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Crop pests and predators exhibit inconsistent responses to surrounding landscape composition

Research output: Contribution to journalArticleResearchpeer review

Authors

  • Daniel S. Karp
  • Rebecca Chaplin-Kramer
  • Timothy D. Meehan
  • Emily A. Martin
  • Ricardo Perez-Alvarez

External Research Organisations

  • University of California at Davis
  • Stanford University
  • National Audubon Society
  • Julius Maximilian University of Würzburg
  • Alliance Bioversity International
  • Cornell University
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  • Brandenburg University of Technology
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  • Ethiopian Biodiversity Institute (EBI)
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  • Ben-Gurion University of the Negev
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  • Agricultural Research Organization of Israel
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  • UK Centre for Ecology & Hydrology
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  • Rochester Institute of Technology
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  • Jiangxi Agricultural University
  • National Agricultural Research Centers Japan
  • National Institute for Environmental Studies of Japan
  • Xi'an Jiaotong-Liverpool University
  • Institut national de la recherche agronomique (INRA)
  • Universite de Bordeaux
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Details

Original languageEnglish
Pages (from-to)E7863-E7870
JournalProceedings of the National Academy of Sciences of the United States of America
Volume115
Issue number33
Early online date2 Aug 2018
Publication statusPublished - 14 Aug 2018
Externally publishedYes

Abstract

The idea that noncrop habitat enhances pest control and represents a win–win opportunity to conserve biodiversity and bolster yields has emerged as an agroecological paradigm. However, while noncrop habitat in landscapes surrounding farms sometimes benefits pest predators, natural enemy responses remain heterogeneous across studies and effects on pests are inconclusive. The observed heterogeneity in species responses to noncrop habitat may be biological in origin or could result from variation in how habitat and biocontrol are measured. Here, we use a pest-control database encompassing 132 studies and 6,759 sites worldwide to model natural enemy and pest abundances, predation rates, and crop damage as a function of landscape composition. Our results showed that although landscape composition explained significant variation within studies, pest and enemy abundances, predation rates, crop damage, and yields each exhibited different responses across studies, sometimes increasing and sometimes decreasing in landscapes with more noncrop habitat but overall showing no consistent trend. Thus, models that used landscape-composition variables to predict pest-control dynamics demonstrated little potential to explain variation across studies, though prediction did improve when comparing studies with similar crop and landscape features. Overall, our work shows that surrounding noncrop habitat does not consistently improve pest management, meaning habitat conservation may bolster production in some systems and depress yields in others. Future efforts to develop tools that inform farmers when habitat conservation truly represents a win–win would benefit from increased understanding of how landscape effects are modulated by local farm management and the biology of pests and their enemies.

Keywords

    Agroecology, Biodiversity, Biological control, Ecosystem services, Natural enemies, Pest Control, Biological, Animals, Crops, Agricultural/growth & development, Models, Biological, Ecosystem

ASJC Scopus subject areas

Cite this

Crop pests and predators exhibit inconsistent responses to surrounding landscape composition. / Karp, Daniel S.; Chaplin-Kramer, Rebecca; Meehan, Timothy D. et al.
In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 115, No. 33, 14.08.2018, p. E7863-E7870.

