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REPRESENTATIVITY OF THE GENUS ASPHONDYLIA LOEW, 1850 (DIPTERA, CECIDOMYIIDAE) IN BRAZIL

ABSTRACT

Representativity of the genus Asphondylia Loew, 1850 (Diptera, Cecidomyiidae) in Brazil. This cosmopolitan genus includes 272 galling species described, of which about 100 occur in the Neotropical Region. The present study goal to evaluate the richness of Asphondylia in Brazil, to provide an updated list of the host plant species, to determine the plant organs where galls are induced, to update the geographic distribution of the genus, to verify it distribution in the Brazilian biomes, and to the list the associated fauna. The survey data was carried out by consulting the Cecidomyiidae collection of the Museu Nacional/UFRJ, the database “Web of Science” using Asphondylia and Brasil/Brazil as keywords, 51 Brazilian inventories and two catalogues. Asphondylia is represented by 58 species in Brazil, among them, twenty are already known and 38 are still undetermined. The Brazilian described species represent 8% of the total of known species of Asphondylia in the world and 21% of species of the Neotropical fauna. This genus is associated with 51 plant species and 20 plant families in Brazil. Asteraceae comprise the greatest richness of Asphondylia species. This genus was found in five biomes, among them the Atlantic forest has the highest species richness. The associated fauna comprises parasitoids (Hymenoptera) and inquilines (Lepidoptera, Coleoptera and Diptera).

KEY-WORDS:
Gall; Insect-plant interaction; Geographic distribution; Host plant

RESUMO

Representatividade do gênero Asphondylia Loew, 1850 (Diptera, Cecidomyiidae) no Brasil. Este gênero cosmopolita inclui 272 espécies galhadoras descritas, das quais cerca de 100 ocorrem na Região Neotropical. O objetivo deste estudo foi avaliar a riqueza de Asphondylia no Brasil, fornecer uma lista atualizada das espécies de plantas hospedeiras, determinar os órgãos das plantas onde as galhas são induzidas, atualizar a distribuição geográfica do gênero, verificar sua distribuição nos biomas do Brasil e uma lista da fauna associada. Os dados da pesquisa foram realizados consultando a coleção de Cecidomyiidae do Museu Nacional/UFRJ, a base de dados “Web of Science”, utilizando as palavras Asphondylia e Brasil/Brazil, 51 inventários brasileiros e dois catálogos. Asphondylia é representada por 58 espécies no Brasil, entre elas, 20 são já conhecidas e 38 ainda são indeterminadas. As espécies descritas no Brasil representam 8% do total de espécies conhecidas de Asphondylia no mundo e 21% das espécies da fauna Neotropical. Este gênero está associado a 51 espécies de plantas e 20 famílias de plantas no Brasil. As Asteraceae hospedam a maior riqueza de espécies de Asphondylia. Este gênero foi encontrado em cinco biomas, entre eles a Mata Atlântica obteve a maior riqueza de espécies. A fauna associada compreende parasitóides (Hymenoptera) e inquilinos (Lepidoptera, Coleoptera e Diptera).

PALAVRAS-CHAVE:
Galhas; Interação inseto-planta; Distribuição geográfica; Planta hospedeira

INTRODUCTION

Asphondylia Loew, 1850 belongs to the tribe Asphondyliini, currently with 505 described species, subtribe Asphondyliina, which is the most diverse in the Neotropics (Gagné & Jaschhof, 2014GAGNÉ, R.J. & JASCHHOF, M. 2014. A Catalog of the Cecidomyiidae (Diptera) of the World. 3.ed. Disponível em: https://www.ars.usda.gov/ARSUserFiles/80420580/Gagne_2014_World_Cecidomyiidae_Catalog_3rd_Edition.pdf.
https://www.ars.usda.gov/ARSUserFiles/80...
). This cosmopolitan genus includes 272 described galling species, of which about 100 occur in the Neotropical Region (Gagné, 2004GAGNÉ, R.J. 2004. A catalog of the Cecidomyiidae (Diptera) of the world. Memoirs of the Entomological Society of Washington, 25:1-408.). Carneiro et al., (2009a)CARNEIRO, M.A.A.; BRANCO, C.S.A.; BRAGA, C.E.D.; ALMADA, E.D.; COSTA, M.B.M.; MAIA, V.C. & FERNANDES, G.W. 2009a. Are gall midge species (Diptera, Cecidomyiidae) host plant-specialists? Revista Brasileira de Entomologia, 53:365-378. reports the importance of genera as one of the dominant among galling found in Brazil, represented by 20 species. Asphondylia species have been recorded on 66 plant families in the world, being most frequent on Asteraceae, Fabaceae and Chenopodiaceae (Maia et al., 2009MAIA, V.C.; SANTOS, J.C. & FERNANDES, G.W. 2009. Asphondylia fructicola, a new species of Cecidomyiidae (Diptera) associated with Solanum sp. (Solanaceae) from Brazil. Revista Brasileira de Entomologia, 53:166-170.).

The genus is morphologically characterized by a needlelike ovipositor, two-toothed gonostylus, three-segmented palpi and presence of upper and lower horns on the pupal frons (Gagné, 1994GAGNÉ, R.J. 1994. The Gall Midges of the Neotropical Region. Ithaca, Cornell University Press. 352p.; Maia et al., 2009MAIA, V.C.; SANTOS, J.C. & FERNANDES, G.W. 2009. Asphondylia fructicola, a new species of Cecidomyiidae (Diptera) associated with Solanum sp. (Solanaceae) from Brazil. Revista Brasileira de Entomologia, 53:166-170.). Asphondylia taxonomy is challenging because adult morphology differs little among species. All species share the neckless, cylindrical antennal flagellomeres in both sexes, the needle-like ovipositor and conspicuously enlarged seventh sternite in the female, and the compact male genitalia with the spherical gonostyli positioned dorsally rather than apically (Gagné, 1994GAGNÉ, R.J. 1994. The Gall Midges of the Neotropical Region. Ithaca, Cornell University Press. 352p.; Dorchin et al., 2015DORCHIN, N.; JOY, B.J.; HILKE, L.K.; WISE, M.J. & ABRAHAMSON, W.G. 2015. Taxonomy and phylogeny of the Asphondylia species (Diptera: Cecidomyiidae) of North American goldenrods: challenging morphology, complex host associations, and cryptic speciation. Zoological Journal of the Linnean Society, 174:265-304.). The third-instar larvae possess a well-developed, usually four-toothed spatula on the first thoracic segment. The pupation in all Asphondylia species takes place inside the gall rather than in the soil (Gagné, 1989GAGNÉ, R.J. 1989. The plant-feeding midges of North America. Ithaca, Comstock. xi + 368p., 1994GAGNÉ, R.J. 1994. The Gall Midges of the Neotropical Region. Ithaca, Cornell University Press. 352p.). The pupae are characterized by well-developed horn-like antennal bases, a varying number of facial horns, and transverse dorsal rows of spines on the abdominal segments (Gagné, 1989GAGNÉ, R.J. 1989. The plant-feeding midges of North America. Ithaca, Comstock. xi + 368p., 1994GAGNÉ, R.J. 1994. The Gall Midges of the Neotropical Region. Ithaca, Cornell University Press. 352p.) that assist in breaking out of the galls just before adults’ emergence.

