BACKGROUND: Modern pest control management systems are based on the support of naturally occurring arthropod predators, as it has been shown that such predators offer an important ecosystem service. However, most naturally occurring arthropod predators are generalists (euryphagous). Their role in the biological control of specific pests has been recognized but remains poorly studied. Here, we focused on the naturally occurring arthropod predators of psyllids - the main insect pest of pear trees. We investigated the abundance of psyllids and all of their potential enemies in an abandoned pear orchard on a weekly basis from early spring to early summer. In addition, employing polymerase chain reaction diagnostics and specific primers, we investigated the predation rate on psyllids in all predators collected. RESULTS: We found four predatory groups: spiders were the most abundant (60%, N = 756), followed by coccinellid beetles, anthocorid bugs and cantharid beetles. Anthocorids and spiders had the highest predation rates among the predatory groups. Among spiders, >50% of foliage-dwelling spiders (belonging to the genera Philodromus and Clubiona; N = 206) were positive for psyllids and showed a numerical response to the abundance of psyllids. CONCLUSION: We conclude that foliage-dwelling spiders are, of the four groups, the most important natural enemies of psyllids on pear trees during spring in Central Europe, as they outnumber specialized Anthocoris bugs. © 2021 Society of Chemical Industry.

Department of Botany and Zoology Faculty of Science Masaryk University Brno Czech Republic

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Pasqualini E, Civolani S and Grappadelli LC, Particle film technology: approach for a biorational control of Cacopsylla pyri (Rhychota, Psyllidae) in northern Italy. Bull Insectol 55:39-42 (2002).

Erler F, Natural enemies of the pear psylla Cacopsylla pyri in treated vs untreated pear orchards in Antalya, Turkey. Phytoparasitica 32:295-304 (2004).

Sigsgaard L, Esbjerg P and Philipsen H, Controlling pear psyllids by mass-releasing Anthocoris nemoralis and A. nemorum (Heteroptera: Anthocoridae). J Fruit Ornam Plant Res 14:89-98 (2006).

Jenser G, Szita E and Bálint J, Measuring pear psylla population density (Cacopsylla pyri L. and C. pyricola Förster): review of previous methods and evaluation of a new technique. North-West J Zool 6:54-62 (2010).

Civolani S, The past and and present of pear protection against the pear Psylla, Cacopsylla pyri L, in Insecticides - Pest Engineering, ed. by Perveen F. Intech Open, London, pp. 385-408 (2012).

Carraro L, Loi N, Ermacora N, Gregoris A, Osler R and Hadidi A, Transmission of pear decline by using naturally infected Cacopsylla pyri L. Acta Hortic 472:665-668 (1988).

Berrada S, Nguyen TX, Merzoug D and Fournier D, Selection for monocrotophos resistance in pear psylla, Cacopsylla pyri (L.) (Hom., Psyllidae). J Appl Entomol 119:507-510 (1995).

van der Blom J, Drukker B and Blommers L, The possible significance of various groups of predators in preventing pear Psylla outbreaks. Mededelingen 50:419-424 (1985).

Pekár S, Spiders (Araneae) in the pesticide world: an ecotoxicological review. Pest Manag Sci 68:1438-1446 (2012).

Lele S, Springate-Baginski O, Lakerveld R, Deb D and Dash P, Ecosystem services: origins, contributions, pitfalls, and alternatives. Conserv Soc 11:343-358 (2013).

Bale JS, Lenteren JC and Bigler F, Biological control and sustainable food production. Phil Trans R Soc B 363:761-776 (2008).

Gurr GM and Wratten SD, Biological Control: Measures of Success. Kluwer Academic, Dordrecht (2000).

Shaltiel L and Coll M, Reduction of pear psylla damage by the predatory bug Anthocoris nemoralis (Heteroptera: Anthocoridae): the importance of orchard colonization time and neighbouring vegetation. Biocontrol Sci Technol 14:811-821 (2004).

Chiverton P, Predator density manipulation and its effects on populations of Ropalosiphum padi (Hom., Aphididae) in spring barley. Ann Appl Biol 109:49-60 (1986).

Landis DA and van der Werf W, Early-season predation impacts the establishment of aphids and spread of beet yellows virus in sugar beet. Entomophaga 42:499-516 (1997).

Wiedenmann RN and Smith JW, Atributes of natural enemies in ephemeral crop habitats. Biol Control 10:16-22 (1997).

Firlej A, Doyon J, Harwood JD and Brodeur J, A multi-approach study to delineate interactions between carabid beetles and soybean aphids. Environ Entomol 42:89-96 (2013).

Civolani S and Pasqualini E, Cacopsylla pyri L. (Hom., Psyllidae) and its predators relationship in Italy's Emilia-Romagna region. J Appl Entomol 127:214-220 (2003).

Erler F, Natural enemies of the pear psylla Cacopsylla pyri in treated vs untreated pear orchards in Antalaya, Turkey. Phytoparasitica 32:295-304 (2004).

Sanchez JA and Ortín-Angulo MC, Abundance and population dynamics of Cacopsylla pyri (Hemiptera: Psyllidae) and its potential natural enemies in pear orchards in southern Spain. Crop Prot 32:24-29 (2012).

