Luana Pfeffer, Uiara Costa Rezende, Gudryan Jackson Barônio, Denis Coelho de Oliveira


Galls are specific interactions between specialist herbivores and their host plants. They are considered neoformed plant organs developed from cellular hypertrophy, tissue hyperplasia and cellular redifferentiation of the host tissues. Among several organisms capable of inducing galls, insects induce them with high morphological complexity. The induction and development of galls depend on the availability of responsive sites in the host plant that react to the chemical and/or mechanical stimuli of galling insects. The synchronization between the timing of availability of these responsive sites and the galling insect life cycle is essential for the establishment of the interaction. Galling insects are subject to several chemical, physiological and phenological changes in their host plant. Thus, changes in the host cycle may alter the insect's life cycle, distribution and abundance. This study focused on the morphological aspects and phenological relationship of the Matayba guianensis Aubl. (Sapindaceae) – Bystracoccus mataybae Hodgson, Isaias & Oliveira (Eriococcidae) system, carried out in a semi-deciduous forest located at the Estação Ecológica do Panga (EEP), Uberlândia, MG, Brazil. We monitored the host plant phenology monthly from April 2015 to April 2016, and galls were sampled throughout the year to determine the stage of development of the galling insect. During leaf flushing, galling insects were collected every two days. The second-instar nymph induced leaf galls during leaf sprouting (peaks in September and October). The growth, development and maturation of the gall and of the galling insect occur concomitant to leaf maturation (peaks from February to May). Before the first leaves fall (August), the first-instar nymph moves from the senescent leaflet gall to branches and induces a stem gall, where it remains during part of the dry season until the next leaf flush. The synchrony between the life cycle of the galling insect and the host plant phenology maintains the univoltine cycle.


insect galls; insect–plant interaction; leaf galls; phenological synchrony; stem galls

Full Text:



Agostinelli, C., & Lund, U. 2013. R package circular: Circular Statistics (version 0.4-3). https://r-forge. r-project. org/projects/circular

Alvarez, C. A., Stape, J. L., Sentelhas, P. C., Gonçalves, J. L. M., & Sparovek, G. Köppen’s climate classification map for Brazil. Meteorologische Zeitschrift, 22(6), 711‒728. DOI: 10.1127/0941-2948/2013/0507

Arduin, M., & Kraus, J. E. 2001. Anatomia de galhas de ambrosia em folhas de Baccharis concinna e Baccharis dracunculifolia (Asteraceae). Revista Brasileira de Botânica, 24(1), 63‒72. DOI: 10.1590/S0100-84042001000100007

Bartlett, L., & Connor, E. F. 2014. Exogenous phytohormones and the induction of plant galls by insects. Arthropod-Plant Interactions, 8(4), 339‒348. DOI: 10.1007/s11829-014-9309-0

Bencke, C. S. A., & Morellato, L. P. C. 2002. Comparação de dois métodos de avaliação da fenologia de plantas, sua interpretação e representação. Revista Brasileira de Botânica, 25(3), 269‒275. DOI: 10.1590/S0100-84042002000300003

Bronner, R. 1992. The role of nutritive cells in the nutrition of cynipids and cecidomyiids. In: J. D. Shorthouse & O. Rohfritsch (Eds.), Biology of insect induced galls. pp. 118‒140. Oxford: Oxford University Press.

Bukatsch, F. 1972. Bermerkungen zur Doppelfärbung Astrablau-Safranin. Mikrokosmos, 61, 255.

Campos, P. T., Costa, M. C. D., Isaias, R. M. S., Moreira, A. S. F. P., Oliveira, D. C., & Lemos Filho, J. P. 2010. Phenological relationships between two insect galls and their host plants: Aspidosperma australe and A. spruceanum (Apocynaceae). Acta Botânica Brasílica, 24(3), 727–733. DOI: 101590/S0102-33062010000300016

Castro, A. C., Oliveira, D. C., Moreira, A. S. F. P., Lemos-Filho, J. P., & Isaias, R. M. S. 2012. Source–sink relationship and photosynthesis in the horn-shaped gall and its host plant Copaifera langsdorffii Desf. (Fabaceae). South African Journal of Botany, 83, 121‒126. DOI: 10.1016/j.sajb.2012.08.007

Floate, K. D., Fernandes, G. W., & Nilsson, J. A. 1996. Distinguishing intrapopulational categories of plants by their insect faunas: galls on rabbitbrush. Oecologia, 105, 221‒229. DOI: 10.1007/BF00328550

Fournier, L. A. 1974. Un método cuantitativo para la medición de características fenológicas em árboles. Turrialba, 24, 422‒423.

