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Diversity of Drosophilidae (Insecta, Diptera) in the Restinga forest of southern Brazil

Abstract

Although members of Drosophilidae are frequently the topic of ecological studies in Brazil, few have explored Restinga or, until only recently, Pampa biome environments. This study proposes to describe the diversity and temporal variation of the Drosophilidae assemblage from a Restinga forest of Rio Grande do Sul, Brazil. We performed monthly collections from February 2013 to January 2014 using yeasted banana-baited traps. A total of 25,093 individuals of 46 species were sampled. Drosophila simulans and the D. willistoni subgroup were the dominant taxa; D. polymorpha, D. immigrans, D. paraguayensis and Zygothrica orbitalis were of intermediate abundance, and the other 40 species were rare. Based on sampling effort estimators, our collections were sufficient. Jaccard and Morisita indices evaluated using ANOSIM reveal little similarity in the composition of samples across months. Canonical correspondence analysis shows that the variables of maximum and minimum temperature are the main factors responsible for differentiation of the species composition of the assemblage throughout the year, whereby collections in the coldest periods (July, August and September) are those with a more differentiated composition. In these months, the dominance of D. simulans and the D. willistoni subgroup decreases while increased abundance of the D. tripunctata group (as D. paraguayensis) and Z. orbitalis occurs. In comparison to other studies carried out in environments in southernmost Brazil, we observed a similar pattern of fluctuation in abundance over the year, with a higher abundance of dominant species in warmer months and population sizes decreasing in colder months.

Keywords:
Biodiversity analysis; Community ecology; New distribution record; Pampa biome; Taxonomic survey

Introduction

Insects play an important role in the diversity of natural habitats and are essential for habitat maintenance (Didham et al., 1996Didham, R.K., Ghazoul, J., Stork, N.E., Davis, A.J., 1996. Insects in fragmented forests: a functional approach. Trends Ecol. Evol. 11, 255-260.; Samways, 2015Samways, M.J., 2015. Future-proofing insect diversity. Curr. Opin. Insect Sci. 12, 71-78.). Studies on Drosophilidae, a well-studied Diptera family, have shed light on species coexistence and the relationship between insects and environments (Shorrocks and Rosewell, 1986Shorrocks, B., Rosewell, J., 1986. Guild size in Drosophilids: a simulation model. J. Anim. Ecol. 55, 527-541.; Sevenster and Van Alphen, 1993Sevenster, J.G., Van Alphen, J.J.M., 1993. A life history trade-off in Drosophila species and community structure in variable environments. J. Anim. Ecol. 62, 720-736.; Yamashita and Hijii, 2003Yamashita, S., Hijii, N., 2003. Effects of mushroom size on the structure of a mycophagous arthropod community: comparison between infracommunities with different types of resource utilization. Ecol. Res. 18, 131-143.; Mata et al., 2008Mata, R.A., McGeoch, M.A., Tidon, R., 2008. Drosophilid assembleges as a bioindicador system of human disturbance in the Brazilian Savanna. Biodivers. Conserv. 17, 2899-2916.), noting that drosophilids are sensitive to changes in habitat conditions, with excellent potential as bioindicators (Mata et al., 2008Mata, R.A., McGeoch, M.A., Tidon, R., 2008. Drosophilid assembleges as a bioindicador system of human disturbance in the Brazilian Savanna. Biodivers. Conserv. 17, 2899-2916., 2010Mata, R.A., McGeoch, M.A., Tidon, R., 2010. Drosophilids (Insecta, Diptera) as tools for conservation biology. Nat. Conservação. 8, 60-65.). Members of Drosophilidae have been studied throughout Brazil, and their assemblages are characteristic of different ecosystems (Martins, 1987Martins, M., 1987. Variação espacial e temporal de algumas espécies e grupos de Drosophila (Diptera) em duas reservas de matas isoladas, nas vizinhanças de Manaus (Amazonas, Brasil). Mus. Para. Emílio Goeldi Ser. Zool. 3, 195-218.; Val and Marques, 1996Val, F.C.do., Marques, M.D., 1996. Drosophilidae (Diptera) from the Pantanal of Mato Grosso (Brazil), with the description of a new species belonging to the bromeliae group of the genus Drosophila. Pap. Avulsos Zool. 39, 223-230.; Schmitz et al., 2007Schmitz, H.J., Valente, V.L.S., Hofmann, P.R.P., 2007. Taxonomic survey of Drosophilidae (Diptera) from mangrove forests of Santa Catarina Island, southern Brazil. Neotrop. Entomol. 36, 53-64.; Döge et al., 2008Döge, J.S., Valente, V.L.S., Hofmann, P.R.P., 2008. Drosophilids (Diptera) from an Atlantic Forest Area in Santa Catarina, Southern Brazil. Rev. Bras. Entomol. 52, 615-624.; Mata et al., 2008Mata, R.A., McGeoch, M.A., Tidon, R., 2008. Drosophilid assembleges as a bioindicador system of human disturbance in the Brazilian Savanna. Biodivers. Conserv. 17, 2899-2916.; Bizzo et al., 2010Bizzo, L., Gottschalk, M.S., De Toni, D.C., Hofmann, P.R.P., 2010. Seasonal dynamics of a drosophilid (Diptera) assemblage and its potencial as bioindicator in open environments. Iheringia Ser. Zool. 100, 185-191.; Rohde et al., 2010Rohde, C., Silva, D.M.I.O., Jucá, J.C.L.de.A., Montes, M.A., Garcia, A.C.L., 2010. Espécies invasoras da família Drosophilidae (Diptera, Insecta) em ambientes da Caatinga de Pernambuco. An. Acad. Pernambucana Cienc Agro. 7, 227-240.; Poppe et al., 2014Poppe, J.L., Schmitz, H.J., Grimaldi, D., Valente, V.L.S., 2014. High diversity of Drosophilidae (Insecta, Diptera) in the Pampas Biome of South America, with descriptions of new Rhioleucophenga species. Zootaxa 3779, 215-245.).

The Brazilian coast is characterized by Restinga forest, a particular ecosystem formed on sandy and nutrient-poor soils that is characterized by heterogeneous vegetation with a strong marine influence. This ecosystem is mainly associated with the Atlantic forest biome and is distributed along the entire Brazilian coast, occupying 80% of the coastal area. The Restinga forest macroclimate fluctuates according to its latitudinal location, being more stable than in field areas but varying more widely than forests with richer soils. The structure and distribution of Restinga forests are a result of depositional features determined by successive changes in sea level during the Quaternary period (Lacerda et al., 1982Lacerda, L.D., Araujo, D.S.D., Maciel, N.C., 1982. Restingas brasileiras: uma bibliografia. Fundação José Bonifácio, Rio de Janeiro.; Coutinho, 2006Coutinho, L.M., 2006. O conceito de bioma. Acta Bot. Bras. 20, 13-23.; Behling et al., 2009Behling, H., Jeske-Pieruschka, V., Schüler, L., Pillar, V.D., 2009. Dinâmica dos campos no sul do Brasil durante o Quaternário Tardio. In: Pillar, V.D., Müller, S.C., Castilhos, Z.M.S., Jacques, A.V.A. (Eds.), Campus Sulinos: Conservação e Uso Sustentável da Biodiversidade. Ministério do Meio Ambiente, Brasília, pp. 13–25.; Magnago et al., 2010Magnago, L.F.S., Martins, S.V., Schaefer, C., Neri, A.V., 2010. Gradiente fitofisionômico-edáfico em formações florestais de Restinga no Sudeste do Brasil. Acta Bot. Bras. 24, 653-665.).

