TY - JOUR
AU - Mulieri, Pablo, R
AB - Abstract Sarcophagidae (Diptera) are of great interest from a veterinary, medical, and forensic viewpoint, and are potential bioindicators for environmental impact assessments. In this study, we evaluated changes in abundance, species richness, and diversity of flesh flies in different habitat types in the Humid Chaco ecoregion of South America: 1) anthropized habitats: urban, cattle farm, and alfalfa crop, and 2) natural habitats: savanna and forest. We hypothesized that sarcophagid fly community parameters are affected by the anthropization and that spatial turnover will contribute more to the overall beta diversity than nestedness between habitats. In each habitat, samplings were conducted monthly from March 2015 to February 2016 in 25 sites, 5 per habitat, totaling 300 independent samples at the end of the study. We collected 5,790 Sarcophagidae (55 species). Community parameters of Sarcophagidae were evaluated and compared. The ecological effects of anthropization and habitat type were observed in the present study. As expected, our results showed the highest abundance, species richness, and diversity in the savanna and forest habitats (natural), whereas the lowest values were registered in the urban and alfalfa crop habitats, supporting the hypotheses of anthropization as the main driver of diversity loss. In addition, sarcophagid assemblages differed between all habitats and the overall dissimilarity was structured by spatial turnover. The main conclusion of this research is that flesh fly community structure is greatly affected by anthropization and habitat type, and this would be related to canopy cover and microclimate conditions of each environment. Graphical Abstract Open in new tabDownload slide Graphical Abstract Open in new tabDownload slide anthropogenic impact, biodiversity, community composition, flesh fly, Neotropical region The human influence in natural ecosystems, environments, and landscapes, also known as anthropization, not only generates changes in vegetative physiognomies promoting habitat fragmentation, but also creates new resources for the development of many invasive organisms (McKinney 2002) and leads to habitat loss for native species (Blair 2001, McKinney 2008). Indeed, destruction of natural habitats is the primary cause of global biodiversity decline across all major taxonomic groups (Dirzo and Raben 2003, Rands et al. 2010, Newbold et al. 2016). Insect biodiversity is threatened worldwide, and the main driver of species decline is habitat loss and conversion to intensive agriculture and urbanization (Sánchez-Bayo and Wyckhuys 2019). Several studies on insect diversity, that compare community compositions among habitats, have shown that the changes in diversity patterns in species composition are essential for the understanding and monitoring of both natural and anthropogenic impacts on the biota of a given area (Lawton et al. 1998, Marinoni and Ganho 2006, Patitucci et al. 2011, Ferraguti et al. 2016, Pereira de Sousa et al. 2016). Thus, insects are an excellent focus group for studying effects from anthropization. They are highly diverse and thus may provide a snapshot of biological diversity in an area, they are relatively easy to sample, and, in some cases, they represent important economic, medical, or social components of human-altered habitats. In fact, insects have many species adapted to environmental changes caused by humans (McIntyre 2000). Investigations on diversity of flies (Diptera) comparing anthropized and natural environments have focused only on some groups like Drosophilidae (Da Mata and Tidon 2013), Psychodidae (Ramos et al. 2014), and some sarcosaprophagous Calyptratae families (Patitucci et al. 2011, 2013; Dufek et al. 2016; Barbosa et al. 2017). Nevertheless, the level of habitat disturbance was crucial for the occurrence of species in all cases. While some species of Calyptratae flies have frequently been associated with human settlements, others can help to indicate the conservation status of an environment owing to their restricted distribution to preserved habitats (Cabrini et al. 2013, Souza and Zuben 2016). Thus, the structure of landscapes may be important for explaining and understanding fly ecology with factors such as the location of breeding sites, resting places, feeding sources, as well as landscape heterogeneity possibly influencing fly movement and spatial distribution. Sarcophagidae (Diptera) is one of the most diverse families of calyptrate flies, with more than 3,000 described species (Pape et al. 2011). They have a high species richness and abundance, are important in ecosystem functioning, play many ecological roles, and have a wide distribution (Pape and Dahlem 2010). Many flesh flies are usually included within the so-called sarcosaprophagous guild because their larvae are scavengers (necrophagous) or dung feeders (coprophagous) (Brown et al. 2010, Marshall 2012). From the medical and veterinary viewpoint, flesh flies are mechanical carriers of human pathogens (Graczyk et al. 2005, Sukontason et al. 2006) and larvae are myiasis producers in humans and domestic animals (Hagman et al. 2005, Bermúdez et al. 2010, Mulieri et al. 2018). Flesh flies are forensically relevant because they are some of the first insects that colonize human cadavers (Amendt et al. 2011). Thus, sarcophagid flies can be used to estimate the minimum postmortem interval (PMImin; Segura et al. 2009, Oliveira and Vasconcelos 2010). In addition, Sarcophagidae species have been identified as indicators of urban or rural environments in forensic investigations (Fremdt and Amendt 2014). Sarcophagid flies are sensitive to anthropogenic impact (Pape and Dahlem 2010). Some species have high preference for human settlements or eusynanthropic behavior and have been proposed as potential bioindicators for impact assessments (Yepes-Gaurisas et al. 2013, Sousa et al. 2015, Dufek et al. 2016, Souza and Zuben 2016). In fact, Sarcophagidae species can be used in monitoring forest restoration, due to their numerical representativity, great variety of occupied niches and interaction at many trophic levels (Majer 1987). Hence, the development of knowledge about communities that occupy different habitats along a gradient of human impact is not only valued by community ecologists, but is also one of the basic tools in the fields of medical, veterinary, and forensic entomology. In the Neotropics, few studies have explored the biodiversity and abundance of Sarcophagidae between environments with different levels of anthropogenic intervention within temperate and tropical areas. These studies attempted to identify which species are associated with a variety of natural habitats, such as endemic species inhabiting pristine forest and open habitats, or those species which are associated with urban and rural environments (Linhares 1981, Mulieri et al. 2011, Beltran et al. 2012, Carmo and Vasconcelos 2016, Dufek et al. 2016, Souza and Zuben 2016). Given this, the type of vegetation and the habitat heterogeneity appear to be the key factors in determining the characteristics of sarcophagid communities (Pereira de Sousa et al. 2016). However, when taking into consideration their high richness and level of endemism, there is a lack of information for a large number of species because many ecoregions remains unstudied. The Chaco region extends from southern Bolivia, west Paraguay, southern Brazil, and North-central Argentina, and is one of the largest forested areas in South America (Olson et al. 2001). Rainfall defines an east–west decreasing gradient of humidity in this region, dividing it into two sectors: the eastern sector, belonging to the Humid Chaco, and the western sector, belonging to the Dry Chaco (Cabrera and Willink 1973). Particularity, due to