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Foothold matters: attachment on plant surfaces promotes the vitality of omnivorous mirid bugs Dicyphus errans

Abstract

Omnivorous predatory mirid bugs Dicyphus errans Wolff and closely related species, belonging to the subfamily Bryocorinae (Heteroptera, Miridae), prefer to live on pubescent plant species, where other entomophagous insects are hampered. Previous studies demonstrated a positive relationship between plant trichome diameter and length with attachment forces of D. errans walking on the plant surface. These force data are now pooled with results obtained in life history and feeding assays. Thus, intriguing relationships in mirid bug–plant associations are elucidated. Foothold matters in the highly complex life of omnivorous D. errans. Similar to previously measured traction forces, corresponding safety factors (attachment force/body weight) increase significantly with trichome diameter and length. Fecundity, hatching rate, and juvenile development relate significantly and positively with increased safety factor. Higher safety factors, i.e., stronger attachment on the plant, correspond to a higher consumption rate. The present study confirms a crucial role of insect–plant interactions at the plant surface–insect integument interface. Insect settlement on plants depends on insect attachment ability (i.e., foothold), which is influenced by plant substrates. Hence, the impact of plant surface structures on mirid bug’s, or even wider, on insect attachment ability and interfacial interactions should further be carefully considered when evaluating insect life history, prey consumption, and multitrophic plant–insect associations in the context of evolution, ecology, and sustainable pest management.

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References

  1. Agustí N, Castañé C, Fraile I, Alomar O (2019) Development of a PCR-based method to monitor arthropod dispersal in agroecosystems: Macrolophus pygmaeus (Hemiptera: Miridae) from banker plants to tomato crops. Insect Sci. https://doi.org/10.1111/1744-7917.12717

    Article  PubMed  Google Scholar 

  2. Albajes R, Alomar O, Riudavets J, Castañe C, Arnó J, Gabarra R (1996) The mirid bug Dicyphus tamaninii: an effective predator for vegetable crops. IOBC-WPRS Bull 19:1–4

    Google Scholar 

  3. Alomar O, Wiedenmann RN (eds) (1996) Zoophytophagous Heteroptera: implications for life history and integrated pest management. Thomas Say Publications in Entomology, Entomological Society of America, Landham

    Google Scholar 

  4. Alomar O, Castañe C, Gabarra R, Albajes R (1990) Mirid bugs—another strategy for IPM on mediterrean vegetable crops? IOBC-WPRS Bull 13:6–9

    Google Scholar 

  5. Alomar O, Goula M, Albajes R (1994) Mirid bugs for biological control: identification, survey in non-cultivated winter plants, and colonization of tomato fields. Bull OILB SROP (Italy) 17:217–223

    Google Scholar 

  6. Alomar O, Goula M, Albajes R (2002) Colonisation of tomato fields by predatory mirid bugs (Hemiptera: Heteroptera) in northern Spain. Agric Ecosyst Environ 89:105–115

    Google Scholar 

  7. Althoff DM (2007) Linking ecological and evolutionary change in multitrophic interactions: assessing the evolutionary consequences of herbivore-induced changes in plant traits. In: Ohgushi T, Craig TP, Price PW (eds) Ecological communities: plant mediation in indirect interaction webs. Cambridge University Press, Cambridge, pp 354–376

    Google Scholar 

  8. Arvaniti KA, Fantinou AA, Perdikis DC (2018) Plant and supplementary food sources effect the development of Dicyphus errans (Hemiptera: Miridae). Appl Entomol Zool 53:493–499

    CAS  Google Scholar 

  9. Arzet H-R (1972) Suchverhalten und Nahrungsverbrauch der Larven von Chrysopa carnea Steph. PhD Thesis, Georg-August-Universität, Göttingen

  10. Arzone A (1992) I miridi predatori: biologia e possibili applicazioni in lotta biologico-integrata. Esperienze in Liguria e Piemonte. Atti delle Giornate di Studio, Cagliari, 30–31 gennaio 1992, ERSAT: 43–53

  11. Arzone A, Alma A, Tavella L (1990) Ruolo dei Miridi (Rhynchota, Heteroptera) nella limitazione di Trialeurodes vaporariorum Westw. (Rhynchota, Aleurodidae) Nota preliminare. Boll Zool Agric Bachic Ser II 22:43–51

    Google Scholar 

  12. Aviron S, Poggi S, Varennes YD, Lefevre A (2016) Local landscape heterogeneity affects crop colonization by natural enemies of pests in protected horticultural cropping systems. Agric Ecosyst Environ 227:1–10

    Google Scholar 

  13. Beard JJ, Walter GH (2001) Host plant specificity in several species of generalist mite predators. Ecol Entomol 46:562–570

    Google Scholar 

  14. Begon M, Townsend CR, Harper JL (2006) Ecology: from individuals to ecosystems, 4th edn. Blackwell Publishing Ltd., Hoboken

