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Shifts in natural enemy assemblages resulting from landscape simplification account for biocontrol loss in wheat fields

  • Original Article
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Ecological Research

Abstract

In recent decades, landscape simplification due to agricultural intensification has resulted in biocontrol loss within agroecosystems leading to an increase in pest outbreaks. Empirical experiments have focused on the relationship between landscape pattern and the abundance of specific species. However, fewer studies have examined the varied responses of multiple natural enemy modules to landscape simplification. In the present study, 23 landscapes were examined to determine the effects of landscape simplification on cereal aphids and their natural enemies. Results showed that landscape simplification can increase cereal aphid populations with no significant effects on the total abundance of natural enemies. For each natural enemy module, it was found that the abundance of parasitic wasps was greatly increased by landscape simplification while the abundance of ground-dwelling predators was significantly reduced. In contrast, the abundance of leaf-dwelling predators was not significantly altered by landscape simplification. Therefore, the varied response of the three natural enemy modules to landscape simplification can result in major fluctuations in natural enemy–pest ratios and ultimately disrupt the top-down control of natural predators and biocontrol services within agroecosystems. In conclusion, quantitative food-web analysis could be a promising technique in clarifying the varied response of the three natural enemy modules to landscape pattern changes and species-specific abundance, a field of biological pest control that requires further study.

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References

  • Batáry P, Holzschuh A, Orci KM, Samu F, Tscharntke T (2012) Responses of plant, insect and spider biodiversity to local and landscape scale management intensity in cereal crops and grasslands. Agric Ecosyst Environ 146:130–136

    Article  Google Scholar 

  • Bianchi FJJA, Booij CJH, Tscharntke T (2006) Sustainable pest regulation in agricultural landscapes: a review on landscape composition, biodiversity and natural pest control. Proc Roy Soc B Biol Sci 273:1715–1727

    Article  CAS  Google Scholar 

  • Bianchi FJJA, Ives AR, Schellhorn NA (2013) Interactions between conventional and organic farming for biocontrol services across the landscape. Ecol Appl 23:1531–1543

    Article  CAS  PubMed  Google Scholar 

  • Blitzer EJ, Dormann CF, Holzschuh A, Klein AM, Rand TA, Tscharntke T (2012) Spillover of functionally important organisms between managed and natural habitats. Agric Ecosyst Environ 146:34–43

    Article  Google Scholar 

  • Brewer MJ, Elliott NC (2004) Biological control of cereal aphids in North America and mediating effects of host plant and habitat manipulations. Annu Rev Entomol 49:219–242

    Article  CAS  PubMed  Google Scholar 

  • Brewer MJ, Goodell PB (2012) Approaches and incentives to implement integrated pest management that addresses regional and environmental issues. Annu Rev Entomol 57:41–59

    Article  CAS  PubMed  Google Scholar 

  • Caballero-Lopez B, Bommarco R, Blanco-Moreno JM, Sans FX, Pujade-Villar J, Rundlof M, Smith HG (2012) Aphids and their natural enemies are differently affected by habitat features at local and landscape scales. Biol Control 63:222–229

    Article  Google Scholar 

  • Chaplin-Kramer R, Kremen C (2012) Pest control experiments show benefits of complexity at landscape and local scales. Ecol Appl 22:1936–1948

    Article  PubMed  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 

  • Chaplin-Kramer R, de Valpine P, Mills NJ, Kremen C (2013) Detecting pest control services across spatial and temporal scales. Agric Ecosyst Environ 181:206–212

    Article  Google Scholar 

  • Clough Y, Kruess A, Kleijn D, Tscharntke T (2005) Spider diversity in cereal fields: comparing factors at local, landscape and regional scales. J Biogeogr 32:2007–2014

    Article  Google Scholar 

  • D’Alberto CF, Hoffmann AA, Thomson LJ (2012) Limited benefits of non-crop vegetation on spiders in Australian vineyards: regional or crop differences? Biocontrol 57:541–552

    Article  Google Scholar 

  • Diehl E, Mader VL, Wolters V, Birkhofer K (2013) Management intensity and vegetation complexity affect web-building spiders and their prey. Oecologia 173:579–589

    Article  PubMed  Google Scholar 

  • Ernoult A, Vialatte A, Butet A, Michel N, Rantier Y, Jambon O, Burel F (2013) Grassy strips in their landscape context, their role as new habitat for biodiversity. Agric Ecosyst Environ 166:15–27

