1932

Abstract

Aphid cornicles are abdominal appendages that secrete an array of volatile and nonvolatile compounds with diverse ecological functions. The emission of alarm pheromones yields altruistic benefits for clone-mates in the aphid colony, which is essentially a superorganism with a collective fate. Secreted droplets also contain unsaturated triglycerides, fast-drying adhesives that can be lethal when smeared on natural enemies but more often impede their foraging efficiency. The longest cornicles have evolved in aphids that feed in exposed locations and are likely used to scent-mark colony intruders. Reduced cornicles are associated with reliance on alternative defenses, such as the secretion of protective waxes or myrmecophily. Root-feeding and gall-forming lifestyles provide protected feeding sites and are associated with an absence of cornicles. In some eusocial gall-formers, soldier morphs become repositories of cornicle secretion used to defend the gall, either as menopausal apterae that defend dispersing alatae or as sterile first instars that dispatch predators with their stylets and use cornicle secretions as a construction material for gall repair. Collectively, the evidence is consistent with an adaptive radiation of derived cornicle functions molded by the ecological lifestyle of the aphid lineage.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-ento-033021-094437
2022-01-07
2024-12-10
Loading full text...

Full text loading...

/deliver/fulltext/ento/67/1/annurev-ento-033021-094437.html?itemId=/content/journals/10.1146/annurev-ento-033021-094437&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Alfaress S, Broderson CR, Ammar ED, Rogers ME, Killiny N 2018. Laser surgery reveals the biomechanical and chemical signalling functions of aphid siphunculi (cornicles). PLOS ONE 13:10e0204984
    [Google Scholar]
  2. 2. 
    Alfaress S, Hijaz F, Killiny N. 2016. Chemical composition of cornicle secretion of the brown citrus aphid Toxoptera citricida. Physiol. Entomol. 41:138–47
    [Google Scholar]
  3. 3. 
    Aoki S, Kurosu U, von Dohlen CD. 2001. Colony defense by wingpadded nymphs in Grylloprociphilus imbricator (Hemiptera: Aphididae). Fla. Entomol. 84:3431–34
    [Google Scholar]
  4. 4. 
    Arakaki N. 1989. Alarm pheromone eliciting attack and escape responses in the sugar cane woolly aphid, Ceratovacuna lanigera (Homoptera, Pemphigidae). J. Ethol. 7:83–90
    [Google Scholar]
  5. 5. 
    Arakaki N. 1992. Feeding behaviour of the ladybeetle, Pseudoscymnus kurohime. J. Ethol. 10:7–13
    [Google Scholar]
  6. 6. 
    Barry A, Ohno K. 2016. Cornicle secretions of Uroleucon nigrotuberculatum (Homoptera: Aphididae) as the last bullet against lady beetle larvae. Entomol. Sci. 19:4410–15
    [Google Scholar]
  7. 7. 
    Battaglia D, Pennacchio F, Marincola G, Tranfaglia A. 1993. Cornicle secretion of Acyrthosiphon pisum (Homoptera, Aphididae) as a contact kairomone for the parasitoid Aphidius ervi (Hymenoptera, Braconidae). Eur. J. Entomol. 90:4423–28
    [Google Scholar]
  8. 8. 
    Battaglia D, Poppy G, Powell W, Romano A, Tranfaglia A, Pennachio F. 2000. Physical and chemical cues influencing the oviposition behaviour of Aphidius ervi. Entomol. Exp. Appl. 94:3219–27
    [Google Scholar]
  9. 9. 
    Bei-Bienko GY, Blagoveshchenskii DI, Chernova OA, Dantsig EM, Emel'yanov AF et al. 1964. Keys to the Insects of the European USSR, Vol. 1: Apterygota, Palaeoptera, Hemimetabola Moscow: Acad. Sci. USSR (transl. Isr. Progr. Sci. Transl., Jerusalem 1967 )
    [Google Scholar]
  10. 10. 
    Blackman RL. 2010. Handbooks for the Identification of British Insects: Aphids—Aphidinae (Macrosiphini) Chiswell Green, UK: R. Entomol. Soc.