Constant assessment of biodiversity knowledge is essential to guide future efforts inventories in poorly studied areas, so that they can conserve endangered species (Toma & Maia, 2012TOMA, T.S.P. & MAIA, V.C. 2012. Representatividade do gênero Clinodiplosis Kieffer (Diptera, Cecidomyiidae) no Brasil. Papéis Avulsos de Zoologia, 52:223-231.). Moreover, considering the great diversity in the Neotropics, little is known about the fauna of Cecidomyiidae in this region, especially compared to other parts of the world, getting to be around six times smaller than the Palaearctic fauna (Gagné, 2007GAGNÉ, R.J. 2007. Species numbers of Cecidomyiidae (Diptera) by zoogeographical Region. Proceedings of the Entomological Society of Washington, 109, 499-499.; Toma & Maia, 2012TOMA, T.S.P. & MAIA, V.C. 2012. Representatividade do gênero Clinodiplosis Kieffer (Diptera, Cecidomyiidae) no Brasil. Papéis Avulsos de Zoologia, 52:223-231.).

The present study goal to evaluate the richness of Asphondylia in Brazil, to determine the plant organs where galls are induced, to give an updated list of the host plant species, highlighting the their endemism and categories of conservational status, as well as to verify the species richness in each Brazilian biome, to update the geographic distribution of the genus and the respective associated fauna.

MATERIAL AND METHODS

The survey data on the species of Asphondylia was carried out by consulting the collection of Cecidomyiidae the Museu Nacional/UFRJ (the only reference collection to the family in Brazil) and, concomitantly, a literature review was performed on the database “Web of Science” using Asphondylia and Brasil/Brazil as keywords. Furthermore, the catalog of Cecidomyiidae of the world (Gagné & Jaschhof, 2014GAGNÉ, R.J. & JASCHHOF, M. 2014. A Catalog of the Cecidomyiidae (Diptera) of the World. 3.ed. Disponível em: https://www.ars.usda.gov/ARSUserFiles/80420580/Gagne_2014_World_Cecidomyiidae_Catalog_3rd_Edition.pdf.
https://www.ars.usda.gov/ARSUserFiles/80...
) was used to check all described Brazilian Asphondylia species until 2014. Besides, all insect galls Brazilian inventories were examined, as well as the catalog of galls of the Central and South Americas (Houard, 1933HOUARD, C. 1933. Les Zoocécidies des Plantes de l’Amérique du Sud e de l’Amérique Central. Paris, Hermann et Cie. 519p.), which comprises data on Brazilian galls.

