i
LAURA JANE GISLOTI
O gênero Neosilba McAlpine (Tephritoidea: Lonchaeidae): revisão,
ocorrência e diversidade
Campinas
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RESUMO
As moscas da família Lonchaeidae (Diptera), juntamente com as da família Tephritidae formam um grupo conhecido como moscas-das-frutas, já que suas larvas utilizam como recurso alimentar frutos de interesse comercial. Espécies de Tephritidae são comumente relatadas como pragas importantes para a fruticultura e têm sua biologia e ecologia profundamente estudadas. Já as espécies de Lonchaeidae, mesmo estando associadas a diversos frutos de interesse agrícola, são pouco estudadas. Isto pode estar relacionado ao fato de que não há estudos distinguindo taxonomicamente esse grupo no nível de gênero e espécies. Paralelamente, esta inconsistência taxonômica dificulta e desencoraja estudos com o grupo, fazendo com que a história natural dessas moscas permaneça desconhecida. Em Neosilba, o gênero de Lonchaeidae alvo deste estudo, a taxonomia tradicional é baseada unicamente na análise da morfologia genital masculina e assim todos os trabalhos a respeito deste grupo excluem grande parte do material obtido: as fêmeas. Alguns estudos já foram desenvolvidos no intuito de facilitar a identificação destas moscas, envolvendo técnicas eletroforéticas de sistemas enzimáticos e análises empregando métodos morfométricos. Porém nenhuma técnica se mostrou específica o bastante para distinguir as espécies neste gênero.
Dentro desse contexto, a tese foi estruturada em três capítulos. No capítulo 1 fazemos uma revisão da biologia, ecologia e taxonomia da família Lonchaeidae. Dentro desse capítulo disponibilizamos um mapa da distribuição mundial dos oito gêneros, além de uma chave taxonômica dicotômica ilustrada, adaptada de McAlpine, para todos os gêneros de Lonchaeidae. No capítulo 2 realizamos uma revisão centrada em diversidade, distribuição e plantas hospedeiras de moscas do gênero Neotropical Neosilba. Listamos a
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distribuição e as plantas hospedeiras das 40 espécies de Neosilba. Por fim, no capítulo 3 estudamos a diversidade de espécies frugívoras do gênero Neosilba em 35 espécies de frutíferas cultivadas, de duas localidades do estado de São Paulo e concluímos que Neosilba
zadolicha é a espécie que apresenta o maior número de plantas hospedeiras e é a mais
abundante entre as sete espécies de Neosilba encontradas. Este trabalho acrescenta informações inéditas ao gênero Neosilba e a compilação de dados a respeito deste grupo pretende estimular o ingresso de novos pesquisadores a fim de preencher as lacunas existentes no âmbito da taxonomia, sistemática, biologia e ecologia desse táxon.
PALAVRAS-CHAVE: Acalyptratae, Diptera, moscas frugívoras, lonchaeids, taxonomia alfa.
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ABSTRACT
The flies of the Lonchaeidae family, alongside with the Tephritidae, form a group known as fruit-flies, since their larvae feed on fruits of huge economical interest in their diet. Species of Tephritidae are generally reported as important pests to the horticulture, with their biology and ecology deeply studied in detail.
However the Lonchaeidae species, despite being associated to many fruits of agricultural interest, are not as studied. This can be related to the fact that there aren’t many studies distinguishing taxonomically this group at the genus or species level. In parallel, this taxonomic inconsistency complicates and discourages studies of the group, keeping the natural history of those flies unknown. In Neosilba, the traditional taxonomy is based only on the analysis of the male genitalia morphology, and so, this method excludes great part of the material collected: the females. Some studies were done on the purpose of facilitating the identification of these flies, involving electrophoresis techniques of enzymatic systems and analysis employing morph metric methods. However, no technique demonstrated to be specific enough to distinguish the species of this genus.
Inside this context, this work was structured in four chapters. In chapter 1 a revision of the biology, ecology, and taxonomy of the Lonchaeidae family is made. Inside this chapter, we make available a map containing the global distribution of all genus, in addition to an illustrated dichotomic taxonomic key, adapted from McAlpine, to all Lonchaeidae genus. In chapter 2 we realize a revision centered in the diversity, distribution and hosting plants of the Neotropical genus Neosilba. We listed a distribution of hosting plants of 40
Neosilba species. In chapter 3, we study the diversity of frugivorous species in the Neosilba
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conclude that Neosilba zadolicha is the species that contains the biggest number of hosting plants, and is also the most abundant compared to the 7 species of Neosilba that were found.
This work adds unpublished information of the Neosilba genus and the compilation of data concerning this group aims to stimulate the entrance of new researchers for the purpose of fill the existing lacunae in the scope of taxonomy, systematics, biology, and ecology of this taxon.
xi SUMÁRIO RESUMO...vii ABSTRACT...ix LISTA DE ILUSTRAÇÕES...xv LISTA DE TABELAS...xvii INTRODUÇÃO GERAL...01 REFERÊNCIAS...04
CAPÍTULO 1. REVIEW OF THE TAXONOMY AND BIOLOGY OF LONCHAEIDAE (DIPTERA), FRUIT FLIES OF ECONOMIC IMPORTANCE IN THE NEOTROPICAL REGION Abstract...9 Introduction...10 Methodology………..………...12 Results………...13 Discussion...27 References...44
CAPÍTULO 2 ESPÉCIES DE Neosilba (DIPTERA, LONCHAEIDAE, LONCHAEINAE): DISTRIBUIÇÃO GEOGRÁFICA E PLANTAS HOSPEDEIRAS Resumo...67
Introdução...68
Material e Métodos ………..…...…………...……...70
Resultados e Discussão …………...71
Referências...95
CAPÍTULO 3. Neosilba McAlpine (Diptera, Lonchaeidae) Diversity on Cultivated Host Plants from Brazilian Cerrado and Atlantic Tropical Forest Biomes Abstract...107
Introduction...108
Material and Methods………..……….…………...109
Results and Discussion………...111
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Agradecimentos
"Aqueles que passam por nós, não vão sós, não nos deixam sós. Deixam um pouco de si, levam um pouco de nós (Antoine de Saint-Exupéry).
Estes 4 anos de pesquisa foram uma árdua jornada de desafio, construção e amadurecimento. De fato, nenhum empreendimento é realizado de forma fácil e sem esforço.
José Saramago discorreu sobre a importância da jornada rumo à vitória: "Nem as
derrotas nem as vitórias são definitivas. Isso dá uma esperança aos derrotados, e deveria dar uma lição de humildade aos vitoriosos.”
Assim, neste período aprendi que uma tese ou qualquer outro trabalho é uma extensão da vida do autor. Então, para que algo de valor seja produzido, o indivíduo deve primeiramente criar algo de valor em si. Indivíduo e obra são consistentes com o resultado. Por estes motivos, agradeço sincera e profundamente todas as pessoas que me ajudaram e me incentivaram a produzir algo de valor em minha vida.
Primeiramente agradeço ao meu grande mestre, Prof. Dr. Angelo Pires do Prado. É uma grande honra tê-lo tido como orientador por 6 anos (desde o mestrado). Jamais me esquecerei de seus ensinamentos, de seus preciosos conselhos e de sua inestimável confiança. Muito Obrigado, Angelo!
Agradeço também a minha orientadora adotiva, Profa. Dra. Silmara Marques Allegretti. O seu apoio e a sua confiança no momento mais difícil desta jornada foram essenciais para que fosse possível finalizar essa etapa.
Manifesto aqui a minha gratidão a todos os professores, funcionários e amigos do Departamento de Biologia Animal do Instituto de Biologia da Unicamp, em particular à Profa. Dra. Marlene Tiduko Ueta, à Carina Mara de Souza, à Rodrigo Labello Barbosa e à David Villas Boas Filho. Foram momentos bastante agradáveis e produtivos ao lado de vocês.
