The Botanical Review

, Volume 85, Issue 1, pp 78–106 | Cite as

Feeding and Other Gall Facets: Patterns and Determinants in Gall Structure

  • Bruno G. FerreiraEmail author
  • Rafael Álvarez
  • Gracielle P. Bragança
  • Danielle R. Alvarenga
  • Nicolás Pérez-Hidalgo
  • Rosy M. S. IsaiasEmail author


Galls are neoformed structures induced by specific animals, fungi, bacteria, virus or some parasitic plants on their host plant organs. Developmental processes are well known in Agrobacterium tumefasciens galls, but the animal-induced galls have a striking anatomical diversity, concerning several patterns, which were reunited herein. Anatomical traits observed in animal-induced galls involve manipulation of plant morphogenesis in convergent ways. Nematode, mite and insect galls usually contain homogeneous storage parenchyma and develop due to hyperplasia and cell hypertrophy. The development of typical nutritive tissues, giant cells, or hypertrophied vascular bundles may occur. Some other anatomical features may be usually restricted to galls induced by specific taxa, but they may eventually be related to the developmental potentialities of the host plants. The combination of distinct morphogenetic peculiarities in each gall system culminates in extant gall structural diversity. Convergent anatomical traits are observed according to the feeding mode of the gall inducers, representing potentiation or inhibition of similar events of host plant morphogenesis and cell redifferentiation, independent of gall-inducing taxa.


Cell redifferentiation Eriophyidae galls Insect galls Nematode galls Nutritive tissue Plant anatomy 



Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, Brazil) provided the scholarship for BGF doctoral internship in Universidad de León, Spain (99999.003956/2015-06); and doctoral scholarship for GPB and BGF. Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Brazil) provided a doctoral scholarship for BGF (140226/2017-6), a postdoctoral grant for BGF (171182/2017-0), and research grants for RMSI (307011/2015-1). Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG, Brazil) provided financial resources for project execution (APQ-02617-15), and a scholarship for DRA.


  1. Álvarez, R. 2011. Initial stages in the formation of galls induced by Geoica utricularia in Pistacia terebinthus leaflets: Origin of the two vascular bundles which characterize the wall of the galls. American Journal of Plant Sciences 2: 175–179.Google Scholar
  2. Álvarez, R., Encina, A. & Pérez-Hidalgo, N. 2009. Histological aspects of three Pistacia terebinthus galls induced by three different aphids: Paracletus cimiciformis, Forda marginata and Forda formicaria. Plant Science 176: 303–314.Google Scholar
  3. Álvarez, R., González-Sierra, S., Candelas, A. & Martinez, J.J.I.. 2013. Histological study of galls induced by aphids on leaves of Ulmus minor: Tetraneura ulmi induces globose galls and Eriosoma ulmi induces pseudogalls. Arthropod-Plant Interactions 7: 643–650.Google Scholar
  4. Álvarez, R., Martinez, J.J.I., Muñoz-Viveros, A.L., Molist, P., Abad-González, J. & Nieto-Nafría, J.M. 2016. Contribution of gall microscopic structure to taxonomy of gallicolous aphids. Plant Biology 8: 868–875.Google Scholar
  5. Álvarez, R., Molist, P., González-Sierra, S., Martinez, J.J.I. & Nieto-Nafría, J.M. 2014. The histo structure of galls induced by aphids as a useful taxonomic character: The case of Rectinasus (Hemiptera, Aphididae, Eriosomatinae). Zootaxa 3861: 487–492.Google Scholar
  6. Amorim, D.O., Ferreira, B.G. & Fleury, G. 2017. Plant potentialities determine anatomical and histochemical diversity in Mikania glomerata Spreng. Galls. Brazilian Journal of Botany 40: 517–527.Google Scholar
  7. Apel, K. & Hirt, H. 2004. Reactive oxygen species: Metabolism, oxidative stress, and signal transduction. Annual Review of Plant Biology 55: 373–399.Google Scholar
  8. Arduin, M. & Kraus, J.E. 1995 Anatomia e ontogenia das galhas foliares de Piptadenia gonoacantha (Fabales, Mimosaceae). Boletim de Botânica da Universidade de São Paulo 14: 109–130.Google Scholar
  9. Arduin, M., Kraus, J.E. 2001. Anatomia de galhas de ambrosia em folhas de Baccharis concinna e Baccharis dracunculifolia (Asteraceae). Brazilian Journal of Botany 24: 63–72.Google Scholar
