Revista de Biología Tropical ISSN Impreso: 0034-7744 ISSN electrónico: 2215-2075

Structural, histochemical and photosynthetic profiles of galls induced by Eugeniamyia dispar (Diptera: Cecidomyiidae) on the leaves of Eugenia uniflora (Myrtaceae)


Chlorophyll a fluorescence
photosynthetic pigments
protein storage
reactive oxygen species
tissue gradients.
fluorescencia de la clorofila a
pigmentos fotosintéticos
almacenamiento de proteínas
especies reactivas de oxígeno
gradientes de tejidos.

How to Cite

Rezende, U. C., Franco Pinheiro Moreira, A. S., Kuster, V. C., & de Oliveira, D. C. (2018). Structural, histochemical and photosynthetic profiles of galls induced by Eugeniamyia dispar (Diptera: Cecidomyiidae) on the leaves of Eugenia uniflora (Myrtaceae). Revista De Biología Tropical, 66(4), 1469–1480.


Gall-inducing insects manipulate the structural, histochemical and physiological profiles of host-plant tissues to develop galls. We evaluated galls induced by Eugeniamyia dispar on the leaves of Eugenia uniflora in an attempt to answer the following questions: (i) How does this gall-inducing insect change the structural and histochemical profiles of the host-plant organ? (ii) Despite structural changes, can gall tissues maintain photosynthetic activity? Starch, proteins, reducing sugars and reactive oxygen species were detected mainly in the nutritive tissue surrounding the larval chamber. Despite structural changes, the galls induced by E. dispar on E. uniflora retain chlorophyllous tissue, although its amount and photosynthetic activity are less than that of non-galled leaves. This reduced photosynthetic activity, in association with the presence of large intercellular spaces, could improve gas diffusion and, consequently, avoid hypoxia and hypercarbia in gall tissue.


Bagatto, G., Paquette, L. C., & Shorthouse, J. D. (1996). Influence of galls of Phanacis taraxaci on carbon partitioning within common dandelion, Taraxacum officinale. Entomologia Experimentalis et Applicata, 79, 111-117. DOI: 10.1111/j.1570-7458.1996.tb00815.x

Baker, J. R. (1958). Note on the use of bromophenol blue for the histochemical recognition of protein. The Quarterly Journal of Microscopical Science, 99, 459-460.

Bolhar-Nordenkampf, H. R., Long, S. P., Baker, N. R., Oquist, G., Schreiber, U., & Lechner, E. G. (1989). Chlorophyll fluorescence as a probe of the photosynthetic competence of leaves in the field: a review of current instrumentation. Functional Ecology, 3, 497-514. DOI: 10.2307/2389624

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 arboreum Aubl. (Piperaceae). Journal of Plant Studies, 6, 11-19. DOI: 10.5539/jps.v6n1p11

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). New York, United States: Oxford University Press.

Brundett, M. C., Kendrick, B., & Peterson, C. A. (1991). Efficient lipid staining in plant material with Sudan Red 7B or fluorol yellow 088 in polyethylene glycol-glycerol. Biotechnic & Histochemistry, 66, 111-116. DOI: 10.3109/10520299109110562

Carneiro, R. G. S., Castro, A. C., & Isaias, R. M. S. (2014). Unique histochemical gradients in a photosynthesis-deficient plant gall. South African Journal of Botany, 92, 97-104. DOI: 10.1016/j.sajb.2014.02.011

Carneiro, R. G. S., & Isaias, R. M. S. (2015). 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. DOI: 10.1007/s00709-014-0709-x

Carneiro, R. G., Isaias, R., Moreira, A. S., & Oliveira, D. C. (2017). Reacquisition of New Meristematic Sites Determines the Development of a New Organ, the Cecidomyiidae Gall on Copaifera langsdorffii Desf. (Fabaceae). Frontiers in Plant Science, 8, 1622.

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). African Journal of Botany, 83, 121-126. DOI: 10.1016/j.sajb.2012.08.007

Del Río, L. A. & Puppo, A. (2009). Reactive oxygen species in plant signaling. Heidelberg, Germany: Springer-Verlag.

Demmig-Adams, B., & Adams, W. W. (1996). The role of xanthophyll cycle carotenoids in the protection of photosynthesis. Trends in Plant Science, 1, 21-26. DOI: 10.1016/S1360-1385(96)80019-7

Fernandes, G. W., Coelho, M. S., & Lüttge, U. (2010). Photosynthetic efficiency of Clusia arrudae leaf tissue with and without Cecidomyiidae galls. Brazilian Journal of Biology, 70, 723-728. DOI: 10.1590/S1519-69842010000400004

Fernandes, G. W., & Santos, J. C. (2014). Neotropical insect galls. Dordrecht, Holland: Springer.

