Abstract
Exotic plants are common in urban landscapes and are often planted by landscape managers in an effort to reduce herbivory damage and improve landscape aesthetics. However, exotic plants may be less palatable to many native insects and reduce herbivore biomass that may fuel higher trophic levels. Furthermore, a loss of herbivores in exotic ornamental landscapes may reduce top-down control by natural enemies. In this study, we compare herbivory in native and exotic congener ornamental landscapes. We also explore if caterpillar abundance, natural enemy abundance, diversity, community composition, spider biomass, and egg predation differ between the two landscape types. We predicted that herbivory, as well as natural enemy abundance and predation would be greater in native landscapes. Although we found that leaf area lost to herbivory was greater in native plots in one of the collection years, this relationship was weak. Natural enemy diversity differed between landscape types, but depended on plant genus. The relationship between plant origin and natural enemy diversity was also weak. Caterpillar abundance, natural enemy community composition, spider biomass, and predation services did not differ between treatments. Overall, our results suggest that ornamental landscapes planted in native plants may not differ from landscapes planted in exotic congeners in the pest management and conservation services they provide, particularly with regard to invertebrate natural enemies. However, our findings cannot be used to make more general claims about plant origin, especially with regard to native plants and non-congeners, as we only compared ornamental landscapes with native plants and their exotic congeners in this study. We conclude that for optimizing natural enemy diversity and biomass on city landscapes, plant choice and other plant traits may be as important as plant origin to consider. Our work demonstrates that both native and exotic congener ornamental landscapes provide valuable ecosystem services and will help guide landscape design that serves both the people and wildlife that use them.
Similar content being viewed by others
References
Alliende MC (1989) Demographic studies of a dioecious tree. II. the distribution of leaf predation within and between trees. J Ecol 77(4):1048–1058
Ambrosino MD, Jepson PC, Luna JM, Wratten SD (2006) Environ Entomol 35(2):394–400
Andow DA (1990) Population dynamics of an insect herbivore in simple and diverse habitats. Ecol 7(3):1006–1017
Andow DA (1991) Vegetational diversity and arthropod population response. Annu Rev Entomol 36(1):561–586
Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67(1):1–48
Bell JRW, Cullen WR, (2001) The implications of grassland and heathland management for the Conservation of spider communities: a review. J Zool 255(3):377–387
Bernays E, Graham M (1988) On the evolution of host specificity in phytophagous arthropods. Ecology 69:886–892
Braman SK, Pendley AF, Corley N (2002) Influence of commercially available wildflower mixes on beneficial arthropod abundance and predation in turfgrass. Environ Entomol 31:564–572
Burghardt KT, Tallamy DW (2013) Plant origin asymmetrically impacts feeding guilds and life stages driving community structure of herbivorous arthropods. Divers Distrib 19:1553–1565
Burghardt KT, Tallamy DW, Shriver WG (2009) Impact of native plants on bird and butterfly biodiversity in suburban landscapes. Conserv Biol 23(1):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(5):22
Burghardt KT, Tallamy DW, Sax D (2015) Not all non-natives are equally unequal: reductions in herbivore β diversity depend on phylogenetic similarity to native plant community. Ecol Lett 18(10):1087–1098
Buri P, Humbert JY, Stanska M, Hajdamowicz I, Tran E, Entling MH, Arlettaz R (2016) Delayed mowing promotes planthoppers, leafhoppers, and spiders in extensively managed meadows. Insect Conserv Divers 9:536–545
Cappuccino N, Arnason JT (2006) Novel chemistry of invasive exotic plants. Biol Let 2(2):189–193
Carpenter D, Cappuccino N (2005) Herbivory, time since introduction and the invasiveness of exotic plants. J Ecol 93(2):315–321
Carvalheiro LG, Buckley YM, Memmott J (2010) Diet breadth influences how the impact of invasive plants is propagated through food webs. Ecology 91(4):1063–1074