Meus respeitosos agradecimentos pela contribuição da banca do Exame de Qualificação e pela participação dos membros da Banca Examinadora da Defesa.
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Meu muito obrigado à meus queridos companheiros que me encorajam em todos os aspectos da minha vida: minhas amigas Patrícia Silvana Barros, Laila Silva Leonel De Ávila Stoppa, Manuela Scarpa Silverio Pinto e meu companheiro Breno Gomes Machado da Silva.
Por fim, agradeço em especial àqueles que sempre me apoiaram incondicionalmente, que apostaram em mim mais do que ninguém e que seguramente são os que mais compartilham da minha alegria: minha mãe Lucia Helena Gisloti e meu filho Lucas Gisloti Martins. Mais uma etapa vencida! Sei que ainda é só o começo.
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LISTA DE ILUSTRAÇÕES Capítulo 1
Figure 1. Geographical distribution of the Lonchaeidae (Diptera: Tephritoidea) species
around the world...29
Figure 2. Distribution of publications about the Lonchaeidae genera (Diptera: Tephritoidea), since 1878 until December 2013 (n = 201) [*other = Papers about Lonchaeidae without specified genus]………..……...………...………..…31
Figure 3. Stigmatal bristles (in red) present on the sclerite above the anterior thoracic spiracles………..…………..……….36
Figure 4. Lunule bare (see arrow in red)………..………….………36
Figure 5. Lunule setulose (in red)………...………..37
Figure 6. Scutellum with four bristles on the edge (in red)………..……..……..37
Figure 7. Scutellum with more them four bristles on the edge (in red)…...…...…...….38
Figure 8. Setae of the frons spaced and short (see arrow in red)………...…….…..38
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Figure 10. Scutellum with setae anterior to the marginal bristles (in red)………39
Figure 11. Cheek and parafacial wide (in red)………. ………..…………..40
Figure 12. Scutellum bare in relation to the marginal bristles (see arrow in red)……..…...40
Figure 13. Cheek and parafacial narrowed (in red)………..………. …………...41
Figure 14. Arista plumose (in red)………...…………...41
Figure 15. Surstylus with prensisetae (in red)………... ………...42
Figure 16. Arista bare (in red)………. ………...42
Figure 17. Surstylus without prensisetae (see arrow in red)………...…………..43
Figure 18. Fringes of calypteres with a cluster of long blackish setae at fold (in red)…….43
Figure 19. Fringes of calypteres without cluster of long blackish setae at fold (see arrow in red)………...……….…44
Capítulo 2 Figure 1. Distribuição geográfica das espécies de Neosilba McAlpine na Região Neotropical...74
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LISTA DE TABELAS Capítulo 2
Tabela 1. Táxons de plantas hospedeiras de espécies de Neosilba (Diptera: Lonchaeidae) no mundo...75
Capítulo 3
Table 1. Indices of infestation and viability of pupae of Neosilba species in 35 cultivated hosts from Cerrado and Tropical Forest of Brazil (January/2010 to March/2012)………..………..………124
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INTRODUÇÃO GERAL
A família Lonchaeidae está classificada dentro da superfamília Tephritoidea, a qual apresenta características notórias como a exibição de padrão de corte em vôo, presença de asas geralmente sem pigmentação ou pigmentação difusa, além de halteres e corpo de coloração preta, sendo comum reflexos metálicos azuis, bronze ou verde no corpo. É composta pelas subfamílias Lonchaeinae e Dasiopinae, as quais apresentam ampla distribuição geográfica, sendo que na região neotropical são conhecidos representantes de ambas as subfamílias (McAlpine 1987).
No Brasil, os lonqueídeos estão representados principalmente pelo gênero Neosilba McAlpine 1962, mas, são encontradas espécies do gênero Lonchaea Fallén 1820 e Dasiops Rondani 1856 (McAlpine & Steyskal 1982, Strikis & Prado 2005).
As larvas de Neosilba são saprófagas, fitófagas ou predadoras e assim estão associadas a frutos, sementes, brotos e flores. Tais órgãos ou tecidos são danificados pela nutrição das larvas nesses substratos (McAlpine 1961, Fehn 1981).
Apesar de a literatura brasileira ter relatado a presença de Neosilba infestando frutos de importância econômica desde a década de 30, por um longo período, os lonqueídeos foram negligenciados e muitas vezes descartados nos levantamentos de moscas frugívoras, pela falta de conhecimento taxonômico e, principalmente, por não serem considerados de notável importância econômica. A partir da década de 70, foi crescente o interesse em estudar a família Lonchaeidae, principalmente espécies do gênero Neosilba, porque passou a ser comum o aparecimento de espécimes em frutos de importância comercial (Gatelli et
2
Já na década posterior os estudos passaram a incluir as espécies desta família e devido a isto foram alistadas dezenas de espécies de frutos hospedeiros, em diversos estados brasileiros (Malavasi et al. 1980, Malavasi & Morgante 1980).
Posteriormente, na década de 90, o interesse em estudar Neosilba foi favorecido em razão da quantidade de pupários de lonqueídeos obtidos em inventários entomofaunísticos e em outros estudos. Assim, Silva (1993), constatou a presença de espécies de Neosilba associadas a 19 espécies de frutos, em quatro locais do Estado do Amazonas.
Nos anos seguintes, Raga et al. (1996, 1997), em um estudo de observação da incidência de moscas das frutas (Tephritidae) em frutos de café Coffea spp. e laranja Citrus
sinensis, no estado de São Paulo, relataram que 17 e 4,9% dos exemplares coletados,
respectivamente, pertenciam à família Lonchaeidae. Também no Estado de São Paulo, Souza Filho (1999) constatou Neosilba associada a 40 espécies de frutos. No estado de Mato Grosso do Sul, estas moscas foram associadas a 22 espécies de frutos (Uchôa et al. 2002). De fato, este gênero havia despertado interesse, principalmente nos pesquisadores de mosca das frutas, e isto possibilitou um aumento considerável de publicações que envolviam Lonchaeidae.
Assim as larvas de Neosilba foram registradas como tendo hospedeiros frutos de acerola, goiaba, tangerina (Araújo & Zucchi 2002), manga, mamão, sete-copas, abacate, carambola, laranja, maracujá (Uchôa et al. 2002); café ( Souza et al. 2005, Aguiar-Menezes et al. 2007); nêspera (Strikis & Prado 2009); pêssego (Striks & Prado 2005), entre diversos outros frutos, confirmando assim a importância desta família para a fruticultura tropical.
Além de frutos, imaturos destes insetos já foram notificados como tendo hospedeiros botões florais de Passiflora spp. (Norrbom & McAlpine 1997, Uchôa &
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Zucchi 1999, Causton & Peña Rangel 2002, Uchôa et al. 2002), Ipomoea spp. (Santos et al. 1992) e Manihot esculenta Crantz (Del Vecchio 1991).
Por outro lado, diversos estudos ilustram a dificuldade em distinguir as espécies das moscas deste gênero, de forma que um número elevado de trabalhos apresentam a ocorrência de espécies não identificadas de Neosilba (Malavasi & Morgante 1980, Raga et al. 2002, Uchôa et al. 2002, Souza et al. 2005, Bittencourt et al. 2006, Minzão & Uchôa 2008, Caires et al. 2009).
De fato, as espécies de Neosilba são estreitamente relacionadas e as divergências morfológicas entre os indivíduos não são detectáveis em uma análise de simples observação. Assim, a taxonomia se mostra bastante complicada para este grupo, o que dificulta os trabalhos com estes Diptera. Adicionalmente, já foi constatado um grande complexo de espécies crípticas neste gênero, o que dificulta ainda mais a identificação de suas espécies, que é baseada integralmente na análise das estruturas da genitália masculina dessas moscas (McAlpine & Steyskal 1982, De Conti 1984). Outrora, este método de identificação requeria bastante treinamento, o que muitas vezes acabava por desestimular os trabalhos com este grupo, prejudicando ainda mais a taxonomia.
