High Abundance of Neotropical Drosophilids (Diptera: Drosophilidae) in Four Cultivated Areas of Central Brazil

The drosophilid assemblages of four cultivated areas (soy, bean, corn, and orange plantations) grown in the core of the Neotropical region were analyzed by comparing their abundances and compositions. The collections, which were gathered using 38 banana traps, captured 12,560 drosophilids, including nine Neotropical and six exotic species. Most of the flies were collected in the bean (43%) and soy (42%) fields. The composition and relative abundance of species also varied among cultivated areas, with orange orchards presenting the highest relative abundance of exotics due to the dominance of the Afrotropical Zaprionus indianus (Gupta). Crop plantations were dominated by a Neotropical species, Drosophila cardini (Sturtevant), which has been shown to be well adapted to dry and disturbed environments. We discuss the drosophilid assemblages of the cultivated areas, comparing them with assemblages from neighbor urban and natural environments. The low drosophilid richness found in this study is similar to the richness found in urban environments and lower than the drosophilid richness of forests, supporting a pattern already known for other taxa. The high abundance of drosophilids in cultivated areas, as well as the dominance of a Neotropical species (D. cardini) in the crop assemblages, was a surprising result.     

Fruit‐breeding drosophilids (Diptera) in the Neotropics: playing the field and specialising in generalism?

1. Species of Drosophilidae are frequently used as model organisms, but their relationships with the environment, particularly in immature stages, remain poorly known. 2. This is the most comprehensive survey to date of fruit‐breeding drosophilids and their hosts in the Neotropics. Drosophilid host‐utilisation patterns were analysed as to geographic origin (native versus exotic) and level of specialisation. 3. The 180 species of plants recorded as drosophilid hosts are distributed across the main Angiosperm lineages and fleshy‐fruited orders; plant families that hosted the greatest number of drosophilid species were Arecaceae, Moraceae, and Myrtaceae. The 100 nominal drosophilid species recorded breeding in fruits belong to just over one‐third of Neotropical genera; most species (91) belong to Drosophila. Drosophilid species with the greatest resource breadth were Drosophila simulans, Drosophila nebulosa, and Zaprionus indianus. 4. Exotic drosophilids breed in more plant species than Neotropical drosophilids and use exotic hosts more frequently, possibly because they are generalists that have survived the trial of introduction and establishment in the Neotropics. Native drosophilids are more variable in resource breadth and sometimes adopt exotic hosts. 5. Amongst the 49 drosophilids with enough records for analysis (> 4), 48 were categorised as generalists. One possible explanation for such overwhelming generalism is the high diversity of Neotropical habitat or hosts. A second, non‐exclusive explanation, suggested by recent studies and empirically supported by the absence of host specialisation found in this study, is that drosophilids could be selective of the dominant yeasts and bacteria in host tissue, and not of the hosts themselves.     

Assemblage of drosophilids (Diptera,Drosophilidae) inhabiting flooded and nonflooded areas in the extreme South of Brazil

Several studies on the potential use of drosophilid assemblages as bioindicator systems have been carried out in the last years. Nevertheless, the successful application of these organisms in these systems requires adequate filling of several knowledge gaps. In this sense, little is known about drosophilid assemblages in wetlands and flooded areas. The present study provides the first survey of drosophilid species inhabiting such environments in the extreme South of Brazil and compares general beta-diversity patterns between assemblages of flooded versus nonflooded areas. The specimens were collected with banana-baited traps, and the assemblages recovered in eight wetlands of the southernmost coast of Brazil were compared to those recovered from seven nonflooded areas of the Pampa and Atlantic Forest biomes. A total of 5028 and 2571 individuals encompassing 27 and 37 species were collected in the flooded and nonflooded areas, respectively. The differential species composition patterns presented between these areas was statistically supported, which seems to be related to the lower beta-diversity presented by swamps, especially in regard to dominance patterns. So, the open and climatically harsher environment provided by wetlands possibly constitutes a hostile environment for the entry and, mainly, for the persistence of several native Drosophilidae species, in contrast to some exotic and more plastic species (as Drosophila simulans and Zaprionus indianus). Since the diversity gradient of flooded areas does not seem to be related to the conservation status of the swamp, our results question the use of Drosophilidae species as bioindicators of environmental disturbance and antropic influence in wetlands.     

