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Organic farming affects the biological control of hemipteran pests and yields in spring barley independent of landscape complexity

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Abstract

Context

Hemipteran pests cause significant yield losses in European cereal fields. It has been suggested that local management interventions to promote natural enemies are most successful in simple landscapes that are dominated by large arable fields.

Objectives

We study how farming category (conventional, new and old organic fields) and landscape complexity affect pests, natural enemies and biological control services in spring barley. We further analyse if yields are related to pest infestation or biological control services.

Methods

The amount of pasture and the length of field borders were used to define landscape complexity around barley fields in Southern Sweden. Arthropods were sampled with an insect suction sampler and predation and parasitism services were estimated by field observations and inspections of pest individuals.

Results

Pest infestation was affected by landscape complexity, with higher aphid, but lower leafhopper numbers in more complex landscapes. Aphid predation was higher under organic farming and affected by effects on predator abundance and community composition independent of landscape complexity. Auchenorrhyncha parasitism was neither significantly affected by landscape complexity nor by farming category. Higher aphid predation rates and lower aphid densities were characteristic for organically managed fields with higher barley yields.

Conclusions

Our results suggest that it is possible to increase both aphid biological control services and barley yield via local management effects on predator communities independent of landscape complexity. However, the success of such management practices is highly dependent on the pest and natural enemy taxa and the nature of the trophic interaction.

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References

  • Agusti N, Shayler SP, Harwood JD, Vaughan IP, Sunderland KD, Symondson WOC (2003) Collembola as alternative prey sustaining spiders in arable ecosystems: prey detection within predators using molecular markers. Mol Ecol 12:3467–3475

    Article  CAS  PubMed  Google Scholar 

  • Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Aust Ecol 26:32–46

    Google Scholar 

  • Anderson MJ, Willis TJ (2003) Canonical analysis of principal coordinates: a useful method of constrained ordination for ecology. Ecology 84:511–525

    Article  Google Scholar 

  • Bianchi FJJA, Van Der Werf W (2005) The function of non-crop habitats for sustainable pest control in agroecosystems. Trends Biodivers Res 147–170:2005

    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 R Soc B 273:1715–1727

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Birkhofer K, Scheu S, Wise DH (2007) Small-scale spatial pattern of web-building spiders (Araneae) in alfalfa: relationship to disturbance from cutting, prey availability, and intraguild interactions. Environ Entomol 36:801–810

    Article  PubMed  Google Scholar 

  • Birkhofer K, Gavish-Regev E, Endlweber K, Lubin YD, Von Berg K, Wise DH, Scheu S (2008a) Cursorial spiders retard initial aphid population growth at low densities in winter wheat. Bull Entomol Res 98:249–255

    CAS  PubMed  Google Scholar 

  • Birkhofer K, Bezemer MT, Bloem J, Bonkowski M, Christensen S, Dubois D, Ekelund F, Fliessbach A, Gunst L, Hedlund K, Maeder P, Mikola J, Robin C, Setala H, Tatin-Froux F, Van Der Putten WH, Scheu S (2008b) Long-term organic farming fosters below and aboveground biota: implications for soil quality, biological control and productivity. Soil Biol Biochem 40:2297–2308

    Article  CAS  Google Scholar 

  • Birkhofer K, Fliessbach A, Wise DH, Scheu S (2008c) Generalist predators in organically and conventionally managed grass-clover fields: implications for conservation biological control. Annals Appl Biol 153:271–280

    Google Scholar 

  • Birkhofer K, Fliessbach A, Wise DH, Scheu S (2011) Arthropod food webs in organic and conventional wheat farming systems of an agricultural long-term experiment: a stable isotope approach. Agric Forest Entomol 13:197–204

    Article  Google Scholar 

  • Birkhofer K, Bezemer TM, Hedlund K, Setälä H (2012) Community composition of soil organisms under different wheat farming systems. In: Cheeke T, Coleman DC, Wall DH (eds) Microbial ecology in sustainable agroecosystems. Advances in agroecology. CRC Press, Boca Raton, p 292

    Google Scholar 

  • Birkhofer K, Entling M, Lubin Y (2013) Agroecology: trait composition, spatial relationships, trophic interactions. In: Penney D (ed) Spider research in the 21st century: trends & perspectives. Siri Scientific Press, Manchester