Research output: Contribution to journalArticleResearchpeer review

Karp, DS, Chaplin-Kramer, R, Meehan, TD, Martin, EA, DeClerck, F, Grab, H, Gratton, C, Hunt, L, Larsen, AE, Martínez-Salinas, A, O’Rourke, ME, Rusch, A, Poveda, K, Jonsson, M, Rosenheim, JA, Schellhorn, NA, Tscharntke, T, Wratten, SD, Zhang, W, Iverson, AL, Adler, LS, Albrecht, M, Alignier, A, Angelella, GM, Anjum, MZ, Avelino, J, Batáry, P, Baveco, JM, Bianchi, FJJA, Birkhofer, K, Bohnenblust, EW, Bommarco, R, Brewer, MJ, Caballero-López, B, Carrière, Y, Carvalheiro, LG, Cayuela, L, Centrella, M, Ćetković, A, Henri, DC, Chabert, A, Costamagna, AC, De la Mora, A, de Kraker, J, Desneux, N, Diehl, E, Diekötter, T, Dormann, CF, Eckberg, JO, Entling, MH, Fiedler, D, Franck, P, van Veen, FJF, Frank, T, Gagic, V, Garratt, MPD, Getachew, A, Gonthier, DJ, Goodell, PB, Graziosi, I, Groves, RL, Gurr, GM, Hajian-Forooshani, Z, Heimpel, GE, Herrmann, JD, Huseth, AS, Inclán, DJ, Ingrao, AJ, Iv, P, Jacot, K, Johnson, GA, Jones, L, Kaiser, M, Kaser, JM, Keasar, T, Kim, TN, Kishinevsky, M, Landis, DA, Lavandero, B, Lavigne, C, Le Ralec, A, Lemessa, D, Letourneau, DK, Liere, H, Lu, Y, Lubin, Y, Luttermoser, T, Maas, B, Mace, K, Madeira, F, Mader, V, Cortesero, AM, Marini, L, Martinez, E, Martinson, HM, Menozzi, P, Mitchell, MGE, Miyashita, T, Molina, GAR, Molina-Montenegro, MA, O’Neal, ME, Opatovsky, I, Ortiz-Martinez, S, Nash, M, Östman, Ö, Ouin, A, Pak, D, Paredes, D, Parsa, S, Parry, H, Perez-Alvarez, R, Perović, DJ, Peterson, JA, Petit, S, Philpott, SM, Plantegenest, M, Plećas, M, Pluess, T, Pons, X, Potts, SG, Pywell, RF, Ragsdale, DW, Rand, TA, Raymond, L, Ricci, B, Sargent, C, Sarthou, JP, Saulais, J, Schäckermann, J, Schmidt, NP, Schneider, G, Schüepp, C, Sivakoff, FS, Smith, HG, Whitney, KS, Stutz, S, Szendrei, Z, Takada, MB, Taki, H, Tamburini, G, Thomson, LJ, Tricault, Y, Tsafack, N, Tschumi, M, Valantin-Morison, M, van Trinh, M, van der Werf, W, Vierling, KT, Werling, BP, Wickens, JB, Wickens, VJ, Woodcock, BA, Wyckhuys, K, Xiao, H, Yasuda, M, Yoshioka, A & Zou, Y 2018, 'Crop pests and predators exhibit inconsistent responses to surrounding landscape composition', Proceedings of the National Academy of Sciences of the United States of America, vol. 115, no. 33, pp. E7863-E7870. https://doi.org/10.1073/pnas.1800042115, https://doi.org/10.1073/pnas.1800042115
Karp, D. S., Chaplin-Kramer, R., Meehan, T. D., Martin, E. A., DeClerck, F., Grab, H., Gratton, C., Hunt, L., Larsen, A. E., Martínez-Salinas, A., O’Rourke, M. E., Rusch, A., Poveda, K., Jonsson, M., Rosenheim, J. A., Schellhorn, N. A., Tscharntke, T., Wratten, S. D., Zhang, W., ... Zou, Y. (2018). Crop pests and predators exhibit inconsistent responses to surrounding landscape composition. Proceedings of the National Academy of Sciences of the United States of America, 115(33), E7863-E7870. https://doi.org/10.1073/pnas.1800042115, https://doi.org/10.1073/pnas.1800042115
Karp DS, Chaplin-Kramer R, Meehan TD, Martin EA, DeClerck F, Grab H et al. Crop pests and predators exhibit inconsistent responses to surrounding landscape composition. Proceedings of the National Academy of Sciences of the United States of America. 2018 Aug 14;115(33):E7863-E7870. Epub 2018 Aug 2. doi: 10.1073/pnas.1800042115, 10.1073/pnas.1800042115
Karp, Daniel S. ; Chaplin-Kramer, Rebecca ; Meehan, Timothy D. et al. / Crop pests and predators exhibit inconsistent responses to surrounding landscape composition. In: Proceedings of the National Academy of Sciences of the United States of America. 2018 ; Vol. 115, No. 33. pp. E7863-E7870.
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@article{367a3b7fa85d40969abf5ca5674f0d2e,
title = "Crop pests and predators exhibit inconsistent responses to surrounding landscape composition",
abstract = "The idea that noncrop habitat enhances pest control and represents a win–win opportunity to conserve biodiversity and bolster yields has emerged as an agroecological paradigm. However, while noncrop habitat in landscapes surrounding farms sometimes benefits pest predators, natural enemy responses remain heterogeneous across studies and effects on pests are inconclusive. The observed heterogeneity in species responses to noncrop habitat may be biological in origin or could result from variation in how habitat and biocontrol are measured. Here, we use a pest-control database encompassing 132 studies and 6,759 sites worldwide to model natural enemy and pest abundances, predation rates, and crop damage as a function of landscape composition. Our results showed that although landscape composition explained significant variation within studies, pest and enemy abundances, predation rates, crop damage, and yields each exhibited different responses across studies, sometimes increasing and sometimes decreasing in landscapes with more noncrop habitat but overall showing no consistent trend. Thus, models that used landscape-composition variables to predict pest-control dynamics demonstrated little potential to explain variation across studies, though prediction did improve when comparing studies with similar crop and landscape features. Overall, our work shows that surrounding noncrop habitat does not consistently improve pest management, meaning habitat conservation may bolster production in some systems and depress yields in others. Future efforts to develop tools that inform farmers when habitat conservation truly represents a win–win would benefit from increased understanding of how landscape effects are modulated by local farm management and the biology of pests and their enemies.",