Spermatogenesis of Zaprionus indianus and Zaprionus sepsoides (Diptera,Drosophilidae): Cytochemical,structural and ultrastructural characterization

Zaprionus indianus is a drosophilid native to the Afrotropical region that has colonized South America and exhibits a wide geographical distribution. In contrast, Z. sepsoides is restricted to certain African regions. The two species differ in the size of their testes, which are larger in Z. indianus than in Z. sepsoides. To better understand the biology and the degree of differentiation of these species, the current study evaluated spermatogenesis in males of different ages by conventional staining techniques and ultrastructural analysis. Spermatogenesis and the ultrastructure of spermatozoa were similar in the two species, and the diploid number was confirmed to be 2n = 12. A greater number of spermatozoa were observed in young Z. indianus (1–3 days old) compared to Z. sepsoides males, which showed a higher frequency of cells at the early stages of spermatogenesis. The head of the sperm was strongly marked by silver staining, lacto-acetic orcein and the Feulgen reaction; the P.A.S. reaction revealed glycogen granules in the testes of both species. Both species presented similar arrangement of microtubules (9+9+2), two mitochondrial derivatives of different size and 64 spermatozoa per bundle. Such similarity within the genus Zaprionus with other species of Drosophila, indicates that these structures are conserved in the family Drosophilidae. The differences observed the number and frequency of sperm cells in the early stages of spermatogenesis, between the young males of Z. indianus and Z. sepsoides, are features that may interfere with reproductive success and be related to the invasive potential of Z. indianus.     

Differences in larval nutritional requirements and female oviposition preference reflect the order of fruit colonization of Zaprionus indianus and Drosophila simulans

Species coexist using the same nutritional resource by partitioning it either in space or time, but few studies explore how species-specific nutritional requirements allow partitioning. Zaprionus indianus and Drosophila simulans co-exist in figs by invading the fruit at different stages; Z. indianus colonizes ripe figs, whereas D. simulans oviposits in decaying fruit. Larvae feed on yeast growing on the fruit, which serves as their primary protein source. Because yeast populations increase as fruit decays, we find that ripe fruit has lower protein content than rotting fruit. Therefore, we hypothesized that Z. indianus and D. simulans larvae differ in their dietary requirements for protein. We used nutritional geometry to assess the effects of protein and carbohydrate concentration in the larval diet on life history characters in both species. Survival, development time, and ovariole number respond differently to the composition of the larval diet, with Z. indianus generally performing better across a wider range of protein concentrations. Correspondingly, we found that Z. indianus females preferred to lay eggs on low protein foods, while D. simulans females chose higher protein foods for oviposition when competing with Z. indianus. We propose the different nutritional requirements and oviposition preference of these two species allows them to temporally partition their habitat.     

Invasive and flexible: niche shift in the drosophilid <Emphasis Type="Italic">Zaprionus indianus</Emphasis> (Insecta,Diptera)

Although predictions of potential distributions of invasive species often assume niche conservatism, recent analyses suggest that niche shifts can also occur. Thus, further studies are necessary to provide a better understanding of niche dynamics and to predict geographic distribution in invaded areas. The present study investigated the niche shift hypothesis at a broad biogeographical scale, using the comprehensive distribution of the invasive species Zaprionus indianus in its native (Africa) and invaded (America and India) ranges. Z. indianus is a very successful invasive species that presents high adaptive flexibility and extreme physiological tolerance. To investigate whether Z. indianus changed its climatic niche from Africa to America and India, multivariate analyses, as well as ecological niche modeling procedures (GARP, MAXENT and Mahalanobis distances), were used. Multivariate analyses showed that the niche spaces of Z. indianus in Africa, India and the Americas were significantly different (Wilks’ λ from a Multivariate Analysis of Variance, MANOVA = 0.115; P < 0.0001). Out of 108 occurrences in America, only 11 (ca 10%) were classified, by Canonical Variate Analysis scores, as belonging to its original range in Africa, whereas only 5% of the 39 occurrences in India were classified as belonging to Z. indianus’ original range. Consensus results from MAXENT, GARP and Mahalanobis distances correctly predicted only 27% of the occurrences in India and 85% of occurrences in America. Thus, all analyses showed that Zaprionus indianus quickly expanded ranges into different environments in the invaded areas, suggesting climatic niche shifts, primarily in India.     

