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Annual Review of Entomology

Volume 60, 2015

Mirid (Hemiptera: Heteroptera) Specialists of Sticky Plants: Adaptations, Interactions, and Ecological Implications

Abstract

Sticky plants—those having glandular trichomes (hairs) that produce adhesive, viscous exudates—can impede the movement of, and entrap, generalist insects. Disparate arthropod groups have adapted to these widespread and taxonomically diverse plants, yet their interactions with glandular hosts rarely are incorporated into broad ecological theory. Ecologists and entomologists might be unaware of even well-documented examples of insects that are sticky-plant specialists. The hemipteran family Miridae (more specifically, the omnivorous Dicyphini: Dicyphina) is the best-known group of arthropods that specializes on sticky plants. In the first synthesis of relationships with glandular plants for any insect family, we review mirid interactions with sticky hosts, including their adaptations (behavioral, morphological, and physiological) and mutualisms with carnivorous plants, and the ecological and agricultural implications of mirid–sticky plant systems. We propose that mirid research applies generally to tritrophic interactions on trichome-defended plants, enhances an understanding of insect-plant interactions, and provides information useful in managing crop pests.

Keyword(s): carnivorous plants, enemy-free space, intraguild predation, mutualisms, omnivory, tritrophic interactions
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2015-01-07
2024-04-20
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Literature Cited

  1. Adamec L. 1.  2011. Ecophysiological look at plant carnivory. Why are plants carnivorous?. See Ref. 100 457–89
  2. Anderson B. 2.  2005. Adaptations to foliar absorption of faeces: a pathway in plant carnivory. Ann. Bot. 95:757–61Establishes that plants lacking digestive enzymes can be considered carnivorous if they engage in mirid mutualisms. [Google Scholar]
  3. Anderson B. 3.  2006. Inferring evolutionary patterns from the biogeographical distributions of mutualists and exploiters. Biol. J. Linn. Soc. 89:541–49 [Google Scholar]
  4. Anderson B, Kawakita A, Tayasu I. 4.  2012. Sticky plant captures prey for symbiotic bug: Is this digestive mutualism?. Plant Biol. 14:888–93 [Google Scholar]
  5. Anderson B, Midgley JJ. 5.  2002. It takes two to tango but three is a tangle: mutualists and cheaters on the carnivorous plant Roridula. Oecologia 132:369–73 [Google Scholar]
  6. Anderson B, Midgley JJ. 6.  2007. Density-dependent outcomes in a digestive mutualism between carnivorous Roridula plants and their associated hemipterans. Oecologia 152:115–20 [Google Scholar]
  7. Anderson B, Midgley JJ, Stewart BA. 7.  2003. Facilitated selfing offers reproductive assurance: a mutualism between a hemipteran and carnivorous plant. Am. J. Bot. 90:1009–115 [Google Scholar]
  8. Andres MR, Connor EF. 8.  2003. The community-wide and guild-specific effects of pubescence on the folivorous insects of manzanitas Arctostaphylos spp. Ecol. Entomol. 28:383–96 [Google Scholar]
  9. Berdegue M, Trumble JT, Hare JD, Redak RA. 9.  1996. Is it enemy-free space? The evidence for terrestrial insects and freshwater arthropods. Ecol. Entomol. 21:203–17 [Google Scholar]
  10. Berenbaum MR, Zangerl AR. 10.  2008. Facing the future of plant-insect interaction research: le retour à la “raison d'être.”. Plant Physiol. 146:804–11 [Google Scholar]
