Variation in pollinator-mediated plant reproduction across an urbanization gradient

Abstract

Urbanization alters the landscape, degrades and fragments habitats, and can have a profound effect on species interactions. Plant–pollinator networks may be particularly sensitive to urbanization, because plants and their insect pollinators have been shown to respond to urbanization both positively and negatively. To better understand the relationship between urbanization, pollinator behavior, and season on pollinator-mediated plant reproduction, we created 30 experimental plant populations along an urbanization gradient in the Greater Toronto Area, Canada. To test how urbanization affects plant reproduction and between-patch pollen dispersal, we created a standard hermaphroditic plant patch at each site, and a male-sterile plant patch at a subset of sites. We measured plant reproduction in the early and late summer in each of 2 years. Plants in urban sites produced significantly fewer flowers than plants in the nonurban sites, whereas seed number per plant either increased or decreased with urbanization, depending on the season. Experimental populations in urban sites also exhibited reduced pollen dispersal between patches. Pollen dispersal between patches was greatest early in the summer and declined with increased impervious surface and proximity to the city. Together, our results are likely caused by variation in environmental conditions and pollinator services across the urban gradient, resulting in pollen limitation and pollen dispersal differences among sites. Our work adds to the small but growing body of literature on urban plant-pollinator interactions and suggests that responses to urbanization are context-dependent.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3

References

  1. Aizen MA, Harder LD (2007) Expanding the limits of the pollen-limitation concept: effects of pollen quantity and quality. Ecology 88:271–281. https://doi.org/10.1890/06-1017

    Article  PubMed  Google Scholar 

  2. Andrieu E et al (2009) The town Crepis and the country Crepis: how does fragmentation affect a plant-pollinator interaction? Acta Oecol 35:1–7. https://doi.org/10.1016/j.actao.2008.07.002

    Article  Google Scholar 

  3. Aronson MF, La Sorte FA, Nilon CH, Katti M, Goddard MA, Lepczyk CA, Warren PS, Williams NS, Cilliers S, Clarkson B, Dobbs C, Dolan R, Hedblom M, Klotz S, Koojmans JL, Kühn I, MacGregor-Fors I, McDonnell M, Mörtberg U, Pyšek P, Siebert S, Sushinsky J, Werner P, Winter M (2014) A global analysis of the impacts of urbanization on bird and plant diversity reveals key anthropogenic drivers. Proc R Soc B Biol Sci 281:20133330. https://doi.org/10.1098/rspb.2013.3330

    Article  Google Scholar 

  4. Aronson MF, Nilon CH, Lepczyk CA, Parker TS, Warren PS, Cilliers SS, Goddard MA, Hahs AK, Herzog C, Katti M, La Sorte FA, Williams NSG, Zipperer W (2016) Hierarchical filters determine community assembly of urban species pools. Ecology 97:2952–2963. https://doi.org/10.1002/ecy.1535

    Article  PubMed  Google Scholar 

  5. Baldock KCR, Goddard MA, Hicks DM, Kunin WE, Mitschunas N, Morse H, Osgathorpe LM, Potts SG, Robertson KM, Scott AV, Stone GN, Vaughan IP, Memmott J (2015) Where is the UK’s pollinator biodiversity? The importance of urban areas for flower-visiting insects. Proc R Soc B Biol Sci 282:20142849. https://doi.org/10.1098/rspb.2014.2849

    Article  Google Scholar 

  6. Baldock KCR, Goddard MA, Hicks DM, Kunin WE, Mitschunas N, Morse H, Osgathorpe LM, Potts SG, Robertson KM, Scott AV, Staniczenko PPA, Stone GN, Vaughan IP, Memmott J (2019) A systems approach reveals urban pollinator hotspots and conservation opportunities. Nat Ecol Evol. https://doi.org/10.1038/s41559-018-0769-y

    Article  PubMed  PubMed Central  Google Scholar 

  7. Banaszak-Cibicka W, Zmihorski 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

    Article  Google 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 6:e23459. https://doi.org/10.1371/journal.pone.0023459

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  9. Burkle LA, Alarcon R (2011) The future of plant-pollinator diversity: understanding interaction networks across time, space, and global change. Am J Bot 98:528–538. https://doi.org/10.3732/ajb.1000391

    Article  PubMed  Google Scholar 

  10. Calatayud A, Iglesias DJ, Talón M, Barreno E (2003) Effects of 2-month ozone exposure in spinach leaves on photosynthesis, antioxidant systems and lipid peroxidation. Plant Physiol Biochem 41:839–845. https://doi.org/10.1016/s0981-9428(03)00123-2

