Abstract
Predation by natural enemies is important for regulating herbivore abundance and herbivory. Theory predicts that complex habitats support more natural enemies, which exert top-down control over arthropods and therefore can reduce herbivory. However, it is unclear if theory developed in other more natural systems similarly apply to predation by vertebrate and invertebrate natural enemies across urban habitats of varying complexity. We used plasticine caterpillar models to assess risk of predation by birds and insects, collected leaf-feeding arthropods, and measured herbivory in willow oak trees (Quercus phellos) in two seasons to determine how predation influenced herbivory across urban forest fragments, street trees planted near forest fragments, and downtown street trees. Predation attempts by birds and abundance of chewing folivores were greater on trees growing in urban forest fragments than downtown street trees. Bird predation attempts and herbivory levels were inconsistent for near-forest trees. Predation attempts by arthropods did not statistically vary among the three urban tree habitats. Contrary to expectations based on theory, chewing folivore abundance and herbivory were generally highest on trees growing in urban forests, the most complex habitat we studied, and the habitat where risk of bird predation was greatest. We suggest that urban forest fragments provide better habitat than other urban landscapes for both urban birds and chewing folivores by having greater habitat complexity. Therefore, basal resources, such as availability of suitable habitat, mediate top-down effects on herbivores in cities.
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References
Agrawal A (1997) Do leaf domatia mediate a plant-mite mutualism? An experimental test of the effects on predators and herbivores. Ecological Entomology 22:371–376
Andow DA, Risch SJ (1985) Predation in diversified Agroecosystems: relations between a Coccinellid predator Coleomegilla maculata and its food. The Journal of Applied Ecology 22:357
Araujo APA, De Paula JD, Carneiro MAA, Schoereder JH (2006) Effects of host plant architecture on colonization by galling insects. Austral Ecology 31:343–348
Aronson MFJ, La Sorte FA, Nilon CH, Katti M, Goddard MA, Lepczyk CA, Warren PS, Williams NSG, Cilliers S, Clarkson B, Dobbs C, Dolan R, Hedblom M, Klotz S, Kooijmans 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
Aronson MF, Lepczyk CA, Evans KL, Goddard MA, Lerman SB, MacIvor JS, Nilon CH, Vargo T (2017) Biodiversity in the city: key challenges for urban green space management. Front Ecol Environ 15:189–196
Asaro C, Chamberlin LA (2015) Outbreak history (1953-2014) of spring defoliators impacting oak-dominated forests in Virginia, with emphasis on gypsy moth ( Lymantria dispar L.) and fall cankerworm ( Alsophila pometaria Harris). Am Entomol 61:174–185
Atlegrim O (1989) Exclusion of birds from bilberry stands: impact on insect larval density and damage to the bilberry. Oecologia 79:136–139
Auman, H.J., Meathrel, C.E. & Richardson, A. (2008) Supersize me: does anthropogenic food change the body condition of silver gulls? A comparison between urbanized and remote, non-urbanized areas. https://doi.org/10.1675/1524-4695(2008)31[122:SMDAFC]2.0.CO;2, 31, 122–127
Barbosa P, Hines J, Kaplan I, Martinson H, Szczepaniec A, Szendrei Z (2009) Associational resistance and associational susceptibility: having right or wrong neighbors. Annu Rev Ecol Evol Syst 40:1–20
