1932

Abstract

Plant susceptibility to herbivore attack is determined not just by the suite of defenses present in different tissues of the plant, but also by the capabilities of the herbivore for tolerating, circumventing, or disarming the defenses. This article reviews the elaborate behaviors exhibited by leaf-chewing insects that appear to function specifically to deactivate hostplant defenses. Shortcomings in our understanding and promising areas for future research are highlighted. Behaviors covered include vein cutting, trenching, girdling, leaf clipping, and application of fluids from exocrine glands. Many of these behaviors have a widespread distribution, having evolved independently in multiple insect lineages. Insects utilizing the behaviors include significant agricultural, horticultural, and forestry pests, as well as numerous species important in natural ecosystems. Behavioral, ecological, and phylogenetic studies have documented the importance of the behaviors and their ancient history, but the molecular analysis of how the behaviors affect plant physiology has scarcely begun.

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2017-01-31
2025-02-13
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Literature Cited

  1. Abarca M, Boege K. 1.  2011. Fitness costs and benefits of shelter building and leaf trenching behaviour in a pyralid caterpillar. Ecol. Entomol. 36564–73 [Google Scholar]
  2. Abarca M, Boege K, Zaldívar-Riverón A. 2.  2014. Shelter-building behavior and natural history of two pyralid caterpillars feeding on Piper stipulaceum. J. Insect Sci. 1439 [Google Scholar]
  3. Acevedo FE, Rivera-Vega LJ, Chung SH, Ray S, Felton GW. 3.  2015. Cues from chewing insects—the intersection of DAMPs, HAMPs, MAMPs and effectors. Curr. Opin. Plant Biol. 26:80–86 [Google Scholar]
  4. Agrawal AA, Ali JG, Rasmann S, Fishbein M. 4.  2015. Macroevolutionary trends in the defense of milkweeds against monarchs. Monarchs in a Changing World: Biology and Conservation of an Iconic Butterfly KS Oberhauser, KR Nail, S Altizer 47–59 Ithaca, NY: Cornell Univ. Press [Google Scholar]
  5. Agrawal AA, Konno K. 5.  2009. Latex: a model for understanding mechanisms, ecology, and evolution of plant defense against herbivory. Annu. Rev. Ecol. Evol. Syst. 40311–31 [Google Scholar]
  6. Agrawal AA, Lajeunesse MJ, Fishbein M. 6.  2008. Evolution of latex and its constituent defensive chemistry in milkweeds (Asclepias): a phylogenetic test of plant defense escalation. Entomol. Exp. Appl. 128:126–38 [Google Scholar]
  7. Agrawal AA, Petschenka G, Bingham RA, Weber MG, Rasmann S. 7.  2012. Toxic cardenolides: chemical ecology and coevolution of specialized plant-herbivore interactions. New Phytol 194:28–45 [Google Scholar]
  8. Akino T. 8.  2005. Chemical and behavioral study on the phytomimetic giant geometer Biston robustum Butler (Lepidoptera: Geometridae). Appl. Entomol. Zool. 40497–505 [Google Scholar]
  9. Albanese G, Nelson MW, Vickery PD, Sievert PR. 9.  2007. Larval feeding behavior and ant association in frosted elfin, Callophrys irus (Lycaenidae). J. Lepid. Soc. 6161–66 [Google Scholar]
  10. Alexander AJ. 10.  1961. A study of the biology and behavior of the caterpillars, pupae and emerging butterflies of the subfamily Heliconiinae in Trinidad, West Indies. Part 1. Some aspects of larval behavior. Zoologica 461–24 [Google Scholar]
  11. Altizer S, de Roode JC. 11.  2015. Monarchs and their debilitating parasites. Monarchs in a Changing World: Biology and Conservation of an Iconic Butterfly KS Oberhauser, KR Nail, S Altizer 83–93 Ithaca, NY: Cornell Univ. Press [Google Scholar]
  12. Andersen PC, Brodbeck BV, Herzog DC. 12.  2002. Girdling-induced nutrient accumulation in above ground tissue of peanuts and subsequent feeding by Spissistilus festinus, the three-cornered alfalfa hopper. Entomol. Exp. Appl. 103:139–49 [Google Scholar]