    Google Scholar 

  15. Benuzzi M, Mosti M (1994) I miridi predatori di aleurodidi. Inf Fitopatol 44:25–30

    Google Scholar 

  16. Betz O (2002) Performance and adaptive value of tarsal morphology in rove beetles of the genus Stenus (Coleoptera, Staphylinidae). J Exp Biol 205:1097–1113

    PubMed  Google Scholar 

  17. Bottrell DG, Barbosa P, Gould F (1998) Manipulating natural enemies by plant variety selection and modification: a realistic strategy? Ann Rev Entomol 43:347–367

    CAS  Google Scholar 

  18. Bouagga S (2018) Enhancing pest management in sweet pepper by the exploitation of zoophytophagy. PhD Thesis, Jaume I University, Castellón de la Plata, Spain

  19. Bouwmeester HJ, Verstappen FWA, Aharoni A, Lücker J, Jongsma MA (2003) Exploring multi-trophic plant-herbivore interactions for new crop protection methods. In: Proceedings of the BCPC International Congress Crop Science & Technology 2003, 10–12 November 2003, Glasgow, Scotland, 2:1123–1134

  20. Bräuer P, Neinhuis C, Voigt D (2017) Attachment of honeybees and greenbottle flies to petal surfaces. Arthropod-Plant Interact 11:171–192

    Google Scholar 

  21. Calvo FJ, Torres A, Gonzalez EJ, Velazque MB (2018) The potential of Dicyphus hesperus as a biological conrol agent of potato psyllid and sweetpotato whitefly in tomato. Bull Entomol Res 108:765–772

    CAS  PubMed  Google Scholar 

  22. Castañe C, Alomar O, Riudavets J (1996a) Management of western flower thrips on cucumber with Dicyphus tamaninii (Heteroptera: Miridae). Biol Control 7:114–120

    Google Scholar 

  23. Castañe C, Arino J, Arno J (1996b) Toxicity of some insecticides and acaricides to the predatory bug Dicyphus tamaninii (Het: Miridae). Entomophaga 41:211–216

    Google Scholar 

  24. Castañe C, Alomar O, Goula M, Gabarra R (2000a) Natural populations of Macrolophus caliginosus and Dicyphus tamaninii in the control of the greenhouse white fly in tomato crops. IOBC-WPRS Bull 23:221–224

    Google Scholar 

  25. Castañe C, Alomar O, Riudavets J (2000b) Dicyphus tamaninii in the biological control of cucumber pests. IOBC-WPRS Bull 23:253–256

    Google Scholar 

  26. Castañe C, Iriarte J, Lucas E (2002) Comparision of prey consumption by Dicyphus tamaninii reared conventionally, and on a meat-based diet. Biocontrol 47:657–666

    Google Scholar 

  27. Castañe C, Alomar O, Goula M, Gabarra R (2004) Colonization of tomato greenhouses by the predatory mirid bugs Macrolophus caliginosus and Dicyphus tamaninii. Biol Control 30:591–597

    Google Scholar 

  28. Castañe C, Arno J, Gabarra R, Alomar O (2011) Plant damage to vegetable crops by zoophytophagous mirid predators. Biol Control 59:22–29

    Google Scholar 

  29. Castañe C, Agusti N, Arno J, Gabarra R, Riudavets J, Comas J, Alomar O (2013) Taxonomic identification of Macrolophus pygmaeus and Macrolophus melanotoma based on morphometry and molecular markers. Bull Entomol Res 103:204–215

    PubMed  Google Scholar 

  30. Castineras A (1995) Natural enemies of Bemisia tabaci (Homoptera: Aleurodidae) in Cuba. Fla Entomol 78:538–540

    Google Scholar 

  31. Ceglarska E (1999) Dicyphus hyalinipennis Burm. (Heteroptera: Miridae) - a potential biological control agent for glasshouse pests. Workshop of IOBC/WPRS Working Group IPM in Greenhouses – Northern section, 25-28 May 1999, Brest France. IOBC-WPRS Bull 22:33–36

  32. Choi B-R, Lee S-W, Yoo J-K (2001) Resistance mechanisms of green peach aphid Myzus persicae (Homoptera, Aphidae) to imidachloprid. Korean J Appl Entomol 40:265–271

    Google Scholar 

  33. Chortyk OT, Kays SJ, Teng Q (1997) Characterization of insecticidal sugar esters of Petunia. J Agric Food Chem 45:270–275

    CAS  Google Scholar 

  34. Cohen AC (1998) Biochemical and morphological dynamics and predatory feeding habits in terrestial Heteroptera. In: Coll M, Ruberson JR (eds) Predatory Heteroptera: their ecology and use in biological control. Thomas Say Publications, New York, pp 21–33

    Google Scholar 

  35. Coll M (1998) Living and feeding on plants in predatory Heteroptera. In: Coll M, Ruberson JR (eds) Predatory Heteroptera: their ecology and use in biological control. Thomas Say Publications, New York, pp 89–130

    Google Scholar 

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

    Google Scholar 

  37. Costanzi M, Pini S (1991) Ruolo di due miridi predatori nella difesa delle colture ortofloricole. Colture Protette 11:49–53

