Biology and development of galls induced by Lopesia sp. (Diptera: Cecidomyiidae) on leaves of Mimosa gemmulata (Leguminosae: Caesalpinioideae)
Elaine Cotrim Costa A , Renê Gonçalves da Silva Carneiro B , Juliana Santos Silva C and Rosy Mary dos Santos Isaias A DA Departamento de Botânica, ICB, Universidade Federal de Minas Gerais, Avenida Antônio Carlos, 6627, Pampulha, 31270-901, Belo Horizonte, Minas Gerais, Brazil.
B Departamento de Botânica, ICB, Universidade Federal de Goiás, Campus Samambaia, Avenida Esperança, s.n., 74690-900, Goiânia, Goiás, Brazil.
C Departamento de Educação, Campus VIII, Universidade do Estado da Bahia, Rua do Gangorra, 503, CHESF, Alves de Souza, 48.608-24, Paulo Afonso, Bahia, Brazil.
D Corresponding author. Email: rosy@icb.ufmg.br
Australian Journal of Botany 66(2) 161-172 https://doi.org/10.1071/BT17099
Submitted: 31 May 2017 Accepted: 28 February 2018 Published: 11 April 2018
Abstract
Analyses of gall biology and development allow determination of morphogenesis events in host-plant organs that are altered by galling insects. Currently, we assume that there is a correlation between Lopesia sp. instars and the alterations in gall tissues on Mimosa gemmulata that generate the gall shape. The development of Lopesia sp. (three larval instars, pupae and adult) correlates positively with gall growth, especially on the anticlinal axis. First-instar larvae are found in galls at the stage of induction, Instar 2 in galls at early growth and development, Instar 3 in galls at late growth and development, pupae in galls at maturation, and the adult emerges from senescent galls. At induction, the larva stimulates cell differentiation in pinnula and pinna-rachis tissues on M. gemmulata. At early growth and development stages, cell division and expansion are increased, and non-glandular trichomes assist gall closing. Homogenous parenchyma and neoformed vascular bundles characterise late growth and development. At maturation, tissues are compartmentalised and cells achieve major expansion through elongation. At senescence, galls open by the falling of trichomes, and mechanical and nutritive cells have thickened walls. The neoformed nutritive tissue nurtures the developing Lopesia sp., whose feeding behaviour influences the direction of cell elongation, predominantly periclinal, determinant for gall bivalve shape.
Additional keywords: cell differentiation, leaf galls, plant cell growth, plant parasites.
References
Abrahamson WG, Weis AE (1997) ‘Evolutionary ecology across three trophic levels: goldenrods, gall-makers and natural enemies.’ (Princeton University Press: Princeton, NJ)Álvarez R, Encina A, Pérez Hidalgo NP (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.
| Histological aspects of three Pistacia terebinthus galls induced by three different aphids: Paracletus cimiciformis, Forda marginata and Forda formicaria.Crossref | GoogleScholarGoogle Scholar |
Amorim DO, Ferreira BG, Fleury G (2017) Plant potentialities determine anatomical and histochemical diversity in Mikania glomerata Spreng. galls. Revista Brasileira de Botanica. Brazilian Journal of Botany 40, 517–527.
| Plant potentialities determine anatomical and histochemical diversity in Mikania glomerata Spreng. galls.Crossref | GoogleScholarGoogle Scholar |
Arduin M, Kraus JE (1995) Anatomia e Ontogenia de galhas foliares de Piptadenia gonoacantha (Fabales, Mimosaceae). Boletim de Botânica da Universidade de São Paulo 14, 109–130.
| Anatomia e Ontogenia de galhas foliares de Piptadenia gonoacantha (Fabales, Mimosaceae).Crossref | GoogleScholarGoogle Scholar |
Baskin TI (2005) Anisotropic expansion of the plant cell wall. Annual Review of Cell and Developmental Biology 21, 203–222.
| Anisotropic expansion of the plant cell wall.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtlektbrO&md5=d8667cbb45e2fc77bec31e3784f26074CAS |
Bedetti CS, Modolo LV, Isaias RMS (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.
| The role of phenolics in the control of auxin in galls of Piptadenia gonoacantha (Mart.) MacBr (Fabaceae: Mimosoideae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtFOjs7vL&md5=f776da9c31ad1c666a643cd39af8282eCAS |
Bissing DR (1974) Haupt’s gelatin adhesive mixed with formalin for affixing paraffin sections to slides. Stain Technology 49, 116–117.
| Haupt’s gelatin adhesive mixed with formalin for affixing paraffin sections to slides.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE2c7it1Wlsg%3D%3D&md5=166f26ef53fd2a262c1aa06d928d303bCAS |
Bragança GP, Oliveira DC, Isaias RMS (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.
