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The Muscidae (Diptera) from the Atlantic Forest of Serra de Paranapiacaba, southestern Brazil

Abstract

A first survey of Muscidae in the State of São Paulo (Southeastern Brazil) is presented here with a one-year of Malaise trap collecting from August 2010 to July 2011 at the Biological Reserve Alto da Serra de Paranapiacaba (23°46′00″-23°47′10″S, 46°18′20″-46°20′40″W, 750-891 m of altitude). A total of 1,284 individuals of muscids were collected, and 15 genera and 39 species of Muscidae were identified. So far, only one muscid species had been recorded to the Reserve, which now has its Muscidae diversity increased to 40 species. Thirteen species are new records for the State of São Paulo. With this, the number of species of Muscidae species known to occur in the State of São Paulo is increased to 169. The interval between November and February was higher in number of individuals and number of species. Muscidae presented a seasonal pattern, with more abundance and diversity in that interval. The study area is covered by secondary forest and very close to São Paulo metropolitan area, and the composition of the fauna of Muscidae signalizes this environment changing and anthropic stress with nine species with synanthropic habits, two of them are typically synanthropic species.

Keywords.
Diversity; Inventory; Neotropical region; Seasonality; State of São Paulo; Survey

INTRODUCTION

The family Muscidae is worldwide distributed and include about 5,200 described species in 187 genera (Pape et al., 2011Pape, T.; Blagoderov, V. & Mostovski, M.B. 2011. Order Diptera Linnaeus, 1758. In: Zhang, Z.-Q. (Ed.). Animal biodiversity: an outline of higher-level classification and survey of taxonomic richness. Zootaxa, 3148: 1-237. http://doi.org/10.11646/zootaxa.3148.1.9
http://doi.org/10.11646/zootaxa.3148.1.9...
). In the Neotropical Region there are over 800 species and 85 genera (Couri & Carvalho, 2005Couri, M.S. & Carvalho, C.J.B. De. 2005. Diptera Muscidae do Estado do Rio de Janeiro (Brasil). Biota Neotropica, 5: 1-18. http://doi.org/10.1590/S1676-06032005000300015
http://doi.org/10.1590/S1676-06032005000...
). The family is greatly abundant in all continents, occurring in most oceanic islands, and also in the Arctic and regions of tundra vegetation (Huckett & Vockeroth, 1987Huckett, H.C. & Vockeroth, J.R. 1987. Muscidae. In: McAlpine, J.F.; Peterson, B.V.; Shewell, G.H.; Teskey, H.J.; Vocheroth, J.R. & Wood, D.M. (Eds.). Manual of Neartic Diptera. Ottawa, Agriculture Canada. v. 2, p. 1115-1131.). Muscid flies have diverse feeding habits, including predators, phytophagous, saprophagous, anthophilous, parasites and haematophagous (Couri, 1999Couri, M.S. 1999. Myiasis caused by obligatory parasites. Ia. Philornis Meinert (Muscidae). In: Guimarães, J.H. & Papavero, N. (Eds.). Myiasis in man and animals in the Neotropical region. São Paulo, Editora Plêiade. p. 44-70.; Savage & Vockeroth, 2010Savage, J. & Vockeroth, J.R. 2010. Family Muscidae. In: Brown, B.V.; Borkent, A.; Cumming, J.M.; Wood, D.M.; Woodley, N.E. & Zumbado, M.A. (Eds.). Manual of Central American Diptera. Ottawa, NRC Research Press. v. 2, p. 1281-1295.; Carvalho et al., 2012Carvalho, C.J.B. De; Rafael, J.A.; Couri, M.S. & Silva, V.C. 2012. Diptera. In: Rafael, J.A.; Melo, G.A.R.; Carvalho, C.J.B. de; Casari, S. & Constantino, R. (Eds.). Insetos do Brasil: diversidade e taxonomia. Ribeirão Preto, Holos Editora. p. 701-743.).