  10. Arduin, M., Kraus, J.E., Otto, P.A. & Venturelli, M. 1989. Caracterização morfológica e biométrica de galhas foliares em Struthanthus vulgaris Mart. (Loranthaceae). Revista Brasileira de Biologia 49: 817–823.Google Scholar
  11. Arduin, M., Kraus, J.E., Fernandes, G.W. & Kraus, J.E. 2005. Morphogenesis of galls induced by Baccharopelma dracunculifoliae (Hemiptera: Psyllidae) on Baccharis dracunculifolia (Asteraceae) leaves. Brazilian Journal of Biology 65: 559–571.Google Scholar
  12. Barceló, R. 1997. Lignification in plant cell walls. International Review of Cytology 176: 87–132.Google Scholar
  13. Barnewall, E. & De Clerck-Floate, R.A. 2012. A preliminary histological investigation of gall induction in an unconventional galling system. Arthropod-Plant Interactions 6: 449–459.Google Scholar
  14. Bedetti, C.S., Ferreira, B.G., Castro, N.M. & Isaias, R.M.S. 2013. The influence of parasitoidism on the anatomical and histochemical profiles of the host leaves in a galling Lepidoptera–Bauhinia ungulata system. Revista Brasileira de Biociências 11: 242–249.Google Scholar
  15. Bedetti, C.S., Modolo, L.V. & Isaias, R.M.S. 2014. The role of phenolics in the control of auxin in galls of Piptadenia gonoacantha (Mart.) MacBr (Fabaceae: Mimosoideae). Biochemical Systematics and Ecology 55: 53–59.Google Scholar
  16. Begum, S., Nakaba, S., Oribe, Y., Kubo, T. & Funada, R. 2010. Changes in the localization and levels of starch and lipids in cambium and phloem during cambial reactivation by artificial heating of main stems of Cryptomeria japonica trees. Annals of Botany 106: 885–895.Google Scholar
  17. Bird, A.F. 1961. The ultrastructure and histochemistry of a nematode-induced giant cell. Journal of Biophysical and Biochemical Cytology 11: 701–715.Google Scholar
  18. Bragança, G.P., Oliveira, D.C. & Isaias, R.M.S. 2017. Compartmentalization of metabolites and enzymatic mediation in nutritive cells of Cecidomyiidae galls on Piper arboretum Aubl. (Piperaceae). Journal of Plant Studies 6: 11–22.Google Scholar
  19. Bronner, R. 1992. The role of nutritive cells in the nutrition of cynipids and cecidomyiids. Pp. 118–140. In: J.D. Shorthouse & O. Rohfritsch, (eds.), Biology of insect-induced galls. Oxford University Press, New York, USA.Google Scholar
  20. Brooks, S.E. & Shorthouse, J.D. 1998. Developmental morphology of stem galls of Diplolepis nodulosa (Hymenoptera: Cynipidae) and those modified by the inquiline Periclistus pirata (Hymenoptera: Cynipidae) on Rosa blanda (Rosaceae). Canadian Journal of Botany 76: 365–381.Google Scholar
  21. Burckhardt, D. 2005. Biology, ecology and evolution of gall-inducing psyllids. Pp. 143–157. In: A. Raman, C.W. Schaefer & T.M. Withers, (eds.), Biology, ecology and evolution of gall-inducing arthropods. Science Publishers Inc., Enfield, USA.Google Scholar
  22. Burckhardt, D., Queiroz, D.L. 2012. Checklist and comments on the jumping plant-lice (Hemiptera: Psylloidea) from Brazil. Zootaxa 3571: 26–48.Google Scholar
  23. Byers, J.A., Brewer, J.W. & Denna, D.W. 1976. Plant growth hormones in pinyon insect galls. Marcellia 39: 125–134.Google Scholar
  24. Carmona, D., Lajeunesse, M.J. & Johnson, M.T.J. 2011. Plant traits that predict resistance to herbivores. Functional Ecology 25: 305–432.Google Scholar
  25. Carneiro, R.G.S. & Isaias, R.M.S. 2014. Cytological cycles and fates in Psidium myrtoides are altered towards new cell metabolism and functionalities by the galling activity of Nothotrioza myrtoidis. Protoplasma 252: 637–646.Google Scholar
  26. Carneiro, R.G.S., & Isaias, R.M.S. 2015. Gradients of metabolite accumulation and redifferentiation of nutritive cells associated with vascular tissues in galls induced by sucking insects. AoB Plants 7: plv086.Google Scholar
  27. Carneiro, R.G.S., Castro, A.C. & Isaias, R.M.S. 2014a. Unique histochemical gradients in a photosynthesis-deficient plant gall. South African Journal of Botany 92: 97–104.Google Scholar
  28. Carneiro, R.G.S., Oliveira, D.C. & Isaias, R.M.S. 2014b. Developmental anatomy and immunocytochemistry reveal the neo-ontogenesis of the leaf tissues of Psidium myrtoides (Myrtaceae) towards the globoid galls of Nothotrioza myrtoidis (Triozidae). Plant Cell Reports 33: 2093–2106.Google Scholar
