Brazilian Journal of and Environmental Research 1374 ISSN: 2595-573X Geographic distribution of eight Neotropical species of (Diptera, Insecta)

Distribuição geográfica de oito espécies neotropicais de Cecidomyiidae (Diptera, Insecta)

DOI: 10.34188/bjaerv4n1-114

Recebimento dos originais: 20/11/2020 Aceitação para publicação: 20/12/2020

Valéria Cid Maia Doutora em Zoologia pelo Museu Nacional/Universidade Federal do Museu Nacional/Universidade Federal do Rio de Janeiro Quinta da Boa Vista, São Cristovão, Rio de Janeiro, RJ, 20.940-040, Brazil. E-mail: [email protected]

ABSTRACT The geographic distribution of eight Neotropical species of gall midges (Diptera, Cecidomyiidae), Couridiplosis vena, Dactylodiplosis heptaphylli, Dasineura couepiae, D. ovalifoliae, Epihormomyia miconiae, Lopesia spinosa, Mayteniella distincta, and Schizomyia macropillata is extended based on data retrieved from galled exsiccates of two herbaria: Museu Nacional (R) and Jardim Botânico do Rio de Janeiro (RB). The geographic distribution of each gall-inducing species was updated, mapped and compared to that of its host species. New geographic records are reported.

Keywords: Endemism, gall, host plant, phytogeographic domains

RESUMO A distribuição geográfica de oito espécies neotropicais de Cecidomyiidae (Diptera), Couridiplosis vena, Dactylodiplosis heptaphylli, Dasineura couepiae, D. ovalifoliae, Epihormomyia miconiae, Lopesia spinosa, Mayteniella distincta e Schizomyia macropillata é ampliada com base em dados obtidos a partir de exsicatas com galhas de dois herbários: Museu Nacional (R) e Jardim Botânico do Rio de Janeiro (RB). A distribuição geográfica de cada espécie galhadora foi atualizada, mapeada e comparada com a distribuição da planta hospedeira. Novos registros geográficos são assinalados.

Palavras-chave: Endemismo, galha, planta hospedeira, domínios fitogeográficos

1 INTRODUCTION Although Cecidomyidae have great ecological and economic importance, the geographical distribution of most Neotropical species is still punctual due to lack of studies (Gagné and Jaschhof, 2014). As most gall midges are monophagous, their occurrence depends on the presence of their host . The increasing deforestation of Brazilian biomes, especially the Atlantic Forest and Cerrado, which concentrate most of the known Cecidomyiidae species, may endanger the preservation of these . In this context, it is essential to know their distributional area. Herbaria can make an important contribution to this knowledge. Examining galled exsiccates Brazilian Journal of Animal and Environmental Research, Curitiba, v.4, n.1, p. 1374-1383 jan./mar. 2021

Brazilian Journal of Animal and Environmental Research 1375 ISSN: 2595-573X may add new geographic records. This procedure is reliable since each gall midge species induces a morphologically unique gall in its host plant (Stone & Schönrogge, 2003). In the this work, data on geographic distribution of eight gall midges species, Couridiplosis vena Maia, 2004, Dactylodiplosis heptaphylli Maia, 2004, Dasineura couepiae Maia, 2001, D. ovalifoliae Fernandes & Maia 2011, Epihormomyia miconiae Maia, 2001, Lopesia spinosa Maia, 2004, Mayteniella distincta Maia, 2001, and Schizomyia macropillata Maia, 2005 obtained from literature and exsiccates examination were compiled in an attempt to establish their distributional limits. Couridiplosis vena induces vein swelling in Croton floribundus Spreng. (Euphorbiaceae), Dactylodiplosis heptaphylli ovoid leaf galls in Protium heptaphyllum (Aubl.) Marchand (Burseraceae), Dasineura couepiae globoid leaf galls in Couepia ovalifolia (Schott) Benth. ex Hook.f. (), D. ovalifoliae lenticular leaf galls in Erythroxylum ovalifolium Peyr. (Erythroxylaceae), Epihormomyia miconiae ovoid bud galls in Miconia cinnamomifolia (DC.) Naudin (Melastomataceae), Lopesia spinosa ovoid leaf galls in Croton floribundus, Mayteniella distincta lenticular leaf galls in Montverdia obtusifolia (Mart.) Biral (Celastraceae), and Schizomyia macrocapillata globoid leaf galls in Bauhinia brevipes Vogel (Fabaceae). Regarding plants, three of them are native to Brazil, Croton floribundus, Protium heptaphyllum, and Bauhinia brevipes; while Monteverdia obtusifolia is endemic of Brazil; Miconia cinnamomifolia and Couepia ovalifolia are endemic of Atlantic Forest; and Erythroxylum ovalifolium is endemic of the state of Rio de Janeiro (Flora do Brasil, 2020).