    [Google Scholar]
  11. 11. 
    Blackman RL, Dransfield RD, Brightwell R. 2019. Handbooks for the Identification of British Insects: Aphids—Anoeciinae, Lachninae, Eristomatidae, Phloeomyzinae, Thelaxinae, Hormaphidinae, Mindarinae Chiswell Green, UK: R. Entomol. Soc.
    [Google Scholar]
  12. 12. 
    Boyle K, Barrows EM. 1976. Oviposition and host feeding behavior of Aphelinus asychis (Hymenoptera: Chalcidoidea: Aphelinidae) on Schizaphis graminum (Homoptera: Aphididae) and some reactions of aphids to this parasite. Proc. Entomol. Soc. Wash. 80:3441–55
    [Google Scholar]
  13. 13. 
    Broughton WB, Harris KM. 1971. First recording of the sound produced by the black citrus aphid, Toxoptera aurantii. Bull. Entomol. Res. 60:4559–63
    [Google Scholar]
  14. 14. 
    Busgen M. 1891. Der Honigtau. Biologische Studien an Pflanzen und Pflanzenläusen. Jena. Z. Naturwiss. 25:339–428
    [Google Scholar]
  15. 15. 
    Butler CD, O'Neil RJ. 2006. Defensive response of soybean aphid (Hemiptera: Aphididae) to predation by insidious flower bug (Hemiptera: Anthocoridae). Ann. Entomol. Soc. Am. 99:2317–20
    [Google Scholar]
  16. 16. 
    Callow RK, Greenway AR, Griffiths DC. 1973. Chemistry of the secretion from the cornicles of various species of aphids. J. Insect Physiol. 19:737–48
    [Google Scholar]
  17. 17. 
    Chau A, Mackauer M 1997. Dropping of pea aphids from feeding site: a consequence of parasitism by the wasp, Monoctonus paulensis. Entomol. Exp. Appl. 83:3247–52
    [Google Scholar]
  18. 18. 
    Chen J, Qiao GX 2012. Wax gland plates in Hormaphidinae (Hemiptera: Aphididae): morphological diversity and evolution. Entomol. News 122:127–45
    [Google Scholar]
  19. 19. 
    Cheng Y-J, Li Z-X. 2019. Both farnesyl diphosphate synthase genes are involved in the production of alarm pheromone in the green peach aphid Myzus persicae. Arch. Insect Biochem. Physiol. 100:3e21530
    [Google Scholar]
  20. 20. 
    Cheng Y-J, Li Z-X. 2019. Spatiotemporal expression profiling of the farnesyl diphosphate synthase genes in aphids and analysis of their associations with the biosynthesis of alarm pheromone. Bull. Entomol. Res. 109:3398–407
    [Google Scholar]
  21. 21. 
    Dardouri T, Gautier H, Ben Issa R, Costaglioli G, Gomez L 2019. Repellence of Myzus persicae (Sulzer): evidence of two modes of action of volatiles from selected living aromatic plants. Pest Manag. Sci. 75:61571–84
    [Google Scholar]
  22. 22. 
    Dawson GW, Griffiths DC, Pickett JA, Wadhams LJ, Woodcock CM. 1987. Plant-derived synergists of alarm pheromone from turnip aphid, Lipaphis (Hyadaphis) erysimi (Homoptera, Aphididae). J. Chem. Ecol. 13:1663–71
    [Google Scholar]
  23. 23. 
    de Vos M, Cheng WY, Summers HE, Raguso RA, Jander G. 2010. Alarm pheromone habituation in Myzus persicae has fitness consequences and causes extensive gene expression changes. PNAS 107:3314673–78
    [Google Scholar]
  24. 24. 
    Dill LM, Fraser AHG, Roitberg BD. 1990. The economics of escape behaviour in the pea aphid, Acyrthosiphon pisum. Oecologia 83:473–78
    [Google Scholar]
  25. 25. 