keywords = "Agroecology, Biodiversity, Biological control, Ecosystem services, Natural enemies, Pest Control, Biological, Animals, Crops, Agricultural/growth & development, Models, Biological, Ecosystem",
author = "Karp, {Daniel S.} and Rebecca Chaplin-Kramer and Meehan, {Timothy D.} and Martin, {Emily A.} and Fabrice DeClerck and Heather Grab and Claudio Gratton and Lauren Hunt and Larsen, {Ashley E.} and Alejandra Mart{\'i}nez-Salinas and O{\textquoteright}Rourke, {Megan E.} and Adrien Rusch and Katja Poveda and Mattias Jonsson and Rosenheim, {Jay A.} and Schellhorn, {Nancy A.} and Teja Tscharntke and Wratten, {Stephen D.} and Wei Zhang and Iverson, {Aaron L.} and Adler, {Lynn S.} and Matthias Albrecht and Audrey Alignier and Angelella, {Gina M.} and Anjum, {Muhammad Zubair} and Jacques Avelino and P{\'e}ter Bat{\'a}ry and Baveco, {Johannes M.} and Bianchi, {Felix J.J.A.} and Klaus Birkhofer and Bohnenblust, {Eric W.} and Riccardo Bommarco and Brewer, {Michael J.} and Berta Caballero-L{\'o}pez and Yves Carri{\`e}re and Carvalheiro, {Lu{\'i}sa G.} and Luis Cayuela and Mary Centrella and Aleksandar {\'C}etkovi{\'c} and Henri, {Dominic Charles} and Ariane Chabert and Costamagna, {Alejandro C.} and {De la Mora}, Aldo and {de Kraker}, Joop and Nicolas Desneux and Eva Diehl and Tim Diek{\"o}tter and Dormann, {Carsten F.} and Eckberg, {James O.} and Entling, {Martin H.} and Daniela Fiedler and Pierre Franck and {van Veen}, {F. J.Frank} and Thomas Frank and Vesna Gagic and Garratt, {Michael P.D.} and Awraris Getachew and Gonthier, {David J.} and Goodell, {Peter B.} and Ignazio Graziosi and Groves, {Russell L.} and Gurr, {Geoff M.} and Zachary Hajian-Forooshani and Heimpel, {George E.} and Herrmann, {John D.} and Huseth, {Anders S.} and Incl{\'a}n, {Diego J.} and Ingrao, {Adam J.} and Phirun Iv and Katja Jacot and Johnson, {Gregg A.} and Laura Jones and Marina Kaiser and Kaser, {Joe M.} and Tamar Keasar and Kim, {Tania N.} and Miriam Kishinevsky and Landis, {Douglas A.} and Blas Lavandero and Claire Lavigne and {Le Ralec}, Anne and Debissa Lemessa and Letourneau, {Deborah K.} and Heidi Liere and Yanhui Lu and Yael Lubin and Tim Luttermoser and Bea Maas and Kevi Mace and Filipe Madeira and Viktoria Mader and Cortesero, {Anne Marie} and Lorenzo Marini and Eliana Martinez and Martinson, {Holly M.} and Philippe Menozzi and Mitchell, {Matthew G.E.} and Tadashi Miyashita and Molina, {Gonzalo A.R.} and Molina-Montenegro, {Marco A.} and O{\textquoteright}Neal, {Matthew E.} and Itai Opatovsky and Sebaastian Ortiz-Martinez and Michael Nash and {\"O}rjan {\"O}stman and Annie Ouin and Damie Pak and Daniel Paredes and Soroush Parsa and Hazel Parry and Ricardo Perez-Alvarez and Perovi{\'c}, {David J.} and Peterson, {Julie A.} and Sandrine Petit and Philpott, {Stacy M.} and Manuel Plantegenest and Milan Ple{\'c}as and Therese Pluess and Xavier Pons and Potts, {Simon G.} and Pywell, {Richard F.} and Ragsdale, {David W.} and Rand, {Tatyana A.} and Lucie Raymond and Beno{\^i}t Ricci and Chris Sargent and Sarthou, {Jean Pierre} and Julia Saulais and Jessica Sch{\"a}ckermann and Schmidt, {Nick P.} and Gudrun Schneider and Christof Sch{\"u}epp and Sivakoff, {Frances S.} and Smith, {Henrik G.} and Whitney, {Kaitlin Stack} and Sonja Stutz and Zsofia Szendrei and Takada, {Mayura B.} and Hisatomo Taki and Giovanni Tamburini and Thomson, {Linda J.} and Yann Tricault and Noelline Tsafack and Matthias Tschumi and Muriel Valantin-Morison and {van Trinh}, Mai and {van der Werf}, Wopke and Vierling, {Kerri T.} and Werling, {Ben P.} and Wickens, {Jennifer B.} and Wickens, {Victoria J.} and Woodcock, {Ben A.} and Kris Wyckhuys and Haijun Xiao and Mika Yasuda and Akira Yoshioka and Yi Zou",
note = "Funding information: We thank the many growers, field assistants, pest-control advisors, funders, agricultural experiment stations, and researchers who provided access to study sites, technical expertise, labor, and other types of investment underlying the studies in our database. This work was supported through the National Socio-Environmental Synthesis Center (SESYNC)—National Science Foundation Award DBI-1052875 for the project “Evidence and Decision-Support Tools for Controlling Agricultural Pests with Conservation Interventions” organized by D.S.K. and R.C.-K. ACKNOWLEDGMENTS. We thank the many growers, field assistants, pest-control advisors, funders, agricultural experiment stations, and researchers who provided access to study sites, technical expertise, labor, and other types of investment underlying the studies in our database. This work was supported through the National Socio-Environmental Synthesis Center (SESYNC)—National Science Foundation Award DBI-1052875 for the project “Evidence and Decision-Support Tools for Controlling Agricultural Pests with Conservation Interventions” organized by D.S.K. and R.C.-K.",
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month = aug,
day = "14",
doi = "10.1073/pnas.1800042115",
language = "English",
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journal = "Proceedings of the National Academy of Sciences of the United States of America",
issn = "0027-8424",
publisher = "National Academy of Sciences",
number = "33",