2 MATERIAL AND METHODS Data were obtained from a review of literature in which these host plant and gall midges species were reported, as well as from direct observation of galled exsiccates from two Brazilian herbaria, Museu Nacional (R) and Jardim Botânico do Rio de Janeiro (RB). Galled exsiccates, their labels and all gall morphotypes were photographed. New records were reported by comparison with published data. Based on localities, phytogeographic domains were verified, using maps of biomes and vegetation of Brazil (IBGE, 2004). The validity of botanic names were checked in the site “Flora do Brasil, 2020”, as well as the distribution of each host plant. Maps of plant distribution were retrieved from the same site and data on each gall-inducing species were added to these maps to represent its current distribution.

3 RESULTS A total of 1,094 exsiccates were examined: Bauhinia brevipes n=160 (3 of them with galls of

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Brazilian Journal of Animal and Environmental Research 1376 ISSN: 2595-573X Schizomyia macrocapillata) (Fig. A), Couepia ovalifolia n=75 (9 of them with galls of Dasineura couepiae) (Fig. B), Croton floribundus n=148 (7 of them with galls of Lopesia spinosa) (Fig. C) and 4 with galls of Couridiplosis vena) (Fig. D), Erythroxylum ovalifolium n=101 (6 of them with galls of Dasineura ovalifoliae) (Fig. E), Miconia cinnamomifolia n=128 (4 of them with galls of Epihormomyia miconiae) (Fig. F), Monteverdia obtusifolia n=319 (55 of them with galls of Mayreniella distincta) (Fig. G), and Protium heptaphyllum n=163 (9 of them with galls of Dactylodiplosis heptaphylli) (Fig. H).

Figures A-H: Galls of Cecidomyiidae (Diptera) in exsiccates. A) Gall of Schizomyia macrocapillata Maia, 2005 in Bauhinia brevipes Vogel (Fabaceae); B) Gall of Dasineura couepiae Maia, 2001 in Couepia ovalifolia (Schott) Benth. ex Hook.f. (Chrysobalanaceae); C) Gall of Lopesia spinosa Maia, 2004 in Croton floribundus; D) Gall of Couridiplosis vena Maia, 2004 in Croton floribundus Spreng. (Euphorbiaceae); E) Gall induced of Dasineura ovalifoliae Fernandes & Maia, 2011 in Erythroxylum ovalifolium Peyr. (Erythroxylaceae); F) Gall of Epihormomyia miconiae Maia, 2001 in Miconia cinnamomifolia (DC.) Naudin (Melastomataceae); G) Gall of Mayteniella distincta Maia, 2001 in Monteverdia obtusifolia (Mart.) Biral (Celastraceae); H) Gall of Dactylodiplosis heptaphylli Maia, 2004 in Protium heptaphyllum (Aubl.) Marchand (Burseraceae).

A B C D

G H E F

New geographic records were reported for these eight gall midge species. One botanical name was updated: Maytenus obtusifolia Mart., basionym synonym of Monteverdia obtusifolia (Mart.) Biral. New geographic records were reported.

New records: Couridiplosis vena Maia, 2004 New state records: Brazil: : Utinga: Fazenda Sossego (semideciduous seasonal forest), 15.IV. 1986, Salim Jordy Filho & H.P. Bautista col., RB365173; Espírito Santo: Santa Leopoldina: Distrito de Mangaraí: Cachoeira do Retiro (secondary forest, Atlantic Forest), 03.IX.2005, Crepaldi, M. O. S. & Carvalho, R. col., RB 440351; Paraná: Diamante do Norte (Estação Ecológica do Caiuá) 19.V.2006, Zeiden D. N. M. col., RB 460265. Dactylodiplosis heptaphylii Maia, 2004 New state records: Brazil: Bahia: Caravelas (Ilha do Cassurubá), 03.V.2007, H. M. Dias 147,