    Dixon AFG. 1958. Escape responses shown by certain aphids to the presence of the coccinellid Adalia decempunctata (L.). Trans. R. Entomol. Soc. 110:11319–34
    [Google Scholar]
  26. 26. 
    Dixon AFG. 2000. Aphid Ecology London, UK: Chapman and Hall
    [Google Scholar]
  27. 27. 
    Duff KM, Mondor EB. 2012. All clone-mates are not created equal: Fitness discounting theory predicts pea aphid colony structure. J. Insect Behav. 25:49–59
    [Google Scholar]
  28. 28. 
    Edwards JS. 1966. Defence by smear: supercooling in the cornicle wax of aphids. Nature 211:73–74
    [Google Scholar]
  29. 29. 
    Eisner T, Hicks M, Eisner M, Robson DS. 1978.. “ Wolf-in-sheep's-clothing” strategy of a predaceous insect larva. Science 199:4330790–94
    [Google Scholar]
  30. 30. 
    Fan J, Zhang Y, Francis F, Cheng DF, Sun JR, Chen JL. 2015. Orco mediates olfactory behaviors and winged morph differentiation induced by alarm pheromone in the grain aphid, Sitobion avenae. Insect Biochem. Mol. Biol. 64:16–24
    [Google Scholar]
  31. 31. 
    Francis F, Lognay G, Haubruge E. 2004. Olfactory responses to aphid and host plant volatile releases: (E)-beta-farnesene an effective kairomone for the predator Adalia bipunctata. J. Chem. Ecol. 30:4741–55
    [Google Scholar]
  32. 32. 
    Gao L, Zhang XT, Zhou F, Chen H, Lin YJ 2015. Expression of a peppermint (E)-beta-farnesene synthase gene in rice has significant repelling effect on bird cherry-oat aphid (Rhopalosiphum padi). Plant Mol. Biol. Rep. 33:61967–74
    [Google Scholar]
  33. 33. 
    Gould SJ, Lewontin R. 1979. The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme. Proc. R. Soc. Lond. B 205:1161589–98
    [Google Scholar]
  34. 34. 
    Grasswitz TR. 1998. Contact kairomones mediating the foraging behavior of the aphid hyperparasitoid Alloxysta victrix (Westwood) (Hymenoptera: Charipidae). J. Insect Behav. 11:539–48
    [Google Scholar]
  35. 35. 
    Greenway AR, Griffiths DC, Furk C, Prior RNB. 1974. Composition of triglycerides from aphids of six different families and from different seasonal forms of Aphis evonymi. J. Insect Physiol. 20:122423–31
    [Google Scholar]
  36. 36. 
    Hartbauer M. 2010. Collective defense of Aphis nerii and Uroleucon hypochoeridis (Homoptera, Aphididae) against natural enemies. PLOS ONE 5:e10417
    [Google Scholar]
  37. 37. 
    Hatano E, Kunert G, Weisser WW. 2010. Aphid wing induction and ecological costs of alarm pheromone emission under field conditions. PLOS ONE 5:6e11188
    [Google Scholar]
  38. 38. 
    Heie OE. 1987. Palaeontology and phylogeny. Aphids: Their Biology, Natural Enemies, and Control 2A AK Minks, P Harrewijn 367–91 Amsterdam: Elsevier
    [Google Scholar]
  39. 39. 
    Holldobler B, Wilson EO. 1990. The Ants Cambridge, MA: Belknap Press
    [Google Scholar]
  40. 40. 
    Holldobler B, Wilson EO. 1994. Journey to the Ants Cambridge, MA: Belknap Press
    [Google Scholar]
  41. 41. 
    Holman J. 1993. Possible sound producing structures present in some Macrosiphini (Homoptera: Aphididae). Eur. J. Entomol. 91:97–101
    [Google Scholar]
  42. 42. 
    Hottes FC. 1928. Concerning the structure, function, and origin of the cornicles of the family Aphididae. Proc. Biol. Soc. Wash. 41:71–84
    [Google Scholar]
  43. 43. 
