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Cityscape quality and resource manipulation affect natural enemy biodiversity in and fidelity to urban agroecosystems

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Abstract

Context

Complex landscapes with high resource availability can support more diverse natural enemy communities and better natural pest control by providing resources and facilitating organism dispersal. Moreover, in agricultural landscapes, local agroecosystem management can support biodiversity maintenance and pest control by adding resources in less complex landscapes with fewer resources. However, we lack an understanding of how local and landscape factors interact to affect natural enemy communities and their site fidelity to agroecosystems in urban landscapes (i.e., cityscapes).

Objective

To better understand how local and landscape factors influence natural enemies in urban agroecosystems, we used urban community gardens as a model system to test if and how local resource manipulation and differences in cityscape quality affect natural enemy (ladybird beetles, parasitoid wasps) communities and their fidelity to urban habitats.

Methods

We performed two manipulations. First, we added local floral resources in 6 of 12 gardens situated in different cityscapes to measure differences in natural enemy biodiversity. Second, in those 12 gardens, with and without resource additions, we manipulated populations of a common natural enemy, Hippodamia convergens, to assess fidelity to the gardens.

Results

Floral resource additions increased parasitoid abundance and changed community composition, but had little effect on ladybeetle abundance, richness or site fidelity. Rather, ladybeetle fidelity to gardens was lower in gardens in low quality cityscapes with high impervious cover.

Conclusions

Cityscape quality influences natural enemies in and fidelity to gardens. Landscape-moderated biodiversity patterns observed in rural landscapes likely differ from urban contexts with implications for pest control.

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References

  • Angold PG, Sadler JP, Hill MO, Pullin A, Rushton S, Austin K, Small E, Wood B, Wadsworth R, Sanderson R, Thompson K (2006) Biodiversity in urban habitat patches. Sci Total Environ 360:196–204

    Article  PubMed  CAS  Google Scholar 

  • Baker SC, Elek JA, Bashford R, Paterson SC, Madden J, Battaglia M (2003) Inundative release of coccinellid beetles into eucalypt plantations for biological control of chrysomelid leaf beetles. Agric For Entomol 5:97–106

    Article  Google Scholar 

  • Balzan MV, Wäckers FL (2013) Flowers to selectively enhance the fitness of a host-feeding parasitoid: adult feeding by Tuta absoluta and its parasitoid Necremnus artynes. Biol Control 67:21–31

    Article  Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S, Christensen RHB, Singmann H (2015) lme4: Linear mixed-effects models using Eigen and S4. R Package 1

  • Bennett AB, Gratton C (2012) Local and landscape scale variables impact parasitoid assemblages across an urbanization gradient. Landsc Urban Plan 104:26–33

    Article  Google Scholar 

  • Brown LM, Fuda RK, Schtickzelle N, Coffman H, Jost A, Kazberouk A, Kemper E, Sass E, Crone EE (2017) Using animal movement behavior to categorize land cover and predict consequences for connectivity and patch residence times. Landsc Ecol 32:1657–1670

    Article  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information—theoretic approach. Springer, New York

    Google Scholar 

  • Cadenasso ML, Pickett STA, Schwarz K (2007) Spatial heterogeneity in urban ecosystems: reconceptualizing land cover and a framework for classification. Front Ecol Environ 5:80–88

    Article  Google Scholar 

  • Calcagno V, De Mazancourt C (2010) glmulti: an R Package for easy automated model selection with (generalized) linear models. J Stat Softw 34:1–29

    Article  Google Scholar 

  • Chaplin-Kramer R, O’Rourke ME, Blitzer EJ, Kremen C (2011) A meta-analysis of crop pest and natural enemy response to landscape complexity. Ecol Lett 14:922–932

    Article  PubMed  Google Scholar 

  • Corbett A, Rosenheim JA (1996) Quantifying movement of a minute parasitoid, Anagrus epos (Hymenoptera: Mymaridae), using fluorescent dust marking and recapture. Biol Control 6:35–44

    Article  Google Scholar 

  • Denys C, Tscharntke T (2002) Plant-insect communities and predator-prey ratios in field margin strips, adjacent crop fields, and fallows. Oecologia 130:315–324

    Article  PubMed  Google Scholar 

  • Egerer MH, Bichier P, Philpott SM (2016) Landscape and local habitat correlates of lady beetle abundance and species richness in urban agriculture. Ann Entomol Soc Am. https://doi.org/10.1093/aesa/saw063

    Article  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 3:1–10

    Article  Google Scholar 

  • Ellis JA, Walter AD, Tooker JF, Ginzel MD, Reagel PF, Lacey ES, Bennett AB, Grossman EM, Hanks LM (2005) Conservation biological control in urban landscapes: manipulating parasitoids of bagworm (Lepidoptera: Psychidae) with flowering forbs. Biol Control 34:99–107