  11. Bernays EA. 11.  1991. Evolution of insect morphology in relation to plants. Philos. Trans. R. Soc. Lond. B 333:257–64 [Google Scholar]
  12. Boughton AJ, Hoover K, Felton GW. 12.  2005. Methyl jasmonate application induces increased densities of glandular trichomes on tomato, Lycopersicon esculentum. J. Chem. Ecol. 31:2211–16 [Google Scholar]
  13. Carmona D, Lajeunesse MJ, Johnson MTJ. 13.  2011. Plant traits that predict resistance to herbivores. Funct. Ecol. 25:358–67 [Google Scholar]
  14. Cassis G, Schuh RT. 14.  2012. Systematics, biodiversity, biogeography, and host associations of the Miridae (Insecta: Hemiptera: Heteroptera: Cimicomorpha). Annu. Rev. Entomol. 57:377–404Reviews mirid systematics, including distributional patterns by biogeographic region and host-plant trends. [Google Scholar]
  15. Castañé C, Arnó J, Gabarra R, Alomar O. 15.  2011. Plant damage to vegetable crops by zoophytophagous mirid predators. Biol. Control 59:22–29 [Google Scholar]
  16. Chase MW, Christenhusz MJM, Sanders D, Fay MF. 16.  2009. Murderous plants: Victorian Gothic, Darwin and modern insights into vegetable carnivory. Bot. J. Linn. Soc. 161:329–56 [Google Scholar]
  17. Clausen J. 17.  1951. Stages in the Evolution of Plant Species Ithaca, NY: Cornell Univ. Press
  18. Cobben RH. 18.  1978. Evolutionary trends in Heteroptera. Part II. Mouthpart-structures and feeding strategies. Meded. Landbouwhogesch. Wagening. 78:51–407 [Google Scholar]
  19. Cohen AC. 19.  1995. Extra-oral digestion in predaceous terrestrial Arthropoda. Annu. Rev. Entomol. 40:85–103 [Google Scholar]
  20. Coll M. 20.  1998. Living and feeding on plants in predatory Heteroptera. Predatory Heteroptera: Their Ecology and Use in Biological Control M Coll, JR Ruberson 89–129 Lanham, MD: Entomol. Soc. Am. [Google Scholar]
  21. Coll M, Guershon M. 21.  2002. Omnivory in terrestrial arthropods: mixing plant and prey diets. Annu. Rev. Entomol. 47:267–97 [Google Scholar]
  22. Darwin C. 22.  1875. Insectivorous Plants New York: Appleton
  23. Davidson NA, Kinsey MG, Ehler LE, Frankie GW. 23.  1992. Tobacco budworm, pest of petunias, can be managed with Bt. Calif. Agric. 46:47–9 [Google Scholar]
  24. Dimock MB, Kennedy GG. 24.  1983. The role of glandular trichomes in the resistance of Lycopersicon hirsutum f. glabratum to Heliothis zea. Entomol. Exp. Appl. 33:263–68 [Google Scholar]
  25. Dolling WR, Palmer JM. 25.  1991. Pameridea (Hemiptera: Miridae): predaceous bugs specific to the highly viscid plant genus Roridula. Syst. Entomol. 16:319–28 [Google Scholar]
  26. Duke SO. 26.  1994. Glandular trichomes—a focal point of chemical and structural interactions. Int. J. Plant Sci. 155:617–20 [Google Scholar]
  27. Economou LP, Lykouressis DP, Barbetaki AE. 27.  2006. Time allocation of activities of two heteropteran predators on the leaves of three tomato cultivars with variable glandular trichome density. Environ. Entomol. 35:387–93 [Google Scholar]
  28. Eigenbrode SD, Trumble JT, White KK. 28.  1996. Trichome exudates and resistance to beet armyworm (Lepidoptera: Noctuidae) in Lycopersicon hirsutum f. typicum accessions. Environ. Entomol. 25:90–95 [Google Scholar]
  29. Eisner T, Aneshansley DJ. 29.  1983. Adhesive strength of the insect-trapping glue of a plant (Befaria racemosa). Ann. Entomol. Soc. Am. 76:295–98 [Google Scholar]
  30. Eisner T, Eisner M, Hoebeke ER. 30.  1998. When defense backfires: detrimental effects of a plant's protective trichomes on an insect beneficial to the plant. Proc. Natl. Acad. Sci. USA 95:4410–14 [Google Scholar]