  29. Carneiro, R.G.S., Pacheco, P. & Isaias, R.M.S. 2015. Could the extended phenotype extend to the cellular and subcellular levels in insect-induced galls? PLoS One 10(6): e0129331.Google Scholar
  30. Castro, A.C.R., Oliveira, D.C. & Isaias, R.M.S. 2012. Morphological patterns of a hymenopteran gall on the leaflets of Caryocar brasiliense Camb. (Caryocaraceae). American Journal of Plant Sciences 3: 921–929.Google Scholar
  31. Chao, J.F. & Liao, G.I. 2013. Histocytological aspects of four types of ambrosia galls on Machilus zuihoensis Hayata (Lauraceae). Flora 208: 157–164.Google Scholar
  32. Crespi, B. & Worobey, M. 1998. Comparative analysis of gall morphology in Australian gall Thrips: The evolution of extended phenotypes. Evolution 52: 1686–1696.Google Scholar
  33. Csóka, G., Stone, G.N. & Melika, G. 2005. Biology, ecology and evolution of gall-inducing Cynipidae. Pp. 573–642. In: A. Raman, C.W. Schaefer & T.M. Withers, (eds.), Biology, ecology and evolution of gall-inducing arthropods. Science Publishers Inc., Enfield, USA.Google Scholar
  34. Di Vito, M., Vovlas, N. & Castillo, P. 2004. Host–parasite relationships of Meloidogyne incognita on spinach. Plant Pathology 53: 508–514.Google Scholar
  35. Dias, G.G., Ferreira, B.G., Moreira, G.R.P. & Isaias, R.M.S. 2013a. Developmental pathway from leaves to galls induced by a sap-feeding insect on Schinus polygamus (Cav.) Cabrera (Anacardiaceae). Anais da Academia Brasileira de Ciências 85: 187–200.Google Scholar
  36. Dias, G.G., Moreira, G.R.P., Ferreira, B.G. & Isaias, R.M.S. 2013b. Why do the galls induced by Calophya duvauae Scott on Schinus polygamus (Cav.) Cabrera (Anacardiaceae) change color? Biochemical Systematics and Ecology 48: 111–122.Google Scholar
  37. Dorchin, N., Freidberg, A. & Aloni, R. 2002. Morphogenesis of stem gall tissues induced by larvae of two cecidomyiid species (Diptera: Cecidomyiidae) on Suaeda monoica (Chenopodiaceae). Candaian Journal of Botany 80: 1141–1150.Google Scholar
  38. Dropkin, V.H. 1969. Cellular responses of plants to nematode infections. Annual Review of Phytopathology 7: 101–122.Google Scholar
  39. Espírito-Santo, M.M. & Fernandes, G.W. 2007. How many species of gall-inducing insects are there on earth, and where are they? Annals of the Entomological Society of America 100: 95–99.Google Scholar
  40. Evert, R.F. 2006. Esau's plant anatomy: Meristems, cells, and tissues of the plant body: Their structure, function, and development. John Wiley & Sons, New Jersey, USA.Google Scholar
  41. Fagan, M.M. 1918. The uses of insect galls. The American Naturalist 52: 155–176.Google Scholar
  42. Favery, B., Quentin, M., Jaubert-Possamai, S. & Abad, P. 2016. Gall-forming root-knot nematodes hijack key plant cellular functions to induce multinucleate and hypertrophied feeding cells. Journal of Insect Physiology 84: 60–69.Google Scholar
  43. Felt, E.P. 1936. The relations of insects and plants in gall production. Annals of the Entomological Society of America 29: 694–700.Google Scholar
  44. Fernandes, G.W. & Price, P.W. 1992. The adaptive significance of insect gall distribution: Survivorship of species in xeric and Mesic habitats. Oecologia 90: 14–20.Google Scholar
  45. Fernandes, G.W., Carneiro, M.A.A. & Isaias, R.M.S. 2012. Gall-inducing insects: From anatomy to biodiversity. Pp. 369–395. In: A.R. Panizzi & J.R.P. Parra, (eds.), Insect bioecology and nutrition for integrated pest management. CRC Press, Boca Raton, USA.Google Scholar
  46. Ferreira, B.G. & Isaias, R.M.S. 2013. Developmental stem anatomy and tissue redifferentiation induced by a galling Lepidoptera on Marcetia taxifolia (Melastomataceae). Botany 91: 752–760.Google Scholar
  47. Ferreira, B.G., & Isaias, R.M.S. 2014. Floral-like destiny induced by a galling Cecidomyiidae on the axillary buds of Marcetia taxifolia (Melastomataceae). Flora 209: 391–400.Google Scholar
  48. Ferreira, B.G., Álvarez, R., Avritzer, S.C. & Isaias, R.M.S. 2017a. Revisiting the histological patterns of storage tissues: Beyond the limits of gall-inducing taxa. Botany 2017a;95: 173–184.Google Scholar