    CAS  Article  Google Scholar 

  11. 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 109–124

    Google Scholar 

  12. Cheptou P-O, Avendaño V LG (2006) Pollination processes and the Allee effect in highly fragmented populations: consequences for the mating system in urban environments. New Phytol 172:774–783. https://doi.org/10.1111/j.1469-8137.2006.01880.x

    Article  PubMed  Google Scholar 

  13. Clark AJ, Landolt W, Bucher JB, Strasser RJ (2000) Beech (Fagus sylvatica) response to ozone exposure assessed with a chlorophyll a fluorescence performance index. Environ Pollut 109:501–507. https://doi.org/10.1016/s0269-7491(00)00053-1

    CAS  Article  PubMed  Google Scholar 

  14. Crittenden PD, Read DJ (1977) The effects of air pollution on plant growth with special reference to sulphur dioxide. II. Growth studies with Lolium perenne L. New Phytol 80:49–62. https://doi.org/10.1111/j.1469-8137.1978.tb02263.x

    Article  Google Scholar 

  15. Deguines N, Julliard R, de Flores M, Fontaine C (2016) Functional homogenization of flower visitor communities with urbanization. Ecol Evol 6:1967–1976. https://doi.org/10.1002/ece3.2009

    Article  PubMed  PubMed Central  Google Scholar 

  16. Geslin B, Gauzens B, Thébault E, Dajoz I (2013) Plant pollinator networks along a gradient of urbanisation. PLoS One 8:e63421. https://doi.org/10.1371/journal.pone.0063421

    Article  PubMed  PubMed Central  Google Scholar 

  17. Gorton AJ, Moeller DA, Tiffin P, Gorton AJ (2018) Little plant, big city: a test of adaptation to urban environments in common ragweed (Ambrosia artemisiifolia). Proc R Soc B Biol Sci 285:20180968. https://doi.org/10.1098/rspb.2018.0968

    Article  Google Scholar 

  18. Harrison T, Winfree R (2015) Urban drivers of plant-pollinator interactions. Funct Ecol 29:879–888. https://doi.org/10.1111/1365-2435.12486

    Article  Google Scholar 

  19. Hennig EI, Ghazoul J (2012) Pollinating animals in the urban environment. Urban Ecosyst 15:149–166. https://doi.org/10.1007/s11252-011-0202-7

    Article  Google Scholar 

  20. Hernandez JL, Frankie GW, Thorp RW (2009) Ecology of urban bees: a review of current knowledge and directions for future study. Cities Environ 2:1–15

    Article  Google Scholar 

  21. Hicks DM et al (2016) Food for pollinators: quantifying the nectar and pollen resources of urban flower meadows. PLoS One 11:e0158117. https://doi.org/10.1371/journal.pone.0158117

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  22. Idso CD, Idso SB, Balling RC Jr (1998) The urban CO2 dome of Pheonix, Arizona. Phys Geogr 19:95–108. https://doi.org/10.1080/02723646.1998.10642642

    Article  Google Scholar 

  23. Irwin RE, Warren PS, Carper AL, Adler LS (2014) Plant-animal interactions in suburban environments: implications for floral evolution. Oecologia 174:803–815. https://doi.org/10.1007/s00442-013-2797-2

    Article  PubMed  Google Scholar 

  24. Irwin RE, Warren PS, Adler LS (2018) Phenotypic selection on floral traits in an urban landscape. Proc R Soc B Biol Sci 285:20181239. https://doi.org/10.1098/rspb.2018.1239

    Article  Google Scholar 

  25. Ison JL, Weis AE (2017) Temporal population genetic structure in the pollen pool for flowering time: a field experiment with Brassica rapa (Brassicaceae). Am J Bot 104:1569–1580. https://doi.org/10.3732/ajb.1700210

    Article  PubMed  Google Scholar 

  26. Jacobson MZ (2010) Enhancement of local air pollution by urban CO2 domes. Environ Sci Technol 44:2497–2502. https://doi.org/10.1021/es903018m

    CAS  Article  PubMed  Google Scholar 

  27. Jochner SC, Sparks TH, Estrella N, Menzel A (2012) The influence of altitude and urbanisation on trends and mean dates in phenology (1980–2009). Int J Biometeorol 56:387–394. https://doi.org/10.1007/s00484-011-0444-3

    Article  PubMed  Google Scholar 

  28. Johnson MTJ, Prashad CM, Lavoignat M, Saini HS (2018) Contrasting the effects of natural selection, genetic drift and gene flow on urban evolution in white clover (Trifolium repens). Proc R Soc B Biol Sci 285:20181019. https://doi.org/10.1098/rspb.2018.1019

    Article  Google Scholar 

  29. Kuznetsova A, Brockhoff PB, Christensen RHB (2017) lmerTest package: tests in linear mixed effects models. J Stat Softw 82:1–26. https://doi.org/10.18637/jss.v082.i13

