Abstract
Agricultural intensification is a major driver of biodiversity decline in many species including arthropods. This may also affect important ecosystem services such as natural pest regulation. Traditional grapevine varieties rely on a high number of fungicide applications, which can be greatly reduced in novel fungus resistant cultivars. Additionally, in contrast to the traditional trellis system, the semi-minimal pruned hedge offers a structurally more diverse habitat for arthropods. We investigated natural control of the grapevine pest Lobesia botrana ([Denis & Schiffermüller], 1775) (Lepidoptera: Tortricidae) with artificial inoculation of grape bunches, egg baits, camera surveillance and beatsheet sampling of predators. Reduced fungicide applications enhanced densities of L. botrana predators along with increased egg predation and reduced damage of inoculated grape bunches. Minimal pruning did not have a clear effect. Improved pest control potential adds to other advantages of reduced fungicide applications. Planting fungus-resistant varieties should be augmented, potentially also in other crop systems that rely heavily on fungicides.
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References
Altieri MA (1999) The ecological role of biodiversity in agroecosystems. Agric Ecosyst Environ 74:19–31
Andow DA, Prokrym DR (1990) Plant structural complexity and host-finding by a parasitoid. Oecologia 82:162–165
Bagnoli B, Lucchi A (2006) Parasitoids of Lobesia botrana (Den. & Schiff.) in Tuscany. IOBC/WPRS Bull 29:139–142
Barnay O, Hommay G, Gertz C, Kienlen JC, Schubert G, Marro JP, Pizzol J, Chavigny P (2001) Survey of natural populations of Trichogramma (Hym., Trichogrammatidae) in the vineyards of Alsace (France). J Appl Entomol 125:469–477
Bartlett BR (1964) Toxicity of some pesticides to eggs, larvae, and adults of the green lacewing, Chrysopa carnea. J Econ Entomol 57:366–369
Beers EH, Martinez-Rocha L, Talley RR, Dunley JE (2009) Lethal, sublethal, and behavioral effects of sulfur-containing products in bioassays of three species of orchard mites. J Econ Entomol 102:324–335
Benton TG, Bryant DM, Cole L, Crick HQP (2002) Linking agricultural practice to insect and bird populations: a historical study over three decades. J Appl Ecol 39:673–687
Bianchi F, Booij CJH, Tscharntke T (2006) Sustainable pest regulation in agricultural landscapes: a review on landscape composition, biodiversity and natural pest control. Proc R Soc London B Biol Sci 273:1715–1727
Bommarco R, Kleijn D, Potts SG (2013) Ecological intensification: harnessing ecosystem services for food security. Trends Ecol Evol 28:230–238
Bruggisser OT, Schmidt-Entling MH, Bacher S (2010) Effects of vineyard management on biodiversity at three trophic levels. Biol Conserv 143:1521–1528
Bundschuh M, Elsaesser D, Stang C, Schulz R (2016) Mitigation of fungicide pollution in detention ponds and vegetated ditches within a vine-growing area in Germany. Ecol Eng 89:121–130
Castaneda-Samayoa O, Holst H, Ohnesorge B (1993) Evaluation of some Trichogramma species with respect to biological control of Eupoecilia ambiguella Hb. and Lobesia botrana Schiff. (Lep., Tortricidae). Zeitschrift für Pflanzenkrankheiten und Pflanzenschutz/ Journal Plant Dis Prot 100:599–610
Childers CC, Villanueva R, Aguilar H, Chewning R, Michaud JP (2001) Comparative residual toxicities of pesticides to the predator Agistemus industani (Acari: Stigmaeidae) on citrus in Florida. Exp Appl Acarol 25:461–474
Desneux N, Decourtye A, Delpuech J-M (2007) The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol 52:81–106
Diehl E, Sanhudo CED, Diehl-Fleig E (2004) Ground-dwelling ant fauna of sites with high levels of copper. Brazilian J Biol 64:33–39
Duso C, Pozzebon A, Kreiter S, Tixier M-S, Candolfi M (2012) Management of phytophagous mites in European vineyards. In: Bostanian NJ, Vincent C, Isaacs R (eds) Arthropod management in vineyards. Springer, New York, pp 191–217
Eijsackers H, Beneke P, Maboeta M, Louw JPE, Reinecke AJ (2005) The implications of copper fungicide usage in vineyards for earthworm activity and resulting sustainable soil quality. Ecotoxicol Environ Saf 62:99–111
Fischer BM, Salakhutdinov I, Akkurt M, Eibach R, Edwards KJ, Töpfer R, Zyprian EM (2004) Quantitative trait locus analysis of fungal disease resistance factors on a molecular map of grapevine. Theor Appl Genet 108:501–515