Cattin MF, Blandenier G, Banasek-Richter C, Bersier LF (2003) The impact of mowing as a management strategy for wet meadows on spider (Araneae) communities. Biol Conserv 113:179–188
Coffelt MA, Schultz PB (1990) Development of an aesthetic injury level to decrease pesticide use against orange striped oakworm in an urban pest management project. J Econ Entomol 83:2044–2049
Colley MR, Luna JM (2000) Relative attractiveness of potential beneficial insectary plants to aphidophagous hoverflies. Environ Entomol 29(5):1054–1059
Cornelius ML, Dieckhoff C, Hoelmer KA, Olsen RT, Weber DC, Herlihy MV, Talamas EJ, Vinyard BT, Greenstone MH (2016) Biological control of sentinel egg masses of the exotic invasive stink bug Halyomorpha halys in mid-atlantic USA ornamental landscapes. Biol Control 103:11–20
Dale AG, Frank SD (2018) Urban plants and climate drive unique arthropod interactions with unpredictable consequences. Curr Opin Insect Sci 29:27–33
Dawson W, Burslem DFRP, Hulme PE (2009) Herbiovry is related to taxonomic isolation, but not to invasiveness of tropical alien plants. Divers Distrib 15:141–147
Dinno A (2017) dunn.test: Dunn's Test of Multiple Comparisons Using Rank Sums. R package version 1.3.5. https://CRAN.R-project.org/package=dunn.test
Ehrlich PR, Raven PH (1964) Butterflies and plants: a study in coevolution. Evolution 19:586–608
Faeth SH, Bang C, Saari S (2011) Urban biodiversity: Patterns and mechanisms. Ann N Y Acad Sci 1223(1):69–81
Faith DP, Minchin PR, Belbin L (1987) Compositional dissimilarity as a robust measure of ecological distance. Vegetatio 69:57–68
Fiedler AK, Landis DA (2007) Attractiveness of Michigan native plants to arthropod natural enemies and herbivores. Environ Entomol 36(4):751–765
Finke DL, Denno RF (2002) Intraguild predation diminished in complex-structured vegetation: Implications for prey suppression. Ecology 83(3):643–652
Forister ML, Wilson JS (2013) The population ecology of novel plant–herbivore interactions. Oikos 122(5):657–666
Frank SD (2014) Bad neighbors: Urban habitats increase cankerworm damage to non-host understory plants. Urban Ecosyst 17(4):1135–1145
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(6):1662–1672
Frank SD, Backe KM, McDaniel C, Green M, Widney S, Dunn RR (2018) Exotic urban trees conserve similar natural enemy communities to native congeners but have fewer pests. Peer J 7:e6531. https://doi.org/10.7717/peerj.6531
Gardiner MM, Landis DA, Gratton C, DiFonzo CD, O'Neal M, Chacon JM, Wayo MT, Schmidt NP, Mueller EE, Heimpei GE (2009) Landscape diversity enhances biological control on an Introduced crop pest in the north-central USA. Ecol Appl 19(1):143–154
Gardiner M, Prajzner S, Burkman C, Albro S, Grewal P (2014) Vacant land conversion to community gardens: Influences on generalist arthropod predators and biocontrol services in urban greenspaces. Urban Ecosyst 17(1):101–122
Greenstone MH, Cornelius ML, Olsen RT, Payton ME (2017) Test of a natural enemy hypothesis on plant provenance: Spider abundance in native and exotic ornamental landscapes. J Entomol Sci 52(4):340–351
Gunnarsson B (2008) Bird predation on spiders: Ecological mechanisms and evolutionary consequences. J Arachnol 35:509–529
Heleno RH, Ceia RS, Ramos JA, Memmott J (2009) Effects of alien plants on insect abundance and biomass: a food-web approach. Conserv Biol 23(2):410–419
Herms DA (2002) Strategies for deployment of insect resistant ornamental plants. In: Wagners MR, Clancy KM, Lieutier F, Pain TD (eds) Mechanisms and deployment of resistance in trees to insects. Kluwer Academic Publishers, New York, pp 217–237
Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17(4):164–170
Kozlov MV, Zverev V, Zvereva EL (2014) Confirmation bias leads to overestimation of losses of woody plant foliage to insect herbivores in tropical regions. PeerJ 2:e709
Landis DA, Wratten SD, Gurr GM (2000) Habitat management to conserve natural enemies of arthropod pests in agriculture. Annu Rev Entomol 45(1):175–201
Langellotto GA, Denno RF (2004) Responses of invertebrate natural enemies to complex structured habitats: a meta-analytical synthesis. Oecologia 139(1):1–10
Larew HG, Knodel-Montz J, Poe SL (1984) Leaf miner damage. Greenhouse Manag 3:53–55