  31. Elle E, Hare JD. 31.  2000. No benefit of glandular trichome production in natural populations of Datura wrightii?. Oecologia 123:57–65 [Google Scholar]
  32. Elle E, van Dam NM, Hare JD. 32.  1999. Cost of glandular trichomes, a “resistance” character in Datura wrightii Regel (Solanaceae). Evolution 53:22–35 [Google Scholar]
  33. Eubanks MD, Styrsky JD, Denno RF. 33.  2003. The evolution of omnivory in heteropteran insects. Ecology 84:2549–56 [Google Scholar]
  34. Fernandes GW. 34.  1994. Plant mechanical defenses against insect herbivory. Rev. Brasil. Entomol. 38:421–33 [Google Scholar]
  35. Gassmann AJ, Hare JD. 35.  2005. Indirect cost of a defensive trait: Variation in trichome type affects the natural enemies of herbivorous insects on Datura wrightii. Oecologia 144:62–71 [Google Scholar]
  36. Gastauer M, Campos LAO, Wittmann D. 36.  2013. Handling sticky resin by stingless bees: adhesive properties of surface structures. An. Acad. Bras. Cienc. 85:1189–96 [Google Scholar]
  37. Gillespie DR, McGregor RR. 37.  2000. The functions of plant feeding in the omnivorous predator Dicyphus hesperus: Water places limits on predation. Ecol. Entomol. 25:380–86 [Google Scholar]
  38. Gillespie DR, VanLaerhoven SL, McGregor RR, Chan S, Roitberg BD. 38.  2012. Plant feeding in an omnivorous mirid, Dicyphus hesperus: why plant context matters. Psyche 2012:495805 [Google Scholar]
  39. Glas JJ, Schimmel BCJ, Alba JM, Escobar-Bravo R, Schuurink RC, Kant MR. 39.  2012. Plant glandular trichomes as targets for breeding or engineering of resistance to herbivores. Int. J. Mol. Sci. 13:17077–103 [Google Scholar]
  40. Gonzáles WL, Negritto MA, Suárez LH, Gianoli E. 40.  2008. Induction of glandular and non-glandular trichomes by damage in leaves of Madia sativa under contrasting water regimes. Acta Oecol. 33:128–32 [Google Scholar]
  41. Goodell PB, Ribeiro B. 41.  2006. Measuring localized movement of Lygus hesperus into San Joaquin Valley cotton fields. Proc. Beltwide Cotton Conf., San Antonio, Texas1375–79 Cordova, TN: Natl. Cotton Counc. [Google Scholar]
  42. Hare JD, Walling LL. 42.  2006. Constitutive and jasmonate-inducible traits of Datura wrightii. J. Chem. Ecol. 32:29–47 [Google Scholar]
  43. Hartmann T. 43.  2008. The lost origin of chemical ecology in the late 19th century. Proc. Natl. Acad. Sci. USA 105:4541–46 [Google Scholar]
  44. Henry TJ. 44.  2009. Biodiversity of Heteroptera. Insect Biodiversity: Science and Society RG Foottit, PH Adler 223–63 Chichester, UK: Wiley-Blackwell [Google Scholar]
  45. Ingegno BL, Pansa MG, Tavella L. 45.  2011. Plant preference in the zoophytophagous generalist predator Macrolophus pygmaeus (Heteroptera: Miridae). Biol. Control 58:174–81 [Google Scholar]
  46. Jaime R, Rey PJ, Alcántara JM, Bastida JM. 46.  2013. Glandular trichomes as an inflorescence defence mechanism against insect herbivores in Iberian columbines. Oecologia 172:1051–60 [Google Scholar]
  47. Johnson JC, Nielsen MT, Collins GB. 47.  1988. Inheritance of glandular trichomes in tobacco. Crop Sci. 28:241–44 [Google Scholar]
  48. Juniper B, Southwood R. 48.  1986. Insects and the Plant Surface London: Edward Arnold
  49. Karban R, Baldwin IT. 49.  1997. Induced Responses to Herbivory Chicago: Univ. Chicago Press
  50. Kellogg DW, Taylor TN, Krings M. 50.  2002. Effectiveness in defense against phytophagous arthropods of the cassabanana (Sicana odorifera) glandular trichomes. Entomol. Exp. Appl. 103:187–89 [Google Scholar]
  51. Kennedy CEJ. 51.  1986. Attachment may be a basis for specialization in oak aphids. Ecol. Entomol. 11:291–300 [Google Scholar]
