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

  • Dagmar VoigtEmail author
Original Paper


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.


Bryocorinae Insect attachment Miridae Pest management Plant surface Trichomes 



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.

Supplementary material

11829_2019_9716_MOESM1_ESM.pdf (894 kb)
Supplementary material 1 (PDF 894 kb)


  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. CrossRefPubMedGoogle 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 19:1–4Google 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, LandhamGoogle Scholar
  4. Alomar O, Castañe C, Gabarra R, Albajes R (1990) Mirid bugs—another strategy for IPM on mediterrean vegetable crops? IOBC-WPRS Bull 13:6–9Google 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) 17:217–223Google 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 89:105–115CrossRefGoogle 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 354–376CrossRefGoogle 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 53:493–499CrossRefGoogle Scholar
  9. Arzet H-R (1972) Suchverhalten und Nahrungsverbrauch der Larven von Chrysopa carnea Steph. PhD Thesis, Georg-August-Universität, GöttingenGoogle Scholar
  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: 43–53Google Scholar
  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 22:43–51Google 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 227:1–10CrossRefGoogle Scholar
  13. Beard JJ, Walter GH (2001) Host plant specificity in several species of generalist mite predators. Ecol Entomol 46:562–570CrossRefGoogle Scholar
  14. Begon M, Townsend CR, Harper JL (2006) Ecology: from individuals to ecosystems, 4th edn. Blackwell Publishing Ltd., HobokenGoogle Scholar
  15. Benuzzi M, Mosti M (1994) I miridi predatori di aleurodidi. Inf Fitopatol 44:25–30Google Scholar
  16. Betz O (2002) Performance and adaptive value of tarsal morphology in rove beetles of the genus Stenus (Coleoptera, Staphylinidae). J Exp Biol 205:1097–1113PubMedGoogle Scholar
  17. Bottrell DG, Barbosa P, Gould F (1998) Manipulating natural enemies by plant variety selection and modification: a realistic strategy? Ann Rev Entomol 43:347–367CrossRefGoogle 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, SpainGoogle Scholar
  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, 2:1123–1134Google Scholar
  20. Bräuer P, Neinhuis C, Voigt D (2017) Attachment of honeybees and greenbottle flies to petal surfaces. Arthropod-Plant Interact 11:171–192CrossRefGoogle 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 108:765–772CrossRefPubMedGoogle Scholar
  22. Castañe C, Alomar O, Riudavets J (1996a) Management of western flower thrips on cucumber with Dicyphus tamaninii (Heteroptera: Miridae). Biol Control 7:114–120CrossRefGoogle Scholar
  23. Castañe C, Arino J, Arno J (1996b) Toxicity of some insecticides and acaricides to the predatory bug Dicyphus tamaninii (Het: Miridae). Entomophaga 41:211–216CrossRefGoogle 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 23:221–224Google Scholar
  25. Castañe C, Alomar O, Riudavets J (2000b) Dicyphus tamaninii in the biological control of cucumber pests. IOBC-WPRS Bull 23:253–256Google 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 47:657–666CrossRefGoogle 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 30:591–597CrossRefGoogle Scholar
  28. Castañe C, Arno J, Gabarra R, Alomar O (2011) Plant damage to vegetable crops by zoophytophagous mirid predators. Biol Control 59:22–29CrossRefGoogle 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 103:204–215CrossRefPubMedGoogle Scholar
  30. Castineras A (1995) Natural enemies of Bemisia tabaci (Homoptera: Aleurodidae) in Cuba. Fla Entomol 78:538–540CrossRefGoogle 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 22:33–36Google Scholar
  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 40:265–271Google Scholar
  33. Chortyk OT, Kays SJ, Teng Q (1997) Characterization of insecticidal sugar esters of Petunia. J Agric Food Chem 45:270–275CrossRefGoogle 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 21–33Google 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 89–130Google Scholar
  36. Cortesero AM, Stapel JO, Lewis WJ (2000) Understanding manipulating plant attributes to enhance biological control. Biol Control 17:35–49CrossRefGoogle Scholar
