Studies on Neotropical Fauna and Environment
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Drosophila (Diptera: Drosophilidae) survey in an ‘island’ of xerophytic vegetation within the Atlantic Forest biome, with emphasis on the repleta species group Rogério Pincela Mateus, Luciana Paes de Barros Machado & Daiane Priscila Simão-Silva To cite this article: Rogério Pincela Mateus, Luciana Paes de Barros Machado & Daiane Priscila Simão-Silva (2018): Drosophila (Diptera: Drosophilidae) survey in an ‘island’ of xerophytic vegetation within the Atlantic Forest biome, with emphasis on the repleta species group, Studies on Neotropical Fauna and Environment, DOI: 10.1080/01650521.2018.1438082 To link to this article: https://doi.org/10.1080/01650521.2018.1438082
Published online: 20 Feb 2018.
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STUDIES ON NEOTROPICAL FAUNA AND ENVIRONMENT, 2018 https://doi.org/10.1080/01650521.2018.1438082
Drosophila (Diptera: Drosophilidae) survey in an ‘island’ of xerophytic vegetation within the Atlantic Forest biome, with emphasis on the repleta species group Rogério Pincela Mateus
a
, Luciana Paes de Barros Machado
a
and Daiane Priscila Simão-Silva
a,b
a
Laboratório de Genética e Evolução, Programa de Pós-Graduação em Biologia Evolutiva, Departamento de Ciências Biológicas, Universidade Estadual do Centro-Oeste-UNICENTRO, Guarapuava, Brazil; bEscola de Saúde Agrociências e Biotecnologia, Pontifícia Universidade Católica do Paraná, PUC/PR, Curitiba, Brazil ABSTRACT
This work performed a seasonal and spatial survey of Drosophila groups, focusing on the repleta group species, in an enclave of xerophytic vegetation in the Araucaria forest phytophysiognomy. The Drosophilidae community, in terms of Drosophila groups, was seasonally affected probably because of cold winters of the highland Araucaria forest surveyed. The spatial variation of groups was not significant, but distinct distributions were observed, both in height and related to the fragment edge/interior, for some groups. Regarding the repleta group, no clear pattern of species seasonal and spatial distribution was detected, probably due to the observation that some species were collected in different seasons and occupied different regions of the area. The considerably high abundance of D. senei, compared to other studies, is one aspect that should be better investigated.
ARTICLE HISTORY
Received 1 July 2016 Accepted 2 February 2018 KEYWORDS
Biodiversity; community structure; Drosophila groups; cactophilic Drosophila; mixed ombrophilous forest
RESUMO
Neste trabalho foi realizado um levantamento espacial e sazonal da comunidade de grupos de Drosophila em um enclave de vegetação xerofítica da fitofisionomia Mata de Araucária, apresentando detalhes para as espécies do grupo repleta. A comunidade de Drosophilidae, em termos da composição de grupos, foi sazonalmente afetada provavelmente por causa dos invernos gelados da Mata de Araucária de altitude amostrada. A variação espacial dos grupos não foi significativa, porém distribuições distintas para alguns grupos foram observadas, tanto nos estratos quanto com relação ao posicionamento dentro do transecto (borda/interior). Com relação ao grupo repleta, não foi detecteado um padrão claro de distribuição sazonal e espacial das espécies, provavelmente devido ao fato de que algumas espécies foram coletadas em diferentes estações e ocuparam regiões diferentes dentro da área. A abundância consideravelmente alta de D. senei, comparada a outros trabalhos, é um aspecto que deve ser melhor investigado.
Introduction The number of Drosophilidae (Diptera) species that occur in Brazil was reported to be 305 (Tidon et al. 2016). According to a previous revision of Gottschalk et al. (2008), Drosophila is the most frequently investigated taxon in the family, the genus with the greatest number of species (181), with the best-resolved species distribution and it presents 28 species groups occurring in Brazil. One of these, the repleta group, currently comprises 105 species mostly allocated to six subgroups (Bächli 2018). Species in this group can be found in a variety of habitats (Sene et al. 1980), but more than half of these species are cactophilic, that is, adults visit several food sources in the environment (Morais et al. 1994) but lay eggs in decaying cactus cladodes. The CONTACT Rogério Pincela Mateus
[email protected]
© 2018 Informa UK Limited, trading as Taylor & Francis Group
Published online 20 Feb 2018
developing larvae feed on the yeasts that are part of the rotting process (Pereira et al. 1983; Starmer et al. 1986), according to the cactus–Drosophila–yeast system. Therefore, cactophilic species distribution is directly influenced by this ecological larval specificity because they are always associated with the host cactus (Sene et al. 1980; Ruiz & Heed 1988; Manfrin & Sene 2006). In South America, two dry woodland areas, the Caatinga in northeastern Brazil and the Chaco in northern Argentina, are isolated by a savanna corridor. This corridor, as described by Bucher (1982), is ‘sandwiched’ between the Atlantic and Amazonian rain forests, and forms the ‘dry diagonal’ (Prado & Gibbs 1993). Both Caatinga and Chaco present high density and diversity of cactus species (Hueck 1972; Prado & Gibbs 1993).
