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Urban tree pests can support biological control services in landscape shrubs

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Abstract

Scale insects are common tree pests in urban ecosystems. Although severe scale infestations can worsen tree condition, trees can tolerate moderate scale densities. Scale insects are prey for many arthropod natural enemies that also feed on plant pests throughout urban landscapes. Because scale-infested trees support natural enemy communities, they may support biological control services on nearby plants and function analogously to banker plants in greenhouse production systems. In this study we tested if sentinel insect prey were more likely to be removed on shrubs below scale-infested trees compared to scale-uninfested trees. We conducted several biological control experiments from 2019 to 2021 using fruit flies, aphids, and caterpillars in potted and planted holly shrubs below scale-infested and scale-uninfested oak trees. We found that caterpillars in potted shrubs and fruit flies in planted landscape shrubs were more likely to be removed underneath scale-infested trees compared to scale-uninfested trees. Caterpillars were also more likely to be removed from landscape Ilex vomitoria shrubs compared to I. cornuta shrubs. In all other experiments we found no effect of scale infestation status or shrub species on prey removal. Our results suggest that scale-infested trees can support biological control services in shrubs below them but that this effect can vary depending on prey and shrub species. The natural enemy communities in urban trees and shrubs appear to be linked and tolerating tree pests can favor conservation biological control services in urban landscapes.

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Data availability

The data used in this manuscript, and the R-script used to analyze the data, are available from the Dryad data repository at the following link: https://doi.org/doi:10.5061/dryad.sbcc2frbm.

References

  • Alverson DR, Allen RK (1991) Life history of the crapemyrtle aphid. In: Proceedings of the SNA research conference, pp 164–167

  • Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48

    Article  Google Scholar 

  • Braman SK, Latimer JG, Oetting RD, McQueen RD, Eckberg TB, Prinster M (2000) Management strategy, shade, and landscape composition effects on urban landscape plant quality and arthropod abundance. J Econ Entomol 93:1464–1472

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Burghardt KT, Tallamy DW, Philips C, Shropshire KJ (2010) Non-native plants reduce abundance, richness, and host specialization in lepidopteran communities. Ecosphere 1:11

    Article  Google Scholar 

  • Camacho ER, Chong JH, Braman SK, Frank SD, Schultz PB (2017) Life history of Parthenolecanium spp. (Hemiptera: Coccidae) in urban landscapes of the southeastern United States. J Econ Entomol 110:1668–1675

    Article  PubMed  Google Scholar 

  • Camacho RC, Chong JH, Braman SK, Frank SD, Schultz PB (2018) Natural enemy communities and biological control of Parthenolecanium spp. (Hemiptera: Coccidae) in the southeastern United States. J Econ Entomol 111:1558–1568

    Article  Google Scholar 

  • Coffelt MA, Schultz PB (1990) Development of an aesthetic injury level to decrease pesticide use against orangestriped oakworm (Lepidoptera: Saturniidae) in an urban pest management project. J Econ Entomol 83:2044–2049

    Article  Google Scholar 

  • Dale AG, Frank SD (2014a) The effects of urban warming on herbivore abundance and street tree condition. PLoS ONE 9(7):e102996

    Article  PubMed  PubMed Central  Google Scholar 

  • Dale AG, Frank SD (2014b) Urban warming trumps natural enemy regulation of herbivorous pests. Ecol Appl 24:1596–1607

    Article  PubMed  Google Scholar 

  • Dale AG, Youngsteadt E, Frank SD (2016) Forecasting the effects of heat and pests on urban trees: impervious surface thresholds and the “pace-to-plant” technique. Arboric Urban for 42:181–191

    Google Scholar 

  • Dale AG, Perry RL, Cope GC, Benda N (2020) Floral abundance and richness drive beneficial arthropod conservation and biological control on golf courses. Urban Ecosyst 23:55–66

    Article  Google Scholar 

  • Didham RK (1993) The influence of honeydew on arthropods associated with beech trees in New Zealand. N Z Nat Sci 20:47–53

    Google Scholar 

  • Egerer MH, Arel C, Otoshi MD, Quistberg RD, Bichier P, Philpott SM (2017) Urban arthropods respond variably to changes in landscape context and spatial scale. J Urban Ecol 3:jux001