  52. Kennedy GG. 52.  2003. Tomato, pests, parasitoids, and predators: tritrophic interactions involving the genus Lycopersicon. Annu. Rev. Entomol. 48:51–72 [Google Scholar]
  53. Koch K, Bhushan B, Barthlott W. 53.  2009. Multifunctional surface structures of plants: an inspiration for biomimetics. Prog. Mater. Sci. 54:137–78 [Google Scholar]
  54. Krimmel BA, Pearse IS. 54.  2013. Sticky plant traps insects to enhance indirect defence. Ecol. Lett. 16:219–24Demonstrates that sticky-plant-trapped insect carrion enhances indirect herbivore defense by increasing scavenging predators. [Google Scholar]
  55. Król E, Płachno BJ, Adamec L, Stolarz M, Dziubińska H, Trębacz K. 55.  2012. Quite a few reasons for calling carnivores ‘the most wonderful plants in the world.’. Ann. Bot. 109:47–64 [Google Scholar]
  56. Kullenberg B. 56.  1944. Studien über die Biologie der Capsiden. Zool. Bidr. Upps. 23:1–522Provides detailed, but underappreciated, treatment of the bionomics of nearly 100 species of Swedish mirids. [Google Scholar]
  57. Lambert AM. 57.  2007. Effects of prey availability, facultative plant feeding, and plant defenses on a generalist insect predator. Arthropod-Plant Interact. 1:167–73 [Google Scholar]
  58. Levin DA. 58.  1973. The role of trichomes in plant defense. Q. Rev. Biol. 48:3–15 [Google Scholar]
  59. Li L, Zhao Y, McCaig BC, Wingerd BA, Wang J. 59.  et al. 2004. The tomato homolog of CORONATINE-INSENSITIVE1 is required for the maternal control of seed maturation, jasmonate-signaled defense responses, and glandular trichome development. Plant Cell 16:126–43 [Google Scholar]
  60. Lin SYH, Trumble JT, Kumamoto J. 60.  1987. Activity of volatile compounds in glandular trichomes of Lycopersicon species against two insect herbivores. J. Chem. Ecol. 13:837–50 [Google Scholar]
  61. Loganathan J, David PMM. 61.  1999. Sticky weeds as an understorey vegetation in intensively managed teak plantation for defoliator management. Crop Prot. 18:577–80 [Google Scholar]
  62. Lowrie A. 62.  1998. Carnivorous Plants of Australia 3 Nedlands, Aust: Univ. West. Aust. Press
  63. Luckwill LC. 63.  1943. The Genus Lycopersicon. Aberdeen, UK: Aberdeen Univ. Press [Google Scholar]
  64. Lykouressis D, Giatropoulos A, Perdikis D, Favas C. 64.  2008. Assesssing the suitability of noncultivated plants and associated insect prey as food sources for the omnivorous predator Macrolophus pygmaeus (Hemiptera: Miridae). Biol. Control 44:142–48 [Google Scholar]
  65. Maluf WR, Inoue IF, Ferreira RPD, Gomes LAA, Castro EM, Cardoso MG. 65.  2007. Higher glandular trichome density in tomato leaflets and repellence to spider mites. Pesqui. Agropecu. Bras. 42:1227–35 [Google Scholar]
  66. Martinez-Cascales JI, Cenis JL, Cassis G, Sanchez JA. 66.  2006. Species identity of Macrolophus melanotoma (Costa 1853) and Macrolophus pygmaeus (Rambur 1839) (Insecta: Heteroptera: Miridae) based on morphological and molecular data and bionomic implications. Insect Syst. Evol. 37:385–404 [Google Scholar]
  67. McDowell ET, Kapteyn J, Schmidt A, Li C, Kang J-H. 67.  et al. 2011. Comparative functional genomic analysis of Solanum glandular trichome types. Plant Physiol. 155:524–39 [Google Scholar]
  68. McGregor RR, Gillespie DR. 68.  2004. Olfactory responses of the omnivorous generalist predator Dicyphus hesperus to plant and prey odours. Entomol. Exp. Appl. 112:201–5 [Google Scholar]
  69. McPherson S. 69.  2008. Glistening Carnivores: The Sticky-Leaved Insect-Eating Plants Dorset, UK: Redfern Nat. Hist. Prod.