}

Download

TY - JOUR

T1 - Crop pests and predators exhibit inconsistent responses to surrounding landscape composition

AU - Karp, Daniel S.

AU - Chaplin-Kramer, Rebecca

AU - Meehan, Timothy D.

AU - Martin, Emily A.

AU - DeClerck, Fabrice

AU - Grab, Heather

AU - Gratton, Claudio

AU - Hunt, Lauren

AU - Larsen, Ashley E.

AU - Martínez-Salinas, Alejandra

AU - O’Rourke, Megan E.

AU - Rusch, Adrien

AU - Poveda, Katja

AU - Jonsson, Mattias

AU - Rosenheim, Jay A.

AU - Schellhorn, Nancy A.

AU - Tscharntke, Teja

AU - Wratten, Stephen D.

AU - Zhang, Wei

AU - Iverson, Aaron L.

AU - Adler, Lynn S.

AU - Albrecht, Matthias

AU - Alignier, Audrey

AU - Angelella, Gina M.

AU - Anjum, Muhammad Zubair

AU - Avelino, Jacques

AU - Batáry, Péter

AU - Baveco, Johannes M.

AU - Bianchi, Felix J.J.A.

AU - Birkhofer, Klaus

AU - Bohnenblust, Eric W.

AU - Bommarco, Riccardo

AU - Brewer, Michael J.