  49. Ferreira, B.G., Avritzer, S.C. & Isaias, R.M.S. 2017b. Totipotent nutritive cells and indeterminate growth in galls of Ditylenchus gallaeformans (Nematoda) on reproductive apices of Miconia. Flora 227: 36–45.Google Scholar
  50. Ferreira, B.G., Carneiro, R.G.S. & Isaias, R.M.S. 2015. Multivesicular bodies differentiate exclusively in nutritive fast-dividing cells in Marcetia taxifolia galls. Protoplasma 252: 1275–1283.Google Scholar
  51. Ferreira, B.S., Falcioni, R., Guedes, L.M., Avritzer, S.C., Antunes, W.C., Souza, L.A. & Isaias, R.M.S. 2017c. Preventing false negatives for histochemical detection of phenolics and lignins in PEG-embedded plant tissues. Journal of Histochemistry and Cytochemistry 65: 105–116. Google Scholar
  52. Ferreira, B.S., Oliveira, D.C., Moreira, A.S.F.P., Faria, A.P., Guedes, L.M., França, M.G.C., Álvarez, R. & Isaias, R.M.S. 2018. Antioxidant metabolism in galls due to the extended phenotypes of the associated organisms. PLoS ONE 13: e0205364.Google Scholar
  53. Finley, A.M. 1981. Histopathology of Meloidogyne chitwoodi (Golden et al.) on russet Burbank potato. Journal of Nematology 13: 486–491.Google Scholar
  54. Fleury, G., Ferreira, B.G., Oliveira, D.C., Soares, G.L.G. & Isaias, R.M.S. 2015. Elucidating the determination of the rosette galls induced by Pisphondylia brasiliensis Couri & Maia 1992 (Cecidomyiidae) on Guapira opposita (Vell.) Reitz (Nyctaginaceae). Australian Journal of Botany 63: 608–617.Google Scholar
  55. Formiga, A.T., Soares, G.L.G. & Isaias, R.M.S. 2011. Responses of the host plant tissues to gall induction in Aspidosperma spruceanum Müell. Arg. (Apocynaceae). American Journal of Plant Sciences 2: 823–834.Google Scholar
  56. Formiga, A.T., Oliveira, D.C., Ferreira, B.G., Magalhães, T.A., Castro, A.C., Fernandes, G.W. & Isaias, R.M.S. 2013. The role of pectic composition of cell walls in the determination of the new shape-functional design in galls of Baccharis reticularia (Asteraceae). Protoplasma 250: 899–908.Google Scholar
  57. Formiga, A.T., Silveira, F.A.O., Fernandes, G.W. & Isaias, R.M.S. 2015. Phenotypic plasticity and similarity among gall morphotypes on a superhost, Baccharis reticularia (Asteraceae). Plant Biology 17: 512–521.Google Scholar
  58. Gonçalves, S.J.M.R., Isaias, R.M.S., Vale, F.H.A. & Fernandes, G.W. 2005. Sexual dimorphism of Pseudotectococcus rolliniae Hodgson & Gonçalves 2004 (Hemiptera Coccoidea Eriococcidae) influences gall morphology on Rollinia laurifolia Schltdl. (Annonaceae). Tropical Zoology 18: 161–169.Google Scholar
  59. Gonçalves, S.J.M.R., Moreira, G.R.P., Isaias, R.M.S. 2009. A unique seasonal cycle in a leaf gall-inducing insect: The formation of stem galls for dormancy. Journal of Natural History 43: 843–854.Google Scholar
  60. Goodey, J.B. 1939. The structure of the leaf galls of Plantago lanceolata L. induced by Anguillulina dipsaci (Kühn) Gerv. & v. Ben. Journal of Helminthology 17: 183–190.Google Scholar
  61. Goodey, J.B. 1948. The galls caused by Anguillulina balsamophila (Thorne) Goodey on the leaves of Wyethia amplexicaulis Nutt. And Balsamorhiza sagittata Nutt. Journal of Helminthology 22: 109–116.Google Scholar
  62. Gopinathan, K. & Ananthakrishnan, T.N. 1985. Morphogenesis and histochemistry of some thrips (Thysanoptera: Insecta) induced galls. PNAS B51: 413–456.Google Scholar
  63. Harris, K.M. 1994. Gall midges (Cecidomyiidae): Classification and biology. In: M.A.J. Williams, (ed.), Plant galls: Organisms, interactions, populations. The Systematics Association Special Volume. 49: 201–211.Google Scholar
  64. Hodgson, C., Oliveira, D.C. & Isaias, R.M.S. 2013. A new gall-inducing genus and species of Eriococcidae (Hemiptera: Sternorrhyncha: Coccoidea) on Sapindaceae from Brazil. Zootaxa 3734: 317–330.Google Scholar
  65. Hodkinson, I.P. 1984. The biology and ecology of the gall-forming Psylloidea (Homoptera). Pp. 59–77. In: T.N. Ananthakrishnan, (ed.), Biology of gall insects. Oxford & IBH Publishing Co., New Delhi, India.Google Scholar
  66. Hough, J.S. 1953. Studies on the common spangle gall of oak. II. A general consideration of past work on gall induction. New Phytologist 52: 218–228.Google Scholar