  37. Costanzi M, Pini S (1991) Ruolo di due miridi predatori nella difesa delle colture ortofloricole. Colture Protette 11:49–53Google Scholar
  38. Dicke M, van Loon JJA (2000) Multitrophic effects of herbivore-induced plant volatiles in an evolutionary context. Entomol Exp Appl 97:237–249CrossRefGoogle 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 151–154Google Scholar
  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 62:243–254CrossRefGoogle Scholar
  41. Drees BM (2002) Aphid management. Texas Agricultural Extension Service, The Texas A&M University System.
  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 113:37–43CrossRefGoogle Scholar
  43. Eigenbrode SD (2004) The effects of plant epicuticular waxy blooms on attachment and effectiveness of predatory insects. Arthr Struct Dev 33:91–102CrossRefGoogle Scholar
  44. Eigenbrode SD, Jetter R (2002) Attachment to plant surface waxes by an insect predator. Integr Comp Biol 42:1091–1099CrossRefPubMedGoogle Scholar
  45. Eigenbrode SD, Kabalo NN (1999) Effects of Brassica oleracea waxblooms on predation and attachment by Hippodamia convergens. Entomol Exp Appl 91:125–130CrossRefGoogle 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 90:225–235CrossRefGoogle 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 157–181CrossRefGoogle 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 58:622–634CrossRefPubMedPubMedCentralGoogle 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 25:140–146CrossRefGoogle Scholar
  50. Eubanks MD, Styrsky JD, Denno RE (2003) The evolution of omnivory in heteropteran insects. Ecology 84:2549–2556CrossRefGoogle Scholar
  51. Evans HF (1976) Mutual interference between predatory anthocorids. Ecol Entomol 1:283–286CrossRefGoogle 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 29:578–609CrossRefGoogle 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 33:219–228CrossRefGoogle 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 5:475–488CrossRefGoogle 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 102:341–348CrossRefGoogle 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 12:543–549Google 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 24:809–817CrossRefGoogle Scholar
  58. Gesse-Solé F (1992) Comportamiento alimenticio de Dicyphus tamaninii Wagner (Heteroptera: Miridae). Bol San Veg Plagas 18:685–691Google 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 47:1–21CrossRefGoogle Scholar
  60. Gillespie DR, Sanchez A, McGregor RR, Quiring D (2001) Dicyphus hesperus—life history, biology and application in tomato greenhouses. Technol Rep 166:1–15Google 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 16:255–267CrossRefGoogle Scholar
  62. Gorb EV, Gorb SN (2002) Attachment ability of the beetle Chrysolina fastuosa on various plant surfaces. Entomol Exp Appl 105:13–28CrossRefGoogle 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 207:2947–2963CrossRefPubMedGoogle 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 2:247–259CrossRefGoogle 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 20:131–143Google Scholar
  66. Goula Goula M, Tavella L (2000) Dicyphini collected on vegetable and wild plants in north-western Italy (Heteroptera, Miridae). IOBC-WPRS Bull 23:257Google Scholar
  67. Guo F, Zhang Z-Q, Zhaoe Z (1998) Pesticide resistance of Tetranychus cinnabarinus (Acari: Tetranychidae) in China: a review. Syst Appl Acar 3:3–7Google Scholar
  68. Gutschick VP (1999) Biotic and abiotic consequences of differences in leaf structure. New Phytol 143:3–18CrossRefGoogle 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 5:5468–5477CrossRefPubMedPubMedCentralGoogle 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 88:685–691CrossRefGoogle Scholar
  71. Hegnauer R (1992) Chemotaxonomie der Pflanzen, eine Übersicht über die Verbreitung und die systematische Bedeutung der Pflanzenstoffe. Birkhäuser Verlag, BaselGoogle Scholar
  72. Holling CS (1966) The functional response of invertebrate predators to prey density. Mem Entomol Soc Can 98:5–86CrossRefGoogle 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 61:139–140Google Scholar
  74. Ingegno BL, Pansa MG, Tavella L (2011) Plant preference in the zoophytophagous generalist predator Macrolophus pygmaeus (Heteroptera: Miridae). Biol Control 58:174–181CrossRefGoogle 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 67:246–252CrossRefGoogle 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 29:117–142CrossRefGoogle Scholar
