Abstract
Galls are products of anatomical, metabolic, and chemical alterations in host plant tissues, caused by parasitic organisms named gall inducers. Gall inducers can potentiate chemical and structural specializations of their host plants for their own benefit, such as the accumulation of bioactive and antioxidant secondary metabolites, which should be tested. This could lead to increased protection against natural enemies, pathogens, and different abiotic stressors. Based on data in the literature, we listed the gall morphotypes found in restingas (threatened coastal vegetations) in Rio de Janeiro State, Brazil, and reunited the anatomical, phytochemical, and medicinal information of the host plants. Superhost plants, capable of hosting more than one gall-inducing species, represented 51% of the hosts, with 80% of the listed galls. Phytochemical and pharmacological potentials were confirmed for 80% of the gall superhosts. Most of the non-medicinal superhosts belong to species or families of toxic plants. These facts indicate the high percentage of superhost species capable of producing and accumulating secondary metabolites. Anatomical, phytochemical, and pharmacological potentials of the 17 most widely distributed superhosts are discussed in detail. These plants have metabolites with antimicrobial and antioxidant activity, among several other pharmacological properties. Data gathered here revealed that superhost plants of galling organisms have wide distribution in restingas, accumulate diverse secondary metabolites, and several of them are reported to have bioactive or pharmacological properties. Families of superhost plants not necessarily are those richer and more diverse in restingas, indicating that specific chemical and structural features of host plants are preponderant in galling arthropod–plant interactions. Based on our results, we indicated some superhosts as study models to test the potentiation of such features in galls, which were selected based on the number of associated galls, the types of secondary metabolites detected, and the presence of bioactive substances.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data Availability
Data available within the article or its supplementary materials.
References
Adam F, Vahirua-Lechat I, Deslandes E, Menut C (2011) Aromatic plants of French Polynesia. V. Chemical composition of essential oils of leaves of Psidium guajava L. and Psidium cattleyanum Sabine. J Essent Oil Res 23:98–101. https://doi.org/10.1080/10412905.2011.9700433
Allison SD, Schultz JC (2005) Biochemical responses of chestnut oak to a galling cynipid. J Chem Ecol 31:151–166. https://doi.org/10.1007/s10886-005-0981-5
Almada ED, Fernandes GW (2011) Insetos indutores de galhas em florestas de terra firme e em reflorestamentos com espécies nativas na Amazônia Oriental, Pará, Brasil. Bol Mus Para Emílio Goeldi Cienc Nat 6:163–196. https://doi.org/10.46357/bcnaturais.v6i2.620
Almeida MZ (2011) Plantas Medicinais, 3rd edn. EDUFBA, Salvador
Almeida-Lafetá RC, Ferreira MJP, Emerenciano VP, Kaplan MAC (2010) Withanolides from Aureliana fasciculata var. fasciculata. Helv Chim Acta 93:2478–2487. https://doi.org/10.1002/hlca.201000126
Alves ES, Tresmondi F, Longui EL (2008) Análise estrutural de folhas de Eugenia uniflora L. (Myrtaceae) coletadas em ambiente rural e urbano, SP, Brasil. Acta Bot Bras 22:241–248. https://doi.org/10.1590/S0102-33062008000100023
Amaral RR, Fernandes CP, Caramel OP, Tietbohl LAC, Santos MG, Carvalho JCT, Rocha L (2013) Essential oils from fruits with different colors and leaves of Neomitranthes obscura (DC.) N. Silveira: an endemic species from Brazilian Atlantic Forest. BioMed Res Int 2013:723181. https://doi.org/10.1155/2013/723181
Arai I, Amagaya S, Komatsu Y, Okada M, Hayashi T, Kasai M, Arisawa M, Momose Y (1999) Improving effects of the extracts from Eugenia uniflora on hyperglycemia and hypertriglyceridemia in mice. J Ethnopharmacol 68:307–314. https://doi.org/10.1016/S0378-8741(99)00066-5
Aranda-Rickert A, Rothen C, Diez P, González AM, Marazzi B (2017) Sugary secretions of wasp galls: a want-to-be extrafloral nectar? Ann Bot 120:765–774. https://doi.org/10.1093/aob/mcx075
Araújo DIAF (2021) Avaliação do perfil químico, variações sazonais e estudo de controle de qualidade de espécies do gênero Monteverdia: Monteverdia obtusifolia (Mart) Biral e Monteverdia rigida (Mart) Biral. PhD Thesis, Universidade Federal da Paraíba
Araújo DSD, Henriques RPB (1984) Análise florística das Restingas do estado do Rio de Janeiro. In: Lacerda LD (Org) Restingas: origem, estrutura, processos. CEUFF, Niterói, pp 150–193
Araújo WS, Maia VC (2021) Topological structure of a tritrophic network composed of host plants, gall-inducing insects and parasitoids in a restinga area in Brazil. Entomol Sci 24:201–216. https://doi.org/10.1111/ens.12468
Araujo FF, Amorin M, Santos VLP, Franco CRC, Folquitto DG, Silva RZ, Farago PV, Takeda IJM, Nakashima T, Budel JM (2015) Pharmacobotanical characters of Mikania micrantha (Asteraceae) and its support for quality control. Lat Am J Pharm 34:437–442
Araújo DIAF, Fernandes APLA, Pinheiro AAV, Souto AL, Sales KA, Araújo PRAF, Andrade RS, Silva MS (2020) Determination of flavan-3-ols by high-performance liquid chromatography-photodiode array, antioxidant potential, antimicrobial activity, and pharmacognostic evaluation of Maytenus obtusifolia (Mart.) leaves. Pharmacogn Res 12:313–321
Arruda RC, Victório CP (2011) Leaf secretory structure and volatile compounds of Eugenia copacabanensis Kiaersk. (Myrtaceae). J Essent Oil Res 23:1–6. https://doi.org/10.1080/10412905.2011.9700472
Auricchio MT, Bacchi EM (2003) Folhas de Eugenia uniflora L. (pitanga): propriedades farmacobotânicas, químicas e farmacológicas. Rev Inst Adolfo Lutz 62:55–61. https://doi.org/10.18241/rial.v62i1.34958
Azevedo CF, Quirino ZGM, Bruno RLA (2015) Estudo farmacobotânico de partes aéreas vegetativas de aroeira-vermelha (Schinus terebinthifolius Raddi, Anacardiaceae). Rev Bras Plant Med 17:26–35. https://doi.org/10.1590/1983-084X/11_090
