Journal of Chemical Ecology

, Volume 32, Issue 7, pp 1379–1397

Early Herbivore Alert: Insect Eggs Induce Plant Defense

Review Article

Abstract

Plants are able to “notice” insect egg deposition and to respond by activating direct and indirect defenses. An overview of these defenses and the underlying mechanisms is given from a tritrophic perspective. First, the interface between plant and eggs is addressed with respect to the mode of attachment of eggs on the plant surface. It is elucidated which plant cells might respond to components from insect eggs or the egg deposition. The scarce knowledge on the elicitors associated with the eggs or the egg-laying female is outlined. Since endosymbiotic microorganisms are often present on the eggs, and microorganisms are also abundant on the leaf surface, the role of these hidden players for eliciting oviposition-induced plant responses is considered. Furthermore, the question of which physiological and molecular processes are induced within the plant in response to egg deposition is addressed. Second, studies on the response of the herbivorous insect to oviposition-induced plant defenses are outlined. Third, the importance of oviposition-induced plant volatiles and contact cues for host and prey location of parasitoids and predators is discussed in the context of other informative chemicals used by carnivores when searching for food. Finally, physiological and ecological costs of oviposition-induced plant responses are addressed.

Keywords

Plant defenses Oviposition Egg Secretion Endosymbiotic microorganisms Elicitor Terpenoids Green leaf volatiles 