AU - Caballero-López, Berta

AU - Carrière, Yves

AU - Carvalheiro, Luísa G.

AU - Cayuela, Luis

AU - Centrella, Mary

AU - Ćetković, Aleksandar

AU - Henri, Dominic Charles

AU - Chabert, Ariane

AU - Costamagna, Alejandro C.

AU - De la Mora, Aldo

AU - de Kraker, Joop

AU - Desneux, Nicolas

AU - Diehl, Eva

AU - Diekötter, Tim

AU - Dormann, Carsten F.

AU - Eckberg, James O.

AU - Entling, Martin H.

AU - Fiedler, Daniela

AU - Franck, Pierre

AU - van Veen, F. J.Frank

AU - Frank, Thomas

AU - Gagic, Vesna

AU - Garratt, Michael P.D.

AU - Getachew, Awraris

AU - Gonthier, David J.

AU - Goodell, Peter B.

AU - Graziosi, Ignazio

AU - Groves, Russell L.

AU - Gurr, Geoff M.

AU - Hajian-Forooshani, Zachary

AU - Heimpel, George E.

AU - Herrmann, John D.

AU - Huseth, Anders S.

AU - Inclán, Diego J.

AU - Ingrao, Adam J.

AU - Iv, Phirun

AU - Jacot, Katja

AU - Johnson, Gregg A.

AU - Jones, Laura

AU - Kaiser, Marina

AU - Kaser, Joe M.

AU - Keasar, Tamar

AU - Kim, Tania N.

AU - Kishinevsky, Miriam

AU - Landis, Douglas A.

AU - Lavandero, Blas

AU - Lavigne, Claire

AU - Le Ralec, Anne

AU - Lemessa, Debissa

AU - Letourneau, Deborah K.

AU - Liere, Heidi

AU - Lu, Yanhui

AU - Lubin, Yael

AU - Luttermoser, Tim

AU - Maas, Bea

AU - Mace, Kevi

AU - Madeira, Filipe

AU - Mader, Viktoria

AU - Cortesero, Anne Marie

AU - Marini, Lorenzo

AU - Martinez, Eliana

AU - Martinson, Holly M.

AU - Menozzi, Philippe

AU - Mitchell, Matthew G.E.

AU - Miyashita, Tadashi

AU - Molina, Gonzalo A.R.

AU - Molina-Montenegro, Marco A.

AU - O’Neal, Matthew E.

AU - Opatovsky, Itai

AU - Ortiz-Martinez, Sebaastian

AU - Nash, Michael

AU - Östman, Örjan

AU - Ouin, Annie

AU - Pak, Damie

AU - Paredes, Daniel

AU - Parsa, Soroush

AU - Parry, Hazel

AU - Perez-Alvarez, Ricardo

AU - Perović, David J.

AU - Peterson, Julie A.

AU - Petit, Sandrine

AU - Philpott, Stacy M.

AU - Plantegenest, Manuel

AU - Plećas, Milan

AU - Pluess, Therese

AU - Pons, Xavier

AU - Potts, Simon G.

AU - Pywell, Richard F.

AU - Ragsdale, David W.

AU - Rand, Tatyana A.

AU - Raymond, Lucie

AU - Ricci, Benoît

AU - Sargent, Chris

AU - Sarthou, Jean Pierre

AU - Saulais, Julia

AU - Schäckermann, Jessica

AU - Schmidt, Nick P.

AU - Schneider, Gudrun

AU - Schüepp, Christof

AU - Sivakoff, Frances S.

AU - Smith, Henrik G.

AU - Whitney, Kaitlin Stack

AU - Stutz, Sonja

AU - Szendrei, Zsofia

AU - Takada, Mayura B.

AU - Taki, Hisatomo

AU - Tamburini, Giovanni

AU - Thomson, Linda J.

AU - Tricault, Yann

AU - Tsafack, Noelline

AU - Tschumi, Matthias

AU - Valantin-Morison, Muriel

AU - van Trinh, Mai

AU - van der Werf, Wopke

AU - Vierling, Kerri T.

AU - Werling, Ben P.

AU - Wickens, Jennifer B.

AU - Wickens, Victoria J.

AU - Woodcock, Ben A.