| Compartmentalization of metabolites and enzymatic mediation in nutritive cells of Cecidomyiidae galls on Piper arboreum Aubl. (Piperaceae).Crossref | GoogleScholarGoogle Scholar |
Carneiro RGS, Burckhardt D, Isaias RMS (2013) Biology and systematics of gall-inducing triozids (Hemiptera: Psylloidea) associated with Psidium spp. (Myrtaceae). Zootaxa 3620, 129–146.
| Biology and systematics of gall-inducing triozids (Hemiptera: Psylloidea) associated with Psidium spp. (Myrtaceae).Crossref | GoogleScholarGoogle Scholar |
Carneiro RGS, Oliveira DC, Isaias RMS (2014) 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.
| Developmental anatomy and immunocytochemistry reveal the neo-ontogenesis of the leaf tissues of Psidium myrtoides (Myrtaceae) towards the globoid galls of Nothotrioza myrtoidis (Triozidae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhsFKmsr%2FN&md5=94fbce1d101202714ddad4c064f73282CAS |
Carneiro RGS, Isaias RMS, Moreira ASFP, Oliveira DC (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
| Reacquisition of new meristematic sites determines the development of a new organ, the Cecidomyiidae gall on Copaifera langsdorffii Desf. (Fabaceae).Crossref | GoogleScholarGoogle Scholar |
Costa EC (2016) Galhas no Parque Estadual da Serra dos Montes Altos e Refúgio de Vida Silvestre: diversidade e desenvolvimento. Dissertação de Mestrado, Universidade do Estado da Bahia, Paulo Afonso, BA, Brazil.
Costa EC, Carvalho-Fernandes SP, Santos-Silva J (2014) Galhas de insetos em uma área de transição caatinga-cerrado no Nordeste do Brasil. Sitientibus. Série Ciências Biológicas 14, 1–9.
| Galhas de insetos em uma área de transição caatinga-cerrado no Nordeste do Brasil.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC283gs1yguw%3D%3D&md5=cda647ff6461b30b7ff08126318adbd1CAS |
Dias GG, Ferreira BG, Moreira GRP, Isaias RMS (2013a) Why do the galls induceb by Calophya duvauae Scott on Schinus polygamous (Cav.) Cabrera (Anacardiaceae) change colors? Biochemical Systematics and Ecology 48, 111–122.
| Why do the galls induceb by Calophya duvauae Scott on Schinus polygamous (Cav.) Cabrera (Anacardiaceae) change colors?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXktlOnsbg%3D&md5=90be043b6f177a9c1fa9a8739d51944cCAS |
Dias GG, Ferreira BG, Moreira GRP, Isaias RMS (2013b) 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.
| Developmental pathway from leaves to galls induced by a sap-feeding insect on Schinus polygamus (Cav.) Cabrera (Anacardiaceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXmvFOmtL4%3D&md5=9e81a79623330d8fb4140d040c3ad5d2CAS |
Ferreira BG, Isaias RMS (2013) Developmental stem anatomy and tissue redifferentiation induced by a galling Lepidoptera on Marcetia taxifolia (Melastomataceae). Botany 91, 752–760.
| Developmental stem anatomy and tissue redifferentiation induced by a galling Lepidoptera on Marcetia taxifolia (Melastomataceae).Crossref | GoogleScholarGoogle Scholar |
Ferreira BG, Isaias RMS (2014) Floral-like destiny induced by a galling Cecidomyiidae on the axillary buds of Marcetia taxifolia (Melastomataceae). Flora 209, 391–400.
| Floral-like destiny induced by a galling Cecidomyiidae on the axillary buds of Marcetia taxifolia (Melastomataceae).Crossref | GoogleScholarGoogle Scholar |
Fleury G, Ferreira BG, Soares GLG, Oliveira DC (2015) Elucidating the determination of the rosette galls induced by Pisphondylia brasiliensis Couri and Maia 1992 (Cecidomyiidae) on Guapira opposita (Nyctaginaceae). Australian Journal of Botany 63, 608–617.
| Elucidating the determination of the rosette galls induced by Pisphondylia brasiliensis Couri and Maia 1992 (Cecidomyiidae) on Guapira opposita (Nyctaginaceae).Crossref | GoogleScholarGoogle Scholar |
Formiga AT, Gonçalves SJMR, Soares GLG, Isaias RMS (2009) Relações entre o teor de fenóis totais e o ciclo das galhas de Cecidomyiidae em Aspidosperma spruceanum Müll. Arg. (Apocynaceae). Acta Botanica Brasílica 23, 93–99.
| Relações entre o teor de fenóis totais e o ciclo das galhas de Cecidomyiidae em Aspidosperma spruceanum Müll. Arg. (Apocynaceae).Crossref | GoogleScholarGoogle Scholar |
Franceschi VR, Nakata VR (2005) Calcium oxalate in plants: formation and function. Annual Review of Plant Biology 56, 41–71.