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Brazilian Journal of Animal and Environmental Research 1377 ISSN: 2595-573X R. R. da Sila & J. A. S. Serafim col., RB507605; Conde (dense ombrophylous forest), 06.XII.1997, J. Costa, M. Clara Ferreira & C.B. Nascimento 97 col., RB 379888; Espírito Santo: Linhares, 13.V.1977, G. Martinelli 2003 et al. col., RB252596; Mato Grosso do Sul: Rio Verde: Alto Pantanal, 02.XI.2012, Barbosa T. D. M. 1550, Carmo J. A. M. & Scatinha A. V. col., RB592342. New municipality record: Brazil, Rio de Janeiro, Macaé, 12.X.2002, C. Farney 4456, M. C. A. Pereira, I. Garay, R. M. Darigo, L. A. F. Santos, RB393518. Dasineura couepiae Maia, 2001 New state record: Brazil: Bahia: Caravelas, Menezes L. T .F. 1554 col., RB 746954. New municipality records: Brazil: Rio de Janeiro: Rio de Janeiro (restinga de Itapeba, Recreio dos Bandeirantes), 01.X.1950, Segadas-Viana 2731, R177629 and 13.VIII.1964, N. Santos col., R177636; Espírito Santo: São Mateus (restinga forest), 17.X.2010, Giaretta A. O., Menezes L. T. F., Ribeiro, M. & Rocha T. L. col. Dasineura ovalifolia Fernandes & Maia 2011 New municipality record: Brazil, Rio de Janeiro, Macaé, low restinga forest, 04.XII.1995, C. Farney 3544 & D. B. Gonçalves col., RB327538. Epihormomyia miconiae Maia 2001 New state record: Brazil: Espírito Santo: Santa Teresa, 27.XI.2006, L. Kollmann 9395, F. Capelo, E. Locac, B. Sampaio & T. Flores col., RB493591. New municipality record: Brazil: Rio de Janeiro: Cabo Frio (restinga de Cabo Frio), 08.X.1968, D. Sucre 3840 col., RB1419. Lopesia spinosa Maia, 2004 New state records: Brazil: Alagoas: Murici (Estação Ecológica de Murici), 31.VII.2008, Haroldo C. de Lima 6983, F. L. R. Filardi, R. D. Ribeiro & A. G. da Silva col., RB470067; Rio de Janeiro: Miguel Pereira (Sítio Xapuri), 11.I.2006, CSS 341 col., RB 461947, Teresópolis (semidecidous forest), 11.X.2005, O. Thier 194 col., RB 428783, Nova Friburgo (Reserva Ecológica Municipal Macaé de Cima), 16.V.1990, R. Guedes et al. col., RB 448931, Rio de Janeiro: Rio de Janeiro (Maciço da Tijuca), 05.I.1987, Mario Gomes 95 col. RB675260, (Jacarepaguá), 15.IV.1959, A. P. Duarte 4730 & E. D. M. Pereira col., RB 109287. New municipality record: São Paulo: Bananal, 12.XII.1998, S. V. A. Pessoa et al. 948 col., RB 343392. Mayteniella distincta Maia, 2001 New state records:Brazil: Pará: Marajó, 16.IV.1927, A. Ducke col., RB20837; Bahia: Nova Viçosa, 22.VII.1979, G. Martinelli 6024 col., RB192329, Alagoinhas, 29.VII.1990, Maria Clara Ferreira 294 col., RB 311342; Espírito Santo: Presidente Kennedy (restinga), 18.V.1994, C. Farney 3332, D. Araújo & L. S. Sarahyba col., RB311268, RB311270, Guarapari (Parque Estadual Paulo

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Brazilian Journal of Animal and Environmental Research 1378 ISSN: 2595-573X César Vinha), 03.XII.1999, , J. M. A. Braga 5935 col., RB530573. Schizomyia macrocapillata Maia, 2005 New state records: Brazil: Mato Grosso: Xavantina (Barra do Garças), R762723; São Paulo: Selviria (Ilha Solteira) (cerradão), 18.X.1990, Santos J. dos col., RB295665. New municipality record:Brazil: Goiás: Monte Alegre (semideciduous forest), 12.IV.2000, M. L. Fonseca, R. C. Mendonça, M. Aparecida da Silva & E. Cardoso col., RB357341.

