1932

Abstract

The relationship between plants and insects is influenced by insects’ behavioral decisions during foraging and oviposition. In mutualistic pollinators and antagonistic herbivores, past experience (learning) affects such decisions, which ultimately can impact plant fitness. The higher levels of dietary generalism in pollinators than in herbivores may be an explanation for the differences in learning seen between these two groups. Generalist pollinators experience a high level of environmental variation, which we suggest favors associative learning. Larval herbivores employ habituation and sensitization—strategies useful in their less variable environments. Exceptions to these patterns based on habitats, mobility, and life history provide critical tests of current theory. Relevant plant traits should be under selection to be easily learned and remembered in pollinators and difficult to learn in herbivores. Insect learning thereby has the potential to have an important, yet largely unexplored, role in plant-insect coevolution.

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2017-01-31
2024-04-19
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Literature Cited

  1. Adler LS, Bronstein JL. 1.  2004. Attracting antagonists: Does floral nectar increase leaf herbivory?. Ecology 85:61519–26 [Google Scholar]
  2. Adler LS, Seifert MG, Wink M, Morse GE. 2.  2012. Reliance on pollinators predicts defensive chemistry across tobacco species. Ecol. Lett. 15:101140–48 [Google Scholar]
  3. Agrawal AA. 3.  2000. Host-range evolution: adaptation and trade-offs in fitness of mites on alternative hosts. Ecology 81:2500–8 [Google Scholar]
  4. Agrawal AA, Vala F, Sabelis MW. 4.  2002. Induction of preference and performance after acclimation to novel hosts in a phytophagous spider mite: adaptive plasticity?. Am. Nat. 159:5553–65 [Google Scholar]
  5. Akhtar Y, Isman MB. 5.  2003. Larval exposure to oviposition deterrents alters subsequent oviposition behavior in generalist, Trichoplusia ni and specialist, Plutella xylostella moths. J. Chem. Ecol. 29:81853–70 [Google Scholar]
  6. Allard RA, Papaj DR. 6.  1996. Learning of leaf shape by pipevine swallowtail butterflies: a test using artificial leaf models. J. Insect Behav. 9:6961–67 [Google Scholar]
  7. Allmann S, Späthe A, Bisch-Knaden S, Kallenbach M, Reinecke A. 7.  et al. 2013. Feeding-induced rearrangement of green leaf volatiles reduces moth oviposition. eLife 2:e00421 [Google Scholar]
  8. Amaya-Márquez M, Wells H. 8.  2008. Social complexity and learning foraging tasks in bees. Caldasia 30:2469–77 [Google Scholar]
  9. Anderson P, Hilker M, Löfqvist J. 9.  1995. Larval diet influence on oviposition behaviour in Spodoptera littoralis. Entomol. Exp. Appl. 74:171–82 [Google Scholar]
  10. Anderson P, Sadek MM, Larsson M, Hansson BS, Thöming G. 10.  2013. Larval host plant experience modulates both mate finding and oviposition choice in a moth. Anim. Behav. 85:61169–75 [Google Scholar]
  11. Arthur AP. 11.  1966. Associative learning in Itoplectis conquisitor (Say) (Hymenoptera: Ichneumonidae). Can. Entomol. 98:2213–23 [Google Scholar]
  12. Arthur AP. 12.  1971. Associative learning by Nemeritis canescens (Hymenoptera: Ichneumonidae). Can. Entomol. 103:81138–41 [Google Scholar]
  13. Avarguès-Weber A, Chittka L. 13.  2014. Local enhancement or stimulus enhancement? Bumblebee social learning results in a specific pattern of flower preference. Anim. Behav. 97:185–91 [Google Scholar]
