Biological Invasions

, Volume 11, Issue 6, pp 1357–1371 | Cite as

Springtime in the city: exotic shrubs promote earlier greenup in urban forests

  • Daniel P. Shustack
  • Amanda D. Rodewald
  • Thomas A. Waite
Original Paper


Despite the widespread recognition that urban areas are frequently dominated by exotic and invasive plants, the consequences of these changes in community structure have not been explicitly considered as an explanation for the pattern of advanced leaf phenology, or early greenup, reported in many urban areas. As such, we evaluated two hypotheses that could account for advanced greenup in forests along an urban to rural gradient: advanced phenology within individual species or differences in woody plant community. We monitored the spring leafing phenology of Aesculus glabra (Ohio buckeye), Lonicera maackii (Amur honeysuckle), and Acer negundo (box elder) in 11 forests spanning an urban to rural gradient in central Ohio, USA. From February to April 2006, we monitored these species, recorded woody plant composition, and documented daily minimum and maximum temperatures at each site. We found a weak but general trend of advanced phenology within species in more urban landscapes. Monthly average minimum temperatures were higher with increasing urbanization while monthly average maximum temperatures were similar across the urban to rural gradient. We also found evidence for shifts in woody plant communities along the urbanization gradient, mainly driven by the abundance of L. maackii, an invasive exotic species, in the more urban forests. Because L. maackii leafs out weeks earlier than native woody species and is very abundant in urban forests, we suggest that the invasion of forests by this species can generate earlier greenup of urban forests.


Acer negundo Aesculus glabra Spring greenup Lonicera maackii Leafing phenology Urban heat island 



Funding for this research was provided by the National Science Foundation (DEB-0340879), Ohio Division of Wildlife, Ohio Agricultural Research and Development Center. E. Norris, E. Interis, and C. Short helped with temperature and phenology data collection. We are grateful to the Franklin County Metro Parks, Columbus Recreation and Parks, and Gahanna Parks and Recreation for their cooperation and access to sites. Discussions with members of the Rodewald lab, especially S. Matthews, improved this research. C. Augspurger provided valuable guidance in study design, analysis, and writing. D. Herms, T. Grubb and two anonymous reviewers provided comments on earlier drafts of this manuscript.