    Article  Google Scholar 

  • ESRI (2011) ArcGIS desktop: release 10. Environmental Systems Research Institute, Redlands

    Google Scholar 

  • Fahrig L (2001) How much habitat is enough? Biol Conserv 100:65–74

    Article  Google Scholar 

  • Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Syst 34:487–515

    Article  Google Scholar 

  • Flint M (2013) Integrated pest management for home gardeners and landscape integrated landscape professionals. University of California Pest Notes Publication, Davis

    Google Scholar 

  • Gámez-Virués S, Perović DJ, Gossner MM, Börschig C, Blüthgen N, de Jong H, Simons NK, Klein A-M, Krauss J, Maier G, Scherber C, Steckel J, Rothenwöhrer C, Steffan-Dewenter I, Weiner CN, Weisser W, Werner M, Tscharntke T, Westphal C (2015) Landscape simplification filters species traits and drives biotic homogenization. Nat Commun 6:8568

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gardiner MM, Landis DA, Gratton C, Schmidt N, O’Neal M, Mueller E, Chacon J, Heimpel GE, Difonzo CD (2009) Landscape composition influences patterns of native and exotic lady beetle abundance. Divers Distrib 15:554–564

    Article  Google Scholar 

  • Jin S, Yang L, Danielson P, Homer C, Fry J, Xian G (2013) A comprehensive change detection method for updating the National Land Cover Database to circa 2011. Remote Sens Environ 132:159–175

    Article  Google Scholar 

  • Kareiva P (1985) Finding and losing host plants by Phyllotreta: patch size and surrounding habitat. Ecology 66:1809–1816

    Article  Google Scholar 

  • Kareiva P, Odell G (1987) Swarms of predators exhibit “preytaxis” if individual predators use area-restricted search. Am Nat 130:233–270

    Article  Google Scholar 

  • Kowarik I (2011) Novel urban ecosystems, biodiversity, and conservation. Environ Pollut 159:1974–1983

    Article  PubMed  CAS  Google Scholar 

  • Kremen C (2005) Managing ecosystem services: what do we need to know about their ecology? Ecol Lett 8:468–479

    Article  PubMed  Google Scholar 

  • Kremen C, Williams NM, Aizen MA, Gemmill-Herren B, LeBuhn G, Minckley R, Packer L, Potts SG, Roulston T, Steffan-Dewenter I, Vázquez DP, Winfree R, Adams L, Crone EE, Greenleaf SS, Keitt TH, Klein AM, Regetz J, Ricketts TH (2007) Pollination and other ecosystem services produced by mobile organisms: a conceptual framework for the effects of land-use change. Ecol Lett 10:299–314

    Article  PubMed  Google Scholar 

  • Lin BB, Egerer MH, Liere H, Jha S, Bichier P, Philpott SM (2018) Local- and landscape-scale land cover affects microclimate and water use in urban gardens. Sci Total Environ 610–611:570–575

    Article  PubMed  CAS  Google Scholar 

  • Longcore T, Rich C (2004) Ecological light pollution. Front Ecol Environ 2:191–198

    Article  Google Scholar 

  • Loreau M, Mouquet N, Gonzalez A (2003) Biodiversity as spatial insurance in heterogeneous landscapes. Proc Natl Acad Sci U S A 100:12765–12770

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lutscher F, Musgrave JA (2017) Behavioral responses to resource heterogeneity can accelerate biological invasions. Ecology 98:1229–1238

    Article  PubMed  Google Scholar 

  • MacArthur RH, Wilson EO (1976) The theory of island biogeography. Princeton University Press, Princeton

    Google Scholar 

  • Martin EA, Seo B, Park CR, Reineking B, Steffan-Dewenter I (2016) Scale-dependent effects of landscape composition and configuration on natural enemy diversity, crop herbivory, and yields. Ecol Appl 26:448–462

    Article  PubMed  Google Scholar 

  • Matteson KC, Langellotto GA (2009) Bumble bee abundance in New York City community gardens: implications for urban agriculture. Cities Environ 2:1–12

    Article  Google Scholar 

  • McIntyre NE (2000) Ecology of urban arthropods: a review and a call to action. Ann Entomol Soc Am 93:825–835

    Article  Google Scholar 

  • Naranjo S (1990) Influence of two mass-marking techniques on survival and flight behavior of Diabrotica virgifera virgifera (Coleoptera: Chrysomelidae). J Econ Entomol 83:1360–1364

    Article  Google Scholar 

  • Oberholtzer L, Dimitri C, Pressman A (2014) Organic agriculture in U.S. urban areas: building bridges between organic farms and education. In: IFOAM organic world congress 2014, ‘Building Organic Bridges’, 13–15 October 2014, Istanbul, Turkey

  • Oksanen J (2015) Multivariate analysis of ecological communities in R. https://doi.org/10.1016/0169-5347(88)90124-3