In the state of Rio Grande do Sul, Brazil, the Restinga forest has a particular physiognomy and flora related to the Pampa biome. This ecosystem is conditioned by a temperate climate, which contrasts with the tropical influence that predominates on the northern coast of the state (Waechter, 1985Waechter, J.L., 1985. Aspectos ecológicos de vegetação de Restinga no Rio Grande do Sul. Comum. Mus. Cienc. Tecnol. PUCRS. Ser. Bot. 33, 49-68.; Bencke, 2009Bencke, G.A., 2009. Diversidade e conservação da fauna dos Campos do Sul do Brasil. In: Pillar, V.D., Müller, S.C., Castilhos, Z.M.S., Jacques, A.V.A. (Eds.), Campos Sulinos: Conservação e Uso Sustentável da Biodiversidade. Ministério do Meio Ambiente, Brasília, pp. 101–121.). Recently, areas of Restinga have been used for the development of commercial forests, mainly eucalyptus and pine, which is changing this environment and giving rise to a new structural configuration (Fonseca and Diehl, 2004Fonseca, R.C., Diehl, E., 2004. Riqueza de formigas (Hymenoptera, Formicidae) epigéicas em povoamentos de Eucalipytus spp. (Myrtaceae) de diferentes idades no Rio Grande do Sul, Brasil. Rev. Bras. Entomol. 48, 95-100.). Overall, in addition to other negative effects, the loss of any natural habitat can cause a severe decrease in biodiversity, affecting the rate of population growth, reducing the length and diversity of the food chain and changing interactions among species (Forero-Medina and Vieira, 2007Forero-Medina, G., Vieira, M.V., 2007. Conectividade funcional e a importância da interação organismo-paisagem. Oecol. Bras. 11, 493-502.).

Different environments of southern Brazil have been characterized in terms of their Drosophilidae fauna. However, most research to date has been conducted in the Atlantic forest, forests and agricultural areas of the Pampa biome and urbanized areas (Valente and Araújo, 1991Valente, V.L.S., Araújo, A.M., 1991. Ecological aspects of Drosophila species in two contrasting environments in Southern Brazil (Diptera, Drosophilidae). Rev. Bras. Entomol. 35, 237-253.; Silva et al., 2005Silva, N.M., Fantinel, C.da.C., Valente, V.L.S., Valiati, V.H., 2005. Ecology and populations dynamics of the invasive species Zaprionus indianus (Gupta) (Diptera: Drosophilidae) on the composition of the drosophilid communities in Porto Alegre city, Southern of Brazil. Neotrop. Entomol. 34, 363-374.; Hochmüller et al., 2010Hochmüller, C.J.C., Silva, L.da.M., Valente, V.L.S., Schmitz, H.J., 2010. The drosophilid fauna (Diptera, Drosophilidae) of the transition between the Pampa and Atlantic Forest Biomes in the state of Rio Grande do Sul, southern Brazil: first records. Pap. Avulsos Zool. 50, 285-295.; Garcia et al., 2012Garcia, C.F., Hochmüller, C.J.C., Valente, V.L.S., Schmitz, H.J., 2012. Drosophilid assemblages at different urbanization levels in the city of Porto Alegre, State of Rio Grande do Sul, Southern Brazil. Neotrop. Entomol. 41, 32-41.; Poppe et al., 2012Poppe, J.L., Valente, V.L.S., Schmitz, H.J., 2012. Structure of Drosophilidae assemblage (Insecta, Diptera) in Pampa Biome (São Luís Gonzaga, RS). Pap. Avulsos Zool. 52, 185-195., 2013Poppe, J.L., Valente, V.L.S., Schmitz, H.J., 2013. Population dynamics of Drosophilids in the Pampa Biome in response to temperature. Neotrop. Entomol. 42, 269-277.). Furthermore, studies of Restinga were performed in Santa Catarina and São Paulo States (Bizzo and Sene, 1982Bizzo, N.M.V., Sene, F.M., 1982. Studies on the natural populations of Drosophila from Peruíbe (SP), Brazil (Diptera, Drosophilidae). Rev. Bras. Biol. 42, 539-544.; Bizzo et al., 2010Bizzo, L., Gottschalk, M.S., De Toni, D.C., Hofmann, P.R.P., 2010. Seasonal dynamics of a drosophilid (Diptera) assemblage and its potencial as bioindicator in open environments. Iheringia Ser. Zool. 100, 185-191.) where the environmental conditions are different due to the Atlantic forest influence. Therefore, the present study sought to report the diversity and temporal variation in Drosophilidae species of Restinga forest in southernmost Brazil, with a goal of joining efforts in characterization of the environments of the Pampa biome. Moreover, investigation of the species richness of the fauna and flora of different environments is a priority measure for studies focused on species conservation and understanding their temporal dynamics. Accordingly, this study in a Restinga forest with permanent conservation area status will assist in the maintenance of its environmental integrity and support future studies.

Material and methods

Studied area

Horto Botânico Irmão Teodoro Luis (HBITL) is located in the municipality of Capão do LeãoEstação Agroclimatológica de Pelotas (Capão do Leão) 1888. Available at: http://agromet.cpact.embrapa.br/estacao/index.html (accessed 12.02.15).
http://agromet.cpact.embrapa.br/estacao/...
, Rio Grande do Sul, Brazil, at 31°47'48"S, 52°15'45"W (Fig. 1A and B). HBITL has been a protected area since 1964, with approximately 25 ha located in the Pampa biome (Guerra et al., 2015Guerra, E., Streher, N.S., Ludtke, R., 2015. Plantas trepadeiras do Horto Botânico Irmão Teodoro Luis, sul do Rio Grande do Sul, Brasil. Rev. Bras. Biocienc. 13, 201-209.). It is composed of a mosaic of Restinga forest surrounded by wetlands and anthropogenic habitats, such as pasture and a few low buildings. The forest consists of different strata: trees, shrubs, and herbaceous plants, with xeromorphic, succulent and thorny vegetation (Rodrigues, 2005Rodrigues, E.N.L., 2005. Araneofauna de serapilheira de duas áreas de uma mata de restinga no município de Capão do Leão, Rio Grande do Sul. Biotemas. 18, 73-92.). Large fig trees are common, and they stand in the forest canopy. HBITL presents a long history of anthropic interference. Intended for research and academic purposes, it has been under the responsibility of the Universidade Federal de Pelotas since the 1960s.