Hill AR, The biology of Anthocoris nemorum (L.) in Scotland (Hemiptera: Anthocoridae). Ecol Entomol 109:379-395 (1957).

Solomon MG, Cross JV, Fitzgerald JD, Campbell CAM, Jolly RL, Olszak RW et al., Biocontrol of pests of apples and pears in northern and Central Europe - 3. Predators. Biocontrol Sci Technol 10:91-128 (2000).

Beninato S and la Morella S, Control of Cacpsylla pyri with massive releases of Anthocoris nemoralis in pear ocrhards. Giornate Fitopatologiche Perugia 1:367-372 (2000).

D'Arcier FF, Millot P and Belzunces LP, Lâchers inoculatifs D'anthocoris nemoralis F en verger de poiriers. Phytoma 544:76-78 (2001).

Bogya S, Spiders (Araneae) as polyphagous natural enemies in orchards. PhD thesis. University of Wageningen, Netherlands (1999).

Horton D, Pear psylla, Cacopsylla pyricola (Foerster) (Hemiptera: Psyllidae), in Encyclopedia of Entomology, ed. by Capinera JL. Springer, Dordrecht, pp. 2772-2775 (2008).

Jouveau S, Delaunay M, Vignes-Lebbe R and Nattier R, A multi-access identification key based on colour patterns in ladybirds (Coleoptera, Coccinellidae). ZooKeys 758:55-73 (2018).

Nentwig W, Blick T, Bosmans R, Gloor D, Hänggi A and Kroopf C, Spiders of Europe Version 07. 2019. https://araneae.nmbe.ch/ .

Macias-Hernández N, Athey K, Tonzo V, Wangensteen OS, Arnedo M and Harwood JD, Molecular gut content analysis of different spider body parts. PLoS One 13:e0196589 (2018).

Krehenwinkel H, Kennedy S, Pekár S and Gillespie G, A cost-efficient and simple protocol to enrich prey DNA from extractions of predatory arthropods for large-scale gut content analysis by Illumina sequencing. Methods Ecol Evol 8:126-134 (2017).

Ammann L, Gann-Moorhouse R, Cuff J, Bertrand C, Metre L, Peréz Hidalgo N et al., Insights into aphid prey consumption by ladybirds: optimising field sampling methods and primer design for high throughput sequencing. PLoS One 15:e0235054 (2020).

Rubbmark OR, Sint D, Cupic S and Traugott M, When to use NGS or diagnostic PCR in diet analysis. Mol Ecol Resour 19:388-399 (2019).

Agustí N, Unruh TR and Walter SC, Detecting Cacopsylla pyricola (Hemiptera: Psyllidae) in predator guts using COI mitochondrial markers. Bull Entomol Res 93:179-185 (2003).

Petráková L, Michalko R, Loverre P, Sentenská L, Korenko S and Pekár S, Intraguild predation among spiders and their effect on the pear psylla during winter. Agric Ecosyst Environ 233:67-74 (2016).

Wood SN, Generalized Additive Models: An Introduction with R, 1st edn. CRC Press, Boca Raton, FL (2006).

Pekár S and Brabec M, Modern Analysis of Biological Data: Generalized Linear Models in R. Masaryk University Press, Brno (2016).

R Core Team, R: A Language and Environment for Statistical Computing, Reference Index Version 3.3.1. R Foundation for Statistical Computing, Vienna (2019). http://www.R-project.org.

Scutareanu P, Lingeman R, Drukker B and Sabelis MW, Cross-correlation analysis of fluctuations in local populations of pear psyllids and anthocorid bugs. Ecol Entomol 24:354-362 (1999).

Sloggett JJ and Majerus MEN, Habitat preferences and diet in the predatory Coccinellidae (Coleoptera): an evolutionary perspective. Biol J Linn Soc 70:63-88 (2000).

Davidson LN, Diets of Ladybird Beetles (Coleoptera: Coccinellidae) in Utah Alfalfa Fields. PhD thesis, Utah State University (2008).

Hodek I and Evans EW, Food relationships, in Ecology and Behaviour of the Ladybird Beetles (Coccinellidae), ed. by Hodek I, van Emden HF and Honek A. Wiley-Blackwell, Chichester, pp. 275-342 (2012).

Honěk A, Brabec M, Martinková Z, Dixon AFG, Pekár S and Skuhrovec J, Factors determining local and seasonal variation in abundance of Harmonia axyridis (Coleoptera: Coccinellidae) in Central Europe. Eur J Entomol 116:93-103 (2019).

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

Birkhofer K, Entling MH and Lubin Y, Agroecology: trait composition, spatial relationships, trophic interactions, in Spider Research in the 21st Century: Trends and Perspectives, ed. by Penney D. SIRI Scientific Press, Manchester, UK, pp. 220-228 (2013).

Michalko R, Pekár S and Entling MH, An updated perspective on spiders as generalist predators in biological control. Oecologia 189:21-36 (2019).

Markó V and Kereszets B, Flowers for better pest control? Ground cover plants enhance apple orchard spiders (Araneae) but not necessarily their impact on pests. Biocontrol Sci Technol 24:574-596 (2014).