There are a number of studies with inventory of Diptera in the Neotropics (e.g.,Carvalho & Couri, 1991Carvalho, C.J.B. De & Couri, M.S. 1991. Muscidae, Fanniidae e Calliphoridae (Diptera) do Projeto Maracá, Roraima, Brasil. Acta Amazonica, 21: 35-43. http://doi.org/10.1590/1809-43921991211043
http://doi.org/10.1590/1809-439219912110...
; Couri et al., 2000Couri, M.S.; Lamas, C.J.E.; De Cima Aires, C.C.; De Mello-Patiu, C.A.; Maia, V.C.; Pamplona, D.M. & Magno, P. 2000. Diptera da Serra do Navio (Amapá, Brasil): Asilidae, Bombyliidae, Calliphoridae, Micropezidae, Muscidae, Sarcophagidae, Stratiomyiidae, Syrphidae, Tabanidae e Tachinidae. Revista Brasileira de Zoociências, 2(1): 91-101.; Pamplona et al., 2000Pamplona, D.; Maia, V.C.; Couri, M.S.; Lamas, C.J.E. & Aires, C.D.C. 2000. A survey of Diptera on Paquetá Island, Rio de Janeiro, Brazil. Entomologist’s Monthly Magazine, 136(1632-1635): 169-175.; Krüger et al., 2010Krüger, R.F.; Carvalho, C.J.B. De & Ribeiro, P.B. 2010. Assembly rules in Muscid fly assemblages in the grasslands biome of Southern Brazil. Neotropical Entomology, 39(3): 345-353. http://doi.org/10.1590/S1519-566X2010000300006
http://doi.org/10.1590/S1519-566X2010000...
; Borkent et al., 2018Borkent, A.; Brown, B.; Adler, P.H.; Amorim, D.S.; Barber, K.; Bickel, D.; Boucher, S.; Brooks, S.E.; Burger, J., Burington, Z.L.; Capellari, R.S.; Costa, D.N.R.; Cumming, J.M.; Curler, G.; Dick, C.W.; Epler, J.H.; Fisher, E.; Gaimari, S.D.; Gelhaus, J.; Grimaldi, D.A.; Hash, J.; Hauser, M.; Hippa, H.; Ibanez-Bernal, S.; Jaschhof, M.; Kameneva, E.P.; Kerr, P.H.; Korneyev, V.; Korytkowski, C.A.; Kung, G.-A.; Kvifte, G.M.; Lonsdale, O.; Marshall, S.A.; Mathis, W.N.; Michelsen, V.; Naglis, S.; Norrbom, A.L.; Paiero, S.; Pape, T.; Pereira-Colavite, A.; Pollet, M.; Rochefort, S.; Rung, A.; Runyon, J.B.; Savage, J.; Silva, V.C.; Sinclair, B.J.; Skevington, J.H.; Stireman, J.O.; Vilkamaa, P.; Wheeler, T.; Whitworth, T.; Wong, M.; Wood, D.M.; Woodley, N.; Yau, T; Zavortink, T.J. & Zumbado, M.A. 2018. Remarkable fly (Diptera) diversity in a patch of Costa Rican cloud forest: Why inventory is a vital science. Zootaxa, 4402: 53-90. http://doi.org/10.11646/zootaxa.4402.1.3
http://doi.org/10.11646/zootaxa.4402.1.3...
; Zafalon-Silva et al., 2018Zafalon-Silva, A.; Kirst, F.D. & Krüger, R.F. 2018. Houseflies speaking for the conservation of natural areas: a broad sampling of Muscidae (Diptera) on coastal plains of the Pampa biome, Southern Brazil. Revista Brasileira de Entomologia, 64(4): 292-303. http://doi.org/10.1016/j.rbe.2018.09.002
http://doi.org/10.1016/j.rbe.2018.09.002...
), on the other hand, several studies focused on groups with agricultural or forensic importance (e.g.,Ferraz et al., 2009Ferraz, A.C.P.; Gadelha, B.Q. & Aguiar-Coelho, V.M. 2009. Análise faunística de Calliphoridae (Diptera) da Reserva Biológica do Tinguá, Nova Iguaçu, Rio de Janeiro. Revista Brasileira de Entomologia, 53(4): 620-628. http://doi.org/10.1590/S0085-56262009000400012
http://doi.org/10.1590/S0085-56262009000...
; Mulieri et al., 2011Mulieri, P.R.; Patitucci, L.D.; Schnack, J.A. & Mariluis, J.C. 2011. Diversity and seasonal dynamics of an assemblage of sarcophagid Diptera in a gradient of urbanization. Journal of Insect Science, 11: 1-15. http://doi.org/10.1673/031.011.9101
http://doi.org/10.1673/031.011.9101...
; Garcia et al., 2003Garcia, F.R.M.; Campos, J.V. & Corseuil, E. 2003. Análise Faunística de Espécies de Moscas-das-Frutas (Diptera: Tephritidae) na Região Oeste de Santa Catarina. Neotropical Entomology, 32(3): 421-426. http://doi.org/10.1590/S1519-566X2003000300006
http://doi.org/10.1590/S1519-566X2003000...
; Cavallari et al., 2015Cavallari, M.L.; Baltazar, F.N.; Nihei, S.S.; Muñoz, D.R. & Tolezano, J.E. 2015. Dipterofauna associated with Sus scrofa Linné, 1758, carcasses in urban and coastal regions of São Paulo State, Brazil. Psyche: A Journal of Entomology, article ID 983980, 12p. http://doi.org/10.1155/2015/983980
http://doi.org/10.1155/2015/983980...
; Carvalho et al., 2017Carvalho, R.P.; Azevedo, W.T.A.; Figueiredo, A.L.; Lessa, C.S.S. & Aguiar, V.M. 2017. Dipterofauna associated with rat carcasses in the Atlantic Forest, Southeastern Brazil. Journal of Medical Entomology, 54(6): 1498-1509. http://doi.org/10.1093/jme/tjx118
http://doi.org/10.1093/jme/tjx118...
; Olea et al., 2017Olea, M.S.; Patitucci, L.D.; Mariluis, J.C.; Alderete, M. & Mulieri, P.R. 2017. Assessment of sampling methods for sarcosaprophagous species and other guilds of Calyptratae (Diptera) in temperate forests of Southern South America. Journal of Medical Entomology, 54(2): 349-361. http://doi.org/10.1093/jme/tjw164
http://doi.org/10.1093/jme/tjw164...
). With regard to Muscidae, there are a number of inventories in Brazil, but unbalanced between the different Brazilian biomes and states. For example, while there is a voluminous literature on Muscidae for the States of Paraná and Rio de Janeiro (e.g.,Carvalho et al., 1984Carvalho, C.J.B. De; Almeida, J.R. & Jesus, C.B. 1984. Dípteros sinantrópicos de Curitiba e arredores (Paraná, Brasil). I: Muscidae. Revista Brasileira de Entomologia, 28(4): 551-560.; D’Almeida, 1991D’Almeida, J.M. 1991. Dípteros caliptrados (Muscidae e Anthomyiidae) da região metropolitana do Rio de Janeiro, RJ: II. Atratividade e freqüência sazonal. Revista Brasileira de Zoologia, 8: 7-16. http://doi.org/10.1590/S0101-81751991000100002
http://doi.org/10.1590/S0101-81751991000...
; Pamplona et al., 2000Pamplona, D.; Maia, V.C.; Couri, M.S.; Lamas, C.J.E. & Aires, C.D.C. 2000. A survey of Diptera on Paquetá Island, Rio de Janeiro, Brazil. Entomologist’s Monthly Magazine, 136(1632-1635): 169-175.; Oliveira et al., 2002Oliveira, V.D.; D’Almeida, J.M.; Paes, M.J. & Sanavria, A. 2002. Population dynamics of calyptrate Diptera (Muscidae and Sarcophagidae) at the Rio-Zoo foundation, Rio de Janeiro, RJ, Brazil. Brazilian Journal of Biology, 62(2): 191-196. http://doi.org/10.1590/S1519-69842002000200002
http://doi.org/10.1590/S1519-69842002000...
; Costacurta et al., 2003Costacurta, N.C.; Marinoni, R.C. & Carvalho, C.J.B. De. 2003. Fauna de Muscidae (Diptera) em três localidades do Estado do Paraná, Brasil, capturada por armadilha Malaise. Revista Brasileira de Entomologia, 47(3): 389-397. http://doi.org/10.1590/S0085-56262003000300005
http://doi.org/10.1590/S0085-56262003000...
; Couri & Carvalho, 2005Couri, M.S. & Carvalho, C.J.B. De. 2005. Diptera Muscidae do Estado do Rio de Janeiro (Brasil). Biota Neotropica, 5: 1-18. http://doi.org/10.1590/S1676-06032005000300015
http://doi.org/10.1590/S1676-06032005000...
; Leandro & D’Almeida, 2005Leandro, M.J. & D’Almeida, J.M. 2005. Levantamento de Calliphoridae, Fanniidae, Muscidae e Sarcophagidae em um fragmento de mata na Ilha do Governador, Rio de Janeiro, Brasil. Iheringia . Série Zoologia, 95(4): 377-381. http://doi.org/10.1590/S0073-47212005000400006
http://doi.org/10.1590/S0073-47212005000...
; Rodríguez-Fernández et al., 2006Rodríguez-Fernández, J.I.; Carvalho, C.J.B. De & Moura, M.O. 2006. Estrutura de assembléias de Muscidae (Diptera) no Paraná: uma análise por modelos nulos. Revista Brasileira de Entomologia, 50: 93-100. http://doi.org/10.1590/S0085-56262006000100014
http://doi.org/10.1590/S0085-56262006000...
; Couri & Barros, 2009Couri, M.S. & Barros, G.D.S. 2009. Muscidae (Diptera) of Rio de Janeiro State (Southeastern Brazil): inventory of species and notes on biology and distribution. Arquivos do Museu Nacional, 67(3-4): 189-206.), the most rich and populous Brazilian State remains with the Muscidae diversity knowledge still incipient. Furthermore, it is relatively scarce the Muscidae surveys in the Neotropics based on the use of non-baited collecting techniques (e.g.,Carvalho & Couri, 1991Carvalho, C.J.B. De & Couri, M.S. 1991. Muscidae, Fanniidae e Calliphoridae (Diptera) do Projeto Maracá, Roraima, Brasil. Acta Amazonica, 21: 35-43. http://doi.org/10.1590/1809-43921991211043
http://doi.org/10.1590/1809-439219912110...
; Costacurta et al., 2003Costacurta, N.C.; Marinoni, R.C. & Carvalho, C.J.B. De. 2003. Fauna de Muscidae (Diptera) em três localidades do Estado do Paraná, Brasil, capturada por armadilha Malaise. Revista Brasileira de Entomologia, 47(3): 389-397. http://doi.org/10.1590/S0085-56262003000300005
http://doi.org/10.1590/S0085-56262003000...
; Rodríguez-Fernández et al., 2006Rodríguez-Fernández, J.I.; Carvalho, C.J.B. De & Moura, M.O. 2006. Estrutura de assembléias de Muscidae (Diptera) no Paraná: uma análise por modelos nulos. Revista Brasileira de Entomologia, 50: 93-100. http://doi.org/10.1590/S0085-56262006000100014
http://doi.org/10.1590/S0085-56262006000...
; Krüger et al., 2010Krüger, R.F.; Carvalho, C.J.B. De & Ribeiro, P.B. 2010. Assembly rules in Muscid fly assemblages in the grasslands biome of Southern Brazil. Neotropical Entomology, 39(3): 345-353. http://doi.org/10.1590/S1519-566X2010000300006
http://doi.org/10.1590/S1519-566X2010000...
; Zafalon-Silva et al., 2018Zafalon-Silva, A.; Kirst, F.D. & Krüger, R.F. 2018. Houseflies speaking for the conservation of natural areas: a broad sampling of Muscidae (Diptera) on coastal plains of the Pampa biome, Southern Brazil. Revista Brasileira de Entomologia, 64(4): 292-303. http://doi.org/10.1016/j.rbe.2018.09.002
http://doi.org/10.1016/j.rbe.2018.09.002...
). The present study is the first exhaustive survey of Muscidae for the State of São Paulo based on non-baited collectings. Previous surveys focused on urban and/or cadaveric fauna (Linhares, 1981Linhares, A.X. 1981. Synanthropy of Muscidae, Fanniidae and Anthomyiidae (Diptera) in the city of Campinas, São Paulo, Brazil. Revista Brasileira de Entomologia, 25(4): 231-243.; Dias et al., 2014Dias, L.S.; Gabriel-Filho, L.R.A. & Guimarães, R.B. 2014. Avaliação do impacto do programa de coleta seletiva de lixo na frequência de Calliphoridae e Muscidae em Tupã, SP. Sociedade & Natureza, 26(1): 127-137. Available: http://www.seer.ufu.br/index.php/sociedadenatureza/article/view/22762.
http://www.seer.ufu.br/index.php/socieda...
; Cavallari et al., 2015Cavallari, M.L.; Baltazar, F.N.; Nihei, S.S.; Muñoz, D.R. & Tolezano, J.E. 2015. Dipterofauna associated with Sus scrofa Linné, 1758, carcasses in urban and coastal regions of São Paulo State, Brazil. Psyche: A Journal of Entomology, article ID 983980, 12p. http://doi.org/10.1155/2015/983980
http://doi.org/10.1155/2015/983980...
). In Brazil, 358 species are described and recorded, 156 of these occur in the State of São Paulo (Lowenberg-Neto & Carvalho, 2013Lowenberg-Neto, P. & Carvalho, C.J.B. De. 2013. Muscidae (Insecta: Diptera) of Latin America and the Caribbean: geographic distribution and check-list by country. Zootaxa, 3650: 1-147. http://doi.org/10.11646/zootaxa.3650.1.1
http://doi.org/10.11646/zootaxa.3650.1.1...
, with updates from Pereira-Colavite & Carvalho, 2012Pereira-Colavite, A. & Carvalho, C.J.B. De. 2012. Taxonomy of Neomuscina Townsend (Diptera, Muscidae) from Brazil. Zootaxa, 3504: 1-55. http://doi.org/10.11646/zootaxa.3504.1.1
http://doi.org/10.11646/zootaxa.3504.1.1...
; Cavallari et al., 2015Cavallari, M.L.; Baltazar, F.N.; Nihei, S.S.; Muñoz, D.R. & Tolezano, J.E. 2015. Dipterofauna associated with Sus scrofa Linné, 1758, carcasses in urban and coastal regions of São Paulo State, Brazil. Psyche: A Journal of Entomology, article ID 983980, 12p. http://doi.org/10.1155/2015/983980
http://doi.org/10.1155/2015/983980...
; Fogaça & Carvalho, 2018Fogaça, J.M. & Carvalho, C.J.B. de. 2018. Neotropical Lispe (Diptera: Muscidae): notes, redescriptions and key to species. Journal of Natural History, 52(33-34): 2147-2184. http://doi.org/10.1080/00222933.2018.1515380
http://doi.org/10.1080/00222933.2018.151...
). In this article we surveyed the Muscidae of the Biological Reserve Alto da Serra de Paranapiacaba (State of São Paulo, southeastern Brazil) in the Atlantic Forest biome, and analyzed its abundance, diversity and seasonality throughout a one-year collecting period. So far, only one muscid species had been recorded to the Biological Reserve of Paranapiacaba (Townsend, 1927Townsend, C.H.T. 1927. Synopse dos gêneros muscoideos da região humida tropical da America, com gêneros e espécies novas. Revista do Museu Paulista, 15: 203-385.; Lowenberg-Neto & Carvalho, 2013Lowenberg-Neto, P. & Carvalho, C.J.B. De. 2013. Muscidae (Insecta: Diptera) of Latin America and the Caribbean: geographic distribution and check-list by country. Zootaxa, 3650: 1-147. http://doi.org/10.11646/zootaxa.3650.1.1
http://doi.org/10.11646/zootaxa.3650.1.1...
).