Fig. 1
Studied area. (A) Map of South America, with Brazil in gray and the state of Rio Grande do Sul highlighted. (B) Map of the state of Rio Grande do Sul, highlighting the Horto Botânico Irmão Teodoro Luís (HBITL) with a circle. (C) Satellite image of the Restinga forest of HBITL, with the positions of the traps shown (Google Earth).

According to Kottek et al. (2006)Kottek, M., Grieser, J., Beck, C., Rudolf, B., Rubel, F., 2006. World Map of the Köppen-Geiger climate classification Updated. Meteorol. Z. 15, 259-263., the climatic classification of this region is Cfa, presenting a mesothermal and super humid climate with no distinct dry season. The climatological normals recorded in 2013 and 2014 included an average annual temperature of 17.2 °C (the lowest and highest average temperatures were 4.2 °C and 24.8 °C, respectively) and 81.6% relative humidity (the lowest and highest average relative humidities were 75.3% and 85.0%, respectively). The environmental data were collected from Estação Agroclimatológica de Pelotas (2015) at 31°52'00"S, 52°21'24"W.

Specimen sampling and identification

From February 2013 to January 2014, specimens were collected monthly using 12 traps constructed according to Tidon and Sene (1988)Tidon, R., Sene, F.M., 1988. A trap that retains and keeps Drosophila alive. Drosoph. Inf. Serv. 67, 89. and baited with approximately 150 g of banana and 1.5 g of dry yeast. The traps were tied to trees at a height of approximately 1.5 m and distanced at 60 m from one another (Fig. 1C). The traps were kept in the field for 3 days.

The collected specimens were preserved in 70% ethanol and identified based on their external morphology according to the current literature. Male terminalia of sibling species were dissected according Bächli et al. (2004)Bächli, G., Vilela, S.A., Saura, A., 2004. The Drosophilidae (Diptera) of Fennoscandia and Denmark. Fauna Ent. Scad. Leiden, Brill. for species-level identification. Females of sibling species were identified by external morphology and, when possible, the species level was determined according to the quantities of males in each trap for analysis purposes. Vouchers were deposited in the Drosophilidae collection of the Museu de Ciências Naturais Carlos Ritter (MCNCR).

Data analysis

To characterize the assemblage, we used the absolute and relative abundances of each species (ni and pi, respectively) and the species richness (number of species in the sample, S). We verified the spatial autocorrelation of the species composition among the traps in each sampling event using Mantel tests with Jaccard and Morisita indices. The significance level was calculated with 999 permutations. To perform the tests, geographic coordinates were determined for the position of each trap. The distances between traps were calculated based on the Euclidean distance. These analyses were conducted in the R program version 3.1.2 (R Core Team, 2013R Core Team, 2013. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Viena, Austria, Available at: http://www.r-project.rg/ (accessed 07.03.15).
http://www.r-project.rg/...
) with the ade4 package (Ecological Data Analysis, 2015Ecological Data Analysis: Exploratory and Euclidean methods in Environmental sciences 2002. Available at: http://pbil.univ-lyon1.fr/ade4/home.php?lang=eng (accessed 13.02.15).
http://pbil.univ-lyon1.fr/ade4/home.php?...
). As we did not observe statistically significant correlations between the distances and assemblage compositions in any of the months studied (Supplementary material 1), we used the composition of individual traps as the statistical unit for subsequent analyses (unless otherwise stated).

We generated a rank-abundance curve to evaluate dominance in the assemblage based on the total relative abundance of species in all samples, and we constructed a randomized accumulation curve of the observed species with 95% confidence intervals using EstimateS v.8.0 software (Colwell, 2006Colwell, R.K., 2006. Estimates: Statistical estimation of species richness and shared species from samples. Version 8. Available at: http://purl.oclc.org/estimates (accessed 12.10.15).
http://purl.oclc.org/estimates...
). Bootstrap and Michaelis-Menten species richness estimators were used to verify the sampling effort.

To evaluate the influence of temporal variation on the assemblage over the sampling period, we conducted canonical correspondence analysis (CCA) using the absolute abundance of species collected in three or more samples or n i > 10 and the climatic variables maximum temperature (TM), minimum temperature (Tm), relative humidity (RH) and precipitation (PR) as independent variables (Supplementary material 2). This analysis was conducted using PAST 3.0 software (Hammer et al., 2001Hammer, O., Harper, D.A.T., Ryan, P.D., 2001. PAST: Paleontological Statistics Software Package for Education and Data Analysis. Palaeontol. Electronica, Avail-able at: http://palaeo-electronica.org/2001_1/past/issue1_01.htm (accessed 07.03.15).
http://palaeo-electronica.org/2001_1/pas...
). For the statistical analysis, we used the average values of each environmental variable over a period of 5 days, 3 days with the traps in the field and 2 days prior to the collections. The environmental data were standardized (Zi=(Xi−X)/S, where Xi is the value of the environmental variable for sample i, S is the standard deviation of the samples, and X is the average of the samples).

Finally, we conducted Spearman correlation analysis between the total abundance and species richness in each month and the environmental variables. We used Bonferroni correction to minimize type I error. The tests were conducted using PAST 3.0 software.

Results

A total of 25,093 individuals, belonging to 46 species in five genera of Drosophilidae, were collected and identified, including the first record of D. neosaltans for the state of Rio Grande do Sul. Twelve females were identified as species groups or subgroups and were not included in the statistical analyses. Table 1 presents the absolute and relative abundances of the specimens identified.

Table 1
Abundances of Drosophilidae species sampled from February 2013 to January 2014 in the Horto Botânico Irmão Teodoro Luís (HBITL), Brazil.

After ranking species based on their relative abundances, we observed two dominant taxa in the assemblage, with pi > 0.10: exotic D. simulans and the Neotropical D. willistoni subgroup (Fig. 2). The intermediary species, at 0.10 ≥ pi > 0.01, were D. polymorpha, D. immigrans, D. paraguayensis and Zygothrica orbitalis. The remaining 40 species, at pi ≤ 0.01, were rare. Among the 46 species sampled, 12 were singletons (just one specimen collected) and four doubletons (only two specimens collected). Thus, 40% of the species were occasionally or poorly sampled. Fig. 3 shows the randomized accumulation curve of the observed species (Sobs) with 95% confidence intervals and the richness curves based on bootstrap and Michaelis-Menten estimators. The bootstrap estimator predicted 51 species, close to the species richness values observed. This estimator curve is entirely within the range of the 95% confidence intervals of the Sobs curve, exhibiting high similarity between them. Furthermore, the Michaelis-Menten estimator showed a lower richness than Sobs, and the meeting point of the curves indicated the inflection point of the Sobs curve (i.e., the point where the species accumulation rate decreases). These results suggest that we collected the majority of the species in this location with this type of baited trap.