    Article  Google Scholar 

  30. Larson JL, Kesheimer AJ, Potter DA (2014) Pollinator assemblages on dandelions and white clover in urban and suburban lawns. J Insect Conserv 18:863–873. https://doi.org/10.1007/s10841-014-9694-9

    Article  Google Scholar 

  31. Leong M, Kremen C, Roderick GK (2014) Pollinator interactions with yellow star thistle (Centaurea solstitialis) across urban, agricultural, and natural landscapes. PLoS One 9:e86357. https://doi.org/10.1371/journal.pone.0086357

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  32. MacIvor JS, Cadotte MW, Livingstone SW, Lundholm JT, Yasui S-LE (2016) Phylogenetic ecology and the greening of cities. J Appl Ecol 53:1470–1476. https://doi.org/10.1111/1365-2664.12667

    Article  Google Scholar 

  33. Matteson KC, Ascher JS, Langellotto GA (2008) Bee richness and abundance in New York City urban gardens. Ann Entomol Soc Am 101:140–150. https://doi.org/10.1603/0013-8746(2008)101%5b140:braain%5d2.0.co;2

    Article  Google Scholar 

  34. Mayer H (1999) Air pollution in cities. Atmos Environ 33:4029–4037. https://doi.org/10.1016/s1352-2310(99)00144-2

    CAS  Article  Google Scholar 

  35. McKinney ML (2008) Effects of urbanization on species richness: a review of plants and animals. Urban Ecosyst 11:161–176. https://doi.org/10.1007/s11252-007-0045-4

    Article  Google Scholar 

  36. Nasrallah J, Nasrallah M (1989) The molecular genetics of self-incompatibility in Brassica. Annu Rev Genet 23:121–139. https://doi.org/10.1146/annurev.genet.23.1.121

    CAS  Article  PubMed  Google Scholar 

  37. Neil K, Wu J (2006) Effects of urbanization on plant flowering phenology: a review. Urban Ecosyst 9:243–257. https://doi.org/10.1007/s11252-006-9354-2

    Article  Google Scholar 

  38. Niemelä J (2011) Urban ecology: patterns, processes, and applications. Oxford University Press, New York

    Google Scholar 

  39. Oke TR (1973) City size and the urban heat island. Atmos Environ 7:769–779. https://doi.org/10.1016/0004-6981(73)90140-6

    Article  Google Scholar 

  40. Olesen JM, Bascompte J, Elberling H, Jordano P (2008) Temporal dynamics in a pollination network. Ecology 89:1573–1582. https://doi.org/10.1890/07-0451.1

    Article  PubMed  Google Scholar 

  41. Parker AJ, Tran JL, Ison JL, Bai JDK, Weis AE, Thomson D (2015) Pollen packing affects the function of pollen on corbiculate bees but not non-corbiculate bees. Arthropod Plant Interact 9:197–203. https://doi.org/10.1007/s11829-015-9358-z

    Article  Google Scholar 

  42. Petanidou T, Potts SG (2006) Mutual use of resources in Mediterranean plant–pollinator communities: how specialized are pollination webs. In: Waser NM, Ollerton J (eds) Plant–pollinator interactions: from specialization to generalization. University of Chicago Press, Chicago, pp 220–244

    Google Scholar 

  43. Pickett STA, Cadenasso ML, Grove JM, Nilon CH, Pouyat RV, Zipperer WC, Constanza R (2001) Urban ecological systems: linking terrestrial ecological, physical, and socioeconomic components of metropolitan areas. Annu Rev Ecol Syst 32:127–157. https://doi.org/10.1007/978-0-387-73412-5_7

    Article  Google Scholar 

  44. Sage TL, Bagha S, Lundsgaard-Nielsen V, Branch HA, Sultmanis S, Sage RF (2015) The effect of high temperature stress on male and female reproduction in plants. Field Crop Res 182:30–42. https://doi.org/10.1016/j.fcr.2015.06.011

    Article  Google Scholar 

  45. Satake T, Yoshida S (1978) High temperature-induced sterility in Indica rices at flowering. Jpn J Crop Sci 49:135–139. https://doi.org/10.1626/jcs.47.6

    Article  Google Scholar 

  46. Satterthwaite FE (1946) An approximate distribution of estimates of variance components. Biometrics Bull 2:110–114. https://doi.org/10.1002/9780470057339.vai016

    CAS  Article  Google Scholar 

  47. Seto KC, Sánchez-Rodríguez R, Fragkias M (2010) The new geography of contemporary urbanization and the environment. Annu Rev Environ Resour 35:167–194. https://doi.org/10.1146/annurev-environ-100809-125336

