Do plant trichomes cause more harm than good to predatory insects?

Pest Management Science

Volumn 70, Issue 11, 2014, Pages 1655-1665

  Riddick, Eric W ^a   Simmons, Alvin M ^b  

^a AGRICULTURAL RESEARCH SERVICE   (United States)

^b AGRICULTURAL RESEARCH SERVICE   (United States)

Author keywords

Biocontrol; Crop protection; Host plant resistance; Natural enemies; Risk assessment

Indexed keywords

BEETLE; BIOCONTROL AGENT; BIOLOGICAL CONTROL; CROP IMPROVEMENT; CULTIVAR; HOST PLANT; MORPHOLOGY; NATURAL ENEMY; RISK ASSESSMENT; TRICHOME;

HEXAPODA;

ADVERSE EFFECTS; ANATOMY AND HISTOLOGY; ANIMAL; CROP; EGG LAYING; INSECT; PEST CONTROL; PHYSIOLOGY; PREDATION; TRICHOME;

ANIMALS; CROPS, AGRICULTURAL; INSECTS; OVIPOSITION; PEST CONTROL; PREDATORY BEHAVIOR; TRICHOMES;

EID: 84908573556     PISSN: 1526498X     EISSN: 15264998     Source Type: Journal    
DOI: 10.1002/ps.3772     Document Type: Review

References (95)