  14. Barron AB. 14.  2001. The life and death of Hopkins’ host-selection principle. J. Insect Behav. 14:6725–37 [Google Scholar]
  15. Bernays EA. 15.  1993. Aversion learning and feeding. 1101–17 [Google Scholar]
  16. Bernays EA, Lee JC. 16.  1988. Food aversion learning in the polyphagous grasshopper Schistocerca americana. Physiol. Entomol. 13:2131–37 [Google Scholar]
  17. Bernays EA, Weiss MR. 17.  1996. Induced food preferences in caterpillars: the need to identify mechanisms. Entomol. Exp. Appl. 78:11–8 [Google Scholar]
  18. Blackiston D, Briscoe AD, Weiss MR. 18.  2011. Color vision and learning in the monarch butterfly, Danaus plexippus (Nymphalidae). J. Exp. Biol. 214:3509–20 [Google Scholar]
  19. Blackiston DJ, Casey ES, Weiss MR. 19.  2008. Retention of memory through metamorphosis: Can a moth remember what it learned as a caterpillar?. PLOS ONE 3:3e1736 [Google Scholar]
  20. Brantjes NBM. 20.  1982. Pollen placement and reproductive isolation between two Brazilian Polygala species (Polygalaceae). Plant Syst. Evol 141:141–52 [Google Scholar]
  21. Byrne RW, Bates LA. 21.  2007. Sociality, evolution and cognition. Curr. Biol. 17:16714–23 [Google Scholar]
  22. Campbell DR, Motten AF. 22.  1985. The mechanism of competition for pollination between two forest herbs. Ecology 66:2554 [Google Scholar]
  23. Chittka L, Thomson JD. 23.  2001. Cognitive Ecology of Pollination: Animal Behavior and Floral Evolution Cambridge, UK: Cambridge Univ. Press
  24. Chittka L, Thomson JD, Waser NM. 24.  1999. Flower constancy, insect psychology, and plant evolution. Naturwissenschaften 86:8361–77 [Google Scholar]
  25. Chow JK, Akhtar Y, Isman MB. 25.  2005. The effects of larval experience with a complex plant latex on subsequent feeding and oviposition by the cabbage looper moth: Trichoplusia ni (Lepidoptera: Noctuidae). Chemoecology 15:129–33 [Google Scholar]
  26. Clarin TMA, Ruczyński I, Page RA, Siemers BM. 26.  2013. Foraging ecology predicts learning performance in insectivorous bats. PLOS ONE 8:6e64823 [Google Scholar]
  27. Clarke D, Whitney H, Sutton G, Robert D. 27.  2013. Detection and learning of floral electric fields by bumblebees. Science 340:612866–69 [Google Scholar]
  28. Corbet SA. 28.  1985. Insect chemosensory responses: a chemical legacy hypothesis. Ecol. Entomol. 10:2143–53 [Google Scholar]
  29. Couvillon MJ, DeGrandi-Hoffman G, Gronenberg W. 29.  2010. Africanized honeybees are slower learners than their European counterparts. Naturwissenschaften 97:2153–60 [Google Scholar]
  30. Craighead FC. 30.  1921. Hopkins host-selection principle as related to certain Cerambycid beetles. J. Agric. Res. 22:189–220 [Google Scholar]
  31. Cunningham JP, Jallow MFA, Wright DJ, Zalucki MP. 31.  1998. Learning in host selection in Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae). Anim. Behav. 55:227–34 [Google Scholar]
  32. Cunningham JP, Moore CJ, Zalucki MP, West SA. 32.  2004. Learning, odour preference and flower foraging in moths. J. Exp. Biol. 207:87–94 [Google Scholar]
  33. Cunningham JP, West SA, Wright DJ. 33.  1998. Learning in the nectar foraging behaviour of Helicoverpa armigera. Ecol. Entomol. 23:4363–69 [Google Scholar]
  34. Cunningham JP, West SA, Zalucki MP. 34.  2001. Host selection in phytophagous insects: a new explanation for learning in adults. Oikos 95:3537–43 [Google Scholar]
  35. Cunningham JP, Zalucki MP, West SA. 35.  1999. Learning in Helicoverpa armigera (Lepidoptera: Noctuidae): a new look at the behaviour and control of a polyphagous pest. Bull. Entomol. Res. 89:201–7 [Google Scholar]