Ballabeni V, Tognolini M, Bertoni S, Bruni R, Guerrini A, Rueda GM, Barocelli E (2007) Antiplatelet and antithrombotic activities of essential oil from wild Ocotea quixos (Lam.) Kosterm. (Lauraceae) calices from Amazonian Ecuador. Farmacol Res 55:23–30. https://doi.org/10.1016/j.phrs.2006.09.009
Barbosa-Filho JM, Cunha RM, Dias CS, Athayde-Filho PF, Silva MS, Da-Cunha EVL, Machado MIL, Craveiro AA, Medeiros IA (2008) GC-MS analysis and cardiovascular activity of the essential oil of Ocotea duckei. Braz J Pharmacogn 18:37–41. https://doi.org/10.1590/S0102-695X2008000100009
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). Biochem Syst Ecol 55:53–59. https://doi.org/10.1016/j.bse.2014.02.016
Betim FCM, Barbosa V, Oliveira CF, Miguel OG, Raman V, Budel JM, Miguel MD, Dias JFG (2020) Microscopy and histochemistry of Ocotea nutans (Nees) Mez (Lauraceae). Flora 273:151708. https://doi.org/10.1016/j.flora.2020.151708
Bhat BA, Dhar KL, Puri SC, Qurishi MA, Khajuria A, Gupta A, Qazi GN (2005) Isolation, characterization and biological evaluation of datura lactones as potential immunomodulators. Bioorg Med Chem 13:6672–6677. https://doi.org/10.1016/j.bmc.2005.07.040
Bomfim PMS, Cardoso JCF, Rezende UC, Martini VC, Oliveira DC (2019) Red galls: the different stories of two gall types on the same host. Plant Biol 21:284–291. https://doi.org/10.1111/plb.12915
Bratti C, Vieira MC, Zárate NAH, Oliveira APA, Marafiga BG, Fernandes SSL (2013) Levantamento de Plantas Medicinais Nativas da Fazenda Azulão em Dourados-MS. Rev Bras Plant Med 15:675–683. https://doi.org/10.1590/S1516-05722013000500008
Bravo JAB, Sauvain M, Gimenez AT, Balanza E, Serani L, Laprévote O, Massiot G, Lavaud C (2001) Trypanocidal withanolides and withanolide glycosides from Dunalia brachyacantha. J Nat Prod 64:720–725. https://doi.org/10.1021/np000527p
Bristot SF, Colle MPD, Rossato AE, Citadini-Zanette V (2021) Uso medicinal de Varronia curassavica Jacq. “erva-baleeira” (Boraginaceae): estudo de caso no sul do Brasil. Braz J Anim Environ Res 4(1):170–182. https://doi.org/10.34188/bjaerv4n1-016
Bronner R (1992) The role of nutritive cells in the nutrition of Cynipids and Cecidomyiids. In: Shorthouse JD, Rohfritsch O (eds) Biology of insect-induced galls. Oxford University Press, Oxford, pp 118–137
Brustulim LJR, Monteiro LM, Almeida VP, Raman V, Maia BHLNS, Casapula I, Paludo KS, Bussade JE, Rehman JU, Kahn IA, Farago PV, Budel JM (2020) Ocotea porosa: anatomy and histochemistry of leaves and stems, chemical composition, cytotoxicity and insecticidal activities of essential oil. Braz Arch Biol Technol 63:e20190082. https://doi.org/10.1590/1678-4324-2020190082
Busato NV, Silveira JC, Alves ED, Tuler AC, Costa AV, Carrijo TT, Rinaldo D, Pinheiro PF (2009) Estudo fitoquímico de folhas e caule de Lepidaploa rufogrisea (St. Hill.) H. Rob. (Assa-peixe-roxo). XVI Encontro Latino-Americano de Iniciação Científica e XII Encontro Latino Americano de Pós-Graduação, Universidade do Vale do Paraíba. http://www.inicepg.univap.br/cd/INIC_2012/anais/arquivos/0148_0027_01.pdf. Accessed 11 Aug 2022
Cáceres A, Cruz SM, Martínez V, Gaitán I, Santizo A, Gattuso S, Gattuso M (2012) Ethnobotanical, pharmacognostical, pharmacological and phytochemical studies on Smilax domingensis in Guatemala. Braz J Pharmacogn 22:239–248. https://doi.org/10.1590/S0102-695X2011005000211
Cândido CS, Portella CSA, Laranjeira BJ, Silva SS, Arriaga AMC, Santiago GMP, Gomes GA, Almeida PC, Carvalho CBM (2010) Effects of Myrcia ovata Cambess. essential oil on planktonic growth of gastrointestinal microorganisms and biofilm formation of Enterococcus faecalis. Braz J Microbiol 41:621–627. https://doi.org/10.1590/S1517-83822010000300012
Cardoso-Lopes EM, De Paula DMB, Barbo FE, Souza A, Blatt CTT, Torres LMB, Young MCM (2009) Chemical composition, acetylcholinesterase inhibitory and antifungal activities of Pera glabrata (Schott) Baill. (Euphorbiaceae). Braz J Bot 32:819–825. https://doi.org/10.1590/S0100-84042009000400019
Carminate B, Carmitante C, Fontana AA, Farias MHA, Silva MB (2016) Estudo fotoquímico e antimicrobiano das folhas de Eugenia astringens Cambess (Myrtaceae). Rev Univap 22:479. https://doi.org/10.18066/revistaunivap.v22i40.1067
Carmona D, Lajeunesse MJ, Johnson MT (2011) Plant traits that predict resistance to herbivores. Funct Ecol 25:358–367. https://doi.org/10.1111/j.1365-2435.2010.01794.x
Carvalho-Fernandes SP, Ascendino S, Maia VC, Couri MS (2016) Diversity of insect galls associated with coastal shrub vegetation in Rio de Janeiro, Brazil. An Acad Bras Ciênc 88:1407–1418. https://doi.org/10.1590/0001-3765201620150658
Carvalho-Júnior ARC, Gomes GA, Ferreira RO, Carvalho MG (2014) Constituintes químicos e atividade antioxidante de folhas e galhos de Eugenia copacabanenses Kiaersk (Myrtaceae). Quim Nova 37:477–482. https://doi.org/10.5935/0100-4042.20140079
Cascaes MM, Guilhon GM, Andrade EHA, Zoghbi MGB, Santos LS (2015) Constituents and pharmacological activities of Myrcia (Myrtaceae): a review of an aromatic and medicinal group of plants. Int J Mol Sci 16:23881–23904. https://doi.org/10.3390/ijms161023881
Cassara F (2019) Investigação do potencial amebicida do extrato bruto e compostos isolados de Eugenia hiemalis frente a Acanthamoeba spp. MSc Dissertation, Universidade Federal de Santa Catarina
Castellucci S, Lima MIS, Nordi N, Marques JGW (2000) Plantas medicinais relatadas pela comunidade residente na estação ecológica de Jataí, município de Luís Antônio/SP: uma abordagem etnobotânica. Rev Bras Plant Med 3:51–60
Castro RRM, Barbosa PEF, Sant’Anna LG, Pereira CMS, Ferreira BG (2023) Sun and shade galls of Clinodiplosis profusa (Cecidomyiidae) on Eugenia uniflora (Myrtaceae): are there differences in their establishment and growth? Flora. https://doi.org/10.1016/j.flora.2023.152281
Chandrasekaran S, Dayakar A, Veronica J, Sundar S, Maurya R (2013) An in vitro study of apoptotic like death in Leishmania donovani promastigotes by withanolides. Parasitol Int 62:253–261. https://doi.org/10.1016/j.parint.2013.01.007
Claudino GP, Simões JB, Vieira IJC, Braz- Filho R, Mathias L (2009) Chemical constituents and lethality of Paullinia weinmanniaefolia (Sapindaceae) against Artemia salina Leach. J Braz Pharmacogn 19(1A):26–28. https://doi.org/10.1590/S0102-695X2009000100006