Gonçalves, S. J. M. R., Isaias, R. M. S., Vale, F. H. A., & Fernandes, G. W. 2005. Sexual dimorphism of Pseudotectococcus rolliniae Hodgson & Gonçalves (Hemiptera: Coccoidea: Eriococcidae) influences gall morphology on Rollinia laurifolia Schltdl. (Annonaceae). Tropical Zoology, 18(2), 161‒169. DOI: 10.1080/03946975.2005.10531219

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(13‒14), 843‒854. DOI: 10.1080/00222930802615690

Gullan, P. J., Miller, D. R., & Cook, L. G. 2005. Gall-inducing scale insects (Hemiptera: Sternorrhyncha: Coccoidea). In: A. Raman, C. W. Schaefer, & T. M. Withers (Eds.), Biology, ecology, and evolution of gall-inducing arthropods. pp. 159–229. Enfield: Science Publishers.

Hodgson, C., Isaias, R. M., & Oliveira, D. C. 2013. A new gall-inducing genus and species of Eriococcidae (Hemiptera: Sternorrhyncha: Coccoidea) on Sapindaceae from Brazil. Zootaxa, 3734(3), 317‒330. DOI: 10.11646/zootaxa.3734.3.2

Huberty, A. F., & Denno, R. F. 2004. Plant water stress and its consequences for herbivorous insects: a new synthesis. Ecology, 85(5), 1383‒1398. DOI: 10.1890/03-0352

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(9), 581‒59. DOI: 10.1139/b11-048

Kraus, J. E., & Arduin, M. 1997. Manual Básico de Métodos em Morfologia vegetal. Seropédica, Rio de Janeiro: Editora da Universidade Federal Rural do Rio de Janeiro: p. 198.

Lemos-Filho, J. P., & Mendonça-Filho, C. V. 2000. Seasonal changes in the water status of three woody legumes from the Atlantic forest, Caratinga, Brazil. Journal of Tropical Ecology, 16(1), 21‒32.

Lenza, E., & Klink, C. A. 2006. Comportamento fenológico de espécies lenhosas em um cerrado sentido restrito de Brasília, DF. Revista Brasileira de Botânica, 29, 627‒638.

Magalhães, T. A., Oliveira, D. C., & Isaias, R. M. 2015. Population dynamics of the gall inducer Eriogallococcus isaias (Hemiptera: Coccoidea: Eriococcidae) on Pseudobombax grandiflorum (Malvaceae). Journal of Natural History, 49(13‒14), 789‒801. DOI: 10.1080/00222933.2014.951083

Mani, M. S. 1964. Ecology of plant galls. Dordrecht: Springer-Science+Business Media: p. 434.

Meyer, J., & Maresquelle, H. J. 1983. Anatomie des Galles. Berlin: Gebrüder Borntraeger: p. 662.

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 (Verbenaceae). Australian Journal of Botany, 56(2), 153‒160. DOI: 10.1071/BT07131

Myers, B. A., Williams, R. J., Fordyce, I., Duff, G. A., & Eamus, D. 1998. Does irrigation affect leaf phenology in deciduous and evergreen trees of the savannas of northern Australia? Australian Journal of Ecology, 23, 329‒239. DOI: 10.1111/j.1442-9993.1998.tb00738.x

O‘Brien, T. P, & Mccully, M. E. 1981. The study of plant structure principles and selected methods. Melbourne: Termarcarphi p. 357

Oliveira, D. C., & Isaias, R. M. S. 2009. Influence of leaflet age in anatomy and possible adaptive values of the midrib gall of Copaifera langsdorffii (Fabaceae: Caesalpinioideae). Revista de Biologia Tropical, 57(1‒2), 293‒302.

Oliveira, D. C., & Isaias, R. M. S. 2010. Cytological and histochemical gradients induced by a sucking insect in galls of Aspidosperma australe Arg. Muell (Apocynaceae). Plant Science, 178(4), 350‒358. DOI: 10.1016/j.plantsci.2010.02.002

Oliveira, D. C., Christiano, J. C. S., Soares, G. L. G., & Isaias, R. M. S. 2006. Structural and chemical defensive reactions of Lonchocarpus muehlbergianus Hassl. (Fabaceae) to Euphalerus ostreoides Crawf. (Hemiptera: Psyllidae) galling stimuli. Revista Brasileira de Botânica, 29(4), 657‒667. DOI: 10.1590/S0100-84042006000400015