Baudry J, Burel F (2004) Trophic flows and spatial heterogeneity in agricultural landscapes. In: Polis GA, Power ME, Huxel GR (eds) Food webs at the landscape level. University of Chicago Press, Chicago, pp 317–322
Beissinger SR, Osborne DR (1982) Effects of urbanization on avian community organization. Condor 84:75
Blair, R. (2004) The effects of urban sprawl on birds at multiple levels of biological organization. Ecology and Society, 9, art2
Blake JG (1983) Trophic structure of bird communities in Forest patches in east-Central Illinois on JSTOR. The Wilson Bulletin 95:416–430
Bock CE, Bock JH, Grant MC (1992) Effects of bird predation on grasshopper densities in an Arizona grassland. Ecology 73:1706–1717
Böhm, S.M., Wells, K. & Kalko, E.K. V. (2011) Top-down control of Herbivory by birds and bats in the canopy of temperate broad-leaved oaks (Quercus robur) ed B. Fenton PLoS ONE, 6, e17857
Bonifacio, R.S. (2008) The effects of structural and floristic diversity of shelterbelts on the abundance and diversity of birds and bats on farms. The University of Sydney, Australia
Borer ET, Seabloom EW, Tilman D (2012) Plant diversity controls arthropod biomass and temporal stability. Ecol Lett 15:1457–1464
Braaker S, Ghazoul J, Obrist MK, Moretti M (2014) Habitat connectivity shapes urban arthropod communities: the key role of green roofs. Ecology 95:1010–1021
Buckner CH, Turnock WJ (1965) Avian predation on the larch sawfly, Pristiphora Erichsonii (HTG.), (Hymenoptera: Tenthredinidae). Ecology 46:223–236
Burghardt KT, Tallamy DW, Shriver GW (2009) Impact of native plants on bird and butterfly biodiversity in suburban landscapes. Conserv Biol 23:219–224
Burghardt KT, Tallamy DW, Philips C, Shropshire KJ (2010) Non-native plants reduce abundance, richness, and host specialization in lepidopteran communities. Ecosphere 1:art11
Chace JF, Walsh JJ (2006) Urban effects on native avifauna: a review. Landsc Urban Plan 74:46–69
Christie, F. & Hochuli, D. (2005) Elevated levels of herbivory in urban landscapes: are declines in tree health more than an edge effect? Ecology And Society, 10
Cobb NS, Mopper S, Gehring CA, Caouette M, Christensen KM, Whitham TG (1997) Increased moth herbivory associated with environmental stress of pinyon pine at local and regional levels. Oecologia 109:389–397
Coffelt MA, Schultz PB (1990) Development of an aesthetic injury level to decrease pesticide use against Orange striped Oakworm (Lepidoptera: Saturniidae) in an urban Pest management project. J Econ Entomol 83:2044–2049
Craig TP, Wagner MR, McCullough DG, Frantz DP (1991) Effects of experimentally altered plant moisture stress on the performance of Neodiprion sawflies. For Ecol Manag 39:247–261
Cregg BM, Dix ME (2001) Tree moisture stress and insect damage in urban areas in relation to heat island effects. J Arboric 27
Crooks KR, Suarez AV, Bolger DT (2004) Avian assemblages along a gradient of urbanization in a highly fragmented landscape. Biol Conserv 115:451–462
Dale AG, Frank SD (2014) The effects of urban warming on herbivore abundance and street tree condition. PLoS One 9:e102996
Dale AG, Frank SD (2018) Urban plants and climate drive unique arthropod interactions with unpredictable consequences. Current Opinion in Insect Science 29:27–33
Dreistadt SH, Dahlsten DL, Frankie GW (1990) Urban forests and insect Ecology. BioScience 40:192–198
Feeny, P. (1976) Plant Apparency and chemical defense. Biochemical Interaction Between Plants and Insects, pp. 1–40. Springer US, Boston, MA
Ferrante M, Lo Cacciato A, Lövei GL (2014) Quantifying predation pressure along an urbanisation gradient in Denmark using artificial caterpillars. European Journal of Entomology 111:649–654