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. DOI: 10.1139/cjb-2013-0125

Ferreira, B. F., Teixeira, C. T., & Isaias, R. M. S. (2014). Efficiency of the polyethylene-glycol (PEG) embedding medium for plant histochemistry. The Journal of Histochemistry and Cytochemistry, 62, 577-583. DOI: 10.1369/0022155414538265

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. DOI: 10.1016/j.flora.2014.06.004

Ferreira, B. G., Álvarez, R., Avritzer, S. C., & Isaias, R. M. S. (2017). Revisiting the histological patterns of storage tissues: beyond the limits of gall-inducing taxa. Botany, 95, 173-184. DOI: 10.1139/cjb-2016-0189

Florentine, S. K., Raman, A., & Dhileepan, K. (2005). Effects of gall induction by Epiblema strenuana on gas exchange, nutrients, and energetics in Parthenium hysterophorus. BioControl, 50, 787-801. DOI: 10.1007/s10526-004-5525-3

Formiga, A. T., Gonçalves, S. J. M. R., Soares, G. L. G., & Isaias, R. M. S. (2009). Relações entre o teor de fenóis totais e o ciclo das galhas de Cecidomyiidae em Aspidosperma spruceanum Müell. Arg. (Apocynaceae). Acta Botanica Brasilica, 23, 93-99. DOI: 10.1590/S0102-33062009000100012

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. DOI: 10.4236/ajps.2011.26097

Gagné, J. R. (1994). The gall midges of the Neotropical region. Ithaca, United States: Cornell University Press.

Genty, B., Briantais, J. M., & Baker, N. R. (1989). The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta, 990, 87-92. DOI: 10.1016/S0304-4165(89)80016-9

Haiden, S. A., Hoffmann, J. H., & Cramer, M. D. (2012). Benefits of photosynthesis for insects in galls. Oecologia, 170, 987-997. DOI: 10.1007/s00442-012-2365-1

Heldt, W., & Piechulla, B. (2010). Plant biochemistry. London, England: Academic Press.

Isaias, R. M. D. S., Coelho, D. D. O., & Carneiro, R. G. D. S. (2011). Role of Euphalerus ostreoides (Hemiptera: Psylloidea) in manipulating leaflet ontogenesis of Lonchocarpus muehlbergianus (Fabaceae). Botany, 89, 581-592. DOI: 10.1139/b11-048

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. DOI: 10.1007/s13744-013-0115-7

Isaias, R. M. S., Oliveira, D. C., Carneiro, R. G. S., & Kraus, J. E. (2014). Developmental anatomy of galls in the neotropics: arthropods stimuli versus host plant constraints. In G. W. Fernandes, & J. C. Santos (Eds.), Neotropical insect galls (pp. 15-34). Brazil: Springer.

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. DOI: 10.1016/j.bbagen.2015.03.007

Johansen, D. A. (1940). Plant microtechnique. New York, United States: McGraw-Hill.

Larson, K. C. (1998). The impact of two gall-forming arthropods on the photosynthetic rates of their hosts. Oecologia, 115, 161-166. DOI: 10.1007/s004420050503

Lev-Yadun, S. (2003). Stem cell in plants are differentiated too. Current Topics in Plant Biology, 4, 93-100. DOI: 10.1016/j.cell.2005.08.006

Lichtenthaler, H. K. & Wellburn, A. R. (1983). Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochemical Society Transactions, 11, 591-592. DOI: 10.1042/bst0110591

Lichtenthaler, H. K. & Miehé, J. A. (1997). Fluorescence imaging as a diagnostic tool for plant stress. Trends in Plant Science, 2, 316-319. DOI: 10.1016/S1360-1385(97)89954-2

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. DOI: 10.1007/s00709-013-0574-z

Maia, V. C., Mendonça, M. S., & Romanowski, H. P. (1996). Eugeniamyia díspar gen.n. and sp.n. (Diptera, Cecidomyiidade, Lasiopteridi) associated with Eugenia uniflora L. (Myrtaceae) in Brazil. Revista Brasileira de Zoologia, 13, 1087-1090. DOI: 10.1590/S0101-81751996000400026

Mani, M. S. (1964). Ecology of Plant Galls. Netherlands: Dr. W. Junk Publishers, The Hague.

Maxwell, K. & Johnson, G. N. (2000). Chlorophyll fluorescence-a practical guide. Journal of Experimental Botany, 51, 659-668.

Mendonça, M. S. & Romanowski, H. P. (2002). Natural enemies of the gall-maker Eugenia dispar (Diptera, Cecidomyiidae): predatory ants and parasitoids. Brazilian Journal of Biology, 62, 269-275. DOI: 10.1590/S1519-69842002000200011

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, 53, 153-160. DOI: 10.1071/BT07131

O’Brien, T. P., Feder, N., & Mccully, M. E. (1964). Polychromatic staining of plant cell walls by toluidine blue O. Protoplasma, 59, 368-373. DOI: 10.1007/BF01248568

Oliveira, D. C., & Isaias, R. M. S. (2010a). Redifferentiation of leaflet tissues during midrib gall development in Copaifera langsdorffii (Fabaceae). South African Journal of Botany, 76, 239-248. DOI: 10.1016/j.sajb.2009.10.011

Oliveira, D. C. & Isaias, R. M. S. (2010b). Cytological and histochemical gradients induced by a sucking insect in galls of Aspidosperma australe Arg. Muell (Apocynaceae). Plant Science (Limerick), 178, 350-358.