  • Otoshi MD, Bichier P, Philpott SM (2015) Local and landscape correlates of spider activity density and species richness in urban gardens. Environ Entomol. https://doi.org/10.1093/ee/nvv098

    Article  PubMed  Google Scholar 

  • Pawelek J, Frankie GW, Thorp RW, Przybylski M (2009) Modification of a community garden to attract native bee pollinators in urban San Luis Obispo, California. Cities Environ 2:1–21

    Article  Google Scholar 

  • Perfecto I, Vandermeer J (2002) Quality of agroecological matrix in a tropical montane landscape: ants in coffee plantations in Southern Mexico. Conserv Biol 16:174–182

    Article  Google Scholar 

  • R Development Core Team (2013) R: a language and environment for statistical computing, vol 55. R Foundation for Statistical Computing, Vienna, pp 275–286

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

    Article  PubMed  CAS  Google Scholar 

  • Ricketts TH (2001) The matrix matters: effective isolation in fragmented landscapes. Am Nat 158:87–99

    Article  PubMed  CAS  Google Scholar 

  • Rourke MEO, Rienzo-stack K, Power AG, El H, Rourke EO (2011) A multi-scale, landscape approach to predicting insect populations in agroecosystems. Ecol Appl 21:1782–1791

    Article  Google Scholar 

  • Schellhorn NA, Gagic V, Bommarco R (2015a) Time will tell: resource continuity bolsters ecosystem services. Trends Ecol Evol 30:524–530

    Article  PubMed  Google Scholar 

  • Schellhorn NA, Parry HR, Macfadyen S, Wang Y, Zalucki MP (2015b) Connecting scales: achieving in-field pest control from areawide and landscape ecology studies. Insect Sci 22:35–51

    Article  PubMed  Google Scholar 

  • Schultz CB (1998) Dispersal behavior and its implications for reserve design in a rare Oregon butterfly. Conserv Biol 12:284–292

    Article  Google Scholar 

  • Schultz CB, Pe’er BG, Damiani C, Brown L, Crone EE (2017) Does movement behaviour predict population densities? A test with 25 butterfly species. J Anim Ecol 86:384–393

    Article  PubMed  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 

  • Tscharntke T, Brandl R (2004) Plant-insect interactions in fragmented landscapes. Annu Rev Entomol 49:405–430

    Article  PubMed  CAS  Google Scholar 

  • Tscharntke T, Tylianakis JM, Rand TA, Didham RK, Fahrig L, Batary P, Bengtsson J, Cloug, Y, Crist TO, Dormann CF, Ewers RM, Frund 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

    Article  PubMed  Google Scholar 

  • Vandermeer J, Carvajal R (2001) Metapopulation dynamics and the quality of the matrix. Am Nat 158:211–220

    Article  PubMed  CAS  Google Scholar 

  • Weber DC, Lundgren JG (2009) Assessing the trophic ecology of the Coccinellidae: their roles as predators and as prey. Biol Control 51:199–214

    Article  Google Scholar 

  • With KA, Pavuk DM, Worchuck JL, Oates RK, Fisher JL (2002) Threshold effects of landscape structure on biological control in agroecosystems. Ecol Appl 12:52–65

    Article  Google Scholar 

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Acknowledgments

We thank C. Adams, Y. Byun, M. Cely-Santos, H. Cohen, E. Connor, D. Hafalia-Yackel, E. Jiménez-Soto, C. Sanchez, and J. Shaw for field and lab assistance. We thank the UCSC Greenhouse Staff J. Velzy and M. Dillingham for growing the experimental plants. We thank C. Anton, T. Ong, J. Suraci, and the Philpott lab group for helpful discussion and feedback on the manuscript. We thank the following gardens and organizations for supporting and providing access for our research: Aptos Community Garden, Beach Flats Community Garden, Live Oak Green Grange Community Garden, MEarth, Mesa Verde Gardens, Middlebury Institute of International Studies, Obama Way Community Garden, Pacific Grove Community Garden, Salinas Chinatown Community Garden and Community Garden of Salinas. This work was supported by a National Science Foundation Graduate Research Fellowship #2016174835 (to M.H.E), a Heller Graduate Research Grant from UC Santa Cruz (to M.H.E), and a United States Department of Agriculture National Institute of Food and Agriculture Award #2016-67019-25185 (to S.M.P. and H.L.). We thank the reviewers for their constructive comments that significantly improved the manuscript.

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Author contributions

MHE, SMP and HL conceived of the study and designed the field experiments. MHE, SMP, HL, and PB carried out the field experiments. MHE conducted statistical analyses and wrote the first draft of the manuscript. All authors improved the manuscript.

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Correspondence to Monika H. Egerer.

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Egerer, M.H., Liere, H., Bichier, P. et al. Cityscape quality and resource manipulation affect natural enemy biodiversity in and fidelity to urban agroecosystems. Landscape Ecol 33, 985–998 (2018). https://doi.org/10.1007/s10980-018-0645-9

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