References

  1. Agrawal, A. A., Tuzun, S., and Bent, E. 1999. Induced Plant Defenses Against Pathogens and Herbivores. APS Press, St. Paul, MN.Google Scholar
  2. Alborn, H. T., Turlings, T. C. J., Jones, T. H., Stenhagen, G., Loughrin, J. H., and Tumlinson, J. H. 1997. An elicitor of plant volatiles from beet armyworm oral secretion. Science 276:945–949.CrossRefGoogle Scholar
  3. Andersson, J., Borg-Karlson, A.-K., and Wiklund, C. 2003. Antiaphrodisiacs in pierid butterflies: a theme of variation. J. Chem. Ecol. 29:1489–1499.CrossRefPubMedGoogle Scholar
  4. Arimura, G.-I., Ozawa, R., Shimoda, T., Nishioka, T., Boland, W., and Takabayashi, J. 2000. Herbivory-induced volatiles elicit defence genes in lima bean leaves. Nature 406:512–515.CrossRefPubMedGoogle Scholar
  5. Balbyshev, N. F. and Lorenzen, J. H. 1997. Hypersensitivity and egg drop, a novel mechanism of host-plant resistance to Colorado potato beetle (Coleoptera: Chrysomelidae). J. Econ. Entomol. 90:652–657.Google Scholar
  6. Bjorksten, T. A. and Hoffmann, A. A. 1998. Persistence of experience effects in the parasitoid Trichogramma nr brassicae. Ecol. Entomol. 23:110–117.CrossRefGoogle Scholar
  7. Blaakmeer, A., Hagenbeek, D., Van Beek, T. A., de Groot, A. E., Schoonhoven, L. M., and Van Loon, J. J. A. 1994. Plant response to eggs vs. host marking pheromone as factors inhibiting oviposition by Pieris brassicae. J. Chem. Ecol. 20:1657–1665.CrossRefGoogle Scholar
  8. Bolter, C. J., Dicke, M., Van Loon, J. J. A., Visser, J. H., and Posthumus, M. A. 1997. Attraction of Colorado potato beetle to herbivore-damaged plants during herbivory and after its termination. J. Chem. Ecol. 23:1003–1023.CrossRefGoogle Scholar
  9. Bown, A. W., Hall, D. E., and MacGregor, K. B. 2002. Insect footsteps on leaves stimulate the accumulation of 4-aminobutyrate and can be visualized through increased chlorophyll fluorescence and superoxide production. Plant Physiol. 129:1430–1434.CrossRefPubMedGoogle Scholar
  10. Clausen, C. P. 1976. Phoresy among entomophagous insects. Annu. Rev. Entomol. 21:343–368.CrossRefGoogle Scholar
  11. Colazza, S., Salerno, G., and Waijnberg, E. 1999. Volatiles and contact chemicals released by Nezara viridula (Heteroptera: Pentatomidae) have a kairomonal effect on the egg parasitoid Trissolcus basalis (Hymenoptera: Scelionidae). Biol. Control 16:310–317.CrossRefGoogle Scholar
  12. Colazza, S., Fucarino, A., Peri, E., Salerno, G., Conti, E., and Bin, F. 2004a. Insect oviposition induces volatile emission in herbaceous plants that attracts egg parasitoids. J. Exp. Biol. 207:47–53.CrossRefPubMedGoogle Scholar
  13. Colazza, S., McElfresh, J. S., and Millar, J. G. 2004b. Identification of volatile synomones, induced by Nezara viridula feeding and oviposition on bean spp., that attract the egg parasitoid Trissolcus basalis. J. Chem. Ecol. 30:945–964.CrossRefPubMedGoogle Scholar
  14. De Jong, E. J. and Pak, G. A. 1984. Factors determining differential host egg recognition of two host species by different Trichogramma sp. Meded. Fac. Landbouwwet. Rijksuniv. Gent. 49:815–825.Google Scholar
  15. De Moraes, C. M., Mescher, M. C., and Tumlinson, J. H. 2001. Caterpillar-induced nocturnal plant volatiles repel conspecific females. Nature 410:577–580.CrossRefPubMedGoogle Scholar
  16. Dicke, M. and Bruin, J. 2001. Chemical information transfer between wounded and unwounded plants: back to the future. Biochem. Syst. Ecol. 29:981–995.CrossRefGoogle Scholar
  17. Dicke, M. and Hilker, M. 2003. Induced plant defences: from molecular biology to evolutionary ecology. Basic Appl. Ecol. 4:3–14.CrossRefGoogle Scholar
  18. Dicke, M. and Van Loon, J. A. A. 2000. Multitrophic effects of herbivore-induced plant volatiles in an evolutionary context. Entomol. Exp. Appl. 97:237–249.CrossRefGoogle Scholar
  19. Dickinson, C. H. and Preece, T. F. 1976. Microbiology of Aerial Plant Surfaces. Academic Press, London.Google Scholar