  67. Hori, K. 1992. Insect secretions and their effect on plant growth, with special reference to hemipterans. Pp. 157–170. In: J.D. Shorthouse & O. Rohfritsch, (eds.), Biology of insect-induced galls. Oxford University Press, New York, USA.Google Scholar
  68. Inbar, M., Eshel, A. & Wool, D. 1995. Interspecific competition among phloem-feeding insects mediated by induced host–plant sinks. Ecology 76: 1506–1515.Google Scholar
  69. Isaias, R.M.S., Oliveira, D.C. & Carneiro, R.G.S. 2011. Role of Euphalerus ostreoides (Hemiptera: Psylloidea) in manipulating leaflet ontogenesis of Lonchocarpus muehlbergianus (Fabaceae). Botany 89: 581–592.Google Scholar
  70. Isaias, R.M.S., Carneiro, R.G.S., Oliveira, D.C. & Santos, J.C. 2013. Illustrated and annotated checklist of Brazilian gall morphotypes. Neotropical Entomology 42:230–239.Google Scholar
  71. Isaias, R.M.S., Oliveira, D.C., Moreira, A.S.F.P., Soares, G.L.G. & Carneiro, R.G.S. 2015. The imbalance of redox homeostasis in arthropod-induced plant galls: Mechanisms of stress generation and dissipation. Biochimica et Biophysica Acta 1850: 1509–1517.Google Scholar
  72. Isaias, R.M.S., Ferreira, B.G., Alvarenga, D.R., Barbosa, L.R., Salminen, J.-P. & Steinbauer, M.J. 2018. Functional compartmentalisation of nutrients and phenolics in the tissues of galls induced by Leptocybe invasa (Hymenoptera: Eulophidae) on Eucalyptus camaldulensis (Myrtaceae). Austral Entomology 57: 238–246.Google Scholar
  73. Jones, M.G.K. & Northcote, D.H. 1972. Nematode-induced syncytium – A multinucleate transfer cell. Journal of Cell Science 10: 789–809.Google Scholar
  74. Jorge, N.C., Cavalleri, A., Bedetti, C. & Isaias, R.M.S. 2016. A new leaf-galling Holopothrips (Thysanoptera: Phlaeothripidae) and the structural alterations on Myrcia retorta (Myrtaceae). Zootaxa 4200: 174–180.Google Scholar
  75. Jorge, N.C., Alvarenga, D.R., Cavalleri, A. & Isaias, R.M.S. 2018a. Anatomical and histometric explanations for leaf folding on Holopothrips striatus galls in Myrcia retorta. Flora 244–245: 24–28.Google Scholar
  76. Jorge, N.C., Souza-Silva, E.S., Alvarenga, D.R., Saboia, G., Soares, G.L.G., Zini, C.A., Cavalleri, A. & Isaias, R.M.S. 2018b. Structural and chemical profiles of Myrcia splendens (Myrtaceae) leaves under the influence of the galling Nexothrips sp. (Thysanoptera). Frontiers in Plant Science 9: 1521.Google Scholar
  77. Kendall, J. 1930. The structure and development of certain eriophyid galls. Zeitschrift Fur Parasitenkunde 2: 477–501.Google Scholar
  78. Kjer, K.M., Carle, F.M., Litman, J. & Ware, J. 2006. A molecular phylogeny of Hexapoda. Arthropod Systematics & Phylogeny 64: 35–44.Google Scholar
  79. Korotyaev, B.A., Konstantinov, A.S., Lingafelter, S.W., Mandelshtam, M.Y. & Volkovitsh, M.G. 2005. Gall-inducing Coleoptera. Pp. 239–271. In: A. Raman, C.W. Schaefer & T.M. Withers, (eds.), Biology, ecology and evolution of gall-inducing arthropods. Science Publishers Inc., Enfield, USA.Google Scholar
  80. Kostoff, D. & Kendall, J. 1929. Studies on the structure and development of certain Cynipid galls. Biological Bulletin 56: 402–458.Google Scholar
  81. Kraus, J.E. & Tanoe, M. 1999. Morpho-ontogenetic aspects of entomogenous galls in roots of Cattleya guttata (Orchidaceae). Lindleyana 14: 204–213.Google Scholar
  82. Kraus, J.E., Arduin, M. & Venturelli, M. 2002. Anatomy and ontogenesis of hymenopteran leaf galls of Struthanthus vulgaris Mart. (Loranthaceae). Revista Brasileira de Botânica 25: 449–458.Google Scholar
  83. Krusberg, L.R. 1963. Host response to nematode infection. Annual Review of Phytopathology 1: 219–240.Google Scholar
  84. Kurzfeld-Zexer, L., Lev-Yadun, S. & Inbar, M. 2015. One aphid species induces three gall types on a single plant: Comparative histology of one genotype and multiple extended phenotypes. Flora 210: 19–30.Google Scholar
  85. Küster, E. 1911. Dier Gallen der Pflanzen. S. Hirzel, Leipzig, Germany.Google Scholar
  86. Larew, H.G. 1981. A comparative anatomical study of galls caused by the major cecidogenetic groups, with special emphasis on the nutritive tissue. PhD Thesis, Oregon State University, USA. Available from:
  87. Lev-Yadun, S. 2003. Stem cell in plants are differentiated too. Current Topics in Plant Bioogy 4: 93–100.Google Scholar