  13. Appel HM, Arnold TM, Schultz JC. 13.  2012. Effects of jasmonic acid, branching and girdling on carbon and nitrogen transport in poplar. New Phytol 195:419–26 [Google Scholar]
  14. Arnold T, Appel H, Patel V, Stocum E, Kavalier A, Schultz J. 14.  2004. Carbohydrate translocation determines the phenolic content of Populus foliage: a test of the sink-source model of plant defense. New Phytol 164:157–64 [Google Scholar]
  15. Attygalle AB, Smedley SR, Meinwald J, Eisner T. 15.  1993. Defensive secretion of two notodontid caterpillars (Schizura unicornis, S. badia). J. Chem. Ecol. 19:2089–104 [Google Scholar]
  16. Barton KE. 16.  2014. Prickles, latex, and tolerance in the endemic Hawaiian prickly poppy (Argemone glauca): variation between populations, across ontogeny, and in response to abiotic factors. Oecologia 174:1273–81 [Google Scholar]
  17. Bauer G, Friedrich C, Gillig C, Vollrath F, Speck T, Holland C. 17.  2014a. Investigating the rheological properties of native plant latex. J. R. Soc. Interface 1120130847 [Google Scholar]
  18. Bauer G, Gorb SN, Klein M-C, Nellesen A, von Tapavicza M, Speck T. 18.  2014b. Comparative study on plant latex particles and latex coagulation in Ficus benjamina, Campanula glomerata and three Euphorbia species. PLOS ONE 911e113336 [Google Scholar]
  19. Becerra JX. 19.  1994. Squirt-gun defense in Bursera and the chrysomelid counterploy. Ecology 751991–96 [Google Scholar]
  20. Becerra JX. 20.  1997. Insects on plants: macroevolutionary chemical trends in host use. Science 276:253–56 [Google Scholar]
  21. Becerra JX. 21.  2003. Synchronous coadaptation in an ancient case of herbivory. PNAS 100:12804–7 [Google Scholar]
  22. Becerra JX, Venable DL. 22.  1999. Macroevolution of insect-plant associations: the relevance of host biogeography to host affiliation. PNAS 9612626–31 [Google Scholar]
  23. Becerra JX, Venable DL, Evans PH, Bowers WS. 23.  2001. Interactions between chemical and mechanical defenses in the plant genus Bursera and their implications for herbivores. Am. Zool. 41865–76 [Google Scholar]
  24. Bede JC, Musser RO, Felton GW, Korth KL. 24.  2006. Caterpillar herbivory and salivary enzymes decrease transcript levels of Medicago truncatula genes encoding early enzymes in terpenoid biosynthesis. Plant Mol. Biol. 60519–31 [Google Scholar]
  25. Bernays EA. 25.  1997. Feeding by lepidopteran larvae is dangerous. Ecol. Entomol. 22:121–23 [Google Scholar]
  26. Bernays EA, Singer MS, Rodrigues D. 26.  2004. Foraging in nature: foraging efficiency and attentiveness in caterpillars with different diet breadths. Ecol. Entomol. 29:389–97 [Google Scholar]
  27. Bernays EA, Singer MS, Rodrigues D. 27.  2004. Trenching behavior by caterpillars of the Euphorbia specialist, Pygarctia roseicapitis: a field study. J. Insect Behav. 17:41–52 [Google Scholar]
  28. Braswell WE, Ott JR. 28.  2000. The biology of Doa ampla (Grote) (Lepidoptera: Doidae) on its hostplant Stillingia texana (Euphorbiaceae). Proc. Entomol. Soc. Wash. 102:507–18 [Google Scholar]
  29. Brown KS Jr. 29.  1981. The biology of Heliconius and related genera. Annu. Rev. Entomol. 26:427–56 [Google Scholar]
  30. Call VB, Dilcher DL. 30.  1997. The fossil record of Eucommia (Eucommiaceae) in North America. Am. J. Bot. 84798–814 [Google Scholar]
  31. Canaveze Y, Machado SR. 31.  2016. The occurrence of intrusive growth associated with articulated laticifers in Tabernaemontana catharinensis A.DC., a new record for Apocynaceae. Int. J. Plant Sci. 177:458–67 [Google Scholar]
  32. Carroll CR, Hoffman CA. 32.  1980. Chemical feeding deterrent mobilized in response to insect herbivory and counteradaptation by Epilachna tredecimnotata. Science 209:414–16 [Google Scholar]
  33. Chambers JLE, Berenbaum MR, Zangerl AR. 33.  2007. Benefits of trenching behavior in the context of an inducible defense. Chemoecology 17:125–30 [Google Scholar]