  77. Ingegno BL, Bodino N, Leman A, Messelink GJ, Tavella J (2017a) Predatory efficacy of Dicyphus errans on different prey. Acta Hortic 1164:425–430CrossRefGoogle 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 107:340–348CrossRefPubMedGoogle 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 1164:377–382CrossRefGoogle 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 92:1457–1466CrossRefGoogle 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 23–64Google Scholar
  82. Jervis M, Kidd N (1996) Insect natural enemies. Practical approaches to their study and evaluation. Chapman & Hall, LondonCrossRefGoogle Scholar
  83. Johnson HB (1975) Plant pubescence: an ecological perspective. Bot Rev 41:233–258CrossRefGoogle 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 157–174Google 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 61:313–318Google Scholar
  86. Kolbe W, Bruns A (1988) Insekten und Spinnen in Land- und Gartenbau. Pflanzenbau/Pflanzenschutz, Heft 25, Rhein. Landwirtschaftverlag, BonnGoogle Scholar
  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 8:1779CrossRefGoogle Scholar
  88. Lauenstein G (1976) Untersuchungen zu Biologie und Verhaltensweisen der Räuberischen Blumenwanze Anthocoris nemorum L. (Het.: Anthocoridae). PhD Thesis, Georg-August-Universität Göttingen, GermanyGoogle Scholar
  89. Lauenstein G (1980) Zum Suchverhalten von Anthocoris nemorum L. (Het. Anthocoridae). Ztschr Angew Entomol 89:428–442CrossRefGoogle Scholar
  90. Levin DA (1973) The role of trichomes in plant defense. Quart Rev Biol 48:3–15CrossRefGoogle 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 47:885–891CrossRefPubMedGoogle Scholar
  92. Lucas É, Alomar Ò (2001) Macrolophus caliginosus (Wagner) as an intraguild prey for the zoophytophagous Dicyphus tamaninii Wagner (Heteroptera: Miridae). Biol Control 20:147–152CrossRefGoogle 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 136:104007CrossRefGoogle 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 298:39–43Google 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 79:92–100CrossRefGoogle 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 139:333–341CrossRefGoogle Scholar
  97. Miller NCE (1971) The biology of the Heteroptera, 2nd edn. E. W. Classey Ltd., HamptonGoogle 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 72:1350–1358CrossRefPubMedGoogle 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 YorkGoogle 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 13:679–683CrossRefGoogle 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 2:185–193CrossRefGoogle 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 98:956–962CrossRefGoogle 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 35:297–306CrossRefGoogle 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 20:241–248Google 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 17:55–60CrossRefGoogle 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 20:222–227CrossRefGoogle Scholar
  107. Perez-Hedo M, Urbaneja A (2015) Prospects for predatory mirid bugs as biocontrol agents of aphids in sweet peppers. J Pest Sci 88:65–73CrossRefGoogle Scholar
  108. Perez-Hedo M, Rambla JL, Granell A, Urbaneja A (2018) Biological activity and specificity of Miridae-induced plant volatiles. Biocontrol 63:203–213CrossRefGoogle 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 23:77–86Google 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 7:1794CrossRefPubMedPubMedCentralGoogle Scholar
  111. Press MC (1999) The functional significance of leaf structure: a search for generalizations. New Phytol 143:213–219CrossRefGoogle Scholar
  112. Price PW (1991) The plant vigor hypothesis and herbivore attack. Oikos 62:244–251CrossRefGoogle 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 11:41–65CrossRefGoogle Scholar
  114. Price PW, Denno RF, Eubanks MD, Finke DL, Kaplan I (2011) Insect ecology: behaviour, populations and communities. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  115. Prüm B, Seidel R, Bohn HF, Speck T (2012) Plant surfaces with cuticular folds are slippery for beetles. J R Soc Interface 9:127–135CrossRefPubMedGoogle 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 9:6360–6368CrossRefPubMedGoogle 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 35:99–111Google 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 106:9–15CrossRefGoogle Scholar