Gary C, Hoffmann C, Mugnai L, Dubois PH, Blum B, Viranyi F, Fermaud M, Wiedemann-Merdinoglu S, Thiery D, Barbier JM (2010) Pesticide use in viticulture, available data on current practices and innovations, bottlenecks and need for research. Deliv DR1 23:1–35
Geiger F, Bengtsson J, Berendse F, Weisser WW, Emmerson M, Morales MB, Ceryngier P, Liira J, Tscharntke T, Winqvist C (2010) Persistent negative effects of pesticides on biodiversity and biological control potential on European farmland. Basic Appl Ecol 11:97–105
Gent DH, James DG, Wright LC, Brooks DJ, Barbour JD, Dreves AJ, Fisher GC, Walton VM (2009) Effects of powdery mildew fungicide programs on twospotted spider mite (Acari: Tetranychidae), hop aphid (Hemiptera: Aphididae), and their natural enemies in hop yards. J Econ Entomol 102:274–286
Gurr GM, Wratten SD, Luna JM (2003) Multi-function agricultural biodiversity: pest management and other benefits. Basic Appl Ecol 4:107–116
Hallmann CA, Sorg M, Jongejans E, Siepel H, Hofland N, Schwan H, Stenmans W, Müller A, Sumser H, Hörren T, Goulson D, De Kroon H (2017) More than 75 percent decline over 27 years in total flying insect biomass in protected areas. PLoS ONE 12(10):e0185809
Hassan SA, Hafes B, Degrande PE, Herai K (1998) The side-effects of pesticides on the egg parasitoid Trichogramma cacoeciae Marchal (Hym., Trichogrammatidae), acute dose-response and persistence tests. J Appl Entomol 122:569–573
Herz H, Hölldobler B, Roces F (2008) Delayed rejection in a leaf-cutting ant after foraging on plants unsuitable for the symbiotic fungus. Behav Ecol 19:575–582
Hoffmann C (2008) Simulation of Lobesia-botrana-egg-laying for autecological and insecticide studies. IOBC/WPRS Bull 36:259–265
Hommay G, Gertz C, Kienlen JC, Pizzol J, Chavigny P (2002) Comparison between the control efficacy of Trichogramma evanescens Westwood (Hymenoptera: Trichogrammatidae) and two Trichogramma cacoeciae Marchal strains against grapevine moth (Lobesia botrana Den. & Schiff.), depending on their release density. Biocontrol Sci Technol 12:569–581
Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biometrical J 50(3):346–363
Huth C, Schirra KJ, Seitz A, Louis F (2009) Investigations of the population ecology and population control of the European earwig Forficula auricularia (Linnaeus)(Dermaptera: Forficulidae) in vineyards of the Palatinate. Mitteilungen der Dtsch Gesellschaft für Allg und Angew Entomol 17:207–210
Intrieri C, Poni G, del Campo MG (2001) Vine performance and leaf physiology of conventionally and minimally pruned Sangiovese grapevines. Vitis J Grapevine Res 40:123–130
Isaia M, Bona F, Badino G (2006) Influence of landscape diversity and agricultural practices on spider assemblage in Italian vineyards of Langa Astigiana (Northwest Italy). Environ Entomol 35:297–307
Kehrli P, Karp J, Burdet JP, Deneulin P, Danthe E, Lorenzini F, Linder C (2012) Impact of processed earwigs and their faeces on the aroma and taste of “Chasselas” and “Pinot Noir”wines. Vitis 51:87–93
Komárek M, Čadková E, Chrastný V, Bordas F, Bollinger J-C (2010) Contamination of vineyard soils with fungicides: a review of environmental and toxicological aspects. Environ Int 36:138–151
Kraus C, Pennington T, Herzog K, Hecht A, Fischer M, Voegele RT, Hoffmann C, Töpfer R, Kicherer A (2018) Effects of canopy architecture and microclimate on grapevine health in two training systems. Vitis 57:53–60
Langellotto GA, Denno RF (2004) Responses of invertebrate natural enemies to complex-structured habitats: a meta-analytical synthesis. Oecologia 139:1–10
Lemtiri A, Colinet G, Alabi T, Cluzeau D, Zirbes L, Haubruge É, Francis F (2014) Impacts of earthworms on soil components and dynamics. A review. Biotechnol Agron Société Environ 18:121–134
Lukianchuk JL, Smith SM (1997) Influence of plant structural complexity on the foraging success of Trichogramma minutum: a comparison of search on artificial and foliage models. Entomol Exp Appl 84:221–228
Mansour F (1987) Effect of pesticides on spiders occurring on apple and citrus in Israel. Phytoparasitica 15:43–50
Marchesini E, Monta LD (1994) Observations on natural enemies of Lobesia botrana (Den. & Schiff.)(Lepidoptera, Tortricidae) in Venetian vineyards. Boll di Zool Agrar e di Bachic 26:201–230