    Google Scholar 

  38. Dicke M, van Loon JJA (2000) Multitrophic effects of herbivore-induced plant volatiles in an evolutionary context. Entomol Exp Appl 97:237–249

    CAS  Google Scholar 

  39. Dixon AFG (1986) Habitat specifity and foraging behaviour of aphidophagous insects. In: Hodek I (ed) Ecology of Aphidophaga, vol 35. Proceedings of the 2nd Symosium held at Zvíkovské Podhradí, September 2–8, 1984, Series Entomologica, pp 151–154

  40. Dos Santos TM, Júnior ALB, Soares JJ (2003) Influência de tricomas do algodoeiro sobre os aspectos biológicos e capacidade predatória de Chrysoperla externa (Hagen) alimentada com Aphis gossypii Glover. Bragantia 62:243–254

    Google Scholar 

  41. Drees BM (2002) Aphid management. Texas Agricultural Extension Service, The Texas A&M University System. http://hortipm.tamu.edu/publications/Aphid.html

  42. Durán Prieto J, Trotta V, Fanti P, Castañe C, Battaglia D (2016) Predation by Macrolophus pygmaeus (Hemiptera: Miridae) on Acyrthosiphon pisum (Hemiptera: Aphididae): Influence of prey age/size and predator’s intraspecific interactions. Eur J Entomol 113:37–43

    Google Scholar 

  43. Eigenbrode SD (2004) The effects of plant epicuticular waxy blooms on attachment and effectiveness of predatory insects. Arthr Struct Dev 33:91–102

    CAS  Google Scholar 

  44. Eigenbrode SD, Jetter R (2002) Attachment to plant surface waxes by an insect predator. Integr Comp Biol 42:1091–1099

    CAS  PubMed  Google Scholar 

  45. Eigenbrode SD, Kabalo NN (1999) Effects of Brassica oleracea waxblooms on predation and attachment by Hippodamia convergens. Entomol Exp Appl 91:125–130

    Google Scholar 

  46. Eigenbrode SD, Kabalo NN, Stoner KA (1999) Predation, behavior, and attachment by Chrysoperla plorabunda larvae on Brassica oleracea with different surface waxblooms. Entomol Exp Appl 90:225–235

    Google Scholar 

  47. Eigenbrode SD, Snyder WE, Clevenger G, Ding H, Gorb SN (2009) Variable attachment to plant surface waxes by predatory insects. In: Gorb SN (ed) Functional surfaces in biology, vol 2. Springer, The Netherlands, pp 157–181

    Google Scholar 

  48. Escobar-Bravo R, Klinkhamer PGL, Leiss KA (2017) Induction of Jasmonic acid-associated defenses by thrips alters host suitability for conspecifics and correlates with increased trichome densities in tomato. Plant Cell Physiol 58:622–634

    CAS  PubMed  PubMed Central  Google Scholar 

  49. Eubanks MD, Denno RF (2000) Health food versus fast food: the effects of prey quality and mobility on prey selection by a generalist predator and interactions among prey species. Ecol Entomol 25:140–146

    Google Scholar 

  50. Eubanks MD, Styrsky JD, Denno RE (2003) The evolution of omnivory in heteropteran insects. Ecology 84:2549–2556

    Google Scholar 

  51. Evans HF (1976) Mutual interference between predatory anthocorids. Ecol Entomol 1:283–286

    Google Scholar 

  52. Ferracini C, Bueno VHP, Dindo ML, Ingegno BL, Luna MG, Salas Gervassio NG, Sánchez NE, Siscaro G, van Lenteren JC, Zappalà L, Tavella L (2019) Natural enemies of in the Mediterranean basin, Europe and South America. Biocontrol Sci Technol 29:578–609

    Google Scholar 

  53. Gabarra R, Castañe C, Bordas E, Albajes R (1988) Dicyphus tamaninii as a beneficial insect and pest in tomato crops in Catalonia, Spain. Entomophaga 33:219–228

    Google Scholar 

  54. Gabarra R, Castañe C, Albajes R (1995) The mirid bug Dicyphus tamaninii as a greenhouse whitefly and western flower thrips predator on cucumber. Biocontrol Sci Technol 5:475–488

    Google Scholar 

  55. Gabarra R, Alomar O, Castañe C, Goula M, Albajes R (2004) Movement of greenhouse whitefly and its predators between in- and outside of Mediterranean greenhouses. Agric Ecosyst Environ 102:341–348

    Google Scholar 

  56. Geiler H (1963) Artenlisten der Wanzen und Zikaden von Feldern sowie deren Abundanz und Aktivitätsdichte während einzelner Jahre mit unterschiedlichem Witterungsverlauf. Wiss Ztschr Techn Univ Dresden 12:543–549

    Google Scholar 

  57. Gervassio NGS, Perez-Hedo M, Luna MG, Urbaneja A (2017) Intraguild predation and competitive displacement between Nesidiocoris tenuis and Dicyphus maroccanus, two biological control agents in tomato pests. Insect Sci 24:809–817

    Google Scholar 

  58. Gesse-Solé F (1992) Comportamiento alimenticio de Dicyphus tamaninii Wagner (Heteroptera: Miridae). Bol San Veg Plagas 18:685–691