hydrological, geomorphological, and climatic characteristics of the Humid Chaco, landscapes are composed of a diverse variety of habitats, both natural (e.g., gallery forests, palms forests, grasslands, savannas, wetlands) and anthropized (e.g., urban areas, exotic tree plantations, cattle farms, small-scale crops) (Ginzburg and Moli 2005, Oakley et al. 2005, Giraudo et al. 2013). Regarding the conservation status of this ecoregion, the main threats to the natural ecosystems are the overgrazing of livestock, seasonal fires and the transformation of natural habitats for agricultural activities. The changes produced by anthropic action, such as the advance of the agricultural frontier, have resulted in deforestation and monospecific crops. In fact, the Chaco region exhibits one of the highest deforestation rates worldwide (Dinerstein et al. 1995, Aide et al. 2013). The main aim of this research was to explore changes in abundance, species richness, and diversity between both natural (savanna and forest) and anthropized (urban, cattle farm, and alfalfa crop) habitats to evaluate the effect of anthropization on flesh fly community composition in the Humid Chaco ecoregion. This research aimed to find the pattern of diversity in sarcophagid flies, describe the community parameters between different types of habitats and test our hypothesis that community parameters of the Sarcophagidae species are affected by anthropization. In addition, we partitioned beta diversity into its turnover and nestedness components to examine the overall dissimilarity of the flesh fly community between habitats. The results of this research may offer a valuable insight to be used in a medical, veterinary, forensic, and environmental context. Materials and Methods Study Area Samplings of flesh flies were carried out in different habitats located in San Lorenzo Department, Chaco Province, Argentina (27° 17′ S; 60° 25′ W) (Fig. 1a). This Department has a population of 14,702 inhabitants (Indec 2010) and an area of 2,135 km2. It is characterized by intense human activities as livestock and wood exploitation for firewood and charcoal (Ginzburg and Moli 2005, Giraudo et al. 2013) and is located in the Humid Chaco ecoregion (Olson et al. 2001). The climate is subtropical with a mean annual precipitation of 1,300 mm and an average temperature of 28°C in the summer and 18°C in the winter (Bruniard 1999, Morello 2012). Fig. 1. Open in new tabDownload slide Location of study area in the Humid Chaco ecoregion of Argentina, showing the general structure of habitats sampled. (a and b) Geographical location of the study area; (c) urban; (d) cattle farm; (e) alfalfa crop; (f) savanna; (g) forest. Fig. 1. Open in new tabDownload slide Location of study area in the Humid Chaco ecoregion of Argentina, showing the general structure of habitats sampled. (a and b) Geographical location of the study area; (c) urban; (d) cattle farm; (e) alfalfa crop; (f) savanna; (g) forest. To evaluate the community composition of flesh flies in different natural and anthropized habitats, we selected five types of representative habitats of this ecoregion, separated by at least 4 km from each other to guarantee spatial independence (Fig. 1b). In this study, a ‘habitat’ is defined as an area with similar environmental characteristics that differ in nature or appearance from the surrounding environment (e.g., differences in land cover or physical structure) and that have biological significance for the organism under consideration (Wiens 1976, Krebs 1994). These five habitats were arranged into two subgroups: 1) anthropized habitats and 2) natural habitats. We considered a habitat as ‘anthropized’ if its original vegetation or structure was modified by human action. 1) Urban: Villa Berthet (27° 17′09″ S; 60° 24′22″ W), Capital City of San Lorenzo Department, with a population of 12,029 inhabitants (Indec 2010). It is characterized by intense human activity, presence of pet animals and exotic vegetation, untreated garbage and houses without sewers. Sample points within this habitat were placed in residential gardens (Fig. 1c). 1) Cattle farm: livestock production on a 300 ha property located at 9 km of Villa Berthet (27° 12′52″ S; 60° 23′14″ W), with a livestock population of approximately 350 animals (mainly cows and pigs; Fig. 1d). 1) Alfalfa crop: a crop field located at 6 km of Villa Berthet (27° 18′42″ S; 60° 21′36″ W), with an extension of 5 ha (Fig. 1e). 2) Savanna: located at 6 km of Villa Berthet (27° 14′59″ S; 60° 23′06″ W), mainly with grasses (Andropogon spp., Leptochloe spp., and Melica spp.) and some trees (Prosopis spp.) (Oakley et al. 2005; Fig. 1f). 2) Forest: located at 10 km of Villa Berthet (27° 13′34″ S; 60° 21′02″ W). This forest is mainly a xeric deciduous forest, with wild animals, Cactaceae, and terrestrial Bromeliaceae characteristic of the Humid Chaco ecoregion (Cabrera 1971; Fig. 1g). The present study used these two anthropization category types for comparative purposes. Anthropized vs nonanthropized areas were compared to evaluate the effect of human presence and, in addition, we compared all habitat types to evaluate specific characteristics of habitats and their Sarcophagidae communities. Sarcophagid Fly Sampling and Identification Flesh flies were collected monthly from March 2015 to February 2016, using van Someren-Rydon canopy traps baited with 250 g of squid exposed at room temperature for 72 h before samplings (Dufek et al. 2019). This type of bait has been used in several ecological studies to attract fly species (Baz et al. 2007; Martin-Vega and Baz 2013; Dufek et al. 2016, 2019) and is very effective because it maintains a moist state of decay for much longer than other baits (e.g., chicken viscera or beef liver; Newton and Peck 1975). Within each habitat, five sites separated by at least 100 m to avoid spatial pseudoreplication were selected (Yepes-Gaurisas et al. 2013, Carvalho et al. 2017). At each site, a van Someren-Rydon canopy trap was placed for a continuous 48-h period per month, and always placed in the same location within each habitat. Each trap was hung with a rope 2 m above the ground from available trees or when trees were not available, hung from metal poles staked into the ground. In total, 300 independent samples were collected throughout the study period (12 months × five habitats × five traps), 60 in each habitat (12 months × five traps). All flies collected were killed in glass vials with ethyl acetate and then transferred in the field to labeled envelopes for further study in the laboratory. Sarcophagidae species were identified using taxonomic keys (Lopes and Tibana 1987; Mulieri et al. 2010, 2017; Vairo et al. 2011; Buenaventura and Pape 2013; Mulieri and Mello-Patiu 2013; Mello-Patiu et al. 2014; Mello-Patiu and Salazar-Souza 2016; Santos and Mello-Patiu 2018; Mulieri and Dufek 2019), descriptions (Carvalho-Filho et al. 2017, Dufek and Mulieri 2017), and by comparison with reference specimens deposited at the Museo Argentino de Ciencias Naturales ‘Bernardino Rivadavia’ (MACN), Buenos Aires, Argentina. Unfortunately, taxonomic keys and descriptions of female Sarcophagidae are scarce, and those available only consider certain genera (Mulieri et al. 2010, Vairo et al. 2015). Therefore, in this present study only males were identified because reliable taxonomic identification of Sarcophagidae is largely based on the aedeagus. Voucher specimens are housed in the Universidad Nacional del Nordeste, Corrientes, Argentina (CARTROUNNE) and MACN. Data Analysis Analyses were alternatively carried out to explore changes in Sarcophagidae community parameters in different land uses, based on two classifications: 1) a dichotomic segregation of data (anthropized vs nonanthropized) and 2) habitat type (with five categories). From each trap, the