Consolini AE, Sarubbio MG (2002) Pharmacological effects of Eugenia uniflora (Myrtaceae) aqueous crude extract on rat’s heart. J Ethnopharmacol 81:57–63. https://doi.org/10.1016/S0378-8741(02)00039-9
Costa JGM, Sousa EO, Rodrigues FFG, Lima SG, Braz-Filho R (2008) Composição química e avaliação das atividades antibacteriana e de toxicidade dos óleos essenciais de Lantana camara L. e Lantana sp. Braz J Pharmacogn 19(3):710–714. https://doi.org/10.1590/S0102-695X2009000500010
Costa IFB, Calixto SD, Araujo MH, Konno TUP, Tinoco LW, Tinoco LW, Guimarães DO, Lasunskaia EB, Leal IC, Muzitano MF (2015) Antimycobacterial and nitric oxide production inhibitory activities of Ocotea notata from Brazilian Restinga. Sci World J. https://doi.org/10.1155/2015/947248
Costa EC, Bragança GPP, Arriola IA, Freitas MSC, Isaias RMS (2022) Host plant traits define the strategies of success to the Cecidomyiidae in a restinga environment. S Afr J Bot 146:751–759. https://doi.org/10.1016/j.sajb.2021.12.015
Cruz RAS, Botas GS, Fernandes CP, Santos MG, Rocha L (2018) Chemical constituents of essential oils from leaves of two Erythroxylum species. Chem Nat Compd 54:185–187. https://doi.org/10.1007/s10600-018-2292-4
Cuca LE, Leon P, Coy ED (2009) Abicyclo (3.2.1) octanoide neolignan and toxicity of the ethanol extract from the fruit of Ocotea heterochroma. Chem Nat Compd 5:179–181. https://doi.org/10.1007/s10600-009-9304-3
Cunha GOS, Cruz DC, Menezes ACS (2019) Na Overview of Miconia genus: chemical constituents and biological activities. Pharmacogn Rev 13:77–88. https://doi.org/10.5530/phrev.2019.2.8
Czelusniak KE, Brocco A, Pereira DF, Freitas GBL (2012) Farmacobotânica, fitoquímica e farmacologia do Guaco: revisão considerando Mikania glomerata Sprengel e Mikania laevigata Schulyz Bip. ex Baker. Rev Bras Plant Med 14:400–409. https://doi.org/10.1590/S1516-05722012000200022
David JM, Souza JC, Guedes MLS, David JP (2006) Estudo fitoquímico de Davilla rugosa: flavonóides e terpenóides. Rev Bras Farmacogn 16:105–108. https://doi.org/10.1590/S0102-695X2006000100019
De Santana Julião JL, Piccinelli AL, Marzocco S, Leitão SG, Lotti C, Autore G, Rastrelli L (2009) Phenylethanoid glycosides from Lantana fucata within vitro anti-inflammatory activity. J Nat Prod 72:1424–1428. https://doi.org/10.1021/np9002383
Després L, David JP, Gallet C (2007) The evolutionary ecology of insect resistance to plant chemicals. Trends Ecol Evol 22:298–307. https://doi.org/10.1016/j.tree.2007.02.010
Dias CS, Silva IG, Cunha EVL, Silva MS, Braz-FIlho R, Barbosa-Filho JM (2003) Isolamento e identificação de novos alcalóides de Ocotea duckei Vattimo (Lauraceae). Rev Bras Farmacogn 13:62–63. https://doi.org/10.1590/S0102-695X2003000300023
Dias GG, Moreira GRP, Ferreira BG, Isaias RMS (2013a) Why do the galls induced by Calophya duvauae Scott on Schinus polygamus (Cav.) Cabrera (Anacardiaceae) change colors? Biochem Syst Ecol 48:111–122. https://doi.org/10.1016/j.bse.2012.12.013
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). An Acad Bras Ciênc 85:187–200. https://doi.org/10.1590/S0001-37652013000100010
Duarte MR, Toledo MG, Oliveira RB (2006) Diagnose morfoanatômica de aroeira (Schinus terebinthifolius Raddi, Anacardiaceae). Visão Acadêmica 7(2):1–14. https://doi.org/10.5380/acd.v7i2.9023
Enriz RD, Baldoni HA, Zamora MA, Jáuregui EA, Sosa ME, Tonn CE, Luco JM, Gordaliza M (2000) Structure antifeedant activity relationship of clerodane diterpenoids. Comparative study with withanolides and azadirachtin. J Agric Food Chem 48:1384–1392. https://doi.org/10.1021/jf990006b
Espírito-Santo MM, Fernandes GW (2007) How many species of gall-inducing insects are there on earth, and where are they? Ann Entomol Soc Am 100:95–99. https://doi.org/10.1603/0013-8746(2007)100[95:HMSOGI]2.0.CO;2
Evert RF (2013) Anatomia das plantas de Esau: meristemas, células e tecidos do corpo da planta: sua estrutura, função e desenvolvimento, 3ª edn. Blucher, São Paulo
Fadin DA, Monquero PA (2019) Leaf characterization of Spermacoce verticillata at three stages of development. Aust J Crop Sci 13:792–797. https://doi.org/10.21475/ajcs.19.13.05.p1663
Faria RX, Rocha LM, Souza EPBSS, Almeida FB, Fernandes CP, Santos JAA (2018) Molluscicidal activity of Manilkara subsericea (Mart.) dubard on Biomphalaria glabrata (Say, 1818). Acta Trop 178:163–168. https://doi.org/10.1016/j.actatropica.2017.11.012
Fenner R, Betti AH, Mentz LA, Rates SMK (2006) Plantas utilizadas na medicina popular brasileira com potencial atividade antifúngica. Rev Bras Ciên Farma 42:369–394. https://doi.org/10.1590/S1516-93322006000300007
Fernandes GW, Price PW (1992) The adaptive significance of insect gall distribution: survivorship of species in xeric and mesic habitats. Oecologia 90:14–20. https://doi.org/10.1007/BF00317803
Fernandes CP, Corrêa AL, Lobo JFR, Caramel OP, Almeida FB, Castro ES, Souza KFCS, Burth P, Amorim LMF, Santos GM, Ferreira JLP, Falcão DQ, Carvalho JCT, Rocha L (2013) Triterpene esters and biological activities from edible fruits of Manilkara subsericea (Mart.) Dubard, Sapotaceae. Biomed Res Int. https://doi.org/10.1155/2013/280810
Ferreira BS, Oliveira DC, Moreira ASFP, Faria AP, Guedes LM, França MGC, Álvarez R, Isaias RMS (2018) Antioxidant metabolism in galls due to the extended phenotypes of the associated organisms. PLoS ONE 13:e0205364. https://doi.org/10.1371/journal.pone.0205364
Ferreira BG, Álvarez R, Bragança GP, Alvarenga DR, Pérez-Hidalgo N, Isaias RMS (2019) Feeding and other gall facets: patterns and determinants in gall structure. Bot Rev 85:78–106. https://doi.org/10.1007/s12229-019-09207-w
Ferreira BG, Moreira GRP, Carneiro RGS, Isaias RMS (2022) Complex meristematic activity induced by Eucecidoses minutanus on Schinus engleri turns shoots into galls. Am J Bot 109:209–225. https://doi.org/10.1002/ajb2.1798
Fidelis QC, Ribeiro TAN, Araújo MF, de Carvalho MG (2014) Ouratea genus: chemical and pharmacological aspects. Rev Bras Farmacogn 24:1–19. https://doi.org/10.1590/0102-695X20142413361
Fitriansyah SN, Fidrianny I, Hartati R (2021) Pharmacological activities and phytochemical compounds: overview of Pouteria genus. Pharmacogn J 13:577–584. https://doi.org/10.5530/pj.2021.13.72