    Google Scholar 

  59. Giles KL, Madden RD, Stockland R, Payton ME, Dillwith JW (2002) Host plants effect predator fitness via nutritional value of herbivore prey: Investigation of a plant-aphid-ladybeetle system. Biocontrol 47:1–21

    Google Scholar 

  60. Gillespie DR, Sanchez A, McGregor RR, Quiring D (2001) Dicyphus hesperus—life history, biology and application in tomato greenhouses. Technol Rep 166:1–15

    Google Scholar 

  61. Glen DM (1973) The food requirements of Blepharidopterus angulatus (Heteroptera: Miridae) as a predator of the lime aphid, Eucallipterus tiliae. Entomol Exp Appl 16:255–267

    Google Scholar 

  62. Gorb EV, Gorb SN (2002) Attachment ability of the beetle Chrysolina fastuosa on various plant surfaces. Entomol Exp Appl 105:13–28

    Google Scholar 

  63. Gorb E, Kastner V, Peressadko A, Arzt E, Gaume L, Rowe N, Gorb S (2004) Structure and properties of the glandular surface in the digestive zone of the pitcher in the carnivorous plant Nepenthes ventrata and its role in insect trapping and retention. J Exp Biol 207:2947–2963

    PubMed  Google Scholar 

  64. Gorb E, Voigt D, Eigenbrode SD, Gorb S (2008) Attachment force of the beetle Cryptolaemus montrouzieri (Coleoptera, Coccinellidae) on leaflet surfaces of mutants of the pea Pisum sativum (Fabaceae) with regular and reduced wax coverage. Arthropod-Plant Interact 2:247–259

    Google Scholar 

  65. Goula M, Alomar O (1994) Míridos (Heteroptera Miridae) de interés en el control integrado de plagas en el tomate. Guía para su identificación. Bol San Veg Plagas 20:131–143

    Google Scholar 

  66. Goula Goula M, Tavella L (2000) Dicyphini collected on vegetable and wild plants in north-western Italy (Heteroptera, Miridae). IOBC-WPRS Bull 23:257

    Google Scholar 

  67. Guo F, Zhang Z-Q, Zhaoe Z (1998) Pesticide resistance of Tetranychus cinnabarinus (Acari: Tetranychidae) in China: a review. Syst Appl Acar 3:3–7

    Google Scholar 

  68. Gutschick VP (1999) Biotic and abiotic consequences of differences in leaf structure. New Phytol 143:3–18

    Google Scholar 

  69. Han P, Dong YC, Lavoir AV, Adamowicz S, Bearez P, Wajnberg E, Desneux N (2015a) Effect of plant nitrogen and water status on the foraging behavior and fitness of an omnivorous arthropod. Ecol Evol 5:5468–5477

    PubMed  PubMed Central  Google Scholar 

  70. Han P, Bearez P, Adamowicz S, Lavoir AV, Amiens-Desneux E, Desneux N (2015b) Nitrogen and water limitations in tomato plants trigger negative bottom-up effects on the omnivorous predator Macrolophus pygmaeus. J Pest Sci 88:685–691

    Google Scholar 

  71. Hegnauer R (1992) Chemotaxonomie der Pflanzen, eine Übersicht über die Verbreitung und die systematische Bedeutung der Pflanzenstoffe. Birkhäuser Verlag, Basel

    Google Scholar 

  72. Holling CS (1966) The functional response of invertebrate predators to prey density. Mem Entomol Soc Can 98:5–86

    Google Scholar 

  73. Ingegno BL, Goula M, Navone P, Tavella L (2008) Distribution and host plants of the genus Dicyphus in the Alpine valleys of NW Italy. Bull Insectol 61:139–140

    Google Scholar 

  74. Ingegno BL, Pansa MG, Tavella L (2011) Plant preference in the zoophytophagous generalist predator Macrolophus pygmaeus (Heteroptera: Miridae). Biol Control 58:174–181

    Google Scholar 

  75. Ingegno BL, Ferracini C, Gallinotti D, Alma A, Tavella L (2013) Evaluation of the effectiveness of Dicyphus errans (Wolff) as predator of Tuta absoluta (Meyrick). Biol Control 67:246–252

    Google Scholar 

  76. Ingegno BL, La-Spina M, Jordan MJ, Tavella L, Sanchez JA (2016) Host plant perception and selection in the sibling species Macrolophus melanotoma and Macrolophus pygmaeus (Hemiptera: Miridae). J Insect Behav 29:117–142

    Google Scholar 

  77. Ingegno BL, Bodino N, Leman A, Messelink GJ, Tavella J (2017a) Predatory efficacy of Dicyphus errans on different prey. Acta Hortic 1164:425–430

    Google Scholar 

  78. Ingegno BL, Candian V, Psomadelis I, Bodino N, Tavella L (2017b) The potential of host plants for biological control of Tuta aboluta by the predator Dicyphus errans. Bull Entomol Res 107:340–348