Finke DL, Denno RF (2002) Intraguild predation diminished in complex structured vegetation: implications for prey suppression. Ecology 83:643–652
Floater G (1997) Rainfall, nitrogen and host plant condition: consequences for the processionary caterpillar, Ochrogaster lunifer. Ecological Entomology 22:247–255
Frank SD (2014) Bad neighbors: urban habitats increase cankerworm damage to non-host understory plants. Urban Ecosyst 17:1135–1145
Frankie GW, Ehler LE (1978) Ecology of insects in urban environments. Annu Rev Entomol 23:367–387
Frey D, Vega K, Zellweger F, Ghazoul J, Hansen D, Moretti M (2018) Predation risk shaped by habitat and landscape complexity in urban environments ed M. Stanley Journal of Applied Ecology 55:2343–2353
Gámez-Virués S, Gurr GM, Raman A, Nicol HI (2010) Plant diversity and habitat structure affect tree growth, herbivory and natural enemies in shelterbelts. Basic and Applied Ecology 11:542–549
Gaston, K.J. (2010) Urban Ecology. Cambridge University Press
Germaine SS, Rosenstock SS, Schweinsburg RE, Richardson WS (1998) Relationships among breeding birds, habitat, and residential development in greater Tucson, Arizona. Ecol Appl 8:680–691
Gilroy JJ, Anderson GQA, Grice PV, Vickery JA, Watts PN, Sutherland WJ (2009) Foraging habitat selection, diet and nestling condition in yellow wagtails Motacilla flava breeding on arable farmland. Bird Study 56:221–232
González-Gómez PL, Estades CF, Simonetti JA (2006) Strengthened insectivory in a temperate fragmented forest. Oecologia 148:137–143
Greenberg R, Bichier P, Angon AC, MacVean C, Perez R, Cano E (2000) The impact of avian insectory on arthropods and leaf damage in some Guatemalan coffee plantations. Ecology 81:1750–1755
Grostal R, O’Dowd DJ (1994) Plants, mites and mutualism: leaf domatia and the abundance and reproduction of mites on Viburnum tinus (Caprifoliaceae). Oecologia 97:308–315
Gunnarsson B (1996) Bird predation and vegetation structure affecting spruce-living arthropods in a temperate Forest. J Anim Ecol 65:389
Haddad NM, Tilman D, Haarstad J, Ritchie M, Knops JM (2001) Contrasting effects of plant richness and composition on insect communities: a field experiment. Am Nat 158:17–35
Hanks LM, Denno RF (1993) Natural enemies and plant water relations influence the distribution of an armored scale insect. Ecology 74:1081–1091
Hanson PJ, Dickson RE, Isebrands JG, Crow TR, Dixon RK (1986) A morphological index of Quercus seedling ontogeny for use in studies of physiology and growth. Tree Physiol 2:273–281
Herms, D.A. (2002) Strategies for deployment of insect resistant ornamental plants. Mechanisms and Deployment of Resistance in Trees to Insects, pp. 217–237. Kluwer academic publishers, Dordrecht
Hochuli, D.F. & Threlfall, C.G. (2017) Planning for protection : promoting pest suppressing urban landscapes through habitat management. Urban Biodiversity From Research to Practice (eds O. Alessandra & N. Jari), pp. 54–70. Routledge
Holmes RT, Schultz JC, Nothnagle P (1979) Bird predation on Forest insects: an Exclosure experiment. Science 206:462–463
Huberty AF, Denno RF (2004) Plant water stress and its consequences for herbivorous insects: a new synthesis. Ecology 85:1383–1398
JMP® Pro, Version 13.0.0. SAS Institute Inc., Cary, NC, 1987–2007
Kareiva P (1987) Habitat fragmentation and the stability of predator–prey interactions. Nature 326:388–390
Kareiva P, Sahakian R (1990) Tritrophic effects of a simple architectural mutation in pea plants. Nature 345:433–434