number of individuals per species was recorded. If the data were transformed during analysis, this was specified within each analysis description. Because the observed number of species is often lower than the number of species actually present, total richness was estimated for each habitat by the first-order jackknife estimator after 1,000 randomized samplings based on the number of traps (Colwell and Coddington 1994). This is a useful estimator of species richness because it is based on the presence or absence of a species in a given area rather than on the abundance of the species (Samarah 2017). The community composition of flesh flies collected in the different habitats were compared based on the abundance of the total flesh flies captured (log n + 1 transformed to reduce the effect of discrepant values), species richness, and alpha diversity (calculated for each sample point using the Shannon–Wiener index). One-way ANOVA, followed by multiple comparisons performed according to the Tukey’s test, was used to find significant differences between these community parameters. Abundance, species richness, and diversity were compared between habitats using boxplots for better data visualization. First-order jackknifes were calculated using EstimateS software version 9.1.0 (Colwell 2013) and the ANOVA was performed using SPSS software version 21 considering P < 0.05 as significance level (IBM Corporation 2012). With the purpose to identify indicator species of a particular habitat or a group of anthropized (urban + cattle farm + alfalfa crop) or nonanthropized (savanna + forest) habitats we used indicator species analysis followed by a Monte Carlo permutation test with 1,000 permutations. The indicator value (IndVal), which is the product of the relative abundance of a species and the relative frequency of that species at a site, ranged from 0 (no indication) to 100 (perfect indication) (Dufrêne and Legendre 1997). PC-ORD version 6.0 program was used to do this analysis. Species whose abundances were ≥10 were analyzed. To recognize differences between habitats based on flesh fly community compositions we performed a nonmetric multidimensional scaling (NMDS) analysis using log n + 1 transformation and Bray–Curtis index as a measure of similarity (Legendre and Legendre 1998). The distortion of the resolution of the two-dimensional arrangement is represented by a stress value. Moreover, the sarcophagid assemblage structures were evaluated by analyses of similarities (ANOSIM) to understand the level of similarity between habitats (Clarke and Green 1988). We used the Bray–Curtis similarity coefficient on square-root-transformed data. The R statistic generated by ANOSIM is a measure of the similarity between habitat types, with values ranging from 0 (100% of similarity) to 1 (0% of similarity). These analyses were conducted using PRIMER version 6 software (Clarke and Gorley 2006) and R package vegan (Oksanen et al. 2017, R Development Core Team 2017). To examine whether the overall dissimilarity of the flesh fly community across all habitats is structured mainly by spatial turnover or nestedness, we partitioned beta diversity into two components following Baselga (2010) as: βsor = βsim + βnes. βsor (Sorensen dissimilarity) represents total beta diversity and incorporates both species turnover (βsim), which considers only species replacement, and nestedness (βnes) or variation in species richness. A transformed presence/absence matrix (as 0 for absence and 1 for values ≥ 1 as presence from abundance data) was used to estimate the incidence-based Sorensen dissimilarity indices using R package betapart (Baselga et al. 2017). We used the method ‘beta.multi’ to calculate these coefficients, which takes into account all the given samples for producing the mean beta coefficient of pairwise beta coefficients calculated for all possible sample combinations (Baselga and Orme 2012). This procedure was repeated for 9,999 iterations. Finally, to evaluate the influence of anthropization (presence/absence) and habitat type (i.e., urban, cattle farm, alfalfa crop, savanna, and forest) on the sarcophagid fauna composition, we made a nonparametric permutation-based multivariable analysis of variance (PERMANOVA), using the Bray–Curtis index as a measure of dissimilarity. This test was conducted using the ‘Adonis’ function of the R package vegan (Oksanen et al. 2017, R Development Core Team 2017). The Adonis function provides a statistic (F), a measure of the ‘effect size’ (R2) and a P value for each factor. Higher R2 indicates higher explanatory power. Results Overall Results In total, 5,790 male sarcophagid flies were collected, representing 15 genera and 55 species, all of which were native species. The largest percentage of individuals were collected in anthropized habitats (51.91%). Among all habitats, the savanna had the highest abundance (28.03% of the total sample) and species richness (39 species), followed by the cattle farm (22.14%, 36 species) and the forest (20.05%, 33 species). The alfalfa crop had the lowest abundance (14.49%), whereas the urban had the lowest species richness (20 species) (Table 1). Table 1. Abundance of Sarcophagidae species captured in the anthropized (urban, cattle farm, and alfalfa crop) and natural (savanna and forest) habitats surveyed in the Humid Chaco ecoregion, Chaco Province, Argentina, between March 2015 and February 2016 Species . Anthropized . Natural . Total . % . . U . C . A . S . F . . . Blaesoxipha (Acanthodotheca) sp. 1 — — 1 — — 1 0.02 Dexosarcophaga ampullula (Engel) — 1 — — — 1 0.02 Dexosarcophaga chaetosa Blanchard — — — 1 — 1 0.02 Dexosarcophaga sp. 1 — 1 — 5 — 6 0.10 Dexosarcophaga sp. 2 — — 1 — — 1 0.02 Helicobia aurescens (Townsend) — — 1 1 35 37 0.64 Helicobia morionella (Aldrich) 3 1 1 5 — 10 0.17 Helicobia sp. 1 1 1 1 2 32 37 0.64 Helicobia sp. 2 — — 1 1 — 2 0.03 Helicobia sp. 3 — 1 1 2 4 8 0.14 Lipoptilocnema crispula (Lopez) 23 12 — 4 121 160 2.76 Lipoptilocnema lanei Townsend — — — — 1 1 0.02 Lipoptilocnema margaretae (Lahille) — 1 — 1 1 3 0.05 Lipoptilocnema salobrensis Lopes 3 — — 1 45 49 0.85 Malacophagomyia rivadavia Mulieri and Mello-Patiu — 20 1 28 1 50 0.86 Microcerella erythropyga (Lopes) — — 1 — — 1 0.02 Microcerella halli (Engel) 7 15 2 4 5 33 0.57 Microcerella muehni (Blanchard) — 0 2 5 — 7 0.12 Microcerella sp. 1 — 1 — 1 — 2 0.03 Microcerella sp. 2 — 3 1 7 — 11 0.19 Oxysarcodexia admixta (Lopes) 13 2 — 2 27 44 0.76 Oxysarcodexia aura (Hall) — 2 52 31 — 85 1.47 Oxysarcodexia avuncula (Lopes) 10 37 2 55 148 252 4.35 Oxysarcodexia berthet Dufek and Mulieri — 6 — 0 1 7 0.12 Oxysarcodexia cocais Carvalho-Filho, Pereira de Sousa and Esposito — — 3 16 — 19 0.33 Oxysarcodexia ibera Dufek and Mulieri — 3 1 6 — 10 0.17 Oxysarcodexia marina (Hall) — — 6 2 — 8 0.14 Oxysarcodexia parva Lopes 6 2 — 3 26 37 0.64 Oxysarcodexia riograndensis Lopes 17 1 2 6 — 26 0.45 Oxysarcodexia terminalis (Wiedemann) 1 16 31 29 6 83 1.43 Oxysarcodexia thornax (Walker) 655 808 504 690 333 2,990 51.64 Oxysarcodexia varia (Walker) — — 10 — — 10 0.17 Oxysarcodexia wygodzinskyi Lopes and Tibana 71 188 80 196 55 590 10.19 Oxyvinia excisa (Lopes) — — — — 79 79 1.36 Peckia (Euboettcheria) anguilla (Curran and Walley) 3 1 1 — 4 9 0.16 Peckia (Euboettcheria) collusor (Curran and Walley) — — — 1 1 2 0.03 Peckia (Peckia) enderleini (Engel) 34 32 13 44 128 251 4.34 Peckia (Peckia) pexata (Wulp) — 1 — 2 — 3 0.05 Peckia (Sarcodexia) florencioi (Prado and Fonseca) — — — 2 7 9 0.16 Peckia (Sarcodexia) lambens (Wiedemann) 16 13 2 27 63 121 2.09 Ravinia advena (Walker) 2 28 — 14 9 53 0.92 Ravinia aureopyga (Hall) — 9 2 1 — 12 0.21 Ravinia belforti (Prado and Fonseca) 2 9 15 21 2 49 0.85 Retrocitomyia mizuguchiana Tibana and Xerez — 2 — 7 2 11 0.19 Retrocitomyia sisbiota Mello-Patiu and Salazar-Souza — 4 — 22 4 30 