1. Lam W-KF and Pedigo LP, Effect of trichome density on soybean pod feeding by adult bean leaf beetles (Coleoptera: Chrysomelidae). J Econ Entomol 94:1459-1463 (2001).
2. Coombs JJ, Douches DS, Grafius EJ and Pett WL, Combining engineered (Bt-cry3A) and natural resistance mechanisms in potato for control of Colorado potato beetle. J Am Soc Hort Sci 127:62-68 (2002).
3. Bleeker PM, Mirabella R, Diergarde PJ, VanDoorn A, Tissier A, Kant MR et al., Improved herbivore resistance in cultivated tomato with the sesquiterpene biosynthetic pathway from a wild relative. Proc Natl Acad Sci 109:20 124-20 129 (2012).
4. Levin DA, The role of trichomes in plant defence. Q Rev Biol 48:3-15 (1973).
5. Johnson HB, Plant pubescence: an ecological perspective. Bot Rev 41:233-258 (1975).
6. Tooker JF, Peiffer M, Luthe DS and Felton GW, Trichomes as sensors: detecting activity on the leaf surface. Plant Signal Behav 5:73-75 (2010).
7. Gannon AJ and Bach CE, Effects of soybean trichome density on Mexican bean beetle (Coleoptera: Coccinellidae) development and feeding preference. Environ Entomol 25:1077-1082 (1996).
8. Andres MR and Connor EF, The community-wide and guild-specific effects of pubescence on the folivorous insects of manzanitas Arctostaphylos spp. Ecol Entomol 28:383-396 (2003).
9. Tian D, Tooker J, Peiffer M, Chung SH and Felton GW, Role of trichomes in defense against herbivores: comparison of herbivore response to woolly and hairless trichome mutants in tomato (Solanum lycopersicum). Planta 236:1053-1066 (2012).
10. Gorb EV and Gorb SN, Attachment ability of the beetle Chrysolina fastuosa on various plant surfaces. Entomol Exp Applic 105:13-28 (2002).
11. Medeiros L and Moreira GRP, Moving on hairy surfaces: modifications of Gratiana spadicea larval legs to attach on its host plant Solanum sisymbriifolium. Entomol Exp Applic 102:295-305 (2002).
12. Cardoso MZ, Herbivore handling of a plant's trichome: the case of Heliconius charithonia (L.) (Lepidoptera: Nymphalidae) and Passiflora lobata (Killip) Hutch. (Passifloraceae). Neotrop Entomol 37:247-252 (2008).
13. Johnson B, The injurious effects of the hooked epidermal hairs of French beans (Phaseolus vulgaris L.) on Aphis craccivora Koch. Bull Entomol Res 44:779-788 (1953).
14. Pillemer EA and Tingey WM, Hooked trichomes: a physical barrier to a major agricultural pest. Science 193:482-484 (1976).
15. Quiring DT, Timmins PR and Park SJ, Effect of variations in hooked trichome densities of Phaseolus vulgaris on longevity of Liriomyza trifolii (Diptera: Agromyzidae) adults. Environ Entomol 21:1357-1361 (1992).
16. Szyndler MW, Haynes KF, Potter MF, Corn RM and Loudon C, Entrapment of bed bugs by leaf trichomes inspires microfabrication of biomimetic surfaces. J R Soc Interface 10:20130174 (2013).
17. Gibson RW, Trapping of the spider mite Tetranychus urticae by glandular hairs on the wild potato Solanum berthaultii. Potato Res 19:179-182 (1976).
18. Tingey WM and Sinden SL, Glandular pubescence, glycoalkaloid composition, and resistance to the green peach aphid, potato leafhopper, and potato fleabeetle in Solanum berthaultii. Am Potato J 59:95-106 (1982).
19. Snyder JC, Simmons AM and Thacker RR, Attractancy and ovipositional response of adult Bemisia argentifolii (Homoptera: Aleyrodidae) to type IV trichome density on leaves of Lycopersicon hirsutum grown in three day-length regimes. J Entomol Sci 33:270-281 (1998).
20. Maluf WR, Campos GA and Cardoso MG, Relationships between trichome types and spider mite (Tetranychus evansi) repellence in tomatoes with respect to foliar zingiberene contents. Euphytica 121:73-80 (2001).
21. Kennedy GG, Tomato, pests, parasitoids, and predators: tritrophic interactions involving the genus Lycopersicon. Annu Rev Entomol 48:51-72 (2003).
22. Sarria E, Palomares-Rius FJ, López-Sesé AI, Heredia A and Gómez-Guillamón ML, Role of leaf glandular trichomes of melon plants in deterrence of Aphis gossypii Glover. Plant Biol 12:503-511 (2009).
23. De Ponti OMB, Romanow LR and Berlinger MJ, Whitefly-plant relationships: plant resistance, in Whiteflies: their Bionomics, Pest Status and Management, ed. by Gerling D. Intercept Ltd, Andover, Hants, UK, pp. 91-106 (1990).