As fêmeas de Neosilba são excluídas nos trabalhos, devido à ausência de ferramentas que possibilitem a sua identificação, que ainda é dificultada pelo fato de que inúmeras espécies não possuem hospedeiros específicos, e um único fruto pode apresentar diferentes espécies e até distintos gêneros de Lonchaeidae. Assim, todos os trabalhos a respeito deste gênero excluem grande parte do material obtido, e isto que pode gerar inconsistência nos dados, principalmente se o trabalho for ao âmbito de biodiversidade Neotropical ou inventários de hospedeiros.
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Alguns estudos já foram desenvolvidos no intuito de facilitar a identificação destas moscas, alguns dos quais envolveram técnicas eletroforéticas de sistemas enzimáticos (De Conti et al. 1984) e análises empregando métodos morfométricos (Oliveira 1992, Freitas 2008), porém nenhuma técnica se mostrou específica o bastante para distinguir espécies de
Neosilba.
Assim, no capítulo 1 revisamos aspectos biológicos, ecológicos e taxonômicos da família Lonchaeidae. No capítulo 2 demos ênfase através de uma revisão centrada em diversidade, distribuição e hospedeiros de moscas do gênero Neotropical Neosilba. E por fim, no capítulo 3 estudamos a diversidade de espécies frugívoras do gênero Neosilba em 35 espécies de frutíferas cultivadas, de duas localidades do estado de São Paulo.
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ARAUJO, E. L.; ZUCCHI, R. A. Hospedeiros e níveis de infestação de Neosilba pendula (Bezzi) (Diptera: Lonchaeidae) na região de Mossoró/Assu, RN. Arquivos do Instituto Biológico, v. 69, p. 91-94, 2002.
BITTENCOURT, M. A. L.; SILVA, A. C. M.; BOMFIM, Z. V.; SILVA, V. E. S.; ARAÚJO, E. L.; STRIKIS, P. C. Novos registros de espécies de Neosilba (Diptera: Lonchaeidae) na Bahia. Neotropical Entomology, v. 35, p. 282-283, 2006.
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CAIRES, C. S.; UCHOA-FERNANDES, M. A.; NICACIO, J.; STRIKIS, P. C. Frugivoria de larvas de Neosilba McAlpine (Diptera, Lonchaeidae) sobre Psittacanthus
plagiophyllus Eichler (Santalales, Loranthaceae) no sudoeste de Mato Grosso do
Sul, Brasil. Revista Brasileira de Entomologia, v. 53, p. 272-277, 2009.
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DE CONTI, E.; DEL VECCHIO, M. C.; DE SOUZA, H. M. L.; MORGANTE, J. S.; PIEDRABUENA, A. E. Allozimic variability in natural Silba spp. populations (Diptera: Lonchaeidae). Revista Brasileira de Genética, v. 3, p. 419-432, 1984. DEL VECCHIO, M. C. Família Lonchaeidae (Diptera: Acalyptratae): Ocorrência de
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FENH, L. M. Coleta e reconhecimento de moscas das frutas em região metropolitana de Curitiba e Irati, Paraná, Brasil. Anais da Sociedade Entomológica do Brasil, v. 10, p. 209-238, 1981.
FREITAS, K. F. Estudos Morfológicos e ecológicos de espécies de Lonchaeidae (Diptera) em frutos de Rubiaceae, Myrtaceae, Rosaceae e Fabaceae. Instituto de Biologia da Universidade de Campinas. (Dissertação de Mestrado). 2008. 98p.
GATTELLI, T.; SILVA, F. F. DA; MEIRELLES, R. N.; REDAELLI, L. R.; DAL SOGLIO, F. K. Moscas frugívoras associadas a mirtáceas e laranjeira "Céu" na
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MALAVASI, A.; MORGANTE, J. S. Biologia de “moscas-das-frutas” (Diptera, Tephritidae): Índices de infestação em diferentes hospedeiros e localidades. Revista Brasileira de Biologia, v. 40, p.17-24, 1980.
MALAVASI, A.; MORGANTE, J. S.; ZUCCHI, R. A. Biologia de “moscas-das-frutas” (Diptera, Tephritidae): Lista de hospedeiros e ocorrência. Revista Brasileira de Biologia, v. 40, p. 9-16, 1980.
McALPINE, J. F. A new species of Dasiops (Diptera:Lonchaeidae) injurious to apricots. Canadian Entomologist, v. 93, p. 539-544, 1961.
McALPINE, J. F.; STEYSKAL, G. C. A revision of Neosilba McAlpine with a key to the world genera of Lonchaeidae (Diptera). Canadian Entomologist, v. 114, p. 105-138, 1982.
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MINZÃO, E. R.; UCHÔA-FERNANDES, M. A. Diversidade de moscas frugívoras (Diptera, Tephritoidea) em áreas de matas decídua e ciliar no Pantanal sul-mato-grossense, Brasil. Revista Brasileira de Entomologia, v. 52, p. 441-445, 2008. NORRBOM, A. L.; McALPINE, J. F. A revision of the neotropical species of Dasiops
Rondani (Diptera: Lonchaeidae) attacking Passifora (Passifloraceae). Memoirs of Entomological Society of Washington v. 18, p. 189-211, 1997.
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OLIVEIRA, A. S. Diferenciação morfométrica e evolução de espécies de Neosilba (Diptera: Lonchaeidae). Instituto de Biologia da Universidade de Campinas. (Dissertação de Mestrado). 1992. 77p.
RAGA, A.; SOUZA FILHO, M. F.; ARTHUR, V.; MARTINS A. L. M. Avaliação da infestação de mosca das frutas em variedades de café (Coffea spp.). Arquivos do Instituto Biológico, v. 63, p. 59-63. 1996.
RAGA, A.; SOUZA FILHO, M. F.; ARTHUR, V.; SATO, M. E.; MACHADO, L. A.; BATISTA FILHO, A. Observações sobre a incidência de moscas-das-frutas (Diptera, Tephritidae) em frutos de laranja (Citrus sinensis). Arquivos do Instituto Biológico, v. 64, p. 125-129, 1997.
RAGA, A.; PRESTES, D. A. O.; SOUZA FILHO, M. F.; SATO, M. E.; SILOTO, R. C.; ZUCCHI, R. A. Occurrence of fruit flies in coffee varieties in the state of São Paulo, Brazil. Boletín de Sanidad Vegetal Plagas, v. 28, p. 519-524, 2002.
SANTOS, C. R.; BAYER, L. L.; CASTELLANI, T. T. Visitantes florais e riscos de pré dispersão em uma espécie de Ipomoeae (Convolvulaceae), Florianópolis. Biotemas, v. 5, p. 91-106, 1992.
SILVA, N. M. da. Levantamento e análise faunística de moscas-das-frutas (Diptera: Tephritidae) em quatro locais do Estado do Amazonas. Escola Superior de Agricultura “Luiz de Queiroz”, Universidade de São Paulo (Tese de Doutorado). 1993. 152p.
SOUZA S. A. S.; RESENDE A. L. S.; STRIKIS P. C.; COSTA J. R.; RICCI M. S. F.; AGUIAR-MENEZES, E. L. Infestação natural de moscas frugívoras (Diptera: Tephritoidea) em café arábica, sob cultivo orgânico arborizado e a pleno sol, em Valença, RJ. Neotropical Entomology, v. 34, p. 639-648, 2005.
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SOUZA FILHO, M. F. Biodiversidade de moscas-das-frutas (Diptera: Tephritidae) e seus parasitóides (Hymenoptera) em plantas hospedeiras no Estado de São Paulo. Escola Superior de Agricultura “Luiz de Queiroz”, Universidade de São Paulo (Tese de Doutorado). 1999. 174p.