Literature data were compiled from six papers retrieved from the Web of Science (Carneiro et al., 2009aCARNEIRO, M.A.A.; BRANCO, C.S.A.; BRAGA, C.E.D.; ALMADA, E.D.; COSTA, M.B.M.; MAIA, V.C. & FERNANDES, G.W. 2009a. Are gall midge species (Diptera, Cecidomyiidae) host plant-specialists? Revista Brasileira de Entomologia, 53:365-378.; Maia, 2013aMAIA, V.C. & FERNANDES, G.W. 2005. Two new species of Asphondylinii (Diptera: Cecidomyiidae) associated with Bahuinia brevipes (Fabaceae) in Brazil. Zootaxa, 1091:27-40.; Maia et al., 2009MAIA, V.C.; SANTOS, J.C. & FERNANDES, G.W. 2009. Asphondylia fructicola, a new species of Cecidomyiidae (Diptera) associated with Solanum sp. (Solanaceae) from Brazil. Revista Brasileira de Entomologia, 53:166-170.; Maia et al., 2008bMAIA, V.C.; SILVEIRA, F.A.O.; OLIVEIRA, L.A. & XAVIER, M.F. 2008b. Asphondylia gochnatiae, a new species of gall midge (Diptera: Cecidomyiidae) associated with Gochnatia polymorpha (Less.) Cabrera (Asteraceae). Zootaxa, 1740:53-58.; Maia & Fernandes, 2005MAIA, V.C. & FERNANDES, G.W. 2005. Two new species of Asphondylinii (Diptera: Cecidomyiidae) associated with Bahuinia brevipes (Fabaceae) in Brazil. Zootaxa, 1091:27-40.; Gagné et al., 2001GAGNÉ, R.J.; ODA, R.A. & MONTEIRO, R.F. 2001. The gall midges (Diptera: Cecidomyiidae) of Mikania glomerata (Asteraceae) in southeastern Brazil. Proceedings of the Entomological Society of Washington, 103:110-134.), 51 Brazilian gall inventories (Almada & Fernandes, 2011ALMADA, E.D. & FERNANDES, G.W. 2011. Insetos indutores de galhas em florestas de terra firme e em reflorestamentos com espécies nativas na Amazônia Oriental, Pará. Brasil. Boletim Museu Paraense Emilio Goeldi, 6:163-196.; Araújo et al., 2011ARAÚJO, W.S.; SANTOS, B.B. & GOMES-KLEIN, V.L. 2011. Insect galls from Serra dos Pireneus, GO, Brazil. Biota Neotropica, 11:357-365.; Araújo et al., 2014ARAÚJO, W.S.; SOBRAL, F.L. & MARACAHIPES, L. 2014. Insect galls of the Parque Nacional das Emas (Mineiros, GO, Brazil). Check List, 10:1445-1451.; Bregonci et al., 2010BREGONCI, J.M.; POLYCARPO, P.V. & MAIA, V.C. 2010. Galhas de insetos do Parque Estadual Paulo César Vinha (Guarapari, ES, Brasil). Biota Neotropica, 10:227-238.; Carneiro et al., 2009bCARNEIRO, M.A.A.; BORGES, R.A.X.; ARAÚJO, A.P.A.; FERNANDES, G.W. 2009b. Insetos indutores de galhas da porção sul da Cadeia do Espinhaço, MG, Brasil. Revista Brasileira de Entomologia, 53:570-592.; Coelho et al., 2009COELHO, M.S.; ALMADA, E.D.; FERNANDES, G.W.; CARNEIRO, M.A.A.; SANTOS, R.M.; SANCHEZ-AZOFEIFA, A. 2009. Gall inducing arthropods from a seasonally dry tropical Forestin Serra do Cipó, Brazil. Revista Brasileira de Entomologia, 53:404-414.; Coelho et al., 2013aCOELHO, M.S.; CARNEIRO, M.A.; BRANCO, C.; BORGES, R.A.X. & FERNANDES, G.W. 2013a. Gall-inducing insects from Campos de Altitude, Brazil. Biota Neotropica, 4:139-151.; Coelho et al., 2013bCOELHO, M.S.; CARNEIRO, M.A.; BRANCO, C.; BORGES, R.A.X. & FERNANDES, G.W. 2013b. Gall-inducing insects from Serra do Cabral, Minas Gerais, Brazil. Biota Neotropica, 3:102-109.; Costa et al., 2014COSTA, E.C.; CARVALHO-FERNANDES, S.P. & SANTOS-SILVA, J. 2014. Galhas de insetos de uma área de transição caatinga-cerrado no Nordeste do Brasil. Sitientibus, Série Ciências Biológicas, 14:1-9.; Dreger-Jauffret & Shorthouse, 1992DREGER-JAUFFRET, F. & SHORTHOUSE, J.D. 1992. Diversity of gall-inducing insects and their galls. In: Shorthouse, J.D. & Rohfritsch, O. (Eds.). Biology of Insect-Induced Galls. Oxford, Oxford University Press. p. 8-33.; Fernandes & Negreiros, 2006FERNANDES, G.W. & NEGREIROS, D. 2006. A comunidade de insetos galhadores da RPPN Fazenda Bulcão, Aimorés, Minas Gerais, Brasil. Lundiana, 7:111-120.; Fernandes et al., 1988FERNANDES, G.W.; TAMEIRÃO-NETO, E. & MARTINS, R.P. 1988. Ocorrência e caracterização de galhas entomógenas na vegetação do campus Pampulha da Universidade Federal de Minas Gerais. Revista Brasileira de Zoologia, 5:11-29.; Fernandes et al., 1997FERNANDES, G.W.; ARAÚJO, R.C.; ARAÚJO, S.C.; LOMBARDI, J.A.; PAULA, A.S.; LOYOLLA JR., R.R. & CORNELISSEN, T.G. 1997. Insect galls from savanna and rocky fields of the Jequitinhonha Valley, Minas Gerais, Brazil. Naturalia, 22:221-224.; Fernandes et al., 2001FERNANDES, G.W.; JULIÃO, G.R.; ARAÚJO, R.C.; ARAÚJO, S.C.; LOMBARDI, J.A.; NEGREIROS, D. & VARNEIRO, M.A.A. 2001. Distribution and morphology of insect galls of the Rio Doce Valley, Brazil. Naturalia, 26:221-244.; Gagné et al., 2001GAGNÉ, R.J.; ODA, R.A. & MONTEIRO, R.F. 2001. The gall midges (Diptera: Cecidomyiidae) of Mikania glomerata (Asteraceae) in southeastern Brazil. Proceedings of the Entomological Society of Washington, 103:110-134.; Gagné, 1994GAGNÉ, R.J. 1994. The Gall Midges of the Neotropical Region. Ithaca, Cornell University Press. 352p.; Gagné, 2004GAGNÉ, R.J. 2004. A catalog of the Cecidomyiidae (Diptera) of the world. Memoirs of the Entomological Society of Washington, 25:1-408.; Gonçalves-Alvim & Fernandes, 2001GONÇALVES-ALVIM, S.J. & FERNANDES, G.W. 2001. Comunidades de insetos galhadores (Insecta) em diferentes fisionomias do cerrado em Minas Gerais, Brasil. Revista Brasileira de Zoologia, 18:289-305.; Julião et al., 2002JULIÃO, G.R.; AMARAL, M.E.C. & FERNANDES, G.W. 2002. Galhas de insetos de suas plantas hospedeiras do Pantanal sul-mato-grossense. Naturalia, 27:47-74.; Maia & Carvalho, 2016MAIA, 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.; Maia & Fernandes, 2004MAIA, V.C. & FERNANDES, G.W. 2004. Insect galls from Serra de São José (Tiradentes, Minas Gerais, Brazil). Brazilian Journal Biology, 64:423-445.; Maia & Fernandes, 2005MAIA, V.C. & FERNANDES, G.W. 2005. Two new species of Asphondylinii (Diptera: Cecidomyiidae) associated with Bahuinia brevipes (Fabaceae) in Brazil. Zootaxa, 1091:27-40.; Maia & Oliveira, 