    CAS  PubMed  Google Scholar 

  79. Ingegno BL, Candian V, Tavella L (2017c) Behavioural study on host plants shared by the predator Dicyphus errans and the prey Tuta absoluta. Acta Hortic 1164:377–382

    Google Scholar 

  80. Ingegno BL, Messelink GJ, Bodino N, Iliadou A, Driss L, Woelke JB, Leman A, Tavella L (2019) Functional response of the mirid predators Dicyphus bolivari and Dicyphus errans and their efficacy as biological control agents of Tuta absoluta on tomato. J Pest Sci 92:1457–1466

    Google Scholar 

  81. Jeffree CF (1986) The cuticle, epicuticular waxes and trichomes of plants, with reference to their structure, functions and evolution. In: Juniper B, Southwood R (eds) Insects and the plant surface. Edward Arnold Publishers, London, pp 23–64

    Google Scholar 

  82. Jervis M, Kidd N (1996) Insect natural enemies. Practical approaches to their study and evaluation. Chapman & Hall, London

    Google Scholar 

  83. Johnson HB (1975) Plant pubescence: an ecological perspective. Bot Rev 41:233–258

    Google Scholar 

  84. Juniper BE (1995) Waxes on plant surfaces and their interactions with insects. In: Hamilton RJ (ed) Waxes: chemistry, molecular biology and functions. Oily, West Ferry, pp 157–174

    Google Scholar 

  85. Kim JG, Lee WH, Yu YM, Yasunaga-Aoki C, Jung SH (2016) Lifecycle, biology, and descriptions of greenhouse biological control agent, Nesidiocoris tenuis (Reuter, 1895) (Hemiptera: Miridae). J Fac Agric Kyushu Univ 61:313–318

    Google Scholar 

  86. Kolbe W, Bruns A (1988) Insekten und Spinnen in Land- und Gartenbau. Pflanzenbau/Pflanzenschutz, Heft 25, Rhein. Landwirtschaftverlag, Bonn

  87. Labbé RM, Gagnier D, Kostic A, Shipp L (2018) The function of supplemental foods for improved crop establishment of generalist predators Orius insidiosus and Dicyphus hesperus. Sci Rep 8:1779

    Google Scholar 

  88. Lauenstein G (1976) Untersuchungen zu Biologie und Verhaltensweisen der Räuberischen Blumenwanze Anthocoris nemorum L. (Het.: Anthocoridae). PhD Thesis, Georg-August-Universität Göttingen, Germany

  89. Lauenstein G (1980) Zum Suchverhalten von Anthocoris nemorum L. (Het. Anthocoridae). Ztschr Angew Entomol 89:428–442

    Google Scholar 

  90. Levin DA (1973) The role of trichomes in plant defense. Quart Rev Biol 48:3–15

    Google Scholar 

  91. Lima-Espindola J, Rodriguez-Leyva E, Lomeli-Flores JR, Velazquez-Gonzalez JC (2018) Does foraging experience affect the response of the predator Dicyphus hesperus Knight to prey-induced volatiles? Neotrop Entomol 47:885–891

    CAS  PubMed  Google Scholar 

  92. Lucas É, Alomar Ò (2001) Macrolophus caliginosus (Wagner) as an intraguild prey for the zoophytophagous Dicyphus tamaninii Wagner (Heteroptera: Miridae). Biol Control 20:147–152

    Google Scholar 

  93. Madeira F, Sossai S, Edo E, Pagès P, Levi N, Albajes R (2019) Attractiveness of uninfested vegetables to the omnivorous predators Dicyphus bolivari and D. errans (Hemiptera: Miridae) and their relative suitability for oviposition. Biol Control 136:104007

    Google Scholar 

  94. Malausa JC (1989) Lutte intégrée sous serre: les punaises prédatrices Mirides dans les cultures de Solanacées du sud-est de la France. PHM Revue Horticole 298:39–43

    Google Scholar 

  95. Maselou DA, Perdikis DC, Sabelis MW, Fantinou AA (2014) Use of plant resources by an omnivorous predator and the consequences for effective predation. Biol Control 79:92–100

    Google Scholar 

  96. Messelink GJ, Bloemhard CMJ, Hoogerbrugge H, van Schelt J, Ingegno BL, Tavella L (2015) Evaluation of mirid predatory bugs and release strategy for aphid control in sweet pepper. J Appl Entomol 139:333–341

    Google Scholar 

  97. Miller NCE (1971) The biology of the Heteroptera, 2nd edn. E. W. Classey Ltd., Hampton

    Google Scholar 

  98. Moerkens R, Berckmoes E, Van Damme V, Ortega-Parra N, Hanssen I, Wuytack M, Wittemans L, Casteels H, Tirry L, De Clercq P, De Vis R (2016) High population densities of Macrolophus pygmaeus on tomato plants can cause economic fruit damage: interaction with Pepino mosaic virus? Pest Manag Sci 72:1350–1358

    CAS  PubMed  Google Scholar 

  99. Obrycki JJ (1986) The influence of foliar pubescence on entomophagous species. In: Boerthel DJ, Eikenbarry RD (eds) Interactions of plant resistance and parasitoids and predators of insects. Wiley, New York