    Ide T, Suzuki N, Katayama N. 2007. The use of honeydew in foraging for aphids by larvae of the ladybird beetle, Coccinella septempunctata L. (Coleoptera: Coccinellidae). Ecol. Entomol. 32:5455–60
    [Google Scholar]
  44. 44. 
    Jazzar C, Meyhofer R, Ebssa L, Poehling HM 2008. Two protagonists on aphidophagous patches: effects of learning and intraguild predation. Entomol. Exp. Appl. 127:88–99
    [Google Scholar]
  45. 45. 
    Joachim C, Hatano E, David A, Kunert M, Linse C, Weisser WW 2013. Modulation of aphid alarm pheromone emission of pea aphid prey by predators. J. Chem. Ecol. 39:6773–82
    [Google Scholar]
  46. 46. 
    Joachim C, Vosteen I, Weisser WW 2015. The aphid alarm pheromone (E)-beta-farnesene does not act as a cue for predators searching on a plant. Chemoecology 25:3105–13
    [Google Scholar]
  47. 47. 
    Joachim C, Weisser WW 2015. Does the aphid alarm pheromone (E)-beta-farnesene act as a kairomone under field conditions?. J. Chem. Ecol. 41:3267–75
    [Google Scholar]
  48. 48. 
    Kanturski M, Karcz J, Kaszyca N, Depa L 2017. Perianal structures in myrmecophilous subterranean aphids (Insecta: Hemiptera: Aphididae)—comparative morphology of trophobiotic organ with its first description in Lachninae. Arthropod Struct. Dev. 46:4496–507
    [Google Scholar]
  49. 49. 
    Kasahara M, Akimoto SI, Hariyama T, Takaku Y, Yusa SI et al. 2019. Liquid marbles in nature: craft of aphids for survival. Langmuir 35:186169–78
    [Google Scholar]
  50. 50. 
    Kutsukake M, Uematsu K, Fukatsu T. 2019. Plant manipulation by gall-forming aphids for waste management. Front. Plant Sci. 10:933
    [Google Scholar]
  51. 51. 
    Keiser CN, Mondor EB. 2014. Cues of predation risk induce instar- and genotype-specific changes in pea aphid colony spatial structure. Ethology 121:2144–51
    [Google Scholar]
  52. 52. 
    Kurosu U, Aoki S, Fukatsu T. 2003. Self-sacrificing gall repair by aphid nymphs. Proc. R. Soc. Lond. B 270:S1S12–14
    [Google Scholar]
  53. 53. 
    Larocca A, Fanti P, Romano VA, Marsicovetere E, Isidoro N et al. 2007. Functional bases of host-acceptance behaviour in the aphid parasitoid Aphidius ervi. Physiol. Entomol. 32:4305–12
    [Google Scholar]
  54. 54. 
    Li JJ, Hu H, Mao J, Yu L, Stoopen G et al. 2019. Defense of pyrethrum flowers: repelling herbivores and recruiting carnivores by producing aphid alarm pheromone. New Phytol 223:31607–20
    [Google Scholar]
  55. 55. 
    Liepert C, Dettner K. 1996. Role of cuticular hydrocarbons of aphid parasitoids in their relationship to aphid-attending ants. J. Chem. Ecol. 22:695–707
    [Google Scholar]
  56. 56. 
    McAllister MK, Roitberg BD, Weldon KL. 1990. Adaptive suicide in pea aphids: decisions are cost-sensitive. Anim. Behav. 40:1167–75
    [Google Scholar]
  57. 57. 
    Micha SG, Wyss U 1996. Aphid alarm pheromone (E)-beta-farnesene: a host finding kairomone for the aphid primary parasitoid Aphidius uzbekistanicus (Hymenoptera: Aphidiinae). Chemoecology 7:132–39
    [Google Scholar]
  58. 58. 
    Michaud JP. 1999. Aggregation by alatae of Toxoptera citricida (Homoptera: Aphididae). Environ. Entomol. 28:2205–11
    [Google Scholar]
  59. 59. 
