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The activities of generalist parasitoids can be segregated between crop and adjacent non-crop habitats

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Abstract

Non-crop habitat adjacent to crops may be important for enhancing the activity of natural enemies in crops. However, it is not always clear whether natural enemies that are active in non-crop habitats actually contribute to pest suppression in adjacent crop habitats. We hypothesised that parasitic wasps that utilise the same hosts can be segregated between crop and non-crop habitats in an agro-ecosystem. We tested this hypothesis using the light brown apple moth, Epiphyas postvittana (Walker) (Lepidoptera: Tortricidae), in vineyards and adjacent native vegetation. We experimentally measured the parasitism rate of larval E. postvittana at six and eight sites in both vineyards and the adjacent native vegetation in two consecutive years. Wild larval Tortricidae were also collected at each experimental site to assess their diversity and related parasitoids. Parasitised hosts were then identified using a PCR-based protocol to examine the parasitoids’ host ranges. The parasitoid Therophilus unimaculatus (Turner) (Hymenoptera: Braconidae) was most active in non-crop native vegetation, whereas Dolichogenidea tasmanica (Cameron) (Hymenoptera: Braconidae) parasitised the most larvae in vineyards. Parasitism of E. postvittana by D. tasmanica was higher on grape than on plantain, which indicates that host plants influence activities in different habitat. Both species shared the same range of tortricid hosts. Overall, our results indicate the two key parasitoids that attack E. postvittana differ in their pattern of habitat use. The native vegetation adjacent to crops may not enhance the activity of some natural enemies for pest control in an agricultural ecosystem.

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References

  • Alhmedi A, Haubruge E, D’Hoedt S, Francis F (2011) Quantitative food webs of herbivore and related beneficial community in non-crop and crop habitats. Biol Control 58:103–112

    Article  Google Scholar 

  • Amat I, Castelo M, Desouhant E, Bernstein C (2006) The influence of temperature and host availability on the host exploitation strategies of sexual and asexual parasitic wasps of the same species. Oecologia 148:153–161

    Article  PubMed  Google Scholar 

  • Baldissera R, Ganade G, Benedet Fontoura S (2004) Web spider community response along an edge between pasture and Araucaria forest. Biol Conserv 118:403–409

    Article  Google Scholar 

  • Begum M, Gurr GM, Wratten SD, Hedberg PR, Nicol HI (2006) Using selective food plants to maximize biological control of vineyard pests. J Appl Ecol 43:547–554

    Article  Google Scholar 

  • Berndt LA, Wratten SD, Scarratt SL (2006) The influence of floral resource subsidies on parasitism rates of leafrollers (Lepidoptera: Tortricidae) in New Zealand vineyards. Biol Control 37:50–55

    Article  Google Scholar 

  • Bianchi F, van der Werf W (2003) The effect of the area and configuration of hibernation sites on the control of aphids by Coccinella septempunctata (Coleoptera: Coccinellidae) in agricultural landscapes: a simulation study. Environ Entomol 32:1290–1304

    Article  Google Scholar 

  • Bianchi F, Booij C, Tscharntke T (2006) Sustainable pest regulation in agricultural landscapes: a review on landscape composition, biodiversity and natural pest control. Pro R Soc B 273:1715–1727

    Article  CAS  Google Scholar 

  • Blaxter M, Mann J, Chapman T, Thomas F, Whitton C, Floyd R, Abebe E (2005) Defining operational taxonomic units using DNA barcode data. Philos Trans R Soc Lond B Biol Sci 360:1935–1943

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bogran CE, Heinz KM, Ciomperlik MA (2002) Interspecific competition among insect parasitoids: field experiments with whiteflies as hosts in cotton. Ecology 83:653–668

    Article  Google Scholar 

  • Brown J (2005) World catalogue of insects. Volume 5: Tortricidae (Lepidoptera). Apollo Books, Stenstrup

    Google Scholar 

  • Carter M, Sutherland D, Dixon A (1984) Plant structure and the searching efficiency of coccinellid larvae. Oecologia 63:394–397