  88. Magalhães, T.A., Oliveira, D.C., Isaias, R.M.S. 2015. Population dynamics of the gall inducer Eriogallococcus isaias (Hemiptera: Coccoidea: Eriococcidae) on Pseudobombax grandiflorum (Malvaceae). Journal of Natural History 49: 789–801.Google Scholar
  89. Magalhães, T.A., Oliveira, D.C., Suzuki, A.Y.M. & Isaias, R.M.S. 2014. Patterns of cell elongation in the determination of the final shape in galls of Baccharopelma dracunculifoliae (Psyllidae) on Baccharis dracunculifolia DC (Asteraceae). Protoplasma 251: 747–753.Google Scholar
  90. Mani, M.S. 1964. Ecology of plant galls. Dr. W. Junk Publishers, The Hague, Netherlands.Google Scholar
  91. Mani, M.S. 1992. Introduction to Cecidology. Pp. 3–7. In: J.D. Shorthouse & O. Rohfritsch, (eds.), Biology of insect induced galls. Oxford University Press, New York, USA.Google Scholar
  92. Mapes, C.C. & Davies, P.J. 2001. Indole-3-acetic acid and ball gall development on Solidago altissima. New Phytologist 151: 195–202.Google Scholar
  93. McCalla, D.R., Genthe, M. & Hovanitz, W. 1962. Chemical nature of an insect gall growth-factor. Plant Physiology 37: 98–103.Google Scholar
  94. Meyer, J. & Maresquelle, H.J. 1983. Anatomie des galles. Gebrüder Borntraeger, Berlin, Germany.Google Scholar
  95. Meyer, J. 1987. Plant galls and gall inducers. Gebrüder Borntraeger, Berlin, Germany.Google Scholar
  96. Miller, W.E. 2005. Gall-inducing Lepidoptera. Pp. 431–465. In: A. Raman, C.W. Schaefer & T.M. Withers, (eds.), Biology, ecology and evolution of gall-inducing arthropods. Science Publishers Inc., Enfield, USA.Google Scholar
  97. Mound, L.A. 1994. Thrips and gall induction: A search for patterns. Pp. 131–149. In: M.A.J. Williams, (ed.), Plant galls: Organisms, interactions, populations. The Systematics Association Special Volume 49: 131–149.Google Scholar
  98. Mound, L.A., & Morris, D.C. 2005. Gall-inducing Thrips: An evolutionary perspective. Pp. 59–72. In: Raman, C.W. Schaefer & T.M. Withers, (eds.), Biology, ecology and evolution of gall-inducing arthropods. Science Publishers Inc., Enfield, USA.Google Scholar
  99. Moura, M.Z.D., Soares, G.L.G. & Isaias, R.M.S. 2008. Species-specific changes in tissue morphogenesis induced by two arthropod leaf gallers in Lantana camara L. (Verbenaceae). Australian Journal of Botany 56: 153–160.Google Scholar
  100. Moura, M.Z.D., Soares, G.L.G., Alves, T.M.A. & Isaias, R.M.S. 2009a. Intra-specific phenotypic variations in Lantana camara leaves affect host selection by the gall maker Aceria lantanae. Biochemical Systematics and Ecology 37: 541–548.Google Scholar
  101. Moura, M.Z.D., Soares, G.L.G., & Isaias, R.M.S. 2009b. Ontogênese da folha e das galhas induzidas por Aceria lantanae Cook (Acarina: Eriophyidae) em Lantana camara L. (Verbenaceae). Revista Brasileira de Botânica 32: 271–282.Google Scholar
  102. Muñoz-Viveros, A.L., Martinez, J.J.I., Molist, P., González-Sierra, S., González, P. & Álvarez, R. 2014. Microscopic study of galls induced by three species of Geopemphigus (Hemiptera: Aphididae: Eriosomatinae) on Pistacia mexicana. Arthropod-Plant Interactions 8: 531–538.Google Scholar
  103. Münzenberger, B., Schneider, B., Nilsson, R.H., Bubner, B., Larsson, K.H. & Hüttl, R.F. 2012. Morphology, anatomy, and molecular studies of the ectomycorrhizal formed axenically by the fungus Sistotrema sp. (Basidiomycota). Mycological Progress 11: 817–826.Google Scholar
  104. Nylund, J.E. & Unestam, T. 1982. Structure and physiology of ectomycorrhizae. New Phytologist 91: 63–79.Google Scholar
  105. Nyman, T., Widmer, A. & Roiniken, H. 2000. Evolution of gall morphology and host-plant relationships in willow-feeding sawflies (Hymenoptera: Tenthredinidae). Evolution 54: 526–533.Google Scholar
  106. Oldfield, G.N. 2005. Biology of gall-inducing Acari. Pp. 35–58. In: A. Raman, C.W. Schaefer & T.M. Withers, (eds.), Biology, ecology and evolution of gall-inducing arthropods. Science Publishers Inc., Enfield, USA.Google Scholar
  107. Oliveira, D.C. & Isaias, R.M.S. 2010a. Cytological and histochemical gradients induced by a sucking insect in galls of Aspidosperma australe Arg. Muell (Apocynaceae). Plant Science 178: 350–358.Google Scholar
  108. Oliveira, D.C., Isaias, R.M.S. 2010b. Redifferentiation of leaflet tissues during midrib gall development in Copaifera langsdorffii (Fabaceae). South African Journal of Botany 76: 239–248.Google Scholar