    Michaud JP, Belliure B. 2000. Consequences of foundress aggregation in the brown citrus aphid, by Toxoptera citricida. Ecol. Entomol. 25:307–14
    [Google Scholar]
  60. 60. 
    Michaud JP, Jyoti JL, Qureshi JA 2006. Positive correlation of fitness with group size in two biotypes of Russian wheat aphid (Homoptera: Aphididae). J. Econ. Entomol. 99:41214–24
    [Google Scholar]
  61. 61. 
    Michaud JP, Mackauer M. 1994. The use of visual cues in host evaluation by aphidiid wasps: I. Comparison between three Aphidius parasitoids of the pea aphid. Entomol. Exp. Appl. 70:3273–83
    [Google Scholar]
  62. 62. 
    Moayeri HRS, Mohandesi AR, Ashouri A. 2012. Fitness costs of cornicle secretions as a defense mechanism for cotton aphid, Aphis gossypii (Hem.: Aphididae). J. Entomol. Soc. Iran 31:51–61
    [Google Scholar]
  63. 63. 
    Moayeri HRS, Rasekh A, Enkegaard A 2014. Influence of cornicle droplet secretions of the cabbage aphid, Brevicoryne brassicae, on parasitism behavior of naive and experienced Diaeretiella rapae. Insect Sci 21:156–64
    [Google Scholar]
  64. 64. 
    Moelke G, Wyss U. 2003. Effect of aphid-infested plants on the host location and learning behaviour of the parasitoid Aphelinus abdominalis. Comm. Agric. Appl. Biol. Sci. 68:4A167–77
    [Google Scholar]
  65. 65. 
    Mondor EB, Addicott JF. 2006. Do exaptations facilitate mutualistic associations between invasive and native species?. Biol. Invasions 9:6623–28
    [Google Scholar]
  66. 66. 
    Mondor EB, Baird DS, Slessor KN, Roitberg BD. 2000. Ontogeny of alarm pheromone secretion in pea aphid, Acyrthosiphon pisum. J. Chem. Ecol. 26:2875–82
    [Google Scholar]
  67. 67. 
    Mondor EB, Messing RH. 2007. Direct versus inclusive fitness in the evolution of aphid cornicle length. J. Evol. Biol. 20:2807–12
    [Google Scholar]
  68. 68. 
    Mondor EB, Roitberg BD. 2000. Has the attraction of predatory coccinellids to cornicle droplets constrained aphid alarm signaling behavior?. J. Insect Behav. 13:321–29
    [Google Scholar]
  69. 69. 
    Mondor EB, Roitberg BD. 2002. Pea aphid, Acyrthosiphon pisum, cornicle ontogeny as an adaptation to differential predation risk. Can. J. Zool. 80:122131–36
    [Google Scholar]
  70. 70. 
    Mondor EB, Roitberg BD. 2003. Age-dependent fitness costs of alarm signaling in aphids. Can. J. Zool. 81:757–62
    [Google Scholar]
  71. 71. 
    Mondor EB, Roitberg BD. 2004. Inclusive fitness benefits of scent-marking predators. Proc. R. Soc. Lond. B 271:Suppl. 5S341–43
    [Google Scholar]
  72. 72. 
    Mondor EB, Roitberg BD, Stadler B. 2002. Cornicle length in Macrosiphini aphids: a comparison of ecological traits. Ecol. Entomol. 27:6758–62
    [Google Scholar]
  73. 73. 
    Moss R, Jackson RR, Pollard SD 2006. Mask of wax: secretions of wax conceal aphids from detection by spider's eyes. N. Z. J. Zool. 33:3215–20
    [Google Scholar]
  74. 74. 
    Muratori F, Hance T, Lonay GC. 2006. Epicuticular factors involved in host recognition for the aphid parasitoid Aphidius rhopalosiphi. J. Chem. Ecol. 32:579–83
    [Google Scholar]
  75. 75. 
    Nault LR, Bowers WS. 1974. Multiple alarm pheromones in aphids. Entomol. Exp. Appl. 17:3455–57
    [Google Scholar]
  76. 76. 