Lee JC, Heimpel GE (2005) Impact of flowering buckwheat on Lepidopteran cabbage pests and their parasitoids at two spatial scales. Biol Control 34:290–301
Lefcheck JS (2015) piecewiseSEM: Piecewise structural equation modeling in R for ecology, evolution, and systematics. Methods Ecol Evol 7(5):573–579
Letourneau DK, Armbrecht I, Rivera BS, Lerma JM, Carmona EJ, Daza MC, Escobar S, Galindo V, Gutierrez C, Lopez SD, Majia JL et al (2011) Does plant diversity benefit agroecosystems? A synthetic review. Ecol App 21(1):9–21
Lieurance D, Cipollini D (2013) Exotic lonicera species both escape and resist specialist and generalist herbivores in the introduced range in north america. Biol Invasions 15(8):1713–1724
Macel M, de Vos RCH, Jansen JJ, van der Putten WH, Dam NM (2014) Novel chemistry of invasive plants: exotic species have more unique metabolomic profiles than native congeners. Ecol Evol 4:2777–2786
Malumbres-Olarte J, Vink CJ, Ross JG, Cruickshank RH, Paterson AM (2013) The role of habitat complexity on spider communities in native alpine grasslands of New Zealand. Insect Conserv Divers 6:124–134
Matter SF, Brzyski JR, Harrison CJ, Hyams S, Loo C, Loomis J, Lubbers HR, Seastrum L, Stamper TI, Stein AM, Stokes R, Wilkerson BS (2012) Invading from the garden? A comparison of leaf herbivory for exotic and native plants in natural and ornamental settings. Insect Sci 19(6):677–682
McKinney M (2008) Effects of urbanization on species richness: a review of plants and animals. Urban Ecosyst 11(2):161–176
Minchin PR (1987) An evaluation of the relative robustness of techniques for ecological ordination. Vegetatio 69:89–107
Moreira X, Abdala-Roberts L, Teran JCB, Covel F, Mata R, Francisco M et al (2019) Impacts of urbanization on insect herbivory and plant defences in oak trees. Oikos 128(1):113–123
Morris MG (2000) The effects of structure and its dynamics on the ecology and conservation of arthropods in British grasslands. Biol Conserv 95(2):129–142
Narango DL, Tallamy DW, Marra PP (2017) Native plants improve breeding and foraging habitat for an insectivorous bird. Biol Conserv 213:42–50
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(3):253–260
Nuessly GS, Sterling WL (1994) Mortality of Helicoverpa zea eggs in cotton as a function of Oviposition sites, predator species, and desiccation. Pop Ecol 23(5):1189–1202
Oksanen J, F. Guillaume Blanchet, Michael Friendly, Roeland Kindt, Pierre Legendre, Dan McGlinn, Peter R. Minchin, R. B. O'Hara, Gavin L. Simpson, Peter Solymos, M. Henry H. Stevens, Eduard Szoecs and Helene Wagner (2017) vegan: Community Ecology Package. R package version 2.4-5. https://CRAN.R-project.org/package=vegan
Owen J (1983) Effects of contrived plant diversity and permanent succession on insects in English suburban gardens. In: Frankie GW, Koehler CS (eds) Urban entomology: interdisciplinary perspectives. Praeger, New York, pp 395–422
Pearse IS, Hipp AL (2009) Phylogenetic and trait similarity to a native species predict herbivory on non-native oaks. PNAS 106(43):18097–18102
Pearse IS, Harris DJ, Karban R, Sih A (2013) Predicting novel herbivore–plant interactions. Oikos 122(11):1554–1564
Peralta G, Frost CM, Didham RK, Pauchard A (2018) Plant, herbivore and parasitoid community composition in native Nothofagaceae forests vs. exotic pine plantations. J Appl Ecol 55(3):1265–1275
Perre P, Loyola R, Lewinsohn T, Almeida-Neto M (2011) Insects on urban plants: contrasting the flower head feeding assemblages on native and exotic hosts. Urban Ecosyst 14(4):711–722
Pfanannenstiel RS, Yeargan KV (2002) Identification and diel activity patterns of predators attacking Helicoverpazea (Lepidoptera: Noctuidae) eggs in soybean and sweet corn. Environ Entomol 31(2):232–241
Pinheiro J, Bates D, DebRoy S, Sarkar D and R Core Team (2017) nlme: Linear and Nonlinear Mixed Effects Models_. R package version 3.1–131, https://CRAN.Rproject.org/package=nlme
Proches S, Wilson JRU, Richardson DM, Chown SL (2008) Herbivores, but not other insects, are scarce on alien plants. Austral Ecol 33(5):691–700
Pumarino L, Alomar O, Lungren JG (2012) Effects of floral and extrafloral resource diversity on fitness of an omnivorous bug Orius insidiosus. Entomol Exp Appl 145:181–190
R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/.