  109. Oliveira, D.C., Carneiro, R.G.S., Magalhães, T.A. & Isaias, R.M.S. 2011. Cytological and histochemical gradients on two Copaifera langsdorffii Desf. (Fabaceae) – Cecidomyiidae gall systems. Protoplasma 248: 829–837.Google Scholar
  110. Oliveira, D.C., Isaias, R.M.S., Fernandes, G.W., Ferreira, B.G., Carneiro, R.G.S. & Fuzaro, L. 2016. Manipulation of host plant cells and tissues by gall-inducing insects and adaptive strategies used by different feeding guilds. Journal of Insect Physiology 84: 103–113.Google Scholar
  111. Oliveira, D.C., Magalhães, T.A., Ferreira, B.G., Teixeira, C.T., Formiga, A.T., Fernandes, G.W. & Isaias, R.M.S. 2014. Variation in the degree of pectin methylesterification during the development of Baccharis dracunculifolia kidney-shaped gall. PLoS One 9: e94588.Google Scholar
  112. Portugal-Santana, A. & Isaias, R.M.S. 2014. Galling insects are bioindicators of environmental quality in a conservation unit. Acta Botanica Brasilica 28(4): 594–608.Google Scholar
  113. Price, P.W., Fernandes, G.W. & Waring, G.L. 1987. Adaptive nature of insect galls. Environmental Entomology 16: 15–24.Google Scholar
  114. Raman, A. 2012. Gall induction by hemipteroid insects. Journal of Plant Interactions 7: 29–44.Google Scholar
  115. Raman, A., & Ananthakrishnan, T.N. 1983. Studies on some thrips (Thysanoptera: Insecta) induced galls. 2. Fine-structure of the nutritive zone. Proceedings of the Indian National Science Academy. Part B, Biological Sciences 49: 525–561.Google Scholar
  116. Raman, A., Schaefer, C.W. & Withers, T.M. 2005. Biology, ecology and evolution of gall-inducing arthropods. Science Publishers Inc., Enfield, USA.Google Scholar
  117. Rancic, D., Stevanovic, B., Petanović, R., Magud, B., Tosevski, I. & Gassmann, A. 2006. Anatomical injury induced by the eriophyid mite Aceria anthocoptes on the leaves of Cirsium arvense. Experimental and Applied Acarology 38: 243–253.Google Scholar
  118. Richardson, R.A., Body, M., Warmund, M.R., Schultz, J.C. & Appel, H.M. 2017. Morphometric analysis of young petiole galls on the narrow-leaf cottonwood, Populus angustifolia, by the sugarbeet root aphid, Pemphigus betae. Protoplasma 254: 203–216.Google Scholar
  119. Rodiuc, N., Vieira, P., Banora, M.Y. & Engler, J.A. 2014. On the track of transfer cell formation by specialized plant-parasitic nematodes. Frontiers in Plant Sciences 5: 1–14.Google Scholar
  120. Rohfritsch, O. 1992. Patterns in gall development. Pp. 60–86. In: J.D. Shorthouse & O. Rohfritsch, (eds.), Biology of insect induced galls. Oxford University Press, New York, USA.Google Scholar
  121. Rohfritsch, O. 2008. Plants, gall midges, and fungi: A three-component system. Entomologia Experimentalis et Applicata 128: 208–216.Google Scholar
  122. Roskam, J.C. 1992. Evolution of the gall-inducing guild. Pp. 34–49. In: J.D. Shorthouse & O. Rohfritsch, (eds.), Biology of insect induced galls. Oxford University Press, New York, USA.Google Scholar
  123. Sá, C.E.M., Silveira, F.A.O., Santos, J.C., Isaias, R.M.S. & Fernandes, G.W. 2009. Anatomical and developmental aspects of leaf galls induced by Schizomyia macrocapillata Maia (Diptera: Cecidomyiidae) on Bauhinia brevipes Vogel (Fabaceae). Brazilian Journal of Botany 32: 319–327.Google Scholar
  124. Sano, M. & Akimoto, S.-Y. 2011. Morphological phylogeny of gall-forming aphids of the tribe Eriosomatini (Aphididae: Eriosomatinae). Systematic Entomology 36: 607–627.Google Scholar
  125. Schreuder, M.D.J., Brewer, C.A. & Heine, C. 2001. Modelled influences of non-exchanging trichomes on leaf boundary layers and gas exchange. Journal of Theoretical Biology 210: 23–32.Google Scholar
  126. Shorthouse, J.D., Wool, D. & Raman, A. 2005. Gall-inducing insects—nature’s most sophisticated herbivores. Basic and Applied Ecology 6: 407–411.Google Scholar
  127. Sinnott, E.W. 1960. Plant morphogenesis. McGraw-HillBook Co. Inc., New York, USA.Google Scholar
  128. Skinner, J.A., Orr, C.C. & Robinson, A.F. 1980. Histopathogenesis of the galls induced by Nothanguina phyllobia in Solanum elaeagnifolium. Journal of Nematology 12: 141–150.Google Scholar