    Nault LR, Edwards LJ, Styer WE. 1973. Aphid alarm pheromones: secretion and reception. Environ. Entomol. 2:1101–5
    [Google Scholar]
  77. 77. 
    Nault LR, Montgomery ME, Bowers WS 1976. Ant-aphid association: role of aphid alarm pheromone. Science 192:42461349–51
    [Google Scholar]
  78. 78. 
    Nishida R, Fukami H. 1989. Host plant iridoid-based chemical defense of an aphid, Acyrthosiphon nipponicus, against ladybird beetles. J. Chem. Ecol. 15:61837–45
    [Google Scholar]
  79. 79. 
    Oliver KM, Noge K, Huang EM, Campos JM, Becerra JX, Hunter MS. 2012. Parasitic wasp responses to symbiont-based defense in aphids. BMC Biol 10:11
    [Google Scholar]
  80. 80. 
    Oluwafemi S, Bruce TJA, Pickett JA, Ton J, Birkett MA. 2011. Behavioral responses of the leafhopper, Cicadulina storeyi China, a major vector of maize streak virus, to volatile cues from intact and leafhopper-damaged maize. J. Chem. Ecol. 37:140–48
    [Google Scholar]
  81. 81. 
    Outreman Y, Le Ralec A, Plantegenest M, Chaubet B, Pierre JS 2001. Superparasitism limitation in an aphid parasitoid: cornicle secretion avoidance and host discrimination ability. J. Insect Physiol. 47:4–5339–48
    [Google Scholar]
  82. 82. 
    Parvizi Y, Rasekh A, Michaud JP 2018. Cornicle secretions by Aphis fabae (Hemiptera: Aphididae) result in age-dependent costs and improved host suitability for Lysiphlebus fabarum (Marshall) (Hymenoptera: Braconidae). Bull. Entomol. Res. 108:5685–93
    [Google Scholar]
  83. 83. 
    Pettersson J, Quiroz A, Stephansson D, Niemeyer HM. 1995. Odour communication of Rhopalosiphum padi on grasses. Entomol. Exp. Appl. 76:325–28
    [Google Scholar]
  84. 84. 
    Pickett J, Wadhams LJ, Woodcock CM. 1992. The chemical ecology of aphids. Annu. Rev. Entomol. 37:67–90
    [Google Scholar]
  85. 85. 
    Pickett JA, Bruce TJA, Glinwood RT 2017. Chemical ecology. Aphids as Crop Pests H van Emden, R Harrington 148–72 Wallingford, UK: CABI
    [Google Scholar]
  86. 86. 
    Pike KS, Boydston LL, Allison DW. 2003. Aphids of western North America north of Mexico Ext. Bull., Wash. State Univ. Pullman:
    [Google Scholar]
  87. 87. 
    Podjacek JO, Bosnjak LM, Brooker DJ, Mondor EB. 2005. Alarm pheromone induces a transgenerational wing polyphenism in the pea aphid, Acyrthosiphon pisum. Can. J. Entomol. 83:81138–41
    [Google Scholar]
  88. 88. 
    Pope RD. 1983. Some aphid waxes, their form and function (Homoptera: Aphididae). J. Nat. Hist. 17:4489–506
    [Google Scholar]
  89. 89. 
    Ramirez-Caceres GE, Moya-Hernandez MG, Quilodran M, Nespolo RF, Ceballos R et al. 2019. Harbouring the secondary endosymbiont Regiella insecticola increases predation risk and reproduction in the cereal aphid Sitobion avenae. J. Pest Sci. 92:31039–47
    [Google Scholar]
  90. 90. 
    Rasekh A, Michaud JP, Kharazi-Pakdel A, Allahyari H. 2010. Ant mimicry by an aphid parasitoid, Lysiphlebus fabarum (Hymenoptera: Aphidiidae). J. Insect Sci. 10:126
    [Google Scholar]
  91. 91. 
    Schwartzberg EG, Haynes KF, Johnson DW, Brown GC 2010. Wax structures of Scymnus louisianae attenuate aggression from aphid-tending ants. Environ. Entomol. 39:41309–14
    [Google Scholar]
  92. 92. 