4 DISCUSSION Couridiplosis vena was previously recorded only in two Brazilian states: Minas Gerais (Serra de São José, municipality of Tiradentes - Maia & Fernandes 2004), and São Paulo (Altinópolis - Ribeiro et al. 2019). Three states were added to its area: Bahia, Espírito Santo, and Paraná, expanding the distributional limits1.430 km to the North, and 748 km to South. Dactylodiplosis heptaphylli was previously recorded in four Brazilian states: (Tamandaré - Santos et al. 2012), Goiás (Serra dos Pireneus -Araújo et al. 2011), Minas Gerais (Tiradentes and Ingaí - Maia & Fernandes 2004 and Malves & Frieiro-Costa 2012, respectively), and Rio de Janeiro (Carapebus and Maricá - Maia 2001, São João da Barra and São Francisco de Itabapoana - Maia & Carvalho-Fernandes 2016). Three states were added to its distribution: Bahia, Espírito Santo, and Mato Grosso do Sul, expanding it 711 Km to West. Dasineura couepiae was restricted to two Brazilian states: Espírito Santo (Guarapari - Bregonci et al. 2010) and Rio de Janeiro (Maricá - Maia 2001, Araruama, Arraial do Cabo, and Cabo Frio - Carvalho-Fernandes et al. 2016. Its area was expanded to Bahia, 351 km to North. Dasineura ovalifoliae remains restricted to Rio de Janeiro, as its host plant occurs only in this state (Flora do Brasil, 2020). This galler has been recorded in several municipalities, namely: Rio de Janeiro (restinga de Marambaia - Maia & Silva 2016 and restinga de Grumari - Oliveira & Maia 2005), Maricá - Maia 2001, Saquarema, Araruama, Arraial do Cabo, and Cabo Frio -Carvalho- Fernandes et al. 2016, Carapebus - Maia 2001, and São João da Barra - Carvalho-Fernandes et al. 2016). A new municipality was added to its distribution: Macaé. Epihormomyia miconiae was known only from the type-locality: state of Rio de Janeiro, municipality of Carapebus (Maia 2001). Its distribution was extended to Espírito Santo, 273 to North. Lopesia spinosa was previously recorded in two Brazilian states: Minas Gerais (Delfinópolis - Urso-Guimarães et al. 2003, Serra de São José - Maia & Fernandes 2004, and São Tomé das Letras - Maia 2013) and São Paulo (Altinópolis - Ribeiro et al. 2019). Two states are added to its area: Rio de Janeiro (four municipalities: Miguel Pereira, Teresópolis, Nova Friburgo, and Rio de Janeiro) and Alagoas (Murici), extending its distribution 1,684 Km to North.

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Brazilian Journal of Animal and Environmental Research 1379 ISSN: 2595-573X Mayteniella distincta was restricted to the state of Rio de Janeiro, with records in ten municipalities: Mangaratiba (Rodrigues et al. 2014), Rio de Janeiro (restinga de Marambaia - Maia & Silva 2016 and restinga de Grumari - Oliveira & Maia 2005), Maricá (Maia 2001), Arraial do Cabo (Monteiro et al., 1994), Carapebus (Maia 2001), São Francisco de Itabapoana (Maia & Carvalho-Fernandes, 2016), Araruama, Cabo Frio, Saquarema, and São João da Barra (Carvalho- Fernandes et al. 2016). Three states were added to its area: Pará, Bahia, and Espírito Santo, expanding its distribution 2,505 km to North. Schizomyia macrocapillata Maia, 2005 was previously reported in three Brazilian states: Bahia (Barreiras - Lima & Calado 2018 and Caetité - Costa et al. 2014), Goiás (Hidrolândia - Silva et al. 2018), and Minas Gerais (Três Marias - Maia & Fernandes 2005). Its area was extended to Mato Grosso, 420Km to West, and São Paulo, 706 km to South. Dasineura ovalifoliae presented the smallest area of distribution (restrict to Rio de Janeiro), followed by Epihormomyia miconiae (from Espírito Santo to Rio de Janeiro), and Dasineura couepiae (from Bahia to Rio de Janeiro). The first species is associated with an endemic plant of Rio de Janeiro State, Erythroxylum ovalifolium, so its distribution is restricted to the same state (Fig. I). The second and the third species are associated with endemic plants of Atlantic Forest, Miconia cinnamomifolia with occurrence from Santa Catarina to Pernambuco, and Couepia ovalifolia from Rio de Janeiro to Pernambuco. Nevertheless, the geographic distribution of both gallers is more restricted than that of their host plant (Figs. J-K), what suggests that these insects may have a larger distribution than the current known. Mayteniella distincta is associated with an endemic plant of Brazil, Monteverdia obtusifolia, with occurrence from Pará to São Paulo (Fig. L). The other gallers are associated with native plants of Brazil. Among the investigated host plants, Protium heptaphyllum has the widest distribution in Brazil, followed by Croton floribundus, and Bauhinia brevipes. However, the current distribution of these gallers does not cover the entire distribution area of their hosts (Figs. M-P), so there are still gaps in their distribution, which can be filled from survey of other herbaria or field works.