| Calcium oxalate in plants: formation and function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmtVaru74%3D&md5=704c808f135c4b9f7d4a0c2f5727e7c2CAS |
Gagné RJ (1994) ‘The gall midges of the Neotropical region.’ (Cornell University: Ithaca, NY)
Gagné RJ, Jaschhof M (2017) ‘A catalog of the Cecidomyiidae (Diptera) of the World.’ 4th edn. (National Museum NHB: Washington, DC)
Gonçalves SJMR, Isaias RMS, Vale FHA, Fernandes GW (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.
| Sexual dimorphism of Pseudotectococcus rolliniae Hodgson & Gonçalves 2004 (Hemiptera Coccoidea Eriococcidae) influences gall morphology on Rollinia laurifolia Schltdl. (Annonaceae).Crossref | GoogleScholarGoogle Scholar |
Gonçalves SJMR, Moreira GRP, Isaias RMS (2009) A unique seasonal cycle in a leaf gallinducing insect: the formation of stem galls for dormancy. Journal of Natural History 43, 843–854.
| A unique seasonal cycle in a leaf gallinducing insect: the formation of stem galls for dormancy.Crossref | GoogleScholarGoogle Scholar |
Haupt AW (1930) A gelatin fixative for paraffin sections. Stain Technology 5, 97–98.
| A gelatin fixative for paraffin sections.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaA3cXjvFKitw%3D%3D&md5=da9efb94640d6034d61fd31c83b53ce0CAS |
Hawkins BA, Gagné RJ (1989) Determinants of assemblage size for the parasitoids of Cecidomyiidae (Diptera). Oecologia 81, 75–88.
| Determinants of assemblage size for the parasitoids of Cecidomyiidae (Diptera).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC1czotVKluw%3D%3D&md5=fc2f5af38f234b657ccacbf760b2b8c7CAS |
Isaias RMS, Oliveira DC, Carneiro RGS (2011) Role of Euphalerus ostreoides (Hemiptera: Psylloidea) in manipulating leaflet ontogenesis of Lonchocarpus muehlbergianus (Fabaceae). Botany 89, 581–592.
| Role of Euphalerus ostreoides (Hemiptera: Psylloidea) in manipulating leaflet ontogenesis of Lonchocarpus muehlbergianus (Fabaceae).Crossref | GoogleScholarGoogle Scholar |
Isaias RMS, Carneiro RGS, Oliveira DC, Santos JC (2013) Illustrated and annotated checklist of Brazilian gall morphotypes. Neotropical Entomology 42, 230–239.
| Illustrated and annotated checklist of Brazilian gall morphotypes.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3sbgtVeguw%3D%3D&md5=6240d5563f5717aeb4880e3aeec7fccbCAS |
Isaias RMS, Carneiro RGS, Santos JC, Oliveira DC (2014) Gall morphotypes in the Neotropics and the need to standardize them. In ‘Neotropical insect galls’. (Eds JC Santos, GW Fernandes) pp. 51–67. (Springer: Dordrecht, The Netherlands).
Isaias RMS, Oliveira DC, Moreira ASFP, Soares GLG, Carneiro RGS (2015) The imbalance of redox homeostasis in arthropod-induced plant galls: mechanisms of stress generation and dissipation. Biochimica et Biophysica Acta 1850, 1509–1517.
| The imbalance of redox homeostasis in arthropod-induced plant galls: mechanisms of stress generation and dissipation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXlsVOjs74%3D&md5=8be720fac92c426ece9aec159cd9da6bCAS |
Johansen DA (1940) ‘Plant microtechnique.’ (McGraw-Hill Book: New York)
Karnovsky MJ (1965) A formaldehyde-glutaraldehyde fixative of hight osmolarity for use in electron microscopy. The Journal of Cell Biology 27, 137–138.
Kraus JE, Arduin M (1997) ‘Manual básico de métodos em morfologia vegetal.’ (Editora Seropédica da Universidade Federal Rural do Rio de Janeiro: Rio de Janeiro, Brazil)
Kraus LE, Sugiura HC, Cutrupi S (1996) Morfologia e ontogenia em galhas entomógenas de Guarea macrophylla subsp. tuberculata (Meliaceae). Fitopatologia Brasileira 21, 349–356.