Tscharntke T, Karp DS, Chaplin-Kramer R, Batáry P, DeClerck F, Gratton C et al., When natural habitat fails to enhance biological pest control-five hypotheses. Biol Conserv 204:449-458 (2016).

Oraze MJ and Grigarick AA, Biological control of aster leafhopper (Homoptera; Cicadelidae) and midges (Diptera: Chironomidae) by Pardosa ramulosa (Araneae: Lycosidae) in California rice fields. J Econ Entomol 82:745-749 (1989).

Reichert SE and Bishop L, Prey control by an assemblage of generalist predators in a garden test system. Ecology 71:1441-1450 (1990).

Carter PE and Rypstra AL, Top-down effects in soybean agroecosystems: spider density affects herbivore damage. Oikos 72:433-439 (1995).

Salman INA, Gavish-Regev E, Saltz D and Lubin Y, The agricultural landscape matters: spider diversity and abundance in pomegranate orchards as a case study. BioControl 64:583-593 (2019).

Reichert SE, The hows and whys of successful pest suppression by spiders: insights from case studies. J Arachnol 27:387-396 (1999).

Rypstra AL and Samu F, Size-dependent intraguild predation and cannibalism in coexisting wolf spiders (Araneae Lycosidae). J Arachnol 33:390-397 (2005).

Schmidt JM and Rypstra AL, Opportunistic predator prefers habitat complexity that exposes prey while reducing cannibalism and intraguild encounters. Oecologia 164:899-910 (2010).

Michalko R and Pekár S, The biocontrol potential of Philodromus (Araneae, Philodromidae) spiders for the suppression of pome fruit orchard pests. Biol Control 82:13-20 (2015).

Bogya S, Kaliptókok (Clubionidae), mint a biológiai védekezés perspectivikus eszközei amagyümölcsösben. Növényvédelem 31:149-153 (1995).

Sanchez JA, López-Gallego E and La-Spina M, The impact of ant mutualistic and antagonistic interactions on the population dynamics of sap-sucking hemipterans in pear orchards. Pest Manag Sci 76:1422-1434 (2020).

Sheppard SK, Bell J, Sunderland KD, Fenlon J, Skervin D and Symondson WOC, Detection of secondary predation by PCR analyses of the gut contents of invertebrate generalist predators. Mol Ecol 14:4461-4468 (2005).

Vickerman GP and Sunderland KD, Arthropods in cereal crops: nocturnal activity, vertical distribution, and aphid predation. J Appl Ecol 12:755-766 (1975).

Triltsch H, Food remains in the guts of Coccinella septempunctata (Coleoptera: Coccinellidae) adults and larvae. Eur J Entomol 96:355-364 (1999).

Omkar O and Pervez A, Ladybird beetles, in Ecofriendly Pest Management for Food Security, ed. by Omkar O. Academic Press, Cambridge, MA, pp. 281-310 (2016).

Nyffeler M, Prey selection of spiders in the field. J Arachnol 27:317-324 (1999).

Korenko S and Pekár S, Is there intraguild predation between winter-active spiders (Araneae) on apple tree bark? Biol Control 54:206-212 (2010).

Traugott M, Bell JR, Raso L, Sint D and Symondson WOC, Generalist predators disrupt parasitoid aphid control by direct and coincidental intraguild predation. Bull Entomol Res 102:239-247 (2012).

Greenstone MH, Payton ME, Weber DC and Simmons AM, The detectability half-life in arthropod predator-prey research: what it is, why we need it, how to measure it, and how to use it. Mol Ecol 23:3799-3813 (2014).

Waldner T, Sint D, Juen A and Traugott M, The effect of predator identity on post-feeding prey DNA detection success in soil-dwelling macro-invertebrates. Soil Biol Biochem 63:116-123 (2013).

Chen Y, Giles KL, Payton ME and Greenstone MH, Identifying key cereal aphid predators by molecular gut analysis. Mol Ecol 9:1887-1898 (2000).

Gagnon AE, Doyon J, Heimpel GE and Brodeur J, Prey DNA detection success following digestion by intraguild predators: influence of prey and predators. Mol Ecol Resour 11:1022-1032 (2011).

Wäckers FL, Do oligosaccharides reduce the suitability of honeydew for predators and parasitoids? A further facet to the function of insect-synthesized honeydew sugars. Oikos 90:197-201 (2000).

Leroy PD, Almohamad RA, Attia S, Capella Q, Verheggen FJ, Haubruge E et al., Aphid honeydew: an arrestant and a contact kairomone for Episyrphus balteatus (Diptera: Syrphidae) larvae and adults. Eur J Entomol 111:237-242 (2014).

Ge Y, Liu P, Zhang L, Snyder WE, Smith OM and Shi W, A sticky situation: honeydew of the pear psylla disrupts feeding by its predator Orious sauteri. Pest Manag Sci 76:75-84 (2019).

The significance of woody vegetation's nonproductive elements for the overwintering of key biocontrol agents in intensively used agricultural areas

Mediterranean vineyards and olive groves in Croatia harbour some rare and endemic invertebrates