Fig. 2
Rank abundance plot of the relative abundances of Drosophilidae species sampled in the Horto Botânico Irmão Teodoro Luis (HBITL), Brazil, from February 2013 to January 2014.

Fig. 3
Randomized accumulated curve of observed species (solid lines, bars are 95% confidence intervals) and bootstrap (dashed line) and Michaelis-Menten (dash-dotted lines) richness estimators constructed with Drosophilidae species sampled in the Horto Botânico Irmão Teodoro Luis (HBITL), Brazil, from February 2013 to January 2014.

Among the four climatic variables considered in our analysis, i.e., the maximum (TM) and minimum temperatures (Tm), relative humidity (RH) and precipitation (PR), TM and Tm had the most influence on Drosophilidae species over the studied year. These variables and PR were highly related to axis 1 of CCA, which explains 52.7% of the variation in the data (Fig. 4). Axis 2, corresponding to 43.5% of the variation in the data, was equally related to TM, Tm and RH. In the CCA plot, February, March, April, May, June, October, November and December 2013 and January 2014 occurred close to the intersection of the axes, where D. simulans, the D. willistoni subgroup and D. polymorpha were the dominant species and the abundance of D. neosaltans, D. prosaltans and D. suzukii increased (Fig. 4). The first three species were present in all months, but their abundances also decreased in July, August and September, when the temperatures decreased (Fig. 5). In months with lower temperatures, i.e., July and August, Zy. orbitalis was the dominant species, and the abundance of D. mediosignata, D. mediopunctata, D. melanogaster, D. paraguayensis, D. griseolineata, D. arassari and D. hydei increased. Other species of Zygothrica were also sampled in August, totaling 226 individuals. In contrast, D. immigrans, D. mercatorum, D. repleta, D. nappae, D. sturtevanti, D. ornatifrons, D. schineri, D. onca, D. mediostriata and D. maculifrons did not show marked variation in abundance during the sampled year. Precipitation (PR) had little influence on species composition in this study.

Fig. 4
Canonical correspondence analysis axes 1 and 2, showing the organization of species according to environmental variables (TM, maximum temperature; Tm, minimum temperature; RH, relative humidity; PR, precipitation) from February 2013 to January 2014.

Fig. 5
Monthly relative abundance of species from February 2013 to January 2014 in the Horto Botânico Irmão Teodoro Luís (HBITL), Brazil.

When we analyzed the monthly variation in terms of the absolute abundance (Fig. 6A) and species richness (Fig. 6B) of Drosophilidae, we observed a high absolute abundance in warmer months. The same pattern was not found for species richness. Using the Spearman test, we correlated absolute abundance with climatic variables and observed abundance to be positively correlated with TM (R = 0.58, p = 0.048) and Tm (R = 0.71, p = 0.01) (Fig. 7), whereas absolute abundance was not correlated with the other two variables (RH: R = −0.15, p = 0.63; and PR: R = −0.46, p = 0.14). Additionally, species richness showed no correlation with any climatic variable (TM: R = −0.03, p = 0.92; Tm: R = −0.12, p = 0.70; RH: R = −0.38, p = 0.22; and PR: R = −0.57, p = 0.053), though the pattern of species dominance changed in the coldest months, as observed in the CCA plot.

Fig. 6
Absolute abundance (A) and absolute richness of species (B) from February 2013 to January 2014 in the Horto Botânico Irmão Teodoro Luís (HBITL), Brazil.

Fig. 7
Correlation analyses between the absolute abundance of species and the maximum and minimum temperatures.

