Journal of Insect Science RESEARCH Open and Disturbed Habitats Support Higher Diversity of Syrphidae (Diptera)? A Case Study During Three Yr of Sampling in a Fragment of Araucaria Forest in Southern Brazil Jana Magaly Tesserolli de Souza,1 Renato Contin Marinoni,2 and Luciane Marinoni Departamento de Zoologia, Universidade Federal do Parana´, Caixa Postal 19020, CEP 81531-980, Curitiba, Parana´, Brazil 1Corresponding author, e-mail: [email protected] 2In memoriam Subject Editor: Marc De Meyer J. Insect Sci. 14(236): 2014; DOI: 10.1093/jisesa/ieu098 ABSTRACT. The diversity of hoverflies in five different habitats of the Parque Estadual de Vila Velha, Ponta Grossa, Parana´, Brazil, from September 1999 to August 2002 was studied. These five areas had been exposed to various types of anthropogenic disturbance at dif- ferent times, which resulted in different stages of plant succession. In total, 2,841 specimens of 151 species of Syrphidae were collected using malaise traps. The highest species richness and abundance were found at the edge of the forest (Forest Edge), whereas the lowest was found in the most conserved areas. Evenness values increased along the succession gradient. The accumulation curve of new oc- currences of syrphid species nearly approached an asymptote starting on the third month of the third year. Estimates of syrphid species richness using different methods indicated that between 155 and 288 species are found in the study area, according the Michaelis–Menten and the Chao2 estimators, respectively. The richness and abundance of representatives of the subfamily Syrphinae were higher in more open areas, where herbaceous plants predominate. Nineteen hoverfly species can be considered as environmental indicators, as they were collected exclusively or mainly in one of the defined habitat types. The degree of opening of the vegetation seems to be the factor determining the distribution of Syrphidae species, a conclusion based on the finding that grassy clearings in Araucaria Forests had more species. Hence, we conclude that, to become established, Syrphidae communities need conserved mosaic landscapes. Key Words: indicator species, hoverfly, malaise trap, plant succession, species richness estimator Insects provide easy, sensitive, and inexpensive ways to measure the limpos” associated with the Mixed Ombrophilous Forest (Araucaria effects of anthropogenic stress on the biodiversity and the environment Forest), which may form gallery forests or isolated woods across the (Kim 1993). Among them, the species of Syrphidae have great potential landscape, where the presence of the Araucaria angustifolia (Bertol.) as indicators of the environmental quality of forests (Thompson 1999, Kuntze (Parana-pine) is evident (Maack 1981, Veloso and Go´es Filho Smith et al. 2008). This is mainly because they are easily found in 1982). nearly all terrestrial ecosystems, and their larvae have highly diverse The survey was carried out in an area of Araucaria Forest at the feeding habits (Sommaggio 1999). PEVV. Five sites, characterized by varying degrees of plant succession Entomofaunistic surveys are relevant for understanding how insect (or environmental conditions due to management) were chosen: 1) for- communities are structured and may broaden our knowledge on est edge (located between the arboreal vegetation and the open area), 2) Neotropical Syrphidae. Thus, this study is an extension of the one de- Araucaria (planted forest of A. angustifolia); 3) Phase 1 (native forest in veloped by Jorge et al. (2007) on the syrphid diversity at the Parque an initial to intermediate stage of plant succession); 4) Phase 2 (native Estadual de Vila Velha (PEVV), Parana´ State, Southern Brazil. Jorge forest in an intermediate to advanced stage of plant succession); and 5) et al. (2007) studied the species collected during the first year of the Phase 3 (native forest in the most well conserved stage). The informa- project “Levantamento da Fauna Entomolo´gica no Parque Estadual de tion on the history of the anthropogenic disturbance and floristic differ- Vila Velha, Ponta Grossa, Parana´ – PROVIVE” (Ganho and Marinoni ences among the areas provided the basis for their recognition as 2003). Our investigation, carried out over a period of 3 yr, has gathered different habitats across the landscape (Ganho and Marinoni 2003). more striking results. We were able to perform both spatial and tempo- Collection, Mounting, and Identification. Insects were collected ral assessments of the diversity of Syrphidae and to establish relation- using malaise traps (Townes 1972). This collecting method has been ships between community structure in each of the five surveyed areas particularly useful in quantitative studies of Syrphidae (Owen and and their