MATERIAL AND METHODS

Study area and collection

This survey took place in the Biological Reserve Alto da Serra de Paranapiacaba (Fig. 1) (23°46′00″, 23°47′10″S; 46°18′20″, 46°20′40″W, 750-891 m of altitude), located in the municipality of Santo André, State of São Paulo, Brazil. The reserve is situated slightly under the Capricorn Tropic (23°27′S), in a transition area between the Tropical and the Subtropical climates zones (Gutjahr & Tavares, 2009Gutjahr, M.R. & Tavares, R. 2009. Clima. In: Lopes, M.I.M.S.; Kirizawa, M. & Mello, M.M.R.F. (Eds.). Patrimômio da Reserva Biológica Alto da Serra de Paranapiacaba. São Paulo, Instituto de Botânica. p. 41-51.). According to Köppen’s classification, the climate type is Cwa, temperate and humid, with dry winter and hot summer. The mean temperature at summer (December-March) is 20ºC, and 14ºC on winter (June-September), with temperature range of 6ºC (Gutjahr & Tavares, 2009Gutjahr, M.R. & Tavares, R. 2009. Clima. In: Lopes, M.I.M.S.; Kirizawa, M. & Mello, M.M.R.F. (Eds.). Patrimômio da Reserva Biológica Alto da Serra de Paranapiacaba. São Paulo, Instituto de Botânica. p. 41-51.). The area is predominantly covered with secondary Atlantic Forest under different successional stages, and that altered flora is due to historical anthropic intervention (Sugiyama et al., 2009Sugiyama, M.; Dos Santos, R.P.; Aguiar, L.S.J.; Kirizawa, M. & Catharino, E.L.M. 2009. Caracterização e Mapeamento da Vegetação. In: Lopes, M.I.M.S.; Kirizawa, M. & Mello, M.M.R.F. (Eds.). Patrimômio da Reserva Biológica Alto da Serra de Paranapiacaba. São Paulo, Instituto de Botânica. p. 41-51.), as this area is very close to São Paulo metropolitan area.

Figure 1
Location of the Biological Reserve Alto da Serra de Paranapiacaba, State of São Paulo, southeastern Brazil (23°46′00″, 23°47′10″S; 46°18′20″, 46°20′40″W, 750-891 m of altitude).

Insects were collected using Malaise traps, installed at three different point of the Reserve: trap 1 was located at 23°46′38″S, 46°18′42,7″W; trap 2 at 23°46′44.6″S, 46°18′40,2″W; and trap 3 at 23°46′45,7″S, 46°18′29,2″W. Traps were installed and material had been collected continuously from August 2010 to July 2011. Sampling vessels were replaced monthly, and the collected material taken to the lab for sorting and identification.

Identification

The specimens were recognized until the genera and species level, using identification keys in Carvalho (2002Carvalho, C.J.B. De. (Ed.). 2002. Muscidae (Diptera) of the Neotropical Region: Taxonomy. Editora Universidade Federal do Paraná, Curitiba, 287p.). When necessary, taxonomic revisions were consulted, containing updated identification keys and descriptions (e.g.,Pereira-Colavite & Carvalho, 2012Pereira-Colavite, A. & Carvalho, C.J.B. De. 2012. Taxonomy of Neomuscina Townsend (Diptera, Muscidae) from Brazil. Zootaxa, 3504: 1-55. http://doi.org/10.11646/zootaxa.3504.1.1
http://doi.org/10.11646/zootaxa.3504.1.1...
; Nihei & Carvalho, 2007Nihei, S.S. & Carvalho, C.J.B. DE. 2007. Phylogeny and classification of Muscini (Diptera, Muscidae). Zoological Journal of the Linnean Society, 149(4): 493-532. http://doi.org/10.1111/j.1096-3642.2007.00252.x
http://doi.org/10.1111/j.1096-3642.2007....
; among others). All studied material was pinned and, in most cases, males and/or females were dissected to study their terminalia, which were compared to drawings and descriptions in the literature. The dissected terminalia were cleared with 10% KOH solution, then neutralized with acetic acid solution and washed with water; after examination, they were stored in microvials with glycerine and pinned with the respective specimen. The material was deposited at the Museu de Zoologia, Universidade de São Paulo, São Paulo (MZSP).

Data analyses

Quantitative data were analyzed by calculating Shannon diversity and Berger-Parker dominance indexes (Magurran, 1988Magurran, A.E. 1988. Ecological diversity and Its measurement. Princeton, Princeton University Press, 179p. http://doi.org/10.1007/978-94-015-7358-0
http://doi.org/10.1007/978-94-015-7358-0...
) to compare the diversity and proportional abundance of species among the four stations of the year. These calculations were performed in the software DivEs v2.0 (Rodrigues, 2005Rodrigues, W.C. 2005. DivEs - Diversidade de espécies . Versão 2.0. Available: Available: http://www.ebras.bio.br/dives . Access: 21/05/2013.
http://www.ebras.bio.br/dives...
). To analyze the seasonality abundance in the four seasons of the year, we conducted the Kruskal-Wallis statistical test for non-parametric samples using the software Past version 2.17c (Hammer et al., 2001Hammer, O.; Harper, D.A.T. & Ryan, P.D. 2001. PAST: Paleontological statistics software package for education and data analysis. Palaeontologia Electronica, 4: 9p. Available: Available: http://palaeo-electronica.org/2001_1/past/issue1_01.htm . Access: 15/05/2013.
http://palaeo-electronica.org/2001_1/pas...
). We have applied a Kruskal-Wallis post-test called Bonferroni Correction, used to reduce the chances of obtaining false-positive results (type I errors) when several pairwise tests are made for one dataset (Nakagawa, 2004Nakagawa, S. 2004. A farewell to Bonferroni: the problems of low statistical power and publication bias. Behavioral Ecology, 15(6): 1044-1045. http://doi.org/10.1093/beheco/arh107
http://doi.org/10.1093/beheco/arh107...
).

The estimation of the number of species and extrapolation of this variable and their respective confidence intervals (95%) as a function of abundance was performed in R using the statistical package iNEXT (Hsieh et al., 2016Hsieh, T.C.; Ma, K.H. & Chao, A. 2016. iNEXT: An R package for rarefaction and extrapolation of species diversity (Hill numbers). Methods in Ecology and Evolution, 7(12): 1451-1456. http://doi.org/10.1111/2041-210X.12613
http://doi.org/10.1111/2041-210X.12613...
) based on the methodologies proposed by Colwell et al. (2012Colwell, R.K.; Chao, A.; Gotelli, N.J.; Lin, S.-Y.; Mao, C.X.; Chazdon, R.L. & Longino, J.T. 2012. Models and estimators linking individual-based and sample-based rarefaction, extrapolation and comparison of assemblages. Journal of Plant Ecology, 5: 3-21. http://doi.org/10.1093/jpe/rtr044
http://doi.org/10.1093/jpe/rtr044...
) and Chao et al. (2014Chao, A.; Gotelli, N.J.; Hsieh, T.C.; Sander, E.L.; Ma, K.H.; Colwell, R.K. & Ellison, A.M. 2014. Rarefaction and extrapolation with Hill numbers: a framework for sampling and estimation in species diversity studies. Ecological Monographs, 84: 45-67. http://doi.org/10.1890/13-0133.1
http://doi.org/10.1890/13-0133.1...
).

Collector curves were obtained for the Biological Reserve Alto da Serra de Paranapiacaba and for each seasonal season within the same area.