  36. Dacks AM, Riffell JA, Martin JP, Gage SL, Nighorn AJ. 36.  2012. Olfactory modulation by dopamine in the context of aversive learning. J. Neurophysiol. 108:2539–50 [Google Scholar]
  37. Daly KC, Smith BH. 37.  2000. Associative olfactory learning in the moth Manduca sexta. J. Exp. Biol. 203:132025–38 [Google Scholar]
  38. Daly M, Rauschenberger J, Behrends P. 38.  1982. Food aversion learning in kangaroo rats: a specialist-generalist comparison. Anim. Learn. Behav. 10:3314–20 [Google Scholar]
  39. Darwin C. 39.  1876. The Effects of Cross and Self Fertilization in the Vegetable Kingdom London: Murray
  40. Dawson EH, Avarguès-Weber A, Chittka L, Leadbeater E. 40.  2013. Learning by observation emerges from simple associations in an insect model. Curr. Biol. 23:8727–30 [Google Scholar]
  41. de Boer G, Hanson FE. 41.  1984. Foodplant selection and induction of feeding preference among host and non-host plants in larvae of the tobacco hornworm Manduca sexta. Entomol. Exp. Appl. 35:2177–93 [Google Scholar]
  42. Dethier VG. 42.  1980. Food-aversion learning in two polyphagous caterpillars, Diacrisia virginica and Estigmene congrua. Physiol. Entomol. 5:4321–25 [Google Scholar]
  43. Dicke M, Baldwin IT. 43.  2010. The evolutionary context for herbivore-induced plant volatiles: beyond the “cry for help.”. Trends Plant Sci. 15:3167–75 [Google Scholar]
  44. Dornhaus A, Chittka L. 44.  1999. Insect behaviour: evolutionary origins of bee dances. Nature 401:674838 [Google Scholar]
  45. Doumbia M, Hemptinne JL, Dixon AFG. 45.  1998. Assessment of patch quality by ladybirds: role of larval tracks. Oecologia 113:2197–202 [Google Scholar]
  46. Dukas R. 46.  2008. Evolutionary biology of insect learning. Annu. Rev. Entomol. 53:145–60 [Google Scholar]
  47. Dukas R, Bernays EA. 47.  2000. Learning improves growth rate in grasshoppers. PNAS 97:62637–40 [Google Scholar]
  48. Dukas R, Real L. 48.  1991. Learning foraging tasks by bees: a comparison between social and solitary species. Anim. Behav. 42:2269–76 [Google Scholar]
  49. Durisko Z, Anderson B, Dukas R. 49.  2013. Adult fruit fly attraction to larvae biases experience and mediates social learning. J. Exp. Biol. 217:1193–97 [Google Scholar]
  50. Facknath S, Wright DJ. 50.  2007. Is host selection in leafminer adults influenced by pre-imaginal or early adult experience?. J. Appl. Entomol. 131:8505–12 [Google Scholar]
  51. Farina WM, Grüter C, Acosta L, Mc Cabe S. 51.  2006. Honeybees learn floral odors while receiving nectar from foragers within the hive. Naturwissenschaften 94:155–60 [Google Scholar]
  52. Farris SM, Schulmeister S. 52.  2011. Parasitoidism, not sociality, is associated with the evolution of elaborate mushroom bodies in the brains of hymenopteran insects. Proc. R. Soc. B 278:1707940–51 [Google Scholar]
  53. Finkbeiner SD, Briscoe AD, Reed RD. 53.  2012. The benefit of being a social butterfly: communal roosting deters predation. Proc. R. Soc. B 279:17392769–76 [Google Scholar]
  54. Fontaine C, Thébault E, Dajoz I. 54.  2009. Are insect pollinators more generalist than insect herbivores?. Proc. R. Soc. B 276:16693027–33 [Google Scholar]
  55. Free JB. 55.  1963. The flower constancy of honeybees. J. Anim. Ecol. 32:1119–31 [Google Scholar]
  56. Free JB. 56.  1970. The flower constancy of bumblebees. J. Anim. Ecol. 39:2395–402 [Google Scholar]
  57. Free JB, Williams IH. 57.  1983. Scent-marking of flowers by honeybees. J. Apic. Res. 22:286–90 [Google Scholar]