2010MAIA, V.C. & OLIVEIRA, J.C. 2010. Galhas de insetos da Reserva Biológica Estadual da Praia do Sul (Ilha Grande, Angra dos Reis, RJ). Biota Neotropica, 10:227-238.; Maia & Souza, 2013MAIA, V.C. & SOUZA, M.C. 2013. Insect galls of the xeric vegetation of Ilha do Cabo Frio (Arraial do Cabo, RJ, Brazil). Biota Neotropica, 13:278-288.; Maia et al., 1992MAIA, V.C.; COURI, M.S. & MONTEIRO, R.F. 1992. Sobre seis espécies de Asphondylia Loew, 1850 do Brasil (Diptera, Cecidomyiidae). Revista Brasileira de Entomologia, 36:653-661.; Maia et al., 2008aMAIA, V.C.; MAGENTA, M.A.G. & MARTINS, S.E. 2008a. Ocorrência e caracterização de galhas de insetos em áreas de restinga de Bertioga (São Paulo, Brasil). Biota Neotropica, 8:167-197.; Maia et al., 2009MAIA, V.C.; SANTOS, J.C. & FERNANDES, G.W. 2009. Asphondylia fructicola, a new species of Cecidomyiidae (Diptera) associated with Solanum sp. (Solanaceae) from Brazil. Revista Brasileira de Entomologia, 53:166-170.; Maia et al., 2014MAIA, V.C.; CARDOSO, L.J.T. & BRAGA, J.M.A. 2014. Insect galls from Atlantic Forest areas of Santa Teresa, Espírito Santo, Brazil: characterization and occurrence. Boletim do MBML, 33:47-129.; Maia, 2001MAIA, V.C. 2001. The gall midges (Diptera, Cecidomyiidae) from three restingas of Rio de Janeiro State, Brazil. Revista Brasileira de Zoologia, 18:583-629.; Maia, 2004MAIA, V.C. 2004. Description of a new species of Bruggmannia Tavares (Diptera, Cecidomyiidae) associated with Guapira opposita (Vell.) Reitz (Nyctaginaceae) from Brazil. Revista Brasileira de Zoologia, 21:761-764.; Maia, 2011MAIA, V.C. 2011. Characterization of insect galls, gall makers, and associated fauna of Platô Bacaba (Porto de Trombetas, Pará, Brazil). Biota Neotropica, 11:37-53.; Maia, 2013bMAIA, V.C. 2013b. Galhas de insetos em restingas da região sudeste do Brasil com novos registros. Biota Neotropica, 13:183-209.; Maia, 2014MAIA, V.C. 2014. Insect galls of Itamonte (Minas Gerais, Brazil): characterization and occurrence. Biota Neotropica, 14:1-17.; Mendonça et al., 2014MENDONÇA, M.S.; TOMA, T.S.P. & SILVA, J.S. 2014. Galls and Galling Arthropods of Southern Brazil. In: Fernandes, G.W. & Santos, J.C. (Eds.). Neotropical Insect Galls. New York, Springer. cap. 14, p. 221-256.; Oliveira & Maia, 2005OLIVEIRA, J.C. & MAIA, V.C. 2005. Ocorrência e caracterização de galhas de insetos na restinga de Grumari (Rio de Janeiro, RJ, Brasil). Arquivo do Museu Nacional, 63:669-676.; Pamplona et al., 2000PAMPLONA, D.M.; MAIA, V.C.; COURI, M.S.; LAMAS, C.J.E. & AIRES, C.C.C. 2000. A survey on Diptera of Paquetá Island, Rio de Janeiro, RJ (Insecta, Diptera). Entomologist’s Monthly Magazine, 136:169-175.; Rodrigues et al., 2014RODRIGUES, 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, 58:173-197.; Rübsaamen, 1907RÜBSAAMEN, E.H. 1907. Beiträge zur Kenntnis aussereuropäischer Zoocecidien. III. Beitrag [cont.]: Gallen aus Brasilien und Peru. Marcellia, 6:110-173.; Rübsaamen, 1916RÜBSAAMEN, E.H. 1916. Beitrag zur Kentnis aussereuropäischer Gallmücken. Sitzungsberichte der Gesellschaft Naturforschender Freunde zu Berlin, 1915:431-481.; Saito & Urso-Guimarães, 2012SAITO, V.S. & URSO-GUIMARÃES, M.V. 2012. Characterization of galls, insect galls and associated fauna of Ecological Station of Jataí (Luiz Antônio, SP). Biota Neotropica, 12:99-107.; Santos et al., 2010SANTOS, B.B.; FERREIRA, H.D. & ARAÚJO, W.S. 2010. Ocorrência e caracterização de galhas entomógenas em uma área de floresta estacional semidecídua em Goiânia, Goiás, Brasil. Acta Botanica Brasilica, 24:243-249.; Santos et al., 2011aSANTOS, J.C.; ALMEIDA-CORTEZ, J.S. & FERNANDES, G.W. 2011a. Diversity of gall-inducing insects in the high altitude wetland forests in Pernambuco, Northeastern, Brazil. Brazilian Journal of Biology, 71:47-56.; Santos et al., 2011bSANTOS, J.C.; ALMEIDA-CORTEZ, J.S. & FERNANDES, G.W. 2011b. Richness of gall-inducing insects in the tropical dry forest (caatinga) of Pernambuco. Revista Brasileira de Entomologia, 55:45-54.; Tavares, 1909TAVARES, J.S. 1909. Contributio prima ad cognitionem cecidologiae braziliae. Brotéria: Série Zoológica, 8:5-28.; Tavares, 1916TAVARES, J.S. 1916. Cecidomyias novas do Brazil. Brotéria, 14:36-57.; Tavares, 1917TAVARES, J.S. 1917. Cecidias brazileiras que se criam em plantas das Compositae, Rubiaceae, Tiliaceae, Lythraceae e Artocarpaceae. Brotéria: Série Zoológica, 15:113-181.; Tavares, 1918TAVARES, J.S. 1918. Cecidologia brazileira. Cecídias que se criam em plantas das famílias das Verbenaceae, Euphorbiaceae, Malvaceae, Anacardiaceae, Labiatae, Rosaceae, Anonaceae, Ampleidaceae, Bignoniaceae, Aristochiaceae e Solanaceae. Brotéria: Série Zoológica, 16:21-68.; Toma & Mendonça, 2013TOMA, T.S.P. & MENDONÇA, M.S. 2013. Gall-inducing insects of an Araucaria Forest in southern Brazil. Revista Brasileira de Entomologia, 57:225-233.; Urso-Guimarães & Amorim 2002URSO-GUIMARÃES, M.V. & AMORIM, D.S. 2002. New Brazilian species of Asphondyliini (Diptera, Cecidomyiidae). Revista Brasileira de Entomologia, 46:561-570.; Urso-Guimarães & Scareli-Santos, 2006URSO-GUIMARÃES, M.V. & SCARELLI-SANTOS, C. 2006. Galls and gall makers in plants fromthe Pé-de-Gigante Cerrado Reserve, Santa Rita do Passa Quatro, SP, Brazil. Brazilian Journal Biology, 66:357-36.; Urso-Guimarães et al., 2003URSO-GUIMARÃES, M.V.; SCARELLI-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, 63:705-715.), and two catalogues (Houard, 1933HOUARD, C. 1933. Les Zoocécidies des Plantes de l’Amérique du Sud e de l’Amérique Central. Paris, Hermann et Cie. 519p.; Gagné & Jaschhof, 2014GAGNÉ, R.J. & JASCHHOF, M. 2014. A Catalog of the Cecidomyiidae (Diptera) of the World. 3.ed. Disponível em: https://www.ars.usda.gov/ARSUserFiles/80420580/Gagne_2014_World_Cecidomyiidae_Catalog_3rd_Edition.pdf.
https://www.ars.usda.gov/ARSUserFiles/80...
).