    Google Scholar 

  • Bommarco R, Wetterlind S, Sigvald R (2007) Cereal aphid populations in non-crop habitats show strong density dependence. J Appl Ecol 44:1013–1022

    Article  Google Scholar 

  • Carter N, Mclean IFG, WattAD Dixon AFG (1980) Cereal aphids: a case study and review. Appl Biol 5:271–348

    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 

  • Costamagna AC, Menalled FD, Landis DA (2004) Host density influences parasitism of the armyworm Pseudaletia unipuncta in agricultural landscapes. Basic Appl Ecol 5:347–355

    Article  Google Scholar 

  • Crowder DW, Northfield TD, Strand MR, Snyder WE (2010) Organic agriculture promotes evenness and natural pest control. Nature 466:109–123

    Article  CAS  PubMed  Google Scholar 

  • Dean GJ (1973) Aphid colonization of spring cereals. Ann Appl Biol 75:183–193

    Article  Google Scholar 

  • Dewar AM, Carter N (1984) Decision trees to assess the risk of cereal aphid (Hemiptera, Aphididae) outbreaks in summer in england. Bull Entomol Res 74:387–398

    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 

  • Dixon AFG, Kundu R (1998) Resource tracking in aphids: programmed reproductive strategies anticipate seasonal trends in habitat quality. Oecologia 114:73–78

    Article  Google Scholar 

  • Dlabola J, Taimr L (1965) Some results obtained with the application of the tracer method in insect migration and dispersion studies. Acta Entomol Bohemoslov 62:413–420

    Google Scholar 

  • Falk BW, Tsai JH (1998) Biology and molecular biology of viruses in the genus Tenuivirus. Ann Rev Phytopathol 36:139–163

    Article  CAS  Google Scholar 

  • Gagic V, Tscharntke T, Dormann CF, Gruber B, Wilstermann A, Thies C (2011) Food web structure and biocontrol in a four-trophic level system across a landscape complexity gradient. Proc R Soc B 278:2946–2953

    Article  PubMed Central  PubMed  Google Scholar 

  • Gardiner MM, Landis DA, Gratton C, Difonzo CD, O’Neal M, Chacon JM, Wayo MT, Schmidt NP, Mueller EE, Heimpel GE (2009) Landscape diversity enhances biological control of an introduced crop pest in the north-central USA. Ecol Appl 19:143–154

    Article  CAS  PubMed  Google Scholar 

  • Grilli MP, Gorla DE (1999) The distribution and abundance of Delphacidae (Homoptera) in Central Argentina. J Appl Entomol 123:13–21

    Article  Google Scholar 

  • Guglielmino A (2002) Dryinidae (Hymenoptera Chrysidoidea): an interesting group among the natural enemies of the Auchenorrhyncha (Hemiptera). Denisia 176:549–556

    Google Scholar 

  • Guglielmino A, Olmi M, Bueckle C (2013) An updated host-parasite catalogue of world Dryinidae (Hymenoptera: Chrysidoidea). Zootaxa 3740:1–98

    Article  PubMed  Google Scholar 

  • Hill DS (1987) Agricultural insect pests of temperate regions and their control. Cambridge University Press, London

    Google Scholar 

  • Holland JM, Oaten H, Moreby S, Birkett T, Simper J, Southway S, Smith BM (2012) Agri-environment scheme enhancing ecosystem services: a demonstration of improved biological control in cereal crops. Agric Ecosyst Environ 155:147–152

    Article  Google Scholar 

  • Hooks CRR, Pandey RR, Johnson MW (2006) Effects of spider presence on Artogeia rapae and host plant biomass. Agric Ecosyst Environ 112:73–77

    Article  Google Scholar 

  • Jmhasly P, Nentwig W (1995) Habitat management in winter-wheat and evaluation of subsequent spider predation on insect pests. Acta Oecol 16:389–403

    Google Scholar 

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

  • Jordbruksverket (2014) Växtskyddsinfo Havrebladlusen och korn. http://www.jordbruksverket.se/etjanster/etjanster/vaxtskyddsinfo.4.35974d0d12179bec28580002425.html. Accessed Aug 2015

  • Jurczyk M, Wolters V, Birkhofer K (2012) Utilization of prey-rich patches leads to reproductive advantages for clustered individuals of a web-building spider. Ecoscience 19:170–176