    Article  Google Scholar 

  • Gagic V, Hanke S, Thies C, Scherber C, Tomanovic Z, Tscharntke T (2012) Agricultural intensification and cereal aphid–parasitoid–hyperparasitoid food webs: network complexity, temporal variability and parasitism rates. Oecologia 170:1099–1109

    Article  PubMed Central  PubMed  Google Scholar 

  • Gardiner MM, Landis DA, Gratton C, Schmidt N, O’Neal M, Mueller E, Chacon J, Heimpel GE (2010) Landscape composition influences the activity density of Carabidae and Arachnida in soybean fields. Biol Control 55:11–19

    Article  Google Scholar 

  • Gladbach DJ, Holzschuh A, Scherber C, Thies C, Dormann CF, Tscharntke T (2011) Crop-noncrop spillover: arable fields affect trophic interactions on wild plants in surrounding habitats. Oecologia 166:433–441

    Article  PubMed  Google Scholar 

  • Jonason D, Smith HG, Bengtsson J, Birkhofer K (2013) Landscape simplification promotes weed seed predation by carabid beetles (Coleoptera: Carabidae). Landsc Ecol 28:487–494

    Article  Google Scholar 

  • Jonsson M, Buckley HL, Case BS, Wratten SD, Hale RJ, Didham RK (2012) Agricultural intensification drives landscape-context effects on host–parasitoid interactions in agroecosystems. J Appl Ecol 49:706–714

    Google Scholar 

  • Kondoh M (2008) Building trophic modules into a persistent food web. Proc Natl Acad Sci USA 105:16631–16635

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Macfadyen S, Gibson RH, Symondson WOC, Memmott J (2011) Landscape structure influences modularity patterns in farm food webs: consequences for pest control. Ecol Appl 21:516–524

    Article  PubMed  Google Scholar 

  • Maisonhaute JE, Peres-Neto P, Lucas E (2010) Influence of agronomic practices, local environment and landscape structure on predatory beetle assemblage. Agric Ecosyst Environ 139:500–507

    Article  Google Scholar 

  • Martin EA, Reineking B, Seo B, Steffan-Dewenter I (2013) Natural enemy interactions constrain pest control in complex agricultural landscapes. Proc Natl Acad Sci USA 110:5534–5539

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Meehan TD, Werling BP, Landis DA, Gratton C (2011) Agricultural landscape simplification and insecticide use in the Midwestern United States. Proc Natl Acad Sci USA 108:11500–11505

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • O’Rourke ME, Rienzo-Stack K, Power AG (2011) A multi-scale, landscape approach to predicting insect populations in agroecosystems. Ecol Appl 21:1782–1791

    Article  PubMed  Google Scholar 

  • Pasari JR, Levi T, Zavaleta ES, Tilman D (2013) Several scales of biodiversity affect ecosystem multifunctionality. Proc Natl Acad Sci USA 110:10219–10222

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pleéaš M, Gagic V, Jankovic M, Petrovic-Obradovic O, Kavallieratos NG, Tomanovic Z, Thies C, Tscharntke T, Cetkovic A (2014) Landscape composition and configuration influence cereal aphid–parasitoid–hyperparasitoid interactions and biological control differentially across years. Agric Ecosyst Environ 183:1–10

    Article  Google Scholar 

  • Poveda K, Martinez E, Kersch-Becker MF, Bonilla MA, Tscharntke T (2012) Landscape simplification and altitude affect biodiversity, herbivory and Andean potato yield. J Appl Ecol 49:513–522

    Article  Google Scholar 

  • Raines GL (2002) Description and comparison of geologic maps with FRAGSTATS—a spatial statistics program. Comput Geosci 28:169–177

    Article  Google Scholar 

  • Rand TA, Tscharntke T (2007) Contrasting effects of natural habitat loss on generalist and specialist aphid natural enemies. Oikos 116:1353–1362

    Article  Google Scholar 

  • Rand TA, Tylianakis JM, Tscharntke T (2006) Spillover edge effects: the dispersal of agriculturally subsidized insect natural enemies into adjacent natural habitats. Ecol Lett 9:603–614

    Article  PubMed  Google Scholar 

  • SAS Institute (2006) SAS user’s guide: version 9.1.2. SAS Institute, Cary

    Google Scholar 

  • Scheid BE, Thies C, Tscharntke T (2011) Enhancing rape pollen beetle parasitism within sown flower fields along a landscape complexity gradient. Agric Forest Entomol 13:173–179

    Article  Google Scholar 

  • Schneider G, Krauss J, Steffan-Dewenter I (2013) Predation rates on semi-natural grasslands depend on adjacent habitat type. Basic Appl Ecol 14:614–621