STRIKIS, P. C.; PRADO, A. P. A new species of the genus Neosilba (Diptera: Lonchaeidae). Zootaxa, v. 828, p. 1-4, 2005.
STRIKIS, P. C.; PRADO, A. P. Lonchaeidae associados a frutos de nêspera, Eryobotria
japonica (Thunb.) Lindley (Rosaceae), com descrição de uma nova espécie de Neosilba (Diptera: Tephritoidea). Arquivos do Instituto Biológico, v. 76, p. 49-54,
2009.
UCHÔA-FERNANDES, M. A.; ZUCCHI, R. A. Metodología de colecta de Tephritidae y Lonchaeidae frugívoros (Diptera: Tephritoidea) y sus parasitóides (Hymenoptera). Anais da Sociedade Entomológica do Brasil, v. 28, 1999.
UCHÔA-FERNANDES, M. A.; OLIVEIRA, I. de, MOLINA, R. M. S.; ZUCCHI, R. A. Species Diversity of Frugivorous Flies (Diptera: Tephritoidea) from Hosts in the Cerrado of the State of Mato Grosso do Sul, Brazil. Neotropical Entomology. v. 31, p. 515-524, 2002.
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CAPÍTULO 1
REVIEW OF THE TAXONOMY AND BIOLOGY OF LONCHAEIDAE (DIPTERA), FRUIT FLIES OF ECONOMIC IMPORTANCE IN THE
NEOTROPICAL REGION
GISLOTI, L. J.¹; PRADO, A. P.¹ ǂ & UCHÔA, M. A.²
¹Departamento de Biologia Animal, UNICAMP, Campinas-SP, Brazil.
lauragisloti@gmail.com 2Laboratório de Insetos Frugívoros, Universidade Federal da
Grande Dourados (UFGD), Dourados-MS, Brazil. Awarded with research grant from CNPq-Brazil.
Abstract - Lonchaeidae consists of robust species of flies, of moderate size (from 3 to 6
mm long), body usually black, dark blue or green, with noticeable metallic reflections in some groups. Although several lonchaeid species have been associated with fruit or flowers of various species of Angiospermae of economic importance, they remain poorly studied. This may be related to the fact that the systematics of this group presents major taxonomic difficulties. The distinction between many species and even between some genera can be quite confusing. In order to elucidate the aspects of biogeography, ecology and taxonomy of the Lonchaeidae, we searched for publications in seven large databases (Web of Knowledge, Scopus, Elsevier, Jstor, Sciencedirect, SpringerLink, and Wiley Inter Science). Papers that presented any aspects on the systematics, taxonomy, bioecology and/or biogeography of any species of Lonchaeidae were selected. From January 1878 to December 2013 we found 201 papers published about Lonchaeids. In total, 538 species are described in two subfamilies and ten genera. Two monotypic genera are fossils: Morgea
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mcalpinei Hennig and Glaesolonchaea electrica Hennig. There are eight living genera with
536 species: 127 species of Dasiops Rondani, eight of Protearomyia McAlpine, seven of
Chaetolonchaea Czerny, 23 of Earomyia Zetterstedt, 20 of Lamprolonchaea Bezzi, 213 of Lonchaea Fallén, 98 of Silba Macquart, and 40 of Neosilba McAlpine. From the nineteenth
to the twentieth century, there was a progressive increase in publications about Lonchaeids worldwide. In the XXI century, the increase of publications on Lonchaeidae reflects the growing interest of researchers in studying their systematics, ecology and biogeography. On the other hand, the evident difficulties in the taxonomy of Lonchaeids can be a limiting factor for the entrance of beginner entomologists in the study of the lance flies. The lack of taxonomic keys and illustrations and the scarcity of research groups specialized in Lonchaeidae hinder and discourage the production of scientific knowledge about these flies. Even though they are responsible for considerable economic losses in crops, several basic aspects of their biology, ecology and biogeography are still unknown. This review provides a map of the world distribution of the species, and a taxonomic key for identification of subfamilies and all living genera worldwide.
Key Words: Lonchaeid, Lance Flies, Hosts, Neotropics, Natural history, Taxonomy.
Introduction
The Lonchaeidae are cyclorraphan acalyptrate Diptera, belonging to the superfamily Tephritoidea which also includes Pallopteridae, Piophilidae, Uliididae (= Otitidae = Pterocallidae), Richardiidae, Platystomatidae, Pyrgotidae, and Tephritidae (Korneyev 1999; Woodley et al. 2009). Lonchaeids in total sum 538 described species (two fossils) in two subfamilies and eight living genera in the world. They can be found in a wide variety of
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habitats, from the Arctic Circle to the Equator. However, there are no reports of endemism or occurrences at the poles or in New Zealand (McAlpine 1962).
Lonchaeidae forms a peculiar group because they present a typical standard body color: black and shiny. Sizes are moderate to small (3-6 mm) and with robust body. The female of all species have long membranous ovipositor, sometimes rigid (aculeus), and when distended it can be as long as the pre-abdomen. The tip of the aculeus is usually fine and slender, but in some species (e.g., some Dasiops) this structure is rather flattened and enlarged, forming a laminated structure similar to a spear, hence the origin of the popular name “lance flies” (Korytkowski & Ojeda 1971).
Formerly all species of Lonchaeidae were included within the family Sapromyzidae, when only a single genus (Lonchaea) was recognized. Lonchaea was originally raised to genus level by Fallén (1820), who had grouped all species of Lonchaea together with the "Ortalides".
Wiedemann (1830), Macquart (1843), Zetterstedt (1848), Walker (1860), and Becker (1895) gradually increased the number of described species in the genus Lonchaea, but their descriptions are superficial compared to modern standards and based on flimsy or variable characters, resulting in taxonomic confusion (Korytkowski & Ojeda 1971).
Lonchaeidae have been recognized as a family since Malloch & McAtee (1924) separated the Sapromyzidae into three families: Lonchaeidae, Sapromyzidae (now Lauxaniidae) and Pallopteridae.
Zetterstedt (1848) described the genus Earomyia; Macquart (1851), the genus Silba; Rondani (1856), Dasiops; Bezzi (1920), Lamprolonchaea; Czerny (1934), Chaetolonchaea, and McAlpine (1962), the two genera: Neosilba and Protearomyia, thus completing the eight genera currently recognized for Lonchaeidae.
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Currently, Lonchaeidae are divided into two subfamilies: Dasiopinae, which includes only the genus Dasiops, and Lonchaeinae, that includes the seven other genera:
Protearomyia, Lamprolonchaea, Chaetolonchaea, Earomyia, Silba, Neosilba and Lonchaea (McAlpine 1987; Korytkowski & Ojeda 1971).
Because most Lonchaeidae species are morphologically similar to each other, their taxonomy is difficult (McAlpine & Steyskal 1982), and identification to the species level can be extremely complicated. Additionally, the lack of comprehensive revisions of most of the lance fly genera, discourages and hinders future work with Lonchaeidae. In this review, we evaluate, interpret and discuss the available literature about Lonchaeidae, with the aim that this work may stimulate advances in the study of these flies.
Methodology
In order to elucidate the biogeographical and ecological aspects of lonchaeid flies, we conducted a literature review, compiling information from seven large databases (Web of Knowledge, Scopus, Elsevier, Jstor, Sciencedirect, SpringerLink and Wiley Inter Science). We also consulted the references cited in publications obtained in these databases. All publications that addressed any issues that would include information regarding Lonchaeidae were selected, reviewed, interpreted, and its content reported in this review. A map of the geographical distribution (by DIVA-GIS 7.5.0), and an illustrated taxonomic key (adapted from McAlpine 1987) with dichotomous entries for the two subfamilies, and the eight living genera of Lonchaeidae is presented, taking in account the current classification (McAlpine 1989).
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Results
Lonchaeidae was first recognized as a family in 1878 by Osten Sacken, in his catalog of species of North America, although Williston (1896) had recognized it as a subfamily of Sapromyzidae.