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Brazilian Journal of Animal and Environmental Research 1380 ISSN: 2595-573X

Figures I-P. Maps of Brazil with the geographic distribution of eight gall midge species (Diptera, Cecidomyiidae) and that of their host plants. I) Dasineura ovalifoliae Fernandes & Maia 2011 and Erythroxylum ovalifolium Peyr. (Erythroxylaceae); J) Epihormomyia miconiae Maia, 2001 and Miconia cinnamomifolia (DC.) Naudin (Melastomataceae); K) Dasineura couepiae Maia, 2001 and Couepia ovalifolia (Schott) Benth. ex Hook.f. (Chrysobalanaceae); L) Mayteniella distincta Maia, 2001 and Monteverdia obtusifolia (Mart.) Biral (Celastraceae); M) Dactylodiplosis heptaphylli Maia, 2004 and Protium heptaphyllum (Aubl.) Marchand (Burseraceae); N) Couridiplosis vena Maia, 2004 and Croton floribundus Spreng. (Euphorbiaceae); O) Lopesia spinosa Maia, 2004 and Croton floribundus; P) Schizomyia macrocapillata Maia, 2005 and Bauhinia brevipes Vogel (Fabaceae). Green circles = geographic distribution of the gall midge species. Colorful areas = geographic distribution of the host plants in Brazil.

I J K

L M N

O P

5 CONCLUSION The geographic distribution of all gall midge species was widened based on galled exsiccates. Dasineura ovalifoliae is restricted to Rio de Janeiro since its host plant occurs only in this state. However, the distribution area of the other gall-inducing species can be wider than the reported, since their host plants occur in other states.

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Brazilian Journal of Animal and Environmental Research 1381 ISSN: 2595-573X This studies showed that galled exsiccates can be a very good tool to increase the knowledge about gallers` distribution.

ACKNOWLEDGEMENTS The author thanks the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for financial support (Proc. 301481/2017-2), Dr. Rafaela Forzza (Jardim Botânico do Rio de Janeiro) and Dr. Ruy José Válka Alves (Museu Nacional) for providing access to the herbaria and the anonymous reviewers.

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Brazilian Journal of Animal and Environmental Research 1382 ISSN: 2595-573X REFERENCES

Araújo, W.S., Santos, B.B. & Gomes-Klein, V.L. 2011. galls from Serra dos Pireneus, GO, Brazil. Biota Neotropica 11(2): 357-365.

Bregonci, J.M., Polycarpo, P.V. & Maia, V.C. 2010. Galhas de insetos do Parque Estadual Paulo César Vinha (Guarapari, ES, Brasil). Biota Neotropica 10(1): 265-274.

Carvalho-Fernandes, S.P., Ascendino, S., Maia, V.C. & Couri, M.S. 2016. Diversity of insect galls associated with coastal shrub vegetation in Rio de Janeiro, Brazil. Anais da Academia Brasileira de Ciências 88(3):1407–1418.

Costa, E.C., Carvalho-Fernandes, S.P. & 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.

Flora do Brasil, 2020. Jardim Botânico do Rio de Janeiro [under construction] http://floradobrasil.jbrj.gov.br. Access on: 10/Dec/2020.