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R. P. MATEUS ET AL.
However, within the corridor and adjacent biomes, cacti can be found as isolated populations in rocky fields or sandy substrates, known as xerophytic enclaves (Ab’Saber 2000). The Atlantic Forest is one of these biomes and shows several phytophysiognomies throughout its distribution. In southern Brazil, the mixed ombrophilous forest is characterized by the presence of Araucaria angustifolia, being therefore also known as Araucaria forest (Galindo-Leal & CâMara 2003). Previous Drosophila surveys conducted in xerophytic enclaves within the Atlantic Forest (Mateus et al. 2006; De Toni et al. 2007) provided evidence that spatial and seasonal distribution of the species in the fragments is not uniform or ubiquitous. Assessing the spatial and temporal variations in the diversity patterns contributes to a better understanding of the processes that regulate biodiversity (Schluter & Ricklefs 1993). Moreover, environmental complexity and heterogeneity are important factors that determine the community composition, and spatial variation in relation to the species abundance is fundamental to understanding the community dynamics (Walla et al. 2004). In addition to structural variations of the Drosophilidae community, populations per se are entities that are in a state of change, and the seasonality of each species reflects a long and continuous process of adaptation to climatic conditions, and, therefore, seasonal variation can be critical for population fluctuation (Brncic et al. 1985). The aim of this work was to provide a pioneer understanding about the seasonal and spatial (border/ interior transect and height) variations in the distribution of Drosophila groups and, more specifically, of species of the repleta group, in an enclave of xerophytic vegetation in the Araucaria forest phytophysiognomy of the Atlantic Forest biome, comparing our data to other surveys in this biome and applying a standardized trapping procedure (Tidon & Sene 1988). Thus, we hope to contribute to better understand the Drosophilidae distribution in several environments within the Atlantic Forest biome helping future biota projects aiming to investigate Drosophilidae biodiversity in the Neotropical region.
Materials and methods
mesotermic subtropical climate (Cfb according to Köppen–Geiger climatic classification), with cool summers (mean temperature lower than 21°C) and cold winters characterized by frequent periods of intense frost. The mean annual temperature is 16.8°C, with mean maximum of 25.3°C and mean minimum of 6.8°C. Rain is evenly distributed all over the year. This fragment of Araucaria forest presents rocky outcrops (rocky fields) with xerophytic vegetation near the border with the crop areas. Sampling of Drosophilidae Samples were obtained during four seasons: winter (August 2004), spring (November 2004); summer (February 2005) and autumn (April 2005). Retention traps (Tidon & Sene 1988) were disposed on trees at two heights (1.5 m and 6.5 m) in five points, totaling 10 traps, making a transect from the border toward the interior of the Araucaria fragment: point 1 = edge – 5 m from the border; point 2 = transition 1 – 25 m; point 3 = transition 2 – 45 m; point 4 = interior 1 – 65 m; point 5 = interior 2 – 85 m. The species of cactus present in this area is predominantly encountered near the edge of the fragment (R. P. Mateus pers. obs.), and was identified as Cereus hildmaniannus. The retention traps, containing fermented banana and orange, were left at the sampling stations (points 1 to 5, at two different heights in each point) for three days. After this period, the adults were collected and transferred to vials containing the standard culture medium (Markow & O’Grady 2006). In the laboratory, non-repleta species were screened based on their distinct pigmentation and morphology patterns (FreireMaia & Pavan 1949; Frota-Pessoa 1954; Markow & O’Grady 2006), and then allocated to the group level. The species of the repleta group are difficult to distinguish because they display a very similar pattern of pigmentation. Therefore, collected males were identified by looking at the aedeagus morphology via genitalia dissections (Vilela 1983), and collected females were set to establish isofemale lines. The aedeagus morphology of the male progeny of these isofemale lines was examined. So, collected females that generated descendants were also identified by examining the aedeagus morphology of male progeny.