  20. Dirie, A. M. and Gabriel, B. P. 1998. The effect of semiochemicals on efficiency and parasitism of Trichogramma evanescens (Westwood), an egg parasitoid of Asian corn borer. Asia Life Sci. 7:131–140.Google Scholar
  21. Doss, R. P., Proebsting, W. M., Potter, S. W., Clement, S. L., and Williamson, R. T. 1995. Response of Np mutant of pea (Pisum sativum L.) to pea weevil (Bruchus pisorum L.) oviposition and extracts. J. Chem. Ecol. 21:97–106.CrossRefGoogle Scholar
  22. Doss, R. P., Oliver, J. E., Proebsting, W. M., Potter, S. W., Kuy, S. R., Clement, S. L., Williamson, R. T., Carney, J. R., and Devilbiss, E. D. 2000. Bruchins-insect-derived plant regulators that stimulate neoplasm formation. Proc. Natl. Acad. Sci. USA 97:6218–6223.CrossRefPubMedGoogle Scholar
  23. Engelberth, J., Koch, T., Kühnemann, F., and Boland, W. 2000. Ionenkanalbildende Peptaibole sind hochwirksame Elicitoren des pflanzlichen Sekundärstoffwechsels und der Rankenkrümmung. Angew. Chem. 112:1928–1930.CrossRefGoogle Scholar
  24. Fatouros, N. E., Bukovinszkine Kiss, G., Kalkers, L. A., Soler Gamborena, R., Dicke, M., and Hilker, M. 2005a. Plant synomone induced by butterfly eggs arrests Trichogramma wasps. Entomol. Exp. Appl. 115:207–215.CrossRefGoogle Scholar
  25. Fatouros, N. E., Huigens, M. E., Van Loon, J. J. A., Dicke, M., and Hilker, M. 2005b. Riders on the storm: hitch-hiking parasitic wasps spy on butterfly anti-aphrodisiac. Nature 433:704.CrossRefPubMedGoogle Scholar
  26. Felton, G. W. and Eichenseer, H. 1999. Herbivore saliva and its effects on plant defense against herbivores and pathogens, pp. 19–36, in A. A. Agrawal, S. Tuzun, and E. Bent (eds.). Induced Plant Defenses Against Pathogens and Herbivores. APS Press, St. Paul, MN.Google Scholar
  27. Fukushima, J., Kainoh, Y., Honda, H., and Takabayashi, J. 2002. Learning of herbivore-induced and nonspecific plant volatiles by a parasitoid, Cotesia kariyai. J. Chem. Ecol. 28:579–586.PubMedCrossRefGoogle Scholar
  28. Hall, D. E., MacGregor, K. B., Nijsse, J., and Bown, A. W. 2004. Footsteps from insect larvae damage leaf surfaces and initiate rapid responses. Eur. J. Plant Pathol. 110:441–447.CrossRefGoogle Scholar
  29. Harari, A. R., Ben-Yakir, D., and Rosen, D. 1994. Mechanism of aggregation behavior in Maladera matrida Argaman (Coleoptera: Scarabaeidae). J. Chem. Ecol. 20:361–371.CrossRefGoogle Scholar
  30. Herms, D. A. and Mattson, W. J. 1992. The dilemma of plants: to grow or defend. Q. Rev. Biol. 67:283–335.CrossRefGoogle Scholar
  31. Hilker, M. 1994. Egg deposition and protection of eggs in Chrysomelidae, pp. 263–276, in P. Jolivet, M. L. Cox, and E. Petitpierre (eds.). Novel Aspects of Biology of Chrysomelidae. Kluwer Academic Publishers, Dordrecht.Google Scholar
  32. Hilker, M. and Meiners, T. 2002. Induction of plant responses towards oviposition and feeding of herbivorous arthropods: a comparison. Entomol. Exp. Appl. 104:181–192.CrossRefGoogle Scholar
  33. Hilker, M., Blaeske, V., Kobs, C., and Dippel, C. 2000. Kairomonal effects of sawfly sex pheromones on egg parasitoids. J. Chem. Ecol. 26:221–231.CrossRefGoogle Scholar
  34. Hilker, M., Kobs, C., Varama, M., and Schrank, K. 2002a. Insect egg deposition induces Pinus sylvestris to attract egg parasitoids. J. Exp. Biol. 205:455–461.PubMedGoogle Scholar
  35. Hilker, M., Rohfritsch, O., and Meiners, T. 2002b. The plant's response towards insect oviposition, pp. 205–234, in M. Hilker and T. Meiners (eds.). Chemoecology of Insect Eggs and Egg Deposition. Blackwell, Berlin.Google Scholar
  36. Hilker, M., Stein, C., Schröder, R., Varama, M., and Mumm, R. 2005. Insect egg deposition induced defence response in Pinus sylvestris. Characterization of the elicitor. J. Exp. Biol. 208:1849–1854.CrossRefPubMedGoogle Scholar
  37. Horiuchi, J.-I., Arimura, G.-I., Ozawa, R., Shimoda, T., Takabayashi, J., and Nishioka, T. 2003. A comparison of the responses of Tetranychus urticae (Acari: Tetranychidae) and Phytoseiulus persimilis (Acari: Phytoseiidae) to volatiles emitted from lima bean leaves with different levels of damage made by T. urticae or Spodoptera exigua (Lepidoptera: Noctuidae). Appl. Entomol. Zool. 38:109–116.CrossRefGoogle Scholar