Information about the host plant (botanical species and family), galled plant organs, shape and type of gall, and geographical distribution for each species were provided, whenever possible. Biomes were defined from the collection locations. Data on origin and categories of the conservational status of the host plants were found in the Lista da Flora do Brasil 2016 website (Flora do Brasil, 2020FLORA DO BRASIL. 2002. Jardim Botânico do Rio de Janeiro. [under construction]. Available on: Available on: http://floradobrasil.jbrj.gov.br . Access on: 24/02/2017.
http://floradobrasil.jbrj.gov.br...
).

According to Carneiro et al., (2009a)CARNEIRO, M.A.A.; BRANCO, C.S.A.; BRAGA, C.E.D.; ALMADA, E.D.; COSTA, M.B.M.; MAIA, V.C. & FERNANDES, G.W. 2009a. Are gall midge species (Diptera, Cecidomyiidae) host plant-specialists? Revista Brasileira de Entomologia, 53:365-378. the gall morphology associated with the identification of host-plant species is a reliable richness indicator of the gall-inducing insects. About 95% of described species of cecidomyiids from Brazil can be identified based on these two data together (Coelho et al., 2013aCOELHO, M.S.; CARNEIRO, M.A.; BRANCO, C.; BORGES, R.A.X. & FERNANDES, G.W. 2013b. Gall-inducing insects from Serra do Cabral, Minas Gerais, Brazil. Biota Neotropica, 3:102-109.). In the present study, we adopted both information to evaluate the richness of the genus Asphondylia.

Considering the high host specificity of the gall midges, the undetermined species probably belong to new species, as they are associated with new records of plants. Based on this specificity, we included also the undetermined species of Asphondylia in the following discussion (Maia & Silva, 2013MAIA, V.C. & SILVA, M.C. 2013. The genus Dasineura Rondani, 1840 (Diptera, Cecidomyiidae). Brazilian Journal Biology, 73:801-807.).

RESULTS

Asphondylia is represented by 58 species in Brazil (21 from the papers retrieved from the Web of Science, 38 from Brazilian gall inventories, 10 exclusively from Gagné & Jaschhof, 2014GAGNÉ, R.J. & JASCHHOF, M. 2014. A Catalog of the Cecidomyiidae (Diptera) of the World. 3.ed. Disponível em: https://www.ars.usda.gov/ARSUserFiles/80420580/Gagne_2014_World_Cecidomyiidae_Catalog_3rd_Edition.pdf.
https://www.ars.usda.gov/ARSUserFiles/80...
, 9 exclusively from the MNRJ, and 47 simultaneously from the MNRJ and literature). The MNRJ comprehended data on 11 determined and 36 undetermined species, all mounted on slide. The later comprised 14 new records. Among them, 20 are known and 38 are still undetermined. The last ones comprise 15 species found in the MNRJ and 23 retrieved from the literature (Maia, 2013aMAIA, V.C. 2013a. Insect galls of São Tomé das Letras (MG, Brazil). Biota Neotropica, 13:164-189.; Maia & Fernandes, 2004MAIA, V.C. & FERNANDES, G.W. 2004. Insect galls from Serra de São José (Tiradentes, Minas Gerais, Brazil). Brazilian Journal Biology, 64:423-445.; Maia & Souza, 2013MAIA, V.C. & SOUZA, M.C. 2013. Insect galls of the xeric vegetation of Ilha do Cabo Frio (Arraial do Cabo, RJ, Brazil). Biota Neotropica, 13:278-288.; Maia et al., 2008aMAIA, V.C.; MAGENTA, M.A.G. & MARTINS, S.E. 2008a. Ocorrência e caracterização de galhas de insetos em áreas de restinga de Bertioga (São Paulo, Brasil). Biota Neotropica, 8:167-197.; Maia et al., 2014MAIA, V.C.; CARDOSO, L.J.T. & BRAGA, J.M.A. 2014. Insect galls from Atlantic Forest areas of Santa Teresa, Espírito Santo, Brazil: characterization and occurrence. Boletim do MBML, 33:47-129.; Mendonça et al., 2014MENDONÇA, M.S.; TOMA, T.S.P. & SILVA, J.S. 2014. Galls and Galling Arthropods of Southern Brazil. In: Fernandes, G.W. & Santos, J.C. (Eds.). Neotropical Insect Galls. New York, Springer. cap. 14, p. 221-256.; Pamplona et al., 2000PAMPLONA, D.M.; MAIA, V.C.; COURI, M.S.; LAMAS, C.J.E. & AIRES, C.C.C. 2000. A survey on Diptera of Paquetá Island, Rio de Janeiro, RJ (Insecta, Diptera). Entomologist’s Monthly Magazine, 136:169-175.; Rodrigues et al., 2014RODRIGUES, 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, 58:173-197.; Urso-Guimarães & Scareli-Santos, 2006URSO-GUIMARÃES, M.V. & SCARELLI-SANTOS, C. 2006. Galls and gall makers in plants fromthe Pé-de-Gigante Cerrado Reserve, Santa Rita do Passa Quatro, SP, Brazil. Brazilian Journal Biology, 66:357-36..) The described species represent 8% of the known species of Asphondylia in the world and 21% of Neotropical species.