    Article  Google Scholar 

  • Kennedy TF, Connery J (2005) Grain yield reductions in spring barley due to barley yellow dwarf virus and aphid feeding. Irish J Agric Food Res 44:111–128

    Google Scholar 

  • Klueken AM, Simon J-C, Hondelmann P, Mieuzet L, Gilabert A, Poehling H-M, Hau B (2012) Are primary woody hosts ‘island refuges’ for host-alternating aphids and important for colonization of local cereals? J Appl Entomol 135:347–360

    Article  Google Scholar 

  • Kuusk A-K, Ekbom B (2010) Lycosid spiders and alternative food: feeding behavior and implications for biological control. Biol Control 55:20–26

    Article  Google Scholar 

  • Lang A, Filser J, Henschel JR (1999) Predation by ground beetles and wolf spiders on herbivorous insects in a maize crop. Agric Ecosys Environ 72:189–199

    Article  Google Scholar 

  • Lapierre H, Signoret P (2004) Viruses and virus diseases of Poaceae (Graminae). Inra-Quae, 857p

  • Larsson H (2005) A crop loss model and economic thresholds for the grain aphid, Sitobion avenae (F.), in winter wheat in Southern Sweden. Crop Prot 24:397–405

    Article  Google Scholar 

  • Leather SR, Walters KFA, Dixon AFG (1989) Factors determining the pest status of the bird cherry-oat aphid, Rhopalosiphum padi (L) (Hemiptera, Aphididae), in Europe—a study and review. Bull Entomol Res 79:345–360

    Article  Google Scholar 

  • Macfadyen S, Gibson R, Raso L, Sint D, Traugott M, Memmott J (2009) Parasitoid control of aphids in organic and conventional farming systems. Agric Ecosyst Environ 133:14–18

    Article  Google Scholar 

  • Marc P, Canard A, Ysnel F (1999) Spiders (Araneae) useful for pest limitation and bioindication. Agric Ecosyst Environ 74:229–273

    Article  Google Scholar 

  • Menalled FD, Costamagna AC, Marino PC, Landis DA (2003) Temporal variation in the response of parasitoids to agricultural landscape structure. Agric Ecosyst Environ 96:29–35

    Article  Google Scholar 

  • Nyffeler M, Benz G (1988) Prey and predatory importance of micryphantid spiders in winter wheat fields and hay meadows. J Appl Entomol 105:190–197

    Article  Google Scholar 

  • Nyffeler M, Sunderland KD (2003) Composition, abundance and pest control potential of spider communities in agroecosystems: a comparison of European and US studies. Agric Ecosyst Environ 95:579–612

    Article  Google Scholar 

  • Öberg S, Ekbom B, Bommarco R (2007) Influence of habitat type and surrounding landscape on spider diversity in Swedish agroecosystems. Agric Ecosyst Environ 122:211–219

    Article  Google Scholar 

  • Oerke EC (2006) Crop losses to pests. J Agric Sci 144:31–43

    Article  Google Scholar 

  • Östman O, Ekbom B, Bengtsson J (2001) Landscape heterogeneity and farming practice influence biological control. Basic Appl Ecol 2:365–371

    Article  Google Scholar 

  • Östman Ö, Ekbom B, Bengtsson J (2003) Yield increase attributable to aphid predation by ground-living polyphagous natural enemies in spring barley in Sweden. Ecol Econ 45:149–158

    Article  Google Scholar 

  • Persson AS, Olsson O, Rundlöf M, Smith HG (2010) Land use intensity and landscape complexity-analysis of landscape characteristics in an agricultural region in Southern Sweden. Agric Ecosyst Environ 136:169–176

    Article  Google Scholar 

  • Plumb RT (1983) Barley yellow dwarf virus-a global problem. In: Plumb RT, Thresh JM (eds) Plant virus epidemiology. The spread and control of insect-borne viruses. Blackwell Science, Oxford, pp 185–198

    Google Scholar 

  • Raatikainen M (1967) Bionomics, enemies and population dynamics of Javasella pellucida Fbr. (Homopt., Delphacidae). Annal Agric Fenniae 6:1–149