Study site Samples were collected in a fragment of Araucaria forest surrounded by crop areas of Rio do Poço farm, a rural area of Guarapuava, PR, Brazil (25°28ʹ67ʺS, 51° 87ʹ62ʺW, 1120 m asl), located 45 km northwest of the city (Rio do Poço hereafter). The region has a humid
Data analyses The absolute (A) and relative (r) abundances, Shannon–Wiener diversity index estimated according to Krebs (1999), Margalef richness (DMg) and Pielou evenness (J′) indices estimated according to Ludwig
STUDIES ON NEOTROPICAL FAUNA AND ENVIRONMENT
and Reynolds (1988) were obtained in PAST software (Hammer et al. 2001). In order to determine the importance of seasonal and spatial collection, we performed a PERMANOVA, i.e. permutational multivariate analysis of variance (Anderson 2001), using the abundance of Drosophila groups and repleta group species. First, a measure of β-diversity, the Bray– Curtis similarity index, was calculated after standardizing the data by the total (this minimizes the effect of different sizes among samples), and then the indices were square root transformed (this balances the contribution of common and rare groups/species). Three factors were used in the analyses: season (fixed), points (fixed) and height (nested into points and, therefore, random). A principal coordinates ordination analysis (PCoA) was also performed to show the dissimilarity relations among samples. Uninformative samples were excluded from the analyses. All these analyses were realized in Primer v7 software (Clarke & Gorley 2015). The changes in composition of groups between seasons and points of collection were analyzed using Morisita similarity index in the UPGMA clustering method (Ludwig & Reynolds 1988).
Results
3
(i.e. those with at least 5% of total relative abundance), a seasonal variation was evident (Table 1). The melanogaster group was the most common in almost all seasons, except spring. In fact, spring and autumn were the seasons when other groups increased their relative abundance (repleta, tripunctata and bromeliae groups in spring; guarani and tripunctata in autumn). The cardini group showed highest relative abundance in summer (Table 1). The PCoA corroborated this seasonal effect (Figure 1a). The PERMANOVA analysis (Table 2) showed that the seasonal variation of the Drosophila groups was the only significant factor and contributed 30.19% to the total variability. The residual variation was also large (24.17%) and it was interpreted as the variability among traps (Table 2). The ecological parameters reflected the significant seasonal variation (Table 3). The number of individuals sampled was highest in summer and lowest in spring. Spring was the more diverse, the second richest, and the most equitable. Also, community structure in summer and winter were more similar to each other than to the other samples, and they were joined in the UPGMA dendrogram, separated from autumn and spring (Figure 2a). This last one was the most dissimilar from the others, according to the Morisita similarity index.
Drosophila groups seasonal distribution A total of 1670 Drosophila individuals of three subgenera (Dorsilopha, Drosophila and Sophophora) and 15 species groups were collected at Rio do Poço (Table 1). No other drosophilid genus was detected in this area during the sampled period. Among the main groups
Drosophila groups spatial distribution Despite no significant variation in the PERMANOVA analysis for both factors (points and heights; Table 2), some patterns of spatial
Table 1. Seasonal absolute (A) and relative (r) abundance of each Drosophila group in the Araucaria forest fragment with enclave of xerophytic vegetation in Rio do Poço farm, Guarapuava, PR, Brazil. Winter Groups Subgenus Dorsilopha - busckii group Subgenus Drosophila - annulimana group - bromeliae group - caponei group - canalinea group - cardini group - coffeata group - dreyfusi group - guarani group - immigrans group - repleta group - tripunctata group Subgenus Sophophora - melanogaster group - saltans group - willistoni group Total specimens
Spring
Summer
Autumn
Total
A
r
A
r
A
r
A
r
A
r
10
2.20
7
4.30
1
0.15
–
–
18
1.08
1 – – – 46 – – 4 – 62 1
0.22 – – – 10.11 – – 0.88 – 13.62 0.22
– 41 – 1 16 – – 5 4 42 26
– 25.15 – 0.61 9.82 – – 3.07 2.45 25.77 15.95
1 – 3 8 148 3 5 8 2 41 34
0.15 – 0.44 1.18 21.80 0.44 0.73 1.18 0.29 6.04 5.01
1 7 – 1 50 8 21 67 – 5 56
0.27 1.88 – 0.27 13.40 2.14 5.63 17.96 – 1.34 15.01
3 48 3 10 260 11 26 84 6 150 117
0.18 2.87 0.18 0.60 15.57 0.66 1.56 5.03 0.36 8.98 7.00
331 – – 455
72.75 – –
18 2 1 163
11.04 1.23 0.61
412 11 2 679
60.68 1.62 0.29
155 – 2 373
41.56 – 0.54
916 13 5 1670
54.85 0.78 0.30
Notes: Winter: August 2004; Spring: November 2004; Summer: February 2005; Autumn: April 2005.