    Article  Google Scholar 

  48. Theodorou P, Radzevičiūtė R, Settele J, Schweiger O, Murray TE, Paxton RJ (2016) Pollination services enhanced with urbanisation despite increasing pollinator parasitism. Proc R Soc B Biol Sci 283:20160561. https://doi.org/10.1098/rspb.2016.0561

    Article  Google Scholar 

  49. Theodorou P, Albig K, Radzevičiūtė R, Settele J, Schweiger O, Murray TE, Paxton RJ (2017) The structure of flower visitor networks in relation to pollination across an agricultural to urban gradient. Funct Ecol 31:838–847. https://doi.org/10.1111/1365-2435.12803

    Article  Google Scholar 

  50. Tomkins SP, Williams PH (1990) Fast plants for finer science—an introduction to the biology of rapid-cycling Brassica campostris (rapa) L. J Biol Educ 24:239–250. https://doi.org/10.1080/00219266.1990.9655152

    Article  Google Scholar 

  51. Tommasi D, Miro A, Higo HA, Winston ML (2004) Bee diversity and abundance in an urban setting. Can Entomol 136:851–894. https://doi.org/10.4039/n04-010

    Article  Google Scholar 

  52. United Nations Department of Economic and Social Affairs (2015) World Urbanization Prospects: the 2014 Revision. ST/ESA/SER.A/366

  53. Ushimaru A, Kobayashi A, Dohzono I (2014) Does urbanization promote floral diversification? Implications from changes in herkogamy with pollinator availability in an urban-rural area. Am Nat 184:258–267. https://doi.org/10.1086/676855

    Article  PubMed  Google Scholar 

  54. Verboven HAF, Brys R, Hermy M (2012) Sex in the city: reproductive success of Digitalis purpurea in a gradient from urban to rural sites. Landsc Urban Plan 106:158–164. https://doi.org/10.1016/j.landurbplan.2012.02.015

    Article  Google Scholar 

  55. Weis AE (2015) Inheritance of rapid cycling in Brassica rapa fast plants: dominance that increases with photoperiod. Int J Plant Sci 176:859–868. https://doi.org/10.1086/683304

    Article  Google Scholar 

  56. Wilcock C, Neiland R (2002) Pollination failure in plants—why it happens and when it matters. Trends Plant Sci 7:270–277. https://doi.org/10.1016/s1360-1385(02)02258-6

    CAS  Article  PubMed  Google Scholar 

  57. Wilkinson S, Mills G, Illidge R, Davies WJ (2012) How is ozone pollution reducing our food supply? J Exp Bot 63:527–536. https://doi.org/10.1093/jxb/err317

    CAS  Article  PubMed  Google Scholar 

  58. Williams PH, Hill CB (1986) Rapid-cycling populations of Brassica. Science 232:1385–1389. https://doi.org/10.1126/science.232.4756.1385

    CAS  Article  PubMed  Google Scholar 

  59. Wilson P, Thomson JD (1991) Heterogeneity among floral visitors leads to discordance between removal and deposition of pollen. Ecology 72:1503–1507. https://doi.org/10.2307/1941124

    Article  Google Scholar 

  60. Yakub M, Tiffin P (2016) Living in the city: urban environments shape the evolution of a native annual plant. Glob Chang Biol 23:2082–2089. https://doi.org/10.1111/gcb.13528

    Article  PubMed  Google Scholar 

  61. Zipper SC, Schatz J, Kucharik CJ, Loheide SP (2017) Urban heat island-induced increases in evapotranspirative demand. Geophys Res Lett 44:873–881. https://doi.org/10.1002/2016gl072190

    Article  Google Scholar 

Download references

Acknowledgements

We thank volunteer residents who donated their lawns to this project, and S. Innes and S. Munim for help with fieldwork and plant care. We thank the handling editor and two anonymous reviewers for their comments and suggestions on the study and manuscript. LRR was funded by a Natural Sciences and Engineering Research Council of Canada—Canada Graduate Scholarship Doctoral. MTJJ and AEW were funded by Natural Sciences and Engineering Research Council of Canada Discovery Grants.

Author information

Affiliations

Authors

Contributions

LRR, MTJJ, and AW conceived the experiments. LRR and MTJ designed the experiment. LRR and VN conducted the experiment, and LRR performed the analyses. LRR wrote and revised the manuscript, with input from all authors.

Corresponding author

Correspondence to L. Ruth Rivkin.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by Anne Worley.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 19 kb)

Supplementary material 2 (XLSX 75 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Rivkin, L.R., Nhan, V.J., Weis, A.E. et al. Variation in pollinator-mediated plant reproduction across an urbanization gradient. Oecologia 192, 1073–1083 (2020). https://doi.org/10.1007/s00442-020-04621-z

Download citation

Keywords

  • Male sterility
  • Plant–pollinator interaction
  • Pollinator services
  • Rapid-cycling Brassica
  • Urban ecology