Coquillett (1902) described some species of Lonchaeidae in North America, and soon after, Meijere (1908, 1910, 1915) examined species from South Asia. Bezzi (1910) pioneered the description of Lonchaeidae in Brazil, when he published a work citing nine species. This author defined two genera: Palloptera Fallén and Lonchaea Fallén. In 1912, Cameron published the first paper on the biology of these flies, having investigated some biological aspects of Lonchaea chorea (Fabricius). In the next year, Towensend (1913) added information about the family, and published the description of Dasiops saltans. Melander (1913) decided to keep the lonchaeids within Sapromyzidae in his review of the species from North America.
In 1917, Silvestri conducted the first study assessing the damage caused by larvae of lonchaeids in host fruits. He also published a thorough morphological description for Silba
adipata (as Lonchaea aristella Becker), and discussed a possible parasitoid associated with
this species.
In 1919, Bezzi began to investigate the African lonchaeids in an important taxonomic and evolutionary study of the species of Lonchaea. In that paper, he established three groups of species, relating them to the habits of their larvae and the characters of the adults, such as feathering of the arista, the width of the antenna, and chaetotaxy of the body. Bezzi (1919) defined as more primitive the Lonchaeidae species whose larvae develop in decaying organic matter or animal excrement.
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Bezzi (1919) assumed that larvae with these habits could successively attack plant organs previously infested by other insects or pathogens, as in the cases of Lonchaea
chorea (Fabricius) and Lonchaea longicornis Williston. The adults of these primitive
species were characterized by having broad antennae, with micro-pubescent arista, and well defined chaetotaxy.
The second group defined by Bezzi (1919) was composed for lonchaeids with larvae galling stems of grass, whose adults were characterized by having very short antennae (not reaching a half of the face), with glabrous arista, and chaetotaxy poorly developed, represented by the species of Dasiops Rondani.
In the third group were included the carpophagous (fruit-feeding) larvae of species from the subtropical zone, in which the adults have a plumose arista, third antennal segment quite long, and well developed chaetotaxy. Bezzi (1919) indicated that the species of this group should be separated into a new taxon, and that the species Lonchaea plumosissima Bezzi and Lonchaea pendula Bezzi should be included in it (Bezzi 1919).
The following year, based on his previous work, Bezzi (1920) recognized three groups as subgenera of Lonchaea: Subgenus Lonchaea, Subgenus Dasiops and Subgenus
Carpolonchaea. In addition, he suggested that anomalous species such as Lonchaea aurea
Macquart, whose larvae live in tomato fruit (Solanum lycopersicum Mill.) (Solanaceae), could be included in another new subgenus, Lamprolonchaea, in which the adults are characterized by having their head with a very peculiar shape, typical wing venation, and metallic body coloration. Bezzi in 1923 made a further contribution by publishing an identification key for the species of Lonchaeidae of Australia.
Malloch (1920) recognized the family Lonchaeidae as distinct from Lauxaniidae, describing some new species of the genus Lonchaea, such as L. major and L.
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nigrocaerulea, based on material from the Amazon and Barbados, respectively. Currently,
these species are classified as belonging to the genus Neosilba McAlpine.
Malloch & McAtee (1924), removed the genera Palloptera and Eurygnathomyia (Czerny, 1904) from Lonchaeidae, and included both in Pallopteridae, thus definitely separating Lonchaeidae from Sapromyzidae. In the following year, Aldrich (1925) included a new species in Lonchaeidae: Lonchaea hirtithorax Aldrich (now Earomyia hirtithorax).
Curran (1932) added new knowledge to the taxonomy of Lonchaeidae, publishing an identification key to species of Lonchaea from Central America. In that key, Curran described Lonchaea luridipennis (= Dasiops) from Venezuela; Lonchaea trita from Panama; Lonchaea bakeri (= Dasiops) from Nicaragua; Lonchaea fuscipennis (= Neosilba) and Lonchaea dimidiata (= Neosilba), both from Panama; Lonchaea ceres from Brazil;
Lonchaea duida from Venezuela; Lonchaea nigrocaerulea Malloch (= Neosilba) from
Barbados; Lonchaea batesi (= Neosilba) from Guatemala, and Lonchaea major Malloch (=
Neosilba) from Peru.
Czerny (1934) investigated the lonchaeids from the Palearctic Region, and Hennig (1941) for the first time included the adult genitalia in the description of species of Lonchaeidae, demonstrating the importance of these characters, which thereafter have generally been used in identification of these Tephritoidea.
Blanchard (1948) published the first revision of the Argentine species of Lonchaeidae, describing some new species, and adding new information about
Carpolonchaea [You already said that]. Blanchard (1948) noted that the species of this
genus are mostly Neotropical, and indicated L. plumossisima Bezzi (1919) as type species and suggested that Carpolonchaea could be elevated to the level of genus.
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Hennig (1948), in his concept of the genus Carpolonchaea, included seven Neotropical species, among them: Carpolonchaea dimidiata (Curran) from Panama and Venezuela, and Carpolonchaea pendula (Bezzi), from Chile, Peru and Costa Rica. In the same paper, Hennig described Carpolonchaea magna from Peru, Carpolonchaea parva from Peru and Costa Rica, Carpolonchaea longicerata from Peru, Carpolonchaea devians from Bolivia (currently in Silba), and Carpolonchaea intermedia from Peru; this last species was later included in the genus Lonchaea.
Collin (1953) reviewed the British lonchaeids, and McAlpine (1956a) analyzed species of the Old World, transferring Lonchaea (Carpolonchaea) plumosissima Bezzi to
Silba, indicating that that species was not correctly described by Bezzi. In another
publication in the same year, McAlpine (1956b) added more information about these flies, clarifying the identities of 15 species, six of which were described as new to science. In the same year, Smith (1956) added information on the biology of Lonchaeidae, describing the immature stages of some Lonchaea species.
Berry & Vaquero (1957) analyzed species of Lonchaeidae as potential pests, pointing out that this group was of little economic importance, composed by few species, and reported Carpolonchaea pendula Bezzi in El Salvador (Central America). In the following years, contributions to lonchaeid taxonomy continued, with several species described or redescribed in different geographical regions (Collin 1957; McAlpine 1958; Sasakawa 1958; Morge 1959; McAlpine 1960).
In the 1960s, publications about the phylogeny and ecology of Lonchaeidae began to appear. McAlpine (1960) published a key based on species from southern Africa, showing how to identifying genera of Lonchaeidae. In this paper, he included
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Silba Macquart and Lonchaea Fallén. The following year started with publications relating
the Lonchaeids as pests of agricultural importance for some cultures, such as the apricot (Moffit & Yaruss 1961; McAlpine 1961). McAlpine (1962) published an extensive review on the Lonchaeidae worldwide, presented a phylogeny, adding new taxa, and updating to eight genera: Dasiops Rondani, Protearomyia McAlpine (new genre); Chaetolonchaea Czerny, Earomyia Zetterstedt, Lamprolonchaea Bezzi, Silba Mcquart, Neosilba McAlpine (= Carpolonchaea) and Lonchaea Fallén. This taxonomist recognized five genera proposed by Hennig (1948), except Spermatolonchaea Bendel, which was included within Earomyia Zetterstedt and Carpolonchaea Bezzi, which according to the principles of priority was designated as Silba Mcquart.
McAlpine (1962) considered Lonchaea as the most evolved genus of Lonchaeidae, defining it as the sister group of Neosilba, assuming that these two genera come from a common ancestor with Silba, very similar to this, but it would have lost the setae of the prosternum. He also pointed out that some changes in morphological characters happened, including decreases in the feathering of arista. He described the genus Neosilba, designating Lonchaea batesi Curran (1932) as type species, previously assigned to the genus Carpolonchaea by Hennig (1948), and to the genus Silba by McAlpine (1960). McAlpine (1962) recognized Silba devians as the single one species of Silba in the Neotropical Region, and transferred all remaining species previously treated as
Carpolonchaea to the genus Neosilba.