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R. P. MATEUS ET AL.
Figure 1. Principal coordinates ordination of collections performed in Rio do Poço farm showing the dissimilarity among seasons. Each point represents the centroid of the trap in a specific point and height. (a) Drosophila groups; (b) D. repleta group species.
Table 2. Permutational multivariate analysis of variance (PERMANOVA) using Bray–Curtis similarity calculated from standardized and square root transformed abundances of Drosophila groups. Drosophila groups Source
df
Pseudo-F
Season Point Height (point) Season × point Residual
3 4 5 12 13
5.4137 1.1461 0.97252 1.064
Drosophila repleta group species Contribution (%) 30.19* 8.29 9.04 23.73 24.17
df
Pseudo-F
3 4 4 7 2
1.0847 0.63564 3.7616 2.8693
Contribution (%) 5.31 17.57 24.56 32.79 3.26
*p < 0.001.
Table 3. Seasonal, height and spatial alpha diversity in the Araucaria forest fragment with enclave of xerophytic vegetation in Rio do Poço farm, Guarapuava, PR. Winter Spring Summer Autumn Height 1.5 m Height 6.5 m Edge Transition 1 Transition 2 Interior 1 Interior 2 Total
A 455 163 679 373 906 764 326 317 352 301 374
H′ 0.8872 1.9101 1.2637 1.6640 1.5746 1.4580 1.4655 1.6317 1.5290 1.2349 1.4677 1.5496
DMg 0.9803 1.9632 1.9937 1.6887 1.7624 1.9583 1.7280 1.9101 1.7054 1.5770 1.8568 1.8866
J′ 0.4559 0.7966 0.4788 0.6939 0.6139 0.5525 0.6112 0.6566 0.6377 0.5363 0.5906 0.5722
Notes: A = absolute abundance; H′ = Shannon-Wiener diversity index; DMg = Margalef richness index; J′ = Pielou evenness index.
variation for the Drosophila groups were observed in Table 4. For example, among the main groups, the repleta group occurred with higher abundance in the
points near the edge (edge and transition 1 and 2 points), the relative abundance of the guarani group was highest in transition 2 and interior 2, and the relative abundances of the cardini, tripunctata and melanogaster groups seemed to be more evenly distributed. Considering the other groups, the canalinea group was detected only near the edge and at 6.5 m from the ground, the saltans, annulimana, caponei, coffeata, immigrans, and willistoni groups had very low abundances and, therefore, no clear pattern (Table 4). Regarding the ecological parameters (Table 3), transition 1 presented the highest and interior 1 the lowest values for all indices, and the community at 1.5 m had higher Shannon diversity and evenness indices, but that at 6.5 m had a higher Margalef richness index. The cluster analysis showed that the community structure was more similar near the edge and then became more dissimilar towards the interior (Figure 2b).