    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(9):922–932

    Article  PubMed  Google Scholar 

  • Cortesero AM, Stapel JO, Lewis WJ (2000) Understanding and manipulating plant attributes to enhance biological control. Biol Control 17:35–49

    Article  Google Scholar 

  • DeBach P, Rosen D (1991) Biological control by natural enemies, 2nd edn. Cambridge University Press, Cambridge

    Google Scholar 

  • Derocles SAP, Ralec AL, Besson MM, Maret M, Walton A, Evans DM, Plantegenest M (2014) Molecular analysis reveals high compartmentalization in aphid–primary parasitoid networks and low parasitoid sharing between crop and noncrop habitats. Mol Ecol 23:3900–3911

    Article  PubMed  Google Scholar 

  • Duelli P, Studer M, Marchand I, Jakob S (1990) Population movements of arthropods between natural and cultivated areas. Biol Conserv 54:193–207

    Article  Google Scholar 

  • Dyer LE, Landis DA (1997) Influence of noncrop habitats on the distribution of Eriborus terebrans (Hymenoptera: Ichneumonidae) in cornfields. Environ Entomol 26:924–932

    Article  Google Scholar 

  • Feng Y, Wratten S, Sandhu H, Keller M (2015) Interspecific competition between two generalist parasitoids that attack the leafroller Epiphyas postvittana (Lepidoptera: Tortricidae). B Entomol Res. 105:426–433

    Article  CAS  Google Scholar 

  • Fink U, Volkl W (1995) The Effect of abiotic factors on foraging and oviposition success of the aphid parasitoid, Aphidius-Rosae. Oecologia 103:371–378

    Article  Google Scholar 

  • Floyd R, Abebe E, Papert A, Blaxter M (2002) Molecular barcodes for soil nematode identification. Mol Ecol 11:839–850

    Article  CAS  PubMed  Google Scholar 

  • Furlong MJ, Zalucki MP (2007) Parasitoid complex of diamondback moth in south-east Queensland: first records of Oomyzus sokolowskii (Hymenoptera: Eulophidae) in Australia. Aust J Entomol 46:167–175

    Article  Google Scholar 

  • Geervliet JBF, Vet LEM, Dicke M (1994) Volatiles from damaged plants as major cues in long-range host-searching by the specialist parasitoid Cotesia rubecula. Entomol Exp Appl 73:289–297

    Article  CAS  Google Scholar 

  • Grevstad FS, Klepetka BW (1992) The influence of plant architecture on the foraging efficiencies of a suite of ladybird beetles feeding on aphids. Oecologia 92:399–404

    Article  Google Scholar 

  • Gurr GM, Wratten SD, Barbosa P (2000) Success in conservation biological control of arthropods. In: Gurr GM, Wratten SD (eds) Biological control: measures of success. Springer, Dordrecht, pp 105–132

    Chapter  Google Scholar 

  • Hajibabaei M, Janzen DH, Burns JM, Hallwachs W, Hebert PD (2006) DNA barcodes distinguish species of tropical Lepidoptera. Proc Natl Acad Sci USA 103:968–971

    Article  PubMed  PubMed Central  Google Scholar 

  • Holland J, Fahrig L (2000) Effect of woody borders on insect density and diversity in crop fields: a landscape-scale analysis. Agric Ecosyst Environ 78:115–122

    Article  Google Scholar 

  • Holt R, Hochberg M (2001) Biological Control: a Theoretical Perspective. In: Wajnberg E, Scott JK, Quimby PC (eds) Evaluating indirect ecological effects of biological control. CAB International, Wallingford, pp 13–37

    Google Scholar 

  • Holzschuh A, Steffan-Dewenter I, Tscharntke T (2010) How do landscape composition and configuration, organic farming and fallow strips affect the diversity of bees, wasps and their parasitoids? J Anim Ecol 79:491–500