Discussion

Southern expansion of the distribution of collected species

The new record of D. neosaltans expands its geographic distribution limit to the latitude of 31°47'48"S (Silva et al., 2005Silva, N.M., Fantinel, C.da.C., Valente, V.L.S., Valiati, V.H., 2005. Ecology and populations dynamics of the invasive species Zaprionus indianus (Gupta) (Diptera: Drosophilidae) on the composition of the drosophilid communities in Porto Alegre city, Southern of Brazil. Neotrop. Entomol. 34, 363-374.; Gottschalk et al., 2008Gottschalk, M.S., Hofmann, P.R.P., Valente, V.L.S., 2008. Diptera, Drosophilidae: historical occurrence in Brasil. Check list. 4, 485-518., 2009Gottschalk, M.S., Bizzo, L., Döge, J.S., Profes, M.S., Hofmann, P.R.P., Valente, V.L.S., 2009. Drosophilidae (Diptera) associated to fungi: differential use of resources in anthropic and Atlantic Rain Forest areas. Iheringia Ser. Zool. 99, 442-448.; Garcia et al., 2012Garcia, C.F., Hochmüller, C.J.C., Valente, V.L.S., Schmitz, H.J., 2012. Drosophilid assemblages at different urbanization levels in the city of Porto Alegre, State of Rio Grande do Sul, Southern Brazil. Neotrop. Entomol. 41, 32-41.; Poppe et al., 2012Poppe, J.L., Valente, V.L.S., Schmitz, H.J., 2012. Structure of Drosophilidae assemblage (Insecta, Diptera) in Pampa Biome (São Luís Gonzaga, RS). Pap. Avulsos Zool. 52, 185-195., 2014Poppe, J.L., Schmitz, H.J., Grimaldi, D., Valente, V.L.S., 2014. High diversity of Drosophilidae (Insecta, Diptera) in the Pampas Biome of South America, with descriptions of new Rhioleucophenga species. Zootaxa 3779, 215-245.; Valer et al., 2013Valer, F.B., Neutzling, A.S., Garcia, F.R.M., Gottschalk, M.S., Blauth, M.L., 2013. The first record of Zygothrica orbitalis (Sturtevant, 1916) for the state of Rio Grande do Sul and the southernmost limits for seven species of Drosophilidae (Insecta: Diptera). Drosoph. Inf. Serv. 96, 120-123.; Deprá et al., 2014Deprá, M., Poppe, J.L., Schmitz, H.J., De Toni, D.C., Valente, V.L.S., 2014. The first records of the invasive pest Drosophila suzukii in the South American continent. J. Pest Sci. 87, 379-383.; Hochmüller et al., 2010Hochmüller, C.J.C., Silva, L.da.M., Valente, V.L.S., Schmitz, H.J., 2010. The drosophilid fauna (Diptera, Drosophilidae) of the transition between the Pampa and Atlantic Forest Biomes in the state of Rio Grande do Sul, southern Brazil: first records. Pap. Avulsos Zool. 50, 285-295.). Before our survey, the southernmost record of D. neosaltans was in Florianópolis, SC (27°35'49"S, 48°32'58"W), and the species was recorded more often in forested areas of the Atlantic forest biome (De Toni et al., 2007De Toni, D.C., Gottschalk, M.S., Cordeiro, J., Hofmann, P.P.R., Valente, V.L.S., 2007. Study of the Drosophilidae (Diptera) communities on Atlantic Forest Islands of Santa Catarina State, Brazil. Neotrop. Entomol. 36, 356-375.; Gottschalk et al., 2007Gottschalk, M.S., DeToni, D.C., Valente, V.L.S., Hofmann, P.R.P., 2007. Changes in Brazilian Drosophilidae (Diptera) assemblages across an Urbanisation gradient. Neotrop. Entomol. 36, 848-862.; Döge et al., 2008Döge, J.S., Valente, V.L.S., Hofmann, P.R.P., 2008. Drosophilids (Diptera) from an Atlantic Forest Area in Santa Catarina, Southern Brazil. Rev. Bras. Entomol. 52, 615-624.). In addition, the limits of the distributions of D. cuaso, D. fuscolineata, D. flexa, D. maculifrons, D. nigricuria and D. papei have been expanded further south. These species, which are rare in samples from different studies, were previously recorded in the northern region of the state of Rio Grande do Sul (Gottschalk et al., 2009Gottschalk, M.S., Bizzo, L., Döge, J.S., Profes, M.S., Hofmann, P.R.P., Valente, V.L.S., 2009. Drosophilidae (Diptera) associated to fungi: differential use of resources in anthropic and Atlantic Rain Forest areas. Iheringia Ser. Zool. 99, 442-448.; Hochmüller et al., 2010Hochmüller, C.J.C., Silva, L.da.M., Valente, V.L.S., Schmitz, H.J., 2010. The drosophilid fauna (Diptera, Drosophilidae) of the transition between the Pampa and Atlantic Forest Biomes in the state of Rio Grande do Sul, southern Brazil: first records. Pap. Avulsos Zool. 50, 285-295.; Garcia et al., 2012Garcia, C.F., Hochmüller, C.J.C., Valente, V.L.S., Schmitz, H.J., 2012. Drosophilid assemblages at different urbanization levels in the city of Porto Alegre, State of Rio Grande do Sul, Southern Brazil. Neotrop. Entomol. 41, 32-41.; Poppe et al., 2012Poppe, J.L., Valente, V.L.S., Schmitz, H.J., 2012. Structure of Drosophilidae assemblage (Insecta, Diptera) in Pampa Biome (São Luís Gonzaga, RS). Pap. Avulsos Zool. 52, 185-195., 2014Poppe, J.L., Schmitz, H.J., Grimaldi, D., Valente, V.L.S., 2014. High diversity of Drosophilidae (Insecta, Diptera) in the Pampas Biome of South America, with descriptions of new Rhioleucophenga species. Zootaxa 3779, 215-245.; Valer et al., 2013Valer, F.B., Neutzling, A.S., Garcia, F.R.M., Gottschalk, M.S., Blauth, M.L., 2013. The first record of Zygothrica orbitalis (Sturtevant, 1916) for the state of Rio Grande do Sul and the southernmost limits for seven species of Drosophilidae (Insecta: Diptera). Drosoph. Inf. Serv. 96, 120-123., 2016Valer, F.B., Bernardi, E., Mendes, M.F., Blauth, M.L., Gottschalk, M.S., 2016. Diversity and associations between Drosophilidae (Diptera) species and Basidiomycetes in a Neotropical forest. An. Acad. Bras. Cienc. 88, 1-14.; Deprá et al., 2014Deprá, M., Poppe, J.L., Schmitz, H.J., De Toni, D.C., Valente, V.L.S., 2014. The first records of the invasive pest Drosophila suzukii in the South American continent. J. Pest Sci. 87, 379-383.).

The Drosophilidae assemblage of HBITL

Of the five genera sampled in our study, Drosophila was the richest. Because this genus frequently uses decaying fruits, a large number of species is expected when sampling is conducted using yeast and banana baits (reviewed in Gottschalk et al., 2008Gottschalk, M.S., Hofmann, P.R.P., Valente, V.L.S., 2008. Diptera, Drosophilidae: historical occurrence in Brasil. Check list. 4, 485-518.). We also sampled one species each of the genera Hirtodrosophila and Leucophenga, in addition to five species of Zygothrica, which are commonly found in mushrooms, where they feed, lay eggs, rear larvae and/or carry out sexual courtship (Grimaldi, 1987Grimaldi, D., 1987. Phylogenetics and taxonomy of Zygothrica (Diptera, Drosophilidae). Bull. Am. Mus. Nat. Hist. 186, 103-268.; Val and Kaneshiro, 1988Val, F.C. do., Kaneshiro, K.Y., 1988. Drosophilidae (Diptera) from the Estação Biológica de Boracéia, on the coastal range of the state of São Paulo, Brazil: geographical distribution. In: Vanzolini, P.E., Heyer, W.R. (Eds.), Proceedings of a Workshop on Neotropical Distribution Patterns. Academia Brasileira de Ciências, Rio de Janeiro, pp. 189–203.; Courtney et al., 1990Courtney, S.P., Kibota, T.T., Singleton, T.A., 1990. Ecology of mushroom-feeding Drosophilidae. In: Begon, B., Fitter, A.H., Macfadyen, A. (Eds.), Advances in Ecological Research. Academic Press, London, pp. 225–274.; Valer et al., 2016Valer, F.B., Bernardi, E., Mendes, M.F., Blauth, M.L., Gottschalk, M.S., 2016. Diversity and associations between Drosophilidae (Diptera) species and Basidiomycetes in a Neotropical forest. An. Acad. Bras. Cienc. 88, 1-14.). The capture of species of these genera with banana baits typically occurs sporadically. Finally, the Drosophilidae assemblage also included the genus Zaprionus, represented by one exotic species, Za. indianus, which is frequently caught by banana traps.

We found seven exotic Drosophilidae species in HBITL, D. ananassae, D. busckii, D. immigrans, D. melanogaster, D. simulans, D. suzukii and Za. indianus, amounting to 11,604 individuals, which is slightly lower than the abundance of native species (13,488 individuals). The presence of exotic species has been observed in areas with different anthropization levels (Ferreira and Tidon, 2005Ferreira, L., Tidon, R., 2005. Colonizing potential of Drosophilidae (Insecta, Diptera) in environments with different grades of urbanization. Biodivers. Conserv. 14, 1809-1821.; De Toni et al., 2007De Toni, D.C., Gottschalk, M.S., Cordeiro, J., Hofmann, P.P.R., Valente, V.L.S., 2007. Study of the Drosophilidae (Diptera) communities on Atlantic Forest Islands of Santa Catarina State, Brazil. Neotrop. Entomol. 36, 356-375.; Gottschalk et al., 2007Gottschalk, M.S., DeToni, D.C., Valente, V.L.S., Hofmann, P.R.P., 2007. Changes in Brazilian Drosophilidae (Diptera) assemblages across an Urbanisation gradient. Neotrop. Entomol. 36, 848-862.; Garcia et al., 2008Garcia, A.C.L., Valiati, V.H., Gottschalk, M.S., Rohde, C., Valente, V.L.S., 2008. Two decades of colonization of the urban environment of Porto Alegre, southern Brazil, by Drosophila paulistorum (Diptera, Drosophilidae). Iheringia Ser. Zool. 98, 329-338.). Although HBITL is currently a protected area and therefore limited to research, the presence of exotic species can nonetheless be associated with anthropic action in HBITL and its surroundings in recent decades. In addition, we sampled a large number of D. suzukii, an invasive species recently introduced to South America; this species was first recorded in Brazil in February 2013 in the southern region (Deprá et al., 2014Deprá, M., Poppe, J.L., Schmitz, H.J., De Toni, D.C., Valente, V.L.S., 2014. The first records of the invasive pest Drosophila suzukii in the South American continent. J. Pest Sci. 87, 379-383.). This species was sampled in October 2013 at HBITL, located approximately 550 km from the site of its first record.