  58. Frisch KV. 58.  1946. Die Tänze der Bienen. Öst. Zool. Z. 1:1–48 [Google Scholar]
  59. Frisch KV. 59.  1967. The Dance Language and Orientation of Bees Cambridge, MA: Harvard Univ. Press
  60. Gandolfi M, Mattiacci L, Dorn S. 60.  2003. Preimaginal learning determines adult response to chemical stimuli in a parasitic wasp. Proc. R. Soc. B 270:15332623–29 [Google Scholar]
  61. Garcia J, Kimeldorf DJ, Hunt EL. 61.  1961. The use of ionizing radiation as a motivating stimulus. Psychol. Rev. 68:6383–95 [Google Scholar]
  62. Gegear RJ. 62.  2005. Multicomponent floral signals elicit selective foraging in bumblebees. Naturwissenschaften 92:6269–71 [Google Scholar]
  63. Gegear RJ, Laverty TM. 63.  2001. The effect of variation among floral traits on the flower constancy of pollinators. 231–20 [Google Scholar]
  64. Gegear RJ, Laverty TM. 64.  2005. Flower constancy in bumblebees: a test of the trait variability hypothesis. Anim. Behav. 69:939–49 [Google Scholar]
  65. Gilbert LE. 65.  1982. The coevolution of a butterfly and a vine. Sci. Am. 247:2110–21 [Google Scholar]
  66. Gould JL. 66.  1993. Ethological and comparative perspectives on honey bee learning. Insect Learning Ecology and Evolutionary Perspectives DR Papaj, AC Lewis 18–50 Boston, MA: Springer [Google Scholar]
  67. Goulson D. 67.  1999. Foraging strategies of insects for gathering nectar and pollen, and implications for plant ecology and evolution. Perspect. Plant Ecol. Evol. Syst. 2:2185–209 [Google Scholar]
  68. Goulson D, Cory JS. 68.  1993. Flower constancy and learning in foraging preferences of the green-veined white butterfly Pieris napi. Ecol. Entomol. 18:4315–20 [Google Scholar]
  69. Goulson D, Mcguire K, Munro EE, Adamson S, Colliar L, Park KJ. 69.  2009. Functional significance of the dark central floret of Daucus carota (Apiaceae) L.; is it an insect mimic?. Plant Species Biol 24:277–82 [Google Scholar]
  70. Goulson D, Ollerton J, Sluman C. 70.  1997. Foraging strategies in the small skipper butterfly, Thymelicus flavus: when to switch?. Anim. Behav. 53:51009–16 [Google Scholar]
  71. Goulson D, Wright NP. 71.  1998. Flower constancy in the hoverflies Episyrphus balteatus (Degeer) and Syrphus ribesii (L.) (Syrphidae). Behav. Ecol. 9:3213–19 [Google Scholar]
  72. Goyret J, Pfaff M, Raguso RA, Kelber A. 72.  2008. Why do Manduca sexta feed from white flowers? Innate and learnt colour preferences in a hawkmoth. Naturwissenschaften 95:6569–76 [Google Scholar]
  73. Goyret J, Raguso RA. 73.  2006. The role of mechanosensory input in flower handling efficiency and learning by Manduca sexta. J. Exp. Biol. 209:1585–93 [Google Scholar]
  74. Grant V. 74.  1950. The flower constancy of bees. Bot. Rev 16:7379–98 [Google Scholar]
  75. Harris LJ, Clay J, Hargreaves FJ, Ward A. 75.  1933. Appetite and choice of diet. The ability of the vitamin B deficient rat to discriminate between diets containing and lacking the vitamin. Proc. R. Soc. Lond. B 113:781161–90 [Google Scholar]
  76. Haupt M, Eccard JA, Winter Y. 76.  2010. Does spatial learning ability of common voles (Microtus arvalis) and bank voles (Myodes glareolus) constrain foraging efficiency?. Anim. Cogn. 13:6783–91 [Google Scholar]
  77. Heinrich B. 77.  1976. The foraging specializations of individual bumblebees. Ecol. Monogr. 46:2105 [Google Scholar]
  78. Hopkins AD. 78.  1916. Economic investigations of the scolytid bark and timber beetles of North America. Program of Work of the United States Department of Agriculture for the Fiscal Year 1917 July 1 353