RESULTS

Within the one-year of Malaise trap collected material, seven families of Calyptrata were surveyed: Calliphoridae, Fanniidae, Mesembrinellidae, Muscidae, Rhinophoridae, Sarcophagidae and Tachinidae. Those seven families accounted a total of 3,451 individuals, with Muscidae as the most abundant, with 1,284 individuals (37%). Excluding the genera formerly belonging to “Coenosiinae” (sensuCarvalho et al., 2005Carvalho, C.J.B. De; Couri, M.S.; Pont, A.C.; Pamplona, D. & Lopes, S.M. 2005. A Catalogue of the Muscidae (Diptera) of the Neotropical Region. Zootaxa, 860: 1-282. http://doi.org/10.11646/zootaxa.860.1.1
http://doi.org/10.11646/zootaxa.860.1.1...
), the collected material of Muscidae was restricted to 397 individuals, and a total of 15 genera and 39 species of Muscidae were identified (Table 1 and Appendix) from the three subfamilies of Muscidae: Muscinae, Cyrtoneurininae and Mydaeinae (following the subfamilial classification sensuHaseyama et al., 2015Haseyama, K.L.; Wiegmann, B.M.; Almeida, E.A. & Carvalho, C.J.B. De. 2015. Say goodbye to tribes in the new house fly classification: a new molecular phylogenetic analysis and an updated biogeographical narrative for the Muscidae (Diptera). Molecular Phylogenetics and Evolution, 89: 1-12. http://doi.org/10.1016/j.ympev.2015.04.006
http://doi.org/10.1016/j.ympev.2015.04.0...
). Thirteen species are new records for the State of São Paulo: Dolichophaonia machadoi (Albuquerque, 1958), D. simplex (Albuquerque, 1958), Helina discreta (Wulp, 1896), H. gigantea Albuquerque, 1956, H. regobarrosi Albuquerque, 1958, Neomuscina anajeensisPereira-Colavite & Carvalho, 2012Pereira-Colavite, A. & Carvalho, C.J.B. De. 2012. Taxonomy of Neomuscina Townsend (Diptera, Muscidae) from Brazil. Zootaxa, 3504: 1-55. http://doi.org/10.11646/zootaxa.3504.1.1
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, N. transporta Snyder, 1949, Neurotrixa sulina Costacurta & Carvalho, 2005, Phaonia advena Snyder, 1957, P. annulata (Albuquerque, 1957), P. grandis (Couri, 1982), P. lentiginosa Snyder, 1957 and Polietina minor (Albuquerque, 1956). With this, the number of species of Muscidae known to occur in the State of São Paulo is increased to 169.

Table 1
Species of Muscidae (excluding “Coenosiinae”) from Biological Reserve Alto da Serra de Paranapiacaba with the number of individuals per season in the period August 2010 to July 2011. Asterisks indicate new records to State of São Paulo.

Quantitative data analysis reveals that the interval between November and February had both more individuals (Fig. 2) and more species (Fig. 3) collected. Those three-month period have a sequence of 60-55-56 individuals, while other months reached up to 36 individuals. For species number, we had a variation of 14 to 18 species. Shannon diversity index confirms summer with the highest diversity, followed by spring, autumn and winter (Table 2). On the other hand, Berger-Parker dominance shows summer with the lowest rate, followed by spring and autumn, and with winter with the highest rate. In Berger-Parker dominance, the lower the index the higher the dominance of such taxon (Table 2).

Figure 2
Number of individuals of Muscidae per month for the whole year of study.

Figure 3
Number of species of Muscidae per month for the whole year of study.

Table 2
Shannon diversity and Berger-Parker dominance indexes. The highest rates are highlighted in bold.

The estimated values of Chao for the richness of muscid species in the Biological Reserve was 65.009 ± 12.198. The Chao estimator is accurate in its lower limit and based on it, we can infer that about 52 species are expected in the area, seven more than the observed richness. This value can reach 105 species, which is an overestimate due to the 14 singletons (species with only one individual) (31.11%) (Table 3). There is also no trend towards stabilization of the collector curve (Fig. 4a), corroborating Chao’s analysis for the Biological Reserve.

Figure 4
Species accumulation curve based on the abundance of muscids captured with Malaise traps at the Biological Reserve Alto da Serra de Paranapiacaba, State of São Paulo. The solid line represents the observed richness of the collection and the dashed line the richness estimated by Chao 1. (A) corresponds to the estimates for the Reserve considering all collections. (B) corresponds to the estimates for each season of the year: spring (green), summer (blue), autumn (purple) and winter (red).

Table 3
Muscidae richness (Chao) from August 2010 to July 2011 at the Biological Reserve Alto da Serra de Paranapiacaba (ReBio) in São Paulo, Brazil. Observed values (Obs), estimated (est), standard error of the estimated values (SE), lower (LL) and upper (UL) limits of the estimated values.

Estimates of Muscidae richness for each season of the year, as well as their extrapolation, reveal interesting patterns of sampling effort for this conservation unit. In Table 3 we can see that there are higher values in the summer than in any other season, without a trend of stabilization in the collector curve for summer, spring and autumn, while in the winter the collections were sufficient (Fig. 4b).

The seasonality analysis using Kruskal-Wallis statistical test (Table 4) showed a seasonal pattern for the abundance of Muscidae throughout the year, with significative difference between the number of individuals distributed in the stations. The difference among the stations found at Kruskal-Wallis test was due to the abundance of individuals in the summer when compared to the winter and fall seasons. Furthermore, the circular analysis (Fig. 5) supported the seasonal variation of Muscidae indicating a clustered distribution (r = 0,913).

Figure 5
Circular representation of the number of collected individuals of Muscidae per month, for the whole year of study. Dark grey = rainy season; light grey = dry season. r = concentration index.

The five most abundant species (Fig. 6) were Phaonia grandis (28.17%), Cyrtoneuropsis maculipennis Macquart, 1843 (19.54%), Phaonia advena (13.45%), Cyrtoneuropsis polystigma (Wulp, 1896) (9.13%), and Phaonia lentiginosa (4,31%).

Figure 6
Relative frequency of 15 most abundant species of Muscidae sampled. The column “others” comprises 24 low abundant species.

Table 4
Pairwise Kruskal-Wallis analyses. Correction of Bonferroni are in gray color. Significative values are underlined.

DISCUSSION

In the Biological Reserve Alto da Serra de Paranapiacaba, only one muscid species, Philornis mima (Townsend, 1927Townsend, C.H.T. 1927. Synopse dos gêneros muscoideos da região humida tropical da America, com gêneros e espécies novas. Revista do Museu Paulista, 15: 203-385.), had been recorded so far (Townsend, 1927Townsend, C.H.T. 1927. Synopse dos gêneros muscoideos da região humida tropical da America, com gêneros e espécies novas. Revista do Museu Paulista, 15: 203-385.; Lowenberg-Neto & Carvalho, 2013Lowenberg-Neto, P. & Carvalho, C.J.B. De. 2013. Muscidae (Insecta: Diptera) of Latin America and the Caribbean: geographic distribution and check-list by country. Zootaxa, 3650: 1-147. http://doi.org/10.11646/zootaxa.3650.1.1
http://doi.org/10.11646/zootaxa.3650.1.1...
). With the 39 species found in the present survey, the Muscidae diversity of the Reserve is increased to a total of 40 species.

Malaise traps are efficient in collecting very active flying insects that can be intercepted by its tents, especially Hymenoptera and Diptera (Campos et al., 2000Campos, W.G.; Pereira, D.B.S. & Schoereder, J.H. 2000. Comparison of the efficiency of flight-interception trap models for sampling hymenoptera and other insects. Anais da Sociedade Entomológica do Brasil, 29(3): 381-389. http://doi.org/10.1590/S0301-80592000000300001
http://doi.org/10.1590/S0301-80592000000...
). In tropical rain forests of the Neotropical Region, Diptera is the most collected order when using Malaise traps (Dutra & Marinoni, 1994Dutra, R.R. & Marinoni, R.C. 1994. Insetos capturados com armadilha Malaise na Ilha do Mel, Baía de Paranaguá, Paraná, Brasil. I Composição de Ordens. Revista Brasileira de Zoologia, 11(2): 227-245. http://doi.org/10.1590/S0101-81751994000200006
http://doi.org/10.1590/S0101-81751994000...
; Brown, 2005Brown, B.V. 2005. Malaise trap catches and the crisis in neotropical Dipterology. American Entomologist, 51(3): 180-183. http://doi.org/10.1093/ae/51.3.180
http://doi.org/10.1093/ae/51.3.180...
). Costacurta et al. (2003Costacurta, N.C.; Marinoni, R.C. & Carvalho, C.J.B. De. 2003. Fauna de Muscidae (Diptera) em três localidades do Estado do Paraná, Brasil, capturada por armadilha Malaise. Revista Brasileira de Entomologia, 47(3): 389-397. http://doi.org/10.1590/S0085-56262003000300005
http://doi.org/10.1590/S0085-56262003000...
) and Rodríguez-Fernández et al. (2006Rodríguez-Fernández, J.I.; Carvalho, C.J.B. De & Moura, M.O. 2006. Estrutura de assembléias de Muscidae (Diptera) no Paraná: uma análise por modelos nulos. Revista Brasileira de Entomologia, 50: 93-100. http://doi.org/10.1590/S0085-56262006000100014
http://doi.org/10.1590/S0085-56262006000...
) analyzed the composition, species richness and abundance of Muscidae in six localities in Paraná State, southern Brazil in the Atlantic Forest biome, during one-year with Malaise traps. Krüger et al. (2010Krüger, R.F.; Carvalho, C.J.B. De & Ribeiro, P.B. 2010. Assembly rules in Muscid fly assemblages in the grasslands biome of Southern Brazil. Neotropical Entomology, 39(3): 345-353. http://doi.org/10.1590/S1519-566X2010000300006
http://doi.org/10.1590/S1519-566X2010000...
) surveyed four localities in southern Brazilian grasslands in the Pampa biome using a one-year Malaise traps collecting; and Zafalon-Silva et al. (2018Zafalon-Silva, A.; Kirst, F.D. & Krüger, R.F. 2018. Houseflies speaking for the conservation of natural areas: a broad sampling of Muscidae (Diptera) on coastal plains of the Pampa biome, Southern Brazil. Revista Brasileira de Entomologia, 64(4): 292-303. http://doi.org/10.1016/j.rbe.2018.09.002
http://doi.org/10.1016/j.rbe.2018.09.002...
) collected Muscidae in the 35 areas in the Coastal Plain of the Rio Grande do Sul State, southern Brazil. Borkent et al. (2018Borkent, A.; Brown, B.; Adler, P.H.; Amorim, D.S.; Barber, K.; Bickel, D.; Boucher, S.; Brooks, S.E.; Burger, J., Burington, Z.L.; Capellari, R.S.; Costa, D.N.R.; Cumming, J.M.; Curler, G.; Dick, C.W.; Epler, J.H.; Fisher, E.; Gaimari, S.D.; Gelhaus, J.; Grimaldi, D.A.; Hash, J.; Hauser, M.; Hippa, H.; Ibanez-Bernal, S.; Jaschhof, M.; Kameneva, E.P.; Kerr, P.H.; Korneyev, V.; Korytkowski, C.A.; Kung, G.-A.; Kvifte, G.M.; Lonsdale, O.; Marshall, S.A.; Mathis, W.N.; Michelsen, V.; Naglis, S.; Norrbom, A.L.; Paiero, S.; Pape, T.; Pereira-Colavite, A.; Pollet, M.; Rochefort, S.; Rung, A.; Runyon, J.B.; Savage, J.; Silva, V.C.; Sinclair, B.J.; Skevington, J.H.; Stireman, J.O.; Vilkamaa, P.; Wheeler, T.; Whitworth, T.; Wong, M.; Wood, D.M.; Woodley, N.; Yau, T; Zavortink, T.J. & Zumbado, M.A. 2018. Remarkable fly (Diptera) diversity in a patch of Costa Rican cloud forest: Why inventory is a vital science. Zootaxa, 4402: 53-90. http://doi.org/10.11646/zootaxa.4402.1.3
http://doi.org/10.11646/zootaxa.4402.1.3...
) surveyed three localities in the Costa Rican cloud forests using 13-month Malaise traps.