    Google Scholar 

  100. Obrycki JJ, Tauber MJ (1984) Natural enemy activity on glandular pubescent potato plants in the greenhouse: an unreliable predictor of effects in the field. Environ Entomol 13:679–683

    Google Scholar 

  101. Pasquier-Barre F, Geri C, Goussard F, Auger-Rozenerg MA, Greiner S (2000) Oviposition preference and larval survival of Diprion pini on Scots pine clones in relation to folliage characteristics. Agric For Entomol 2:185–193

    Google Scholar 

  102. Pazyuk IM, Dolgovskaya MY, Reznik SY, Musolin DL (2018) Photoperiodic control of pre-adult development and adult diapause induction in zoophytophagous bug Dicyphus errans (Wolff) (Heteroptera, Miridae). Entomol Rev 98:956–962

    Google Scholar 

  103. Perdikis D, Arvaniti K (2016) Nymphal development on plant vs. leaf with and without prey for two omnivorous predators: Nesidiocoris tenuis (Reuter, 1895) (Hemiptera: Miridae) and Dicyphus errans (Wolff, 1804) (Hemiptera: Miridae). Entomol Gen 35:297–306

    Google Scholar 

  104. Perdikis DC, Lykouressis DP (1997) Rate of development and mortality of nymphal stages of the predator Macrolophus pygmaeus Rambur feeding on various prey and host plants. Bull SROP 20:241–248

    Google Scholar 

  105. Perdikis DC, Lykouressis DP (2000) Effects of various items, host plants, and temperatures on the development and survival of Macrolophus pygmaeus Rambur (Hemiptera: Miridae). Biol Control 17:55–60

    Google Scholar 

  106. Perdikis DC, Lykouressis DP (2001) Nymphal development and survival of Macrolophus pygmaeus Rambur (Heteroptera, Miridae) on two eggplant varieties as affected by temperature and presence/absence of prey. Biol Control 20:222–227

    Google Scholar 

  107. Perez-Hedo M, Urbaneja A (2015) Prospects for predatory mirid bugs as biocontrol agents of aphids in sweet peppers. J Pest Sci 88:65–73

    Google Scholar 

  108. Perez-Hedo M, Rambla JL, Granell A, Urbaneja A (2018) Biological activity and specificity of Miridae-induced plant volatiles. Biocontrol 63:203–213

    CAS  Google Scholar 

  109. Petacchi P, Rossi E (1991) Prime osservazioni su Dicyphus (Dicyphus) errans (Wolff) (Heteroptera Miridae) diffuso sul pomodoro in serre della Liguria. Boll Zool Agr Bachic Ser II 23:77–86

    Google Scholar 

  110. Peterson JA, Ode PJ, Oliveira-Hofman C, Harwood JD (2016) Integration of plant defense traits with biological control of arthropod pests: challenges and opportunities. Front Plant Sci 7:1794

    PubMed  PubMed Central  Google Scholar 

  111. Press MC (1999) The functional significance of leaf structure: a search for generalizations. New Phytol 143:213–219

    Google Scholar 

  112. Price PW (1991) The plant vigor hypothesis and herbivore attack. Oikos 62:244–251

    Google Scholar 

  113. Price PW, Bouton CE, Gross P, McPheron BA, Thompson JN, Weis AE (1980) Interactions among three trophic levels: influence of plants on interactions between insect herbivores and natural enemies. Ann Rev Ecol Syst 11:41–65

    Google Scholar 

  114. Price PW, Denno RF, Eubanks MD, Finke DL, Kaplan I (2011) Insect ecology: behaviour, populations and communities. Cambridge University Press, Cambridge

    Google Scholar 

  115. Prüm B, Seidel R, Bohn HF, Speck T (2012) Plant surfaces with cuticular folds are slippery for beetles. J R Soc Interface 9:127–135

    PubMed  Google Scholar 

  116. Prüm B, Bohn HF, Seidel R, Rubach S, Speck T (2013) Plant surfaces with cuticular folds and their replicas: Influence of microstructuring and surface chemistry on the attachment of a leaf beetle. Acta Biomater 9:6360–6368

    PubMed  Google Scholar 

  117. Quilici S, Iperti G (1986) The influence of host plant on the searching ability of first instar larvae of Propylea quadrodecimpunctata. Ser Entomol 35:99–111

    Google Scholar 

  118. Ramirez-Ahuja MD, Rodriguez-Leyva E, Lomeli-Flores JR, Torres-Ruiz A, Guzman-Franco AW (2017) Evaluating combined use of a parasitoid and a zoophytophagous bug for biological control of the potato psyllid, Bactericera cockerelli. Biol Control 106:9–15

    Google Scholar 

  119. Raworth, DA (2001) Control of two-spotted spider mite by Phytoseiulus persimilis. J Asia-Pacific Entomol 4:157–163

    Google Scholar 

  120. Reinhold M (1975) Eignung verschiedener Blattlausarten für ihre Feinde. Diploma Thesis, Institut für Pflanzenpathologie und Pflanzenschutz, Georg-August-Universität Göttingen, Germany