    Article  Google Scholar 

  • Stutz S, Entling MH (2011) Effects of the landscape context on aphid–ant–predator interactions on cherry trees. Biol Control 57:37–43

    Article  Google Scholar 

  • Thies C, Roschewitz I, Tscharntke T (2005) The landscape context of cereal aphid–parasitoid interactions. Proc Roy Soc B Biol Sci 272:203–210

    Article  Google Scholar 

  • Tscharntke T, Bommarco R, Clough Y, Crist TO, Kleijn D, Rand TA, Tylianakis JM, van Nouhuys S, Vidal S (2008) Conservation biological control and enemy diversity on a landscape scale. Biol Control 45:238–253

    Article  Google Scholar 

  • Tscharntke T, Clough Y, Wanger TC, Jackson L, Motzke I, Perfecto I, Vandermeer J, Whitbread A (2012a) Global food security, biodiversity conservation and the future of agricultural intensification. Biol Conserv 151:53–59

    Article  Google Scholar 

  • Tscharntke T, Tylianakis JM, Rand TA, Didham RK, Fahrig L, Batáry P, Bengtsson J, Clough 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 (2012b) Landscape moderation of biodiversity patterns and processes—eight hypotheses. Biol Rev 87:661–685

    Article  PubMed  Google Scholar 

  • Tylianakis JM, Tscharntke T, Lewis OT (2007) Habitat modification alters the structure of tropical host-parasitoid food webs. Nature 445:202–205

    Article  CAS  PubMed  Google Scholar 

  • Veres A, Petit S, Conord C, Lavigne C (2013) Does landscape composition affect pest abundance and their control by natural enemies? A review. Agric Ecosyst Environ 166:110–117

    Article  Google Scholar 

  • Woltz JM, Isaacs R, Landis DA (2012) Landscape structure and habitat management differentially influence insect natural enemies in an agricultural landscape. Agric Ecosyst Environ 152:40–49

    Article  Google Scholar 

  • Zhao ZH, He DH, Hui C (2012) From the inverse density–area relationship to the minimum patch size of a host-parasitoid system. Ecol Res 27:303–309

    Article  Google Scholar 

  • Zhao ZH, Hui C, He DH, Ge F (2013a) Effects of position within wheat field and adjacent habitats on the density and diversity of cereal aphids and their natural enemies. Biocontrol 58:765–776

    Article  CAS  Google Scholar 

  • Zhao ZH, Hui C, Ouyang F, Liu JH, Guan XQ, He DH, Ge F (2013b) Effects of inter-annual landscape change on interactions between cereal aphids and their natural enemies. Basic Appl Ecol 14:472–479

    Article  Google Scholar 

  • Zhao ZH, Liu JH, He DH (2013c) Species composition and diversity of parasitoids and hyperparasitoids in different wheat agro-farming systems. J Insect Sci 13:162

    PubMed Central  PubMed  Google Scholar 

  • Zhao ZH, Hui C, He DH, Li BL (2015) Effects of agricultural intensification on ability of natural enemies to control aphids. Sci Rep 5:8024

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Acknowledgments

We are grateful to two anonymous reviewers for their valuable comments and thoughtful suggestions on an earlier draft, and to many farmers for their facilitation during the field work. We also thank Tingting Zhang, Ying Wang, Jia Hang, Chun Lu, and Xiaohu Li for their help in collecting field data. This work is partly supported by the National Natural Science Foundation of China (31400349; 31101491).

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Authors and Affiliations

  1. Department of Entomology, College of Agriculture and Biotechnology, China Agricultural University, 2 Yuanmingyuan West Road, Haidian District, Beijing, 100193, China

    Zi-Hua Zhao & Feng Gao

  2. Everglades Research and Education Center, University of Florida, Belle Glade, FL, 33430, USA

    Hardev S. Sandhu

  3. College of Agronomy, Ningxia University, Yinchuan, 750021, China

    Da-Han He

Authors
  1. Zi-Hua Zhao
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  2. Hardev S. Sandhu
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  3. Feng Gao
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Correspondence to Zi-Hua Zhao.

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Zhao, ZH., Sandhu, H.S., Gao, F. et al. Shifts in natural enemy assemblages resulting from landscape simplification account for biocontrol loss in wheat fields. Ecol Res 30, 493–498 (2015). https://doi.org/10.1007/s11284-015-1245-7

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  • DOI: https://doi.org/10.1007/s11284-015-1245-7

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