  38. Ignacimuthu, S., Wäckers, F. L., and Dorn, S. 2000. The role of chemical cues in host finding and acceptance by Callosobruchus chinensis. Entomol. Exp. Appl. 96:213–219.CrossRefGoogle Scholar
  39. Kalberer, N., Turlings, T. C. J., and Rahier, M. 2001. Attraction of a leaf beetle (Oreina cacaliae) to damaged host plants. J. Chem. Ecol. 27:647–661.CrossRefPubMedGoogle Scholar
  40. Karban, R. and Baldwin, I. T. 1997. Induced Responses to Herbivory. Chicago University Press, Chicago.Google Scholar
  41. Kelling, F. J., Ialenti, F., and Den Otter, C. J. 2002. Background odour induces adaptation and sensitization of olfactory receptors in the antennae of houseflies. Med. Vet. Entomol. 16:161–169.CrossRefPubMedGoogle Scholar
  42. Kellner, R. L. L. 2002. The role of microorganisms for eggs and progeny, pp. 149–170, in M. Hilker and T. Meiners (eds.). Chemoecology of Insect Eggs and Egg Deposition. Blackwell, Berlin.Google Scholar
  43. Kessler, A. and Baldwin, I. T. 2001. Defensive function of herbivore-induced plant volatile emissions in nature. Science 291:2141–2144.CrossRefPubMedGoogle Scholar
  44. Kessler, A. and Baldwin, I. T. 2002. Plant responses to insect herbivory: the emerging molecular analysis. Annu. Rev. Plant Biol. 53:299–328.CrossRefPubMedGoogle Scholar
  45. Kinkel, L. L. 1997. Microbial population dynamics on leaves. Annu. Rev. Phytopathol. 35:327–347.CrossRefPubMedGoogle Scholar
  46. Landolt, P. J. 1993. Effects of host plant leaf damage on cabbage looper moth attraction and oviposition. Entomol. Exp. Appl. 67:79–85.CrossRefGoogle Scholar
  47. Lait, C. G., Albron, H. T., Teal, P. E. A., and Tumlinson, J. H. 2003. Rapid biosynthesis of N-linolenoyl-l-glutamine, an elicitor of plant volatiles, by membrane-associated enzymes in Manduca sexta. Proc. Natl. Acad. Sci. USA 100:7027–7032.CrossRefPubMedGoogle Scholar
  48. Loughrin, J. H., Potter, D. A., Hamilton, K. T., and Byers, M. E. 1996. Role of feeding-induced plant volatiles in aggregative behavior of the Japanese beetle (Coleoptera: Scarabaeidae). Environ. Entomol. 25:1188–1191.Google Scholar
  49. Maffei, M., Bossi, S., Spiteller, D., Mithöfer, A., and Boland, W. 2004. Effects of feeding Spodoptera littoralis on lima bean leaves. I. Membrane potentials, intracellular calcium variations, oral secretions, and regurgitate components. Plant Physiol. 134:1752–1762.CrossRefPubMedGoogle Scholar
  50. McGregor, R. and Henderson, D. 1998. The influence of oviposition experience on response to host pheromone in Trichogramma sibericum (Hymenoptera: Trichogrammatidae). J. Insect Behav. 11:621–632.CrossRefGoogle Scholar
  51. Meiners, T. and Hilker, M. 1997. Host location in Oomyzus gallerucae (Hymenoptera: Eulophidae), an egg parasitoid of the elm leaf beetle Xanthogaleruca luteola (Coleoptera, Chrysomelidae). Oecologia 112:87–93.CrossRefGoogle Scholar
  52. Meiners, T. and Hilker, M. 2000. Induction of plant synomones by oviposition of a phytophagous insect. J. Chem. Ecol. 26:221–232.CrossRefGoogle Scholar
  53. Meiners, T., Wäckers, F., and Lewis, J. 2003. Associative learning of complex odors in parasitoid host location. The effect of molecule structure on the olfactory discrimination by the parasitoid Microplitis croceipes. Chem. Senses 28:231–236.CrossRefPubMedGoogle Scholar
  54. Meiners, T., Hacker, N., Anderson, P., and Hilker, M. 2005. Response of the elm leaf beetle to host plants induced by oviposition and feeding: the infestation rate matters. Entomol. Exp. Appl. 115:171–177.CrossRefGoogle Scholar
  55. Minardi, P. 1995. Cellular recognition in plant–bacteria interactions: biological and molecular aspects. Riv. Patol. Veg. 5:9–34.Google Scholar
  56. Morris, C. E., Nicot, P. C., and Nguyen-The, C. 1996. Aerial Plant Surface Microbiology. Plenum Press, New York.Google Scholar