    Article  Google Scholar 

  • Ewers R (2002) The influence of honeydew on arthropod community composition in a New Zealand beech forest. N Z J Ecol 26:23–29

    Google Scholar 

  • Finke DL, Denno RF (2006) Spatial refuge from intraguild predation: implications for prey suppression and trophic cascades. Oecologia 149:265–275

    Article  PubMed  Google Scholar 

  • Frank SD (2010) Biological control of arthropod pests using banker plant systems: past progress and future directions. Biol Control 52:8–16

    Article  Google Scholar 

  • Frank SD, Shrewsbury PM (2004) Consumption of black cutworms, Agrotis ipsilon (Lepidoptera: Noctuidae), and alternative prey by common golf course predators. Environ Entomol 33:1681–1688

    Article  Google Scholar 

  • Frank SD, Shrewsbury PM (2009) 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

    Article  Google Scholar 

  • Frank SD, Wratten SD, Sandhu HS, Shrewsbury PM (2007) Video analysis to determine how habitat strata affects predator diversity and predation of Epiphyas postvittana (Lepidoptera: Tortricidae) in a vineyard. Biol Control 41:230–236

    Article  Google Scholar 

  • Frank SD, Klingeman WE, White SA, Fulcher A (2013) Biology, injury, and management of maple tree pests in nurseries and urban landscapes. J Integr Pest Manag 4:1–14

    Article  Google Scholar 

  • Frank SD, Backe KM, McDaniel C, Green M, Widney S, Dunn RR (2019) Exotic urban trees conserve similar natural enemy communities to native congeners but have fewer pests. PeerJ 7:e6531

    Article  PubMed  PubMed Central  Google Scholar 

  • García LF, Velasco A, Colmenárez YC, Pétillon J, Cantor F (2022) Intra- and inter-specific effects in prey size capture by wolf spiders (Araneae: Lycosidae) against the fall armyworm Spodoptera frugiperda under laboratory conditions. Biocontrol Sci Technol 32:1132–1138

    Article  Google Scholar 

  • Guillebeau LP, All JN (1990) Big-eyed bugs (Hemiptera: Lygaeidae) and the striped lynx spider (Araneae: Oxyopidae): intra- and interspecific interference on predation of first instar corn earworm (Lepidoptera: Noctuidae). J Entomol Sci 25:30–33

    Google Scholar 

  • Gurr GM, Wratten SD, Landis DA, You M (2017) Habitat management to suppress pest populations: progress and prospects. Annu Rev Entomol 62:91–109

    Article  CAS  PubMed  Google Scholar 

  • Hanks LM, Denno RF (1993) Natural enemies and plant water relations influence the distribution of an armored scale insect. Ecology 74:1081–1091

    Article  Google Scholar 

  • Heng-moss T, Baxendale F, Riordan T (1998) Beneficial arthropods associated with Buffalograss. J Econ Entomol 91:1167–1172

    Article  Google Scholar 

  • Hermes DA, Akers RC, Nielsen DG (1984) The ornamental landscape as an ecosystem: implications for pest management. J Arboric 10:303–307

    Google Scholar 

  • Hodges GS, Braman SK (2004) Seasonal occurrence, phenological indicators and mortality factors affecting five scale insect species (Hemiptera: Diaspididae, Coccidae) in the urban landscape setting. J Entomol Sci 39:611–622

    Google Scholar 

  • Huang N, Enkegaard A, Osborne LS, Ramakers PMJ, Messelink GJ, Pijnakker J, Murphy G (2011) The banker plant method in biological control. CRC Crit Rev Plant Sci 30:259–278

    Article  Google Scholar 

  • Isenhour DJ, Wiseman BR, Layton RC (1989) Enhanced predation by Orius insidiosus (Hemiptera: Anthocoridae) on larvae of Heliothis zea and Spodoptera frugiperda (Lepidoptera: Noctuidae) caused by prey feeding on resistant corn genotypes. Environ Entomol 18:418–422

  • Jemal A, Hugh-Jones M (1993) A review of the red imported fire ant (Solenopsis invicta Buren) and its impacts on plant, animal, and human health. Prev Vet Med 17:19–32

    Article  Google Scholar 

  • Joseph SV, Braman SK (2009) Predatory potential of Geocoris spp. and Orius insidiosus on fall armyworm in resistant and susceptible turf. J Econ Entomol 102:1151–1156