Asphondylia is associated with 51 plant species and 20 plant families in Brazil. Asteraceae comprise the greatest richness of Asphondylia species (n = 23). Data on other families are shown in Table 1. Baccharis L. and Mikania Willd. (Asteraceae) were the plant genera that host the greatest number of Asphondylia species, both with five. Mikania glomerata (Asteraceae) was the unique plant species that comprised more than one species of Asphondylia.

TABLE 1:
Distribution of the number of Asphondylia species (Diptera, Cecidomyiidae) per host plant families and species with information on their origin in Brazil. Note: Three botanical names were updated: Vanillosmopsis erythropappa (DC.) Sch. Bip. was replaced by Eremanthus polycephalus (DC.) MacLeish (Asteraceae), and Cordia curassavica Jacq. and Cordia verbenacea DC. were replaced by Varronia curassavica Jacq. (Boraginaceae).

Seventeen species of host plants are endemic in Brazil, thirty four are native, and one is exotic. The endemic plants host Asphondylia maricensisMaia & Couri, 1992MAIA, V.C.; COURI, M.S. & MONTEIRO, R.F. 1992. Sobre seis espécies de Asphondylia Loew, 1850 do Brasil (Diptera, Cecidomyiidae). Revista Brasileira de Entomologia, 36:653-661., A. peploniaeMaia, 2001MAIA, V.C. 2001. The gall midges (Diptera, Cecidomyiidae) from three restingas of Rio de Janeiro State, Brazil. Revista Brasileira de Zoologia, 18:583-629., A. serrataMaia, 2004MAIA, V.C. 2004. Description of a new species of Bruggmannia Tavares (Diptera, Cecidomyiidae) associated with Guapira opposita (Vell.) Reitz (Nyctaginaceae) from Brazil. Revista Brasileira de Zoologia, 21:761-764., and 13 undetermined species. Concerning the conservational status, Baccharis concinna was the single species categorized as a vulnerable, seven were categorized as less concerning (C. serrata, G. polymorpha, M. glomerata, P. cf. cinerea, P. notata, Z. montana, A. fasciculata), and the remaining have not been yet evaluated for threat of extinction. Baccharis concinna host a single species of Asphondylia, whereas the less concerning plants host nine species and the others 48.

The galls of Asphondylia were found on leaves, stems, flower buds, buds, flowers, fruits, inflorescences and simultaneously on leaves/stems. Leaves comprised the greatest richness of Asphondylia species (n = 14) (Table 2). Many gall shapes were found: globose, ovoid, rosette, spherical, elliptic, swollen, cylindrical, conical, drop-shaped, amorphous, aggregate and fusiform (the terminology used by each author was repeated in the present work). The majority of the analyzed morphotypes were glabrous and one-chambered. There was an evident predominance of green (n = 18) galls, the color of the most galled plant organ (leaf). But, yellow, brown, black and cream galls were also found (again, we repeat the color information given by each author) (Table 3).

TABLE 2:
Distribution of the number of Asphondylia species (Diptera, Cecidomyiidae) per plant organs in Brazil.

TABLE 3:
Host plants, gall characterization and geographic distribution of Asphondylia species (Diptera Cecidomyiidae) in Brazil (AF: Atlantic Forest). Note: Three botanical names were updated. Cordia curassavica and Cordia verbenacea were replaced by Varronia curassavica (Boraginaceae) and Vanillosmopsis erythropappa by Eremanthus polycephalus (Asteraceae).

The genus was found in five biomes, Atlantic forest, Cerrado, Caatinga, Pampa, and Amazonian forest (Fig. 1). The gall midges were found mainly in restingas (18 spp.), the most surveyed physiognomy of the Atlantic forest. As the restingas comprise several multivoltine gall midges, specimens are more easily obtained. The Cerrado was second biome in richness of species, followed by Pampa, Caatinga and Amazonian Forest, with 10, 5, 3 and 1 species, respectively.

FIGURE 1:
Distribution of the number of Asphondylia species (Diptera, Cecidomyiidae) per Brazilian biomes.

All species were found in a single biome, excepting Asphondylia moehni Skuhravá, 1989, with occurrence in the Pampa and Atlantic forest. The species were collected in Para (PA), Sergipe (SE), Ceará (CE), Pernambuco (PE), Bahia (BA), Espírito Santo (ES), Minas Gerais (MG), Rio de Janeiro (RJ), São Paulo (SP), and Rio Grande do Sul (RS) (Fig. 2). The majority of the species were found in RJ, SP, MG, and RS, the best surveyed states. The other states have been less surveyed. All species were recorded in a single Brazilian state, with four exception, A. moehni (in RJ, SP and RS), A. glomerata (in RJ and SP) A. cfr. cordiae (in RJ and SP) and Asphondylia sp. (in ES and SP) (Table 3).

FIGURE 2:
Distribution of the number of Asphondylia species (Diptera, Cecidomyiidae) per Brazilian states. Legends: AC: Acre; AM: Amazonas; AP: Amapá; MA: Maranhão; AL: Alagoas; BA: Bahia; CE: Ceará; PB: Paraíba; TO: Tocantins; PA: Pará; RO: Roraima; PE: Pernambuco; PI: Piauí; RN: Rio Grande do Norte; SE: Sergipe; DF: Distrito Federal; GO: Goiás; MT: Mato Grosso; MS: Mato Grosso do Sul; ES: Espirito Santo; MG: Minas Gerais; RJ: Rio de Janeiro; SP: São Paulo; PR: Paraná; SC: Santa Catarina and RS: Rio Grande do Sul.

As the geographical distribution of all host plant species is wider than that of the galler (Table 4), we expect that researches in less sampled states can result in an expansion of the galling species distribution.

TABLE 4:
Species of host plants, their distribution in Brazil and the galling species distribution.

Only five species from Brazil are known in the larval stage, pupa and adult of both sexes (Table 5). Asphondylia ulei, characterized only in the larval stage, is the described species that most lacks morphological information. The number of undescribed species to Brazil indicates that Asphondylia is more diverse than it seems.

TABLE 5:
Brazilian species of Asphondylia (Diptera, Cecidomyiidae) and described life cycle phases. The letter “x” indicates known phase.

