Abstract
The extent to which urban trees can support associated biodiversity and provide ecosystem services depends on how urbanization affects the relationship between plants and the herbivorous arthropods that feed on them. Previous studies suggest that urbanization tends to increase the abundance, but decrease the diversity of herbivorous arthropods, but also reveal that this pattern may be an artifact of a narrow focus on pests and ornamental plants. We aimed to assess the effect of urbanization on whole leaf herbivore communities of three native canopy trees, red oak (Quercus rubra), white oak (Quercus alba), and sugar maple (Acer saccharum). For each species we compared the extent of herbivory (assessed as percent leaf loss) and diversity of herbivores (using the number of identifiable damage types as a proxy for feeding guild diversity) between sites in southeast Michigan that were more forested vs. more urbanized (with lower tree density and canopy coverage and higher percent hardscape and turf). We found that across all three species and sites compared, both the percent leaf area lost to herbivory and the number of different types of herbivory were consistently and significantly higher in forested than urbanized sites. While future studies are needed to confirm the mechanisms responsible, we conclude that at least for native canopy tree species, trees in more urbanized sites do not appear to experience higher herbivory, and instead support diminished herbivore communities compared to the same trees in a more forested setting.
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Adams JM, Fang W, Callaway RM, Cipollini D, Newell E, Transatlantic Acer platanoides Invasion Network (TRAIN) (2009) A cross-continental test of the enemy release hypothesis: leaf herbivory on Acer platanoides (L.) is three times lower in North America than in its native Europe. Biol Invasions 11:1005–1016. https://doi.org/10.1007/s10530-008-9312-4
Aronson MFJ, Sorte FAL, Nilon CH et al (2014) A global analysis of the impacts of urbanization on bird and plant diversity reveals key anthropogenic drivers. Proc R Soc B 281:20133330. https://doi.org/10.1098/rspb.2013.3330
Balder H, Jäckel B, Pradel B (1999) Investigations on the existence of beneficial organisms on urban trees in Berlin. Acta Hortic:189–196. https://doi.org/10.17660/ActaHortic.1999.496.24
Bartens J, Day SD, Harris JR, Wynn TM, Dove JE (2009) Transpiration and root development of urban trees in structural soil Stormwater reservoirs. Environ Manag 44:646–657. https://doi.org/10.1007/s00267-009-9366-9
Beninde J, Veith M, Hochkirch A (2015) Biodiversity in cities needs space: a meta-analysis of factors determining intra-urban biodiversity variation. Ecol Lett 18:581–592. https://doi.org/10.1111/ele.12427
Bergh JC, Leskey TC, Walgenbach JF, Klingeman WE, Kain DP, Zhang A (2009) Dogwood borer (Lepidoptera: Sesiidae) abundance and seasonal flight activity in apple orchards, urban landscapes, and woodlands in five eastern states. Environ Entomol 38:530–538. https://doi.org/10.1603/022.038.0304
Bolger DT, Suarez AV, Crooks KR, Morrison SA, Case TJ (2000) Arthropods in urban habitat fragments in southern California: area, age, and edge effects. Ecol Appl 10:1230–1248. https://doi.org/10.1890/1051-0761(2000)010[1230:AIUHFI]2.0.CO;2
Cardinale BJ, Duffy JE, Gonzalez A, Hooper DU, Perrings C, Venail P, Narwani A, Mace GM, Tilman D, Wardle DA, Kinzig AP, Daily GC, Loreau M, Grace JB, Larigauderie A, Srivastava DS, Naeem S (2012) Biodiversity loss and its impact on humanity. Nature 486:59–67. https://doi.org/10.1038/nature11148
Carvalho MR, Wilf P, Barrios H, Windsor DM, Currano ED, Labandeira CC, Jaramillo CA (2014) Insect leaf-chewing damage tracks herbivore richness in modern and ancient forests. PLoS One 9:e94950. https://doi.org/10.1371/journal.pone.0094950
Christie FJ, Hochuli DF (2005) Elevated levels of herbivory in urban landscapes: are declines in tree health more than an edge effect? Ecol Soc 10(1):10
Christie FJ, Cassis G, Hochuli DF (2010) Urbanization affects the trophic structure of arboreal arthropod communities. Urban Ecosyst 13:169–180. https://doi.org/10.1007/s11252-009-0115-x
City of Ann Arbor (2014) City of Ann Arbor urban and community Forest management plan. Forestry Public Works, Ann Arbor. Available at https://www.a2gov.org/departments/forestry/Documents/UCFMP_FINAL_022515.pdf