    Article  PubMed  Google Scholar 

  • Janković M, Plećaš M, Sandić D, Popović A, Petrović A, Petrović-Obradović O et al (2016) Functional role of different habitat types at local and landscape scales for aphids and their natural enemies. J Pest Sci. doi:10.1007/s10340-016-0744-9

    Google Scholar 

  • Kruess A, Tscharntke T (1994) Habitat fragmentation, species Loss, and biological-control. Science 264:1581–1584

    Article  CAS  PubMed  Google Scholar 

  • Landis DA, Wratten SD, Gurr GM (2000) Habitat management to conserve natural enemies of arthropod pests in agriculture. Annu Rev Entomol 45:175–201

    Article  CAS  PubMed  Google Scholar 

  • Lee JC, Heimpel GE (2008) Floral resources impact longevity and oviposition rate of a parasitoid in the field. J Anim Ecol 77:565–572

    Article  PubMed  Google Scholar 

  • Letourneau D, Altieri M (1999) Environmental management to enhance biological control in agroecosystems. In: Fisher TWTSB, Caltagirone LE, Dahlsten DL (eds) Handbook of biological control. Academic, San Diego, pp 319–354

    Chapter  Google Scholar 

  • Martin TJ, Major RE (2001) Changes in wolf spider (Araneae) assemblages across woodland–pasture boundaries in the central wheat-belt of New South Wales, Australia. Austral Ecol 26:264–274

    Article  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  CAS  PubMed  PubMed Central  Google Scholar 

  • Miliczky E, Horton D (2005) Densities of beneficial arthropods within pear and apple orchards affected by distance from adjacent native habitat and association of natural enemies with extra-orchard host plants. Biol Control 33:249–259

    Article  Google Scholar 

  • Oksanen T (1990) Exploitation ecosystems in heterogeneous habitat complexes. Evol Ecol 4:220–234

    Article  Google Scholar 

  • Olson DM, Wäckers FL (2007) Management of field margins to maximize multiple ecological services. J Appl Ecol 44:13–21

    Article  Google Scholar 

  • Orr DB, Garcia-Salazar C, Landis DA (2000) Trichogramma nontarget impacts: a method for biological control risk assessment. In: Follett P, Duan JJ (eds) Nontarget effects of biological control. Springer, New York, pp 111–125

    Chapter  Google Scholar 

  • Papaj DR, Vet LE (1990) Odor learning and foraging success in the parasitoid, Leptopilina heterotoma. J Chem Ecol 16:3137–3150

    Article  CAS  PubMed  Google Scholar 

  • Paull C (2007) The ecology of key arthropods for the management of Epiphyas postvittana (Walker) (Lepidoptera: Tortricidae) in Coonawarra vineyards, South Australia. PhD dissertation, School of Earth and Environmental Sciences, University of Adelaide, Adelaide, South Australia

  • Paull C, Austin AD (2006) The hymenopteran parasitoids of light brown apple moth, Epiphyas postvittana (Walker) (Lepidoptera: Tortricidae) in Australia. Aust J Entomol 45:142–156

    Article  Google Scholar 

  • Paull C, Schellhorn N, Austin A (2013) Response to host density by the parasitoid Dolichogenidea tasmanica (Hymenoptera: Braconidae) and the influence of grapevine variety. Bull Entomol Res 104:1–9

    Google Scholar 

  • Pfannenstiel RS, Mackey BE, Unruh TR (2012) Leafroller parasitism across an orchard landscape in central Washington and effect of neighboring rose habitats on parasitism. Biol Control 62:152–161

    Article  Google Scholar 

  • Poelman EH, Bruinsma M, Zhu F, Weldegergis BT, Boursault AE, Jongema Y, van Loon JJ, Vet LE, Harvey JA, Dicke M (2009) Field parasitism rates of caterpillars on Brassica oleracea plants are reliably predicted by differential attraction of Cotesia parasitoids. Funct Ecol 23:951–962