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 adaptative strategies used by different feeding guilds. Journal of Insect Physiology, 84, 103‒113. DOI: 10.1016/j.jinsphys.2015.11.012

Oliveira, D. C., Magalhães, T. A., Carneiro, R. G. S., Alvim, M. N., & Isaias, R. M. S. 2010. Do Cecidomyiidae galls of Aspidosperma spruceanum (Apocynaceae) fit the pre-established cytological and histochemical patterns? Protoplasma, 242, 81‒93. DOI: 10.1007/s00709-010-0128-6

Oliveira, D. C., Mendonça, M. S., Moreira, A. S. F. P., Lemos-Filho, J. P., & Isaias, R. M. S. 2013. Water stress and phenological synchronism between Copaifera langsdorffii (Fabaceae) and multiple galling insects: formation of seasonal patterns. Journal of Plant Interactions, 8(3), 225‒233. DOI: 10.1080/17429145.2012.705339

Oliveira, P. E., & Gibbs, P. E. 2000. Reproductive biology of woody plants in a Cerrado community of the central Brazil. Flora, 195(4), 311‒329. DOI: 10.1016/S0367-2530(17)30990-8

Pedroni, F., Sanchez, M., & Santos, F. A. M. 2002. Fenologia da copaíba (Copaifera langsdorffii Desf. – Leguminosae - Caesalpinioideae) em uma floresta semidecídua no sudeste do Brasil, Campinas, SP. Revista Brasileira de Botânica, 25, 183–194.

Pianka E. R. 1973. The structure of lizard communities. Annual Review of Ecology and Systematics, 4, 53‒74.

Price, P. W., & Hunter, M. D. 2005. Long‐term population dynamics of a sawfly show strong bottom‐up effects. Journal of Animal Ecology, 74, 917‒925. DOI: 10.1111/j.1365-2656.2005.00989.x

Price, P. W., Waring, G. L., & Fernandes, G. W. 1986. Hypothesis on the adaptive nature of galls. Proceedings of the Entomological Society of Washington, 88, 361‒363.

R Core Team. 2014. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.

Rohfritsch, O., & Anthony, M. 1992. Strategies on gall induction by two groups of homopterans. In: J. D. Shorthouse, & O. Rohfritsch (Eds.), Biology of insect induced Galls. pp. 102‒117. New York: Oxford University Press.

Rohfritsch, O. 1992. Patterns in gall development. In: J. D. Shorthouse, & O. Rohfritsch (Eds.), Biology of insect induced galls. pp. 60‒86. New York: Oxford University Press.

Rosa, R. L. S. C., Lima, S. D. C., & Assunção, W. L. 1991. Abordagem preliminar das condições climáticas de Uberlândia (MG). Sociedade e Natureza, 3, 91‒108.

Roskam, J. C. 1992. Evaluation of gall-inducing guild. In: J. D. Shorthouse ,& O. Rohfritsch (Eds.), Biology of insect induced Galls. pp. 34‒50. Oxford: Oxford University Press.

Schiavini, I., & Araújo, G.M. 1989. Considerações sobre a vegetação da Reserva Ecológica do Panga (Uberlândia). Sociedade & Natureza, 1, 61‒66.

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 LF (Moraceae) induced by Gynaikothrips ficorum Marchal (Thysanoptera). Acta Botanica Brasilica, 14(1), 57‒69. DOI: 10.1590/S0102-33062000000100006

Stone, G. N., & Schrönrogge, K. 2003. The adaptive significance of insect gall morphology. Trends in Ecology & Evolution, 18(10), 512‒577. DOI: 10.1016/S0169-5347(03)00247-7

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(6), 1363‒1368. DOI: 10.1007/s00709-013-0519-6

Weis, A. E., Walton, R., & Crego, C. L. 1988. Reactive plant tissue sites and the population biology of gall makers. Annual Review of Entomology, 33, 467‒486. DOI: 10.1146/annurev.en.33.010188.002343

Wright, S. J., & Van Schaik, C. P. 1994. Light and the phenology of tropical trees. American Naturalist, 143(1), 192‒199. DOI: 10.1086/285600

Yukawa, J. 2000. Synchronization of gallers with host plant phenology. Population Ecology, 42, 105‒113. DOI: 10.1007/PL00011989

Zar, J. H. 2010. Biostatistical Analysis. 5th ed. Englewood Cliffs, NJ: Prentice Hall: p. 944.



  • There are currently no refbacks.

 SCImago Journal & Country Rank