McAlpine (1962) realized that the genus Neosilba is quite similar to Silba, except by having the third antennal segment usually three times longer than wide (usually in Silba this segment is four to five times longer than broad); arista with well developed feathering or rarely glabrous, and scutellum with setulae between the basal and apical to the scutellar
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arrows. He mentioned that its larvae in some cases are associated with the fruit pest species, particularly with Tephritidae or frugivorous larvae of Lepidoptera, causing physiological or mechanical injury in the host fruit. McAlpine (1962) reported that Neosilba pendula (Bezzi) had been reported as primary pest of pepper (Capsicum sp.) (Solanaceae) in Peru.
One of the most important contributions of McAlpine (1962) was the provision a key to identify species Neosilba, including N. intermedia (Hennig) (Peru), N. devians (Hennig) (Bolivia), N. flavipennis (Morge) (Holartico), N. fuscipennis (Curran) (Panama),
N. longicerata (Hennig) (Peru), N. dimidiata (Curran) (Panama), N. magna (Hennig)
(Peru), N. glaberrima (Wiedemann) (Western India, South and Central America), N. batesi (Curran) (Guatemala), N. nigrocaerulea (Malloch) (Barbados), N. major (Malloch) (Brazil), N. parva (Hennig) (Peru), and N. pendula (Bezzi) from Brazil.
Morge (1963) proposed a new phylogenetic scheme based on species from Palaearctic, in which the Lonchaeids were subdivided into three subfamilies: Dasiopinae which includes the genera Silvestrodasiops Morge and Dasiops Rondani; Earomyiinae, comprising the genera Priscoearomyia Morge; Chaetolonchaea Czerny, Earomyia Zetterstedt and Lamprolonchaea Bezzi, and Lonchaeinae with Silba Macquart,
Setisquamalonchaea (new genre) and Lonchaea Fallén. However, this classification has
never been well accepted by the experts in Lonchaeidae.
McAlpine (1964) presented a crucial paper to broaden the knowledge of Lonchaeidae, with an extensive list of new species, as result of his elegant paper published in 1962, which describes 160 species from different regions of the world, with 20 of them from Neotropics, being 17 species of Dasiops, and three of Lonchaea.
The 1960s were marked by publications on the taxonomy and biology of Lonchaeids, with descriptions of several new species in distinct genera, and records of
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species occurrences from different localities worldwide (Romero & Ruppel 1973; Sasakawa 1964; Johnsen et al. 1965; Nuorteva 1967; Hennig 1967).
Hennig (1967) did a remarkable study of fossils of Lonchaeids in amber, describing the species Morgea mcalpinei Hennig and Glaesolonchaea electrica Hennig. The age of those extinct species was estimated between 48.6 and 40.4 million years ago. He proposed a phylogenetic model for Lonchaeidae, very similar to that presented by McAlpine (1962). In the same year, Beaver (1967) and Nuorteva (1967) added information on biology to some species Lonchaea.
Later on, McAlpine & Munroe (1968) published important information on ecology of some species of Lonchaeids, and described four new species. These authors noted a bit peculiar behavior for that flies: the swarming (formation of leks for mating). In fact, the first author continued studying these flies, producing two more publications on the biology and taxonomy of lance flies (McAlpine 1970; McAlpine & Morge 1970).
In the 70s, many articles were published on Lonchaeidae. Some authors emphasized predation by larvae of lonchaeids (Lonchaea) on larvae of other insects (Harman & Wallace 1971; Kishi 1972). Other publications have been devoted to the economic importance of lonchaeids as agricultural pests (Romero & Ruppel 1973; Stegmaier 1973; Brinholi et al. 1974; Boza & Waddill 1978; Steyskal 1978; Waddill & Weems 1978; Pena & Waddill 1982). But in fact, the vast majority of publications at that time continued toward the description of new species and new habitats, such as the samplings on Lonchaeids diversity undertaken in Russia (Kovalev 1973, 1976, 1978), Austria (Morge 1974), Sri Lanka (McAlpine 1975a), Malaysia (McAlpine 1975b), Afghanistan (Soos 1977) and Chile (McAlpine 1974).
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Korytkowski & Ojeda (1971) reviewed the species of Lonchaeidae from Peru, based on material collected in the North of that country, and reported a list with 80 Neotropical species, distributed in three genera. In fact, many species treated in 1971 by Korytkowski & Ojeda as Silba, currently are species of Neosilba.
In the 80s were published some fundamental papers to consolidate the knowledge about Lonchaeidae, with revisions of three genus: Chaetolonchaea (McAlpine & Steyskal 1982), Neosilba (McAlpine & Steyskal 1982), and Protearomyia (McAlpine 1983), which updated the information about these taxa. It is remarkable that the work McApine (1982) remains the main reference on Lonchaeids the Neotropics.
Another important contribution was the publication of a Lonchaeidae checklist, in which 17 species of Dasiops, one species of Lamprolonchaea, 17 species of Lonchaea, and 17 of Silba were registered to the tropical regions of Africa (McAlpine 1981).
Papers on the biology and ecology of these flies were also published in the same decade. The investigation of the predatory behavior of Lonchaea corticis Taylor upon larvae of weevils was presented by several authors (Alfaro & Borden 1980; Hulme 1989) that investigated this aspect in many laboratory experiments. The biology of Lonchaeidae was also investigated, such as some aspects of Earomyia species (Hedlin et al. 1981; Morge & Nanu 1981), species of Lonchaea (Hedlin et al. 1981; Kovalev 1984), species of
Silba (Awadallah et al. 1980; Katsoyannos 1983a) and species of Dasiops in South
America (Peñaranda et al. 1986).
Other important biological data were added in the years 80s, such as the swarming courtship behavior of Lamprolonchaea species, and the discovery of a potent attractant to catch Silba adipata (a key pest of figs, Ficus carica L.) in traps was provided by Katsoyannos (1983b). Guerin & Katsoyannos (1984) published a further contribution,
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clarifying the biology of lance flies. Also, in this decade was published for the first time, the only paper one that studied the aspects of molecular biology on Lonchaeids (De Conti
et al. 1984).
Regarding the damage caused by larvae of Lonchaeids in plant tissues, were published three important papers in the years 80s, involving different Lonchaeidae species, attacking different organs of different plant species. The first study was about species of
Dasiops attacking fruits and flowers of passion fruit (Passiflora sp.) (Steyskal 1978). The
second paper refers to the attack of some species of Earomyia in seeds of fir (Abies
amabiles) (Hedlin et al. 1981). The third paper refers to the damages caused by larvae of Neosilba perezi in terminal buds of cassava (Manihot esculenta) (Pena 1982). Within the
taxonomy of Lonchaeidae, were published keys to characterize different Lonchaeids species, including the Dasiops from Africa (Morge 1980; Shtakel'berg 1989), and
Lonchaea species from Europe (Kovalev 1981, 1984). Lonchaeidae species from Ireland
were also investigated for the first time (Chandler 1986). Also in the 80s, two important book chapters were published about the Lonchaeids in the Manual of Nearctic Diptera. In Volume II, the taxonomy and biology of that family were fully explored, with several illustrations that have enriched the work. Moreover, the author has provided a key for identification of living Lonchaeidae genera, such as be currently accepted: Chaetolonchaea Czerny, Dasiops Rondani, Earomyia Zelterstedt, Lamprolonchaea Bezzi, Lonchaea Fallén,
Neosilba McAlpine, Protearomyia McAlpine, and Silba Macquart (McAlpine 1987 - see
key adapted to the end of this review). Phylogeny and classification of Lonchaeidae were presented in Volume III of that same publication. McAlpine (1989) suggested that the aedeagus of the most ancient species of Lonchaeid was simple (unsegmented and without apical glands), membranous and subsequently were modified to form the several types of
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aedeagus currently found in Lonchaeids. Other plesiomorphics characteristics indicated by McAlpine are entirely black color of body, including the head and legs, the presence of the seven abdominal spiracles in males and females, and three spermathecae in females. While none of these features is unique to Lonchaeidae, no other families of Tephritoidea present all of them together. Thus, the author suggested that Lonchaeidae could be the sister group of all other Tephritoidea.