Raupp MJ, Davidson JA, Koehler CS, Sadof CS, Reichelderfer K (1988) Decision-making considerations for aesthetic damage caused by pests. Bull Entomol Soc Am 34:27–32
Raupp MJ, Koehler CS, Davidson JA (1992) Advances in implementing integrated pest management for woody landscape plants. Annu Rev Entomol 37:561–585
Raupp MJ, Shrewsbury PM, Herms DA (2010) Ecology of herbivorous arthropods in urban landscapes. Annu Rev Entomol 55(1):19–38
Raupp et al (2012) Raupp MJ, Shrewsbury PM, Herms DA (2012) Disasters by design: outbreaks along urban gradients. In: Barbosa P, Letourneau DK, Agrawal AA (eds) Insect outbreaks revisited, 1st edn. Blackwell Publishing, Hoboken, pp 314–333
Richard M, Tallamy DW, Mitchell AB (2018) Introduced plants reduce species interactions. Biol Invasions 21:983–992
Rogers H, Lambers JHR, Miller R, Tewksbury JJ (2012) ‘Natural experiment’ Demonstrates top-down control of spiders by birds on a landscape level. PLoS ONE 7(9):e43446
Root RB (1973) Organization of a plant-arthropod association in simple and diverse habitats: the fauna of collards (Brassica: Oleracea). Ecol Monogr 43(1):95–124
Rosenthal GA, Janzen DH (1979) Herbivores: their interaction with secondary plant metabolites. Academic Press, New York
Rusch A, Chaplin-Kramer R, Gardiner MM, Hawro V, Holland J, Landis D, Thies C, Tscharntke T, Weisser WW, Winquist C, Woltz M, Bommarco R (2016) Agricultural landscape simplification reduces natural pest control: a quantitative synthesis. Agric Ecosyst Environ 221:198–204
Schierenbeck KA, Mack RN, Sharitz RR (1994) Effects of herbivory on growth and biomass allocation in native and introduced species of "lonicera.". Ecology 75(6):1661
Schindelin J, Arganda-Carreras I, Frise E et al (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 9(7):676–682. https://doi.org/10.1038/nmeth.2019
Schmitz OJ (2003) Top predator control of plant biodiversity and productivity in old field ecosystems. Ecol Lett 6:156–163
Schmitz OJ (2007) Predator diversity and trophic interactions. Ecology 88:2415–2426
Southwood T, Wint G, Kennedy C, Greenwood SR (2005) The composition of the arthropod fauna of the canopies of some species of oak (quercus). Eur J Entomol 102(1):65–72
Tallamy DW (2004) Do alien plants reduce insect biomass? Conserv Biol 18(6):1689–1692
Tallamy DW, Shropshire KJ (2009) Ranking Lepidopteran use of native versus introduced plants. Conserv Biol 23(4):941–947
Tallamy DW, Ballard M, D'Amico V (2010) Can alien plants support generalist insect herbivores? Biol Invasions 12(7):2285–2292
Williams VJ, Sahli HF (2016) A comparison of herbivore damage on three invasive plants and their native congeners: implications for the enemy release hypothesis. Castanea 81(2):128–137
Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extension in ecology with R. Springer, New York
Zuur AF, Ieno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems. Methods Ecol Evol 1:3–14
Acknowledgements
We thank Matt Greenstone, Mary Cornelius, Dawn Gundersen-Rindal with USDA-ARS-BARC for sharing their plots with us at the U.S. Arboretum and providing helpful advice and thoughts along the way. We thank Tom Wentworth, George Hess, and Michael Reiskind, who provided helpful guidance on this journey. We also thank Elsa Youngsteadt, Emily Griffith, and Michael Just for statistical guidance and feedback. We thank Matt Bertone, who provided helpful identification advice, as well as Annemarie Nagle, Leo Kerner, Cat Crofton, Ian McAreavy, Danielle Schmidt, Nicole Bissonnette, Aimee Dalsimer, Janis Arrojado, Kelly Harris, Logan Tyson, Doua Jim Lor, Tommy Pleasant, Anna Holmquist and all of the dedicated lab members who helped collect and analyze data for this project. This project was supported, in part, 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 the Southeast Climate Adaptation Science Center graduate fellowship awarded to S.E.P. The North Carolina State University Department of Entomology also contributed support for this research, as well as the Office of Undergraduate Research at NC State University.
Author information
Authors and Affiliations
Contributions
SEP and SDF conceived of experimental design. SEP and LMK collected and analyzed the data. All authors contributed to drafts and gave approval for publication.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by David Hawksworth.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
This article belongs to the Topical Collection: Invasive species.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Parsons, S.E., Kerner, L.M. & Frank, S.D. Effects of native and exotic congeners on diversity of invertebrate natural enemies, available spider biomass, and pest control services in residential landscapes. Biodivers Conserv 29, 1241–1262 (2020). https://doi.org/10.1007/s10531-020-01932-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10531-020-01932-8