  1. Ahlgren CE (1957) Phenological observations of nineteen native tree species in northeastern Minnesota. Ecology 38:622–628. doi: 10.2307/1943128 CrossRefGoogle Scholar
  2. Altman PL, Dittmer DS (1962) Biological handbooks: growth including reproduction and morphological development. Federation of American Societies for Experimental Biology, Washington, DCGoogle Scholar
  3. Augspurger CK, Bartlett EA (2003) Differences in leaf phenology between juvenile and adult trees in a temperate deciduous forest. Tree Physiol 23:517–525PubMedGoogle Scholar
  4. Bartuszevige AM, Gorchov DL (2006) Avian seed dispersal of an invasive shrub. Biol Invas 8:1013–1022. doi: 10.1007/s10530-005-3634-2 CrossRefGoogle Scholar
  5. Borgmann KL, Rodewald AD (2005) Forest restoration in urbanizing landscapes: interactions between land use and an exotic shrub. Res Econ 13:334–340Google Scholar
  6. Chen X (2003) Assessing phenology at the biome level. In: Schwartz MD (ed) Phenology: an integrative environmental science. Kluwer Academic Publishers, Dordecht, The NetherlandsGoogle Scholar
  7. Chuine I (2000) A unified model for budburst of trees. J Theor Biol 207:337–347. doi: 10.1006/jtbi.2000.2178 PubMedCrossRefGoogle Scholar
  8. Chuine I, Cour P, Rousseau DD (1999) Selecting models to predict the timing of flowering of temperate trees: implications for tree phenology modelling. Plant Cell Environ 22:1–13. doi: 10.1046/j.1365-3040.1999.00395.x CrossRefGoogle Scholar
  9. Collier MH, Vankat JL, Hughes MR (2002) Diminished plant richness and abundance below Lonicera maackii, an invasive shrub. Am Midl Nat 147:60–71. doi: 10.1674/0003-0031(2002)147[0060:DPRAAB]2.0.CO;2 CrossRefGoogle Scholar
  10. Defila C, Clot B (2003) Long-term urban-rural comparisons. In: Schwartz MD (ed) Phenology: an integrative environmental science. Kluwer Academic Publishers, Dordecht, The NetherlandsGoogle Scholar
  11. Dorning M, Cipollini D (2006) Leaf and root extracts of the invasive shrub, Lonicera maackii, inhibit seed germination of three herbs with no autotoxic effects. Plant Ecol 184:287–296. doi: 10.1007/s11258-005-9073-4 CrossRefGoogle Scholar
  12. Drayton B, Primack RB (1996) Plant species lost in an isolated conservation area in metropolitan Boston from 1894 to 1993. Conserv Biol 10:30–39. doi: 10.1046/j.1523-1739.1996.10010030.x CrossRefGoogle Scholar
  13. Dufrêne M, Legendre P (1997) Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecol Monogr 67:345–366Google Scholar
  14. Duguay S, Eigenbrod F, Fahrig L (2007) Effects of surrounding urbanization on non-native flora in small forest patches. Land Econ 22:589–599. doi: 10.1007/s10980-006-9050-x CrossRefGoogle Scholar
  15. Fisher JI, Mustard JF, Vadeboncoeur MA (2006) Green leaf phenology at Landsat resolution: scaling from the field to the satellite. Remote Sens Environ 100:265–279. doi: 10.1016/j.rse.2005.10.022 CrossRefGoogle Scholar
  16. Gaston KJ, Warren PH, Thompson K, Smith RM (2005) Urban domestic gardens (IV): the extent of the resource and its associated features. Biodivers Conserv 14:3327–3349. doi: 10.1007/s10531-004-9513-9 CrossRefGoogle Scholar
  17. Godefroid S, Koedam N (2007) Urban plant species patterns are highly driven by density and function of built-up areas. Land Econ 22:1227–1239. doi: 10.1007/s10980-007-9102-x CrossRefGoogle Scholar
  18. Gomez F, Gaja E, Reig A (1998) Vegetation and climatic changes in a city. Ecol Eng 10:355–360. doi: 10.1016/S0925-8574(98)00002-0 CrossRefGoogle Scholar
  19. Gorchov DL, Trisel DE (2003) Competitive effects of the invasive shrub, Lonicera maackii (Rupr.) Herder (Caprifoliaceae), on the growth and survival of native tree seedlings. Plant Ecol 166:13–24. doi: 10.1023/A:1023208215796 CrossRefGoogle Scholar
  20. Gould AMA, Gorchov DL (2000) Effects of the exotic invasive shrub Lonicera maackii on the survival and fecundity of three species of native annuals. Am Midl Nat 144:36–50. doi: 10.1674/0003-0031(2000)144[0036:EOTEIS]2.0.CO;2 CrossRefGoogle Scholar