Karp, D.S., Mendenhall, C.D., Sandí, R.F., Chaumont, N., Ehrlich, P.R., Hadly, E.A. & Daily, G.C. (2013) Forest bolsters bird abundance, pest control and coffee yield ed J Lawler Ecology Letters, 16, 1339–1347
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
La Sorte FA, Lepczyk CA, Aronson MFJ, Goddard MA, Hedblom M, Katti M, MacGregor-Fors I, Mörtberg U, Nilon CH, Warren PS, Williams NSG, Yang J (2018) The phylogenetic and functional diversity of regional breeding bird assemblages is reduced and constricted through urbanization. Divers Distrib 24:928–938
Langellotto GA, Denno RF (2004) Responses of invertebrate natural enemies to complex-structured habitats: a meta-analytical synthesis. Oecologia 139:1–10
Long LC, D’Amico V, Frank SD (2019) Urban forest fragments buffer trees from warming and pests. Sci Total Environ 658:1523–1530
Loram A, Warren PH, Gaston KJ (2008) Urban domestic gardens (XIV): the characteristics of gardens in five cities. Environ Manag 42:361–376
Lunney, D. & Burgin, S. (2004) Ecology of Sydney’s urban fragments: has fragmentation taken the sting outof insect herbivory? Forum on Urban Wildlife - More than meets the Eye. Royal Zoological Society of New South Wales., pp. 63–69. Royal Zoological Society of New South Wales, Mosman, Australia
Lys J-A, Zimmermann M, Nentwig W (1994) Increase in activity density and species number of carabid beetles in cereals as a result of strip-management. Entomologia Experimentalis et Applicata 73:1–9
Maas B, Clough Y, Tscharntke T (2013) Bats and birds increase crop yield in tropical agroforestry landscapes ed F. Courchamp. Ecol Lett 16:1480–1487
MacArthur RH, MacArthur JW (1961) On bird species diversity. Ecology 42:594–598
Marquis RJ, Whelan CJ (1994) Insectivorous birds increase growth of White oak through consumption of leaf-chewing insects. Ecology 75:2007–2014
Marzluff, J.M. (1997) Effects of urbanization and recreation on songbirds. In: songbird Ecology in southwestern ponderosa pine forests: a literature review. Gen. Tech. Re RM-GTR-292. US Department of Agriculture, Forest Service
Mattson WJ, Haack RA (1987) The role of drought stress in provoking outbreaks of phytophagous insects. In: Barbosa P, Schultz J (eds) Insect outbreaks. Academic Press, San Diego, pp 365–407
Meineke E, Youngsteadt E, Dunn RR, Frank SD (2016) Urban warming reduces aboveground carbon storage. Proc R Soc B Biol Sci 283:20161574
Meyer ST, Scheithe L, Hertzog L, Ebeling A, Wagg C, Roscher C, Weisser WW (2017) Consistent increase in herbivory along two experimental plant diversity gradients over multiple years. Ecosphere 8:e01876
Moorman CE, Bowen LT, Kilgo JC, Sorenson CE, Hanula JL, Horn S, Ulyshen MD (2007) Seasonal diets of insectivorous birds using canopy gaps in a bottomland forest. Journal of Field Ornithology 78:11–20
Mopper S, Whitham TG (1992) The plant stress paradox: effects on Pinyon sawfly sex ratios and fecundity. Ecology 73:515–525
Muiruri EW, Rainio K, Koricheva J (2016) Do birds see the forest for the trees? Scale-dependent effects of tree diversity on avian predation of artificial larvae. Oecologia 180:619–630
Nelson, G., Earle, C.J., Spellenberg, R., More, D. & Hughes, A.K. (2014) Trees of Eastern North America (ed a.K. Hughes). Princeton University press
Noukoun C, Bryant G, Frank SD (2014) The effect of sticky bands on cankerworm abundance and defoliation in urban trees, discovery Service for North Carolina State Univ Libraries. Arboricult Urban For 40:135–142
Nuckols MS, Connor EF (1995) Do trees in urban or ornamental plantings receive more damage by insects than trees in natural forests? Ecological Entomology 20:253–260