The species sampled in our study represent approximately 40% of the Drosophilidae species recorded in the Pampa biome (Poppe et al., 2016Poppe, J.L., Schmitz, H.J., Valente, V.L.S., 2016. The diversity of Drosophilidae in the South American pampas: update of the species records in an environment historically neglected. Drosoph. Inf. Serv. 98, 47-51.). The species richness observed in HBITL corroborates other studies of Drosophilidae diversity using the same sampling method in different areas of the Pampa and Atlantic forest biomes of the state of RS. These studies recorded 26-53 species, with Drosophila being the most abundant and specious genus (Hochmüller et al., 2010Hochmüller, C.J.C., Silva, L.da.M., Valente, V.L.S., Schmitz, H.J., 2010. The drosophilid fauna (Diptera, Drosophilidae) of the transition between the Pampa and Atlantic Forest Biomes in the state of Rio Grande do Sul, southern Brazil: first records. Pap. Avulsos Zool. 50, 285-295.; Garcia et al., 2012Garcia, C.F., Hochmüller, C.J.C., Valente, V.L.S., Schmitz, H.J., 2012. Drosophilid assemblages at different urbanization levels in the city of Porto Alegre, State of Rio Grande do Sul, Southern Brazil. Neotrop. Entomol. 41, 32-41.; Poppe et al., 2012Poppe, J.L., Valente, V.L.S., Schmitz, H.J., 2012. Structure of Drosophilidae assemblage (Insecta, Diptera) in Pampa Biome (São Luís Gonzaga, RS). Pap. Avulsos Zool. 52, 185-195., 2014Poppe, J.L., Schmitz, H.J., Grimaldi, D., Valente, V.L.S., 2014. High diversity of Drosophilidae (Insecta, Diptera) in the Pampas Biome of South America, with descriptions of new Rhioleucophenga species. Zootaxa 3779, 215-245.).

Our sampled assemblage was characterized by the dominance of D. simulans and the D. willistoni subgroup. Despite the fact that it is an exotic species, D. simulans is frequently found in different habitats in the Neotropical region (Sene et al., 1980Sene, F.M., Val, F.C., Vilela, C.R., Pereira, M.A.Q.R., 1980. Preliminary data on the geographical distribution of Drosophila species within morphoclimatic domains of Brazil. Pap. Avulsos Zool. 33, 315-326.; Torres and Madi-Ravazzi, 2006Torres, F.R., Madi-Ravazzi, L., 2006. Seasonal variation in natural populations of Drosophila spp. (Diptera) in two woodlands in the State of São Paulo, Brazil. Iheringia Ser. Zool. 96, 437-444.; Bizzo et al., 2010Bizzo, L., Gottschalk, M.S., De Toni, D.C., Hofmann, P.R.P., 2010. Seasonal dynamics of a drosophilid (Diptera) assemblage and its potencial as bioindicator in open environments. Iheringia Ser. Zool. 100, 185-191.; Schmitz et al., 2010Schmitz, H.J., Hofmann, P.R.P., Valente, V.L.S., 2010. Assemblages of drosophilids (Diptera, Drosophilidae) in mangrove forests: community ecology and species diversity. Iheringia Ser. Zool. 100, 133-140.; Garcia et al., 2012Garcia, C.F., Hochmüller, C.J.C., Valente, V.L.S., Schmitz, H.J., 2012. Drosophilid assemblages at different urbanization levels in the city of Porto Alegre, State of Rio Grande do Sul, Southern Brazil. Neotrop. Entomol. 41, 32-41.), and a high abundance of this species has also been verified in areas of the Pampa biome (Hochmüller et al., 2010Hochmüller, C.J.C., Silva, L.da.M., Valente, V.L.S., Schmitz, H.J., 2010. The drosophilid fauna (Diptera, Drosophilidae) of the transition between the Pampa and Atlantic Forest Biomes in the state of Rio Grande do Sul, southern Brazil: first records. Pap. Avulsos Zool. 50, 285-295.; Poppe et al., 2012Poppe, J.L., Valente, V.L.S., Schmitz, H.J., 2012. Structure of Drosophilidae assemblage (Insecta, Diptera) in Pampa Biome (São Luís Gonzaga, RS). Pap. Avulsos Zool. 52, 185-195.), as well as in urbanized areas (Gottschalk et al., 2007Gottschalk, M.S., DeToni, D.C., Valente, V.L.S., Hofmann, P.R.P., 2007. Changes in Brazilian Drosophilidae (Diptera) assemblages across an Urbanisation gradient. Neotrop. Entomol. 36, 848-862.; Garcia et al., 2012Garcia, C.F., Hochmüller, C.J.C., Valente, V.L.S., Schmitz, H.J., 2012. Drosophilid assemblages at different urbanization levels in the city of Porto Alegre, State of Rio Grande do Sul, Southern Brazil. Neotrop. Entomol. 41, 32-41.). The occurrence of the D. willistoni subgroup as the second most abundant taxon disagrees with the results of other studies from the Pampa biome (Hochmüller et al., 2010Hochmüller, C.J.C., Silva, L.da.M., Valente, V.L.S., Schmitz, H.J., 2010. The drosophilid fauna (Diptera, Drosophilidae) of the transition between the Pampa and Atlantic Forest Biomes in the state of Rio Grande do Sul, southern Brazil: first records. Pap. Avulsos Zool. 50, 285-295.; Poppe et al., 2012Poppe, J.L., Valente, V.L.S., Schmitz, H.J., 2012. Structure of Drosophilidae assemblage (Insecta, Diptera) in Pampa Biome (São Luís Gonzaga, RS). Pap. Avulsos Zool. 52, 185-195.), where it was uncommon or rare, most likely because other studies in the Pampa biome were conducted in areas of grassland vegetation or more anthropized environments. In contrast, the D. willistoni subgroup has been well recorded in natural environments (Martins, 1987Martins, M., 1987. Variação espacial e temporal de algumas espécies e grupos de Drosophila (Diptera) em duas reservas de matas isoladas, nas vizinhanças de Manaus (Amazonas, Brasil). Mus. Para. Emílio Goeldi Ser. Zool. 3, 195-218.; Saavedra et al., 1995Saavedra, C.C.R., Callegari-Jacques, S.M., Napp, M., Valente, V.L.S., 1995. A descriptive and analytical study of four Neotropical drosophilid communities. J. Zool. Syst. Evol. Res. 33, 62-74.), though its abundance decreases in urbanized areas (Gottschalk et al., 2007Gottschalk, M.S., DeToni, D.C., Valente, V.L.S., Hofmann, P.R.P., 2007. Changes in Brazilian Drosophilidae (Diptera) assemblages across an Urbanisation gradient. Neotrop. Entomol. 36, 848-862.; Hochmüller et al., 2010Hochmüller, C.J.C., Silva, L.da.M., Valente, V.L.S., Schmitz, H.J., 2010. The drosophilid fauna (Diptera, Drosophilidae) of the transition between the Pampa and Atlantic Forest Biomes in the state of Rio Grande do Sul, southern Brazil: first records. Pap. Avulsos Zool. 50, 285-295.; Poppe et al., 2012Poppe, J.L., Valente, V.L.S., Schmitz, H.J., 2012. Structure of Drosophilidae assemblage (Insecta, Diptera) in Pampa Biome (São Luís Gonzaga, RS). Pap. Avulsos Zool. 52, 185-195.).