    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 

  • Ries L, Fletcher RJ Jr, Battin J, Sisk TD (2004) Ecological responses to habitat edges: mechanisms, models, and variability explained. Annu Rev Ecol Evol Syst 35:491–522

    Article  Google Scholar 

  • Rougerie R, Smith MA, Fernandez-Triana J, Lopez-Vaamonde C, Ratnasingham S, Hebert PD (2011) Molecular analysis of parasitoid linkages (MAPL): gut contents of adult parasitoid wasps reveal larval host. Mol Ecol 20:179–186

    Article  PubMed  Google Scholar 

  • Rubinoff D, Holland BS, San Jose M, Powell JA (2011) Geographic proximity not a prerequisite for invasion: Hawaii not the source of California invasion by light brown apple moth (Epiphyas postvittana). PLoS One 6:e16361

    Article  PubMed  PubMed Central  Google Scholar 

  • Scarratt SL, Wratten SD, Shishehbor P (2008) Measuring parasitoid movement from floral resources in a vineyard. Biol Control 46:107–113

    Article  Google Scholar 

  • Scholefield P, Morison J (2010) Assessment of economic cost of endemic pests & diseases on the Australian grape & wine industry (GWR 08/04). Final report to the Grape & Wine Research & Development Corporation, Adelaide, SA, Australia. Avaliable via DIALOG. http://research.agwa.net.au/completed_projects/assessment-of-economic-cost-of-endemic-pests-and-diseases-on-the-australian-grape-and-wine-industry/. Accessed 14 Feb 2015

  • Segoli M, Rosenheim JA (2013) The link between host density and egg production in a parasitoid insect: comparison between agricultural and natural habitats. Funct Ecol 27:1224–1232

    Article  Google Scholar 

  • Smith L, Rutz DA (1991) The influence of light and moisture gradients on the attack rate of parasitoids foraging for hosts in a laboratory arena (Hymenoptera, Pteromalidae). J Insect Behav 4:195–208

    Article  Google Scholar 

  • Smith MA, Fisher BL, Hebert PD (2005) DNA barcoding for effective biodiversity assessment of a hyperdiverse arthropod group: the ants of Madagascar. Philos Trans R Soc Lond B Biol Sci 360:1825–1834

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith MA, Rodriguez JJ, Whitfield JB, Deans AR, Janzen DH, Hallwachs W, Hebert PD (2008) Extreme diversity of tropical parasitoid wasps exposed by iterative integration of natural history, DNA barcoding, morphology, and collections. Proc Natl Acad Sci USA 105:12359–12364

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith MA, Fernandez-Triana J, Roughley ROB, Hebert PDN (2009) DNA barcode accumulation curves for understudied taxa and areas. Mol Ecol Resour 9:208–216

    Article  CAS  PubMed  Google Scholar 

  • Steinberg S, Dicke M, Vet L, Wanningen R (1992) Response of the braconid parasitoid Cotesia (=Apanteles) glomerata to volatile infochemicals: effects of bioassay set-up, parasitoid age and experience and barometric flux. Entomol Exp Appl 63:163–175

    Article  CAS  Google Scholar 

  • Stephens MJ, France CM, Wratten SD, Frampton C (1998) Enhancing biological control of leafrollers (Lepidoptera: Tortricidae) by sowing buckwheat (Fagopyrum esculentum) in an orchard. Biocontrol Sci Technol 8:547–558

    Article  Google Scholar 

  • Suckling DM, Brockerhoff EG (2010) Invasion biology, ecology, and management of the light brown apple moth (Tortricidae). Annu Rev Entomol 55:285–306

    Article  CAS  PubMed  Google Scholar 

  • Suckling DM, Burnip GM, Walker JTS (1998) Abundance of leaf rollers and their parasitoids on selected host plants in New Zealand. N Z J Crop Hortic Sci 26:193–203

    Article  Google Scholar 

  • Suckling DM, Burnip GM, Gibb AR, Daly JM, Armstrong KF (2001) Plant and host effects on the leafroller parasitoid Dolichogenidia tasmanica. Entomol Exp Appl 100:253–260