Pagani-Núñez E, Renom M, Mateos-Gonzalez F, Cotín J, Senar JC (2017) The diet of great tit nestlings: comparing observation records and stable isotope analyses. Basic and Applied Ecology 18:57–66
Parsons, S.E. & Frank, S.D. (2019) Urban tree pests and natural enemies respond to habitat at different spatial scales. Journal of Urban Ecology, 5
Philpott SM, Bichier P (2017) Local and landscape drivers of predation services in urban gardens. Ecol Appl 27:966–976
Poch TJ, Simonetti JA (2013) Insectivory in Pinus radiata plantations with different degree of structural complexity. For Ecol Manag 304:132–136
Posa MRC, Sodhi NS, Koh LP (2007) Predation on artificial nests and caterpillar models across a disturbance gradient in Subic Bay, Philippines. J Trop Ecol 23:27–33
Poulin B, Lefebvre G (1996) Dietary relationships of migrant and resident birds from a humid Forest in Central Panama. Auk 113:277–287
Price PW, Bouton CE, Gross P, McPheron BA, Thompson JN, Weis AE (1980) Interactions among three trophic levels: influence of plants on interactions between insect herbivores and natural enemies. Annu Rev Ecol Syst 11:41–65
Raupp MJ, Shrewsbury PM, Holmes JJ, Davidson JA (2001) Plant species diversity and abundance affects the number of arthropod pests in residential landscapes. J Arboric 27
Raupp MJ, Shrewsbury PM, Herms DA (2010) Ecology of herbivorous arthropods in urban landscapes. Annu Rev Entomol 55:19–38
Riechert SE, Bishop L (1990) Prey control by an assemblage of generalist predators: spiders in garden test systems. Ecology 71:1441–1450
Roda A, Nyrop J, Dicke M, English-Loeb G (2000) Trichomes and spider-mite webbing protect predatory mite eggs from intraguild predation. Oecologia 125:428–435
Rodewald P (ed) (2015) The birds of North America. Cornell Laboratory of Ornithology, Ithaca
Root RB (1973) Organization of a Plant-Arthropod Association in simple and diverse habitats: the Fauna of collards (Brassica Oleracea). Ecol Monogr 43:95–124
Sanders D, Nickel H, Grützner T, Platner C (2008) Habitat structure mediates top–down effects of spiders and ants on herbivores. Basic and Applied Ecology 9:152–160
Sattler T, Obrist MK, Duelli P, Moretti M (2011) Urban arthropod communities: added value or just a blend of surrounding biodiversity? Landsc Urban Plan 103:347–361
Schneider CA, Rasband WS, Eliceiri KW (2012) NIH image to Image J: 25 years of image analysis. Nat Methods 9:671–675
Schulz, B.K., Bechtold, W.A. & Zarnoch, S.J. (2009) Sampling and estimation procedures for the vegetation diversity and structure Indicator
Sekercioglu CH, Ehrlich PR, Daily GC, Aygen D, Goehring D, Sandi RF (2002) Disappearance of insectivorous birds from tropical forest fragments. Proceedings of the National Academy of Sciences of the United States of America 99:263–267
Shrewsbury PM, Raupp MJ (2000) Evaluation of components of Vegetational texture for predicting azalea lace bug, Stephanitis pyrioides (Heteroptera: Tingidae), abundance in managed landscapes. Environ Entomol 29:919–926
Shrewsbury PM, Raupp MJ (2006) Do top-down or bottom-up forces determine Stephanitis Pyrioides abundance in urban landscapes? Ecol Appl 16:262–272
Sipura M (1999) Tritrophic interactions: willows, herbivorous insects and insectivorous birds. Oecologia 121:537–545
Sloan JL, Jacobs DF (2016) Ontogeny influences developmental physiology of post-transplant Quercus rubra seedlings more than genotype. Ann For Sci 73:987–993
Southwood TRE (1961) The number of species of insect associated with various trees. J Anim Ecol 30:1
Southwood TRE, Moran VC, Kennedy CEJ (1982) The richness, abundance and biomass of the arthropod communities on trees. J Anim Ecol 51:635