Abiotic variables

Corroborating the literature to date, the studied Drosophilidae assemblage responds to climatic variation (Martins, 1987Martins, M., 1987. Variação espacial e temporal de algumas espécies e grupos de Drosophila (Diptera) em duas reservas de matas isoladas, nas vizinhanças de Manaus (Amazonas, Brasil). Mus. Para. Emílio Goeldi Ser. Zool. 3, 195-218.; Mata et al., 2008Mata, R.A., McGeoch, M.A., Tidon, R., 2008. Drosophilid assembleges as a bioindicador system of human disturbance in the Brazilian Savanna. Biodivers. Conserv. 17, 2899-2916.; Rohde et al., 2010Rohde, C., Silva, D.M.I.O., Jucá, J.C.L.de.A., Montes, M.A., Garcia, A.C.L., 2010. Espécies invasoras da família Drosophilidae (Diptera, Insecta) em ambientes da Caatinga de Pernambuco. An. Acad. Pernambucana Cienc Agro. 7, 227-240.). In temperate regions with four well-marked seasons, abundance of specimens is high in warm months but with low diversity, whereas abundance is low in cold months but with high richness (Petersen, 1960Petersen, J.A., 1960. Studies on the ecology of the genus Drosophila. I. Collections in two different life zones and seasonal variations in Rio Grande do Sul, Brazil. Rev. Bras. Biol. 20, 3-16.; Araújo and Valente, 1981Araújo, A.M., Valente, V.L.S., 1981. Observações sobre alguns lepidópteros e drosofilídeos do Parque do Turvo, RS. Cienc. Cult. 33, 1485-1490.; Franck and Valente, 1985Franck, G., Valente, V.L.S., 1985. Study on the fluctuation in Drosophila populations of Bento Gonçalves, RS, Brazil. Rev. Bras. Biol. 45, 133-141.; Saavedra et al., 1995Saavedra, C.C.R., Callegari-Jacques, S.M., Napp, M., Valente, V.L.S., 1995. A descriptive and analytical study of four Neotropical drosophilid communities. J. Zool. Syst. Evol. Res. 33, 62-74.; De Toni et al., 2007De Toni, D.C., Gottschalk, M.S., Cordeiro, J., Hofmann, P.P.R., Valente, V.L.S., 2007. Study of the Drosophilidae (Diptera) communities on Atlantic Forest Islands of Santa Catarina State, Brazil. Neotrop. Entomol. 36, 356-375.; Gottschalk et al., 2007Gottschalk, M.S., DeToni, D.C., Valente, V.L.S., Hofmann, P.R.P., 2007. Changes in Brazilian Drosophilidae (Diptera) assemblages across an Urbanisation gradient. Neotrop. Entomol. 36, 848-862.; Poppe et al., 2013Poppe, J.L., Valente, V.L.S., Schmitz, H.J., 2013. Population dynamics of Drosophilids in the Pampa Biome in response to temperature. Neotrop. Entomol. 42, 269-277.). Of the climatic variables, the maximum and minimum temperatures were those that most influenced the assemblage, with the minimum temperature being the most determinant in terms of species composition, as described in other studies conducted in different environments (Torres and Madi-Ravazzi, 2006Torres, F.R., Madi-Ravazzi, L., 2006. Seasonal variation in natural populations of Drosophila spp. (Diptera) in two woodlands in the State of São Paulo, Brazil. Iheringia Ser. Zool. 96, 437-444.; Bizzo et al., 2010Bizzo, L., Gottschalk, M.S., De Toni, D.C., Hofmann, P.R.P., 2010. Seasonal dynamics of a drosophilid (Diptera) assemblage and its potencial as bioindicator in open environments. Iheringia Ser. Zool. 100, 185-191.; Poppe et al., 2013Poppe, J.L., Valente, V.L.S., Schmitz, H.J., 2013. Population dynamics of Drosophilids in the Pampa Biome in response to temperature. Neotrop. Entomol. 42, 269-277.). In our study, 14 species exhibited well-marked seasonality, with abundance variation largely related to temperature changes (as evidenced by CCA). However, in the area studied by Torres and Madi-Ravazzi (2006)Torres, F.R., Madi-Ravazzi, L., 2006. Seasonal variation in natural populations of Drosophila spp. (Diptera) in two woodlands in the State of São Paulo, Brazil. Iheringia Ser. Zool. 96, 437-444., a positive correlation between species richness and rainfall was described. Associations between Drosophilidae assemblages and rainfall were also stronger in studies performed in the Brazilian Cerrado, where the annual fluctuation in temperature year is smaller and the years are characterized by two seasons, one wet and one dry (Mata et al., 2008Mata, R.A., McGeoch, M.A., Tidon, R., 2008. Drosophilid assembleges as a bioindicador system of human disturbance in the Brazilian Savanna. Biodivers. Conserv. 17, 2899-2916.). According to Dobzhansky and Pavan (1950)Dobzhansky, T., Pavan, C., 1950. Local and seasonal variations in relative frequencies of species of Drosophila in Brazil. J. Anim. Ecol. 19, 1-14., precipitation should be more important for Drosophila species abundance because precipitation is essential for the flowering and fruiting of plants used as a trophic resource for Drosophilidae. In the HBITL area, precipitation has a secondary influence on the assemblage composition of Drosophilidae species (Fig. 4), most likely because fluctuation in this abiotic variable is less marked in southern Brazil.