Finally, McAlpine (1989) defined the Lonchaeidae into two subfamilies: Dasiopinae (oldest lineage) containing the genus Dasiops, and Lonchaeinae (more recent), containing the tribe Earomyiini, with the genera: Protearomyia, Chaetolonchaea, Earomyia,
Lamprolonchaea, and the tribe Lonchaeini, with the genera: Lonchaea,
Setisquantalonchaea (= now Silba), Silba, and Neosilba. In addition, he reports that
Lonchaeidae should contain about 700 species worldwide, of which about a half were undescribed species. McAlpine (op. cit.) highlights that Dasiops and Lonchaea are the most specious genera, with distribution in all zoogeographic regions; that Protearomyia,
Chaetolonchaea, and Earomyia are present throughout the Holoartic region, but Protearomyia also occurs in Patagonia. Lamprolonchaea and Silba are distributed mainly
in the Oriental region, but also occur in Ethiopia and Australia; that Neosilba is limited to Neotropical Region, and Setisquamalonchaea (= now Silba) is endemic to the Palearctic Region.
In the 90s, many papers about lonchaeids were published, addressing mainly on the fact that several species of Lonchaeidae are characterized as potential pests for agriculture. Causton (1993) reported the first attack in a species of passion fruit by a species of Dasiops in Venezuela. Norrbom & McAlpine (1997) reviewed the genus Dasiops, highlighting some pest species in passion fruit (Passiflora spp.), and they suggested that other species
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have potential to be used in biological control against invasive species of Passifloraceae in Hawaii, and worldwide. Lourenção et al. (1996) and Bellotti et al. (1999) evaluated the infestation Neosilba perezi in shoots of cassava, reporting this species as an important pest for cassava in South America. Ahlmark & Steck (1997) pointed out the importance
Neosilba batesi as a secondary pest of avocado (Persea americana) in Florida. Finally,
Owens & Morris (1998) identified larvae Earomyia abietum causing damage in seeds of firs.
Uchôa (1999), in a pioneering study on the diversity and trophic interactions of Tephritoidea with their host plants in southwest Brazil, found that lonchaeids in many species of native and cultivated fruits, including Citrus sinensis and Citrus reticulata (Rutaceae) are even more abundant and economically important that Tephritidae. This research provided information that led to other Brazilian researchers to launch a different look on Lonchaeidae, whose species were previously considered secondary invaders of fruits and vegetables (Uchôa & Zucchi 1999; Uchôa et al. 2002; Uchôa et al. 2003a; Uchôa
et al. 2003b; Uchôa et al. 2003c; Uchôa 2012).
From the 90s, the Lonchaeidae have been considered as potential pests of vegetables and fruit, beginning of the first studies related to control these flies. In Chile, Sánchez et al. (1991) evaluated the effect of four different insecticides for the control of Neosilba species. Other important studies were related to natural enemies, seeing the use of parasitoids for biological control of lance flies. Wharton et al. (1998) made associations of some species of Eucoilidae as parasitoid in larva of Lonchaeidae that eat pulp of fruit. Gallardo et al. (2000) has described a new species of Trybliographa (Eucoilidae) in Brazil (Trybliographa
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of: orange, Citrus sinensis, tangerine, Citrus reticulata (Rutaceae) and pequi, Caryocar
brasiliense (Caryocaraceae) in the Cerrado.
The 90s were also marked by the presence of numerous records for lonchaeids in Europe. Werner (1995), and Maca (1999) had records of species in Germany; Maca (1997) recorded species lonchaeids the Czech Republic, and Slovakia. Chandler (1998) listed the British species of Dasiops, and MacGowan & Rotheray (2008), reported Lonchaea species in the UK.
Dobson (1992) published a rather curious observation, pointing out that the adults of Lonchaeid species are possible cleptoparasites of spider’s web. Since that time, this is the only paper that suggests this kind of behavior for Lonchaeidae.
The papers published during the last decade, left quite clear the need for taxonomic studies on Lonchaeids. Thus, various specimens deposited in museums were analyzed and from this material, some new species have been described. MacGowan (2004a, 2006a, 2007a, 2008) examined specimens from European museums and corrected numerous taxonomic errors in samples. He examined specimens from Malaysia deposited in the Natural History Museum of Sweden, described a new species of Dasiops, two of Lonchaea, and nine of Silba (MacGowan 2005a). MacGowan et al. (2007) also examined specimens from a museum in Switzerland, and illustrated for the first time the male genitalia for
Lonchaea hyalipennis Zetterstedt 1848. On the other hand, some researchers explored the
Neotropical species of Neosilba, publishing papers on the ecological context (Araújo & Zucchi 2002; Bomfim et al. 2007, Caires et al. 2009).
On taxonomy, more recently several authors described new species of lonchaeids. Species were described in Brazil (Strikis & Prado 2005; Strikis & Prado 2006; Strikis & Lerena 2009; Strikis & Prado 2009), Spain (MacGowan 2000; MacGowan 2009); UK
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(MacGowan & Rotheray 2000), Andorra (MacGowan 2001a), Switzerland (MacGowan 2001b), Taiwan (MacGowan 2004b, 2007b), Israel (MacGowan & Freidberg 2008), from Central and Southern Africa (MacGowan 2005b), China (MacGowan 2007b), and Thailand (MacGowan 2007b).
About Lonchaeidae diversity were reported species in the Great Britain region (MacGowan 2001c, 2006b, MacGowan & Rothery 2008), Denmark (MacGowan 2001d, 2005c), Czech Republic (Maca & Bartak 2001), London (Allen 2002, 2003), Spain (Carles-Tolra 2004), and Brazil (Bittencourt et al. 2006).
Statement about species considered pests remained fairly addressed in this decade. Aluja & Díaz-Fleischer (2004) found N. batesi infesting fruit avocado Persea americana in Mexico. In Brazil, Araújo & Zucchi (2002) evaluated the levels of infestation by N.
pendula on native and exotic fruits, finding quite high infestation levels for fruits in
barbado's cherry (Malpighia emarginata). Carvalho & Marques (2004) and Santos et al. (2004) reported N. zadolicha attacking umbu-caja fruit's (Spondias sp.). Still in Brazil,
Neosilba species attacking loquat's fruit (Eriobotryia japonica), and coffee (Coffea arabica) (Strikis & Prado 2005; Strikis & Prado 2006, respectively) were reported.
Fruits of fig (Ficus carica) (Moraceae) were also reported as being quite attractive to lonchaeids. Larvae of Lonchaeid species such as Silba adipata were reported (in Iraq, in Montenegro, and in South Africa) (Abdullah & Fandy 2006; Giliomee et al. 2007; Radonjic & Hrnci 2009), and Lonchaea aristella (in Portugal) (Gonçalves et al. 2008) as pests of fruits of Moraceae. Dasiops caustonae was also recorded infesting passion fruit (Passiflora
edulis) in Colombia (Umana 2005).
The last decade was marked by a large increase in publications on the genus
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varieties of peach (Prunus persica). Uchôa & Nicácio (2010) associated larvae of Neosilba species with 38 host fruit species. Gisloti & Prado (2011a, 2011b), and Strikis et al. (2012), analyzed the infestation of a Neosilba species in cassava (Manihot esculenta), and Lopes et
al. (2008) analyzed the infestation by larvae of Neosilba in tangerine (Citrus reticulata)
orchards. Aguiar-Menezes et al. (2007) reviewed the species Neosilba infestation in different varieties of coffee (Coffea arabica). In the same period were recorded parasitoids associated with larvae of several species of Lonchaeidae (Aguiar-Menezes et al. 2008; Souza et al. 2012), including a new species of parasitoid (Arouca & Penteado-Dias 2011; Gisloti & Prado 2012; Marsaro-Junior et al. 2012, Fernandes et al. 2013).
