Entomological Society of America, Lanham, pp 113–126Google Scholar
  12. Cane JH (2005) Bees, pollination, and the challenges of sprawl. In: Johnson EA, Klemens MW (eds) Nature in fragments: the legacy of sprawl. Columbia University Press, New York, pp 109–124Google Scholar
  13. Carper AL, Adler LS, Warren PS, Irwin RE (2014) Effects of suburbanization on forest bee communities. Environ Entomol 43:253–262PubMedCrossRefGoogle Scholar
  14. Cheptou PO, Avendaño VLG (2006) Pollination processes and the Allee effect in highly fragmented populations: consequences for the mating system in urban environments. New Phytol 172:774–783PubMedCrossRefGoogle Scholar
  15. 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 78:227–246CrossRefGoogle Scholar
  16. Ghazoul J (2006) Floral diversity and the facilitation of pollination. J Ecol 94:295–304CrossRefGoogle Scholar
  17. Greenleaf SS, Williams NM, Winfree R, Kremen C (2007) Bee foraging ranges and their relationship to body size. Oecologia 153:589–596PubMedCrossRefGoogle Scholar
  18. Grimm NB, Faeth SH, Golubiewski NE, Redman CL, Wu J, Bai X, Briggs JM (2008) Global change and the ecology of cities. Science 319:756–760PubMedCrossRefGoogle Scholar
  19. Grove JM, Burch WR Jr (1997) A social ecology approach and applications of urban ecosystem and landscape analyses: a case study of Baltimore Maryland. Urban Ecosyst 1:259–275CrossRefGoogle Scholar
  20. Hegland SJ, Grytnes J-A, Totland Ø (2009) The relative importance of positive and negative interactions for pollinator attraction in a plant community. Ecol Res 24:929–936CrossRefGoogle Scholar
  21. Hennig EI, Ghazoul J (2011) Plant pollinator interactions within the urban environment. Perspect Plant Eco Evol Syst 13:137–150CrossRefGoogle Scholar
  22. Hoehn P, Tscharntke T, Tylianakis JM, Steffan-Dewenter I (2008) Functional group diversity of bee pollinators increases crop yield. Proc R Soc B 275:2283–2291PubMedCentralPubMedCrossRefGoogle Scholar
  23. Jędrzejewska-Szmek K, Zych M (2013) Flower-visitor and pollen transport networks in a large city: structure and properties. Arthropod-Plant Interact 7:503–516CrossRefGoogle Scholar
  24. Jha S, Kremen C (2013) Resource diversity and landscape-level homogeneity drive native bee foraging. Proc Natl Acad Sci 110:555–558PubMedCentralPubMedCrossRefGoogle Scholar
  25. Kendal D, Williams KJH, Williams NSG (2012) Plant traits link people’s plant preferences to the composition of their gardens. Landsc Urban Plan 105:34–42CrossRefGoogle Scholar
  26. Kinzig AP, Warren P, Martin C, Hope D, Katti M (2005) The effects of human socioeconomic status and cultural characteristics on urban patterns of biodiversity. Ecol Soc 10:23Google Scholar
  27. Klein AM, Steffan-Dewenter I, Tscharntke T (2003) Fruit set of highland coffee increases with the diversity of pollinating bees. Proc R Soc B 270:955–961PubMedCentralPubMedCrossRefGoogle Scholar
  28. Klein AM, Vaissiere BE, Cane JH, Steffan-Dewenter I, Cunningham SA, Kremen C, Tscharntke T (2007) Importance of pollinators in changing landscapes for world crops. Proc R Soc B 274:303–313PubMedCentralPubMedCrossRefGoogle Scholar
  29. Kremen C, Williams NM, Thorp RW (2002) Crop pollination from native bees at risk from agricultural intensification. Proc Natl Acad Sci 99:16812–16816PubMedCentralPubMedCrossRefGoogle Scholar
  30. Ksiazek K, Fant J, Skogen K (2012) An assessment of pollen limitation on Chicago green roofs. Landsc and Urban Plan 107:401–408CrossRefGoogle Scholar