STUDIES ON NEOTROPICAL FAUNA AND ENVIRONMENT
5
Figure 2. UPGMA clustering dendrograms, using Morisita similarity indexes, among collections in the Araucaria forest fragment with enclave of xerophytic vegetation in Rio do Poço farm, Guarapuava, PR. (a) Seasonal collections (r = 0.9877); (b) Spatial collections (r = 0.8626). Points are described in the Materials and methods section. Table 4. Spatial absolute (A) and relative (r) abundance of each Drosophila group in the Araucaria forest fragment with enclave of xerophytic vegetation in Rio do Poço farm, Guarapuava, PR. The points are described in the Materials and methods section. Edge Groups Subgenus Dorsilopha
1.5 m A
- busckii group 6 Subgenus Drosophila - annulimana group – - bromeliae group 7 - caponei group – - canalinea group – - cardini group 34 - coffeata group 9 - dreyfusi group 1 - guarani group 1 - immigrans group – - repleta group 24 - tripunctata group 24 Subgenus Sophophora - melanogaster group 127 - saltans group 5 - willistoni group – Total 238
Transition 1 6.5 m
1.5 m
Transition 2
6.5 m
1.5 m
Interior 1
6.5 m
1.5 m
Interior 2
6.5 m
1.5 m
6.5 m
r
A
r
A
r
A
r
A
r
A
r
A
r
A
r
A
r
A
r
2.52
–
–
1
0.54
2
1.54
3
1.22
–
–
5
5.10
–
–
1
0.72
–
–
– 1 – – 17 – 4 5 – 23 21
– 0.54 – – 9.09 – 2.14 2.67 – 12.3 11.23
1 9 – 8 19 – 3 4 – 24 6
0.77 6.92 – 6.15 14.61 – 2.31 3.08 – 18.46 4.62
1 1 – – 27 1 6 30 – 21 8
0.41 0.41 – – 11.02 0.41 2.45 12.24 – 8.57 3.27
– 9 – – 22 1 3 6 – 23 2
– – – 8.41 – – – – – – – – 20.56 26 26.53 0.93 – – 2.80 4 4.08 5.61 6 6.12 – 4 4.08 21.50 2 2.04 1.87 14 14.29
– 5 – – 13 – – – – 16 6
– 2.46 – – 6.40 – – – – 7.88 2.96
1 3 – – 26 – 5 15 – – 17
0.72 2.17 – – 18.84 – 3.62 10.87 – – 12.32
– 13 3 – 64 – – 17 2 6 9
– 5.51 1.27 – 27.12 – – 7.20 0.85 2.54 3.81
– – – 2.94 – – – – – – 2 2.27 14.28 12 13.64 3.78 – – 0.42 – – 0.42 – – – – – 10.09 11 12.50 10.09 10 11.36
53.36 53 60.23 108 57.75 54 41.54 147 60.00 38 35.51 36 36.73 163 80.30 70 50.72 120 50.85 2.1 – – 3 1.6 – – – – 3 2.80 – – – – – – 2 0.85 – 1 1.02 – – – – – – – – – 4 2.14 – – – – – 88 187 130 245 107 98 203 138 236
The repleta group A total of 150 specimens were identified as members of the repleta group: 89 males and 61 females of which 10 (all D. mercatorum) were identified after the establishment of isofemale lines (Tables 5 and 6). Among the six identified species of the repleta group, the most abundant were D. mercatorum (57), D. antonietae (23) and D. senei (12). Drosophila mercatorum was more evenly distributed
through the seasons, with exception of the autumn (only one specimen collected). Drosophila antonietae and D. senei were most abundant in winter and less abundant in autumn (Table 5). Drosophila mercatorum and D. antonietae were collected in all seasons; the only specimen of D. onca was collected during summer, D. fascioloide occurred in the winter and spring, and D. hydei was collected in the winter and summer.
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R. P. MATEUS ET AL.