Clarke KM, Fisher BL, LeBuhn G (2008) The influence of urban park characteristics on ant (Hymenoptera, Formicidae) communities. Urban Ecosyst 11:317–334. https://doi.org/10.1007/s11252-008-0065-8
Connor EF (1988) Plant water deficits and insect responses: the preference of Corythucha arcuata (Heteroptera: Tingidae) for the foliage of white oak, Quercus alba. Ecol Entomol 13:375–381. https://doi.org/10.1111/j.1365-2311.1988.tb00369.x
Connor EF, Hafernik J, Levy J, Lee Moore V, Rickman JK (2002) Insect conservation in an urban biodiversity hotspot: the San Francisco Bay Area. J Insect Conserv 6:247–259. https://doi.org/10.1023/A:1024426727504
Coulson RN, Witter JA (1984) Forest entomology: ecology and management, 1st edn. Wiley-Interscience, New York
Cranshaw W, Shetlar D (2017) Garden insects of North America: the ultimate guide to backyard bugs. Princeton University Press, Princeton
Cuevas-Reyes P, Gilberti L, González-Rodríguez A, Fernandes GW (2013) Patterns of herbivory and fluctuating asymmetry in Solanum lycocarpum St. Hill (Solanaceae) along an urban gradient in Brazil. Ecol Indic 24:557–561. https://doi.org/10.1016/j.ecolind.2012.08.011
Czech B (2005) Urbanization as a threat to biodiversity: trophic theory, economic geography, and implications for conservation land acquisition. Bengston David N Tech Ed Policies Manag Urban Growth Landsc Change Key Conserv 21st Century Gen Tech Rep NC-265 St Paul MN US Dep Agric For Serv North Cent Res Stn 8-13 265:
Dale AG, Frank SD (2014a) The effects of urban warming on herbivore abundance and street tree condition. PLoS One 9:e102996. https://doi.org/10.1371/journal.pone.0102996
Dale AG, Frank SD (2014b) Urban warming trumps natural enemy regulation of herbivorous pests. Ecol Appl 24:1596–1607. https://doi.org/10.1890/13-1961.1
Dickman CR (1987) Habitat fragmentation and vertebrate species richness in an urban environment. J Appl Ecol 24:337–351. https://doi.org/10.2307/2403879
Dreistadt SH, Dahlsten DL, Frankie GW (1990) Urban forests and insect ecology. BioScience 40:192–198. https://doi.org/10.2307/1311364
Faeth SH, Bang C, Saari S (2011) Urban biodiversity: patterns and mechanisms. Ann N Y Acad Sci 1223:69–81. https://doi.org/10.1111/j.1749-6632.2010.05925.x
Frank SD, Shrewsbury PM (2004) Effect of conservation strips on the abundance and distribution of natural enemies and predation of Agrotis ipsilon (Lepidoptera: Noctuidae) on golf course fairways. Environ Entomol 33:1662–1672. https://doi.org/10.1603/0046-225X-33.6.1662
Frankie GW, Ehler LE (1978) Ecology of insects in urban environments. Annu Rev Entomol 23:367–387. https://doi.org/10.1146/annurev.en.23.010178.002055
Gershenzon J (1984) Changes in the levels of plant secondary metabolites under water and nutrient stress. In: Phytochemical adaptations to stress. Springer, Boston, pp 273–320
Gossner MM, Pašalić E, Lange M, Lange P, Boch S, Hessenmöller D, Müller J, Socher SA, Fischer M, Schulze ED, Weisser WW (2014) Differential responses of herbivores and herbivory to Management in Temperate European Beech. PLoS One 9:e104876. https://doi.org/10.1371/journal.pone.0104876
Hanks LM, Denno RF (1993) Natural enemies and plant water relations influence the distribution of an armored scale insect. Ecology 74:1081–1091. https://doi.org/10.2307/1940478
Herms DA (2002) Effects of fertilization on insect resistance of Woody ornamental plants: reassessing an entrenched paradigm. Environ Entomol 31:923–933. https://doi.org/10.1603/0046-225X-31.6.923
Hiura T, Nakamura M (2013) Different mechanisms explain feeding type-specific patterns of latitudinal variation in herbivore damage among diverse feeding types of herbivorous insects. Basic Appl Ecol 14:480–488. https://doi.org/10.1016/j.baae.2013.06.004
Huberty AF, Denno RF (2004) Plant water stress and its consequences for herbivorous insects: a new synthesis. Ecology 85:1383–1398
Inbar M, Doostdar H, Mayer RT (2001) Suitability of stressed and vigorous plants to various insect herbivores. Oikos 94:228–235. https://doi.org/10.1034/j.1600-0706.2001.940203.x
Kozlov MV, Zvereva EL (2017) Background insect herbivory: impacts, patterns and methodology. In: Progress in botany, vol 79. Springer, Cham, pp 313–355