0.52 Retrocitomyia sp. 1 1 — — — — 1 0.02 Sarcofahrtiopsis cuneata (Townsend) — — — 2 5 7 0.12 Sarcofahrtiopsis spinetta Mulieri and Dufek — 2 — — 4 6 0.10 Titanogrypa (Airipel) cryptopyga (Lopes) 5 18 26 110 4 163 2.82 Titanogrypa (Cucullomyia) larvicida (Lopes) — 1 — — — 1 0.02 Titanogrypa (Sarconeiva) fimbriata (Aldrich) — — 1 — 1 2 0.03 Tricharaea (Sarcophagula) occidua (Fabricius) 12 35 74 266 4 391 6.75 Udamopyga helicivora Lopes — 4 — — 2 6 0.10 Udamopyga sp. 1 — 1 — — — 1 0.02 Udamopyga sp. 2 — — — — 1 1 0.02 Abundance 885 1,282 839 1,623 1,161 5,790 100 Abundance (%) 15.28 22.14 14.49 28.03 20.05 100 Richness 20 36 30 39 33 55 Species . Anthropized . Natural . Total . % . . U . C . A . S . F . . . Blaesoxipha (Acanthodotheca) sp. 1 — — 1 — — 1 0.02 Dexosarcophaga ampullula (Engel) — 1 — — — 1 0.02 Dexosarcophaga chaetosa Blanchard — — — 1 — 1 0.02 Dexosarcophaga sp. 1 — 1 — 5 — 6 0.10 Dexosarcophaga sp. 2 — — 1 — — 1 0.02 Helicobia aurescens (Townsend) — — 1 1 35 37 0.64 Helicobia morionella (Aldrich) 3 1 1 5 — 10 0.17 Helicobia sp. 1 1 1 1 2 32 37 0.64 Helicobia sp. 2 — — 1 1 — 2 0.03 Helicobia sp. 3 — 1 1 2 4 8 0.14 Lipoptilocnema crispula (Lopez) 23 12 — 4 121 160 2.76 Lipoptilocnema lanei Townsend — — — — 1 1 0.02 Lipoptilocnema margaretae (Lahille) — 1 — 1 1 3 0.05 Lipoptilocnema salobrensis Lopes 3 — — 1 45 49 0.85 Malacophagomyia rivadavia Mulieri and Mello-Patiu — 20 1 28 1 50 0.86 Microcerella erythropyga (Lopes) — — 1 — — 1 0.02 Microcerella halli (Engel) 7 15 2 4 5 33 0.57 Microcerella muehni (Blanchard) — 0 2 5 — 7 0.12 Microcerella sp. 1 — 1 — 1 — 2 0.03 Microcerella sp. 2 — 3 1 7 — 11 0.19 Oxysarcodexia admixta (Lopes) 13 2 — 2 27 44 0.76 Oxysarcodexia aura (Hall) — 2 52 31 — 85 1.47 Oxysarcodexia avuncula (Lopes) 10 37 2 55 148 252 4.35 Oxysarcodexia berthet Dufek and Mulieri — 6 — 0 1 7 0.12 Oxysarcodexia cocais Carvalho-Filho, Pereira de Sousa and Esposito — — 3 16 — 19 0.33 Oxysarcodexia ibera Dufek and Mulieri — 3 1 6 — 10 0.17 Oxysarcodexia marina (Hall) — — 6 2 — 8 0.14 Oxysarcodexia parva Lopes 6 2 — 3 26 37 0.64 Oxysarcodexia riograndensis Lopes 17 1 2 6 — 26 0.45 Oxysarcodexia terminalis (Wiedemann) 1 16 31 29 6 83 1.43 Oxysarcodexia thornax (Walker) 655 808 504 690 333 2,990 51.64 Oxysarcodexia varia (Walker) — — 10 — — 10 0.17 Oxysarcodexia wygodzinskyi Lopes and Tibana 71 188 80 196 55 590 10.19 Oxyvinia excisa (Lopes) — — — — 79 79 1.36 Peckia (Euboettcheria) anguilla (Curran and Walley) 3 1 1 — 4 9 0.16 Peckia (Euboettcheria) collusor (Curran and Walley) — — — 1 1 2 0.03 Peckia (Peckia) enderleini (Engel) 34 32 13 44 128 251 4.34 Peckia (Peckia) pexata (Wulp) — 1 — 2 — 3 0.05 Peckia (Sarcodexia) florencioi (Prado and Fonseca) — — — 2 7 9 0.16 Peckia (Sarcodexia) lambens (Wiedemann) 16 13 2 27 63 121 2.09 Ravinia advena (Walker) 2 28 — 14 9 53 0.92 Ravinia aureopyga (Hall) — 9 2 1 — 12 0.21 Ravinia belforti (Prado and Fonseca) 2 9 15 21 2 49 0.85 Retrocitomyia mizuguchiana Tibana and Xerez — 2 — 7 2 11 0.19 Retrocitomyia sisbiota Mello-Patiu and Salazar-Souza — 4 — 22 4 30 0.52 Retrocitomyia sp. 1 1 — — — — 1 0.02 Sarcofahrtiopsis cuneata (Townsend) — — — 2 5 7 0.12 Sarcofahrtiopsis spinetta Mulieri and Dufek — 2 — — 4 6 0.10 Titanogrypa (Airipel) cryptopyga (Lopes) 5 18 26 110 4 163 2.82 Titanogrypa (Cucullomyia) larvicida (Lopes) — 1 — — — 1 0.02 Titanogrypa (Sarconeiva) fimbriata (Aldrich) — — 1 — 1 2 0.03 Tricharaea (Sarcophagula) occidua (Fabricius) 12 35 74 266 4 391 6.75 Udamopyga helicivora Lopes — 4 — — 2 6 0.10 Udamopyga sp. 1 — 1 — — — 1 0.02 Udamopyga sp. 2 — — — — 1 1 0.02 Abundance 885 1,282 839 1,623 1,161 5,790 100 Abundance (%) 15.28 22.14 14.49 28.03 20.05 100 Richness 20 36 30 39 33 55 Flesh flies were captured for 1 yr in 25 sampling points (five per habitat) using van Someren–Rydon canopy traps baited with rotten squid. The traps were exposed for 48 h in each habitat per month. References: U, urban; C, cattle farm; A, alfalfa crop; S, savanna; F, forest. Richness: total number of species. Bold entries show the most abundant species in each habitat. Open in new tab Table 1. Abundance of Sarcophagidae species captured in the anthropized (urban, cattle farm, and alfalfa crop) and natural (savanna and forest) habitats surveyed in the Humid Chaco ecoregion, Chaco Province, Argentina, between March 2015 and February 2016 Species . Anthropized . Natural . Total . % . . U . C . A . S . F . . . Blaesoxipha (Acanthodotheca) sp. 1 — — 1 — — 1 0.02 Dexosarcophaga ampullula (Engel) — 1 — — — 1 0.02 Dexosarcophaga chaetosa Blanchard — — — 1 — 1 0.02 Dexosarcophaga sp. 1 — 1 — 5 — 6 0.10 Dexosarcophaga sp. 2 — — 1 — — 1 0.02 Helicobia aurescens (Townsend) — — 1 1 35 37 0.64 Helicobia morionella (Aldrich) 3 1 1 5 — 10 0.17 Helicobia sp. 1 1 1 1 2 32 37 0.64 Helicobia sp. 2 — — 1 1 — 2 0.03 Helicobia sp. 3 — 1 1 2 4 8 0.14 Lipoptilocnema crispula (Lopez) 23 12 — 4 121 160 2.76 Lipoptilocnema lanei Townsend — — — — 1 1 0.02 Lipoptilocnema margaretae (Lahille) — 1 — 1 1 3 0.05 Lipoptilocnema salobrensis Lopes 3 — — 1 45 49 0.85 Malacophagomyia rivadavia Mulieri and Mello-Patiu — 20 1 28 1 50 0.86 Microcerella erythropyga (Lopes) — — 1 — — 1 0.02 Microcerella halli (Engel) 7 15 2 4 5 33 0.57 Microcerella muehni (Blanchard) — 0 2 5 — 7 0.12 Microcerella sp. 1 — 1 — 1 — 2 0.03 Microcerella sp. 2 — 3 1 7 — 11 0.19 Oxysarcodexia admixta (Lopes) 13 2 — 2 27 44 0.76 Oxysarcodexia aura (Hall) — 2 52 31 — 85 1.47 Oxysarcodexia avuncula (Lopes) 10 37 2 55 148 252 4.35 Oxysarcodexia berthet Dufek and Mulieri — 6 — 0 1 7 0.12 Oxysarcodexia cocais Carvalho-Filho, Pereira de Sousa and Esposito — — 3 16 — 19 0.33 Oxysarcodexia ibera Dufek and Mulieri — 3 1 6 — 10 0.17 Oxysarcodexia marina (Hall) — — 6 2 — 8 0.14 Oxysarcodexia parva Lopes 6 2 — 3 26 37 0.64 Oxysarcodexia riograndensis Lopes 17 1 2 6 — 26 0.45 Oxysarcodexia terminalis (Wiedemann) 1 16 31 29 6 83 1.43 Oxysarcodexia thornax (Walker) 655 808 504 690 333 2,990 51.64 Oxysarcodexia varia (Walker) — — 10 — — 10 0.17 Oxysarcodexia wygodzinskyi Lopes and Tibana 71 188 80 196 55 590 10.19 Oxyvinia excisa (Lopes) — — — — 79 79 1.36 Peckia (Euboettcheria) anguilla (Curran and Walley) 3 1 1 — 4 9 0.16 Peckia (Euboettcheria) collusor (Curran and Walley) — — — 1 1 2 0.03 Peckia (Peckia) enderleini (Engel) 34 32 13 44 128 251 4.34 Peckia (Peckia) pexata (Wulp) — 1 — 2 — 3 0.05 Peckia (Sarcodexia) florencioi (Prado and Fonseca) — — — 2 7 9 0.16 Peckia (Sarcodexia) lambens (Wiedemann) 16 13 2 27 63 121 2.09 Ravinia advena (Walker) 2 28 — 14 9 53 0.92 Ravinia aureopyga (Hall) — 9 2 1 — 12 0.21 Ravinia belforti (Prado and Fonseca) 2 9 15 21 2 49 0.85 Retrocitomyia mizuguchiana Tibana and Xerez — 2 — 7 2 11 0.19 Retrocitomyia sisbiota Mello-Patiu and Salazar-Souza — 4 — 22 4 30 0.52 Retrocitomyia sp. 1 1 — — — — 1 0.02 Sarcofahrtiopsis cuneata (Townsend) — — — 2 5 7 0.12 Sarcofahrtiopsis spinetta Mulieri and Dufek — 2 — — 4 6 0.10 Titanogrypa (Airipel) cryptopyga (Lopes) 5 18 26 110 4 163 2.82 Titanogrypa (Cucullomyia) larvicida (Lopes) — 1 — — — 1 0.02 Titanogrypa (Sarconeiva) fimbriata (Aldrich) — — 1 — 1 2 0.03 Tricharaea (Sarcophagula) occidua (Fabricius) 12 35 74 266 4 391 6.75 Udamopyga helicivora Lopes — 4 — — 2 6 0.10 Udamopyga sp. 1 — 1 — — — 1 0.02 Udamopyga sp. 2 — — — — 1 1 0.02 Abundance 885 1,282 839 1,623 1,161 5,790 100 Abundance (%) 15.28 22.14 14.49 28.03 20.05 100 Richness 20 36 30 39 33 55 Species . Anthropized . Natural . Total . % . . U . C . A . S . F . . . Blaesoxipha (Acanthodotheca) sp. 1 — — 1 — — 1 0.02 Dexosarcophaga ampullula (Engel) — 1 — — — 1 0.02 Dexosarcophaga chaetosa Blanchard — — — 1 — 1 0.02 Dexosarcophaga sp. 1 — 1 — 5 — 6 0.10 Dexosarcophaga sp. 2 — — 1 — — 1 0.02 Helicobia aurescens (Townsend) — — 1 1 35 37 0.64 Helicobia morionella (Aldrich) 3 1 1 5 — 10 0.17 Helicobia sp. 1 1 1 1 2 32 37 0.64 Helicobia