  34. Chen Y, Duan J, Yang S, Yang E, Jiang Y. 34.  2009. Effect of girdling on levels of catechins in fresh leaf in relation to quality of ‘Huang Zhi Xiang’ Oolong tea. Plant Foods Hum. Nutr. 64293–96 [Google Scholar]
  35. Cho WK, Jo Y, Chu H, Park SH, Kim KH. 35.  2014. Integration of latex protein sequence data provides comprehensive functional overview of latex proteins. Mol. Biol. Rep. 411469–81 [Google Scholar]
  36. Clarke AR, Zalucki MP. 36.  2000. Foraging and vein-cutting behaviour of Euploea core corinna (W. S. Macleay) (Lepidoptera: Nymphalidae) caterpillars feeding on latex-bearing leaves. Aust. J. Entomol 39:283–90 [Google Scholar]
  37. Cohen JA. 37.  1983. Chemical interactions among milkweed plants (Asclepiadaceae) and lepidopteran herbivores PhD Thesis, Univ. Florida [Google Scholar]
  38. Compton SG. 38.  1987. Aganais speciosa and Danaus chrysippus (Lepidoptera) sabotage the latex defences of their host plants. Ecol. Entomol. 12:115–18 [Google Scholar]
  39. Compton SG. 39.  1989. Sabotage of latex defences by caterpillars feeding on fig trees. S. Afr. J. Sci. 85:605–6 [Google Scholar]
  40. Darling C. 40.  2007. Holey aroids: circular trenching behavior by a leaf beetle in Vietnam. Biotropica 39:555–58 [Google Scholar]
  41. Dehgan B, Craig ME. 41.  1978. Types of laticifers and crystals in Jatropha and their taxonomic implications. Am. J. Bot. 65:345–52 [Google Scholar]
  42. Delaney KJ. 42.  2008. Injured and uninjured leaf photosynthetic responses after mechanical injury on Nerium oleander leaves, and Danaus plexippus herbivory on Asclepias curassavica leaves. Plant Ecol. 199:187–200 [Google Scholar]
  43. Delaney KJ, Higley LG. 43.  2006. An insect countermeasure impacts plant physiology: midrib vein cutting, defoliation and leaf photosynthesis. Plant Cell Environ. 29:1245–58 [Google Scholar]
  44. Delphia CM, Mescher MC, Felton GW, De Moraes CM. 44.  2006. The role of insect-derived cues in eliciting indirect plant defenses in tobacco, Nicotiana tabacum. Plant Signal. Behav. 1243–50 [Google Scholar]
  45. Demarco D, Castro MDM. 45.  2008. Laticíferos articulados anastomosados em espécies de Asclepiadeae (Asclepiadoideae, Apocynaceae) e suas implicações ecológicas [Articulated anastomosing laticifers in species of Asclepiadeae (Asclepiadoideae, Apocynaceae) and their ecological significance]. Rev. Bras. Bot. 31701–13 [Google Scholar]
  46. Demarco D, Castro MDM, Ascensão L. 46.  2013. Two laticifer systems in Sapium haematospermum—new records for Euphorbiaceae. Botany 91545–54 [Google Scholar]
  47. Demarco D, Kinoshita LS, Castro MDM. 47.  2006. Laticíferos articulados anastomosados—novos registros para Apocynaceae [Articulated anastomosing laticifers—new records for Apocynaceae]. Rev. Bras. Bot. 29:133–44 [Google Scholar]
  48. Denno RF, McClure MS. 48.  1983. Variable Plants and Herbivores in Natural and Managed Systems New York: Academic [Google Scholar]
  49. Dillon PM, Lowrie S, McKey D. 49.  1983. Disarming the “Evil Woman”: petiole constriction by a sphingid larva circumvents mechanical defenses of its host plant, Cnidoscolus urens (Euphorbiaceae). Biotropica 15:112–16 [Google Scholar]
  50. Dobler S, Petschenka G, Wagschal V, Flacht L. 50.  2015. Convergent adaptive evolution—how insects master the challenge of cardiac glycoside-containing host plants. Entomol. Exp. Appl. 157:30–39 [Google Scholar]
  51. Dussourd DE. 51.  1993. Foraging with finesse: caterpillar adaptations for circumventing plant defenses. Caterpillars: Ecological and Evolutionary Constraints on Foraging NE Stamp, TM Casey 92–131 New York: Chapman and Hall [Google Scholar]
  52. Dussourd DE. 52.  1995. Entrapment of aphids and whiteflies in lettuce latex. Ann. Entomol. Soc. Am. 88163–72 [Google Scholar]
  53. Dussourd DE. 53.  1997. Plant exudates trigger leaf-trenching by cabbage loopers, Trichoplusia ni (Noctuidae). Oecologia 112:362–69 [Google Scholar]