Kozlov MV, Lanta V, Zverev V, Rainio K, Kunavin MA, Zvereva EL (2017) Decreased losses of woody plant foliage to insects in large urban areas are explained by bird predation. Glob Chang Biol 23:4354–4364. https://doi.org/10.1111/gcb.13692
Kytö M, Niemelä P, Larsson S (1996) Insects on trees: population and individual response to fertilization. Oikos 75:148–159. https://doi.org/10.2307/3546238
Labandeira CC, Wilf P, Johnson KR, Marsh F (2007) Guide to insect (and other) damage types on compressed plant fossils. Version 3.0. Smithson Inst Wash DC 25 p
Letourneau DK, Jedlicka JA, Bothwell SG, Moreno CR (2009) Effects of natural enemy biodiversity on the suppression of arthropod herbivores in terrestrial ecosystems. Annu Rev Ecol Evol Syst 40:573–592. https://doi.org/10.1146/annurev.ecolsys.110308.120320
Luck GW, Smallbone LT (2010) Species diversity and urbanization: patterns, drivers and implications. In: Gaston KJ (ed) Urban ecology. Cambridge University Press, Cambridge, pp 88–119
Mata L, Threlfall CG, Williams NSG, Hahs AK, Malipatil M, Stork NE, Livesley SJ (2017) Conserving herbivorous and predatory insects in urban green spaces. Sci Rep 7:40970. https://doi.org/10.1038/srep40970
Mattson WJ, Haack RA (1987) The role of drought in outbreaks of plant-eating insects. BioScience 37:110–118. https://doi.org/10.2307/1310365
McDonnell MJ, Pickett STA (1990) Ecosystem structure and function along urban-rural gradients: an unexploited opportunity for ecology. Ecology 71:1232–1237. https://doi.org/10.2307/1938259
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
McIntyre NE (2000) Ecology of urban arthropods: a review and a call to action. Ann Entomol Soc Am 93:825–835. https://doi.org/10.1603/0013-8746(2000)093[0825:EOUAAR]2.0.CO;2
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
Metcalfe DB, Asner GP, Martin RE, Silva Espejo JE, Huasco WH, Farfán Amézquita FF, Carranza-Jimenez L, Galiano Cabrera DF, Baca LD, Sinca F, Huaraca Quispe LP, Taype IA, Mora LE, Dávila AR, Solórzano MM, Puma Vilca BL, Laupa Román JM, Guerra Bustios PC, Revilla NS, Tupayachi R, Girardin CAJ, Doughty CE, Malhi Y (2014) Herbivory makes major contributions to ecosystem carbon and nutrient cycling in tropical forests. Ecol Lett 17:324–332. https://doi.org/10.1111/ele.12233
Nowak DJ, Greenfield EJ (2018) US urban Forest statistics, values, and projections. J For 116:164–177. https://doi.org/10.1093/jofore/fvx004
Nowak DJ, Crane DE, Stevens JC (2006) Air pollution removal by urban trees and shrubs in the United States. Urban For Urban Green 4:115–123. https://doi.org/10.1016/j.ufug.2006.01.007
Nuckols MS, Connor EF (1995) Do trees in urban or ornamental plantings receive more damage by insects than trees in natural forests? Ecol Entomol 20:253–260. https://doi.org/10.1111/j.1365-2311.1995.tb00455.x
Öckinger E, Dannestam Å, Smith HG (2009) The importance of fragmentation and habitat quality of urban grasslands for butterfly diversity. Landsc Urban Plan 93:31–37. https://doi.org/10.1016/j.landurbplan.2009.05.021
Pataki DE, Alig RJ, Fung AS et al (2006) Urban ecosystems and the north American carbon cycle. Glob Chang Biol 12:2092–2102. https://doi.org/10.1111/j.1365-2486.2006.01242.x
Pineda A, Pangesti N, Soler R, Dam NM, Loon JJA, Dicke M (2016) Negative impact of drought stress on a generalist leaf chewer and a phloem feeder is associated with, but not explained by an increase in herbivore-induced indole glucosinolates. Environ Exp Bot 123:88–97. https://doi.org/10.1016/j.envexpbot.2015.11.007
Raupp MJ, Shrewsbury PM, Herms DA (2010) Ecology of herbivorous arthropods in urban landscapes. Annu Rev Entomol 55:19–38. https://doi.org/10.1146/annurev-ento-112408-085351
Rogers LE, Grant JF (1991) Seasonal incidence of male dogwood borer (Lepidoptera: Sesiidae) and other species of clearwing moths in selected habitats in Tennessee. Environ Entomol 20:520–525. https://doi.org/10.1093/ee/20.2.520
Saari S, Richter S, Higgins M, Oberhofer M, Jennings A, Faeth SH (2016) Urbanization is not associated with increased abundance or decreased richness of terrestrial animals - dissecting the literature through meta-analysis. Urban Ecosyst 19:1251–1264. https://doi.org/10.1007/s11252-016-0549-x