    Seibert TF. 1992. Mutualistic interactions of the aphid Lachnus allegheniensis (Homoptera: Aphididae) and its tending ant Formica obscuripes (Hymenoptera: Formicidae). Ann. Entomol. Soc. Am. 85:2173–78
    [Google Scholar]
  93. 93. 
    Shingleton AW, Stern DL, Foster WA. 2005. The origin of a mutualism: a morphological trait promoting the evolution of ant-aphid mutualisms. Evolution 59:4921–26
    [Google Scholar]
  94. 94. 
    Shonouda ML, Bombosch S, Shalaby AM, Osman SL. 1998. Biological and chemical characterization of a kairomone excreted by the bean aphids, Aphis fabae Scop. (Hom., Aphididae) and its effect on the predator Metasyrphus corollae F. I. Isolation, identification and bioassay of aphid-kairomone. J. Appl. Entomol. 122:1–515–23
    [Google Scholar]
  95. 95. 
    Smith RG. 1999. Wax glands, wax production and the functional significance of wax use in three aphid species (Homoptera: Aphididae). J. Nat. Hist. 33:4513–30
    [Google Scholar]
  96. 96. 
    Stadler B, Dixon AFG. 2005. Ecology and evolution of aphid-ant interactions. Annu. Rev. Entomol. 36:345–72
    [Google Scholar]
  97. 97. 
    Stern DL, Foster WA. 1996. The evolution of soldiers in aphids. Biol. Rev. Camb. Phil. Soc. 71:127–79
    [Google Scholar]
  98. 98. 
    Strong FE. 1967. Observations on aphid cornicle secretions. Ann. Entomol. Soc. Am. 60:3668–73
    [Google Scholar]
  99. 99. 
    Su M, Tan XM, Yang QM, Wang JQ, Wan FH, Zhou HX 2016. Distribution of wax gland pores on the body surface and the dynamics of wax secretion of wooly apple aphid Eriosoma lanigerum (Hemiptera: Aphididae). Entomol. News 126:2106–20
    [Google Scholar]
  100. 100. 
    Sun C-X, Li Z-X. 2019. Production of alarm pheromone starts at embryo stage and is modulated by rearing conditions and farnesyl diphosphate synthase genes in the bird cherry-oat aphid Rhopalosiphum padi. Bull. Entomol. Res. 109:6821–30
    [Google Scholar]
  101. 101. 
    Takada H, Tokumaru S. 1996. Observations on oviposition and host-feeding behavior of Aphelinus gossypii Timberlake (Hymenoptera: Aphelinidae). Appl. Entomol. Zool. 31:2263–70
    [Google Scholar]
  102. 102. 
    Tang YQ, Yokomi RK. 1996. Biology of Aphelinus spiraecolae (Hymenoptera: Aphelinidae), a parasitoid of the spirea aphid (Homoptera: Aphididae). Environ. Entomol. 25:2519–23
    [Google Scholar]
  103. 103. 
    Tegelaar K, Leimar O. 2014. Alate production in an aphid in relation to ant tending and alarm pheromone. Ecol. Entomol. 39:5578–88
    [Google Scholar]
  104. 104. 
    Thomas AM, Williams RS, Swarthout RF. 2019. Distribution of the specialist aphid Uroleucon nigrotuberculatum (Homoptera: Aphididae) in response to host plant semiochemical induction by the gall fly Eurosta solidaginis (Diptera:Tephritidae). Environ. Entomol. 48:51138–48
    [Google Scholar]
  105. 105. 
    Turchin P, Kareiva P. 1989. Aggregation in Aphis varians: an effective strategy for reducing predation risk. Ecology 70:41008–16
    [Google Scholar]
  106. 106. 
    Uematsu K, Kutsukake M, Fukatsu T 2018. Water-repellent plant surface structures induced by gall-forming insects for waste management. Biol. Lett. 14:20180470
    [Google Scholar]
  107. 107. 