sp. 2 — — 1 1 — 2 0.03 Helicobia sp. 3 — 1 1 2 4 8 0.14 Lipoptilocnema crispula (Lopez) 23 12 — 4 121 160 2.76 Lipoptilocnema lanei Townsend — — — — 1 1 0.02 Lipoptilocnema margaretae (Lahille) — 1 — 1 1 3 0.05 Lipoptilocnema salobrensis Lopes 3 — — 1 45 49 0.85 Malacophagomyia rivadavia Mulieri and Mello-Patiu — 20 1 28 1 50 0.86 Microcerella erythropyga (Lopes) — — 1 — — 1 0.02 Microcerella halli (Engel) 7 15 2 4 5 33 0.57 Microcerella muehni (Blanchard) — 0 2 5 — 7 0.12 Microcerella sp. 1 — 1 — 1 — 2 0.03 Microcerella sp. 2 — 3 1 7 — 11 0.19 Oxysarcodexia admixta (Lopes) 13 2 — 2 27 44 0.76 Oxysarcodexia aura (Hall) — 2 52 31 — 85 1.47 Oxysarcodexia avuncula (Lopes) 10 37 2 55 148 252 4.35 Oxysarcodexia berthet Dufek and Mulieri — 6 — 0 1 7 0.12 Oxysarcodexia cocais Carvalho-Filho, Pereira de Sousa and Esposito — — 3 16 — 19 0.33 Oxysarcodexia ibera Dufek and Mulieri — 3 1 6 — 10 0.17 Oxysarcodexia marina (Hall) — — 6 2 — 8 0.14 Oxysarcodexia parva Lopes 6 2 — 3 26 37 0.64 Oxysarcodexia riograndensis Lopes 17 1 2 6 — 26 0.45 Oxysarcodexia terminalis (Wiedemann) 1 16 31 29 6 83 1.43 Oxysarcodexia thornax (Walker) 655 808 504 690 333 2,990 51.64 Oxysarcodexia varia (Walker) — — 10 — — 10 0.17 Oxysarcodexia wygodzinskyi Lopes and Tibana 71 188 80 196 55 590 10.19 Oxyvinia excisa (Lopes) — — — — 79 79 1.36 Peckia (Euboettcheria) anguilla (Curran and Walley) 3 1 1 — 4 9 0.16 Peckia (Euboettcheria) collusor (Curran and Walley) — — — 1 1 2 0.03 Peckia (Peckia) enderleini (Engel) 34 32 13 44 128 251 4.34 Peckia (Peckia) pexata (Wulp) — 1 — 2 — 3 0.05 Peckia (Sarcodexia) florencioi (Prado and Fonseca) — — — 2 7 9 0.16 Peckia (Sarcodexia) lambens (Wiedemann) 16 13 2 27 63 121 2.09 Ravinia advena (Walker) 2 28 — 14 9 53 0.92 Ravinia aureopyga (Hall) — 9 2 1 — 12 0.21 Ravinia belforti (Prado and Fonseca) 2 9 15 21 2 49 0.85 Retrocitomyia mizuguchiana Tibana and Xerez — 2 — 7 2 11 0.19 Retrocitomyia sisbiota Mello-Patiu and Salazar-Souza — 4 — 22 4 30 0.52 Retrocitomyia sp. 1 1 — — — — 1 0.02 Sarcofahrtiopsis cuneata (Townsend) — — — 2 5 7 0.12 Sarcofahrtiopsis spinetta Mulieri and Dufek — 2 — — 4 6 0.10 Titanogrypa (Airipel) cryptopyga (Lopes) 5 18 26 110 4 163 2.82 Titanogrypa (Cucullomyia) larvicida (Lopes) — 1 — — — 1 0.02 Titanogrypa (Sarconeiva) fimbriata (Aldrich) — — 1 — 1 2 0.03 Tricharaea (Sarcophagula) occidua (Fabricius) 12 35 74 266 4 391 6.75 Udamopyga helicivora Lopes — 4 — — 2 6 0.10 Udamopyga sp. 1 — 1 — — — 1 0.02 Udamopyga sp. 2 — — — — 1 1 0.02 Abundance 885 1,282 839 1,623 1,161 5,790 100 Abundance (%) 15.28 22.14 14.49 28.03 20.05 100 Richness 20 36 30 39 33 55 Flesh flies were captured for 1 yr in 25 sampling points (five per habitat) using van Someren–Rydon canopy traps baited with rotten squid. The traps were exposed for 48 h in each habitat per month. References: U, urban; C, cattle farm; A, alfalfa crop; S, savanna; F, forest. Richness: total number of species. Bold entries show the most abundant species in each habitat. Open in new tab Oxysarcodexia Townsend (Diptera: Sarcophagidae) and Peckia Robineau-Desvoidy (Diptera: Sarcophagidae) were the most representative genera, with 13 and 6 species, respectively. Oxysarcodexia thornax (Walker) (Diptera: Sarcophagidae) was the most abundant species captured in each habitat and represented the 51.64% of the total sample. Eleven species were captured in all habitats, whereas 12 were found only in one habitat (one in urban, three in cattle farm, four in alfalfa crop, one in savanna, and three in forest; Table 1). The sampling efficiency varied between 71% in the alfalfa crop and 87% in the urban and forest habitats, indicating that the sampling effort was sufficient to estimate species richness (Table 2). Table 2. Sampling efficiency (observed and estimated species richness using first-order jackknife) of the Sarcophagidae species in the anthropized (urban, cattle farm and alfalfa crop) and natural (savanna and forest) habitats surveyed in the Humid Chaco ecoregion, Chaco Province, Argentina, between March 2015 and February 2016 . Urban . Cattle farm . Alfalfa crop . Savanna . Forest . Observed richness 20 36 30 39 33 Estimated richness 23.2 (± 1.95) 46.4 (± 4.66) 42 (± 2.52) 46.2 (± 2.33) 38.6 (± 2.03) Sampling efficiency (%) 87% 78% 71% 85% 87% . Urban . Cattle farm . Alfalfa crop . Savanna . Forest . Observed richness 20 36 30 39 33 Estimated richness 23.2 (± 1.95) 46.4 (± 4.66) 42 (± 2.52) 46.2 (± 2.33) 38.6 (± 2.03) Sampling efficiency (%) 87% 78% 71% 85% 87% Open in new tab Table 2. Sampling efficiency (observed and estimated species richness using first-order jackknife) of the Sarcophagidae species in the anthropized (urban, cattle farm and alfalfa crop) and natural (savanna and forest) habitats surveyed in the Humid Chaco ecoregion, Chaco Province, Argentina, between March 2015 and February 2016 . Urban . Cattle farm . Alfalfa crop . Savanna . Forest . Observed richness 20 36 30 39 33 Estimated richness 23.2 (± 1.95) 46.4 (± 4.66) 42 (± 2.52) 46.2 (± 2.33) 38.6 (± 2.03) Sampling efficiency (%) 87% 78% 71% 85% 87% . Urban . Cattle farm . Alfalfa crop . Savanna . Forest . Observed richness 20 36 30 39 33 Estimated richness 23.2 (± 1.95) 46.4 (± 4.66) 42 (± 2.52) 46.2 (± 2.33) 38.6 (± 2.03) Sampling efficiency (%) 87% 78% 71% 85% 87% Open in new tab The results obtained indicated significant differences in the abundance (F4,20 = 13.58, P < 0.001), species richness (F4,20 = 16.32, P < 0.001) and diversity (F4,20 = 36.87, P < 0.001) between habitats. The cattle farm and savanna habitats showed a similar abundance whereas species richness and diversity were higher in the natural habitats (forest and savanna). The lowest abundance, species richness, and diversity were obtained in the urban and alfalfa crop habitats (Fig. 2). Fig. 2. Open in new tabDownload slide Abundance (log n + 1), species richness and diversity (based on Shannon–Wiener index) of Sarcophagidae (whiskers, median, and outliers) in the anthropized (urban, cattle farm, and alfalfa crop) and natural (savanna and forest) habitats surveyed in the Humid Chaco ecoregion, Chaco Province, Argentina, between March 2015 and February 2016. References: U, urban; C, cattle farm; A, alfalfa crop; S, savanna; F, forest. Different letters above the boxplots indicate significant differences (Tukey’s test, α = 0.05). Fig. 2. Open in new tabDownload slide Abundance (log n + 1), species richness and diversity (based on Shannon–Wiener index) of Sarcophagidae (whiskers, median, and outliers) in the anthropized (urban, cattle farm, and alfalfa crop) and natural (savanna and forest) habitats surveyed in the Humid Chaco ecoregion, Chaco Province, Argentina, between March 2015 and February 2016. References: U, urban; C, cattle farm; A, alfalfa crop; S, savanna; F, forest. Different letters above the boxplots indicate significant differences (Tukey’s test, α = 0.05). Indicator Species of Sarcophagidae The indicator species analysis was able to detect nine species as indicators of a particular habitat (species with an IndVal > 70 and P < 0.05): six for forest [Helicobia aurescens (Townsend) (Diptera: Sarcophagidae), Helicobia sp. 1 (Diptera: Sarcophagidae), Lipoptilocnema crispula (Lopes) (Diptera: Sarcophagidae), Lipoptilocnema salobrensis Lopes (Diptera: Sarcophagidae), Oxysarcodexia parva Lopes (Diptera: Sarcophagidae), and Oxyvinia excisa (Lopes) (Diptera: Sarcophagidae)], two for savanna [Oxysarcodexia cocais Da Silva Carvalho-Filho, Pereira de Sousa and Esposito (Diptera: Sarcophagidae) and Retrocitomyia sisbiota Mello-Patiu and Salazar-Souza (Diptera: Sarcophagidae)], and one for alfalfa crop [Oxysarcodexia varia (Walker) (Diptera: Sarcophagidae)], whereas nine species were identified as indicator species for natural and four for anthropized habitats (Table 3). Table 3. Significant indicator species identified