  70. Mechaber WL, Marshall DB, Mechaber RA, Jobe RT, Chew FS. 70.  1996. Mapping leaf surface landscapes. Proc. Natl. Acad. Sci. USA 93:4600–3 [Google Scholar]
  71. Medeiros L, Moreira GRP. 71.  2002. Moving on hairy surfaces: modifications of Gratiana spadicea larval legs to attach on its host plant Solanum sisymbriifolium. Entomol. Exp. Appl. 102:295–305 [Google Scholar]
  72. Moayeri HRS, Ashouri A, Poll L, Enkegaard A. 72.  2007. Olfactory response of a predatory mirid to herbivore induced plant volatiles: multiple herbivory vs. single herbivory. J. Appl. Entomol. 131:326–32 [Google Scholar]
  73. Moreno-Ripoll R, Agustí N, Berruezo R, Gabarra R. 73.  2012. Conspecific and heterospecific interactions between two omnivorous predators on tomato. Biol. Control 62:189–96 [Google Scholar]
  74. Obrycki JJ, Tauber MJ. 74.  1984. Natural enemy activity on glandular pubescent potato plants in the greenhouse: an unreliable predictor of effects in the field. Environ. Entomol. 13:679–83 [Google Scholar]
  75. Obrycki JJ, Tauber MJ, Tingey WM. 75.  1983. Predator and parasitoid interaction with aphid-resistant potatoes to reduce aphid densities: a two-year field study. J. Econ. Entomol. 76:456–62 [Google Scholar]
  76. Painter RH. 76.  1951. Insect Resistance in Crop Plants New York: Macmillan
  77. Peeters PJ. 77.  2002. Correlations between leaf structural traits and the densities of herbivorous insect guilds. Biol. J. Linn. Soc. 77:43–65 [Google Scholar]
  78. Peiffer M, Tooker JF, Luthe DS, Felton GW. 78.  2009. Plants on early alert: glandular trichomes as sensors for insect herbivores. New Phytol. 184:644–56 [Google Scholar]
  79. Peterson JK, Horvat RJ, Elsey KD. 79.  1994. Squash leaf glandular trichome volatiles: identification and influence on behavior of female pickleworm moth [Diaphania nitidalis (Stoll.)] (Lepidoptera: Pyralidae). J. Chem. Ecol. 20:2099–109 [Google Scholar]
  80. Płachno BJ, Adamec L, Lichtscheidl IK, Peroutka M, Adlassnig W, Vrba J. 80.  2006. Fluorescence labelling of phosphatase activity in digestive glands of carnivorous plants. Plant Biol. 8:813–20 [Google Scholar]
  81. Price PW, Bouton CE, Gross P, McPheron BA, Thompson JN, Weis AE. 81.  1980. Interactions among three trophic levels: influence of plants on interactions between insect herbivores and natural enemies. Annu. Rev. Ecol. Syst. 11:41–65 [Google Scholar]
  82. Raman K, Sanjayan KP. 82.  1984. Host plant relationships and population dynamics of the mirid, Cyrtopeltis tenuis Reut. (Hemiptera: Miridae). Proc. Indian Natl. Sci. Acad. B 50:355–61 [Google Scholar]
  83. Rautio P, Markkola A, Martel J, Tuomi J, Härmä E. 83.  et al. 2002. Developmental plasticity in birch leaves: defoliation causes a shift from glandular to nonglandular trichomes. Oikos 98:437–46 [Google Scholar]
  84. Rice BA. 84.  2008. Reassessing commensal-enabled carnivory in Proboscidea and Ibicella?. Carniv. Plant Newsl. 37:15–19 [Google Scholar]
  85. Rice BA. 85.  2011. Reversing the roles of predator and prey: a review of carnivory in the botanical world. See Ref. 100 493–518