Gagné, R.J. & Jaschhof, M. 2014. A catalog of the Cecidomyiidae (Diptera) of the world. 3rd Edition. Digital version. 493 pp. https://www.ars.usda.gov/SP2UserFiles/Place/80420580/Gagne_2014_World_Cecidomyiida e_Catalog_3rd_Edition.pdf

IBGE, 2004. Mapas de Biomas do Brasil. http://www.ibge.gov.br/home/presidencia/noticias/ 21052004 biomashtml.shtm. Accessed on: 2019–5–25.

Lima, V.P. & Calado, D. 2018. Morphological characterization of insect galls and new records of associated invertebrates in a Cerrado area in Bahia State, Brazil. Brazilian Journal of Biology 78(4): 636-643.

Maia, V.C. 2001. The gall midges (Diptera, Cecidomyiidae) from three restingas of Rio de Janeiro State, Brazil. Revista Brasileira de Zoologia 18(2):583–629. https://doi.org/10.1590/S0101- 81752001000200028

Maia, V.C. 2013. Insect galls of São Tomé das Letras (MG, Brazil). Biota Neotropica 13(4): 164- 189.

Maia, V.C. & Carvalho-Fernandes, S.P. 2016. Insect galls of a protected remnant of the Atlantic Forest tableland from Rio de Janeiro State (Brazil). Revista Brasileira de Entomologia 60:40-56. https://doi.org/10.1016/j.rbe.2015.09.001

Maia, V.C. & Fernandes, G.W. 2004. Insect galls from Serra de São José (Tiradentes, Minas Gerais, Brazil). Brazilian Journal Biology 64:423–445.

Maia, V.C. & Fernandes, G.W. 2005. Two new species of (Diptera: Cecidomyiidae) associated with Bauhinia brevipes (Fabaceae) in Brazil. Zootaxa 1091: 27–40.

Maia, V.C. & Silva, L.O. 2016. Insect galls of restinga de Marambaia (Barra de Guaratiba, Rio de Janeiro, RJ). Brazilian Journal of Biology 73(6):787–795.

Malves, K. & Frieiro-Costa, F.A. 2012. List of Plants with Galls Induced by Insects from the UNILAVRAS/Boqueirão Biological Reserve, Ingaí, state of Minas Gerais, Brazil. Check List 8(3): 426-431.

Brazilian Journal of Animal and Environmental Research, Curitiba, v.4, n.1, p. 1374-1383 jan./mar. 2021

Brazilian Journal of Animal and Environmental Research 1383 ISSN: 2595-573X Oliveira, J.C. & Maia, V.C. 2005. Ocorrência e Caracterização de Galhas de Insetos na Restinga de Grumari (Rio de Janeiro, RJ, Brasil). Arquivos do Museu Nacional 63(4): 669-675.

Ribeiro, A.N., Balbi, M.I.P.A. & Urso-Guimarães, M.V. 2019. Characterization of insect galls from a vegetation area in Altinópolis, São Paulo State, Brazil. Papéis Avulsos de Zoologia 59: e20195904.

Rodrigues, A.R., Maia, V.C. & Couri, M.S. 2014. Insect galls of restinga areas of Ilha da Marambaia, Rio de Janeiro, Brazil. Revista Brasileira de Entomologia 58(2):173–197. https://doi.org/10.1590/S0085-56262014000200010

Santos, J.C., Almeida-Cortez, J.S. & Fernandes, G.W. 2012. Gall-inducing insects from Atlantic forest of Pernambuco, Northeastern Brazil. Biota Neotropica 12(3):196-212.

Silva, E.C., Santos, B.B. & Araújo, W.S. 2018. Insect gall occurrence in savanna and forest remnant sites of Hidrolândia, GO, Brazil Central. Papéis Avulsos de Zoologia 58: e20185804.

Stone, G.N. & Schönrogge, K. 2003. The adaptive significance of insect gall morphology. Trends in Ecology and Evolution 18(10): 512-522.

Urso-Guimarães, M.V., Scareli-Santos, C. & Bonifácio-Silva, A.C. 2003. Occurrence and Characterization of Entomogen Galls in Plants from Natural Vegetation Areas in Delfinópolis, MG, Brazil. Brazilian Journal of Biology 63(4): 705-715.

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