  79. Jaenike J. 79.  1983. Induction of host preference in Drosophila melanogaster. Oecologia 58:3320–25 [Google Scholar]
  80. Janz N, Söderlind L, Nylin S. 80.  2009. No effect of larval experience on adult host preferences in Polygonia c-album (Lepidoptera: Nymphalidae): on the persistence of Hopkins’ host selection principle. Ecol. Entomol. 34:150–57 [Google Scholar]
  81. Jermy T. 81.  1987. The role of experience in the host selection of phytophagous insects. Perspectives in Chemoreception and Behavior143–57 New York: Springer [Google Scholar]
  82. Jermy T, Hanson FE, Dethier VG. 82.  1968. Induction of specific food preference in lepidopterous larvae. Entomol. Exp. Appl. 11:2211–30 [Google Scholar]
  83. Jones CE. 83.  1978. Pollinator constancy as a pre-pollination isolating mechanism between sympatric species of Cercidium. Evolution 32:1189–98 [Google Scholar]
  84. Jones PL, Agrawal AA. 84.  2016. Consequences of toxic secondary compounds in nectar for mutualist bees and antagonist butterflies. Ecology 97:2570–79 [Google Scholar]
  85. Kandori I, Yamaki T, Okuyama S-I, Sakamoto N, Yokoi T. 85.  2009. Interspecific and intersexual learning rate differences in four butterfly species. J. Exp. Biol. 212:233810–16 [Google Scholar]
  86. Karban R, Myers JH. 86.  1989. Induced plant responses to herbivory. Annu. Rev. Ecol. Syst. 20:331–48 [Google Scholar]
  87. Karowe DN. 87.  1989. Facultative monophagy as a consequence of prior feeding experience: behavioral and physiological specialization in Colias philodice larvae. Oecologia 78:1106–11 [Google Scholar]
  88. Kawecki TJ. 88.  2010. Evolutionary ecology of learning: insights from fruit flies. Popul. Ecol. 52:115–25 [Google Scholar]
  89. Kelber A, Pfaff M. 89.  2013. Spontaneous and learned preferences for visual flower features in a diurnal hawkmoth. Isr. J. Plant Sci. 45:2–3235–45 [Google Scholar]
  90. Kerpel SM, Moreira GRP. 90.  2005. Absence of learning and local specialization on host plant selection by Heliconius erato. J. Insect Behav. 18:3433–52 [Google Scholar]
  91. Kevan PG, Lane MA. 91.  1985. Flower petal microtexture is a tactile cue for bees. PNAS 82:144750–52 [Google Scholar]
  92. Kinoshita M, Shimada N, Arikawa K. 92.  1999. Colour vision of the foraging swallowtail butterfly Papilio xuthus. J. Exp. Biol. 202:295–102 [Google Scholar]
  93. Kulahci IG, Dornhaus A, Papaj DR. 93.  2008. Multimodal signals enhance decision making in foraging bumble-bees. Proc. R. Soc. B 275:1636797–802 [Google Scholar]
  94. Lee JC, Bernays EA. 94.  1988. Declining acceptability of a food plant for the polyphagous grasshopper Schistocerca americana: the role of food aversion learning. Physiol. Entomol. 13:3291–301 [Google Scholar]
  95. Lewis WJ, Tumlinson JH. 95.  1988. Host detection by chemically mediated associative learning in a parasitic wasp. Nature 331:6153257–59 [Google Scholar]
  96. Liu S-S, Li Y-H, Liu Y-Q, Zalucki MP. 96.  2005. Experience-induced preference for oviposition repellents derived from a non-host plant by a specialist herbivore. Ecol. Lett. 8:7722–29 [Google Scholar]
  97. Manning A. 97.  1967. “Pre-imaginal conditioning” in Drosophila. Nature 216:5113338–40 [Google Scholar]
  98. Manson JS, Rasmann S, Halitschke R, Thomson JD, Agrawal AA. 98.  2012. Cardenolides in nectar may be more than a consequence of allocation to other plant parts: a phylogenetic study of Asclepias. Funct. Ecol. 26:51100–10 [Google Scholar]