  119. Raworth, DA (2001) Control of two-spotted spider mite by Phytoseiulus persimilis. J Asia-Pacific Entomol 4:157–163CrossRefGoogle Scholar
  120. Reinhold M (1975) Eignung verschiedener Blattlausarten für ihre Feinde. Diploma Thesis, Institut für Pflanzenpathologie und Pflanzenschutz, Georg-August-Universität Göttingen, GermanyGoogle Scholar
  121. Ronco C, Faure E (1993) Monitoraggio di miridi spontanei su pomodoro in tunnel. L´Informatore Agrario 45:61–62Google 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 376:577–578Google 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 8:10975CrossRefPubMedPubMedCentralGoogle 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 112:7–19CrossRefGoogle Scholar
  125. Saulich AK, Musolin DL (2019) Seasonal development of plant bugs (Heteroptera, Miridae): subfamily Bryocorinae. Entomol Rev 99:275–291CrossRefGoogle Scholar
  126. Schewket Bey N (1930) Zur Biologie der phytophagen Wanze Dicyphus errans Wolff (Capsidae). Z Insbiol XXV:179–183Google Scholar
  127. Schuh RT (1976) Pretarsal structure in the Miridae (Hemiptera) with a cladistic analysis of relationships within the family. Am Mus Novit 2601:1–39Google Scholar
  128. Seidenstücker G (1967) Eine Phyline mit Dicyphus-Kralle (Heteroptera, Miridae). Reichenbachia 8:215–220Google 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 75:161–165Google 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 76–88Google 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 6:12–13Google 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 3–23Google 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 1–22Google Scholar
  134. Stork NE (1980) Role of wax blooms in preventing attachment to brassicas by the mustard beetle, Phaedon cochleariae. Entomol Exp Appl 28:100–107CrossRefGoogle 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, GermanyGoogle Scholar
  136. Utsumi S (2013) Evolutionary community ecology of plant-associated arthropods in terrestrial ecosystems. Ecol Res 28:359–371CrossRefGoogle 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 14:424–432CrossRefGoogle 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 108:109–116CrossRefGoogle 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 3:141–149CrossRefGoogle 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:270–285Google Scholar
  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, GermanyGoogle Scholar
  142. Voigt D (2004) Eine Bereicherung für den Bio-Anbau? Die räuberische Weichwanze Dicyphus errans Wolff. Das Taspo Magazin 2/2004:18–20Google Scholar
  143. Voigt D (2005) Untersuchungen zur Morphologie, Biologie und Ökologie der räuberischen Weichwanze Dicyphus errans Wolff (Heteroptera, Miridae, Bryocorinae). PhD Thesis, Technische Universität Dresden, GermanyGoogle Scholar
  144. Voigt D, Gorb S (2010) Locomotion in a sticky terrain. Arthropod-Plant Interact 4:69–79CrossRefGoogle 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 15:305–308Google Scholar
  146. Voigt D, Gorb E, Gorb S (2007) Plant surface–bug interactions: Dicyphus errans stalking along trichomes. Arthropod-Plant Interact 1:221–243CrossRefGoogle 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 12:415–421CrossRefGoogle Scholar
  148. Wagner E (1955) Bemerkungen zum System der Miridae (Hemiptera, Heteroptera). Dtsch Entomol Z 2:230–242CrossRefGoogle Scholar
  149. Walters PJ (1974) A method for culturing Stethorus spp. (Coleoptera: Coccinellidae) on Tetranychus urticae (Koch) (Acarina: Tetranychidae). J Aust Entomol Soc 13:245–246CrossRefGoogle Scholar
  150. Wheeler AG (2001) Biology of the plant bugs (Hemiptera: Miridae): pests, predators, opportunists. Cornell University Press, LondonGoogle Scholar
  151. White C, Eigenbrode SD (2000) Leaf surface waxbloom in Pisum sativum influences predation and intra-guild interactions involving two predator species. Oecologia 124:252–259CrossRefPubMedGoogle 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 86:119–124CrossRefGoogle 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 127:80–84CrossRefGoogle Scholar

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© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Faculty of BiologyInstitute for Botany, Technische Universität DresdenDresdenGermany

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