    Uematsu K, Kutsukake M, Fukatsu T, Shimada M, Shibao H. 2007. Altruistic defenders in a Japanese gall-forming aphid, Quadrartus yoshinomiyai (Homoptera: Aphididae: Hormaphidinae). Sociobiology 50:3711–24
    [Google Scholar]
  108. 108. 
    Uematsu K, Kutsukake M, Fukatsu T, Shimada M, Shibao H. 2010. Altruistic colony defense by menopausal female insects. Curr. Biol. 20:131182–86
    [Google Scholar]
  109. 109. 
    van Emden HF, Dingley J, Dewhirst SY, Pickett JA, Woodcock CM, Wadhams LJ. 2014. The effect of artificial diet on the production of alarm pheromone by Myzus persicae. Physiol. Entomol. 39:4285–91
    [Google Scholar]
  110. 110. 
    Vandermoten S, Mescher MC, Francis F, Haubruge E, Verheggen FJ 2012. Aphid alarm pheromone: an overview of current knowledge on biosynthesis and functions. Insect Biochem. Mol. Biol. 42:3155–63
    [Google Scholar]
  111. 111. 
    Verheggen FJ, Haubruge E, De Moraes CM, Mescher MC. 2009. Social environment influences aphid production of alarm pheromone. Behav. Ecol. 20:2283–88
    [Google Scholar]
  112. 112. 
    Verma SS, Sinha RK, Jajoo A. 2015. (E)-beta-farnesene gene reduces Lipaphis erysimi colonization in transgenic Brassica juncea lines. Plant Signal. Behav. 10:e1042636
    [Google Scholar]
  113. 113. 
    Volkl W, Mackauer M. 2000. Oviposition behaviour of aphidiine wasps (Hymenoptera: Braconidae, Aphidiinae): morphological adaptations and evolutionary trends. Can. Entomol. 132:2197–212
    [Google Scholar]
  114. 114. 
    Vosteen I, Weisser WW, Kunert G. 2016. Is there any evidence that aphid alarm pheromones work as prey and host finding kairomones for natural enemies?. Ecol. Entomol. 41:11–12
    [Google Scholar]
  115. 115. 
    Wang LB, Bi YD, Liu M, Li W, Liu M et al. 2020. Identification and expression profiles analysis of odorant-binding proteins in soybean aphid, Aphis glycines (Hemiptera: Aphididae). Insect Sci 27:51019–30
    [Google Scholar]
  116. 116. 
    Wang X, Gao Y, Chen Z, Li JD, Huang JP et al. 2019. (E)-beta-farnesene synthase gene affects aphid behavior in transgenic Medicago sativa. Pest Manag. Sci. 75:3622–31
    [Google Scholar]
  117. 117. 
    Way MJ, Banks CJ 1967. Intra-specific mechanisms in relation to the natural regulation of numbers of Aphis fabae Scop. Ann. Appl. Biol. 59:2189–205
    [Google Scholar]
  118. 118. 
    Wu GM, Boivin G, Brodeur J, Giraldeau LA, Outreman Y. 2010. Altruistic defence behaviours in aphids. BMC Evol. Ecol. 10:19
    [Google Scholar]
  119. 119. 
    Wu H, Li RT, Dong JF, Jiang NJ, Huang LQ, Wang CZ. 2019. An odorant receptor and glomerulus responding to farnesene in Helicoverpa assulta (Lepidoptera: Noctuidae). Insect Biochem. Mol. Biol. 115:103106
    [Google Scholar]
  120. 120. 
    Wynn GG. 1968. Observations on the cornicles of aphids PhD Thesis, La. State Univ. Baton Rouge:
    [Google Scholar]
  121. 121. 
    Yu X, Jia D, Duan P 2019. Plasmid engineering of aphid alarm pheromone in tobacco seedlings affects the preference of aphids. Plant Signal. Behav. 14:5e1588669
    [Google Scholar]
/content/journals/10.1146/annurev-ento-033021-094437
Loading
/content/journals/10.1146/annurev-ento-033021-094437
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error