Sperry CE, Chaney WR, Shao G, Sadof C (2001) Effects of tree density, tree species diversity, and percentage of hardscape on three insect pests of honeylocust. J Arboric 27:263–271
Tallamy DW, Shropshire KJ (2009) Ranking Lepidopteran use of native versus introduced plants. Conserv Biol 23:941–947
Thomas AT, Hodkinson ID (1991) Nitrogen, water stress and the feeding efficiency of Lepidopteran herbivores. The Journal of Applied Ecology 28:703
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
Tratalos J, Fuller RA, Warren PH, Davies RG, Gaston KJ (2007) Urban form, biodiversity potential and ecosystem services. Landsc Urban Plan 83:308–317
Tremblay A, Mineau P, Stewart R (2001) Effects of bird predation on some pest insect populations in corn. Agric Ecosyst Environ 83:143–152
Tscharntke T, Tylianakis JM, Rand TA, Didham RK, Fahrig L, Batáry P, Bengtsson J, Clough Y, Crist TO, Dormann CF, Ewers RM, Fründ J, Holt RD, Holzschuh A, Klein AM, Kleijn D, Kremen C, Landis DA, Laurance W, Lindenmayer D, Scherber C, Sodhi N, Steffan-Dewenter I, Thies C, van der Putten WH, Westphal C (2012) Landscape moderation of biodiversity patterns and processes - eight hypotheses. Biol Rev 87:661–685
Turrini T, Sanders D, Knop E (2016) Effects of urbanization on direct and indirect interactions in a tri-trophic system. Ecol Appl 26:664–675
Van Bael SA, Brawn JD (2005) The direct and indirect effects of insectivory by birds in two contrasting Neotropical forests. Oecologia 145:658–668
Van Bael SA, Philpott SM, Greenberg R, Bichier P, Barber NA, Mooney KA, Gruner DS (2008) Birds as predators in tropical agroforestry systems. Ecology 89:928–934
Vehviläinen H, Koricheva J, Ruohomäki K (2007) Tree species diversity influences herbivore abundance and damage: meta-analysis of long-term forest experiments. Oecologia 152:287–298
White AJ, Wratten SD, Berry NA, Weigmann U (1995) Habitat manipulation to enhance biological control of Brassica pests by hover flies (Diptera: Syrphidae). J Econ Entomol 88:1171–1176
Woronecki, P.P. & Dolbeer, R.A. (1980) The influence of insects in bird damage control. Conference, Proceedings of the 9th Vertebrate Pest, pp. 53–59
Acknowledgements
This project was supported by Cooperative Agreement no. G15AP00153 from the United States Geological Survey. Its contents are solely the responsibility of the authors and do not necessarily represent the views of the Department of the Interior Southeast Climate Adaptation Science Center or the USGS. Funding for this work was also provided by a Southeast Climate Adaptation Science Center graduate fellowship awarded to L.C.L. This study was funded by an Agricultural and Food Research Initiative Competitive grant no. (2013-02476) and an ARDP grant no. (2016-70006-25827 from the USDA National Institute of Food and Agriculture to S.D.F.). The North Carolina State University Department of Entomology also contributed support for this research. We thank Michael Reiskind, Barbara Fair, Vince D’Amico, Rob Dunn, Michael Just and two anonymous reviewers for providing valuable comments on the manuscript.
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Long, L.C., Frank, S.D. Risk of bird predation and defoliating insect abundance are greater in urban forest fragments than street trees. Urban Ecosyst 23, 519–531 (2020). https://doi.org/10.1007/s11252-020-00939-x
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DOI: https://doi.org/10.1007/s11252-020-00939-x
Keywords
- Forest fragments
- Urban birds
- Defoliators
- Street trees
- Top-down control