  99. Mayr E. 99.  1974. Behavior programs and evolutionary strategies. Am. Sci. 62:6650–59 [Google Scholar]
  100. McCormick AC, Unsicker SB, Gershenzon J. 100.  2012. The specificity of herbivore-induced plant volatiles in attracting herbivore enemies. Trends Plant Sci. 17:5303–10 [Google Scholar]
  101. Menzel R, Muller U. 101.  1996. Learning and memory in honeybees: from behavior to neural substrates. Annu. Rev. Neurosci. 19:379–404 [Google Scholar]
  102. Mery F, Kawecki TJ. 102.  2002. Experimental evolution of learning ability in fruit flies. PNAS 99:2214274–79 [Google Scholar]
  103. Mettke-Hofmann C. 103.  2014. Cognitive ecology: ecological factors, life-styles, and cognition. WIREs Cogn. Sci. 5:3345–60 [Google Scholar]
  104. Moeller DA. 104.  2004. Facilitative interactions among plants via shared pollinators. Ecology 85:123289–301 [Google Scholar]
  105. Muth F, Papaj DR, Leonard AS. 105.  2015. Colour learning when foraging for nectar and pollen: Bees learn two colours at once. Biol. Lett. 11:920150628 [Google Scholar]
  106. Muth F, Papaj DR, Leonard AS. 106.  2016. Bees remember flowers for more than one reason: Pollen mediates associative learning. Anim. Behav. 111:93–100 [Google Scholar]
  107. Olsson P-OC, Anderbrant O, Löfstedt C. 107.  2006. Experience influences oviposition behaviour in two pyralid moths, Ephestia cautella and Plodia interpunctella. Anim. Behav. 72:545–51 [Google Scholar]
  108. Papaj DR. 108.  1986. Conditioning of leaf-shape discrimination by chemical cues in the butterfly, Battus philenor. Anim. Behav. 34:51281–88 [Google Scholar]
  109. Papaj DR. 109.  1986. Interpopulation differences in host preference and the evolution of learning in the butterfly, Battus philenor. Evolution 40:3518–30 [Google Scholar]
  110. Papaj DR, Lewis AC. 110.  2012. Insect Learning: Ecology and Evolutionary Perspectives Boston, MA: Springer
  111. Papaj DR, Prokopy RJ. 111.  1989. Ecological and evolutionary aspects of learning in phytophagous insects. Annu. Rev. Entomol. 34:315–50 [Google Scholar]
  112. Parmesan C, Singer MC, Harris I. 112.  1995. Absence of adaptive learning from the oviposition foraging behavior of a checkerspot butterfly. Anim. Behav. 50:161–75 [Google Scholar]
  113. Poolman Simons MTT, Suverkropp BP, Vet LEM, de Moed G. 113.  1992. Comparison of learning in related generalist and specialist eucoilid parasitoids. Entomol. Exp. Appl. 64:2117–24 [Google Scholar]
  114. Proffit M, Khallaf MA, Carrasco D, Larsson MC, Anderson P. 114.  2015. “Do you remember the first time?” Host plant preference in a moth is modulated by experiences during larval feeding and adult mating. Ecol. Lett. 18:4365–74 [Google Scholar]
  115. Prokopy RJ, Lewis WJ. 115.  1993. Application of learning to pest management. 110308–42 [Google Scholar]
  116. Raguso RA. 116.  2008. Wake up and smell the roses: the ecology and evolution of floral scent. Annu. Rev. Ecol. Evol. Syst. 39:549–69 [Google Scholar]
  117. Raine NE, Chittka L. 117.  2007. Pollen foraging: learning a complex motor skill by bumblebees (Bombus terrestris). Naturwissenschaften 94:6459–64 [Google Scholar]
  118. Rausher MD. 118.  1978. Search image for leaf shape in a butterfly. Science 200:43451071–73 [Google Scholar]
  119. Ray S. 119.  1999. Survival of olfactory memory through metamorphosis in the fly Musca domestica. Neurosci. Lett. 259:137–40 [Google Scholar]
  120. Reisenman CE, Riffell JA, Duffy K, Pesque A, Mikles D, Goodwin B. 120.  2013. Species-specific effects of herbivory on the oviposition behavior of the moth Manduca sexta. J. Chem. Ecol. 39:176–89 [Google Scholar]