for anthropized (urban, cattle farm and alfalfa crop) and natural (savanna and forest) habitats surveyed in the Humid Chaco ecoregion, Chaco Province, Argentina, between March 2015 and February 2016 (Monte Carlo test, α = 0.05) Habitat . Species . IndVal . Mean . SD . P value . Forest H. aurescens 94.6 22.7 9.9 0.001 Forest Helicobia sp. 1 86.5 25.1 9.8 0.001 Forest L. crispula 75.6 31.2 9.0 0.001 Forest L. salobrensis 91.8 24.9 10.7 0.001 Savanna Oxys. cocais 84.2 23.5 9.6 0.001 Forest Oxys. parva 70.3 26.3 9.2 0.002 Alfalfa crop Oxys. varia 80 19.9 10.8 0.002 Forest Oxyv. excisa 100 20.9 10.3 0.001 Savanna Re. sisbiota 73.3 25.4 10.0 0.003 Natural H. aurescens 97.3 46.6 14.6 0.013 Natural Helicobia sp. 1 91.9 50.6 12.9 0.013 Natural L. crispula 78.1 59.4 6.65 0.013 Natural L. salobrensis 93.9 55.8 12.8 0.013 Anthropized Mi. halli 72.7 58.6 5.7 0.037 Natural Oxys. avuncula 80.6 59 6.9 0.013 Natural Oxys. cocais 84.2 55.1 12.1 0.037 Natural Oxys. parva 78.4 57.1 9.3 0.029 Anthropized Oxys. riograndensis 76.9 57.2 9.3 0.047 Anthropized Oxys. varia 80 37.5 14.6 0.042 Natural Oxyv. excisa 100 42.5 15.6 0.013 Natural P. lambens 74.4 57 5.3 0.013 Anthropized Ra. aureopyga 73.3 42 13.7 0.046 Habitat . Species . IndVal . Mean . SD . P value . Forest H. aurescens 94.6 22.7 9.9 0.001 Forest Helicobia sp. 1 86.5 25.1 9.8 0.001 Forest L. crispula 75.6 31.2 9.0 0.001 Forest L. salobrensis 91.8 24.9 10.7 0.001 Savanna Oxys. cocais 84.2 23.5 9.6 0.001 Forest Oxys. parva 70.3 26.3 9.2 0.002 Alfalfa crop Oxys. varia 80 19.9 10.8 0.002 Forest Oxyv. excisa 100 20.9 10.3 0.001 Savanna Re. sisbiota 73.3 25.4 10.0 0.003 Natural H. aurescens 97.3 46.6 14.6 0.013 Natural Helicobia sp. 1 91.9 50.6 12.9 0.013 Natural L. crispula 78.1 59.4 6.65 0.013 Natural L. salobrensis 93.9 55.8 12.8 0.013 Anthropized Mi. halli 72.7 58.6 5.7 0.037 Natural Oxys. avuncula 80.6 59 6.9 0.013 Natural Oxys. cocais 84.2 55.1 12.1 0.037 Natural Oxys. parva 78.4 57.1 9.3 0.029 Anthropized Oxys. riograndensis 76.9 57.2 9.3 0.047 Anthropized Oxys. varia 80 37.5 14.6 0.042 Natural Oxyv. excisa 100 42.5 15.6 0.013 Natural P. lambens 74.4 57 5.3 0.013 Anthropized Ra. aureopyga 73.3 42 13.7 0.046 IndVal, indicator value. Open in new tab Table 3. Significant indicator species identified for anthropized (urban, cattle farm and alfalfa crop) and natural (savanna and forest) habitats surveyed in the Humid Chaco ecoregion, Chaco Province, Argentina, between March 2015 and February 2016 (Monte Carlo test, α = 0.05) Habitat . Species . IndVal . Mean . SD . P value . Forest H. aurescens 94.6 22.7 9.9 0.001 Forest Helicobia sp. 1 86.5 25.1 9.8 0.001 Forest L. crispula 75.6 31.2 9.0 0.001 Forest L. salobrensis 91.8 24.9 10.7 0.001 Savanna Oxys. cocais 84.2 23.5 9.6 0.001 Forest Oxys. parva 70.3 26.3 9.2 0.002 Alfalfa crop Oxys. varia 80 19.9 10.8 0.002 Forest Oxyv. excisa 100 20.9 10.3 0.001 Savanna Re. sisbiota 73.3 25.4 10.0 0.003 Natural H. aurescens 97.3 46.6 14.6 0.013 Natural Helicobia sp. 1 91.9 50.6 12.9 0.013 Natural L. crispula 78.1 59.4 6.65 0.013 Natural L. salobrensis 93.9 55.8 12.8 0.013 Anthropized Mi. halli 72.7 58.6 5.7 0.037 Natural Oxys. avuncula 80.6 59 6.9 0.013 Natural Oxys. cocais 84.2 55.1 12.1 0.037 Natural Oxys. parva 78.4 57.1 9.3 0.029 Anthropized Oxys. riograndensis 76.9 57.2 9.3 0.047 Anthropized Oxys. varia 80 37.5 14.6 0.042 Natural Oxyv. excisa 100 42.5 15.6 0.013 Natural P. lambens 74.4 57 5.3 0.013 Anthropized Ra. aureopyga 73.3 42 13.7 0.046 Habitat . Species . IndVal . Mean . SD . P value . Forest H. aurescens 94.6 22.7 9.9 0.001 Forest Helicobia sp. 1 86.5 25.1 9.8 0.001 Forest L. crispula 75.6 31.2 9.0 0.001 Forest L. salobrensis 91.8 24.9 10.7 0.001 Savanna Oxys. cocais 84.2 23.5 9.6 0.001 Forest Oxys. parva 70.3 26.3 9.2 0.002 Alfalfa crop Oxys. varia 80 19.9 10.8 0.002 Forest Oxyv. excisa 100 20.9 10.3 0.001 Savanna Re. sisbiota 73.3 25.4 10.0 0.003 Natural H. aurescens 97.3 46.6 14.6 0.013 Natural Helicobia sp. 1 91.9 50.6 12.9 0.013 Natural L. crispula 78.1 59.4 6.65 0.013 Natural L. salobrensis 93.9 55.8 12.8 0.013 Anthropized Mi. halli 72.7 58.6 5.7 0.037 Natural Oxys. avuncula 80.6 59 6.9 0.013 Natural Oxys. cocais 84.2 55.1 12.1 0.037 Natural Oxys. parva 78.4 57.1 9.3 0.029 Anthropized Oxys. riograndensis 76.9 57.2 9.3 0.047 Anthropized Oxys. varia 80 37.5 14.6 0.042 Natural Oxyv. excisa 100 42.5 15.6 0.013 Natural P. lambens 74.4 57 5.3 0.013 Anthropized Ra. aureopyga 73.3 42 13.7 0.046 IndVal, indicator value. Open in new tab Community Structure and Decomposition of Beta Diversity The ordination analysis (NMDS) showed the urban, alfalfa crop, and forest habitats were well separated from the assemblage formed by the cattle farm and savanna (2D stress: 0.09; Fig. 3). Also, the ANOSIM results suggest that habitats differ greatly in community composition (global R = 0.84, P = 0.001) and the lowest similarity was found between the forest and the other habitats. In all comparisons significant differences were found (Table 4). Table 4. ANOSIM displaying R statistics and significance levels for similarities in Sarcophagidae communities between anthropized (urban, cattle farm, and alfalfa crop) and natural (savanna and forest) habitats surveyed in the Humid Chaco ecoregion, Chaco Province, Argentina, between March 2015 and February 2016 Habitats . R statistic . P value . Global 0.84 0.001 Urban and cattle farm 0.46 0.014 Urban and alfalfa crop 0.50 0.007 Urban and savanna 0.98 0.008 Urban and forest 1.00 0.007 Cattle farm and alfalfa crop 0.66 0.007 Cattle farm and savanna 0.75 0.007 Cattle farm and forest 1.00 0.008 Alfalfa crop and savanna 0.93 0.008 Alfalfa crop and forest 1.00 0.007 Savanna and forest 1.00 0.007 Habitats . R statistic . P value . Global 0.84 0.001 Urban and cattle farm 0.46 0.014 Urban and alfalfa crop 0.50 0.007 Urban and savanna 0.98 0.008 Urban and forest 1.00 0.007 Cattle farm and alfalfa crop 0.66 0.007 Cattle farm and savanna 0.75 0.007 Cattle farm and forest 1.00 0.008 Alfalfa crop and savanna 0.93 0.008 Alfalfa crop and forest 1.00 0.007 Savanna and forest 1.00 0.007 Open in new tab Table 4. ANOSIM displaying R statistics and significance levels for similarities in Sarcophagidae communities between anthropized (urban, cattle farm, and alfalfa crop) and natural (savanna and forest) habitats surveyed in the Humid Chaco ecoregion, Chaco Province, Argentina, between March 2015 and February 2016 Habitats . R statistic . P value . Global 0.84 0.001 Urban and cattle farm 0.46 0.014 Urban and alfalfa crop 0.50 0.007 Urban and savanna 0.98 0.008 Urban and forest 1.00 0.007 Cattle farm and alfalfa crop 0.66 0.007 Cattle farm and savanna 0.75 0.007 Cattle farm and forest 1.00 0.008 Alfalfa crop and savanna 0.93 0.008 Alfalfa crop and forest 1.00 0.007 Savanna and forest 1.00 0.007 Habitats . R statistic . P value . Global 0.84 0.001 Urban and cattle farm 0.46 0.014 Urban and alfalfa crop 0.50 0.007 Urban and savanna 0.98 0.008 Urban and forest 1.00 0.007 Cattle farm and alfalfa crop 0.66 0.007 Cattle farm and savanna 0.75 0.007 Cattle farm and forest 1.00 0.008 Alfalfa crop and savanna 0.93 0.008 Alfalfa crop and forest 1.00 0.007 Savanna and forest 1.00 0.007 Open in new tab Fig. 3. Open in new tabDownload slide NMDS based on Sarcophagidae community composition species in the anthropized (urban, cattle farm, and alfalfa crop) and natural (savanna and forest) habitats surveyed in the Humid Chaco ecoregion, Chaco Province, Argentina, between March 2015 and February 2016. Fig. 3. Open in new tabDownload slide NMDS based on Sarcophagidae community composition species in the anthropized (urban, cattle farm, and alfalfa crop) and natural (savanna and forest) habitats surveyed in the Humid Chaco ecoregion, Chaco Province, Argentina, between March 2015 and February 2016. Species turnover was the main process shaping flesh fly