Fleury G, Ferreira BG, Soares GLG, Oliveira DC, Isaias RMS (2015) Elucidating the determination of the rosette galls induced by Pisphondylia brasiliensis Couri and Maia 1992 (Cecidomyiidae) on Guapira opposita (Nyctaginaceae). Aust J Bot 63:608–617. https://doi.org/10.1071/BT15106
Flora e Funga do Brasil (2022) Flora e Funga do Brasil. Jardim botânico do Rio de Janeiro, Rio de Janeiro. http://floradobrasil.jbrj.gov.br. Accessed 11 Aug 2022
Fonseca-Kruel VS, Araujo DSD, Sá CFC, Peixoto AL (2009) Quantitative ethnobotany of a restinga forest fragment in Rio de Janeiro, Brazil. Rodriguésia 60:187–202. https://doi.org/10.1590/2175-7860200960110
França CV, Perfeito JPS, Resck IS, Gomes SM, Fagg CW, Castro CFS, Simeoni LA, Silveira D (2016) Potential radical-scavenging activity of Pouteria caimito leaves extracts. J Appl Pharm Sci 6:184–188. https://doi.org/10.7324/JAPS.2016.60727
Funasaki M, Lordello ALL, Viana AM, Catarina-Santa C, Floh EIS, Yoshida M, Kato MJ (2009) Neolignans and Sesquiterpenes from leaves and embryogenic cultures of Ocotea catharinensis (Lauraceae). J Braz Chem Soc 20(5):853–859. https://doi.org/10.1590/S0103-50532009000500008
Furtado FB, Aquino FJ, Nascimento EA, Martins CDM, Morais SA, Chang R, Cunha LCS, Leandro LF, Martins CHG, Martins MM, Silva CV, Machado FC, Oliveira A (2014) Seasonal variation of the chemical composition and antimicrobial and cytotoxic activities of the essential oils from Inga laurina (Sw.) Willd. Molecules 19:4560–4577. https://doi.org/10.3390/molecules19044560
Galvão JGFM (2014) Aspectos fitoquímicos, Etnobotânicos e farmacológicos da Schinus terebinthifolius Raddi: Uma revisão bibliográfica. Undergraduate Thesis, Universidade Federal da Paraíba
Garcez FR, Nuñez CV, Garcez WS, Almeida RM, Roque NF (1998) Sesquiterpenes, limonoid and coumarin from the wood bark of Guarea guidoniaI. Planta Med 64:79–80. https://doi.org/10.1055/s-2006-957375
Garrett R, Romanos MTV, Borges RM, Santos MG, Rocha L, Silva AJR (2012) Antiherpetic activity of a flavonoid fraction from Ocotea notata leaves. Braz J Pharmacogn 22(2):306–313. https://doi.org/10.1590/S0102-695X2012005000003
Ghisalberti EL (2000) Lantana camara L. (Verbenaceae). Fitoterapia 71(5) 467–486. https://doi.org/10.1016/S0367-326X(00)00202-1
Gilbert B, Favoreto R (2011) Schinus Terebinthifolius Radd. Rev Fitos 6:43–56
Gomes LFS (2011) Abordagem fitoquímica, determinação da atividade antiplasmódica in vitro e avaliação preliminar da toxicidade do extrato hidroetanólico das cascas de Aspidosperma excelsum Benth (Apocynaceae). MSc Dissertation, Universidade Federal do Pará
Gomes GA, Martins-Cardoso K, Santos FR, Florencio M, Rosa D, Zuma AA, Santiago GMP, Motta MCM, Carvalho MG, Fampa P (2020) Antileishmanial activity of the essential oils of Myrcia ovata Cambess. and Eremanthus erythropappus (DC) McLeisch leads to parasite mitochondrial damage. Nat Prod Res 35:6117–6121. https://doi.org/10.1080/14786419.2020.1827402
Gonçalves-Alvim SJ, Fernandes GW (2001) Biodiversity of galling insects: historical, community and habitat effects in four Neotropical savanas. Biodivers Conserv 10:79–98. https://doi.org/10.1023/A:1016602213305
Guedes LM, Aguilera N, Ferreira BG, Becerra J, Hernández V, Isaias RMS (2018) Anatomical and phenological implications between Schinus polygama (Cav.) (Cabrera) (Anacardiaceae) and the galling insect Calophya rubra (Blanchard) (Hemiptera: Psylloidea). Plant Biol 20:507–515. https://doi.org/10.1111/plb.12696
Guedes LM, Aguilera N, Ferreira BG, Riquelme S, Sáez-Carrillo K, Becerra J, Pérez C, Bustos E, Isaias RMS (2019) Spatiotemporal variation in phenolic levels in galls of calophyids on Schinus polygama (Anacardiaceae). J Plant Res 132:509–520. https://doi.org/10.1007/s10265-019-01118-6
Guedes LM, Sanhueza C, Torres S, Figueroa C, Gavilán E, Pérez CI, Aguilera N (2023) Gall-inducing Eriophyes tiliae stimulates the metabolism of Tilia platyphyllos leaves towards oxidative protection. Plant Physiol Biochem 195:25–36. https://doi.org/10.1016/j.plaphy.2022.12.014
Guimarães ALA, Neufeld PM, Santiago-Fernandes LDR, Vieira ACM (2014) Structure and development of ‘witches’ broom’ galls in reproductive organs of Byrsonima sericea (Malpighiaceae) and their effects on host plants. Plant Biol 14:493–504. https://doi.org/10.1111/plb.12231
Helayel MA, França TN, Seixas JN, Nogueira VA, Caldas SA, Peixoto PV (2009) Morte súbita em bovinos causada pela ingestão de Pseudocalymma elegans (Bignoniaceae) no município de Rio Bonito, RJ. Pesqui Vet Bras 29:498–508. https://doi.org/10.1590/S0100-736X2009000700003
Helayel MA, Caldas SA, Peixoto TC, França TN, Tokarnia CH, Döbereiner J, Nogueira VA, Peixoto PV (2011) O antagonismo com acetamida em experimentos com ovinos, caprinos e coelhos indica mono_luoroacetato como princípio tóxico de Pseudocalymma elegans Bignoniaceae. Pesqui Vet Bras 31:867–887. https://doi.org/10.1590/S0100-736X2011001000006
IBGE (2012) Manual técnico da vegetação brasileira. 2nd edn, IBGE, Rio de Janeiro. https://biblioteca.ibge.gov.br/index.php/biblioteca-catalogo?view=detalhes&id=263011. Accessed 11 Aug 2022
Ichikawa H, Takada Y, Shishodia S, Jayaprakassam B, Nair MG, Aggarwal BB (2006) Withanolides potentiate apoptosis, inhibit invasion, and abolish osteoclastogenesis through suppression of nuclear factor-KB (NF-KB) activation and NF-KB–regulated gene expression. Mol Cancer Ther 5:1434–1445. https://doi.org/10.1158/1535-7163.MCT-06-0096
Isaias RMS, Carneiro RGS, Oliveira DC, Santos JC (2013) Illustrated and annotated checklist of Brazilian gall morphotypes. Neotrop Entomol 42:230–239. https://doi.org/10.1007/s13744-013-0115-7
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. Biochim Biophys Acta 1850:1509–1517. https://doi.org/10.1016/j.bbagen.2015.03.007
Isaias RMS, Ferreira BG, Alvarenga DR, Barbosa LR, Salminen JP, Steinbauer MJ (2018) Functional compartmentalization of nutrients and phenolics in the tissues of galls induced by Leptocybe invasa (Hymenoptera: Eulophidae) on Eucalyptus camaldulensis (Myrtaceae). Aust Entomol 57:238–246. https://doi.org/10.1111/aen.12336
Jabour FF, Seixas JN, Tokarnia CH, Brito MF (2006) Variação da toxidez da Arrabidaea bilabiata (Bignoniaceae). Pesqui Vet Bras 26:171–176. https://doi.org/10.1590/S0100-736X2006000300008