    Article  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thies C, Tscharntke T (1999) Landscape structure and biological control in agroecosystems. Science 285:893–895

    Article  CAS  PubMed  Google Scholar 

  • Thomas M, Wratten S, Sotherton N (1991) Creation of ‘island’ habitats in farmland to manipulate populations of beneficial arthropods: predator densities and emigration. J Appl Ecol 28:906–917

    Article  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thomson LJ, Hoffmann AA (2010) Natural enemy responses and pest control: importance of local vegetation. Biol Control 52:160–166

    Article  Google Scholar 

  • van Emden H (1965) The role of uncultivated land in the biology of crop pests and beneficial insects. Sci Hortic 17:121–136

    Google Scholar 

  • Vet LE, Dicke M (1992) Ecology of infochemical use by natural enemies in a tritrophic context. Annu Rev Entomol 37:141–172

    Article  Google Scholar 

  • Vet LE, Lewis WJ, Carde RT (1995) Parasitoid foraging and learning. In: Carde RT, Bell WJ (eds) Chemical ecology of insects 2. Springer, New York, pp 65–101

    Chapter  Google Scholar 

  • Wilby A, Thomas MB (2002) Natural enemy diversity and pest control: patterns of pest emergence with agricultural intensification. Ecol Lett 5:353–360

    Article  Google Scholar 

  • Williams L, Martinson TE (2000) Colonization of New York vineyards by Anagrus spp. (Hymenoptera: Mymaridae): overwintering biology, within-vineyard distribution of wasps, and parasitism of grape leafhopper, Erythroneura spp. (Homoptera: Cicadellidae), eggs. Biol Control 18:136–146

    Article  Google Scholar 

  • Wissinger SA (1997) Cyclic colonization in predictably ephemeral habitats: a template for biological control in annual crop systems. Biol Control 10:4–15

    Article  Google Scholar 

  • Wratten SD, Lavandero BI, Tylianakis J, Vattala D, Cilgi T, Sedcole R (2004) Effects of flowers on parasitoid longevity and fecundity. N Z Plant Prot 56:239–245

    Google Scholar 

  • Yazdani M, Feng Y, Glatz R, Keller MA (2014) Host stage preference of Dolichogenidea tasmanica (Cameron, 1912) (Hymenoptera: Braconidae), a parasitoid of Epiphyas postvittana (Walker, 1863) (Lepidoptera: Tortricidae). Aust Entomol. 54:325–331

    Article  Google Scholar 

  • Zar JH (1999) Biostatistical analysis, 2nd edn. Prentice-Hall, Englewood Cliffs

    Google Scholar 

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Acknowledgments

This research was made possible through scholarships to Yi Feng awarded by the Grape and Wine Research Development Corporation, the China Scholarship Council and the University of Adelaide. We thank managers who allowed us to conduct experiments in their vineyards: Craig Markby, Janet Klein, Dave Hamilton, Greg Horner, Katrina Horner, James Thorpe, Murray Leake, Mike Harms, Peter McIntyre and Geoff Hardy. We thank Roberta Hitchcock for her help with the molecular identification of tortricid species and Nicholas Stevens for his help in identifying Therophilus unimaculatus. We thank Arthur Selwyn Mark, Ahmad Chatha, Maryam Yazdani, Mitch Flint, Tao Wang, Yan Ma and Yulin Zhang for their assistance with field experiments and insect sampling. We thank Michael Nash and Maarten van Helden for their valuable comments on an early version of this paper. There are no sources of conflict of interest.

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Communicated by B. Lavandero.

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Sequences deposited in GenBank (Accession Numbers: KF146183-KF146214; KM115588-KM115616).

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Feng, Y., Kravchuk, O., Sandhu, H. et al. The activities of generalist parasitoids can be segregated between crop and adjacent non-crop habitats. J Pest Sci 90, 275–286 (2017). https://doi.org/10.1007/s10340-016-0775-2

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