  121. Ronco C, Faure E (1993) Monitoraggio di miridi spontanei su pomodoro in tunnel. L´Informatore Agrario 45:61–62

    Google Scholar 

  122. Saleh A, Sengonca C (2000) Untersuchungen über die Raubwanze Dicyphus tamaninii Wagner (Heteroptera: Miridae) als natürlicher Feind von Aphis gossypii Glover (Homoptera: Aphididae). Mitt Biol Bundesanst Land Forstwirtsch 376:577–578

    Google Scholar 

  123. Salerno G, Rebora M, Gorb E, Gorb S (2018) Attachment ability of the polyphagous bug Nezara viridula (Heteroptera: Pentatomidae) to different host plant surfaces. Sci Rep 8:10975

    PubMed  PubMed Central  Google Scholar 

  124. Sanchez JA, Gillespie DR, McGregor RR (2004) Plant preference in relation to life history traits in the zoophytophagous predator Dicyphus hesperus. Entomol Exp Appl 112:7–19

    Google Scholar 

  125. Saulich AK, Musolin DL (2019) Seasonal development of plant bugs (Heteroptera, Miridae): subfamily Bryocorinae. Entomol Rev 99:275–291

    Google Scholar 

  126. Schewket Bey N (1930) Zur Biologie der phytophagen Wanze Dicyphus errans Wolff (Capsidae). Z Insbiol XXV:179–183

    Google Scholar 

  127. Schuh RT (1976) Pretarsal structure in the Miridae (Hemiptera) with a cladistic analysis of relationships within the family. Am Mus Novit 2601:1–39

    Google Scholar 

  128. Seidenstücker G (1967) Eine Phyline mit Dicyphus-Kralle (Heteroptera, Miridae). Reichenbachia 8:215–220

    Google Scholar 

  129. Sengonca C, Kranz J, Blaeser P (2002) Attractiveness of three weed species to polyphagous predators and their influence on aphid populations in adjacent lettuce cultivations. J Pest Sci 75:161–165

    Google Scholar 

  130. Shanower TG, Romeis J, Peter AJ (1996) Pigeonpea plant trichomes: Multiple trophic level interactions. In: Ananthakrishnan TN (ed) Biotechnological perspectives in chemical ecology of insects. Oxford & IBH, New Delhi, pp 76–88

    Google Scholar 

  131. Slobodynayuk GA, Ignatjewa TN, Pilipjuk WI (1995) Biologicheskaja zaschita owoschnyich kultur w zakryitom gruntje kurortnoi zoni g. Sotschi (Biological protection of vegetable crops in greenhouses in health-resort zone in City of Sotschi). Zascita Rastenij 6:12–13

    Google Scholar 

  132. Southwood TRE (1972) The insect/plant relationship—an evolutionary perspective. In: van Emden HF (ed) Insect/plants relationships, vol 6. Blackwell Scientific Publications, Symposia of the Royal Entomological Society of London, London, pp 3–23

    Google Scholar 

  133. Southwood R (1986) Plant surfaces and insects-an overview. In: Juniper B, Southwood R (eds) Insects and the plant surface. Edward Arnold Publishers, London, pp 1–22

    Google Scholar 

  134. Stork NE (1980) Role of wax blooms in preventing attachment to brassicas by the mustard beetle, Phaedon cochleariae. Entomol Exp Appl 28:100–107

    Google Scholar 

  135. Ter Horst S (2000) Einfluss verschiedener Temperaturen, Wirtspflanzen und Beutetiere auf die Entwicklung von Macrolophus pygmaeus Rambur (Heteroptera: Miridae). Diploma Thesis, Fachbereich Gartenbau, Institut für Pflanzenschutz und Pflanzenkrankheiten, Universität Hannover, Germany

  136. Utsumi S (2013) Evolutionary community ecology of plant-associated arthropods in terrestrial ecosystems. Ecol Res 28:359–371

    Google Scholar 

  137. Valverde PL, Fornoni J, Núnez-Farfán J (2001) Defensive role of leaf trichomes in resistance to herbivorous insects in Datura stramonium. J Evol Biol 14:424–432

    Google Scholar 

  138. Vankosky MA, VanLaerhoven SL (2015) Plant and prey quality interact to influence the foraging behaviour of an omnivorous insect, Dicyphus hesperus. Anim Behav 108:109–116

    Google Scholar 

  139. Verheggen FJ, Capella Q, Schwartzberg EG, Voigt D, Haubruge E (2009) Tomato-aphid-hoverfly: A tritrophic interaction incompatible for pest management. Arthropod-Plant Interact 3:141–149

    Google Scholar 

  140. Viggiani G (1971) Osservazioni biologiche sul miride predatore De-raecoris ruber (L.) (Rhynchota, Heteroptera). Boll Lab Ent Agr “Filippo Silvestri” Portici Napoli XXIX:270–285