Jacobo-Herrera NJ, Bremner P, Márquez N, Gupta MP, Gibbons S, Muñoz E, Heinrich M (2006) Physalins from Witheringia solanacea as modulators of the NF-κB cascade. J Nat Prod 69(3):328–331. https://doi.org/10.1021/np050225t
Joffily A, Vieira RC (2005) Anatomia foliar de Maytenus Mol. emend Mol. (Celastraceae), ocorrente no Estado do Rio de Janeiro, Brasil. Acta Bot Bras 19:549–461. https://doi.org/10.1590/S0102-33062005000300016
Kinghorn AD, Su BN, Jang DS, Chang LC, Lee D, Gu JQ, Carcache-Blanco EJ, Pawlus AD, Lee SK, Park EJ, Cuendet M, Gills JJ, Bhat K, Park HS, Mata-Greenwood E, Song LL, Jang M, Pezzuto JM (2004) Natural inhibitors of carcinogenesis. Plant Med 70:691–705. https://doi.org/10.1055/s-2004-827198
Kohli RK, Batish DR, Singh HP, Dogra KS (2006) Status, invasiveness and environmental threats of three tropical American invasive weeds (Parthenium hysterophorus L., Ageratum conyzoides L., Lantana camara L.) in India. Biol Invasions 8:1501–1510. https://doi.org/10.1007/s10530-005-5842-1
Krebs HC, Kemmerling W, Habermehl G (1994) Qualitative and quantitative determination of fluoroacetic acid in Arrabidea bilata and Palicourea marcgravii by F-NMR spectroscopy. Toxicon 32:909–913. https://doi.org/10.1016/0041-0101(94)90369-7
Kumar P (2016) Ultrastructural and biochemical studies on insect induced leaf galls in Alstonia scholaris L. Int J Plant Reprod Biol 8:64–81. https://doi.org/10.14787/ijprb.2016
Kuster VC, Rezende UC, Cardoso JCF, Isaias RMS, Oliveira DC (2019) How galling organisms manipulate the secondary metabolites in the host plant tissues?: a histochemical overview in Neotropical gall systems. In: Ramawat K (ed) Co-evolution of secondary metabolites. Reference series in phytochemistry. Springer, Cham. https://doi.org/10.1007/978-3-319-76887-8_29-1
Lima MAA, Oliveira FFM, Gomes GA, Lavor PL, Santiago GMP, Nagao-Dias AT, Arriaga AMC, Lemos TLG, Carvalho MG (2011) Evaluation of larvicidal activity of the essential oils of plants from Brazil against Aedes aegypti (Diptera: Culicidae). Afr J Biotechnol 10:11716–11720. https://doi.org/10.5897/AJB11.1102
Lima GS, Camara CAG, Moraes MM (2015) Composição de óleo essencial a partir de folhas de Byrsonima sericea. Chem Nat Comp 51:581–582
Lima SCM, Pacheco JS, Marques AM, Veltri ERP, Almeida-Lafetá RC, Figueiredo MR, Kaplan MAC, Torres-Santos EC (2018) Leishmanicidal activity of Withanolides from Aureliana fasciculata var. Fasciculata. Molecules 23:3160. https://doi.org/10.3390/molecules23123160
Lopes LCM, Lobão AQ (2013) Etnobotânica em uma comunidade de pescadores artesanais no litoral norte do Espírito Santo, Brasil. Bol Mus Mello Leitão 32:29–52
Luz FA, Mendonça-Jr MS (2019) Guilds in insect galls: who is who. Fla Entomol 102:207–210. https://doi.org/10.1653/024.102.0133
Magnago LFS, Martins SV, Schaefer CEGR, Neri AV (2012) Restinga forests of the Brazilian coast: richness and abundance of tree species on different soils. An Acad Bras Ciênc 84:807–822. https://doi.org/10.1590/S0001-37652012000300023
Maia VC (1999) Cecidomyiinae (Diptera, Cecidomyiidae) das restingas da Barra de Maricá, Itaipuaçu e Carapebus (Rio de janeiro, Brasil): Descrições e Dados Biológicos. PhD Thesis, Universidade Federal do Rio de Janeiro – Museu Nacional
Maia VC (2001) The gall midges (Diptera, Cecidomyiidae) from three restingas of Rio de Janeiro State, Brazil. Rev Bras Zool 18:583–629. https://doi.org/10.1590/S0101-81752001000200028
Maia VC (2018) Gall-inducing insects of restinga areas (Atlantic Forest) in Brazil: economic importance. Pap Avulsos Zool 58:1–13. https://doi.org/10.11606/1807-0205/2018.58.50
Maia VC (2020) Insect galls of Paraty (State of Rio de Janeiro, Southeastern Brazil)/Galhas de insetos de Paraty (estado do Rio de Janeiro, Sudeste do Brasil). Braz J Anim Environ Res 3:4104–4115. https://doi.org/10.34188/bjaerv3n4-106
Maia VC (2021) New biological data on Eugeniamyia dispar (Diptera, Cecidomyiidae), a pest on Eugenia uniflora L. (Myrtaceae). Biota Amazôn 11:17–21. https://doi.org/10.18561/2179-5746/biotaamazonia.v11n1p17-21
Maia VC, Oliveira JC (2010) Galhas de insetos da Reserva Biológica Estadual da Praia do Sul (Ilha Grande, Angra dos Reis, RJ). Biota Neotrop 10:227–237. https://doi.org/10.1590/S1676-06032010000400028
Maia VC, Silva LO (2016) Insect galls of Restinga de Marambaia (Barra de Guaratiba, Rio de Janeiro, RJ). Braz J Biol 76:787–795. https://doi.org/10.1590/1519-6984.05314
Maia VC, Souza MC (2013) Insect galls of the xeric vegetation of Ilha do Cabo Frio (Arraial do Cabo, RJ, Brazil). Biota Neotrop 13:278–288. https://doi.org/10.1590/S1676-06032013000300030
Mani MS (1964) Ecology of plant galls. Dr. W. Junk Publishers, The Hague
Manickam M, Padma P, Chansouria JPN, Ray AB (1997) Evaluation of antistress activity of Withafastousin D, a Withanolide of Datura fastuosa. Phytoter Res 11:384–385. https://doi.org/10.1002/(SICI)1099-1573(199708)11:5%3c384::AID-PTR105%3e3.0.CO;2-S
Mantuano DG, Barros CF, Scarano FR (2006) Variação da anatomia foliar dentro e entre três populações de restinga de Erythroxylum ovalifolium Peyr: (Erythroxylaceae) no Sudeste do Brasil. Rev Bras Bot 29(2):209–215. https://doi.org/10.1590/s0100-84042006000200002
Marques CA (2001) Importância econômica da família Lauraceae Lindl. Florest Amb 81(1):195–206
Martins AR, Bombo AB, Soares AN, Appezzato-da-Glória B (2013) Aerial stem and leaf morphoanatomy of some species of Smilax. Braz J Pharmacogn 23:576–584. https://doi.org/10.1590/S0102-695X2013005000043
Martins AR, Soares MKM, Redher VL, Bajay MM, Villela PMS, Zucchi MI, Appezzato-da-Glória B (2014) Use of anatomical, chemical, and molecular genetic characteristics in the quality control of medicinal species: a case study of Sarsaparilla (Smilax spp.). Econ Bot 20:1–16. https://doi.org/10.1007/s12231-014-9287-2
Medeiros MFT, Senna-Valle L, Andreata RHP (2007) Histórico e o uso da “salsa parrilha” (Smilax spp.) pelos boticários no Mosteiro de São Bento. Rev Bras Biociên 5:27–29
Melo LFM (2018) Extratos de Coccoloba alnifolia Casar e suas atividades biológicas. MSc Dissertation, Universidade Federal do Rio Grande do Norte