24. Simmons AM and Levi A, Sources of whitefly (Homoptera: Aleyrodidae) resistance in Citrullus for the improvement of cultivated watermelon. HortScience 37:581-584 (2002).
25. Soroka JJ, Holowachuk JM, Gruber MY and Grenkow LF, Feeding by flea beetles (Coleoptera: Chrysomelidae: Phyllotreta spp.) is decreased on canola (Brassica napus) seedlings with increased trichome density. J Econ Entomol 104:125-136 (2011).
26. Wagner GJ, Wang E and Shepherd RW, New approaches for studying and exploiting an old protuberance, the plant trichome. Ann Bot 93:3-11 (2004).
27. Glas JJ, Schimmel BCJ, Alba JM, Escobar-Bravo R, Schuurink RC and Kant MR, Plant glandular trichomes as targets for breeding or engineering of resistance to herbivores. Int J Mol Sci 13:17 077-17 103 (2012).
28. Wissinger SA, Cyclic colonization in predictably ephemeral habitats: a template for biological control in annual crop systems. Biol Control 10:4-15 (1997).
29. Tscharntke T, Bommarco R, Clough Y, Crist TO, Kleijn D, Rand TA et al., Conservation biological control and enemy diversity on a landscape scale. Biol Control 43:294-309 (2007).
30. Bellows TS, Restoring population balance through natural enemy introductions. Biol Control 21:199-205 (2001).
31. Collier T and Van Steenwyk R, A critical evaluation of augmentative biological control. Biol Control 31:245-256 (2004).
32. Crowder DW, Impact of release rates on the effectiveness of augmentative biological control agents. J Insect Sci 7:15 (2007).
33. Stiling P, Biological control not on target. Biol Invasions 6:151-159 (2004).
34. Bottrell DG, Barbosa P and Gould F, Manipulating natural enemies by plant variety selection and modification: a realistic strategy? Annu Rev Entomol 43:347-367 (1998).
35. Verheggen FJ, Capella Q, Schwartzberg EG, Voigt D and Haubruge E, Tomato-aphid-hoverfly: a tritrophic interaction incompatible for pest management. Arthropod-Plant Interact 3:141-149 (2009).
36. Boethel DJ and Eikenbary RD, Interactions of Plant Resistance and Parasitoids and Predators of Insects. Ellis Horwood Ltd, Chichester, UK, 224 pp. (1986).
37. Cortesero AM, Stapel JO and Lewis WJ, Understanding and manipulating plant attributes to enhance biological control. Biol Control 17:35-49 (2000).
38. Simmons AT and Gurr GM, Trichome-based host plant resistance of Lycopersicon species and the biocontrol agent Mallada signata: are they compatible? Entomol Exp Applic 113:95-101 (2004).
39. Simmons AT and Gurr GM, Trichomes of Lycopersicon species and their hybrids: effects on pests and natural enemies. Agric For Entomol 7:265-276 (2005).
40. Riddick EW and Wu Z, Lima bean-lady beetle interactions: hooked trichomes affect survival of Stethorus punctillum larvae. BioControl 56:55-63 (2011).
41. Putman WL, Bionomics of Stethorus punctillum Weise (Coleoptera: Coccinellidae) in Ontario. Can Entomol 87:9-33 (1955).
42. Belcher DW and Thurston R, Inhibition of movement of larvae of the convergent lady beetle by leaf trichomes of tobacco. Environ Entomol 11:91-94 (1982).
43. Biddinger DJ, Toxicity, stage specificity, and sublethal effects of abamectin and several classes of insect growth regulators to Platynota idaeusalis (Lepidoptera: Tortricidae) and Stethorus punctum (Coleoptera: Coccinellidae). PhD Dissertation, Pennsylvania State University, University Park, PA (1993).
44. Ricci C and Cappelletti G, Relationship between some morphological structures and locomotion of Clitostethus arcuata Rossi (Coleoptera: Coccinellidae), a whitefly predator. Frustula Entomol 11:195-202 (1988).
45. Obrycki JJ, The influence of foliar pubescence on entomophagous species, in Interactions of Plant Resistance and Parasitoids and Predators of Insects, ed. by Boethel DJ and Eikenbary RD. Ellis Horwood Ltd, Chichester, UK, pp. 61-83 (1986).
46. Schmidt RA, Leaf structures affect predatory mites (Acari: Phytoseiidae) and biological control: a review. Exp Appl Acarol 62:1-17 (2014).
47. Obrycki JJ, Tauber MJ and Tingey WM, Predator and parasitoid interaction with aphid-resistant potatoes to reduce aphid densities: a two-year field study. J Econ Entomol 76:456-462 (1983).
48. Obrycki JJ and Tauber MJ, Natural enemy activity on glandular pubescent potato plants in the greenhouse: an unreliable predictor of success in the field. Environ Entomol 13:679-683 (1984).