assemblages in the entire landscape of the Humid Chaco ecoregion (Fig. 4). Community composition variation was explained mainly by species turnover (species replacement between habitats), rather than nestedness (species loss from one habitat to another) with values ranging from 0.32 to 0.64 and from 0.02 to 0.15. The nestedness component of beta diversity was higher between the urban and cattle farm, savanna and forest habitats (Fig. 4). Fig. 4. Open in new tabDownload slide Partitioning of incidence beta diversity into the turnover and nestedness components for Sarcophagidae assemblages between anthropized (urban, cattle farm, and alfalfa crop) and natural (savanna and forest) habitats surveyed in the Humid Chaco ecoregion, Chaco Province, Argentina, between March 2015 and February 2016. References: U, urban; C, cattle farm; A, alfalfa crop; S, savanna; F, forest. Fig. 4. Open in new tabDownload slide Partitioning of incidence beta diversity into the turnover and nestedness components for Sarcophagidae assemblages between anthropized (urban, cattle farm, and alfalfa crop) and natural (savanna and forest) habitats surveyed in the Humid Chaco ecoregion, Chaco Province, Argentina, between March 2015 and February 2016. References: U, urban; C, cattle farm; A, alfalfa crop; S, savanna; F, forest. The PERMANOVA analyses showed that both the habitat type (R2 = 0.535, P = 0.001) and anthropization (presence/absence; R2 = 0.236, P = 0.001) explained differences in the community composition of Sarcophagidae, and showed that the type of habitat has a higher explanatory power (Table 5). Table 5. Permutation-based multivariable analysis of variance (PERMANOVA) results (through the ‘Adonis’ function in R, using a Bray–Curtis index as a dissimilarity measure) between two factors: anthropization (presence/absence) and habitat type (urban, cattle farm, alfalfa crop, savanna, and forest) to evaluate the influence of these factors on Sarcophagidae species composition surveyed in the Humid Chaco ecoregion, Chaco Province, Argentina, between March 2015 and February 2016 Factors . df . Ssq . Mean . F . R2 . P value . Anthropization (presence/absence) 1 0.509 0.509 20.632 0.236 0.001 Habitat type 3 1.152 0.384 15.575 0.535 0.001 Residuals 20 0.493 0.025 0.229 Factors . df . Ssq . Mean . F . R2 . P value . Anthropization (presence/absence) 1 0.509 0.509 20.632 0.236 0.001 Habitat type 3 1.152 0.384 15.575 0.535 0.001 Residuals 20 0.493 0.025 0.229 Open in new tab Table 5. Permutation-based multivariable analysis of variance (PERMANOVA) results (through the ‘Adonis’ function in R, using a Bray–Curtis index as a dissimilarity measure) between two factors: anthropization (presence/absence) and habitat type (urban, cattle farm, alfalfa crop, savanna, and forest) to evaluate the influence of these factors on Sarcophagidae species composition surveyed in the Humid Chaco ecoregion, Chaco Province, Argentina, between March 2015 and February 2016 Factors . df . Ssq . Mean . F . R2 . P value . Anthropization (presence/absence) 1 0.509 0.509 20.632 0.236 0.001 Habitat type 3 1.152 0.384 15.575 0.535 0.001 Residuals 20 0.493 0.025 0.229 Factors . df . Ssq . Mean . F . R2 . P value . Anthropization (presence/absence) 1 0.509 0.509 20.632 0.236 0.001 Habitat type 3 1.152 0.384 15.575 0.535 0.001 Residuals 20 0.493 0.025 0.229 Open in new tab Discussion In this investigation we showed that spatially structured environmental variables influence the assembly of flesh flies. This study represents a first step in understanding what drives patterns of biodiversity for this taxon in complex ecosystems with different habitat types. The taxonomic difficulty of female identification has resulted in a significant number of Sarcophagidae ecological studies based on male specimens only. Frequently, female Sarcophagidae are much more abundant on carcasses and baited traps than males. For this reason, our results which are based solely on males should be interpreted with caution as our results might be affected by potential spatial biases present among the sexes. Some studies carried out in anthropized gradients in South America have demonstrated the influence of environmental modification on flesh fly communities (Linhares 1981, Mulieri et al. 2011, Beltran et al. 2012, Yepes-Gaurisas et al. 2013, Dufek et al. 2016, Souza and Zuben 2016). However, these studies only analyze the diversity of flies considering three categorical types of habitats (i.e., urban, rural, and wild). This is the first work that considers the three most frequent fates of human modification to the natural environment which drive biodiversity loss (i.e., urbanization, cattle farming, and intensive agriculture) versus two natural habitats (i.e., savanna and forest) to evaluate the habitat effect on sarcophagid fly community structure. All community parameters evaluated in this investigation (i.e., abundance, species richness, and diversity) showed that anthropized areas result in poorer communities of flesh flies. Indeed, we found the lowest community parameters in the urban habitat, where the greatest modification on the original vegetation or native environmental structure by human action were made. Our results support the hypothesis that anthropization determines the community structure of flesh flies, with habitat loss from human influence recognized as the main cause of biodiversity decline (Maxwell et al. 2016, Ceballos et al. 2017). According to the intermediate disturbance hypothesis (Connell 1978), the diversity is higher at intermediate levels of disturbance, because original dominant competitors and colonizers can coexist. Thus, land uses that preserve native elements (e.g., canopy and native vegetation) would also preserve the sarcophagid diversity. This intermediate disturbance that maintains high diversity was observed in this investigation within the cattle farm habitat where some native elements like trees and wild animals were still present. Therefore, this would explain the higher diversity that was found at the cattle farm when compared with the results obtained in the urban and alfalfa crop habitats. This is not surprising as other studies have also shown that other taxa exhibit such pattern of response along anthropization gradients (Blair and Launer 1997, Chapman and Reich 2007, Dufek et al. 2019, Ramírez-Ponce et al. 2019). The availability of diversified microhabitats increases with vegetation complexity, which has been shown to correlate with invertebrate diversity, including Diptera (Reid and Hochuli 2007). The highest diversity in this study was found in the nonanthropized habitats. Savannas as open habitats where the sunlight is intense and direct, usually represent areas successfully colonized by sarcophagid flies, likely due to their cuticles having high thermal reflectance and their active thermoregulatory behavior (Willmer 1982, Mulieri et al. 2011). In fact, Sarcophagidae are usually associated with sites with high temperatures and insolation degree (Mulieri et al. 2011, Souza and Zuben 2016). These characteristics, such as being heliophilous, are adaptative advantages for these flies, allowing them to exploit ephemeral resources presents in open areas. In addition, species of Sarcophagidae are mainly sarcosaprophagous, feeding on feces and carrion (Pape and Dahlem 2010). Therefore, these flies have a very important role in the recycling of organic waste and the incorporation of nutrients into the soil (Savage 2002). Both, the sarcosaprophagous lifecycle and sun-loving behavior may explain the high abundance of sarcophagid flies recorded in the cattle farm where a greater abundance of potential food-resource patches (such as cow dung) and sunny sites were available. The heterogeneity of the environment, that provides a variety of niches, has been proposed to