  54. Dussourd DE. 54.  1999. Behavioral sabotage of plant defense: Do vein cuts and trenches reduce insect exposure to exudate?. J. Insect Behav. 12:501–15 [Google Scholar]
  55. Dussourd DE. 55.  2003. Chemical stimulants of leaf-trenching by cabbage loopers: natural products, neurotransmitters, insecticides, and drugs. J. Chem. Ecol. 29:2023–47 [Google Scholar]
  56. Dussourd DE. 56.  2005. In the trenches: bioprospecting with a caterpillar probe. Wings: Essays Invertebr. Conserv. 28:20–24 [Google Scholar]
  57. Dussourd DE. 57.  2009. Do canal-cutting behaviors facilitate host-range expansion by insect herbivores?. Biol. J. Linn. Soc. 96715–31 [Google Scholar]
  58. Dussourd DE. 58.  2015. Theroa zethus caterpillars use acid secretion of anti-predator gland to deactivate plant defense. PLOS ONE 1010e0141924 [Google Scholar]
  59. Dussourd DE, Denno RF. 59.  1991. Deactivation of plant defense: correspondence between insect behavior and secretory canal architecture. Ecology 721383–96 [Google Scholar]
  60. Dussourd DE, Denno RF. 60.  1994. Host range of generalist caterpillars: trenching permits feeding on plants with secretory canals. Ecology 7569–78 [Google Scholar]
  61. Dussourd DE, Eisner T. 61.  1987. Vein-cutting behavior: insect counterploy to the latex defense of plants. Science 237:898–901 [Google Scholar]
  62. Dussourd DE, Hoyle AM. 62.  2000. Poisoned plusiines: toxicity of milkweed latex and cardenolides to some generalist caterpillars. Chemoecology 10:11–16 [Google Scholar]
  63. Dussourd DE, Peiffer M, Felton GW. 63.  2016. Chew and spit: tree-feeding notodontid caterpillars anoint girdles with saliva. Arthropod-Plant Interact 10:143–50 [Google Scholar]
  64. Edwards PB, Wanjura WJ. 64.  1989. Eucalypt-feeding insects bite off more than they can chew: sabotage of induced defenses?. Oikos 54246–48 [Google Scholar]
  65. Eichenseer H, Mathews MC, Powell JS, Felton GW. 65.  2010. Survey of a salivary effector in caterpillars: glucose oxidase variation and correlation with host range. J. Chem. Ecol. 36885–97 [Google Scholar]
  66. Elpino-Campos A. 66.  2012. Feeding behavior of Heliconius erato phyllis (Fabricius) (Lepidoptera: Nymphalidae) larvae on passion vines. Acta Ethol 15:107–18 [Google Scholar]
  67. Endress ME, Liede-Schumann S, Meve U. 67.  2014. An updated classification for Apocynaceae. Phytotaxa 159:175–94 [Google Scholar]
  68. Fahn A. 68.  1979. Secretory Tissues in Plants New York: Academic [Google Scholar]
  69. Farmer EE. 69.  2014. Leaf Defence Oxford, UK: Oxford Univ. Press [Google Scholar]
  70. Farrell BD, Dussourd DE, Mitter C. 70.  1991. Escalation of plant defense: Do latex and resin canals spur plant diversification?. Am. Nat. 138:881–900 [Google Scholar]
  71. Farrell BD, Mitter C. 71.  1998. The timing of insect/plant diversification: Might Tetraopes (Coleoptera: Cerambycidae) and Asclepias (Asclepiadaceae) have co-evolved?. Biol. J. Linn. Soc. 63553–77 [Google Scholar]
  72. Felton GW. 72.  2008. Caterpillar secretions and induced plant responses. Induced Plant Resistance to Herbivory A Schaller 369–87 Berlin: Springer [Google Scholar]
  73. Felton GW, Chung SH, Hernandez MGE, Louis J, Peiffer M, Tian D. 73.  2014. Herbivore oral secretions are the first line of protection against plant-induced defences. Annual Plant Reviews Vol. 47: Insect-Plant Interactions C Voelckel, G Jander 37–76 Oxford, UK: Wiley [Google Scholar]
  74. Ferreira PPS, Rodrigues D. 74.  2015. Sabotaging behavior and decision-making in larvae of the Queen butterfly Danaus gilippus. J. Insect Behav. 28:460–72 [Google Scholar]
  75. Fiehn O. 75.  2003. Metabolic networks of Cucurbita maxima phloem. Phytochem 62875–86 [Google Scholar]
  76. Fitzgerald TD. 76.  1995. Caterpillars roll their own. Nat. Hist. 10430–37 [Google Scholar]