  121. Rietdorf K, Steidle J. 121.  2002. Was Hopkins right? Influence of larval and early adult experience on the olfactory response in the granary weevil Sitophilus granarius (Coleoptera, Curculionidae). Physiol. Entomol. 27:3223–27 [Google Scholar]
  122. Riffell JA. 122.  2011. The neuroecology of a pollinator's buffet: olfactory preferences and learning in insect pollinators. Integr. Comp. Biol. 51:5781–93 [Google Scholar]
  123. Riffell JA, Alarcón R, Abrell L, Davidowitz G, Bronstein JL, Hildebrand JG. 123.  2008. Behavioral consequences of innate preferences and olfactory learning in hawkmoth-flower interactions. PNAS 10593404–9
  124. Riffell JA, Lei H, Abrell L, Hildebrand JG. 124.  2013. Neural basis of a pollinator's buffet: olfactory specialization and learning in Manduca sexta. Science 339:6116200–4 [Google Scholar]
  125. Salloum A, Colson V, Marion-Poll F. 125.  2011. Appetitive and aversive learning in Spodoptera littoralis larvae. Chem. Senses 36:8725–31 [Google Scholar]
  126. Sarin S, Dukas R. 126.  2009. Social learning about egg-laying substrates in fruitflies. Proc. R. Soc. B 276:16774323–28 [Google Scholar]
  127. Schaefer HM, Schaefer V, Levey DJ. 127.  2004. How plant–animal interactions signal new insights in communication. Trends Ecol. Evol. 19:11577–84 [Google Scholar]
  128. Scheirs J, De Bruyn L. 128.  2002. Integrating optimal foraging and optimal oviposition theory in plant–insect research. Oikos 96:1187–91 [Google Scholar]
  129. Scheirs J, De Bruyn L, Verhagen R. 129.  2000. Optimization of adult performance determines host choice in a grass miner. Proc. R. Soc. Lond. B 267:14572065–69 [Google Scholar]
  130. Sheehan MJ, Tibbetts EA. 130.  2011. Specialized face learning is associated with individual recognition in paper wasps. Science 334:60601272–75 [Google Scholar]
  131. Sherry DF, Strang CG. 131.  2014. Contrasting styles in cognition and behaviour in bumblebees and honeybees. Behav. Process. 117:59–69 [Google Scholar]
  132. Shikano I, Isman MB. 132.  2009. A sensitive period for larval gustatory learning influences subsequent oviposition choice by the cabbage looper moth. Anim. Behav. 77:1247–51 [Google Scholar]
  133. Simoes P, Ott SR, Niven JE. 133.  2011. Associative olfactory learning in the desert locust, Schistocerca gregaria.. J. Exp. Biol. 214:152495–503 [Google Scholar]
  134. Simpson SJ, White PR. 134.  1990. Associative learning and locust feeding: Evidence for a “learned hunger” for protein. Anim. Behav. 40:3506–513 [Google Scholar]
  135. Snell-Rood EC, Papaj DR. 135.  2009. Patterns of phenotypic plasticity in common and rare environments: a study of host use and color learning in the cabbage white butterfly Pieris rapae. Am. Nat. 173:5615–31 [Google Scholar]
  136. Stephens DW. 136.  1993. Learning and behavioral ecology: incomplete information and environmental predictability. 110195–218 [Google Scholar]
  137. Swihart CA, Swihart SL. 137.  1970. Colour selection and learned feeding preferences in the butterfly, Heliconius charitonius Linn. Anim. Behav. 18:60–64 [Google Scholar]
  138. Thöming G, Larsson MC, Hansson BS, Anderson P. 138.  2013. Comparison of plant preference hierarchies of male and female moths and the impact of larval rearing hosts. Ecology 94:81744–52 [Google Scholar]
  139. Thomson JD, Draguleasa MA, Tan MG. 139.  2015. Flowers with caffeinated nectar receive more pollination. Arthropod Plant Interact 9:11–7 [Google Scholar]