  141. Voigt D (2002) Untersuchungen zur Biologie der räuberischen Weichwanze Dicyphus errans Wolff, insbesondere zum Beutetierspektrum und zur Wirtspflanzenpräferenz im Botanischen Garten der TU Dresden. Diploma Thesis, Institut für Waldbau und Forstschutz, Technische Universität Dresden, Germany

  142. Voigt D (2004) Eine Bereicherung für den Bio-Anbau? Die räuberische Weichwanze Dicyphus errans Wolff. Das Taspo Magazin 2/2004:18–20

  143. Voigt D (2005) Untersuchungen zur Morphologie, Biologie und Ökologie der räuberischen Weichwanze Dicyphus errans Wolff (Heteroptera, Miridae, Bryocorinae). PhD Thesis, Technische Universität Dresden, Germany

  144. Voigt D, Gorb S (2010) Locomotion in a sticky terrain. Arthropod-Plant Interact 4:69–79

    Google Scholar 

  145. Voigt D, Pohris V, Wyss U (2006) Zur Nahrungsaufnahme von Dicyphus errans Wolff (Heteroptera, Miridae, Bryocorinae): Nahrungsspektrum, Potenzial und Verhalten. Mitt Dtsch Ges Allg Angew Entomol 15:305–308

    Google Scholar 

  146. Voigt D, Gorb E, Gorb S (2007) Plant surface–bug interactions: Dicyphus errans stalking along trichomes. Arthropod-Plant Interact 1:221–243

    Google Scholar 

  147. Voigt D, Perez Goodwyn PJ, Fujisaki K (2018) Attachment ability of the southern green stink bug, Nezara viridula (L.), on plant surfaces. Arthropod-Plant Interact 12:415–421

    Google Scholar 

  148. Wagner E (1955) Bemerkungen zum System der Miridae (Hemiptera, Heteroptera). Dtsch Entomol Z 2:230–242

    Google Scholar 

  149. Walters PJ (1974) A method for culturing Stethorus spp. (Coleoptera: Coccinellidae) on Tetranychus urticae (Koch) (Acarina: Tetranychidae). J Aust Entomol Soc 13:245–246

    Google Scholar 

  150. Wheeler AG (2001) Biology of the plant bugs (Hemiptera: Miridae): pests, predators, opportunists. Cornell University Press, London

    Google Scholar 

  151. White C, Eigenbrode SD (2000) Leaf surface waxbloom in Pisum sativum influences predation and intra-guild interactions involving two predator species. Oecologia 124:252–259

    CAS  PubMed  Google Scholar 

  152. Yasuda T (1998) Role of chlorophyll content of prey diets in prey-locating behaviour of a generalist predatory stink bug, Eocanthecona furcellata. Entomol Exp Appl 86:119–124

    Google Scholar 

  153. Zhao YX, Kang L (2003) Olfactory responses of the leafminer Liriomyza sativae (Dipt., Agromyzidae) to the odours of host and non-host plants. J Appl Entomol 127:80–84

    Google Scholar 

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Acknowledgements

Thanks to C. Neinhuis and the staff of the Botanical Garden as well as V. Pohris, M. Müller, and the staff of the Chair for Forest Protection at the Institute of Silviculture and Forest Protection, Faculty of Forestry, Geo and Hydro Sciences, Department of Forestry, Technische Universität Dresden (Dresden, Germany) for providing space for the rearing of test plants and insects and for discussions. I. and M. Voigt (Zwickau/Sa., Germany) generously delivered material, intellectual, and active support. The bug species was determined by K. Arnold (Geyer, Germany). U. Wyss (Entofilm, Kiel, Germany) facilitated scientific video recordings. The German companies Ernst Benary Samenzucht GmbH (Muenden), Quedlinburger Saatgut GmbH (Quedlinburg), Bruno Nebelung GmbH & Co. (Everswinkel), JULIWA-HESA GmbH (Heidelberg), Cyclamen-Sprünken (Straelen), Florensis Deutschland GmbH (Weeze), Klemm + Sohn GmbH & Co. KG (Stuttgart), EICH Jungpflanzen Vertriebs GmbH (Grolsheim), Kartoffellager Großwaltersorf (Großwaltersdorf), Friweika eG (Weidensdorf) provided free seeds and young plants; Floragard Vertriebs GmbH für Gartenbau (Oldenburg), Klasmann-Deilmann GmbH (Geeste-Groß Hesepe), and Compo GmbH (Münster) provided free substrates and fertilizers. The populations of Aphis gossypii and Myzus persicae were obtained from Bayer Cropscience AG (P. Meisner & G. Trautmann, BCS-R-I-BISE-E, Entomology, Monheim, Germany). The German National Academic Foundation (doctoral scholarship, E2002D0730) partially funded the project. Valuable suggestions by two anonymous reviewers are appreciated.

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Voigt, D. Foothold matters: attachment on plant surfaces promotes the vitality of omnivorous mirid bugs Dicyphus errans. Arthropod-Plant Interactions 13, 819–834 (2019). https://doi.org/10.1007/s11829-019-09716-w

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Keywords

  • Bryocorinae
  • Insect attachment
  • Miridae
  • Pest management
  • Plant surface
  • Trichomes