  77. Ganong CN, Dussourd DE, Swanson J-D. 77.  2012. Girdling by notodontid caterpillars: distribution and occurrence. Arthropod-Plant Interact 6621–33 [Google Scholar]
  78. Gaupels F, Ghirardo A. 78.  2013. The extrafascicular phloem is made for fighting. Front. Plant Sci. 4187 [Google Scholar]
  79. Goren R, Huberman M, Goldschmidt EE. 79.  2004. Girdling: physiological and horticultural aspects. Hortic. Rev. 301–36 [Google Scholar]
  80. Green ES, Zangerl AR, Berenbaum MR. 80.  2001. Effects of phytic acid and xanthotoxin on growth and detoxification in caterpillars. J. Chem. Ecol. 27:1763–73 [Google Scholar]
  81. Hagel JM, Yeung EC, Facchini PJ. 81.  2008. Got milk? The secret life of laticifers. Trends Plant Sci 13:631–39 [Google Scholar]
  82. Heinrich B. 82.  1971. The effect of leaf geometry on the feeding behaviour of the caterpillar of Manduca sexta (Sphingidae). Anim. Behav. 19:119–24 [Google Scholar]
  83. Heinrich B, Collins SL. 83.  1983. Caterpillar leaf damage, and the game of hide-and-seek with birds. Ecology 64592–602 [Google Scholar]
  84. Helmus MR, Dussourd DE. 84.  2005. Glues or poisons: Which triggers vein cutting by monarch caterpillars?. Chemoecology 15:45–49 [Google Scholar]
  85. Herrick GW, Detwiler JD. 85.  1919. Notes on the repugnatorial glands of certain notodontid caterpillars. Ann. Entomol. Soc. Am. 12:44–48 [Google Scholar]
  86. Hilker M, Fatouros NE. 86.  2015. Plant responses to insect egg deposition. Annu. Rev. Entomol. 60493–515 [Google Scholar]
  87. Hilker M, Meiners T. 87.  2010. How do plants “notice” attack by herbivorous arthropods?. Biol. Rev. 85267–80 [Google Scholar]
  88. Hölldobler B, Wilson EO. 88.  2011. The Leafcutter Ants: Civilization by Instinct New York: Norton [Google Scholar]
  89. Huber M, Triebwasser-Freese D, Reichelt M, Heiling S, Paetz C. 89.  et al. 2015. Identification, quantification, spatiotemporal distribution and genetic variation of major latex secondary metabolites in the common dandelion (Taraxacum officinale agg.). Phytochemistry 115:89–98 [Google Scholar]
  90. Hulley PE. 90.  1988. Caterpillar attacks plant mechanical defence by mowing trichomes before feeding. Ecol. Entomol. 13:239–41 [Google Scholar]
  91. Hurley KW, Dussourd DE. 91.  2015. Toxic geranium trichomes trigger vein cutting by soybean loopers, Chrysodeixis includens (Lepidoptera: Noctuidae). Arthropod-Plant Interact. 933–43 [Google Scholar]
  92. Kant MR, Jonckheere W, Knegt B, Lemos F, Liu J. 92.  et al. 2015. Mechanisms and ecological consequences of plant defence induction and suppression in herbivore communities. Ann. Bot. 115:1015–51 [Google Scholar]
  93. Karban R. 93.  2011. The ecology and evolution of induced resistance against herbivores. Funct. Ecol. 25:339–47 [Google Scholar]
  94. Karban R, Agrawal AA. 94.  2002. Herbivore offense. Annu. Rev. Ecol. Syst. 33641–64 [Google Scholar]
  95. Kehr J. 95.  2006. Phloem sap proteins: their identities and potential roles in the interaction between plants and phloem-feeding insects. J. Exp. Bot. 57767–74 [Google Scholar]
  96. Klok CJ, Chown SL. 96.  1999. Assessing the benefits of aggregation: thermal biology and water relations of anomalous Emperor Moth caterpillars. Funct. Ecol. 13:417–27 [Google Scholar]
  97. Kobayashi C, Okuyama Y, Kawazoe K, Kato M. 97.  2012. The evolutionary history of maternal plant-manipulation and larval feeding behaviours in attelabid weevils (Coleoptera; Curculionoidea). Mol. Phylogenet. Evol. 64318–30 [Google Scholar]
  98. Konno K. 98.  2011. Plant latex and other exudates as plant defense systems: roles of various defense chemicals and proteins contained therein. Phytochemistry 721510–30 [Google Scholar]
  99. Konno K, Hirayama C, Nakamura M, Tateishi K, Tamura Y et al.99.  2004. Papain protects papaya trees from herbivorous insects: role of cysteine proteases in latex. Plant J 37370–78 [Google Scholar]