Shrewsbury PM, Raupp MJ (2006) Do top-down or bottom-up forces determine Stephanitis Pyrioides abundance in urban landscapes? Ecol Appl 16:262–272. https://doi.org/10.1890/04-1347
Shrewsbury PM, Lashomb JH, Hamilton GC et al (2004) The influence of flowering plants on herbivore and natural enemy abundance in ornamental landscapes. Int J Ecol Environ Sci 30:23–33
Speight MR, Hails RS, Gilbert M, Foggo A (1998) Horse chestnut scale (pulvinaria Regalis) (homoptera: Coccidae) and urban host tree environment. Ecology 79:1503–1513. https://doi.org/10.1890/0012-9658(1998)079[1503:HCSPRH]2.0.CO;2
Sperling CD, Lortie CJ (2010) The importance of urban backgardens on plant and invertebrate recruitment: a field microcosm experiment. Urban Ecosyst 13:223–235. https://doi.org/10.1007/s11252-009-0114-y
Sperry CE, Chaney WR, Shao G, Sadof CS (2001) Effects of tree density, tree species diversity and percentage of hardscape on three insect pests of honeylocust. J Arboric 27:263–271
Sternburg JG, Waldbauer GP, Scarbrough AG (1981) Distribution of cecropia moth (Saturniidae) in Central Illinois: a study in urban ecology. J Lepidopterists Soc 35:304–320
Su Z, Zhang R, Qiu J (2011) Decline in the diversity of willow trunk-dwelling weevils (Coleoptera: Curculionoidea) as a result of urban expansion in Beijing, China. J Insect Conserv 15:367–377. https://doi.org/10.1007/s10841-010-9310-6
Suarez AV, Bolger DT, Case TJ (1998) Effects of fragmentation and invasion on native ant communities in coastal Southern California. Ecology 79:2041–2056. https://doi.org/10.2307/176708
Sushinsky JR, Rhodes JR, Possingham HP, Gill TK, Fuller RA (2013) How should we grow cities to minimize their biodiversity impacts? Glob Chang Biol 19:401–410. https://doi.org/10.1111/gcb.12055
Szczepaniec A, Creary SF, Laskowski KL, Nyrop JP, Raupp MJ (2011) Neonicotinoid insecticide Imidacloprid causes outbreaks of spider mites on elm trees in urban landscapes. PLoS One 6:e20018. https://doi.org/10.1371/journal.pone.0020018
Tallamy DW (2004) Do alien plants reduce insect biomass? Conserv Biol 18:1689–1692. https://doi.org/10.1111/j.1523-1739.2004.00512.x
Tallamy DW (2009) Bringing nature home: how you can sustain wildlife with native plants, updated and expanded. Timber Press, Portland
Tooker JF, Hanks LM (2000) Influence of plant community structure on natural enemies of pine needle scale (Homoptera: Diaspididae) in urban landscapes. Environ Entomol 29:1305–1311. https://doi.org/10.1603/0046-225X-29.6.1305
USDM (2018) U.S. Drought Monitor National Drought Mitigation Center University of Nebraska-Lincoln - Time Series. http://droughtmonitor.unl.edu/Data/Timeseries.aspx. Accessed 4 May 2018
White TCR (1969) An index to measure weather-induced stress of trees associated with outbreaks of psyllids in Australia. Ecology 50:905–909. https://doi.org/10.2307/1933707
White TCR (1984) The abundance of invertebrate herbivores in relation to the availability of nitrogen in stressed food plants. Oecologia 63:90–105. https://doi.org/10.1007/BF00379790
Wilson EO (1987) The little things that run the world (the importance and conservation of invertebrates). Conserv Biol 1:344–346
Wood BC, Pullin AS (2002) Persistence of species in a fragmented urban landscape: the importance of dispersal ability and habitat availability for grassland butterflies. Biodivers Conserv 11:1451–1468. https://doi.org/10.1023/A:1016223907962
Acknowledgments
We thank data collection assistants Cria Kay, Vitor Machado Lira, Lingzi Liu, Elissa Mueller, Emily Nummer, and Ryan Moya. Maricela Avalos and Jane Immonen provided tree density information on sites. Dan Katz and Eliot Jackson gave valuable comments on earlier drafts of the manuscript. This project was an extension of laboratory activities in ecology which were funded in part by a donation from Greg Goldring in support of field-based learning opportunities at the University of Michigan School for Environment and Sustainability.
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Schueller, S.K., Paul, S., Payer, N. et al. Urbanization decreases the extent and variety of leaf herbivory for native canopy tree species Quercus rubra, Quercus alba, and Acer saccharum. Urban Ecosyst 22, 907–916 (2019). https://doi.org/10.1007/s11252-019-00866-6
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DOI: https://doi.org/10.1007/s11252-019-00866-6