Table 5. Seasonal absolute (A) and relative (r) abundance of the Drosophila species of the repleta group collected in the Araucaria forest fragment with enclave of xerophytic vegetation in Rio do Poço farm, Guarapuava, PR. Winter Species D. antonietae D. fascioloide D. hydei D. mercatorum D. senei D. onca Unidentified females Total
A 11 1 1 21 9 – 19 62
Spring
r 17.74 1.61 1.61 33.87 14.52 – 30.65
A 7 2 – 18 1 – 14 42
Summer r 16.67 4.76 – 42.86 2.38 – 33.33
A 4 – 2 17 2 1 15 41
Autumn
r 9.76 – 4.88 41.46 4.88 2.44 36.58
A 1 – – 1 – – 3 5
Total
r 20.00 – – 20.00 – – 60.00
A 23 3 3 57 12 1 51 150
r 15.33 2.00 2.00 38.00 8.00 0.67 34.00
Table 6. Spatial absolute (A) and relative (r) abundance of the Drosophila species of the repleta group collected in the Araucaria forest fragment with enclave of xerophytic vegetation in Rio do Poço farm, Guarapuava, PR. The points are described in the Materials and methods section. Edge 1.5
Transition 1 6.5
1.5
Transition 2
6.5
1.5
Interior 1
6.5
1.5
Interior 2 6.5
1.5
6.5
Species
A
r
A
r
A
r
A
r
A
r
A
r
A
r
A
r
A
r
A
r
D. antonietae D. fascioloide D. hydei D. mercatorum D. senei D. onca Unidentified females Total
13 1 – 2 – – 8 24
54.17 4.17 – 8.33 – – 33.33
– – 1 5 1 – 4 11
– – 9.09 45.45 9.09 – 36.36
3 – – 9 3 – 8 23
13.04 – – 39.13 13.04 – 34.78
– 2 2 11 – 1 8 24
– 8.33 8.33 45.83 – 4.17 33.33
7 – – 2 5 – 7 21
33.33 – – 9.52 23.81 – 33.33
– – – 15 – – 8 23
– – – 65.22 – – 34.78
– – – 1 – – 1 2
– – – 50.00 – – 50.00
– – – 9 2 – 5 16
– – – 56.25 12.50 – 31.25
– – – – – – – –
– – – – – – –
– – – 3 1 – 2 6
– – – 50.00 16.67 – 33.33
Spatially, no fly of the repleta group was obtained at 1.5 m of the interior 2 point. Drosophila mercatorum was collected in all points of the transect, and it was almost threefold more abundant in the upper stratum of the forest. Drosophila antonietae, the second most abundant, was found only in the lower stratum of the forest and over the three first points, that is, closer to cacti. The third most abundant species, D. senei, had twice the number of individuals collected in the lower (8) than in the upper (4) stratum. Drosophila hydei and D. onca had low abundances, and, therefore, no clear pattern can be attributed to these species (Table 6). However, the PERMANOVA analysis evidenced that no factor, season, point or height, contributed significantly to these variations pointed out above (Table 2). This result was corroborated by the PCoA analysis (Figure 1b).
Discussion Drosophila groups: seasonal and spatial distribution The significant variation of the Drosophila groups and the ecological indices, considering seasons, reinforces that this aspect is important and must be considered when performing collections of Drosophilidae in any area of interest (Da Mata
et al. 2015a). Bizzo et al. (2010), collecting in a well preserved beach forest fragment (restinga) at the south Brazilian coast, observed lower abundances in winters, the coldest and driest period, as also previously registered in several other Brazilian localities (Saavedra et al. 1995; Tidon-Sklorz 2006; Torres & Madi-Ravazzi 2006; De Toni et al. 2007; Mendes et al. 2017). They also detected the highest species diversity in this season, irrespectively of abundance. They stated that these results seem to be common of drosophilid assemblages. However, our data did not corroborate that, as the lowest abundance and the highest diversity were detected in spring. TidonSklorz and Sene (1992) also reported the same pattern as detected here, collecting in woodland of semideciduous seasonal forest in the interior of São Paulo state. In our case, the results are probably related to the fact that the highland Araucaria forest surveyed presents much colder winters, allowing mostly the melanogaster group species to survive/breed and lowering the possibility of species other than those to increase their number. Comparing our summer data with two other surveys made in the same season, Mateus et al. (2006) and De Toni et al. (2007), two groups (canalinea and coffeata) were exclusive of Rio do Poço. Five groups (caponei, dreyfusi, repleta, saltans, and tripunctata) had abundances similar to other areas of xerophytic vegetation
STUDIES ON NEOTROPICAL FAUNA AND ENVIRONMENT