  140. Thompson JN. 140.  2005. The Geographic Mosaic of Coevolution Chicago, IL: Univ. Chicago Press
  141. Thorpe WH. 141.  1939. Further studies on pre-imaginal olfactory conditioning in insects. Proc. R. Soc. Lond. B 127:848424–33 [Google Scholar]
  142. Thorpe WH, Jones F. 142.  1937. Olfactory conditioning in a parasitic insect and its relation to the problem of host selection. Proc. R. Soc. Lond. B 124:83456–81 [Google Scholar]
  143. Traynier R. 143.  1986. Visual learning in assays of sinigrin solution as an oviposition releaser for the cabbage butterfly, Pieris rapae. Entomol. Exp. Appl. 40:125–33 [Google Scholar]
  144. Tully T, Cambiazo V, Kruse L. 144.  1994. Memory through metamorphosis in normal and mutant Drosophila. J. Neurosci. 14:168–74 [Google Scholar]
  145. Turlings TCJ, Wäckers FL, Vet LEM, Lewis WJ, Tumlinson JH. 145.  1993. Learning of host-finding cues by Hymenopterous parasitoids.. 11051–78 [Google Scholar]
  146. van Nouhuys S, Kaartinen R. 146.  2008. A parasitoid wasp uses landmarks while monitoring potential resources. Proc. R. Soc. B 275:1633377–85 [Google Scholar]
  147. Waller DA, Gilbert LE. 147.  1982. Roost recruitment and resource utilization: observations on a Heliconius charitonia L. roost in Mexico (Nymphalidae). J. Lepidopterists Soc. 36:6178–84 [Google Scholar]
  148. Wardle AR. 148.  1990. Learning of host microhabitat colour by Exeristes roborator (F.) (Hymenoptera: Ichneumonidae). Anim. Behav. 39:5914–23 [Google Scholar]
  149. Weiss MR. 149.  1995. Associative colour learning in a nymphalid butterfly. Ecol. Entomol. 20:3298–301 [Google Scholar]
  150. Weiss MR. 150.  1997. Innate colour preferences and flexible colour learning in the pipevine swallowtail. Anim. Behav. 53:51043–52 [Google Scholar]
  151. Weiss MR. 151.  2001. Vision and learning in some neglected pollinators: beetles, flies, moths, and butterflies.. 23171–90 [Google Scholar]
  152. Weiss MR, Papaj DR. 152.  2003. Colour learning in two behavioural contexts: How much can a butterfly keep in mind?. Anim. Behav. 65:3425–34 [Google Scholar]
  153. Wertheim B, Allemand R, Vet LEM, Dicke M. 153.  2006. Effects of aggregation pheromone on individual behaviour and food web interactions: a field study on Drosophila. Ecol. Entomol. 31:3216–26 [Google Scholar]
  154. Wertheim B, Marchais J, Vet LEM, Dicke M. 154.  2002. Allee effect in larval resource exploitation in Drosophila: an interaction among density of adults, larvae, and micro-organisms. Ecol. Entomol. 27:5608–17 [Google Scholar]
  155. Williams KS, Gilbert LE. 155.  1981. Insects as selective agents on plant vegetative morphology: Egg mimicry reduces egg-laying by butterflies. Science 212:4493467–69 [Google Scholar]
  156. Wilson P, Stine M. 156.  1996. Floral constancy in bumble bees: handling efficiency or perceptual conditioning?. Oecologia 106:4493–99 [Google Scholar]
  157. Wright GA, Baker DD, Palmer MJ, Stabler D, Mustard JA. 157.  et al. 2013. Caffeine in floral nectar enhances a pollinator's memory of reward. Science 339:61241202–4 [Google Scholar]
  158. Wright GA, Schiestl FP. 158.  2009. The evolution of floral scent: the influence of olfactory learning by insect pollinators on the honest signaling of floral rewards. Funct. Ecol. 23:5841–51 [Google Scholar]
  159. Zhang P-J, Liu S-S, Wang H, Zalucki MP. 159.  2007. The influence of early adult experience and larval food restriction on responses toward nonhost plants in moths. J. Chem. Ecol. 33:81528–41 [Google Scholar]
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