When considering the main surveys of Muscidae for southern Brazil (Rodríguez-Fernández et al., 2006Rodríguez-Fernández, J.I.; Carvalho, C.J.B. De & Moura, M.O. 2006. Estrutura de assembléias de Muscidae (Diptera) no Paraná: uma análise por modelos nulos. Revista Brasileira de Entomologia, 50: 93-100. http://doi.org/10.1590/S0085-56262006000100014
http://doi.org/10.1590/S0085-56262006000...
; Krüger et al., 2010Krüger, R.F.; Carvalho, C.J.B. De & Ribeiro, P.B. 2010. Assembly rules in Muscid fly assemblages in the grasslands biome of Southern Brazil. Neotropical Entomology, 39(3): 345-353. http://doi.org/10.1590/S1519-566X2010000300006
http://doi.org/10.1590/S1519-566X2010000...
; Zafalon-Silva et al., 2018Zafalon-Silva, A.; Kirst, F.D. & Krüger, R.F. 2018. Houseflies speaking for the conservation of natural areas: a broad sampling of Muscidae (Diptera) on coastal plains of the Pampa biome, Southern Brazil. Revista Brasileira de Entomologia, 64(4): 292-303. http://doi.org/10.1016/j.rbe.2018.09.002
http://doi.org/10.1016/j.rbe.2018.09.002...
), we observe that the richness in this family, disregarding the Coenosiinae, is 109 species for Paraná State (Rodríguez-Fernández et al., 2006Rodríguez-Fernández, J.I.; Carvalho, C.J.B. De & Moura, M.O. 2006. Estrutura de assembléias de Muscidae (Diptera) no Paraná: uma análise por modelos nulos. Revista Brasileira de Entomologia, 50: 93-100. http://doi.org/10.1590/S0085-56262006000100014
http://doi.org/10.1590/S0085-56262006000...
), 59 species for localities in the grasslands and south coast of Lagoa dos Patos (Krüger et al., 2010Krüger, R.F.; Carvalho, C.J.B. De & Ribeiro, P.B. 2010. Assembly rules in Muscid fly assemblages in the grasslands biome of Southern Brazil. Neotropical Entomology, 39(3): 345-353. http://doi.org/10.1590/S1519-566X2010000300006
http://doi.org/10.1590/S1519-566X2010000...
) and 63 species for the coastal plain of the Rio Grande do Sul (Zafalon-Silva et al., 2018Zafalon-Silva, A.; Kirst, F.D. & Krüger, R.F. 2018. Houseflies speaking for the conservation of natural areas: a broad sampling of Muscidae (Diptera) on coastal plains of the Pampa biome, Southern Brazil. Revista Brasileira de Entomologia, 64(4): 292-303. http://doi.org/10.1016/j.rbe.2018.09.002
http://doi.org/10.1016/j.rbe.2018.09.002...
), values that are 31 to 132% higher than that found for Biological Reserve of Paranapiacaba. It is worth mentioning that the morphospecies richness values are also much higher than those found here, varying from 23% of the fauna in Krüger et al. (2010Krüger, R.F.; Carvalho, C.J.B. De & Ribeiro, P.B. 2010. Assembly rules in Muscid fly assemblages in the grasslands biome of Southern Brazil. Neotropical Entomology, 39(3): 345-353. http://doi.org/10.1590/S1519-566X2010000300006
http://doi.org/10.1590/S1519-566X2010000...
) to 38% in Rodríguez-Fernández et al. (2006Rodríguez-Fernández, J.I.; Carvalho, C.J.B. De & Moura, M.O. 2006. Estrutura de assembléias de Muscidae (Diptera) no Paraná: uma análise por modelos nulos. Revista Brasileira de Entomologia, 50: 93-100. http://doi.org/10.1590/S0085-56262006000100014
http://doi.org/10.1590/S0085-56262006000...
), while in this work only four species were not nominally identified (8.89%). Therefore, when disregarding morphospecies, the richness in the Biological Reserve of Paranapiacaba was of 41 species, values close to those found by Krüger et al. (2010Krüger, R.F.; Carvalho, C.J.B. De & Ribeiro, P.B. 2010. Assembly rules in Muscid fly assemblages in the grasslands biome of Southern Brazil. Neotropical Entomology, 39(3): 345-353. http://doi.org/10.1590/S1519-566X2010000300006
http://doi.org/10.1590/S1519-566X2010000...
) and Zafalon-Silva et al. (2018Zafalon-Silva, A.; Kirst, F.D. & Krüger, R.F. 2018. Houseflies speaking for the conservation of natural areas: a broad sampling of Muscidae (Diptera) on coastal plains of the Pampa biome, Southern Brazil. Revista Brasileira de Entomologia, 64(4): 292-303. http://doi.org/10.1016/j.rbe.2018.09.002
http://doi.org/10.1016/j.rbe.2018.09.002...
), 45 and 42 species, respectively. In Paraná, the richness was of 67 species (Rodríguez-Fernández et al., 2006Rodríguez-Fernández, J.I.; Carvalho, C.J.B. De & Moura, M.O. 2006. Estrutura de assembléias de Muscidae (Diptera) no Paraná: uma análise por modelos nulos. Revista Brasileira de Entomologia, 50: 93-100. http://doi.org/10.1590/S0085-56262006000100014
http://doi.org/10.1590/S0085-56262006000...
), remaining 63% higher than in Paranapiacaba. The collections carried out at the Biological Reserve of Paranapiacaba used traps that were placed close to each other (separated by hundreds of meters), and this may explain the much higher values in Paraná, where the collections were carried out in almost the entire State (separated by hundreds of kilometers). Nevertheless, we can estimate a great richness for Muscidae in the Atlantic Forest of São Paulo State, since in a reduced area as the Biological Reserve of Paranapiacaba, the richness found was to similar to that found in areas of much larger collections as Rio Grande do Sul, wherein sampled localities were separated by dozens of kilometers. In fact, the Chao estimate in Table 3 extrapolates more species to be collected at Paranapiacaba and, in this case, we can consider estimates higher than the estimated one. Thus, the curve of the collector is still increasing for this area.

Interestingly, the fauna found in the Biological Reserve of Paranapiacaba is more similar to the fauna of Paraná, sharing 31.71% of the species, while only 8% of Paranapiacaba species were also observed in Rio Grande do Sul and in Paraná. However, none of those shared species occurs either in the Coastal Plain of RS or in the Sul-rio-grandense Shield. And ten species (24.4%) occur in all these locations and have a wide distribution in Brazil.