  21. Hansell MH (2000) Bird nests and construction behaviour. Cambridge University Press, UKGoogle Scholar
  22. Hartman KM, McCarthy BC (2004) Restoration of a forest understory after the removal of an invasive shrub, Amur honeysuckle (Lonicera maackii). Restor Ecol 12:154–165. doi: 10.1111/j.1061-2971.2004.00368.x CrossRefGoogle Scholar
  23. Houle G (2007) Spring-flowering herbaceous plant species of the deciduous forests of eastern Canada and 20th century climate warming. Can J For Res-Revue Can De Rech For 37:505–512. doi: 10.1139/X06-239 CrossRefGoogle Scholar
  24. Kane B (2005) Value, benefits, and costs of urban trees, Virginia Cooperative Extension Publication, pp 420–181,
  25. Lamb GN (1915) A calendar of the leafing, flowering, and seeding of the common trees of the eastern United States. Mon Weather Rev Suppl 2:3–16Google Scholar
  26. Lamptey BL, Barron EJ, Pollard D (2005) Impacts of agriculture and urbanization on the climate of the Northeastern United States. Glob Planet Change 49:203–221. doi: 10.1016/j.gloplacha.2005.10.001 CrossRefGoogle Scholar
  27. Lechowicz MJ (1984) Why do temperate deciduous trees leaf out at different times adaptation and ecology of forest communities. Am Nat 124:821–842. doi: 10.1086/284319 CrossRefGoogle Scholar
  28. Leps J, Smilauer P (2003) Multivariate analysis of ecological data using CANOCO. Cambridge University Press, UKGoogle Scholar
  29. Leston LFV, Rodewald AD (2006) Are urban forests ecological traps for understory birds? An examination using Northern cardinals. Biol Conserv 131:566–574. doi: 10.1016/j.biocon.2006.03.003 CrossRefGoogle Scholar
  30. Lu PL, Yu Q, Liu JD, Lee XH (2006) Advance of tree-flowering dates in response to urban climate change. Agric For Meteorol 138:120–131. doi: 10.1016/j.agrformet.2006.04.002 CrossRefGoogle Scholar
  31. Luken JO, Thieret JW (1996) Amur honeysuckle, its fall from grace. Bioscience 46:18–24. doi: 10.2307/1312651 CrossRefGoogle Scholar
  32. McCune B, Mefford MJ (1999) PC-ORD multivariate analysis of ecological data. Version 5.0.—MjM Software. Gleneden Beach, Oregon, USAGoogle Scholar
  33. McGee CE (1986) Budbreak for twenty-three upland hardwoods compared under forest canopies and in recent clearcuts. For Sci 32:924–935Google Scholar
  34. McKinney ML (2002) Urbanization, biodiversity, and conservation. Bioscience 52:883–890. doi: 10.1641/0006-3568(2002)052[0883:UBAC]2.0.CO;2 CrossRefGoogle Scholar
  35. McKinney ML (2006) Urbanization as a major cause of biotic homogenization. Biol Conserv 127:247–260. doi: 10.1016/j.biocon.2005.09.005 CrossRefGoogle Scholar
  36. Meiners SJ (2007) Apparent competition: an impact of exotic shrub invasion on tree regeneration. Biol Invasions 9:849–855. doi: 10.1007/s10530-006-9086-5 CrossRefGoogle Scholar
  37. Menzel A (2002) Phenology: its importance to the global change community—An editorial comment. Clim Change 54:379–385. doi: 10.1023/A:1016125215496 CrossRefGoogle Scholar
  38. Miller KE, Gorchov DL (2004) The invasive shrub, Lonicera maackii, reduces growth and fecundity of perennial forest herbs. Oecologia 139:359–375. doi: 10.1007/s00442-004-1518-2 PubMedCrossRefGoogle Scholar
  39. Moffatt SF, McLachlan SM (2004) Understorey indicators of disturbance for riparian forests along an urban-rural gradient in Manitoba. Ecol Indic 4:1–16. doi: 10.1016/j.ecolind.2003.08.002 CrossRefGoogle Scholar
  40. Mussey GJ, Potter DA (1997) Phenological correlations between flowering plants and activity of urban landscape pests in Kentucky. J Econ Entomol 90:1615–1627Google Scholar
  41. Pellis A, Laureysens I, Ceulemans R (2004) Genetic variation of the bud and leaf phenology of seventeen poplar clones in a short rotation coppice culture. Plant Biol 6:38–46. doi: 10.1055/s-2003-44746 PubMedCrossRefGoogle Scholar