conservation status. Because differences in species composi- Owen 1990, Sommaggio 1999), even though it is logistically costly, tion decrease with increasing mobility of the organisms studied, we which makes it necessary to reduce replications (Burgio and also evaluated whether syrphid species, known for their outstanding Sommaggio 2007). Even if a small number of malaise traps are used, capacity to fly, are distributed evenly across the environment. the information provided by long-term monitoring can be very useful Furthermore, this study revealed potential indicator species of because these traps can sample both singletons and the most abundant Araucaria Forest habitats. species (Fraser et al. 2008). A trap was placed in each site, and the mate- rial was removed weekly for 3 yr (September 1999 to August 2002), Materials and Methods totaling 153 samples per area. Characterization of the Biome. The vegetation formation Campos After sorting and mounting the specimens, we identified them based Gerais do Parana´ is located in the Eastern region of the second plateau on keys available in the literature (Thompson 1999, Borges and of Parana´ (Southern Brazil), immediately following the Devonian Pamplona 2003, Marinoni et al. 2007, Borges and Couri 2009)by ridge, including a broad north–south stretch of natural grassland forma- comparing them with reference material in the Colec¸a˜o Entomolo´gica tions. It is characterized as a phytogeographical zone of “campos Padre Jesus Santiago Moure of the Zoology Department at the VC The Author 2014. Published by Oxford University Press on behalf of the Entomological Society of America. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact [email protected] 2 JOURNAL OF INSECT SCIENCE VOLUME 14 Universidade Federal do Parana´ (DZUP-UFPR) and using the help of Dr. Christian F. Thompson of the National Museum of Natural History, Table 1. Total abundance of Syrphidae and its subfamilies resulting Smithsonian Institution. As a result of our investigations, some changes from a survey using malaise traps in five areas of the PEVV, Ponta in the definition of complexes of cryptic species, as well as species with Grossa, Parana´, shown separately for each of the 3 yr and for the high intraspecific variability, were made, resulting in slight differences entire dataset (September 1999 to August 2002) between the current data and those presented by Jorge et al. (2007). Eristalinae Microdontinae Syrphinae Syrphidae These differences, however, have not resulted in a noticeable effect in 1999–2000 Forest edge 16 5 663 684 the comparisons of species richness and abundance and, therefore, have Araucaria 11 42 109 162 not altered the interpretations made in that study. Phase 1 26 33 191 250 The material has been deposited in the Colec¸a˜o Entomolo´gica Phase 2 26 26 51 103 Phase 3 12 44 90 146 Padre Jesus Santiago Moure (DZUP-UFPR). All the data are at the Total 91 150 1,104 1,345 database of the Taxonline - Rede Paranaense de Colec¸o˜es Biolo´gicas 2000–2001 Forest edge 4 10 459 473 (www.taxonline.ufpr.br) and the species list is in Appendix 1. Araucaria 8 25 39 72 Data Analysis Phase 1 6 14 48 68 Abundance and Species Richness. Abundance and species rich- Phase 2 5 26 22 53 Phase 3 4 13 15 32 ness were compared among the areas and the subfamilies of Syrphidae Total 27 88 583 698 (Eristalinae, Microdontinae, and Syrphinae) using generalized linear 2001–2002 Forest edge 4 4 534 542 models with a Poisson error distribution. Analyses and graphs were car- Araucaria 5 28 49 82 ried out in STATISTICA software 7.1 (StatSoft 2005). Phase 1 6 5 45 56 Evenness Index. The Simpson’s index (SD) provides the probabil- Phase 2 7 20 33 60 Phase 3 4 14 40 58 ity that two randomly selected individuals from an infinitely large com- Total 26 71 701 798 munity belong to the same species. It is one of the most popular and 1999–2002 Forest edge 24 (1) 19 (1) 1,656 (98) 1,699 robust diversity measures, because it captures the variance in the distri- Araucaria 24 (8) 95 (30) 197 (62) 316 bution of species abundance. It is heavily weighed by the most abun- Phase 1 38 (10) 52 (14) 284 (76) 374 Phase 2 38 (18) 72 (33) 106 (49) 216 dant species in the sample and less sensitive to species richness Phase 3 20 (8) 71 (30) 145 (61) 236 (Magurran 2004). The complement of this index (1 À SD ¼ SE) can be Total 144 (5) 309 (11) 2,388 (84) 2,841 considered a way of expressing the Simpson’s evenness index. The Values in parentheses correspond to relative frequency in percentage. dominance index of Berger and Parker (BPD) is defined by the ratio of the number of individuals in the most abundant species by the total number of captured individuals. The reciprocal of this index (1/BPD ¼ BPE) is the Berger and Parker evenness index.