The seasonal pattern of Muscidae showed the family individuals more abundant on summer, based on Kruskal-Wallis statistical test (Table 4) and circular analysis (Fig. 5). Previous studies have demonstrated that tropical insect abundance decreases in the dry season (e.g.,Pinheiro et al., 2002Pinheiro, F.; Diniz, I.R.; Coelho, D. & Bandeira, M.P.S. 2002. Seasonal pattern of insect abundance in the Brazilian cerrado. Austral Ecology, 27(2): 132-136. http://doi.org/10.1046/j.1442-9993.2002.01165.x
http://doi.org/10.1046/j.1442-9993.2002....
; Da Silva et al., 2011Da Silva, N.P.P.; Frizzas, M.R. & De Oliveira, C.M. 2011. Seasonality in insect abundance in the “Cerrado” of Goiás State, Brazil. Revista Brasileira de Entomologia, 55: 79-87. http://doi.org/10.1590/S0085-56262011000100013
http://doi.org/10.1590/S0085-56262011000...
), but far less than in temperate zones (Wolda, 1988Wolda, H. 1988. Insect seasonality: Why? Annual Review of Ecology, Evolution and Systematics, 19: 1-18. http://doi.org/10.1146/annurev.es.19.110188.000245
http://doi.org/10.1146/annurev.es.19.110...
). The pairwise test comparing summer and spring resulted in a statistically relevant difference, but after Bonferroni Correction, this difference was not considered statistically significant (Table 4). On the other hand, Bonferroni tests confirmed seasonal pattern of Muscidae with high abundance in the summer and less in autumn and winter.

Da Silva et al. (2011Da Silva, N.P.P.; Frizzas, M.R. & De Oliveira, C.M. 2011. Seasonality in insect abundance in the “Cerrado” of Goiás State, Brazil. Revista Brasileira de Entomologia, 55: 79-87. http://doi.org/10.1590/S0085-56262011000100013
http://doi.org/10.1590/S0085-56262011000...
) and Pinheiro et al. (2002Pinheiro, F.; Diniz, I.R.; Coelho, D. & Bandeira, M.P.S. 2002. Seasonal pattern of insect abundance in the Brazilian cerrado. Austral Ecology, 27(2): 132-136. http://doi.org/10.1046/j.1442-9993.2002.01165.x
http://doi.org/10.1046/j.1442-9993.2002....
) performed seasonal analyses for insect abundance in the Brazilian Cerrado (savannah) and found that most insect orders (Coleoptera, Hymenoptera, Hemiptera, Isoptera, etc.) showed a clustered distribution, being more abundant in the wet season. However, in both studies, the order Diptera was randomly distributed, contrary to the results observed here and focused on Muscidae. This could be related to the groups studied in each case, revealing perhaps the most abundant groups of Diptera might be equally distributed the whole year, while Muscidae might be more vulnerable to environmental and/or biotic conditions that affect their abundance. Moreover, these studies were performed in different biomes other than Atlantic Forest. Traditionally, Cerrado is characterized by a bimodal rainfall distribution, with two well-defined, dry and wet, seasons (Silva et al., 2008Silva, F.A.M.; Assad, E.A. & Evangelista, B.A. 2008. Caracterização climática do bioma Cerrado. In: Sano, S.M.; Almeida, S.P. & Ribeiro, J.F. (Eds.). Cerrado: ecologia e flora. Brasília, EMBRAPA Informação Tecnológica. p. 69-88.), whereas Atlantic Forest is characterized by having high temperature and precipitation during the whole year (IBGE, 1992Instituto Brasileiro de Geografia e Estatística (IBGE). 1992. Manual técnico da vegetação brasileira. Rio de Janeiro, IBGE. 92p.). However, climatic studies in Paranapiacaba have demonstrated that precipitation suffers a decrease in December and January (Gutjahr & Tavares, 2009Gutjahr, M.R. & Tavares, R. 2009. Clima. In: Lopes, M.I.M.S.; Kirizawa, M. & Mello, M.M.R.F. (Eds.). Patrimômio da Reserva Biológica Alto da Serra de Paranapiacaba. São Paulo, Instituto de Botânica. p. 41-51.), when Muscidae reached its peaks in both abundance and diversity. Unfortunately, there are just a few studies with seasonality of Neotropical muscids. Using fruit-baited traps, Azevedo et al. (2015Azevedo, F.R.; Azevedo, R.; Dos Santos, C.A.M.; Moura, E.S. & Nere, D.R. 2015. Análise Faunística e Flutuação Populacional da Dipterofauna de Ecossistemas da Área de Proteção Ambiental do Araripe, Barbalha, CE. EntomoBrasilis, 8: 117-124. http://doi.org/10.12741/ebrasilis.v8i2.423
http://doi.org/10.12741/ebrasilis.v8i2.4...
) found the muscids much less abundant in the rainy season in Barbalha municipality (State of Ceará, northeastern Brazil), characterized by Cerrado (savannah) and Caatinga (semi-arid) vegetations. Results of Costacurta et al. (2003Costacurta, N.C.; Marinoni, R.C. & Carvalho, C.J.B. De. 2003. Fauna de Muscidae (Diptera) em três localidades do Estado do Paraná, Brasil, capturada por armadilha Malaise. Revista Brasileira de Entomologia, 47(3): 389-397. http://doi.org/10.1590/S0085-56262003000300005
http://doi.org/10.1590/S0085-56262003000...
) in three localities of State of Paraná (southern Brazil) also supports the correlation between Muscidae abundance and air humidity: the lower the humidity, the higher the abundance. However, as pointed out by Azevedo & Krüger (2013Azevedo, R.R. & Krüger, R.F. 2013. The influence of temperature and humidity on abundance and richness of Calliphoridae (Diptera). Iheringia . Série Zoologia, 103(2): 145-152. http://doi.org/10.1590/S0073-47212013000200010
http://doi.org/10.1590/S0073-47212013000...
) for southern Brazilian calliphorids, each species may respond differently (even inversely) to temperature and humidity interactions, therefore, it demands a careful examination on the species other than all the family.

The Paranapiacaba Reserve is covered by secondary Atlantic Forest under different successional stages (Sugiyama et al., 2009Sugiyama, M.; Dos Santos, R.P.; Aguiar, L.S.J.; Kirizawa, M. & Catharino, E.L.M. 2009. Caracterização e Mapeamento da Vegetação. In: Lopes, M.I.M.S.; Kirizawa, M. & Mello, M.M.R.F. (Eds.). Patrimômio da Reserva Biológica Alto da Serra de Paranapiacaba. São Paulo, Instituto de Botânica. p. 41-51.). The composition of the Muscidae fauna from the Paranapiacaba Reserve comprises mostly tipically forest species, however there is a number of species with some degree of synanthropic habits. Within its 39 species, only two species, Myospila meditabunda (Fabricius, 1781) and Synthesiomyia nudiseta (Wulp, 1883), are considered tipically synanthropic (Carvalho et al., 2005Carvalho, C.J.B. De; Couri, M.S.; Pont, A.C.; Pamplona, D. & Lopes, S.M. 2005. A Catalogue of the Muscidae (Diptera) of the Neotropical Region. Zootaxa, 860: 1-282. http://doi.org/10.11646/zootaxa.860.1.1
http://doi.org/10.11646/zootaxa.860.1.1...
; Lowenberg-Neto & Carvalho, 2013Lowenberg-Neto, P. & Carvalho, C.J.B. De. 2013. Muscidae (Insecta: Diptera) of Latin America and the Caribbean: geographic distribution and check-list by country. Zootaxa, 3650: 1-147. http://doi.org/10.11646/zootaxa.3650.1.1
http://doi.org/10.11646/zootaxa.3650.1.1...
). In Colombia, S. nudiseta was classified as having “strong preference for dense human settlements” (Uribe et al., 2010Uribe, N.; Wolff, M. & De Carvalho, C.J.B. De. 2010. Synanthropy and ecological aspects of Muscidae (Diptera) in a tropical dry forest ecosystem in Colombia. Revista Brasileira de Entomologia, 54(3): 462-470. http://doi.org/10.1590/S0085-56262010000300018
http://doi.org/10.1590/S0085-56262010000...
), and in Brazil we have it recorded in rural and urban environments and forest fragments (D’Almeida & Almeida, 1998D’Almeida, J.M. & Almeida, J.D. 1998. Nichos tróficos em dípteros caliptrados, no Rio de Janeiro, RJ. Revista Brasileira de Biologia, 58(4): 563-570. http://doi.org/10.1590/S0034-71081998000400004
http://doi.org/10.1590/S0034-71081998000...
). Besides, seven species found in Paranapiacaba have some association to human inhabited areas in Brazil: Cyrtoneuropsis maculipennis, C. polystigma, Morellia humeralis (Stein, 1919), Mydaea plaumanni Snyder, 1941, Phaonia trispila (Bigot, 1885), Pseudoptilolepis fulvapoda Snyder, 1949 and Psilochaeta pampiana (Shannon & Del Ponte, 1926) (Linhares, 1981Linhares, A.X. 1981. Synanthropy of Muscidae, Fanniidae and Anthomyiidae (Diptera) in the city of Campinas, São Paulo, Brazil. Revista Brasileira de Entomologia, 25(4): 231-243.; Carvalho et al., 1984Carvalho, C.J.B. De; Almeida, J.R. & Jesus, C.B. 1984. Dípteros sinantrópicos de Curitiba e arredores (Paraná, Brasil). I: Muscidae. Revista Brasileira de Entomologia, 28(4): 551-560.; Oliveira, 1986Oliveira, G.P. 1986. Distribuição sazonal de dípteros muscóides sinantrópicos, simbovinos e foréticos de Dermatobia hominis L. Jr. em São Carlos, Estado de São Paulo. I. Estábulo. Arquivo de Biologia e Tecnologia, 29(2): 311-325.; Kasai et al., 1990Kasai, N.; Schumaker, T.T.S.; Dell’Porto, A. & La Salvia, V. 1990. Variação sazonal de dípteros capturados em armadilhas de Magoon modificada, em Santana do Parnaíba, Estado de São Paulo. Revista Brasileira de Entomologia, 34(2): 369-380.; Lomônaco & Almeida, 1995Lomônaco, C. & Almeida J.R. 1995. Sazonalidade e uso de recursos para alimentação e oviposição de dípteros muscóideos na restinga de Jacarepaguá, Rio de Janeiro, Brasil. Revista Brasileira de Entomologia, 39(4): 883-890.; Moura et al., 1997Moura, M.O.; Carvalho, C.J.B. De & Monteiro-Filho, E.L. 1997. A preliminary analysis of insects of medico-legal importance in Curitiba, State of Paraná. Memórias do Instituto Oswaldo Cruz, 92(2): 269-274. http://doi.org/10.1590/S0074-02761997000200023
http://doi.org/10.1590/S0074-02761997000...
; Pamplona et al., 2000Pamplona, D.; Maia, V.C.; Couri, M.S.; Lamas, C.J.E. & Aires, C.D.C. 2000. A survey of Diptera on Paquetá Island, Rio de Janeiro, Brazil. Entomologist’s Monthly Magazine, 136(1632-1635): 169-175.; Carvalho et al., 2002Carvalho, C.J.B. De; Moura, M.O. & Ribeiro, P.B. 2002. Chave para adultos de dípteros (Muscidae, Fanniidae, Anthomyiidae) associados ao ambiente humano no Brasil. Revista Brasileira de Entomologia, 46(2): 107-144. http://doi.org/10.1590/S0085-56262002000200001
http://doi.org/10.1590/S0085-56262002000...
; Barbosa et al., 2009Barbosa, R.R.; Mello-Patiu, C.A.; Mello, R.P. & Queiroz, M.M.C. 2009. New records of calyptrate dipterans (Fanniidae, Muscidae and Sarcophagidae) associated with the decomposition of domestic pigs in Brazil. Memórias do Instituto Oswaldo Cruz, 104(6): 923-926. http://doi.org/10.1590/S0074-02762009000600018
http://doi.org/10.1590/S0074-02762009000...
). And Cyrtoneuropsis polystigma was also considered symbovine (Oliveira, 1986Oliveira, G.P. 1986. Distribuição sazonal de dípteros muscóides sinantrópicos, simbovinos e foréticos de Dermatobia hominis L. Jr. em São Carlos, Estado de São Paulo. I. Estábulo. Arquivo de Biologia e Tecnologia, 29(2): 311-325.). However, some species have contrasting information, for example, in Colombia (Uribe et al., 2010Uribe, N.; Wolff, M. & De Carvalho, C.J.B. De. 2010. Synanthropy and ecological aspects of Muscidae (Diptera) in a tropical dry forest ecosystem in Colombia. Revista Brasileira de Entomologia, 54(3): 462-470. http://doi.org/10.1590/S0085-56262010000300018
http://doi.org/10.1590/S0085-56262010000...
), C. maculipennis is classified as a species with “complete avoidance of human settlements”, as well as Polietina orbitalis (Stein, 1904).