Melo-Júnior JF, Boeger MRT (2015) Riqueza, estrutura e interações edáficas em um gradiente de restinga do parque estadual do Acaraí, estado de Santa Catarina, Brasil. Hoehnea 42(2):207–232. https://doi.org/10.1590/2236-8906-40/2014
Meneguelli AZ, Camargo EES, Buccini DF, Roriz BC, Cerqueira GR, Moreno SE (2020) Ethnopharmacological and botanical evaluation of medicinal plants used by Brazilian Amazon Indian Community. Interações 21:633–645. https://doi.org/10.20435/inter.v21i3.2926
Moreira VF, Oliveira RR, Mathias L, Braz-Filho R, Vieira IJC (2010) New chemical constituents from Borreria verticillata (Rubiaceae). Helv Chim Acta 93:1751–1757. https://doi.org/10.1002/hlca.200900457
Moura MDB, Agra MF (1989) Apocynaceae tóxicas e medicinais ocorrentes nos Estados de Pernambuco e Paraíba, Brasil. Acta Bot Bras 3:273–279. https://doi.org/10.1590/S0102-33061989000300022
Moura MZD, Soares GLG, Isaias RMS (2005) Ontogenesis of internal secretory cells in Lantana camara L. (Verbenaceae). Bot J Linn Soc 148:427–431. https://doi.org/10.1111/j.1095-8339.2005.00426.x
Moura MZD, Soares GLG, Isaias RMS (2008) Species-specific changes in tissue morphogenes isinduced by two arthropod leaf gallers in Lantana camara L. (Verbenaceae). Aust J Bot 56:153–160. https://doi.org/10.1071/BT07131
Moura MZD, Soares GLG, Isaias RMS (2009a) Ontogenesis of the leaf and leaf galls induced by Aceria lantanae Cook (Acarina: Eriophyidae) in Lantana camara L. (Verbenaceae). Rev Bras Bot 32:271–282. https://doi.org/10.1590/S0100-84042009000200007
Moura MZD, Alves TMA, Soares GLG, Isaias RMS (2009b) Intra-specific phenotypic variations in Lantana camara leaves affect host selection by the gall maker Aceria lantanae. Biochem System Ecol 37:541–548. https://doi.org/10.1016/j.bse.2009.08.007
Nobrega LP, Silva JB, Luna BL, Ferreira BG (2021) Modulation of anatomical adaptations of leaves of Avicennia schaueriana (Acanthaceae) by a galling Meunieriella (Cecidomyiidae). Flora 274:151750. https://doi.org/10.1016/j.flora.2020.151750
Novaes P, Molinillo JMG, Varela RM, Macías FA (2013) Ecological phytochemistry of Cerrado (Brazilian savanna) plants. Phytochem Rev 12:839–855. https://doi.org/10.1007/s11101-013-9315-3
Novakova J, Vlkova E, Bonusova B, Rada V, Kokoska L (2013) In vitro selective inhibitory effect of 8-hydroxyquinoline against bifidobacteria and clostridia. Anaerobe 22:134–136. https://doi.org/10.1016/j.anaerobe.2013.05.008
Okoh-Esene RU, Suleiman JH, Thomas SA (2011) Proximate and phytochemical analysis of leaf, stem and root of Eugenia uniflora (Surinam or Pitanga cherry). J Nat Prod Plant Res 1:1–4
Oler JRL, Amorozo MCM, Monteiro R, Butturi-Gomes D (2019) Etnobotânica de plantas tóxicas como subsídio para campanhas de prevenção de acidentes: um estudo de caso em Cananéia, São Paulo, Brasil. Sci Plena. https://doi.org/10.14808/sci.plena.2019.111201
Oliveira RN, Dias IJM, Câmara CAG (2005a) Estudo comparativo do óleo essencial de Eugenia punicifolia (HBK) DC. de diferentes localidades de Pernambuco. Rev Bras Farmacogn 15:39–43. https://doi.org/10.1590/S0102-695X2005000100009
Oliveira FA, Chaves MH, Almeida FRC, Lima RCP, Silva RM, Maia JL, Brito GAAC, Santos FA, Rao VS (2005b) Protective effect of α- and β-amyrin, a triterpene mixture from Protium heptaphyllum (Aubl.) March. trunk wood resin, against acetaminophen-induced liver injury in mice. J Ethnopharmacol 98:103–108. https://doi.org/10.1016/j.jep.2005.01.036
Oliveira DC, Isaias RMS, Moreira ASFP, Magalhães TA, Lemos-Filho JP (2011) Is the oxidative stress caused by Aspidosperma spp. galls capable of altering leaf photosynthesis? Plant Sci 180:489–495. https://doi.org/10.1016/j.plantsci.2010.11.005
Oliveira DC, Moreira ASFP, Isaias RMS, Martini V, Rezende UC (2017) Sink status and photosynthetic rate of the leaflet galls induced by Bystracoccus mataybae (Eriococcidae) on Matayba guianensis (Sapindaceae). Front Plant Sci 8:1249. https://doi.org/10.3389/fpls.2017.01249
Olivero-Verbel J, Parra-Guerra A, Caballero-Gallardo K, Sierra-Marquez L, Fuentes-Lopez K, Franco-Marmolejo J, Jannasch AS, Sepulveda MS, Stashenko E (2021) The aqueous extract of Fridericia chica grown in northern Colombia ameliorates toxicity induced by Tergitol on Caenorhabditis elegans. Comp Biochem Physiol C 244:109026. https://doi.org/10.1016/j.cbpc.2021.109026
Pace MR, Lohmann LG, Angyalossy V (2011) Evolution of disparity between the regular and variant phloem in Bignonieae (Bignoniaceae). Am J Bot 98:602–618. https://doi.org/10.3732/ajb.1000269
Pace MR, Lohmann LG, Olmstead RG, Angyalossy V (2015) Wood anatomy of major Bignoniaceae clades. Plant Syst Evol 301:967–995. https://doi.org/10.1007/s00606-014-1129-2
Passos Oliveira A, Raith M, Kuster R, Rocha L, Hamburger M, Potterat O (2012) Metabolite profiling of the leaves of the brazilian folk medicine Sideroxylon obtusifolium. Planta Med 78:703–710. https://doi.org/10.1055/s-0031-1298269
Pereira RJ, Cardoso MG (2012) Metabólitos secundários vegetais e benefícios antioxidantes. J Biotechnol Biodivers 3:146–152
Pereira RV, Mecenas AS, Malafaia CRA, Amaral ACF, Muzitano MF, Simas NK, Leal ICR (2019) Evaluation of the chemical composition and antioxidant activity of extracts and fractions of Ocotea notata (Ness) Mez (Lauraceae). Nat Prod Res 34:3004–3007. https://doi.org/10.1080/14786419.2019.1602828
Pessini GL, Holetz FB, Sanches NR, Cortez DAG, Dias Filho BP, Nakamura CV (2003) Avaliação da atividade antibacteriana e antifúngica de extratos de plantas utilizados na medicina popular. Rev Bras Farmacogn 13:21–24. https://doi.org/10.1590/S0102-695X2003000300009
Pitz HS, Pereira A, Blasius MB, Voytena APL, Affonso RCL, Fanan S, Trevisan ACD, Ribeiro-do-Valle RM, Maraschin M (2016) In vitro evaluation of the antioxidant activity and wound healing properties of jaboticaba (Plinia peruviana) fruit peel hydroalcoholic extract. Oxidat Med Cell Longev 2016:3403586. https://doi.org/10.1155/2016/3403586
Pollitos PAZ, Tomazello-Filho M (2007) Espécies lenhosas do gênero Croton L. (Euphorbiaceae) no Estado do Acre. Rev Bras Biociênc 5:177–179
Pontes FC, Abdalla VCP, Imatomi M, Fuentes LFG, Gualtieri SCJ (2018) Antifungal and antioxidant activities of mature leaves of Myrcia splendens (Sw.) DC. Braz J Biol 79:127–132. https://doi.org/10.1590/1519-6984.179829