49. Gamarra DC, Bueno VH, Moraes JC and Auad AM, Influence of glandular trichomes of Solanum berthaultii on the predation of Scymnus (Pullus) argentinicus (Weise) (Coleoptera: Coccinellidae) on Myzus persicae (Sulzer) (Homoptera: Aphididae) (in Portuguese). Anais Soc Entomol Brasil 27:59-65 (1998).
50. Barbour JD, Farrar RR and Kennedy GG, Interaction of Manduca sexta resistance in tomato with insect predators of Helicoverpa zea. Entomol Exp Applic 68:143-155 (1993).
51. Barbour JD, Farrar RR, Jr, and Kennedy GG, Populations of predaceous natural enemies developing on insect-resistant and susceptible tomato in North Carolina. Biol Control 9:173-184 (1997).
52. Heinz KM and Zalom FG, Performance of the predator Delphastus pusillus on Bemisia resistant and susceptible tomato lines. Entomol Exp Applic 81:345-352 (1996).
53. Shah MA, The influence of plant surfaces on the searching behaviour of coccinellid larvae. Entomol Exp Applic 31:377-380 (1982).
54. Seagraves MP and Yeargan KV, Selection and evaluation of a companion plant to indirectly augment densities of Coleomegilla maculata (Coleoptera: Coccinellidae) in sweet corn. Environ Entomol 35:1334-1341 (2006).
55. Elsey KD, Influence of plant host on searching speed of two predators. Entomophaga 19:3-6 (1974).
56. Cottrell TE and Yeargan KV, Factors influencing dispersal of larval Coleomegilla maculata from the weed Acalypha ostryaefolia to sweet corn. Entomol Exp Applic 90:313-322 (1999).
57. Griffin ML and Yeargan KV, Factors potentially affecting oviposition site selection by the lady beetle Coleomegilla maculata (Coleoptera: Coccinellidae). Environ Entomol 31:112-119 (2002).
58. Staley AC and Yeargan KV, Oviposition behavior of Coleomegilla maculata (Coleoptera: Coccinellidae): diel periodicity and choice of host plants. Environ Entomol 34:440-445 (2005).
59. Walters PJ, A method for culturing Stethorus spp. (Coleoptera: Coccinellidae) on Tetranychus urticae (Koch) (Acarina: Tetranychidae). J Aust Entomol Soc 13:245-246 (1974).
60. Biddinger DJ, Weber DC and Hull LA, Coccinellidae as predators of mites: Stethorini in biological control. Biol Control 51:268-283 (2009).
61. Dai H, Wang Y, Du Y and Ding J, Effects of plant trichomes on herbivores and predators on soybeans. Insect Sci 17:406-413 (2010).
62. Guershon M and Gerling D, Predatory behavior of Delphastus pusillus in relation to the phenotypic plasticity of Bemisia tabaci nymphs. Entomol Exp Applic 92:239-248 (1999).
63. Guershon M and Gerling D, Effects of plant and prey characteristics on the predatory behavior of Delphastus catalinae. Entomol Exp Applic 121:15-21 (2006).
64. Gurney B and Hussey NW, Evaluation of some coccinellid species for biological control of aphids in protected cropping. Ann Appl Biol 65:451-458 (1970).
65. Hoelmer KA and Pickett CH, Geographic origin and taxonomic history of Delphastus spp. (Coleoptera: Coccinellidae) in commercial culture. Biocontrol Sci Technol 13:529-535 (2003).
66. Heinz KM and Parrella MP, Poinsetta (Euphorbia pulcherrima Willd. ex Koltz.) cultivar-mediated differences in performance of five natural enemies of Bemisia argentifolii Bellows and Perring, n. sp. (Homoptera: Aleyrodidae). Biol Control 4:305-318 (1994).
67. Lucas E, Labrecque C and Coderre D, Delphastus catalinae and Coleomegilla maculata lengi (Coleoptera: Coccinellidae) as biological control agents of greenhouse whitefly, Trialeurodes vaporariorum (Homoptera: Aleyrodidae). Pest Manag Sci 60:1073-1078 (2004).
68. Eisner T, Eisner M and Hoebeke ER, When defense backfires: detrimental effect of a plant's protective trichomes on an insect beneficial to the plant. Proc Natl Acad Sci USA 95:4410-4414 (1998).
69. Marler TE, Boomeranging in structural defense: phytophagous insect uses cycad trichomes to defend against entomophagy. Plant Signal Behav 7:1484-1487 (2012).
70. Coll M and Ridgway RL, Functional and numerical responses of Orius insidiosus (Heteroptera: Anthocoridae) to its prey in different vegetable crops. Ann Entomol Soc Am 88:732-738 (1995).
71. Coll M, Smith LA and Ridgway RL, Effect of plants on the searching efficiency of a generalist predator: the importance of predator-prey spatial association. Entomol Exp Applic 83:1-10 (1997).