explain differences in calyptrate species diversity. A complex environment will provide a greater number of potential niches and microclimatic conditions, which allows the coexistence of a greater number of sarcophagid fly species. Indeed, a heterogeneous habitat like a forest, can provide a stable environment with a greater diversity of potential sources of food, such as feces and animal carcasses, for both adults and larvae, as well as more stable environments (Pereira de Sousa et al. 2016). On the other hand, the anthropization decreases abundance and species richness because it presumably eliminates several types of substrates necessary for larvae development. This is due to the increase of paved and built areas, the removal of native shrubs and trees in urban settlement, and the deforestation and use of chemical fertilizers and pesticides in cattle raising and agroecosystems (McKinney 2002, 2005; Landis 2016). Moreover, the change in gas composition in the atmosphere and pollution resulting from urbanization represents limitations for the maintenance of native biodiversity in cities (Alberti 2005, McKinney 2008). Our results support the heterogeneity of the environment as a determinant factor of sarcophagid community structure, since we found the lowest abundance, species richness and diversity in two of the anthropized habitats here evaluated (urban and alfalfa crop). In this investigation species turnover contributed more to the high beta diversity than nestedness. These results reinforce the findings of previous studies that demonstrated that environmental filtering reveals species turnover (including within invertebrates) over a large scale (Alahuhta et al. 2017, Zellweger et al. 2017). Overall beta diversity and the contribution of its turnover component showed a positive association with environmental heterogeneity. This in turn suggests that each habitat has the capacity to accommodate unique flesh fly species, which emphasizes their value for biodiversity conservation. The observed variation of flesh fly community composition likely relates to canopy cover and microclimate conditions. In this study we show that beta diversity of these fly communities is dominated by balanced variation in abundance and turnover of species between sites. In addition, we demonstrate that the habitat type was the key factor to configuration of flesh fly community structure, showing that not only the anthropization (presence/absence) played a crucial role in the insect diversity but also the type of human impact. The anthropogenic alteration of environments has dramatic effects on the calyptrate fly community (Nuorteva 1963), with direct changes like habitat loss or indirect changes such as alteration of the microclimate which affect the distribution and abundance of species. Nevertheless, the available information about habitat preference of sarcophagid species is scarce. In this study only native species were found in our samples as compared with Mulieri et al. (2011) who found exotic Sarcophagidae species in association with highly urbanized sites in Buenos Aires. Based on species-specific association with a particular habitat, we detected some species that agree with previous reports: Oxys. varia as indicator of the alfalfa crop which was related to rural settings (Mulieri et al. 2011) and Oxys. parva as indicator of forest which was regarded as an urban avoider species (Dias et al. 1984). On the other hand, in this work we found that H. aurescens was an indicator species of forests, but in Brazil this species has shown a preference for populated areas (Ferreira 1979). Our results show that the forest was the most dissimilar habitat when compared with the others, mainly due to the contribution of several species, which had a high abundance in this habitat (e.g., H. aurescens, Helicobia sp. 1, L. crispula, L. salobrensis, Oxys. parva, and Oxyv. excisa). When analyzing the species preference based on groups of anthropized (urban + cattle farm + alfalfa crop) or natural (savanna + forest) habitats, H. aurescens, Helicobia sp. 1, L. crispula, L. salobrensis, Oxysarcodexia avuncular (Lopes) (Diptera: Sarcophagidae), Oxyv. excisa, Peckia (Sarcodexia) florencioi (Prado and Fonseca) (Diptera: Sarcophagidae), and Peckia (Sarcodexia) lambens (Wiedemann) (Diptera: Sarcophagidae) were found associated with natural habitats with a significantly higher abundance, as observed by Souza and Zuben (2016), whereas Microcerella halli (Engel) (Diptera: Sarcophagidae) and Oxysarcodexia riograndensis Lopes (Diptera: Sarcophagidae) were most abundant in the anthropized habitats. Some species such as Oxysarcodexia terminalis (Wiedemann) (Diptera: Sarcophagidae), Oxys. thornax, Oxysarcodexia wygodzinskyi Lopes and Tibana (Diptera: Sarcophagidae), Peckia (Peckia) enderleini (Engel) (Diptera: Sarcophagidae), Ravinia advena (Walker) (Diptera: Sarcophagidae), Ravinia belforti (Prado and Fonseca) (Diptera: Sarcophagidae), and Tricharaea (Sarcophagula) occidua (Fabricius) (Diptera: Sarcophagidae) seem to be tolerant and resilient to land-use intensification, as indicated by their presence in both anthropized and natural habitats. These species could be considered as ‘urban adapters’ in the Humid Chaco ecoregion due to their high relative abundance in all sites surveyed (McKinney 2002, Mulieri et al. 2011). Several species recorded in all habitat types evaluated in this study stand out in several contexts: P. (S.) lambens can causes myiasis on domestic animals and humans (Neiva and Faria 1913, Guimarães et al. 1983) and Oxys. thornax, the most abundant species on this research, can affect human and animal health by acting as a potential carrier of enteric pathogens (e.g., bacteria, fungi, protozoa, viruses, worms, and helminthic eggs) because it uses feces and dung as a substrate to lay larvae (Mulieri et al. 2010). It is possible that our findings may not be directly extrapolated to forensic studies due to the use of cephalopod molluscs as bait, which are inherently very different from mammal corpse. However, our results show that even without mammalian bait, we still show strong evidence for necrophilous Sarcophagidae as many of the flesh fly species we collected have been previously recorded on corpses and are regarded as forensic indicators [e.g., Mi. halli, Oxys. riograndensis, Oxys. thornax, P. (S.) lambens, Ra. Belforti, and Tr. (S.) occidua] (Alves et al. 2014, Vairo et al. 2017), as well as our bait attracting many well-known Calliphoridae (Diptera) indicator species (Dufek et al. 2019). This contextualizes the medical, veterinary, and forensic importance of the Sarcophagidae species registered herein. This study provides strong support for the hypothesis of anthropization, which results in habitat loss and land conversion into intensive agriculture and urbanization as the main drivers of diversity decline. This research represents the first ecological evaluation of flesh fly community composition in the unsurveyed Humid Chaco ecoregion of Argentina and is, to our knowledge, the first analysis of different land-use environments based on sarcophagid flies. The information here presented seeks to generate knowledge about ecological aspects of Sarcophagidae that can be used not only in medical and veterinary investigations but also in an environmental context. 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TI - The Effect of Anthropization on Sarcophagidae (Diptera: Calyptratae) Community Structure: An Assessment on Different Types of Habitats in the Humid Chaco Ecoregion of Argentina
JO - Journal of Medical Entomology
DO - 10.1093/jme/tjaa071
DA - 2020-09-07
UR - https://www.deepdyve.com/lp/oxford-university-press/the-effect-of-anthropization-on-sarcophagidae-diptera-calyptratae-5tk3gHDBzn
SP - 1468
EP - 1479
VL - 57
IS - 5
DP - DeepDyve
ER -