    Article  CAS  PubMed  Google Scholar 

  • Just MG, Frank SD, Dale AG (2018) Impervious surface thresholds for urban tree site selection. Urban for Urban Green 34:141–146

    Article  Google Scholar 

  • Just MG, Dale AG, Long LC, Frank SD (2019) Urbanization drives unique latitudinal patterns of insect herbivory and tree condition. Oikos 128:984–993

    Article  Google Scholar 

  • Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170

    Article  Google Scholar 

  • Konrad R, Wäckers FL, Romeis J, Babendreier D (2009) Honeydew feeding in the solitary bee Osmia bicornis as affected by aphid species and nectar availability. J Insect Physiol 55:1158–1166

    Article  CAS  PubMed  Google Scholar 

  • Krimmel BA, Pearse IS (2013) Sticky plant traps insects to enhance indirect defence. Ecol Lett 16:219–224

    Article  CAS  PubMed  Google Scholar 

  • Langellotto GA, Denno RF (2004) Responses of invertebrate natural enemies to complex-structured habitats: a meta-analytical synthesis. Oecologia 139:1–10

    Article  PubMed  Google Scholar 

  • Long LC, D’Amico V, Frank SD (2019) Urban forest fragments buffer trees from warming and pests. Sci Total Environ 658:1523–1530

    Article  CAS  PubMed  Google Scholar 

  • Meineke EK, Frank SD (2018) Water availability drives urban tree growth responses to herbivory and warming. J Appl Ecol 55:1701–1713

    Article  Google Scholar 

  • Meineke EK, Dunn RR, Sexton JO, Frank SD (2013) Urban warming drives insect pest abundance on street trees. PLoS ONE 8(3):e59687

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meineke EK, Dunn RR, Frank SD (2014) Early pest development and loss of biological control are associated with urban warming. Biol Lett 10:20140586

    Article  PubMed  PubMed Central  Google Scholar 

  • Mizell RF, Schiffhauer DE (1987) Seasonal abundance of the crapemyrtle aphid Sarucallis kahawaloukalani in relation to the pecan aphids Monellia caryella and Monelliopsis pecanis and their common predators. Entomophaga 32:511–520

    Article  Google Scholar 

  • Nelson PN, Burrack HJ, Sorenson CE (2020) Arthropod carrion influences plant choice, oviposition, and cannibalism by a specialist predator on a sticky plant. Ecol Entomol 45:182–189

    Article  Google Scholar 

  • Nighswander GP, Sinclair JS, Dale AG, Qiu J, Iannone BV III (2021) Importance of plant diversity and structure for urban garden pest resistance. Landsc Urban Plan 215:104211

    Article  Google Scholar 

  • Norton BA, Thomson LJ, Williams NSG, McDonnell MJ (2014) The effect of urban ground covers on arthropods: an experiment. Urban Ecosyst 17:77–99

    Article  Google Scholar 

  • Parsons SE, Frank SD (2019) Urban tree pests and natural enemies respond to habitat at different spatial scales. J Urban Ecol 5:1–15

    Article  Google Scholar 

  • Parsons SE, Kerner LM, Frank SD (2020a) 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

    Article  Google Scholar 

  • Parsons SE, Sozanski KS, Wilson AA, Frank SD (2020b) Effects of temperature and habitat complexity on an urban tree pest (Tinocallis kahawaluokalani), natural enemies, and predation services in the city. Urban Ecosyst 23:13–26

    Article  Google Scholar 

  • Pfannenstiel RS (2015) Extended survival of spiders (Aranaeae) feeding on whitefly (Homoptera: Aleyrodidae) honeydew. J Entomol Sci 50:110–118

    Google Scholar 

  • Prado SG, Frank S (2014) Optimal foraging by an aphid parasitoid affects the outcome of apparent competition. Ecol Entomol 39:236–244

    Article  Google Scholar 

  • R Core Team (2022) R: a language and environment for statistical computing. R foundation for statistical computing, Vienna. https://www.r-project.org/

  • Raupp M, Davidson J, Homes J, Hellman J (1985) The concept of key plants in integrated pest management for landscapes. J Arboric 11:317–322