Markheiser A, Rid M, Biancu S, Gross J, Hoffmann C (2018) Physical factors influencing the oviposition behaviour of European grapevine moths Lobesia botrana and Eupoecilia ambiguella. J Appl Entomol 142:201–210
McArt SH, Urbanowicz C, McCoshum S, Irwin RE, Adler LS (2017) Landscape predictors of pathogen prevalence and range contractions in US bumblebees. Proc R Soc B Biol Sci 284:20172181
McMahon TA, Halstead NT, Johnson S, Raffel TR, Romansic JM, Crumrine PW, Rohr JR (2012) Fungicide-induced declines of freshwater biodiversity modify ecosystem functions and services. Ecol Lett 15:714–722
Migula P, Głowacka E (1996) Heavy metals as stressing factors in the red wood ants (Formica polyctena) from industrially polluted forests. Fresenius J Anal Chem 354:653–659
Miles A, Wilson H, Altieri M, Nicholls C (2012) Habitat diversity at the field and landscape level: Conservation biological control research in California viticulture. In: Bostanian NJ, Vincent C, Isaacs R (eds) Arthropod management in vineyards: Pests, approaches, and future directions. Springer, Dordrecht, pp 159–189
Moura AP, Carvalho GA, Botton M (2012) Residual effect of pesticides used in integrated apple production on Chrysoperla externa (Hagen)(Neuroptera: Chrysopidae) larvae. Chil J Agric Res 72:217–223
Olotu MI, Maniania NK, Ekesi S, Seguni ZS, Du Plessis H (2013) Effect of fungicides used for powdery mildew disease management on African weaver ant Oecophylla longinoda (Hymenoptera: Formicidae), a biocontrol agent of sap-sucking pests in cashew crop in Tanzania. Int J Trop Insect Sci 33:283–290
Pennington T, Kraus C, Alakina E, Entling MH, Hoffmann C (2017) Minimal pruning and reduced plant protection promote predatory mites in grapevine. Insects, 8(3):86. http://www.mdpi.com/2075-4450/8/3/86
Pertot I, Caffi T, Rossi V, Mugnai L, Hoffmann C, Grando MS, Gary C, Lafond D, Duso C, Thiery D (2017) A critical review of plant protection tools for reducing pesticide use on grapevine and new perspectives for the implementation of IPM in viticulture. Crop Prot 97:70–84
Pinheiro, Jose, Bates D, DebRoy S, Sarkar D, Team RC (2016) nlme: Linear and nonlinear mixed effects models. http://CRAN.R-project.org/package=nlme
Prischmann DA, James DG, Wright LC, Snyder WE (2006) Effects of generalist phytoseiid mites and grapevine canopy structure on spider mite (Acari: Tetranychidae) biocontrol. Environ Entomol 35:56–67
R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/
Ruyters S, Salaets P, Oorts K, Smolders E (2013) Copper toxicity in soils under established vineyards in Europe: a survey. Sci Total Environ 443:470–477
Thomson LJ, Glenn DC, Hoffmann AA (2000) Effects of sulfur on Trichogramma egg parasitoids in vineyards: measuring toxic effects and establishing release windows. Aust J Exp Agric 40:1165–1171
Töpfer R, Hausmann L, Harst M, Maul E, Zyprian E, Eibach R (2011) New horizons for grapevine breeding. Methods temp fruit breeding fruit, veg cereal sci biotechnol 5:79–100
Varela LG, Smith RJ, Cooper ML, Hoenisch RW (2010) European grapevine moth, Lobesia botrana. Napa Val vineyards-Practical Winer Vineyard, March/April 1–5
Way MJ, Khoo KC (1992) Role of ants in pest management. Annu Rev Entomol 37:479–503
Wightwick A, Walters R, Allinson G, Reichman S, Menzies N (2010) Environmental risks of fungicides used in horticultural production systems. Fungicides. InTech, Shanghai
Wilby A, Thomas MB (2002) Natural enemy diversity and pest control: patterns of pest emergence with agricultural intensification. Ecol Lett 5:353–360
Acknowledgements
We are grateful to Daniel Zendler for his help with programming the raspberry pi, Sandra Biancu and Anna Markheiser for rearing L. botrana for use in our experiments, and Thomas Gramm for managing the experimental vineyard. This study is part of the project “NoViSys” funded by the German Federal Ministry of Education and Research (031A349I).
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Pennington, T., Reiff, J.M., Theiss, K. et al. Reduced fungicide applications improve insect pest control in grapevine. BioControl 63, 687–695 (2018). https://doi.org/10.1007/s10526-018-9896-2
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DOI: https://doi.org/10.1007/s10526-018-9896-2