  57. Müller, C. and Riederer, M. 2005. Plant surface properties in chemical ecology. J. Chem. Ecol. 31:3621–3651.CrossRefGoogle Scholar
  58. Mumm, R. and Hilker, M. 2005. The significance of background odour for an egg parasitoid to detect plants with host eggs. Chem. Senses 30:1–7.CrossRefPubMedGoogle Scholar
  59. Mumm, R., Schrank, K., Wegener, R., Schulz, S., and Hilker, M. 2003. Chemical analysis of volatiles emitted by Pinus sylvestris after induction by insect oviposition. J. Chem. Ecol. 29:1235–1252.CrossRefPubMedGoogle Scholar
  60. Nordlund, D. A. 1994. Habitat location by Trichogramma, pp. 155–164, in E. Waijnberg and S. A. Hassan (eds.). Biological Control with Egg Parasitoids. CAB International, Oxon.Google Scholar
  61. Oliver, J. E., Doss, R. P., Williamson, R. T., Carney, J. R., and De Vilbiss, E. D. 2000. Bruchins-mitogenic 3-(hydroxy-propanoyl) esters of long chain diols from weevils of the Bruchidae. Tetrahedron 56:7633–7641.CrossRefGoogle Scholar
  62. Prokopy, R. J. and Roitberg, B. D. 2001. Joining and avoidance behavior in non-social insects. Annu. Rev. Entomol. 41:631–665.CrossRefGoogle Scholar
  63. Reddy, G. V. P., Holopainen, J. K., and Guerrrero, A. 2002. Olfactory responses of Plutella xylostella natural enemies to host pheromone, larval frass, and green leaf cabbage volatiles. J. Chem. Ecol. 28:131–143.CrossRefPubMedGoogle Scholar
  64. Rohfritsch, O. 1992. Patterns in gall development, pp. 87–101, in J. D. Shorthouse and O. Rohfritsch (eds.). Biology of Insect-Induced Galls. Oxford University Press, Oxford.Google Scholar
  65. Romeis, J., Shanower, T. G., and Zebitz, C. P. W. 1997. Volatile plant infochemicals mediate plant preference of Trichogramma chilonis. J. Chem. Ecol. 23:2455–2465.CrossRefGoogle Scholar
  66. Romeis, J., Shanower, T. G., and Zebitz, C. P. W. 1998. Physical and chemical plant character inhibiting the searching behaviour of Trichogramma chilonis. Entomol. Exp. Appl. 87:275–284.CrossRefGoogle Scholar
  67. Romeis, J., Babendreier, D., Wäckers, F. L., and Shanower, G. 2005. Habitat and plant specificity of Trichogramma egg parasitoids - Underlying mechanisms and implications. Basic Appl. Ecol. 3:215–236.CrossRefGoogle Scholar
  68. Rosetto, M., Belardinelli, M., Fausto, A. M., Marchini, D., Bongiorno, G., Maroli, M., and Mazzini, M. 2003. A mammalian-like lipase gene is expressed in the female reproductive accessory glands of the sand fly Phlebotomus papatasi (Diptera, Psychodidae). Insect Mol. Biol. 12:501–508.CrossRefPubMedGoogle Scholar
  69. Ruther, J., Reinecke, A., Thiemann, K., Tolasch, T., and Hilker, M. 2000. Mate finding in the forest cockchafer, Melolontha hippocastani, mediated by volatiles from plants and females. Physiol. Entomol. 25:172–179.CrossRefGoogle Scholar
  70. Schaller, F. and Weiler, E. W. 2002. Wound- and mechanical signalling, pp. 20–44, in D. Scheel and C. Wasternack (eds.). Plant Signal Transduction. Oxford University Press, Oxford.Google Scholar
  71. Schroeder, R., Forstreuther, M., and Hilker, M. 2005. A plant notices insect egg deposition and changes its rate of photosynthesis. Plant Physiol. 138:470–477.CrossRefPubMedGoogle Scholar
  72. Seino, Y., Suzuki, Y., and Sogawa, K. 1996. An ovicidal substance produced by rice plants in response to oviposition by the whitebacked planthopper, Sogatella furcifera (Horvath) (Homoptera: Delphacidae). Appl. Entomol. Zool. 31:467–473.Google Scholar
  73. Shapiro, A. M. and DeVay, J. E. 1987. Hypersensitivity reaction of Brassica nigra L. (Cruciferae) kills eggs of Pieris butterflies (Lepidoptera: Pieridae). Oecologia 71:631–632.CrossRefGoogle Scholar
  74. Shiojiri, K. and Takabayashi, J. 2003. Effect of specialist parasitoids on oviposition preference of phytophagous insects: encounter-dilution effects in a tritrophic interaction. Ecol. Entomol. 28:573–578.CrossRefGoogle Scholar
  75. Shorthouse, J. D. and Rohfritsch, O. 1992. Biology of Insect-Induced Galls. Oxford University Press, Oxford.Google Scholar