Lev-Yadun S (2003) Stem cells in plants are differentiated too. Current Opinion in Plant Biology 4, 93–100.
| Stem cells in plants are differentiated too.Crossref | GoogleScholarGoogle Scholar |
Magalhães TA, Oliveira DC, Isaias RMS (2014a) Population dynamics of the gall inducer Eriogallococcus isaias (Hemiptera: Coccoidea: Eriococcidae) on Pseudobombax grandiflorum (Malvaceae). Journal of Natural History 49, 789–801.
| Population dynamics of the gall inducer Eriogallococcus isaias (Hemiptera: Coccoidea: Eriococcidae) on Pseudobombax grandiflorum (Malvaceae).Crossref | GoogleScholarGoogle Scholar |
Magalhães TA, Oliveira DC, Suzuki AYM, Isaias RMS (2014b) 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.
| Patterns of cell elongation in the determination of the final shape in galls of Baccharopelma dracunculifoliae (Psyllidae) on Baccharis dracunculifolia DC (Asteraceae).Crossref | GoogleScholarGoogle Scholar |
Motulsky H. (1992–2009) ‘Analyzing data with GraphPad Prism software.’ (GraphPad Software Inc.: San Diego, CA)
Moura MZD, Soares GLG, Isaias RMS (2009) Ontogênese da folha e das galhas induzidas por Aceria lantanae Cook (Acarina: Eriophyidae) em Lantana camara L. (Verbenaceae). Revista Brasileira de Botanica. Brazilian Journal of Botany 32, 271–282.
| Ontogênese da folha e das galhas induzidas por Aceria lantanae Cook (Acarina: Eriophyidae) em Lantana camara L. (Verbenaceae).Crossref | GoogleScholarGoogle Scholar |
Oliveira DC, Isaias RMS (2009) Influence of leaflet age in anatomy and possible adaptive values of the midrib gall of Copaifera langsdorffii (Fabaceae: Caesalpinioideae). Revista de Biología Tropical 57, 293–302.
Oliveira DC, Isaias RMS (2010) Redifferentiation of leaflet tissues during midrib gall development in Copaifera langsdorffii (Fabaceae). South African Journal of Botany 76, 239–248.
| Redifferentiation of leaflet tissues during midrib gall development in Copaifera langsdorffii (Fabaceae).Crossref | GoogleScholarGoogle Scholar |
Paiva JGA, Fank-De-Carvalho SM, Magalhães MP, Graciano-Ribeiro D (2006) Verniz vitral incolor 500®: uma alternativa de meio de montagem economicamente viável. Acta Botanica Brasílica 20, 257–264.
| Verniz vitral incolor 500®: uma alternativa de meio de montagem economicamente viável.Crossref | GoogleScholarGoogle Scholar |
Rohfritsch O (1992) Patterns in gall development. In ‘Biology of insect-induced galls’. (Eds JD Shorthouse, O Rohfritsch) pp. 60–86. (Oxford University Press: New York)
Santos-Silva J, Simon MF, Tozzi AMGA (2015) Revisão taxonômica das espécies de Mimosa ser. Leiocarpae sensu lato (Leguminosae – Mimosoideae). Rodriguésia 66, 95–154.
| Revisão taxonômica das espécies de Mimosa ser. Leiocarpae sensu lato (Leguminosae – Mimosoideae).Crossref | GoogleScholarGoogle Scholar |
Simon MF, Grether R, Queiroz LP, Särkinen TE, Dutra VF, Hughes CE (2011) The evolutionary history of Mimosa (Leguminosae): toward a phylogeny of the sensitive plants. American Journal of Botany 98, 1201–1221.
| The evolutionary history of Mimosa (Leguminosae): toward a phylogeny of the sensitive plants.Crossref | GoogleScholarGoogle Scholar |
Stone GN, Schönrogge K (2003) The adaptive significance of insect gall morphology. Trends in Ecology & Evolution 18, 512–522.
| The adaptive significance of insect gall morphology.Crossref | GoogleScholarGoogle Scholar |
Suzuki AY, Bedetti CS, Isaias RMS (2015) Detection and distribution of cell growth regulators and of cellulose microfibrils during the development of Lopesia sp. galls on Lonchocarpus cultratus (Fabaceae). Botany 93, 435–444.
| Detection and distribution of cell growth regulators and of cellulose microfibrils during the development of Lopesia sp. galls on Lonchocarpus cultratus (Fabaceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXptFSms7k%3D&md5=8508556d7b63e1f6d2af745904acaa34CAS |
Ullrich CI, Aloni R (2000) Vascularization is a general requirement for growth of plant and animal tumours. Journal of Experimental Botany 51, 1951–1960.
| Vascularization is a general requirement for growth of plant and animal tumours.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXns1eksg%3D%3D&md5=e25438bf49bf374d27b869149b4ff2f0CAS |
Wiebes-Rijks AA, Shorthouse JD (1992) Ecological relationships of insects inhabiting cynipid galls. In ‘Biology of insect-induced galls’. (Eds JD Shorthouse, O Rohfritsch) pp. 238–257. (Oxford University Press: Oxford, NY, USA)