  100. Labandeira CC, Dilcher DL, Davis DR, Wagner DL. 100.  1994. Ninety-seven million years of angiosperm-insect association: paleobiological insights into the meaning of coevolution. PNAS 9112278–82 [Google Scholar]
  101. Langenheim JH. 101.  1990. Plant resins. Am. Sci. 7816–24 [Google Scholar]
  102. Langenheim JH. 102.  2003. Plant Resins: Chemistry, Evolution, Ecology, and Ethnobotany Portland, OR: Timber Press [Google Scholar]
  103. Lewinsohn TM. 103.  1991. The geographical distribution of plant latex. Chemoecology 264–68 [Google Scholar]
  104. Lewinsohn TM, Vasconcellos-Neto J. 104.  2000. Como insetos sabotam defesas de plantas: o caso do látex. Ecologia e Comportamento de Insetos RP Martins, TM Lewinsohn, MS Barbeitos 281–98 Série Oecologia Brasiliensis VIII Rio de Janeiro, Brazil: PPGE-UFRJ [Google Scholar]
  105. Lewis PA, Metcalf RL. 105.  1996. Behavior and ecology of Old World Luperini beetles of the genus Aulacophora (Coleoptera: Chrysomelidae). Chemoecology 7:150–55 [Google Scholar]
  106. Lill JT, Marquis RJ. 106.  2007. Microhabitat manipulation: ecosystem engineering by shelter-building insects. Ecosystem Engineers: Plants to Protists K Cuddington, JE Byers, WG Wilson, A Hastings 107–38 New York: Academic [Google Scholar]
  107. Lin MK, Lee YJ, Lough TJ, Phinney BS, Lucas WJ. 107.  2009. Analysis of the pumpkin phloem proteome provides insights into angiosperm sieve tube function. Mol. Cell. Proteom. 8343–56 [Google Scholar]
  108. MacGibbon DB, Mann JD. 108.  1986. Inhibition of animal and pathogenic fungal proteases by phloem exudate from pumpkin fruits (Cucurbitaceae). J. Sci. Food Agric. 37515–22 [Google Scholar]
  109. Mahlberg PG. 109.  1961. Embryogeny and histogenesis in Nerium oleander. II. Origin and development of the non-articulated laticifer. Am. J. Bot. 4890–99 [Google Scholar]
  110. Mahlberg PG, Field DW, Frye JS. 110.  1984. Fossil laticifers from Eocene brown coal deposits of the Geiseltal. Am. J. Bot. 711192–200 [Google Scholar]
  111. Malcolm SB. 111.  1991. Cardenolide-mediated interactions between plants and herbivores. Herbivores: Their Interactions with Secondary Plant Metabolites. Vol. I. The Chemical Participants GA Rosenthal, MR Berenbaum 251–96 New York: Academic [Google Scholar]
  112. McCloud ES, Tallamy DW, Halaweish FT. 112.  1995. Squash beetle trenching behaviour: avoidance of cucurbitacin induction or mucilaginous plant sap?. Ecol. Entomol. 20:51–59 [Google Scholar]
  113. Mescher MC, De Moraes CM. 113.  2014. The role of plant sensory perception in plant–animal interactions. J. Exp. Bot. 66425–33 [Google Scholar]
  114. Musser RO, Hum-Musser SM, Eichenseer H, Peiffer M, Ervin G. 114.  et al. 2002. Caterpillar saliva beats plant defenses. Nature 416:599–600 [Google Scholar]
  115. Nitao JK, Zangerl AR. 115.  2004. Microwave-facilitated extraction of furanocoumarins onto paper substrates: an imaging technique to analyse spatial distribution and abundance in leaves. Phytochem. Anal. 15:262–66 [Google Scholar]
  116. Onoyovwe A, Hagel JM, Chen X, Khan MF, Schriemer DC, Facchini PJ. 116.  2013. Morphine biosynthesis in opium poppy involves two cell types: sieve elements and laticifers. Plant Cell 254110–22 [Google Scholar]
  117. Oppel CB, Dussourd DE, Garimella U. 117.  2009. Visualizing a plant defense and insect counterploy: alkaloid distribution in Lobelia leaves trenched by a plusiine caterpillar. J. Chem. Ecol. 35625–34 [Google Scholar]
  118. Ota E, Tsuchiya W, Yamazaki T, Nakamura M, Hirayama C, Konno K. 118.  2013. Purification, cDNA cloning and recombinant protein expression of a phloem lectin-like anti-insect defense protein BPLP from the phloem exudate of the wax gourd, Benincasa hispida. Phytochemistry 8915–25 [Google Scholar]
  119. Paro CM, Arab A, Vasconcellos-Neto J. 119.  2014. Specialization of Atlantic rain forest twig-girdler beetles (Cerambycidae: Lamiinae: Onciderini): variation in host–plant use by microhabitat specialists. Arthropod-Plant Interact 8557–69 [Google Scholar]