  76. Smith, B. H. 1998. Analysis of interaction in binary mixtures. Physiol. Behav. 65:397–407.CrossRefPubMedGoogle Scholar
  77. Spiteller, D., Dettner, K., and Boland, W. 2000. Gut bacteria may be involved in interactions between plants, herbivores and their predators: microbial biosynthesis of N-acylglutamine surfactants as elicitors of plant volatiles. Biol. Chem. 381:755–762.CrossRefPubMedGoogle Scholar
  78. Steidle, J. L. M. and Van Loon, J. J. A. 2002a. Chemoecology of parasitoid and predator oviposition behaviour, pp. 291–348, in M. Hilker and T. Meiners (eds.). Chemoecology of Insect Eggs and Egg Deposition. Blackwell, Berlin.Google Scholar
  79. Steidle, J. L. M. and Van Loon, J. J. A. 2002b. Dietary specialization and infochemical use in carnivorous arthropods: testing a concept. Entomol. Exp. Appl. 108:133–148.CrossRefGoogle Scholar
  80. Steidle, J. L. M., Fischer, A., and Gantert, C. 2005. Do grains whisper for help? Evidence for herbivore-induced synomones in granary weevil infested wheat grains. Entomol. Exp. Appl. 115:239–245.CrossRefGoogle Scholar
  81. Suzuki, Y., Sogawa, K., and Seino, Y. 1996. Ovicidal reaction of rice plants against the whitebacked planthopper, Sogatella furcifera Horvath (Homoptera: Delphacidae). Appl. Entomol. Zool. 31:111–118.Google Scholar
  82. Tooker, J. F. and De Moraes, C. M. 2005. Jasmonate in lepidopteran eggs and neonates. J. Chem. Ecol. 31:2753–2759.CrossRefPubMedGoogle Scholar
  83. Truitt, C. L., Wei, H. X., and Paré, P. W. 2004. A plasma membrane protein from Zea mays binds with the herbivore elicitor volicitin. Plant Cell 16:523–532.CrossRefPubMedGoogle Scholar
  84. Tumlinson, J. H. and Lait, C. G. 2005. Biosynthesis of fatty acid amide elicitors of plant volatiles by insect herbivores. Arch. Insect Biochem. Physiol. 58:54–68.CrossRefPubMedGoogle Scholar
  85. Tumlinson, J. H., Turlings, T. C. J., and Lewis, W. J. 1993. Semiochemically mediated foraging behavior in beneficial parasitic insects. Arch. Insect Biochm. Physiol. 22:385–391.CrossRefGoogle Scholar
  86. Turlings, T. C. J. and Wäckers, F. 2004. Recruitment of predators and parasitoids by herbivore injured plants, pp. 21–75, in R. T. Cardé and J. G. Millar (eds.). Advances in Insect Chemical Ecology. Cambridge University Press, Cambridge.Google Scholar
  87. Underwood N., Anderson K., and Inouye B. D. 2005. Induced vs. constitutive resistance and the spatial distribution of insect herbivores among plants. Ecology 26:594–602.CrossRefGoogle Scholar
  88. Varma, A., Abbott, L., Werner, D., and Hampp, R. 2004. Plant Surface Microbiology. Springer, Berlin Heidelberg New York.Google Scholar
  89. Vet, L. E. M. and Dicke, M. 1992. Ecology of infochemical use by natural enemies in a tritrophic context. Annu. Rev. Entomol. 37:141–172.CrossRefGoogle Scholar
  90. Wegener, R., Schulz, S., Meiners, T., Hadwich, K., and Hilker, M. 2001. Analysis of volatiles induced by oviposition of a phytophagous insect. J. Chem. Ecol. 27:499–515.CrossRefPubMedGoogle Scholar
  91. Yamasaki, M., Yoshimura, A., and Yasui, H. 2003. Genetic basic of ovicidal response to whitebacked planthopper (Sogatella furcifera Horvath) in rice (Oryza sativa L.). Mol. Breed. 12:133–143.CrossRefGoogle Scholar
  92. Zimmermann, S., Ehrhardt, T., Plesch, G., and Mueller-Roeber, B. 1999. Ion channels in plant signaling. Cell. Mol. Life Sci. 55:183–203.CrossRefGoogle Scholar
  93. Zuk, M. and Kolluru, G. R. 1998. Exploitation of sexual signals by predators and parasitoids. Q. Rev. Biol. 73:415–438.CrossRefGoogle Scholar
  94. Zweigelt, F. 1931. Blattlausgallen. Histologische und biologische Studien an Tetraneura- und Schizoneuragallen. Die Blattlausgallen im Dienste prinzipieller Gallenforschung. Monogr. Angew. Entomol. (Suppl. Z. Angew. Entomol. 27) 11:1–684.Google Scholar

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© Springer Science + Business Media, Inc. 2006

Authors and Affiliations

  1. 1.Freie Universität Berlin, Institut für BiologieBerlinGermany

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