  86. Riddick EW, Simmons AM. 86.  2014. Do plant trichomes cause more harm than good to predatory insects?. Pest Manag. Sci. 701655–65
  87. Roitberg BD, Gillespie DR, Quiring DMJ, Alma CR, Jenner WH. 87.  et al. 2005. The cost of being an omnivore: mandible wear from plant feeding in a true bug. Naturwissenschaften 92:431–34 [Google Scholar]
  88. Romero GQ, Souza JC, Vasconcellos-Neto J. 88.  2008. Anti-herbivore protection by mutualistic spiders and the role of plant glandular trichomes. Ecology 89:3105–15 [Google Scholar]
  89. Russell MC. 89.  1953. Notes on insects associated with sundews (Drosera) at Lesmurdie. West. Aust. Nat. 4:9–12 [Google Scholar]
  90. Saeidi Z, Mallik B, Kulkarni RS. 90.  2007. Inheritance of glandular trichomes and two-spotted spider mite resistance in cross Lycopersicon esculentum “Nandi” and L. pennellii “LA2963.”. Euphytica 154:231–38 [Google Scholar]
  91. Sánchez JA, Gillespie DR, McGregor RR. 91.  2003. The effects of mullein plants (Verbascum thapsus) on the population dynamics of Dicyphus hesperus (Heteroptera: Miridae) in tomato greenhouses. Biol. Control 28:313–19 [Google Scholar]
  92. Schilmiller AL, Last RL, Pichersky E. 92.  2008. Harnessing plant trichome biochemistry for the production of useful compounds. Plant J. 54:702–11 [Google Scholar]
  93. Schmidt RA. 93.  2014. Leaf structures affect predatory mites (Acari: Phytoseiidae) and biological control: a review. Exp. Appl. Acarol. 62:1–17 [Google Scholar]
  94. Schuh RT. 94.  1976. Pretarsal structure in the Miridae (Hemiptera) with a cladistic analysis of relationships within the family. Am. Mus. Novit. 2601:1–39 [Google Scholar]
  95. Schuh RT. 95.  2001. Revision of New World Plagiognathus Fieber, with comments on the Palearctic fauna and the description of a new genus (Heteroptera: Miridae: Phylinae). Bull. Am. Mus. Nat. Hist. 266:1–267 [Google Scholar]
  96. Schuh RT. 96.  2013. On-line Systematic Catalog of Plant Bugs (Insecta: Heteroptera: Miridae) New York: Am. Mus. Nat. Hist., updated Mar 2013, accessed on Mar. 4, 2014. http://research.amnh.org/pbi/catalog/ [Google Scholar]
  97. Schuh RT, Slater JA. 97.  1995. True Bugs of the World (Hemiptera: Heteroptera): Classification and Natural History Ithaca, NY: Cornell Univ. Press [Google Scholar]
  98. Schwartz MD, Foottit RG. 98.  1998. Revision of the Nearctic species of the genus Lygus Hahn, with a review of the Palaearctic species (Heteroptera: Miridae). Mem. Entomol. Int. 10:1–428 [Google Scholar]
  99. Schwoerbel W. 99.  1956. Beobachtungen und Untersuchungen zur Biologie einiger einheimischer Wanzen. Zool. Jahrb. 84:329–54 [Google Scholar]
  100. Seckbach J, Dubinsky Z. 100.  2011. All Flesh Is Grass: Plant-Animal Interrelationships. Dordrecht, Neth: Springer
  101. Seidenstücker G. 101.  1967. Eine Phyline mit Dicyphus-Kralle (Heteroptera, Miridae). Reichenbachia 8:215–20 [Google Scholar]
  102. Serna L, Martin C. 102.  2006. Trichomes: Different regulatory networks lead to convergent structures. Trends Plant Sci. 11:274–80 [Google Scholar]