AU - Wyckhuys, Kris

AU - Xiao, Haijun

AU - Yasuda, Mika

AU - Yoshioka, Akira

AU - Zou, Yi

N1 - Funding information: We thank the many growers, field assistants, pest-control advisors, funders, agricultural experiment stations, and researchers who provided access to study sites, technical expertise, labor, and other types of investment underlying the studies in our database. This work was supported through the National Socio-Environmental Synthesis Center (SESYNC)—National Science Foundation Award DBI-1052875 for the project “Evidence and Decision-Support Tools for Controlling Agricultural Pests with Conservation Interventions” organized by D.S.K. and R.C.-K. ACKNOWLEDGMENTS. We thank the many growers, field assistants, pest-control advisors, funders, agricultural experiment stations, and researchers who provided access to study sites, technical expertise, labor, and other types of investment underlying the studies in our database. This work was supported through the National Socio-Environmental Synthesis Center (SESYNC)—National Science Foundation Award DBI-1052875 for the project “Evidence and Decision-Support Tools for Controlling Agricultural Pests with Conservation Interventions” organized by D.S.K. and R.C.-K.

PY - 2018/8/14

Y1 - 2018/8/14

N2 - The idea that noncrop habitat enhances pest control and represents a win–win opportunity to conserve biodiversity and bolster yields has emerged as an agroecological paradigm. However, while noncrop habitat in landscapes surrounding farms sometimes benefits pest predators, natural enemy responses remain heterogeneous across studies and effects on pests are inconclusive. The observed heterogeneity in species responses to noncrop habitat may be biological in origin or could result from variation in how habitat and biocontrol are measured. Here, we use a pest-control database encompassing 132 studies and 6,759 sites worldwide to model natural enemy and pest abundances, predation rates, and crop damage as a function of landscape composition. Our results showed that although landscape composition explained significant variation within studies, pest and enemy abundances, predation rates, crop damage, and yields each exhibited different responses across studies, sometimes increasing and sometimes decreasing in landscapes with more noncrop habitat but overall showing no consistent trend. Thus, models that used landscape-composition variables to predict pest-control dynamics demonstrated little potential to explain variation across studies, though prediction did improve when comparing studies with similar crop and landscape features. Overall, our work shows that surrounding noncrop habitat does not consistently improve pest management, meaning habitat conservation may bolster production in some systems and depress yields in others. Future efforts to develop tools that inform farmers when habitat conservation truly represents a win–win would benefit from increased understanding of how landscape effects are modulated by local farm management and the biology of pests and their enemies.

AB - The idea that noncrop habitat enhances pest control and represents a win–win opportunity to conserve biodiversity and bolster yields has emerged as an agroecological paradigm. However, while noncrop habitat in landscapes surrounding farms sometimes benefits pest predators, natural enemy responses remain heterogeneous across studies and effects on pests are inconclusive. The observed heterogeneity in species responses to noncrop habitat may be biological in origin or could result from variation in how habitat and biocontrol are measured. Here, we use a pest-control database encompassing 132 studies and 6,759 sites worldwide to model natural enemy and pest abundances, predation rates, and crop damage as a function of landscape composition. Our results showed that although landscape composition explained significant variation within studies, pest and enemy abundances, predation rates, crop damage, and yields each exhibited different responses across studies, sometimes increasing and sometimes decreasing in landscapes with more noncrop habitat but overall showing no consistent trend. Thus, models that used landscape-composition variables to predict pest-control dynamics demonstrated little potential to explain variation across studies, though prediction did improve when comparing studies with similar crop and landscape features. Overall, our work shows that surrounding noncrop habitat does not consistently improve pest management, meaning habitat conservation may bolster production in some systems and depress yields in others. Future efforts to develop tools that inform farmers when habitat conservation truly represents a win–win would benefit from increased understanding of how landscape effects are modulated by local farm management and the biology of pests and their enemies.

KW - Agroecology

KW - Biodiversity

KW - Biological control

KW - Ecosystem services

KW - Natural enemies

KW - Pest Control, Biological

KW - Animals

KW - Crops, Agricultural/growth & development

KW - Models, Biological

KW - Ecosystem

UR - http://www.scopus.com/inward/record.url?scp=85050686845&partnerID=8YFLogxK

U2 - 10.1073/pnas.1800042115

DO - 10.1073/pnas.1800042115

M3 - Article

C2 - 30072434

VL - 115

SP - E7863-E7870

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

SN - 0027-8424

IS - 33

ER -