72. Economou LP, Lykouressis DP and Barbetaki AE, Time allocation of activities of two heteropteran predators on the leaves of three tomato cultivars with variable glandular trichome density. Environ Entomol 35:387-393 (2006).
73. Lambert AM, Effect of prey availability, facultative plant feeding, and plant defenses on a generalist insect predator. Arthropod-Plant Interact 1:167-173 (2007).
74. De Clercq P, Mohaghegh J and Tirry L, Effect of host plant on the functional response of the predator Podisus nigrispinus (Heteroptera: Pentatomidae). Biol Control 18:65-70 (2000).
75. Weinhold A and Baldwin IT, Trichome-derived O-acyl sugars are a first meal for caterpillars that tags them for predation. Proc Natl Acad Sci USA 108:7855-7859 (2011).
76. Gassmann AJ and Hare JD, Indirect cost of a defensive trait: variation in trichome type affects the natural enemies of herbivorous insects on Datura wrightii. Oecologia 144:62-71 (2005).
77. van Dam NM and Hare JD, Differences in distribution and performance of two sap-sucking herbivores on glandular and non-glandular Datura wrightii. Ecol Entomol 23:22-32 (1998).
78. Lundgren JG, Fergen JK and Riedell WE, The influence of plant anatomy on oviposition and reproductive success of the omnivorous bug Orius insidiosus. Anim Behav 75:1495-1502 (2008).
79. Powell JE and Lambert L, Soybean genotype effects on bigeyed bug feeding on corn earworm in the laboratory. Crop Sci 33:556-559 (1993).
80. Laycock A, Camm E, Van Laerhoven S and Gillespie D, Cannibalism in a zoophytophagous omnivore is mediated by prey availability and plant substrate. J Insect Behav 19:219-229 (2006).
81. Björkman C and Ahrné K, Influence of leaf trichome density on the efficiency of two polyphagous insect predators. Entomol Exp Applic 115:179-186 (2005).
82. Björkman C and Liman A-S, Foraging behaviour influences the outcome of predator-predator interactions. Ecol Entomol 30:164-169 (2005).
83. Simmons AT and Gurr GM, The effect of the biological control agent Mallada signata of trichomes of F1 Lycopersicon esculentum × L. cheesmanii f. minor and L. pennellii hybrids. Biol Control 38:174-178 (2006).
84. Rao RSN and Chandra IJ, Brinckochrysa scelestes (Neur.: Chrysopidae) as predator of Myzus persicae (Hom.: Aphididae) on tobacco. Entomophaga 29:283-285 (1984).
85. Santos TM, Boiça Júnior AL and Soares JJ, Influence of cotton trichomes on biological aspects and predatory ability of Chrysoperla externa (Hagen) fed with Aphis gossypii Glover (in Portuguese). Bragantia 62:243-254 (2003).
86. Treacy MF, Zummo GR and Benedict JH, Interactions of host plant resistance in cotton with predators and parasites. Agric Ecosyst Environ 13:151-157 (1985).
87. Treacy MF, Benedict JH, Lopez JD and Morrison RK, Functional response of a predator (Neuroptera: Chrysopidae) to bollworm (Lepidoptera: Noctuidae) eggs on smoothleaf, hirsute, and pilose cottons. J Econ Entomol 80:376-379 (1987).
88. Fordyce JA and Agrawal AA, The role of plant trichomes and caterpillar group size on growth and defence of the pipevine swallowtail Battus philenor. J Anim Ecol 70:997-1005 (2001).
89. Eisner T, Carrel JE, Tassel EV, Hoebeke ER and Eisner M, Construction of a defensive trash packet from sycamore leaf trichomes by a chrysopid larva (Neuroptera: Chrysopidae). Proc Entomol Soc Wash 104:437-446 (2002).
90. Styrsky JD, Kaplan I and Eubanks MD, Plant trichomes indirectly enhance tritrophic interactions involving a generalist predator, the red imported fire ant. Biol Control 36:375-384 (2006).
91. Lucas E and Brodeur J, Oviposition site selection by the predatory midge Aphidoletes aphidimyza (Diptera: Cecidomyiidae). Environ Entomol 28:622-627 (1999).
92. Sengonca C and Gerlach S, Einfluss der Blattoberfläche auf die Wirksamkeit des räuberischen thrips, Scolothrips longicornis (Thysan.: Thripidae). Entomophaga 29:55-61 (1984).
93. Voigt D, Gorb E and Gorb S, Plant surface-bug interactions: Dicyphus errans stalking along trichomes. Arthropod-Plant Interact 1:221-243 (2007).
94. Voigt D and Gorb S, 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 211:2647-2657 (2008).
95. Voigt D and Gorb S, Locomotion in a sticky terrain. Arthropod-Plant Interact 4:69-79 (2010).