On the diversity of host fruits of Lonchaeidae in Brazil, Uchôa (2012) related species Neosilba as possible candidates for biological control of mistletoe Psittacanthus
acinarius (Martius) (misidentified the Psittacanthus plagiophyllus Eichler) (Santalales:
Loranthaceae) a hemi-parasite of tropical trees; Montes et al. (2012) and Camargos et al. (2011) investigated the infestation of these flies in Coffea arabica; Adaime et al. (2012) associated with species of Neosilba in fruits of murici (Byrsonima crassifolia), Dias et al. (2012) found larvae Neosilba attacking fruits of Jatropha curcas, Bittencourt et al. (2013) reported five new occurrences of Neosilba species in Brazil, and Nicácio & Uchôa (2011) investigated the biodiversity of these flies in the Pantanal region.
The taxonomy of Neosilba species were well explored in the recent years. Strikis (2011) described eleven new species in Brazil, and Galeano-Olaya & Canal (2012) described ten new species of Neosilba from Colombia. The genus Lamprolonchaea also had a major publication recently (Blacket & Malipatil 2010).
The species of Dasiops have been explored in recent papers, pointing out about their status as pests in plants of economic interest. They were considered major pests of the
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cactus (Selenicereus megalanthus) (Medina & Kondo, 2012), and in flowers of passion fruits, (Passiflora sp). (Imbachi et al. 2012; Quintero et al. 2012; Wyckhuys et al. 2012).
In the last decade the lonchaeids remained being reported in Spain (Carles-Tolra et
al. 2010), France (MacGowan 2012), Russia (MacGowan 2010), in UK (Perry 2010), the
Czech Republic (Barták & Roháček 2011), India (MacGowan et al. 2012), and Japan (MacGowan & Okamoto 2013). Finally, MacGowan & Okamoto (2013) modified the classification of Lonchaeidae, reassessing the genus Silba, and concluding that the genus
Setisquamalonchaea Morge is a junior synonym of Silba Macquart.
Discussion
The Lonchaeid family consists of two subfamilies: Dasiopinae, containing a single genus Dasiops, and Lonchaeinae, the more biologically diverse subfamily, containing the remaining seven genera (see adapted key from McAlpine 1987, available at the end of this paper). The classification of Lonchaeids has been relatively stable. Czerny (1934) erected the genus Chaetolonchaea, and McAlpine (1962) described the genus Protearomyia, then
Setisquamalonchaea was added by Morge in 1963, but it is now regarded as a synonym of Silba (MacGowan & Okamoto 2013).
Species of Dasiops are mainly found in the Nearctic region, though some species are found less frequently in the Palaearctic region, southern Africa, Asia, Australasia and South America. The species of Earomyia and Chaetolonchaea are restricted to the Nearctic and Palaearctic regions. Lonchaea species are commonly found in the Palaearctic, but there are some records of endemic species in both Nearctic and Asian regions. Protearomyia species are distributed primarily by Nearctic region, but there are also some species of this genus in the Palaearctic and southern Chile. Lamprolonchaea species are confined to the
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Palaearctic and Australasian regions. Silba species are present mainly in Africa, Asia and Australia, having a single species in South America, but the species of Neosilba are restricted to the Neotropical region (Fig. 1).
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About 201 papers on Lonchaeidae species (Fig. 2) were published from 1878 to November 2013. A total of 538 species were described in two monotypic genera from fossils, and eight living genera, being 127 species of Dasiops (Fig. 3), 8 species of
Protearomyia (Fig. 6), 20 species of Lamprolonchaea (Fig. 8), 7 species of Chaetolonchaea (Fig. 10, 11), 23 species of Earomyia (Figs. 12, 13), 213 species of Lonchaea (Figs. 16, 17), 40 species of Neosilba (Fig. 18), and 98 species of Silba (Fig.
19).
Of total publications (201) about Lonchaeidae in 135 years (1878-2013), the species of Neosilba are pointed out in 60 papers, standing out in the publications. That paper mainly makes associations of larvae of Neosilba species as potential pests of several species of fruit, being many of them of commercial interest (Lourenção et al. 1996; Araújo & Zucchi 2002; Santos et al. 2004; Uchôa 2012). The species of Neosilba appear to be the ecological equivalent for the species of Silba in the New World. Both genera are very similar in their morphological and ecological aspects. The species of Neosilba are known from Caribe, Mexico, Colombia to Brazil. Forty species were described, and at least more 60 species waits for description in the Neotropical region (McAlpine & Steyskal 1982).
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Figure 2. Distribution of publications about the Lonchaeidae genera (Diptera: Tephritoidea), since 1878 until December 2013 (n = 201) [*other = Papers about Lonchaeidae without specified genus].
Although Araújo & Zucchi (2002) have speculated that the species of Neosilba probably occurs as secondary invaders of fruits, after the primary attack by species Tephritidae, nowadays it is known that the larvae of several Neosilba species infest a wide variety of fruits and vegetables from different angiosperm families, acting as primary invaders.
The genus Chaetolonchaea has the lowest number of publications; just a revision of it by McAlpine in 1956b, beyond that, there are record of two species in Hungary (MacGowan 2007a). This genus is restricted to the Nearctic and Palaearctic regions. Three species were recorded in Europe and two in the Nearctic. Information regarding to the natural history and ecology of Chaetolonchaea species are scarce.
The genera Protearomyia (2 papers), Lamprolonchaea (4 papers), and Earomyia (9 papers), are poorly studied. The publications on Earomyia are mainly lists of species
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records, and some aspects of their geographical distribution worldwide (Skrzypczyńska 1984; Perry 2010). Protearomyia is poor in described species, with records of occurrence in the Nearctic and Europe (Palearctic). Earomyia is composed by species distributed in the Palearctic and Nearctic regions.
The genus Lamprolonchaea is composed by colorful species with metallic tones, mainly distributed in the Oriental region, and in the Australasia. One species, L. smaragdi (Walker), was found in the Mediterranean and Northern Europe (Netherlands and Germany), associated with fruits of the following hosts: Capsicum sp. (Solanaceae), Prunus
armeniaca and Prunus persica (Rosaceae), Citrus paradisi, Citrus limon, Citrus reticulata
(Rutaceae), and Persea americana (Lauraceae) (Blacket & Malipatil 2010).
The genus Lonchaea (51 publications) has been the best studied. It has the largest number of described species in Lonchaeidae, with a wide geographic distribution. There are 213 named species, present in areas of boreal forest of Palaearctic and Nearctic regions. Currently, there are about 65 species recorded in Europe, and 72 in Nearctic region. Researches about the species of this genus have focused on investigations of predatory potential of their larvae on larvae of wood-destroying beetles (Harman & Wallace 1971; Kishi 1972; Alfaro & Borden 1980; Hulme 1989; Hulme 1990).
Many species of Dasiops are commonly associated as pests of fruit of some species, especially of Passifloraceae (Moffit & Yaruss 1961; Stegmaier 1973; Steyskal 1980; Norrbom & McAlpine 1997; Causton & Rangel 2002; Uchôa et al. 2003a, 2003c, Amaya et
al. 2009; Delgado et al. 2010; Quintero et al. 2012; Carrero et al. 2013). This genus is the
second most species rich in Lonchaeidae, with greater species richness in Nearctic Region. On the other hand, the genus Silba, even with a large number of described species (98), is a little-studied taxon (12 papers). Furthermore, most studies on the species of Silba focused