  120. Perkins LE, Cribb BW, Brewer PB, Hanan J, Grant M. 120.  et al. 2013. Generalist insects behave in a jasmonate-dependent manner on their host plants, leaving induced areas quickly and staying longer on distant parts. Proc. R. Soc. B 28020122646 [Google Scholar]
  121. Petschenka G, Agrawal AA. 121.  2015. Milkweed butterfly resistance to plant toxins is linked to sequestration, not coping with a toxic diet. Proc. R. Soc. B 28220151865 [Google Scholar]
  122. Pickard WF. 122.  2008. Laticifers and secretory ducts: two other tube systems in plants. New Phytol 177:877–88 [Google Scholar]
  123. Ralph SG. 123.  2009. Studying Populus defenses against insect herbivores in the post-genomic era. Crit. Rev. Plant Sci. 28:335–45 [Google Scholar]
  124. Rasmann S, Johnson MD, Agrawal AA. 124.  2009. Induced responses to herbivory and jasmonate in three milkweed species. J. Chem. Ecol. 351326–34 [Google Scholar]
  125. Rhoades DF. 125.  1983. Herbivore population dynamics and plant chemistry. Variable Plants and Herbivores in Natural and Managed Systems RF Denno, MS McClure 155–220 New York: Academic [Google Scholar]
  126. Rhoades DF. 126.  1985. Offensive-defensive interactions between herbivores and plants: their relevance in herbivore population dynamics and ecological theory. Am. Nat. 125:205–38 [Google Scholar]
  127. Richards AM, Filewood LW. 127.  1990. Feeding behaviour and food preferences of the pest species comprising the Epilachna vigintioctopunctata (F.) complex (Col., Coccinellidae). J. Appl. Entomol. 110:501–15 [Google Scholar]
  128. Risley LS. 128.  1986. The influence of herbivores on seasonal leaf-fall: premature leaf abscission and petiole clipping. J. Agri. Entomol. 3152–62 [Google Scholar]
  129. Risley LS, Crossley DA Jr. 129.  1988. Herbivore-caused greenfall in the southern Appalachians. Ecology 691118–27 [Google Scholar]
  130. Robbers JE, Speedie MK, Tyler VE. 130.  1996. Pharmacognosy and pharmacobiotechnology Baltimore, MD: Williams and Wilkins [Google Scholar]
  131. Robertson NR. 131.  1996. Reduced water potential in cucumber: effect on exudation of defensive secretions and on caterpillar growth MS Thesis, Univ. Central Arkansas [Google Scholar]
  132. Rodrigues D, Maia PHS, Trigo JR. 132.  2010. Sabotaging behaviour and minimal latex of Asclepias curassavica incur no cost for larvae of the southern monarch butterfly Danaus erippus. Ecol. Entomol. 35504–13 [Google Scholar]
  133. Roslin T, Syrjälä H, Roland J, Harrison PJ, Fownes S, Matter SF. 133.  2008. Caterpillars on the run—induced defences create spatial patterns in host plant damage. Ecography 31335–47 [Google Scholar]
  134. Rudall PJ. 134.  1987. Laticifers in Euphorbiaceae—a conspectus. Bot. J. Linn. Soc. 94143–63 [Google Scholar]
  135. Schintlmeister A. 135.  2013. Notodontidae and Oenosandridae (Lepidoptera) Boston: Brill [Google Scholar]
  136. Schultz JC. 136.  1983. Habitat selection and foraging tactics of caterpillars in heterogeneous trees. Variable Plants and Herbivores in Natural and Managed Systems RF Denno, MS McClure 61–90 New York: Academic [Google Scholar]
  137. Scriber JM. 137.  1996. Tiger tales: natural history of native North American swallowtails. Am. Entomol. 4219–22 [Google Scholar]
  138. Seiber JN, Tuskes PM, Brower LP, Nelson CJ. 138.  1980. Pharmacodynamics of some individual milkweed cardenolides fed to larvae of the monarch butterfly (Danaus plexippus L.). J. Chem. Ecol. 6321–39 [Google Scholar]
  139. Singer MS, Bernays EA, Carrière Y. 139.  2002. The interplay between nutrient balancing and toxin dilution in foraging by a generalist insect herbivore. Anim. Behav. 64629–43 [Google Scholar]
  140. Singer MS, Mason PA, Smilanich AM. 140.  2014. Ecological immunology mediated by diet in herbivorous insects. Integr. Comp. Biol. 54913–21 [Google Scholar]