Portugal-Santana A, Isaias RMS (2014) Galling insects are bioindicators of environmental quality in a Conservation Unit. Acta Bot Bras 28:594–608. https://doi.org/10.1590/0102-33062014abb3510
Price PW, Fernandes GW, Waring GL (1987) Adaptative nature of galls. Environ Entomol 16:15–24. https://doi.org/10.1093/ee/16.1.15
Rebelo AM, Piovezan M, Silva-Júnior AA, Micke GA (2011) Eletroforese capilar como ferramenta de “screening” fitoquímico. Resumos da 33a Reunião Anual da Sociedade Brasileira de Química. Sociedade Brasileira de Química. http://sec.sbq.org.br/cdrom/33ra/resumos/T0404-2.pdf. Accessed 11 Aug 2022
Reddy NM (2013) Lantana camara Linn. chemical constituents and medicinal properties: a review. Sch Acad J Pharm 2(6):445–448
Rezende UC, Moreira ASFP, Kuster VC, Oliveira DC (2018) Structural, histochemical and photosynthetic profiles of galls induced by Eugeniamyia dispar (Diptera: Cecidomyiidae) on the leaves of Eugenia uniflora (Myrtaceae). Rev Biol Trop 66:1469–1480. https://doi.org/10.15517/rbt.v66i4.32531
Ribeiro RS (2007). Imunomodulação e ação anti-Leishmania (Viannia) braziliensis por Ouratea cuspidata (Ochnaceae). MSc Dissertation, Universidade Federal Rural do Rio de Janeiro
Rodrigues PA, Morais SM, Souza CM, Magalhães DV, Vieira ÍG, Andrade GM, Vietla SR, Santos FA (2012) Gastroprotective effect of Byrsonima sericea DC leaf extract against ethanol-induced gastric injury and its possible mechanisms of action. An Acad Bras Ciên 84:113–122. https://doi.org/10.1590/S0001-37652012000100011
Rodrigues AR, Maia VC, Couri MS (2014) Insect galls of restinga areas of Ilha da Marambaia, Rio de Janeiro, Brazil. Rev Bras Entomol 58:173–197. https://doi.org/10.1590/S0085-56262014000200010
Rombola TH (2014) Efeito do extrato aquoso de folhas de guanandi (Calophyllum brasiliense Cambess) no controle do crescimento de Microcystis aeruginosa. PhD Thesis, Universidade Estadual Paulista
Rovedder APM, Piazza EM, Thomas PA, Felker RM, Hummel RB, Farias JAD (2016) Potential medicinal use of forest species of the deciduous seasonal forest from Atlantic forest biome, south Brazil. Braz Arch Biol Technol 59:e16150329. https://doi.org/10.1590/1678-4324-2016150329
Sá RD, Santana ASCO, Randau KP (2016) Caracterização anatômica e histoquímica das folhas de Eugenia uniflora L. J Environ Anal Progress 1:96–105. https://doi.org/10.24221/jeap.1.1.2016.1001.96-105
Salvi-Júnior A (2009) Schinus terebinthifolius Raddi: estudo anatômico e histoquímico das folhas e investigação do potencial farmacêutico do extrato etanólico e suas frações. MSc Dissertation, Universidade Estadual Paulista
Sampaio TS, Blank AF, Gagliardi PR, Wisniewski JA, Arrigoni-Blank MF, Nizio DAC, Alves MF, Nascimento-Junior AF (2020) Antifungal activity of essential oils of Myrcia ovata chemotypes and their major compounds on phytopathogenic fungi. Biosci J 36:364–375. https://doi.org/10.14393/BJ-v36n2a2020-42315
Santos MG, Fevereiro PCA, Reis GL, Barcelos JI, Ney FMMA (2009) Plantas da Restinga: potencial econômico, 1st edn. Technical Books, Rio de Janeiro
Santos M, Fermino-Junior PC, Vailati MG, Paulilo MTS (2010) Aspectos estruturais de folhas de indivíduos de Guapira opposita (Vell) Reitz (Nyctaginaceae) ocorrentes em restinga e na floresta ombrófila densa. Rev Bot Insula 39:59–78. https://doi.org/10.5007/2178-4574.2010v39p59
Santos IBS, Santos dos Santos B, Oliveira JRS, Costa WK, Zagmignan A, Silva LCN, Ferreira MRA, Lermen VL, de Sousa Lermen MSB, da Silva AG, Ximenes RM, Soares LAL, Paiva PMG, Lima VLM, Correia MTS, da Silva MV (2020) Antioxidant action and in vivo anti-inflammatory and antinociceptive activities of Myrciaria floribunda fruit peels: possible involvement of opioidergic system. Adv Pharmacol Pharm Sci 2020:1258707. https://doi.org/10.1155/2020/1258707
Schapoval EES, Silveira SM, Miranda ML, Alice CB, Henriques AT (1994) Evaluation of some pharmacological activities of Eugenia uniflora L. J Ethnopharmacol 44:137–142. https://doi.org/10.1016/0378-8741(94)01178-8
Severi JA (2010) Uso sustentável da biodiversidade brasileira: prospecção químico-farmacológica em plantas superiores: Guapira ssp. Thesis Universidade Estadual Paulista Júlio de Mesquita Filho
Siani AC, Garrido IS, Monteiro SS, Carvalho ES, Ramos MFS (2004) Protium icicariba as a source of volatile essences. Biochem System Ecol 32:477–489. https://doi.org/10.1016/j.bse.2003.11.003
Silva JS, Araújo T (2020) Are Fabaceae the principal super-hosts of galls in Brazil? An Acad Bras Ciênc 92:e20181115. https://doi.org/10.1590/0001-3765202020181115
Silva VC, Alves AN, Santana A, Carvalho MG (2006) Constituintes fenólicos e terpenóides isolados das raízes de Andira fraxinifolia (Fabaceae). Quím Nova 29:1184–1186. https://doi.org/10.1590/S0100-40422006000600007
Silva CAM, Simeoni LA, Silveira D (2009) Genus Pouteria: chemistry and biological activity. Braz J Pharmacogn 19:501–509. https://doi.org/10.1590/S0102-695X2009000300025
Silva TBC, Costa COD, Galvão AFC, Bomfim LM, Rodrigues ACBC, Mota MCS, Dantas AA, Santos TR, Soares MBP, Bezerra DP (2016) Cytotoxic potential of selected medicinal plants in northeast Brazil. BMC Complement Altern Med 16:199. https://doi.org/10.1186/s12906-016-1166-1
Silva RHM, Lima NFM, Lopes AJO, Vasconcelos CC, Mesquita JWC, Mesquita LSS, Lima FCVM, Ribeiro MNS, Ramos RM, Cartágenes MSS, Garcia JBS (2017) Antinociceptive activity of Borreria verticillata: in vivo and in silico studies. Front Pharmacol 8:283. https://doi.org/10.3389/fphar.2017.00283
Silva AL, Terceiro LEL, Lima MF, Costa-Silva R, Santos EAV, Agra MF (2019) Leaf and stem micromorphology of Byrsonima sericea DC. by light and scanning electron microscopy. Micros Res Tech 83:287–296. https://doi.org/10.1002/jemt.23412
Silvia MS, Connor EF (2017) Differences in meristems between monocots and dicots and susceptibility to attack by gall-inducing insects. Arthropod Plant Interact 11:485–494. https://doi.org/10.1007/s11829-017-9502-z
Soares GLG, Isaias RMS, Gonçalves SJMR, Christiano JCS (2000) Alterações químicas induzidas por coccídeos galhadores (Coccoidea: Brachyscelidae) em folhas de Rollinia laurifolia Schdtl. (Annonaceae). Rev Bras Zoociênc 2:103–116