within dense ombrophilous forest phytophysiognomy of the Atlantic Forest remnants of Santa Catarina state (De Toni et al. 2007). Two groups (busckii and melanogaster) were more similar with samples of the seasonal semideciduous forest phytophysiognomy of the Atlantic Forest of Paraná state (Mateus et al. 2006). Three groups, immigrans, immigrans, and annulimana, were similar with both other surveys above. Finally, two groups, guarani, and willistoni, had peculiar abundances, that is, their abundances were not similar with any other area. Both spatial distributions, points in the transect and height, of Drosophila groups did not show significant variation, probably because different species within groups occupy distinct regions of the area, preventing the observation of clear patterns of Drosophila group spatial distribution. This was clear when the distribution of species of the Drosophila repleta group was analyzed. However, a closer look at the Drosophila group data, despite no significant variation, revealed some interesting results. For example, despite showing opposite results, a stratified distribution was also observed by Tidon-Sklorz and Sene (1992) in a seasonal semidecidual forest, another phytophysiognomy of the Atlantic Forest biome. They detected that almost all species were collected in the lower stratum of the forest and, among the main collected species (abundance > 30 individuals) that presented clear pattern of height distribution, most occurred above 6 m from the ground, showing greater richness in the lower portion and higher diversity in the upper portion of the forest. In temperate regions, studies of Drosophilidae showed the same type of vertical distribution, with preferential occurrence in the canopy, and some species being restricted to this stratum (Shorrocks 1975; Lumme et al. 1979; Beppu 1985; Toda 1986; Tanabe 2002). We detected the opposite, i.e. higher diversity in the lower portion and higher richness in the upper portion of the Araucaria forest. These results are in agreement with Young and Mitchell (1994), who showed that forests with closed canopy tend to have more heterogeneous vertical/horizontal diversity, and forests with openings and edge areas have a more complex threedimensional pattern. Regarding the Drosophila groups’ distribution in the transect, Penariol and Madi-Ravazzi (2013), studying the distribution gradient in the abundance of drosophilid species along an edge–interior transect in a semideciduous forest fragment, established an edge extent of 60 m, with the edge region being characterized by the presence of invader species (such as D. simulans and Z. indianus). Native species (such as those belonging to D. willistoni and D. tripunctata groups) were mainly associated with the forest interior. Here we detected a similar pattern
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when analyzing the native guarani group, which occurred mostly in the interior. However, a different pattern was observed for the native tripunctata and the exotic melanogaster groups while the low abundance of the willistoni group precluded such conclusions. Another observation that is interesting to point out is the absence of other genera of Drosophilidae in our surveys, in spite of four samplings made over the course of one year. Cavasini et al. (2014) performed collections with similar sampling effort in two other Araucaria forests close to Guarapuava (however, without an enclave of xerophytic vegetation), and they obtained two species of genera other than Drosophila: Scaptodrosophila latifasciaeformis, and Zaprionus indianus. Mateus et al. (2006), collecting in eight inland Atlantic Forest areas with enclaves of xerophytic vegetation (including four located in Paraná), also detected these two other genera. De Toni et al. (2007), collecting in Atlantic Forest areas with xerophytic enclaves on islands of the Santa Catarina state coast, also detected these two genera, and two others, Rhinoleucophenga and Zygothrica. All these previous studies obtained a small number of individuals for these genera, indicating that they probably naturally occur with very low abundances. Three aspects could be responsible for these results: humidity, temperature and the mode of sampling. Several examples are available in the literature showing that high humidity results in higher abundance and diversity of Drosophila community in distinct Neotropical environments (Saavedra et al. 1995; Torres & Madi-Ravazzi 2006; De Toni et al. 2007; Bizzo et al. 2010; Roque et al. 2013; Da Mata et al. 2015b; Monteiro et al. 2016). The same has been observed regarding temperature (Torres & Madi-Ravazzi 2006; HochmüLler et al. 2010; Poppe et al. 2012; Mendes et al. 2017). Also the type of bait used could be another factor for this result because it attracts mainly the frugivorous species. Fungivorous, florivorous, cactophilic and leaf-mining species, and/or species that feed on decomposing wood or that show parasitic/predatory behavior are only seldom attracted by the bait used (Gottschalk et al. 2008). Poppe et al. (2012) suggested that the lower frequency of invasive Z. indianus in the Pampa could be due to the proximity to the southernmost limit that the distribution of this species reached after the invasion event in 1999 (Moraes et al. 2000), being therefore composed of marginal populations that are submitted to suboptimal conditions and also limited by climatic features, such as lower temperatures. Cavasini et al. (2014) also indicated that the limiting factor for the establishment of Z. indianus in highland Araucaria forest is probably lower temperatures, mostly because the collected individuals were obtained during summer.