The associated arthropod fauna comprises parasitoids and inquilines. The former are represented by three families of Hymenoptera: Eurytomidae, Braconidae and Pteromalidae, and the later by three insects orders: Lepidoptera, Coleoptera and Diptera. The beetles are represented by a single family, Curculionidae, whereas the flies are represented by three, Tephritidae, Sciaridae and Cecidomyiidae (Table 6). The taxonomical knowledge of the associated fauna is superficial, with most records at order or family level and only two in genus level.

TABLE 6:
Asphondylia species (Diptera, Cecidomyiidae) and associated fauna in Brazil.

Nine species of Asphondylia were attacked by Hymenoptera, the most important natural enemy of these midges in the world (Gagné, 1994GAGNÉ, R.J. 1994. The Gall Midges of the Neotropical Region. Ithaca, Cornell University Press. 352p.). In Brazil, Eurytomidae and Pteromalidae are very frequent parasitoids in Cecidomyiidae galls; while Braconidae are less common (Maia & Azevedo, 2009MAIA, V.C. & AZEVEDO, M.A.P. 2009. Micro-himenópteros associados com galhas de Cecidomyiidae (Diptera) em Restingas do Estado do Rio de Janeiro (Brasil). Biota Neotropica, 9:151-164.). Five species of Asphondylia induce galls which are invaded by inquilines. Lepidoptera, Curculionidae, Tephritidae, Sciaridae, and Cecidomyiidae are frequent inquilines of Cecidomyiidae galls in Brazil.

DISCUSSION

This genus is one of the most frequent in Brazil, represented by 20 described species (Carneiro et al., 2009aCARNEIRO, M.A.A.; BRANCO, C.S.A.; BRAGA, C.E.D.; ALMADA, E.D.; COSTA, M.B.M.; MAIA, V.C. & FERNANDES, G.W. 2009a. Are gall midge species (Diptera, Cecidomyiidae) host plant-specialists? Revista Brasileira de Entomologia, 53:365-378.). All determined species reported in the present study were cited by Carneiro et al., (2009a)CARNEIRO, M.A.A.; BRANCO, C.S.A.; BRAGA, C.E.D.; ALMADA, E.D.; COSTA, M.B.M.; MAIA, V.C. & FERNANDES, G.W. 2009a. Are gall midge species (Diptera, Cecidomyiidae) host plant-specialists? Revista Brasileira de Entomologia, 53:365-378., except Asphondylia gochnatiaeMaia, 2008MAIA, V.C.; SILVEIRA, F.A.O.; OLIVEIRA, L.A. & XAVIER, M.F. 2008b. Asphondylia gochnatiae, a new species of gall midge (Diptera: Cecidomyiidae) associated with Gochnatia polymorpha (Less.) Cabrera (Asteraceae). Zootaxa, 1740:53-58..

According to Maia et al. (2009MAIA, V.C.; SANTOS, J.C. & FERNANDES, G.W. 2009. Asphondylia fructicola, a new species of Cecidomyiidae (Diptera) associated with Solanum sp. (Solanaceae) from Brazil. Revista Brasileira de Entomologia, 53:166-170.), Asphondylia is associated with 66 plant families in the world, being more frequent on Asteraceae, Fabaceae and Chenopodiaceae. In the present study, Asteraceae are also pointed out as an important host plant family, but this is not the case of Fabaceae and Chenopodiaceae. Another difference is the indication of Rubiaceae as an important host family.

Eighteen Asphondylia species are associated with these endemic hosts. Among them, three are identified at species level, Asphondylia maricensis, A. peploniae and A. serrata. As they induce gall exclusively on endemic plants, they are proposed here as endemic too. The other 15 species, although still undetermined, probably are endemic based on the high specificity between the gallers and the host plants, but more comparative morphological studies among them are necessary before proposing it. Unfortunately, the available material is not enough, as the species are represented by different life cycle stages.

Baccharis concinna was categorized as a vulnerable species, so the undetermined galler which is associated with this host can be also vulnerable, if it occurs exclusively on it. It is important to highlight this situation, where a probably new species can be considered vulnerable. So, it can become extinct before being formally described, implying silent extinction.

The highest incidence of galling species on leaves confirmed the global pattern pointed out by Felt (1940FELT, E.P. 1940. Plant Galls and Gall Makers. Ithaca, N.Y., Constable and Co. 364p.), probably because the leaves represent an abundant and frequent resource (Maia et al., 2008aMAIA, V.C.; MAGENTA, M.A.G. & MARTINS, S.E. 2008a. Ocorrência e caracterização de galhas de insetos em áreas de restinga de Bertioga (São Paulo, Brasil). Biota Neotropica, 8:167-197.).

The highest number of species (39 spp.) was recorded in the Atlantic forest, what corresponds to about 67% of the total, but this result does not necessarily indicate that the Atlantic forest comprises the greatest richness of Asphondylia species, as the highest number of inventories developed by taxonomists was carried out in this biome. In addition to that, there are more available specimens of the Atlantic forest for identification.

In spite of being one of the most surveyed biomes, the Cerrado comprises only 10 Asphondylia species. This can be explained by the low number of available specimens for identification. Differing from the multivoltine species of the restingas, the gall midges of the Cerrado are generally univoltine, with longer life cycles and consequently lower success of rearing. The other biomes have been little studied.

Considering all species (58 spp.), the genus in Brazil is quite representative of the Neotropical fauna, although the morphological knowledge of many species is partial due to the lack of knowledge of the life cycle phases or both sexes. The species described in the larval stage, pupal and adult male and female correspond to the more recently described, and indicate the current tendency to describe a new taxon only when all stages are shown (except egg, which contributes little to the taxonomy).

The records of inquilines exemplify some ecological interactions between Asphondylia species and other insects and suggest the role of these gall midges as ecosystem engineers. The importance of the parasitoid wasps as natural enemies of the cecidomyiids are confirmed. These can be evaluated as more data on the associated fauna are known.

CONCLUSIONS

The taxonomical knowledge of the Brazilian species of Asphondylia is still incipient. Asphondylia maricensis, A. peploniae and A. serrata are endemic based on their occurrence exclusively on endemic host plants. Asteraceae is confirmed as the botanical family which hosts the greatest richness of Asphondylia species. The geographic distribution of the Brazilian Asphondylia species is poorly known. The genus exhibits genetic plasticity to different environmental conditions, as it has been recorded in five Brazilian biomes. The associated fauna is little studied.

ACKNOWLEDGMENTS

We thank the anonymous reviewers for suggestions on earlier versions of the manuscript.