  141. Spencer KC. 141.  1988. Chemical mediation of coevolution in the Passiflora–Heliconius interaction. Chemical Mediation of Coevolution KC Spencer 167–40 New York: Academic [Google Scholar]
  142. Tallamy DW. 142.  1985. Squash beetle feeding behavior: an adaptation against induced cucurbit defenses. Ecology 661574–79 [Google Scholar]
  143. Thaler JS, Humphrey PT, Whiteman NK. 143.  2012. Evolution of jasmonate and salicylate signal crosstalk. Trends Plant Sci 17:260–70 [Google Scholar]
  144. Tooker JF, Helms AM. 144.  2014. Phytohormone dynamics associated with gall insects, and their potential role in the evolution of the gall-inducing habit. J. Chem. Ecol. 40742–53 [Google Scholar]
  145. Tune R, Dussourd DE. 145.  2000. Specialized generalists: constraints on host range in some plusiine caterpillars. Oecologia 123:543–49 [Google Scholar]
  146. Voelckel C, Jander G. 146.  2014. Annual Plant Reviews Vol. 47: Insect-Plant Interactions Oxford, UK: Wiley [Google Scholar]
  147. Weech M, Chapleau M, Pan L, Ide C, Bede JC. 147.  2008. Caterpillar saliva interferes with induced Arabidopsis thaliana defence responses via the systemic acquired resistance pathway. J. Exp. Bot. 592437–48 [Google Scholar]
  148. Weinstein P. 148.  1990. Leaf petiole chewing and the sabotage of induced defences. Oikos 58231–33 [Google Scholar]
  149. Wilf P, Labandeira CC, Kress WJ, Staines CL, Windsor DM. 149.  et al. 2000. Timing the radiations of leaf beetles: hispines on gingers from latest Cretaceous to recent. Science 289:291–94 [Google Scholar]
  150. Wilkens RT, Shea GO, Halbreich S, Stamp NE. 150.  1996. Resource availability and the trichome defense of tomato plants. Oecologia 106:181–91 [Google Scholar]
  151. Wilson KJ, Nessler CL, Mahlberg PG. 151.  1976. Pectinase in Asclepias latex and its possible role in development in laticifer growth and development. Am. J. Bot. 631140–44 [Google Scholar]
  152. Wu J, Baldwin IT. 152.  2009. Herbivory-induced signalling in plants: perception and action. Plant Cell Environ 321161–74 [Google Scholar]
  153. Wu S, Peiffer M, Luthe DS, Felton GW. 153.  2012. ATP hydrolyzing salivary enzymes of caterpillars suppress plant defenses. PLOS ONE 7e41947 [Google Scholar]
  154. Yu SJ. 154.  1983. Age variation in insecticide susceptibility and detoxification capability of fall armyworm (Lepidoptera: Noctuidae) larva. J. Econ. Entomol. 76219–22 [Google Scholar]
  155. Zalucki MP, Brower LP. 155.  1992. Survival of first instar larvae of Danaus plexippus (Lepidoptera: Danainae) in relation to cardiac glycoside and latex content of Asclepias humistrata (Asclepiadaceae). Chemoecology 381–93 [Google Scholar]
  156. Zalucki MP, Brower LP, Alonso-M A. 156.  2001. Detrimental effects of latex and cardiac glycosides on survival and growth of first-instar monarch butterfly larvae Danaus plexippus feeding on the sandhill milkweed Asclepias humistrata. Ecol. Entomol. 26:212–24 [Google Scholar]
  157. Zalucki MP, Malcolm SB, Hanlon CC, Paine TD. 157.  2012. First-instar monarch larval growth and survival on milkweeds in southern California: effects of latex, leaf hairs and cardenolides. Chemoecology 22:75–88 [Google Scholar]
  158. Zeng RS, Wen Z, Niu G, Berenbaum MR. 158.  2013. Aflatoxin B1: toxicity, bioactivation and detoxification in the polyphagous caterpillar, Trichoplusia ni. Insect Sci 20:318–28 [Google Scholar]
  159. Zhang B, Tolstikov V, Turnbull C, Hicks LM, Fiehn O. 159.  2010. Divergent metabolome and proteome suggest functional independence of dual phloem transport systems in cucurbits. PNAS 107:13532–37 [Google Scholar]
  160. Zhang C, Yu X, Ayre BG, Turgeon R. 160.  2012. The origin and composition of cucurbit “phloem” exudate. Plant Physiol 158:1873–82 [Google Scholar]
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