The occurrence of exotic and/or synanthropic species in natural preserved areas has been associated to edge effect by some authors (Lima-Ribeiro, 2008Lima-Ribeiro, M.S. 2008. Efeitos de borda sobre a vegetação e estruturação populacional em fragmentos de Cerradão no Sudoeste Goiano, Brasil. Acta Botanica Brasilica, 22(2): 535-545. http://doi.org/10.1590/S0102-33062008000200020
http://doi.org/10.1590/S0102-33062008000...
; Ferraz et al., 2010Ferraz, A.C.P.; Gadelha, B.Q. & Aguiar-Coelho, V.M. 2010. Effects of forest fragmentation on dipterofauna (Calliphoridae) at the Reserva Biológica do Tinguá, Nova Iguaçu, RJ. Brazilian Journal of Biology, 70: 55-63. http://doi.org/10.1590/S1519-69842010000100009
http://doi.org/10.1590/S1519-69842010000...
; Barbosa et al., 2014Barbosa, L.S.; Cunha, A.M.; Couri, M.S. & Maia, V.C. 2014. Muscidae, Sarcophagidae, Calliphoridae e Mesembrinellidae (Diptera) da Estação Biológica de Santa Lúcia (Santa Teresa, Espírito Santo, Brasil). Boletim do Museu Biológico Mello Leitão, 33: 131-140.). Furthermore, the complex composition of the Muscidae fauna in the Biological Reserve of Paranapiacaba reveals that while this Reserve still bears most of its fauna with typically forest species, the presence of some typically synanthropic species may signalize that its proximity to São Paulo metropolitan area has imposed an increasing anthropic pressure (Leandro & D’Almeida, 2005Leandro, M.J. & D’Almeida, J.M. 2005. Levantamento de Calliphoridae, Fanniidae, Muscidae e Sarcophagidae em um fragmento de mata na Ilha do Governador, Rio de Janeiro, Brasil. Iheringia . Série Zoologia, 95(4): 377-381. http://doi.org/10.1590/S0073-47212005000400006
http://doi.org/10.1590/S0073-47212005000...
).

ACKNOWLEDGMENTS

We thank Filipe Gudin for helping with the material sorting; Filipe Gudin, Julia Calhau, Marcos Ribeiro, Mayra Sato, Nelly Araya, Rodrigo Dios and Pedro Souza-Dias for helping in the collecting, and Julia Benetti, Glauco Machado and Daniel Caetano for suggestions on earlier versions. We also thank the financial support from FAPESP with research grant (Proc. № 2007/50836-7 for SSN) and scholarships (Proc. № 2007/52314-7 for ATT and 2010/07185-8 for PM) and CNPq research grant (Proc. № 562199/2010-1 for SSN), scholarship (Proc. № 107159/2011-2 for ATT) and fellowship (Proc. № 309192/2018-8 for SSN).

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APPENDIX: LIST OF EXAMINED MATERIAL

The species are listed in alphabetical order. Asterisk indicates new records to State of São Paulo. All material deposited at the Museu de Zoologia, Universidade de São Paulo, Brazil (MZSP).

Cyrtoneurina alifusca Couri, 1982: 1 male, 21.x-19.xi.2010, Gudin & Nihei col.; 1 male, 19.xi-21.xii.2010, Gudin, Araya & Nihei col.; 3 males, 21.xii.2010-21.i.2011, Sato & Nihei col.; 2 males, 21.i-22.ii.2011, Gudin & Dios col.

Cyrtoneurina costalis (Walker, 1853): 1 male, 22.iii-19.iv.2011, Moll & Nihei col.

Cyrtoneuropsis maculipennis Macquart, 1843: 1 female, 21.vii-21.viii.2010, Moll & Nihei col.; 2 males, 1 female, 21.viii-21.ix.2010, Gudin & Nihei col.; 3 females, 21.ix-21.x.2010, Dios & Nihei col.; 1 male, 4 females, 21.x-19.xi.2010, Gudin & Nihei col.; 1 male, 13 females, 19.xi-21.xii.2010, Gudin, Araya & Nihei col.; 1 male, 8 females, 21.xii.2010-21.i.2011, Sato & Nihei col.; 3 males, 13 females, 21.i-22.ii.2011, Gudin & Dios col.; 6 females, 23.ii-21.iii.2011, Moll, Nihei & Dias col.; 1 male, 3 females, 22.iii-19.iv.2011, Moll & Nihei col.; 2 males, 6 females, 19.iv-23.v.2011, Moll & Gudin col.; 3 females, 23.v-20.vi.2011, Moll, Almeida & Tamakoshi col.; 2 males, 1 female, 20.vi-23.vii.2011, Moll, Tamakoshi, Ribeiro col.

Cyrtoneuropsis polystigma (Wulp, 1896): 1 female, 21.vii-21.viii.2010, Moll & Nihei col.; 2 males, 21.viii-21.ix.2010, Gudin & Nihei col.; 4 males, 2 females, 21.ix-21.x.2010, Dios & Nihei col.; 2 males, 4 females, 21.x-19.xi.2010, Gudin & Nihei col.; 5 males, 4 females, 19.xi-21.xii.2010, Gudin, Araya & Nihei col.; 4 males, 1 female, 21.xii.2010-21.i.2011, Sato & Nihei col.; 3 males, 4 females, 21.i-22.ii.2011, Gudin & Dios col.

Dolichophaonia machadoi (Albuquerque, 1958)*: 4 females, 21.vii-21.viii.2010, Moll & Nihei col.; 2 females, 21.viii-21.ix.2010, Gudin & Nihei col.; 4 females, 21.x-19.xi.2010, Gudin & Nihei col.; 2 females, 19.xi-21.xii.2010, Gudin, Araya & Nihei col.; 1 female, 21.i-22.ii.2011, Gudin & Dios col.; 1 female, 19.iv-23.v.2011, Moll & Gudin col.; 1 female, 20.vi-23.vii.2011, Moll, Tamakoshi, Ribeiro col.

Dolichophaonia simplex (Albuquerque, 1958)*: 1 female, 21.viii-21.ix.2010, Gudin & Nihei col.

Helina aff. discreta (Wulp, 1896)*: 3 females, 21.xii.2010-21.i.2011, Sato & Nihei col.; 1 female, 23.ii-21.iii.2011, Moll, Nihei & Dias col.