  31. Larson M (2005) Higher pollinator effectiveness by specialist than generalist flower-visitors of unspecialized Knautia arvensis (Dipsacaceae). Oecologia 146:394–403CrossRefGoogle Scholar
  32. Lázaro A, Totland Ø (2010) Population dependence in the interactions with neighbors for pollination: a field experiment with Taraxacum officinale. Am J Bot 97:760–769PubMedCrossRefGoogle Scholar
  33. Leong M, Kremen C, Roderick GK (2014) Pollinator interactions with yellow starthistle (Centaurea solstitialis) across urban, agricultural, and natural landscapes. PLoS ONE 9:e86357PubMedCentralPubMedCrossRefGoogle Scholar
  34. Lonsdorf E, Kremen C, Ricketts T, Winfree R, Williams N, Greenleaf S (2009) Modelling pollination services across agricultural landscapes. Ann Bot 103:1589–1600PubMedCentralPubMedCrossRefGoogle Scholar
  35. Loram A, Tratalos J, Warren PH, Gaston KJ (2007) Urban domestic gardens (X): the extent & structure of the resource in five major cities. Landsc Ecol 22:601–615CrossRefGoogle Scholar
  36. Matteson KC, Langellotto GA (2010) Determinates of inner city butterfly and bee species richness. Urban Ecosyst 13:333–347CrossRefGoogle Scholar
  37. Matteson KC, Ascher JS, Langellotto GA (2008) Bee richness and abundance in New York City gardens. Ann Entomol Soc Am 101:140–150CrossRefGoogle Scholar
  38. Matteson KC, Grace JB, Minor ES (2013) Direct and indirect effects of land use on floral resources and flower-visiting insects across an urban landscape. Oikos 122:682–694CrossRefGoogle Scholar
  39. McClintock N (2010) Why farm the city? Theorizing urban agriculture through a lens of metabolic rift. Camb J Reg Econ Soc 3:191–207CrossRefGoogle Scholar
  40. McCune B, Grace JB (2002) Analysis of ecological communities. MjM Software Design, Gleneden BeachGoogle Scholar
  41. McCune B, Mefford MJ (2011) PC-ORD. Multivariate analysis of ecological data. Version 6. MjM Software, Gleneden BeachGoogle Scholar
  42. McDonald RI, Marcotullio PJ, Güneralp B (2013) Urbanization and global trends in biodiversity and ecosystem services. In: Elmqvist T, Fragkias M, Goodness J, Güneralp B, Marcotullio PJ, McDonald RI, Parnell S, Schewenius M, Sendstad M, Seto KC, Wilkinson C (eds) Urbanization, biodiversity and ecosystem services: challenges and opportunities. Springer, New YorkGoogle Scholar
  43. McIntyre NE, Hostetler ME (2001) Effects of urban land use on pollinator communities in a desert metropolis. Basic Appl Ecol 2:209–218CrossRefGoogle Scholar
  44. McKinney ML (2002) Urbanization, biodiversity, and conservation. Bioscience 52:883–890CrossRefGoogle Scholar
  45. McKinney ML (2004) Measuring floristic homogenization by non-native plants in north America. Glob Ecol Biogeogr 13:47–53CrossRefGoogle Scholar
  46. McKinney ML (2008) Effects of urbanization on species richness: a review of plants and animals. Urban Ecosyst 11:161–176CrossRefGoogle Scholar
  47. Michener CD (2006) The bees of the World, 2nd edn. Johns Hopkins University Press, BaltimoreGoogle Scholar
  48. Moeller DA (2004) Facilitative interactions among plants via shared pollinators. Ecology 84:3289–3301CrossRefGoogle Scholar
  49. 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 12:716–728PubMedCrossRefGoogle Scholar
  50. Owen J (1991) The ecology of a garden, the first fifteen years. Cambridge University Press, Cambridge, p 225Google Scholar