REFERENCES

  • ALMADA, E.D. & FERNANDES, G.W. 2011. Insetos indutores de galhas em florestas de terra firme e em reflorestamentos com espécies nativas na Amazônia Oriental, Pará. Brasil. Boletim Museu Paraense Emilio Goeldi, 6:163-196.
  • ARAÚJO, W.S.; SANTOS, B.B. & GOMES-KLEIN, V.L. 2011. Insect galls from Serra dos Pireneus, GO, Brazil. Biota Neotropica, 11:357-365.
  • ARAÚJO, W.S.; SOBRAL, F.L. & MARACAHIPES, L. 2014. Insect galls of the Parque Nacional das Emas (Mineiros, GO, Brazil). Check List, 10:1445-1451.
  • BREGONCI, J.M.; POLYCARPO, P.V. & MAIA, V.C. 2010. Galhas de insetos do Parque Estadual Paulo César Vinha (Guarapari, ES, Brasil). Biota Neotropica, 10:227-238.
  • CARNEIRO, M.A.A.; BRANCO, C.S.A.; BRAGA, C.E.D.; ALMADA, E.D.; COSTA, M.B.M.; MAIA, V.C. & FERNANDES, G.W. 2009a. Are gall midge species (Diptera, Cecidomyiidae) host plant-specialists? Revista Brasileira de Entomologia, 53:365-378.
  • CARNEIRO, M.A.A.; BORGES, R.A.X.; ARAÚJO, A.P.A.; FERNANDES, G.W. 2009b. Insetos indutores de galhas da porção sul da Cadeia do Espinhaço, MG, Brasil. Revista Brasileira de Entomologia, 53:570-592.
  • COELHO, M.S.; ALMADA, E.D.; FERNANDES, G.W.; CARNEIRO, M.A.A.; SANTOS, R.M.; SANCHEZ-AZOFEIFA, A. 2009. Gall inducing arthropods from a seasonally dry tropical Forestin Serra do Cipó, Brazil. Revista Brasileira de Entomologia, 53:404-414.
  • COELHO, M.S.; CARNEIRO, M.A.; BRANCO, C.; BORGES, R.A.X. & FERNANDES, G.W. 2013a. Gall-inducing insects from Campos de Altitude, Brazil. Biota Neotropica, 4:139-151.
  • COELHO, M.S.; CARNEIRO, M.A.; BRANCO, C.; BORGES, R.A.X. & FERNANDES, G.W. 2013b. Gall-inducing insects from Serra do Cabral, Minas Gerais, Brazil. Biota Neotropica, 3:102-109.
  • COSTA, E.C.; CARVALHO-FERNANDES, S.P. & SANTOS-SILVA, J. 2014. Galhas de insetos de uma área de transição caatinga-cerrado no Nordeste do Brasil. Sitientibus, Série Ciências Biológicas, 14:1-9.
  • DORCHIN, N.; JOY, B.J.; HILKE, L.K.; WISE, M.J. & ABRAHAMSON, W.G. 2015. Taxonomy and phylogeny of the Asphondylia species (Diptera: Cecidomyiidae) of North American goldenrods: challenging morphology, complex host associations, and cryptic speciation. Zoological Journal of the Linnean Society, 174:265-304.
  • DREGER-JAUFFRET, F. & SHORTHOUSE, J.D. 1992. Diversity of gall-inducing insects and their galls. In: Shorthouse, J.D. & Rohfritsch, O. (Eds.). Biology of Insect-Induced Galls. Oxford, Oxford University Press. p. 8-33.
  • FELT, E.P. 1940. Plant Galls and Gall Makers. Ithaca, N.Y., Constable and Co. 364p.
  • FERNANDES, G.W. & NEGREIROS, D. 2006. A comunidade de insetos galhadores da RPPN Fazenda Bulcão, Aimorés, Minas Gerais, Brasil. Lundiana, 7:111-120.
  • FERNANDES, G.W.; ARAÚJO, R.C.; ARAÚJO, S.C.; LOMBARDI, J.A.; PAULA, A.S.; LOYOLLA JR., R.R. & CORNELISSEN, T.G. 1997. Insect galls from savanna and rocky fields of the Jequitinhonha Valley, Minas Gerais, Brazil. Naturalia, 22:221-224.
  • FERNANDES, G.W.; JULIÃO, G.R.; ARAÚJO, R.C.; ARAÚJO, S.C.; LOMBARDI, J.A.; NEGREIROS, D. & VARNEIRO, M.A.A. 2001. Distribution and morphology of insect galls of the Rio Doce Valley, Brazil. Naturalia, 26:221-244.
  • FERNANDES, G.W.; TAMEIRÃO-NETO, E. & MARTINS, R.P. 1988. Ocorrência e caracterização de galhas entomógenas na vegetação do campus Pampulha da Universidade Federal de Minas Gerais. Revista Brasileira de Zoologia, 5:11-29.
  • FLORA DO BRASIL. 2002. Jardim Botânico do Rio de Janeiro. [under construction]. Available on: Available on: http://floradobrasil.jbrj.gov.br Access on: 24/02/2017.
    » http://floradobrasil.jbrj.gov.br
  • GAGNÉ, R.J. 1989. The plant-feeding midges of North America. Ithaca, Comstock. xi + 368p.
  • GAGNÉ, R.J. 1994. The Gall Midges of the Neotropical Region. Ithaca, Cornell University Press. 352p.
  • GAGNÉ, R.J. 2004. A catalog of the Cecidomyiidae (Diptera) of the world. Memoirs of the Entomological Society of Washington, 25:1-408.
  • GAGNÉ, R.J. 2007. Species numbers of Cecidomyiidae (Diptera) by zoogeographical Region. Proceedings of the Entomological Society of Washington, 109, 499-499.
  • GAGNÉ, R.J. & JASCHHOF, M. 2014. A Catalog of the Cecidomyiidae (Diptera) of the World. 3.ed. Disponível em: https://www.ars.usda.gov/ARSUserFiles/80420580/Gagne_2014_World_Cecidomyiidae_Catalog_3rd_Edition.pdf
    » https://www.ars.usda.gov/ARSUserFiles/80420580/Gagne_2014_World_Cecidomyiidae_Catalog_3rd_Edition.pdf
  • GAGNÉ, R.J.; ODA, R.A. & MONTEIRO, R.F. 2001. The gall midges (Diptera: Cecidomyiidae) of Mikania glomerata (Asteraceae) in southeastern Brazil. Proceedings of the Entomological Society of Washington, 103:110-134.
  • GONÇALVES-ALVIM, S.J. & FERNANDES, G.W. 2001. Comunidades de insetos galhadores (Insecta) em diferentes fisionomias do cerrado em Minas Gerais, Brasil. Revista Brasileira de Zoologia, 18:289-305.
  • HOUARD, C. 1933. Les Zoocécidies des Plantes de l’Amérique du Sud e de l’Amérique Central. Paris, Hermann et Cie. 519p.
  • JULIÃO, G.R.; AMARAL, M.E.C. & FERNANDES, G.W. 2002. Galhas de insetos de suas plantas hospedeiras do Pantanal sul-mato-grossense. Naturalia, 27:47-74.
  • MAIA, V.C. 2001. The gall midges (Diptera, Cecidomyiidae) from three restingas of Rio de Janeiro State, Brazil. Revista Brasileira de Zoologia, 18:583-629.
  • MAIA, V.C. 2004. Description of a new species of Bruggmannia Tavares (Diptera, Cecidomyiidae) associated with Guapira opposita (Vell.) Reitz (Nyctaginaceae) from Brazil. Revista Brasileira de Zoologia, 21:761-764.
  • MAIA, V.C. 2011. Characterization of insect galls, gall makers, and associated fauna of Platô Bacaba (Porto de Trombetas, Pará, Brazil). Biota Neotropica, 11:37-53.
  • MAIA, V.C. 2013a. Insect galls of São Tomé das Letras (MG, Brazil). Biota Neotropica, 13:164-189.
  • MAIA, V.C. 2013b. Galhas de insetos em restingas da região sudeste do Brasil com novos registros. Biota Neotropica, 13:183-209.
  • MAIA, V.C. 2014. Insect galls of Itamonte (Minas Gerais, Brazil): characterization and occurrence. Biota Neotropica, 14:1-17.
  • MAIA, V.C. & AZEVEDO, M.A.P. 2009. Micro-himenópteros associados com galhas de Cecidomyiidae (Diptera) em Restingas do Estado do Rio de Janeiro (Brasil). Biota Neotropica, 9:151-164.
  • 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.
  • 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 Asphondylinii (Diptera: Cecidomyiidae) associated with Bahuinia brevipes (Fabaceae) in Brazil. Zootaxa, 1091:27-40.
  • MAIA, V.C. & OLIVEIRA, J.C. 2010. Galhas de insetos da Reserva Biológica Estadual da Praia do Sul (Ilha Grande, Angra dos Reis, RJ). Biota Neotropica, 10:227-238.
  • MAIA, V.C. & SILVA, M.C. 2013. The genus Dasineura Rondani, 1840 (Diptera, Cecidomyiidae). Brazilian Journal Biology, 73:801-807.
  • MAIA, V.C. & SOUZA, M.C. 2013. Insect galls of the xeric vegetation of Ilha do Cabo Frio (Arraial do Cabo, RJ, Brazil). Biota Neotropica, 13:278-288.
  • MAIA, V.C.; CARDOSO, L.J.T. & BRAGA, J.M.A. 2014. Insect galls from Atlantic Forest areas of Santa Teresa, Espírito Santo, Brazil: characterization and occurrence. Boletim do MBML, 33:47-129.
  • MAIA, V.C.; COURI, M.S. & MONTEIRO, R.F. 1992. Sobre seis espécies de Asphondylia Loew, 1850 do Brasil (Diptera, Cecidomyiidae). Revista Brasileira de Entomologia, 36:653-661.
  • MAIA, V.C.; MAGENTA, M.A.G. & MARTINS, S.E. 2008a. Ocorrência e caracterização de galhas de insetos em áreas de restinga de Bertioga (São Paulo, Brasil). Biota Neotropica, 8:167-197.
  • MAIA, V.C.; SILVEIRA, F.A.O.; OLIVEIRA, L.A. & XAVIER, M.F. 2008b. Asphondylia gochnatiae, a new species of gall midge (Diptera: Cecidomyiidae) associated with Gochnatia polymorpha (Less.) Cabrera (Asteraceae). Zootaxa, 1740:53-58.
  • MAIA, V.C.; SANTOS, J.C. & FERNANDES, G.W. 2009. Asphondylia fructicola, a new species of Cecidomyiidae (Diptera) associated with Solanum sp. (Solanaceae) from Brazil. Revista Brasileira de Entomologia, 53:166-170.
  • MENDONÇA, M.S.; TOMA, T.S.P. & SILVA, J.S. 2014. Galls and Galling Arthropods of Southern Brazil. In: Fernandes, G.W. & Santos, J.C. (Eds.). Neotropical Insect Galls. New York, Springer. cap. 14, p. 221-256.
  • OLIVEIRA, J.C. & MAIA, V.C. 2005. Ocorrência e caracterização de galhas de insetos na restinga de Grumari (Rio de Janeiro, RJ, Brasil). Arquivo do Museu Nacional, 63:669-676.
  • PAMPLONA, D.M.; MAIA, V.C.; COURI, M.S.; LAMAS, C.J.E. & AIRES, C.C.C. 2000. A survey on Diptera of Paquetá Island, Rio de Janeiro, RJ (Insecta, Diptera). Entomologist’s Monthly Magazine, 136:169-175.
  • 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, 58:173-197.
  • RÜBSAAMEN, E.H. 1907. Beiträge zur Kenntnis aussereuropäischer Zoocecidien. III. Beitrag [cont.]: Gallen aus Brasilien und Peru. Marcellia, 6:110-173.
  • RÜBSAAMEN, E.H. 1916. Beitrag zur Kentnis aussereuropäischer Gallmücken. Sitzungsberichte der Gesellschaft Naturforschender Freunde zu Berlin, 1915:431-481.
  • SAITO, V.S. & URSO-GUIMARÃES, M.V. 2012. Characterization of galls, insect galls and associated fauna of Ecological Station of Jataí (Luiz Antônio, SP). Biota Neotropica, 12:99-107.
  • SANTOS, B.B.; FERREIRA, H.D. & ARAÚJO, W.S. 2010. Ocorrência e caracterização de galhas entomógenas em uma área de floresta estacional semidecídua em Goiânia, Goiás, Brasil. Acta Botanica Brasilica, 24:243-249.
  • SANTOS, J.C.; ALMEIDA-CORTEZ, J.S. & FERNANDES, G.W. 2011a. Diversity of gall-inducing insects in the high altitude wetland forests in Pernambuco, Northeastern, Brazil. Brazilian Journal of Biology, 71:47-56.
  • SANTOS, J.C.; ALMEIDA-CORTEZ, J.S. & FERNANDES, G.W. 2011b. Richness of gall-inducing insects in the tropical dry forest (caatinga) of Pernambuco. Revista Brasileira de Entomologia, 55:45-54.
  • TAVARES, J.S. 1909. Contributio prima ad cognitionem cecidologiae braziliae. Brotéria: Série Zoológica, 8:5-28.
  • TAVARES, J.S. 1916. Cecidomyias novas do Brazil. Brotéria, 14:36-57.
  • TAVARES, J.S. 1917. Cecidias brazileiras que se criam em plantas das Compositae, Rubiaceae, Tiliaceae, Lythraceae e Artocarpaceae. Brotéria: Série Zoológica, 15:113-181.
  • TAVARES, J.S. 1918. Cecidologia brazileira. Cecídias que se criam em plantas das famílias das Verbenaceae, Euphorbiaceae, Malvaceae, Anacardiaceae, Labiatae, Rosaceae, Anonaceae, Ampleidaceae, Bignoniaceae, Aristochiaceae e Solanaceae. Brotéria: Série Zoológica, 16:21-68.
  • TOMA, T.S.P. & MAIA, V.C. 2012. Representatividade do gênero Clinodiplosis Kieffer (Diptera, Cecidomyiidae) no Brasil. Papéis Avulsos de Zoologia, 52:223-231.
  • TOMA, T.S.P. & MENDONÇA, M.S. 2013. Gall-inducing insects of an Araucaria Forest in southern Brazil. Revista Brasileira de Entomologia, 57:225-233.
  • URSO-GUIMARÃES, M.V. & AMORIM, D.S. 2002. New Brazilian species of Asphondyliini (Diptera, Cecidomyiidae). Revista Brasileira de Entomologia, 46:561-570.
  • URSO-GUIMARÃES, M.V. & SCARELLI-SANTOS, C. 2006. Galls and gall makers in plants fromthe Pé-de-Gigante Cerrado Reserve, Santa Rita do Passa Quatro, SP, Brazil. Brazilian Journal Biology, 66:357-36.
  • URSO-GUIMARÃES, M.V.; SCARELLI-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, 63:705-715.
  • 1
    Editor Responsável: Carlos José Einicker Lamas
  • Publicado com o apoio financeiro do Programa de Apoio às Publicações Científicas Periódicas da USP
  • 3
    Os periódicos Papéis Avulsos de Zoologia e Arquivos de Zoologia estão licenciados sob uma Licença CC-BY da Creative Commons.

Publication Dates

  • Publication in this collection
    2017

History

  • Received
    29 June 2017
  • Accepted
    15 Sept 2017
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