Helina gigantea Albuquerque, 1956*: 2 females, 21.x-19.xi.2010, Gudin & Nihei col.

Helina praecipua (Walker, 1853): 1 male, 23.v-20.vi.2011, Moll, Almeida & Tamakoshi col.

Helina regobarrosi Albuquerque, 1958*: 1 male, 19.xi-21.xii.2010, Gudin, Araya & Nihei col.; 1 female, 21.xii.2010-21.i.2011, Sato & Nihei col.; 1 female, 21.i-22.ii.2011, Gudin & Dios col.

Morellia humeralis (Stein, 1919): 1 female, 21.i-22.ii.2011, Gudin & Dios col.

Morellia nigricosta Hough, 1900: 3 females, 21.i-22.ii.2011, Gudin & Dios col.

Mydaea plaumanni Snyder, 1941: 1 female, 21.ix-21.x.2010, Dios & Nihei col.; 3 females, 21.xii.2010-21.i.2011, Sato & Nihei col.; 1 female, 19.iv-23.v.2011, Moll & Gudin col.; 1 female, 23.v-20.vi.2011, Moll, Almeida & Tamakoshi col.; 2 females, 20.vi-23.vii.2011, Moll, Tamakoshi, Ribeiro col.

Myospila meditabunda (Fabricius, 1781): 1 female, 21.x-19.xi.2010, Gudin & Nihei col.; 1 female, 19.xi-21.xii.2010, Gudin, Araya & Nihei col.

Neomuscina anajeensis Pereira-Colavite & Carvalho 2012*: 1 female, 21.x-19.xi.2010, Gudin & Nihei col.

Neomuscina atincticosta Snyder, 1949: 1 male, 21.xii.2010-21.i.2011, Sato & Nihei col.

Neomuscina inflexa (Stein, 1918): 2 females, 21.xii.2010-21.i.2011, Sato & Nihei col.

Neomuscina neosimilis Snyer, 1949: 1 female, 19.xi-21.xii.2010, Gudin, Araya & Nihei col.; 1 female, 21.xii.2010-21.i.2011, Sato & Nihei col.

Neomuscina schadei Snyder, 1949: 1 female, 23.ii-21.iii.2011, Moll, Nihei & Dias col.

Neomuscina transporta Snyder, 1949*: 1 female, 21.x-19.xi.2010, Gudin & Nihei col.

Neurotrixa sulina Costacurta & Carvalho, 2005*: 1 female, 19.xi-21.xii.2010, Gudin, Araya & Nihei col.

Phaonia advena Snyder, 1957*: 2 females, 21.vii-21.viii.2010, Moll & Nihei col.; 2 males, 7 females, 21.viii-21.ix.2010, Gudin & Nihei col.; 3 females, 21.ix-21.x.2010, Dios & Nihei col.; 1 male, 5 females, 21.x-19.xi.2010, Gudin & Nihei col.; 1 male, 13 females, 19.xi-21.xii.2010, Gudin, Araya & Nihei col.; 5 females, 21.xii.2010-21.i.2011, Sato & Nihei col.; 1 male, 21.i-22.ii.2011, Gudin & Dios col.; 4 females, 23.ii-21.iii.2011, Moll, Nihei & Dias col.; 2 females, 22.iii-19.iv.2011, Moll & Nihei col.; 6 females, 19.iv-23.v.2011, Moll & Gudin col.; 1 female, 23.v-20.vi.2011, Moll, Almeida & Tamakoshi col.; 2 females, 20.vi-23.vii.2011, Moll, Tamakoshi, Ribeiro col.

Phaonia annulata (Albuquerque, 1957)*: 1 female, 21.xii.2010-21.i.2011, Sato & Nihei col.; 1 male, 19.iv-23.v.2011, Moll & Gudin col.

Phaonia grajauensis (Albuquerque, 1957): 2 female, 21.xii.2010-21.i.2011, Sato & Nihei col.

Phaonia grandis (Couri, 1982)*: 1 male, 12 females, 21.vii-21.viii.2010, Moll & Nihei col.; 3 males, 9 females, 21.viii-21.ix.2010, Gudin & Nihei col.; 1 male, 6 females, 21.ix-21.x.2010, Dios & Nihei col.; 5 females, 21.x-19.xi.2010, Gudin & Nihei col.; 11 females, 19.xi-21.xii.2010, Gudin, Araya & Nihei col.; 1 male, 4 females, 21.xii.2010-21.i.2011, Sato & Nihei col.; 3 males, 13 females, 21.i-22.ii.2011, Gudin & Dios col.; 1 male, 5 females, 23.ii-21.iii.2011, Moll, Nihei & Dias col.; 2 male, 5 females, 22.iii-19.iv.2011, Moll & Nihei col.; 1 male, 11 females, 19.iv-23.v.2011, Moll & Gudin col.; 8 females, 23.v-20.vi.2011, Moll, Almeida & Tamakoshi col.; 2 males, 6 females, 20.vi-23.vii.2011, Moll, Tamakoshi, Ribeiro col.

Phaonia lentiginosa Snyder 1957*: 2 males, 21.vii-21.viii.2010, Moll & Nihei col.; 1 female, 21.viii-21.ix.2010, Gudin & Nihei col.; 1 female, 21.ix-21.x.2010, Dios & Nihei col.; 3 females, 21.x-19.xi.2010, Gudin & Nihei col.; 1 male, 5 females, 21.xii.2010-21.i.2011, Sato & Nihei col.; 1 female, 21.i-22.ii.2011, Gudin & Dios col.; 1 female, 22.iii-19.iv.2011, Moll & Nihei col.; 2 females, 19.iv-23.v.2011, Moll & Gudin col.

Phaonia shannoni (Carvalho & Pont, 1993): 1 female, 21.vii-21.viii.2010, Moll & Nihei col.; 1 female, 21.viii-21.ix.2010, Gudin & Nihei col.; 1 female, 21.i-22.ii.2011, Gudin & Dios col.; 1 female, 20.vi-23.vii.2011, Moll, Tamakoshi, Ribeiro col.

Phaonia similata (Albuquerque, 1957): 1 female, 21.viii-21.ix.2010, Gudin & Nihei col.

Phaonia trispila (Bigot, 1885): 1 male, 1 female, 23.v-20.vi.2011, Moll, Almeida & Tamakoshi col.

Philornis amazonenses Couri, 1983: 1 female, 21.viii-21.ix.2010, Gudin & Nihei col.; 1 female, 21.i-22.ii.2011, Gudin & Dios col.

Polietina minor (Albuquerque, 1956)*: 1 female, 21.i-22.ii.2011, Gudin & Dios col.

Polietina orbitalis (Stein, 1904): 1 female, 19.xi-21.xii.2010, Gudin, Araya & Nihei col.

Polietina prima (Couri & Machado, 1990): 2 females, 21.xii.2010-21.i.2011, Sato & Nihei col.; 1 female, 21.i-22.ii.2011, Gudin & Dios col.; 2 females, 23.ii-21.iii.2011, Moll, Nihei & Dias col.; 1 male, 22.iii-19.iv.2011, Moll & Nihei col.; 1 female, 19.iv-23.v.2011, Moll & Gudin col.

Polietina steini (Enderlein, 1927): 2 females, 19.xi-21.xii.2010, Gudin, Araya & Nihei col.

Polietina univittata Couri & Carvalho, 1996: 1 female, 19.xi-21.xii.2010, Gudin, Araya & Nihei col.; 2 females, 21.i-22.ii.2011, Gudin & Dios col.; 1 female, 23.ii-21.iii.2011, Moll, Nihei & Dias col.

Pseudoptilolepis fulvapoda Snyder, 1949: 2 females, 21.viii-21.ix.2010, Gudin & Nihei col.; 3 females, 21.ix-21.x.2010, Dios & Nihei col.; 1 female, 21.x-19.xi.2010, Gudin & Nihei col.; 1 female, 19.xi-21.xii.2010, Gudin, Araya & Nihei col.; 1 male, 1 female, 21.xii.2010-21.i.2011, Sato & Nihei col.; 1 female, 21.i-22.ii.2011, Gudin & Dios col.; 1 female, 23.ii-21.iii.2011, Moll, Nihei & Dias col.; 1 female, 20.vi-23.vii.2011, Moll, Tamakoshi, Ribeiro col.

Pseudoptilolepis nudapleura Snyder, 1949: 1 female, 21.xii.2010-21.i.2011, Sato & Nihei col.

Psilochaeta pampiana (Shannon & Del Ponte, 1926): 1 male, 19.xi-21.xii.2010, Gudin, Araya & Nihei col.; 1 male, 21.xii.2010-21.i.2011, Sato & Nihei col.

Synthesiomyia nudiseta (Wulp, 1883): 1 female, 23.ii-21.iii.2011, Moll, Nihei & Dias col.

Edited by

Carlos José Einicker Lamas

Publication Dates

  • Publication in this collection
    17 Sept 2021
  • Date of issue
    2021

History

  • Received
    07 May 2021
  • Accepted
    26 May 2021
  • Published
    30 July 2021
Museu de Zoologia da Universidade de São Paulo Av. Nazaré, 481, Ipiranga, 04263-000 São Paulo SP Brasil, Tel.: (55 11) 2065-8133 - São Paulo - SP - Brazil
E-mail: einicker@usp.br