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
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
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
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
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
Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information—theoretic approach. Springer, New York
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
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
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
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
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
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
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
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
ESRI (2011) ArcGIS desktop: release 10. Environmental Systems Research Institute, Redlands
Fahrig L (2001) How much habitat is enough? Biol Conserv 100:65–74
Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Syst 34:487–515
Flint M (2013) Integrated pest management for home gardeners and landscape integrated landscape professionals. University of California Pest Notes Publication, Davis
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
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
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
Kareiva P (1985) Finding and losing host plants by Phyllotreta: patch size and surrounding habitat. Ecology 66:1809–1816
Kareiva P, Odell G (1987) Swarms of predators exhibit “preytaxis” if individual predators use area-restricted search. Am Nat 130:233–270
Kowarik I (2011) Novel urban ecosystems, biodiversity, and conservation. Environ Pollut 159:1974–1983
Kremen C (2005) Managing ecosystem services: what do we need to know about their ecology? Ecol Lett 8:468–479
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
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
Longcore T, Rich C (2004) Ecological light pollution. Front Ecol Environ 2:191–198
Loreau M, Mouquet N, Gonzalez A (2003) Biodiversity as spatial insurance in heterogeneous landscapes. Proc Natl Acad Sci U S A 100:12765–12770
Lutscher F, Musgrave JA (2017) Behavioral responses to resource heterogeneity can accelerate biological invasions. Ecology 98:1229–1238
MacArthur RH, Wilson EO (1976) The theory of island biogeography. Princeton University Press, Princeton
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
Matteson KC, Langellotto GA (2009) Bumble bee abundance in New York City community gardens: implications for urban agriculture. Cities Environ 2:1–12
McIntyre NE (2000) Ecology of urban arthropods: a review and a call to action. Ann Entomol Soc Am 93:825–835
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
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
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
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
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
Ricketts TH (2001) The matrix matters: effective isolation in fragmented landscapes. Am Nat 158:87–99
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
Schellhorn NA, Gagic V, Bommarco R (2015a) Time will tell: resource continuity bolsters ecosystem services. Trends Ecol Evol 30:524–530
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
Schultz CB (1998) Dispersal behavior and its implications for reserve design in a rare Oregon butterfly. Conserv Biol 12:284–292
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
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
Tscharntke T, Brandl R (2004) Plant-insect interactions in fragmented landscapes. Annu Rev Entomol 49:405–430
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
Vandermeer J, Carvajal R (2001) Metapopulation dynamics and the quality of the matrix. Am Nat 158:211–220
Weber DC, Lundgren JG (2009) Assessing the trophic ecology of the Coccinellidae: their roles as predators and as prey. Biol Control 51:199–214
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
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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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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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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DOI: https://doi.org/10.1007/s10980-018-0645-9