  129. Souza, S.C.P.M., Kraus, J.E., Isaias, R.M.S. & Neves, L.J. 2000. Anatomical and ultrastructural aspects of leaf galls in Ficus microcarpa L. F. (Moraceae) induced by Gynaikothrips ficorum Marchal (Thysanoptera). Acta Botanica Brasilica 14: 57–69.Google Scholar
  130. Stone, G.N. & Schonrögge, K. 2003. The adaptive significance of insect gall morphology. Trends Ecology and Evolution 18: 512–522.Google Scholar
  131. Suzuki, A.Y.M., Bedetti, C.S., Isaias, R.M.S. 2015. Detection and distribution of cell growth regulators and cellulose microfibrils during the development of Lopesia sp. galls on Lonchocarpus cultratus (Fabaceae). Botany 93: 435–444.Google Scholar
  132. Taiz, L., Zeiger, E., Moller, I.M. & Murphy, A. 2015. Plant physiology and development. 6th. ed. Sinauer Associates, Sunderland, UK.Google Scholar
  133. Tooker, J.F. & Helms, A.M. 2014. Phytohormone dynamics associated with gall insects, and their potential role in the evolution of the gall-inducing habit. Journal of Chemical Ecology 40: 742–753.Google Scholar
  134. Vecchi, C., Menezes, N.L., Oliveira, D.C., Ferreira, B.G. & Isaias, R.M.S. 2013. The redifferentiation of nutritive cells in galls induced by Lepidoptera on Tibouchina pulchra (Cham.) Cogn. Reveals predefined patterns of plant development. Protoplasma 250: 1363–1368.Google Scholar
  135. Watson, A.K. & Shorthouse, J.D. 1979. Gall formation on Cirsium arvense by Ditylenchus dipsaci. Journal of Nematology 11: 16–22.Google Scholar
  136. Weischer, B. & Wyss, U. 1976. Feeding behaviour and pathogenicity of Xiphinema index on grapevine roots. Nematologica 22: 319–325.Google Scholar
  137. Wells, B.W. 1920. Early stages in the development of certain Pachypsylla galls on Celtis. American Journal of Botany 7: 275–285.Google Scholar
  138. Westphal, E., Bronner, R. & Le Ret, M. 1981. Changes in leaves of susceptible and resistant Solanum dulcamara infested by the gall mite Eriophyes cladophthirus (Acarina, Eriophyoidea). Canadian Journal of Botany 59: 875–882.Google Scholar
  139. White, O.E. 1948. Fasciation. The Botanical Review 14: 319–358.Google Scholar
  140. Williams, M.A.J. 1994. Plant galls: Organisms, interactions, populations. The systematics association special volume 49. The Systematics Association, Oxford, UK.Google Scholar
  141. Wool, D. 2004. Galling aphids: Specialization, biological complexity, and variation. Annual Review of Entomology 49: 175–192.Google Scholar
  142. Wyss, U. 1997. Root parasitic nematodes: An overview. Pp. 5–22. In: C. Fenoll, F.M.W. Grundler & S.A. Ohl, (eds.), Cellular and molecular aspects of plant-nematode interactions. Kluwer Academic Publishers, Dordrecht, Netherlands.Google Scholar
  143. Wyss, U. 2002. Feeding behavior of plant-parasitic nematodes. Pp. 462–513. In: D. Lee, (ed.), The biology of nematodes. CRC Press, London, UK.Google Scholar
  144. Yang, M.M., Mitter, C. & Miller, D.R. 2001. First incidence of inquilinism in gall-forming psyllids, with a description of the new inquiline species (Insecta, Hemiptera, Psylloidea, Psyllidae, Spondyliaspidinae). Zoologica Scripta 30: 97–113.Google Scholar
  145. Yousif, G.M. 1979. Histological responses of four leguminous crops infected with Meloidogyne incognita. Journal of Nematology 11: 395–401.Google Scholar
  146. Zha, Y.-P., Yang, Z.-X., Chen, J.-Y. & Cai, S.-S. 2016. Relationship between population dynamics and gall development of the gall aphid Kaburagia rhusicola (Hemiptera: Aphididae). Acta Entomologica Sinica 59: 791–796.Google Scholar

Copyright information

© The New York Botanical Garden 2019

Authors and Affiliations

  • Bruno G. Ferreira
    • 1
    • 2
    Email author
  • Rafael Álvarez
    • 3
  • Gracielle P. Bragança
    • 2
  • Danielle R. Alvarenga
    • 2
  • Nicolás Pérez-Hidalgo
    • 4
  • Rosy M. S. Isaias
    • 2
    Email author
  1. 1.Department of Botany, Instituto de BiologiaUniversidade Federal do Rio de JaneiroRio de JaneiroBrazil
  2. 2.Department of BotanyUniversidade Federal de Minas GeraisBelo HorizonteBrazil
  3. 3.Department of Molecular BiologyUniversidad de LeónLeónSpain
  4. 4.Department of Genetics, Instituto Cavanilles de Biodiversidad y Biología EvolutivaUniversidad de ValenciaValenciaSpain

Personalised recommendations