    Google Scholar 

  • 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

    Google Scholar 

  • Raupp MJ, Davidson JA, Koehler CS, Sadof CS, Reichelderfer K (1989) Economic and aesthetic injury levels and thresholds for insect pests of ornamental plants. Florida Entomol 72:403–407

    Article  Google Scholar 

  • Raupp MJ, Holmes JJ, Sadof C, Shrewsbury P, Davidson JA (2001) Effects of cover sprays and residual pesticides on scale insects and natural enemies in urban forests. J Arboric 27:203–214

    Google Scholar 

  • Raupp MJ, Shrewsbury PM, Herms DA (2010) Ecology of herbivorous arthropods in urban landscapes. Annu Rev Entomol 55:19–38

    Article  CAS  PubMed  Google Scholar 

  • Rochefort S, Shetlar DJ, Brodeur J (2006) Ground beetle assemblages (Coleoptera: Carabidae) and their seasonal abundance in cool season turfgrass lawns of Quebec. Environ Entomol 35:1508–1514

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Schultz PB (1984) Natural enemies of oak lecanium (Homoptera: Coccidae) in eastern virginia. Environ Entomol 13:1515–1518

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Shrewsbury PM, Raupp MJ (2006) Do top-down or bottom-up forces determine Stephanitis pyrioides abundance in urban landscapes? Ecol Appl 16:262–272

    Article  PubMed  Google Scholar 

  • Silverman J, Brightwell RJ (2008) The argentine ant: challenges in managing an invasive unicolonial pest. Annu Rev Entomol 53:231–252

    Article  CAS  PubMed  Google Scholar 

  • Speight MR, Hails RS, Gllbkrt M, Foggo A (1998) Horse chestnut scale (Pulvinaria regalis) (Homoptera: Coccidae) and urban host tree environment. Ecology 79:1503–1513

    Article  Google Scholar 

  • Stern VM, Smith RF, Van den Bosch R, Hagen KS (1959) The integrated control concept. Hilgardia 29:81–101

    Article  CAS  Google Scholar 

  • 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(5):e20018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tena A, Wäckers FL, Heimpel GE, Urbaneja A, Pekas A (2016) Parasitoid nutritional ecology in a community context: The importance of honeydew and implications for biological control. Curr Opin Insect Sci 14:100–104

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Vanek SJ, Potter DA (2010) Ant-exclusion to promote biological control of soft scales (Hemiptera: Coccidae) on woody landscape plants. Environ Entomol 39:1829–1837

    Article  PubMed  Google Scholar 

  • Wilson CJ, Frank SD (2022) Scale insects support natural enemies in both landscape trees and shrubs below them. Environ Entomol 51:1094–1105

    Article  PubMed  Google Scholar 

  • Wimp GM, Whitham TG (2001) Biodiversity consequences of predation and host plant hybridization on an aphid-ant mutualism. Ecology 82:440–452

    Google Scholar 

  • Wong SK, Frank SD (2013) Pollen increases fitness and abundance of Orius insidiosus Say (Heteroptera: Anthocoridae) on banker plants. Biol Control 64:45–50

    Article  Google Scholar 

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Acknowledgements

We would like to thank Jasmine Travieso, Molly Carlson, Chandler Purser, Sophia Copeman and Jane Petzoldt for assisting with field work. We would also like to thank Christina Mitchell, Rebecca Irwin, Anders Huseth, Clyde Sorenson, the handling editor, the editor in chief of the journal BioControl, and anonymous reviewers for feedback on earlier drafts of this manuscript.

Funding

This research was funded by the United States Department of Agriculture, National Institute of Food and Agriculture (Award Numbers: 2021-70006-35670, 2018-70006-28914, 2016-70006-25827) and by the Southern IPM Center (Project S21-008) as part of USDA NIFA CPPM RCP (Agreement No. 2018-70006-28884).

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CJW and SDF designed all experiments. SDF acquired funding. CJW conducted field experiments, statistical analyses, and wrote the first draft of the manuscript. All authors edited the manuscript.

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Correspondence to Caleb J. Wilson.

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Handling Editor: Josep Anton Jaques Miret.

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Wilson, C.J., Frank, S.D. Urban tree pests can support biological control services in landscape shrubs. BioControl 68, 375–386 (2023). https://doi.org/10.1007/s10526-023-10192-8

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