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.

Oliveira, D. C., Carneiro, R. G. S., Magalhaes, T. A., & Isaias, R. M. S. (2011a). Cytological and histochemical gradients on two Copaifera langsdorffii Desf. (Fabaceae) - Cecidomyiidae gall systems. Protoplasma, 248, 829-837. DOI: 10.1105/tpc.010454

Oliveira, D. C., Isaias, R. M. S., Moreira, A. S. F. P., Magalhães, T. A., & Lemos-Filho, J. P. (2011b). Is the oxidative stress caused by Aspidosperma spp. galls capable of altering leaf photosynthesis? Plant Sciences, 180, 489-495. DOI: 10.1016/j.plantsci.2010.11.005

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. DOI: 10.1016/j.jinsphys.2015.11.012

Oliveira, D. C., Moreira, A. S. F. P., Isaias, R. M. S., Martini, V., & Rezende, U. (2017). Sink status and photosynthetic rate of the leaflet galls induced by Bystracoccus mataybae (Eriococcidae) on Matayba guianensis (Sapindaceae). Frontiers in Plant Science, 8, 1-12. DOI: 10.3389/fpls.2017.01249

Oxborough, K. (2004). Imaging of chlorophyll a: theoretical and practical aspects of an emerging technique for the monitoring of photosynthetic performance. Journal of Experimental Botany, 55, 1195-1205. DOI: 10.1093/jxb/erh145

Petrov, V. D. & Van Breusegem, F. (2012). Hydrogen peroxide-a central hub for information flow in plant cells. AoB Plants, 2012, pls014. DOI: 10.1093/aobpla/pls014

Pincebourde, S., & Casas, J. (2016). Hypoxia and hypercarbia in endophagous insects: Larval position in the plant gas exchange network is key. Journal of Insect Physiology, 84, 137-153. DOI: 10.1016/j.jinsphys.2015.07.006

Price, P. W., Fernandes, G. W., & Warring, G. L. (1987). Adaptive nature of insect galls. In V. Labeyre, G. Fabres, & D. Lachaise (Eds.), Insects-plants (pp. 15-24). Dordrecht, Netherlands: Dr. W. Junk Publish.

Raman, A., Schaefer, C. W., & Withers, T. M. (2005). Biology, ecology, and evolution of gall-inducing arthropods. New Hampshire, United States: Science Publishers, Inc.

Raman, A., Cruz, Z. T., Muniappan, R., & Reddy, G. V. P. (2007). Biology and host specificity of gall-inducing Acythopeus (Coleoptera: Curculionidae: Baridinae), a biological control agent for the invasive weed Coccinia grandis (Cucurbitaceae) in Guam and Saipan. Tijdschrift voor Entomologie, 150, 181-191. DOI: 10.1163/22119434-900000217

Roskam, J. C. (1992). Evaluation of the gall-inducing guild. In J. D. Shorthouse & O. Rohfritsch (Eds.), Biology of insect-induced galls (pp. 34-39). New York, United States: Oxford.

Rossetti, S. & Bonnatti, P. M. (2001). In situ histochemical monitoring of ozone- and TMV induced reactive oxygen species in tobacco leaves. Plant Physiology and Biochemistry, 39, 433-442. DOI: 10.1016/S0981-9428(01)01250-5

Sass, J. E. (1951). Botanical microtechnique. Ames, United States: Iowa State College Press.

Schönrogge, K., Harper, L. J., & Lichtenstein, C. P. (2000). The protein contente of tissue in cynipid galls (Hymenoptera: Cynipidae): similarities between cynipid galls and seeds. Plant, Cell & Environment, 23, 215-222. DOI: 10.1046/j.1365-3040.2000.00543.x

Shorthouse, J. D. & Rohfritsch, O. (1992). Biology of insect-induced galls. New York, United States: Oxford University Press.

Shorthouse, J. D., Wool, D., & Raman, A. (2005). Gall-inducing insects - Nature´s most sophisticated herbivores. Basic and Applied Ecology, 6, 407-411. DOI: 10.1016/j.baae.2005.07.001

Stone, G. N., & Schönrogge, K. (2003). The adaptive significance of insect gall morphology. Trends in Ecology & Evolution, 18, 512-522. 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, 1363-1368. DOI: 10.1007/s00709-013-0519-6

Victoria, F. N., Lenardão, E. J., Savegnago, L., Perin, G., Jacob, R. G., Alves, D., & da Silva Nascente, P. (2012). Essential oil of the leaves of Eugenia uniflora L.: antioxidant and antimicrobial properties. Food and chemical toxicology, 50, 2668-2674. DOI: 10.1016/j.fct.2012.05.002



Download data is not yet available.