  103. Simmons AT, Gurr GM. 103.  2005. Trichomes of Lycopersicon species and their hybrids: effects on pests and natural enemies. Agric. For. Entomol. 7:265–76 [Google Scholar]
  104. Simone-Finstrom M, Spivak M. 104.  2010. Propolis and bee health: the natural history and significance of resin use by honey bees. Apidologie 41:295–311 [Google Scholar]
  105. Southwood R. 105.  1986. Plant surfaces and insects—an overview. See Ref. 48 1–22
  106. Spomer GG. 106.  1999. Evidence of protocarnivorous capabilities in Geranium viscosissimum and Potentilla arguta and other sticky plants. Int. J. Plant Sci. 160:98–101 [Google Scholar]
  107. Stonedahl GM, Schwartz MD. 107.  1986. Revision of the plant bug genus Pseudopsallus Van Duzee (Heteroptera: Miridae). Am. Mus. Novit. 2842:1–58 [Google Scholar]
  108. Sugiura S, Yamazaki K. 108.  2006. Consequences of scavenging behaviour in a plant bug associated with a glandular plant. Biol. J. Linn. Soc. 88:593–602 [Google Scholar]
  109. Sutherst RW, Jones RJ, Schnitzerling HJ. 109.  1982. Tropical legumes of the genus Stylosanthes immobilize and kill cattle ticks. Nature 295:320–21 [Google Scholar]
  110. Sweet MH. 110.  1979. On the original feeding habits of the Hemiptera (Insecta). Ann. Entomol. Soc. Am. 72:575–79 [Google Scholar]
  111. Tissier A, Sallaud C, Rontein D. 111.  2013. Tobacco trichomes as a platform for terpenoid biosynthesis engineering. Isoprenoid Synthesis in Plants and Microorganisms: New Concepts and Experimental Approaches TJ Bach, M Rohmer 271–83 New York: Springer [Google Scholar]
  112. Torres JB, Barros EM, Coelho RR, Pimentel RMM. 112.  2010. Zoophytophagous pentatomids feeding on plants and implications for biological control. Arthropod-Plant Interact. 4:219–27 [Google Scholar]
  113. van Dam NM, Hare JD. 113.  1998. Biological activity of Datura wrightii glandular trichome exudate against Manduca sexta larvae. J. Chem. Ecol. 24:1529–49 [Google Scholar]
  114. van Dam NM, Hare JD. 114.  1998. Differences in distribution and performance of two sap-sucking herbivores on glandular and non-glandular Datura wrightii. Ecol. Entomol. 23:22–32 [Google Scholar]
  115. Verheggen FJ, Capella Q, Schwartzberg EG, Voigt D, Haubruge E. 115.  2009. Tomato-aphid-hoverfly: a tritrophic interaction incompatible for pest management. Arthropod-Plant Interact. 3:141–49 [Google Scholar]
  116. Vila E, Parra A, Beltrán D, Gallego JR, Fernandez FJ, Cabello T. 116.  2012. IPM strategies in tomato crops in Spanish greenhouses: effects of cultivars and the integration of natural enemies. IOBC-WPRS Bull. 80:245–51 [Google Scholar]
  117. Voigt D, Gorb E, Gorb S. 117.  2007. Plant surface–bug interactions: Dicyphus errans stalking along trichomes. Arthropod-Plant Interact. 1:221–43 [Google Scholar]
  118. Voigt D, Gorb S. 118.  2008. An insect trap as habitat: Cohesion-failure mechanism prevents adhesion of Pameridea roridulae bugs to the sticky surface of the plant Roridula gorgonias. J. Exp. Biol. 211:2647–57Demonstrates that an epicuticular grease layer prevents a dicyphine mirid's entrapment in sticky host exudates. [Google Scholar]