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Therefore, the absence of these other genera, Zaprionus, Scaptodrosophila, Rhinoleucophenga, and Zygothrica, in our samples, despite collecting during a period of one year (including summer), might be due to their natural low abundance in drosophilid surveys in South America (e.g. Döge et al. 2008; Bizzo et al. 2010; Penariol & MadiRavazzi 2013), associated with the limiting factor low mean temperature in the area of collection. The repleta group The temporal and both spatial (points in the transect and height) distributions of the species of the Drosophila repleta group showed no significant variation. This result is due to the observation that few species of this group were collected in distinct seasons and that they occupied different regions of the sampled area, resulting in the absence of clear patterns of distribution. Those that presented some visual pattern had low abundance. From our data, it can be pointed out that the repleta group composition observed here was similar to the general data obtained by De Toni et al. (2007). The exceptions were that they collected D. repleta and D. zottii, which we did not observe here, and the third most abundant species we collected was Drosophila senei, which they did not detect there. In fact, this is the first record of this species in Paraná state, despite other collections in several other areas made by Mateus et al. (2006). Drosophila mercatorum was the most abundant species of the repleta group in our survey and in all collection sites of De Toni et al. (2007). It was collected in our work in all seasons, points of the transect and in both strata of the forest. De Toni et al. (2007) observed higher abundances in spring and summer. Thus, it seems that the repleta group composition in xerophytic vegetation within Araucaria forest (mixed ombrophilous forest) and within dense ombrophilous forest phytophysiognomies of the Atlantic Forest are strongly shaped by the xeric vegetation. Our second most abundant species of the repleta group was D. antonietae, which was found only in the lower stratum of the forest and over the three first points (edge and transitions 1 and 2), that is, closer to cacti. This species belongs to the cactophilic D. buzzatii cluster, together with six other species: D. borborema, D. buzzatii, D. gouveai, D. koepferae, D. serido, and D. seriema (Manfrin & Sene 2006). The distribution of D. antonietae is mainly associated with cacti of the genus Cereus, which can be found in remnants of xerophytic vegetation in the Paraná river basin, in the south and southeastern regions of Brazil, and north of the eastern limits of the Argentinean Chaco (Tidon-Sklorz & Sene 2001; Manfrin & Sene 2006;
Mateus et al. 2006). The Rio do Poço farm is located in the Cavernoso river basin, which is a tributary of the Iguassu river that flows into the Paraná river. Thus, as expected, in our collections D. antonietae was one of the most abundant species of the repleta group, after D. mercatorum. Mateus et al. (2006), collecting with open traps, obtained much higher numbers of this species in half of their sample locations (four of eight), but lower numbers than ours in the other half. They argued that the low numbers obtained in some areas are due to their high level of environmental degradation. Therefore, our results for this species, associated with Mateus et al. (2006), revealed that not only the type of trap but also the conservation status of the location is important when performing collections of endemic drosophilids. In conclusion, our surveys provided information that, together with previous published data, can give a robust base of knowledge that can help other researchers interested in studying the Drosophilidae biodiversity in the Neotropical region. The main contributions are the clear seasonal variation, probably because of much colder winters of this region compared to other similar areas in Brazil, the specificity of some groups concerning height and/or location distribution related to the edge/interior of the fragment, and, regarding the repleta group, the clear pattern of D. antonietae spatial distribution due to the presence of its host cactus. Finally, the considerably higher abundance of D. senei than in other studies is one aspect that should be further investigated.
Acknowledgments We are thankful to A Scherloski, R Cavasini, EC Gustani, JP Pericolo, K dos Santos, KCB Oliveira, NS Alves, NP Heinz, PT Rodrigues and VF Lopes for technical assistance in the collections; to Dr. Maria Luisa T Buschini for help with the ecological analyses; to the two referees for the useful suggestions; and to Dr. Anne Zillikens, Editor-in-Chief of SNFE, for the first and last comments and suggestions that truly improved this article.
Disclosure statement No potential conflict of interest was reported by the authors.
Funding This work was supported by the Fundação Araucária [grants 103/2005, 231/2007 and 415/2009] (Rogerio P. Mateus); and Master Fellowship (Daiane P. Simão-Silva); Conselho Nacional de Desenvolvimento Científico e Tecnológico – CNPq [grant 477696/2004-0] (Rogério P. Mateus); FINEP [grants 01.05.0420.00/2003, 1663/2005], CAPES and UNICENTRO.
STUDIES ON NEOTROPICAL FAUNA AND ENVIRONMENT
ORCID Rogério Pincela Mateus http://orcid.org/0000-00017874-1149 http://orcid.org/0000Luciana Paes de Barros Machado 0002-3197-0187 http://orcid.org/0000-0002Daiane Priscila Simão-Silva 1633-9899
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