  42. Remes V (2003) Effects of exotic habitat on nesting success, territory density, and settlement patterns in the Blackcap (Sylvia atricapilla). Conserv Biol 17:1127–1133. doi: 10.1046/j.1523-1739.2003.01611.x CrossRefGoogle Scholar
  43. Rodewald AD, Bakermans MH (2006) What is the appropriate paradigm for riparian forest conservation? Biol Conserv 128:193–200. doi: 10.1016/j.biocon.2005.09.041 CrossRefGoogle Scholar
  44. Rodewald AD, Shustack DP (2008) Urban flight: understanding individual and population-level responses of Nearctic-Neotropical migratory birds to urbanization. J Anim Ecol 77:83–91PubMedCrossRefGoogle Scholar
  45. Roetzer T, Wittenzeller M, Haeckel H, Nekovar J (2000) Phenology in central Europe—differences and trends of spring phenophases in urban and rural areas. Int J Biometeorol 44:60–66. doi: 10.1007/s004840000062 PubMedCrossRefGoogle Scholar
  46. Schwartz MD (2003) Phenology: an integrative environmental science. Kluwer Academic Publishers, Dordrecht, The NetherlandsGoogle Scholar
  47. Seiwa K (1999) Changes in leaf phenology are dependent on tree height in Acer mono, a deciduous broad-leaved tree. Ann Bot (Lond) 83:355–361. doi: 10.1006/anbo.1998.0831 CrossRefGoogle Scholar
  48. Shustack DP (2008) Reproductive timing of passerines in urbanizing landscapes. PhD dissertation, Ohio State University, Columbus, OH, USA, 236 ppGoogle Scholar
  49. Smith JW (1915) Phenological dates and meteorological data recorded by Thomas Mikesell at Wauseon, Fulton County, Ohio. Mon Weather Rev Suppl 2:21–93Google Scholar
  50. ter Braak CJF, Smilauer P (2002) Canoco reference manual and CanoDraw for windows user’s guide: software for canonical community ordination (version 4.5). Microcomputer PowerGoogle Scholar
  51. Tomita M, Seiwa K (2004) Influence of canopy tree phenology on understory populations of Fagus crenata. J Veg Sci 15:379–388. doi: 10.1658/1100-9233(2004)015[0379:IOCTPO]2.0.CO;2 Google Scholar
  52. Trelease W (1884) When the leaves appear. Wisc Agric Stn Annu Rep 1:56–73Google Scholar
  53. Tyrväinen L, Silvennoinen H, Kolehmainen O (2003) Ecological and aesthetic values in urban forest management. Urban For Urban Green 1:135–149. doi: 10.1078/1618-8667-00014 CrossRefGoogle Scholar
  54. Uemura S (1994) Patterns of leaf phenology in forest understory. Can J Bot 72:409–414. doi: 10.1139/b94-055 CrossRefGoogle Scholar
  55. Visser ME, van Noordwijk AJ, Tinbergen JM, Lessells CM (1998) Warmer springs lead to mistimed reproduction in great tits (Parus major). Proc Roy Soc Lond Ser B-Bio Sci 265:1867–1870CrossRefGoogle Scholar
  56. Visser ME, Holleman LJM, Gienapp P (2006) Shifts in caterpillar biomass phenology due to climate change and its impact on the breeding biology of an insectivorous bird. Oecologia 147:164–172. doi: 10.1007/s00442-005-0299-6 PubMedCrossRefGoogle Scholar
  57. White MA, Nemani RR, Thornton PE, Running SW (2002) Satellite evidence of phenological differences between urbanized and rural areas of the Eastern United States deciduous broadleaf forest. Ecosystems (NY, Print) 5:260–273. doi: 10.1007/s10021-001-0070-8 CrossRefGoogle Scholar
  58. Whitney GG, Adams SD (1980) Man as a maker of new plant communities. J App Ecol 17:431–448. doi: 10.2307/2402338 CrossRefGoogle Scholar
  59. Zhang X, Friedl MA, Schaaf CB et al (2004) The footprint of urban climates on vegetation phenology. Geophys Res Lett 31:L12209. doi: 10.1029/2004GL020137 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  • Daniel P. Shustack
    • 1
    • 2
  • Amanda D. Rodewald
    • 1
  • Thomas A. Waite
    • 3
  1. 1.School of Environment and Natural ResourcesOhio State UniversityColumbusUSA
  2. 2.Massachusetts College of Liberal ArtsNorth AdamsUSA
  3. 3.Department of Evolution, Ecology, and Organismal BiologyOhio State UniversityColumbusUSA

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