    Google Scholar 

  • Roschewitz I, Hucker M, Tscharntke T, Thies C (2005) The influence of landscape context and farming practices on parasitism of cereal aphids. Agric Ecosys Environ 108:218–227

    Article  Google Scholar 

  • Rusch A, Valantin-Morison M, Sarthou J-P, Roger-Estrade J (2010) Biological control of insect pests in agroecosystems: effects of crop management, farming systems, and seminatural habitats at the landscape scale: a review. Adv Agron 109:219–259

    Article  Google Scholar 

  • Rusch A, Bommarco R, Jonsson M, Smith HG, Ekbom B (2013) Flow and stability of natural pest control services depend on complexity and crop rotation at the landscape scale. J Appl Ecol 50:345–354

    Article  Google Scholar 

  • Schmidt MH, Lauer A, Purtauf T, Thies C, Schaefer M, Tscharntke T (2003) Relative importance of predators and parasitoids for cereal aphid control. Proc R Soc B 270:1905–1909

    Article  PubMed Central  PubMed  Google Scholar 

  • Schmidt JM, Harwood JD, Rypstra AL (2012) Foraging activity of a dominant epigeal predator: molecular evidence for the effect of prey density on consumption. Oikos 121:1715–1724

    Article  Google Scholar 

  • Shackelford G, Steward PR, Benton TG, Kunin WE, Potts SG, Biesmeijer JC, Sait SM (2013) Comparison of pollinators and natural enemies: a meta-analysis of landscape and local effects on abundance and richness in crops. Biol Rev 88:1002–1021

    Article  PubMed  Google Scholar 

  • Sigvald R (2011) Forecasting and warning systems for pests and diseases of field crops in Sweden. NJF Report 7:25–30

    Google Scholar 

  • Snyder WE, Wise DH (1999) Predator interference and the establishment of generalist predator populations for biocontrol. Biol Control 15:283–292

    Article  Google Scholar 

  • Sunderland KD, Fraser AM, Dixon AFG (1986) Distribution of linyphiid spiders in relation to capture of prey in cereal fields. Pedobiologia 29:367–375

    Google Scholar 

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

    Article  PubMed Central  PubMed  Google Scholar 

  • Thies C, Haenke S, Scherber C, Bengtsson J, Bommarco R, Clement LW, Ceryngier P, Dennis C, Emmerson M, Gagic V, Hawro V, Liira J, Weisser WW, Winqvist C, Tscharntke T (2011) The relationship between agricultural intensification and biological control: experimental tests across Europe. Ecol Appl 21:2187–2196

    Article  PubMed  Google Scholar 

  • Tscharntke T, Klein AM, Kruess A, Steffan-Dewenter I, Thies C (2005) Landscape perspectives on agricultural intensification and biodiversity—ecosystem service management. Ecol Lett 8:857–874

    Article  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 

  • Von Berg K, Thies C, Tscharntke T, Scheu S (2010) Changes in herbivore control in arable fields by detrital subsidies depend on predator species and vary in space. Oecologia 163:1033–1042

    Article  Google Scholar 

  • Winqvist C, Bengtsson J, Aavik T, Berendse F, Clement LW, Eggers S, Fischer C, Flohre A, Geiger F, Liira J, Paert T, Thies C, Tscharntke T, Weisser WW, Bommarco R (2011) Mixed effects of organic farming and landscape complexity on farmland biodiversity and biological control potential across Europe. J Appl Ecol 48:570–579

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Zhao Z-H, Hui C, Hardev S, Ouyang F, Dong Z, Ge F (2014) Responses of cereal aphids and their parasitic wasps to landscape complexity. J Econ Entomol 107:630–637

    Article  PubMed  Google Scholar 

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Acknowledgments

We are grateful to three anonymous referees that helped improving a previous version of the manuscript. We thank the farmers for letting us work on their fields and Herbert Nickel for the identification of leafhoppers. The project was financed by The Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning (FORMAS) and the Crafoordska Stiftelsen.

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Birkhofer, K., Arvidsson, F., Ehlers, D. et al. Organic farming affects the biological control of hemipteran pests and yields in spring barley independent of landscape complexity. Landscape Ecol 31, 567–579 (2016). https://doi.org/10.1007/s10980-015-0263-8

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  • DOI: https://doi.org/10.1007/s10980-015-0263-8

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