  51. Pauw A (2007) Collapse of a pollination web in small conservation areas. Ecology 88:1759–1769PubMedCrossRefGoogle Scholar
  52. Pollard E (1977) A method for assessing changes in the abundance of butterflies. Biol Conserv 12:115–134CrossRefGoogle Scholar
  53. Ricketts TH, Regetz J, Steffan-Dewenter I, Cunningham SA, Kremen C, Bogdanski A, Gemmill-Herren B, Greenleaf SS, Klein AM, Mayfield MM, Morandin LA, Ochieng A, Viana BF (2008) Landscape effects on crop pollination services: are there general patterns? Ecol Lett 11:499–515PubMedCrossRefGoogle Scholar
  54. Samnegard U, Persson AS, Smith HG (2011) Gardens benefit bees and enhance pollination in intensively managed farmland. Biol Conserv 144:2602–2606CrossRefGoogle Scholar
  55. Swift MJ, Izac AMN, van Noordwijk M (2004) Biodiversity and ecosystem services in agricultural landscapes–are we asking the right questions? Agric Ecosyst Environ 104:113–134CrossRefGoogle Scholar
  56. 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 103:102–108CrossRefGoogle Scholar
  57. United Nations Population Division (2006) World Urbanization Prospects: The 2005 Revision. United Nations, Department of Economic and Social Affairs, New York, New York, USAGoogle Scholar
  58. Vazquez DP, Morris WF, Jordano P (2005) Interaction frequency as a surrogate for the total effect of animal mutualists on plants. Ecol Lett 8:1088–1094CrossRefGoogle Scholar
  59. Vicens N, Bosch J (2000) Weather-dependent pollinator activity in an apple orchard, with special reference to Osmia cornuta and Apis mellifera (Hymenoptera: Megachilidae and Apidae). Environ Entomol 29:413–420CrossRefGoogle Scholar
  60. Wagenius W, Lyon SP (2010) Reproduction of Echinacea angustifolia in fragmented prairie is pollen-limited but not pollinator-limited. Ecology 91:733–742PubMedCrossRefGoogle Scholar
  61. Willmer PG (1983) Thermal constraints on activity patterns in nectar-feeding insects. Ecol Entomol 8:455–469CrossRefGoogle Scholar
  62. Winfree R, Kremen C (2009) Are ecosystem services stabilized by differences among species? A test using crop pollination. Proc R Soc B 276:229–237PubMedCentralPubMedCrossRefGoogle Scholar
  63. Winfree R, Griswold T, Kremen C (2007) Effects of human disturbance on bee communities in a forested ecosystem. Conserv Biol 21:213–223PubMedCrossRefGoogle Scholar
  64. Winfree R, Williams NM, Gaines H, Ascher JS, Kremen C (2008) Wild bee pollinators provide the majority of crop visitation across land-use gradients in New Jersey and Pennsylvania, USA. J Appl Ecol 45:793–802CrossRefGoogle Scholar
  65. Wojcik VA, McBride JR (2012) Common factors influence bee foraging in urban and wildland landscapes. Urban Ecosyst 15:581–598CrossRefGoogle Scholar
  66. Zych M, Goldstein J, Roguz K, Stpiczynska M (2013) The most effective pollinator revisited: pollen dynamics in a spring-flowering herb. Arthropod-Plant Interact 7:315–322CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • David M. Lowenstein
    • 1
  • Kevin C. Matteson
    • 1
    • 2
  • Iyan Xiao
    • 3
  • Alexandra M. Silva
    • 1
  • Emily S. Minor
    • 1
    • 4
  1. 1.Department of Biological SciencesUniversity of Illinois at ChicagoChicagoUSA
  2. 2.Department of BiologyMiami UniversityOxfordUSA
  3. 3.State Key Laboratory of Vegetation and Environmental Change, Institute of BotanyChinese Academy of SciencesBeijingPeople’s Republic of China
  4. 4.Institute for Environmental Science and PolicyUniversity of Illinois at ChicagoChicagoUSA

Personalised recommendations