Solovchenko A, Schmitz-Eiberger M (2003) Significance of skin flavonoids for UV-B-protection in apple fruits. J Exp Bot 54(389):1977–1984. https://doi.org/10.1093/jxb/erg199
Stone GN, Schonrögge K (2003) The adaptive significance of insect gall morphology. Trend Ecol Evol 18:512–522. https://doi.org/10.1016/S0169-5347(03)00247-7
Su BN, Gu JQ, Kang YH, Park EJ, Pezzuto JM, Kinghorn AD (2004) Induction of the phase II enzyme, quinone reductase, by withanolides and norwithanolides from Solanaceous species. Minii-Rev Organ Chem 1:115–123. https://doi.org/10.2174/1570193043488926
Sudhir S, Budhiraja RD, Miglani GP, Arora B, Gupta LC, Garg KN (1985) Pharmacological studies on leaves of Withania somnifera. Plant Med 52:61–63. https://doi.org/10.1055/s-2007-969072
Sultan SS (2000) Phenotypic plasticity for plant development, function and life history. Trend Plant Sci 5:537–542. https://doi.org/10.1016/S1360-1385(00)01797-0
Takenaka IKTM, Amorim JM, Barros PAV, Brandão GC, Contarini SML, Melo ELSS, Almeida-Leite CM, Martins FS, Cardoso VN, Castilho RO, Fernandes SOA (2020) Chemical characterization and anti-inflammatory assessment of the hydroethanolic extract of Fridericia chica. Rev Bras Farmacogn 30:559–567. https://doi.org/10.1007/s43450-020-00085-7
Tanaka JCA, Silva CCD, Dias Filho BP, Nakamura CV, Carvalho JED, Foglio MA (2005) Chemical constituents of Luehea divaricata Mart. (Tiliaceae). Quím Nova 28:834–837. https://doi.org/10.1590/S0100-40422005000500020
Thomas E, Van Damme P (2010) Plant use and management in homegardens and swiddens: evidence from the Bolivian Amazon. Agrofor Syst 80:131–152. https://doi.org/10.1007/s10457-010-9315-x
Thomas E, Semo L, Morales M, Noza Z, Nuñez H, Cayuba A, Noza M, Humaday N, Vaya J, Van Damme P (2011) Ethnomedicinal practices and medicinal plant knowledge of the Yuracarés and Trinitarios from Indigenous Territory and National Park Isiboro-Sécure, Bolivian Amazon. J Ethnopharmacol 133:153–163. https://doi.org/10.1016/j.jep.2010.09.017
Thomazi RD, Rocha R, Oliveira M, Bruno AV, Silva AG (2013) Um panorama da vegetação das restingas do Espírito Santo no contexto do litoral brasileiro. Natureza Online 11(1):1–6
Tokarnia CH, Döbereiner J, Canella CFC, Guimarães DJ (1969) Intoxicação experimental por Pseudocalymma elegans (Vell.) Kuhlm. em bovinos. Pesqui Agropecu Bras 4:195–204
Uchôa PKS, Silva JND Jr, Silveira ER, Lima MAS, Braz-Filho R, Costa-Lotufo LV, Araújo AJ, Moraes MO, Pessoa CDO (2013) Trachylobane and kaurane diterpenes from Croton floribundus Spreng. Quím Nova 36:778–782. https://doi.org/10.1590/S0100-40422013000600006
Ushie OA, Adamu HM (2010) Phytochemical screening of Borreria verticillata leaves. J Agric Biotechnol Ecol 3:108–117
Vieira ACM, Kraus JE (2007) Biologia e estrutura da galha do pedicelo de Byrsonima sericea DC. (Malpighiaceae) induzida por Lepidoptera. Rev Bras Biociênc 5:402–404
Vieira ACM, Cravo ACP, Ferraris GK, Ferreira APRC, Souza MAA, Konno TUP, Campos NV, Guimarães ALA, Xavier QMP, Vieira MAS (2021) Estudo morfológico e anatômico de galhas foliares induzidas por Cecidomyiidae em espécies da restinga de Maricá – RJ. In: Prata EG (ed) Biologia: ensino, pesquisa e extensão - uma abordagem do conhecimento científico nas diferentes esferas do saber - volume 2. Científica Digital, Guarujá, pp 113–128. https://doi.org/10.37885/210805620
Wiczkowski W, Szawara-Nowak D, Topolska J (2013) Red cabbage anthocyanins: profile, isolation, identification, and antioxidant activity. Food Res Int 51:303–309. https://doi.org/10.1016/j.foodres.2012.12.015
Zamberlan PM (2012) Estudos filogenéticos e filogeográficos nos gêneros Athenaea sendtn. e Aureliana sendtn. (solanaceae). PhD Thesis, Universidade Federal do Rio Grande do Sul
Zani SMW, Lordello ALL (2007) Alcalóides aporfinóides do gênero Ocotoea (Lauraceae). Quím Nova 30:92–98. https://doi.org/10.1590/S0100-40422007000100020
Zeni ALB, Bosio F (2011) Use de plantas medicinais em uma comunidade rural de Mata Atlântica - Nova Rússia, SC. Neotrop Biol Conserv 6:55–63. https://doi.org/10.4013/nbc.2011.61.07
Zuque ALF, Watanabe ES, Ferreira AMT, Arruda ALA, Resende UM, Bueno NR, Castilho RO (2004) Avaliação das atividades antioxidante, antimicrobiana e citotóxica de Couepia grandiflora Benth. (Chrysobalanaceae). Rev Bras Farmacogn 14:129–136. https://doi.org/10.1590/S0102-695X2004000200006
Acknowledgements
We are grateful to Nathan Smith for reviewing the English.
Funding
We thank the following: the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, Brazil) for the master’s scholarships given to LPN and RRMC (Finance Code 001); the Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ, Brazil) for the financial support (ARC E-26/010.002709/2019; APQ1 E-26/211.608/2021; E-26/010.001384/2019) and scientific initiation scholarships given to LGS and GSM; and the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Brazil) for the scientific initiation scholarship given to PEFB.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that there are no conflicts of interest.
Additional information
Handling Editor: Makoto Tokuda.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
11829_2023_9997_MOESM1_ESM.xlsx
Supplementary file1 (XLSX 55 kb)
Online Resource 1 Host plants and gall morphotypes in restingas of Rio de Janeiro State, Brazil. Municipalities of occurrence: ANG Angra dos Reis, ARC Arraial do Cabo, ARA Araruama, BAG Barra de Guaratiba, CAR Carapebus, CBF Cabo Frio, MAC Macaé, MAR Maricá, MNG Mangaratiba, PAR Paraty, RIO Rio de Janeiro, SAQ Saquarema, SFI São Francisco de Itabapoana, SJB São João da Barra. References: [1] Maia, (1999), [2] Maia and Oliveira (2010), [3] Maia and Souza, (2013), [4] Rodrigues et al. (2014), [5] Carvalho-Fernandes et al. (2016), [6] Maia and Silva, (2016), [7] Maia, (2018), [8] Maia, (2020).
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Martins, G.S., Nobrega, L.P., Castro, R.R.M. et al. Who are the superhosts? The chemical and structural profiles of superhosts of galling arthropods and the gaps in gall studies. Arthropod-Plant Interactions 17, 705–740 (2023). https://doi.org/10.1007/s11829-023-09997-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11829-023-09997-2