Only three taxa were sampled during all 12 months of collection: D. simulans, D. polymorpha and the D. willistoni subgroup. These taxa show fluctuation in their abundance according to climatic variation. Drosophila simulans was dominant in April, November and December 2013, whereas the D. willistoni subgroup and D. polymorpha were dominant in January 2014, with the D. willistoni subgroup reaching an abundance that was greater than 90% of the total in that month. This pattern demonstrated that the dominant species were most abundant during warmer months, with an average temperature of 25 °C in April, November, and December of 2013 and January of 2014.

Zygothrica orbitalis was the dominant species in July and August 2013, when the maximum and minimum temperatures were low; for this species specifically, it is assumed that a lack of trophic resources for imagoes (i.e., mushrooms, Valer et al., 2016Valer, F.B., Bernardi, E., Mendes, M.F., Blauth, M.L., Gottschalk, M.S., 2016. Diversity and associations between Drosophilidae (Diptera) species and Basidiomycetes in a Neotropical forest. An. Acad. Bras. Cienc. 88, 1-14.) causes them to visit the bait used. This fact, associated with the low abundance of the dominant Drosophila species, makes Zy. orbitalis the dominant species in August. In a recent study by our group, we sampled Zy. orbitalis emerging profusely from the fruits of Psychotria sp. (Rubiaceae, Magnoliophyta), a common bush present in HBITL (Mayara Ferreira Mendes, unpublished data), which may indicate that this fly species is attracted to these fruits for oviposition. When sampling in an area with a similar climate, Garcia et al. (2012)Garcia, C.F., Hochmüller, C.J.C., Valente, V.L.S., Schmitz, H.J., 2012. Drosophilid assemblages at different urbanization levels in the city of Porto Alegre, State of Rio Grande do Sul, Southern Brazil. Neotrop. Entomol. 41, 32-41. verified the same pattern in winter, with substitution of the dominant species in warmer times.

Drosophilidae of the Restinga forest

In Brazil, two studies focusing on Drosophilidae from Restinga environments have been performed (Bizzo and Sene, 1982Bizzo, N.M.V., Sene, F.M., 1982. Studies on the natural populations of Drosophila from Peruíbe (SP), Brazil (Diptera, Drosophilidae). Rev. Bras. Biol. 42, 539-544.; Bizzo et al., 2010Bizzo, L., Gottschalk, M.S., De Toni, D.C., Hofmann, P.R.P., 2010. Seasonal dynamics of a drosophilid (Diptera) assemblage and its potencial as bioindicator in open environments. Iheringia Ser. Zool. 100, 185-191.). The areas sampled by Bizzo and Sene (1982)Bizzo, N.M.V., Sene, F.M., 1982. Studies on the natural populations of Drosophila from Peruíbe (SP), Brazil (Diptera, Drosophilidae). Rev. Bras. Biol. 42, 539-544. and Bizzo et al. (2010)Bizzo, L., Gottschalk, M.S., De Toni, D.C., Hofmann, P.R.P., 2010. Seasonal dynamics of a drosophilid (Diptera) assemblage and its potencial as bioindicator in open environments. Iheringia Ser. Zool. 100, 185-191. have comparatively sparser vegetation and a greater marine influence (Falkenberg, 1999Falkenberg, D.de.B., 1999. Aspectos da flora e da vegetação secundária da Restinga de Santa Catarina. Sul do Brasil. Insula. 28, 1-30.; Martins et al., 2008Martins, S.E., Rossi, L., Sampaio, P.S.P., Magenta, M.A.G., 2008. Caracterização florística de comunidades vegetais de restinga em Bertioga, SP, Brasil. Acta Bot. Bras. 22, 249-274.). Moreover, due to latitudinal differences, HBITL has a lower average temperature in the coldest month (approximately 4 °C) than the areas studied by Bizzo and Sene (1982)Bizzo, N.M.V., Sene, F.M., 1982. Studies on the natural populations of Drosophila from Peruíbe (SP), Brazil (Diptera, Drosophilidae). Rev. Bras. Biol. 42, 539-544. in São Paulo (46°56'W; 24°14'S) and by Bizzo et al. (2010)Bizzo, L., Gottschalk, M.S., De Toni, D.C., Hofmann, P.R.P., 2010. Seasonal dynamics of a drosophilid (Diptera) assemblage and its potencial as bioindicator in open environments. Iheringia Ser. Zool. 100, 185-191. in Santa Catarina (48°27'49"W; 27°38'21"S), with averages in the coldest month of approximately 18 °C. Nonetheless, the average temperature in the warmest month is the same in the areas covered by these three studies (approximately 25 °C). Therefore, few similarities in species composition were observed when compared with our data, whereby the dominant species, with the exception of D. simulans and the D. willistoni subgroup, were different from Bizzo and Sene (1982)Bizzo, N.M.V., Sene, F.M., 1982. Studies on the natural populations of Drosophila from Peruíbe (SP), Brazil (Diptera, Drosophilidae). Rev. Bras. Biol. 42, 539-544. and Bizzo et al. (2010)Bizzo, L., Gottschalk, M.S., De Toni, D.C., Hofmann, P.R.P., 2010. Seasonal dynamics of a drosophilid (Diptera) assemblage and its potencial as bioindicator in open environments. Iheringia Ser. Zool. 100, 185-191.. In the Restinga forest of São Paulo, the D. cardini group (non-D. polymorpha) and D. sturtevanti were common, and D. malerkotliana was uncommon; in Restinga of Santa Catarina, Za. indianus and D. fumipennis were common and D. nebulosa was uncommon.

Conclusion

Foremost, our study increases knowledge about Drosophilidae fauna in the Restinga forest of the Pampa biome. The assemblage species richness observed and the record of D. neosaltans for the state of Rio Grande do Sul suggest that HBITL is an important area for the maintenance of the species of this family in this ecosystem. Temperature was found to be the predominant influence on the assemblage; D. simulans and the D. willistoni subgroup display positive relationships with this climatic variable, whereas this relationship is negative for other species. Due to differences in latitude and physiognomy, the Drosophilidae taxa observed were distinct from those of Restinga forests in northern areas.

Acknowledgments

We would like to thank Prof. Dr. Vera Lúcia da Silva Valente, Prof. Dr. Lucas Poppe, Prof. Dr. Cristiano Agra Iserhard, Prof. Dr. Rafael Antunes Dias and the anonymous reviewers for their helpful comments. This work was supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) under grant n° 472973/2013-4. The collection was authorized by the Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio), under permanent license for collecting biological material n° 25454-1.

Appendix A Supplementary data

Supplementary data associated with this article can be found, in the online version, at doi:10.1016/j.rbe.2017.05.002.

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Publication Dates

  • Publication in this collection
    Jul-Sep 2017

History

  • Received
    14 Dec 2016
  • Accepted
    8 May 2017
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