  119. Voigt D, Gorb S. 119.  2010. Desiccation resistance of adhesive secretion in the protocarnivorous plant Roridula gorgonias as an adaptation to periodically dry environment. Planta 232:1511–15 [Google Scholar]
  120. Voigt D, Gorb S. 120.  2010. Locomotion in a sticky terrain. Arthropod-Plant Interact. 4:69–79 [Google Scholar]
  121. Wagner GJ, Wang E, Shepherd RW. 121.  2004. New approaches for studying and exploiting an old protuberance, the plant trichome. Ann. Bot. 93:3–11 [Google Scholar]
  122. Wang E, Wang R, DeParasis J, Loughrin JH, Gan S, Wagner GJ. 122.  2001. Suppression of a P450 hydroxylase gene in plant trichome glands enhances natural-product-based aphid resistance. Nat. Biotechnol. 19:371–74 [Google Scholar]
  123. Watson AP, Matthiessen JN, Springett BP. 123.  1982. Arthropod associates and macronutrient status of the red-ink sundew (Drosera erythrorhiza Lindl.). Aust. J. Ecol. 7:13–22 [Google Scholar]
  124. Weinhold A, Baldwin IT. 124.  2011. Trichome-derived O-acyl sugars are a first meal for caterpillars that tags them for predation. Proc. Natl. Acad. Sci. USA 108:7855–59 [Google Scholar]
  125. Weirauch C. 125.  2008. Cladistic analysis of Reduviidae (Heteroptera: Cimicomorpha) based on morphological characters. Syst. Entomol. 33:229–74 [Google Scholar]
  126. Wheeler AG Jr. 126.  1974. Studies on the arthropod fauna of alfalfa VI. Plant bugs (Miridae). Can. Entomol. 106:1267–75 [Google Scholar]
  127. Wheeler AG Jr. 127.  2001. Biology of the Plant Bugs (Hemiptera: Miridae): Pests, Predators, Opportunists Ithaca, NY: Cornell Univ. PressProvides first worldwide review and synthesis of literature on mirid biology. [Google Scholar]
  128. Wheeler AG Jr, McCaffrey JP. 128.  1984. Ranzovius contubernalis: seasonal history, habits, and description of fifth instar, with speculation on the origin of spider commensalism in the genus Ranzovius (Hemiptera: Miridae). Proc. Entomol. Soc. Wash. 86:68–81 [Google Scholar]
  129. Wheeler AG Jr, Miller GL, Henry TJ. 129.  1979. Biology and habits of Macrolophus tenuicornis (Hemiptera: Miridae) on hay-scented fern (Pteridophyta: Polypodiaceae). Melsheimer Entomol. Ser. 27:11–17 [Google Scholar]
  130. Wheeler QD, Wheeler AG Jr. 130.  1994. Mycophagous Miridae? Associations of Cylapinae (Heteroptera) with pyrenomycete fungi (Euascomycetes: Xylariaceae). J. N. Y. Entomol. Soc. 102:114–17 [Google Scholar]
  131. Wilkens RT, Shea GO, Halbreich S, Stamp NE. 131.  1996. Resource availability and the trichome defenses of tomato plants. Oecologia 106:181–91 [Google Scholar]
  132. Zamora R. 132.  1995. The trapping success of a carnivorous plant, Pinguicula vallisneriifolia: the cumulative effects of availability, attraction, retention and robbery of prey. Oikos 73:309–22 [Google Scholar]
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Mirid (Hemiptera: Heteroptera) Specialists of Sticky Plants: Adaptations, Interactions, and Ecological Implications
Annual Review of Entomology 60, 393 (2015); https://doi.org/10.1146/annurev-ento-010814-020932
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