Comparison of overwintering survival and fertility of Zaprionus indianus (Diptera: Drosophilidae) flies from native and invaded ranges

Zaprionus indianus is a fly species native to the Afrotropical biogeographic region that invaded the South American continent 20 years ago. Its southernmost record is 34°S in areas with temperate climates with cold winters. To better understand its invasion biology, we investigated physiological responses to winter-like abiotic conditions that may be relevant in Z. indianus geographic expansion. We characterized Z. indianus females reproductive traits (ovarian maturation and fertility) and survival in response to cold treatments with summer-like and winter-like photoperiods. We also compared these traits between native (Yokadouma, Africa) and invasive (Yuto, South America) range wild-derived flies. We showed that Z. indianus females have the ability to arrest ovarian maturation and maintain fertility following recovery from cold stress. The critical temperature for ovarian maturation of this species was estimated at c. 13 °C, an intermediate value between those of tropical and temperate drosophilid species. Wild-derived females from Yuto responded to winter-like photoperiod by slowing down ovarian maturation at low but permissive temperatures of 14 °C and 16 °C and also delayed the start of oviposition after cold treatment. Yuto flies also survived better and recovered 20% faster from chill coma than flies from Yokadouma. These results are consistent with a scenario of local adaptations or phenotypic plasticity in the invaded range, and suggest that photoperiod could act as modulator of ovarian arrest. Conversely, the fact that native range flies showed higher fertility after cold recovery than females from invaded range is not indicative of local adaptation. All in all, our findings report a set of physiological responses that would enable Z. indianus expansion to temperate and cold areas, but also results that are compatible with a limitation to the invasion process.     

Population genetics and recent colonization history of the invasive drosophilid Zaprionus indianus in Mexico and Central America

Zaprionus indianus, also known as the African fig fly, is an invasive pest of a variety of commercial and native fruit. The species was first reported in Brazil in 1999, but has established itself in much of the New World within the last 10–15 years. We used nucleotide sequences from a segment of the mitochondrial cytochrome c oxidase subunit I (COI) gene to examine haplotype relationships, population structure, and infer the colonization history of Z. indianus in Mexico and Panama. Construction of a haplotype network showed that six COI haplotypes, obtained from flies collected at six localities in Mexico and one in Panama, clustered into three distinct clades. Clade composition was generally consistent in flies from Panama to northwestern Mexico, and analysis of molecular variance indicated no significant structure among populations. Three of the six haplotypes from Mexico and Panama were identical to previously reported haplotypes from Brazil. None of the six haplotypes, however, were shared with previously reported haplotypes from potential source populations in the Old World. The results of our genetic analysis suggest that the invasion of Z. indianus into Central America and Mexico most probably includes a northward migration of individuals from Brazil, with the possibility of at least one additional introduction of Z. indianus to the New World. Additional sequence data from potential source populations in the Old World will be required to confidently determine the number of introductions of Z. indianus into the New World, and to identify the geographic source.     

Simulating natural light and temperature cycles in the laboratory reveals differential effects on activity/rest rhythm of four Drosophilids

Recent studies under semi-natural conditions have revealed various unique features of activity/rest rhythms in Drosophilids that differ from those under standard laboratory conditions. An additional afternoon peak (A-peak) has been reported for Drosophila melanogaster and another species D. malerkotliana while D. ananassae exhibited mostly unimodal diurnal activity. To tease apart the role of light and temperature in mediating these species-specific behaviours of four Drosophilid species D. melanogaster, D. malerkotliana, D. ananassae, and Zaprionus indianus we simulated gradual natural light and/or temperature cycles conditions in laboratory. The pattern observed under semi-natural conditions could be reproduced in the laboratory for all the species under a variety of simulated conditions. D. melanogaster and D. malerkotliana showed similar patterns where as D. ananassae consistently exhibited predominant morning activity under almost all regimes. Z. indianus showed clearly rhythmic activity mostly when temperature cycles were provided. We find that gradually changing light intensities reaching a sufficiently high peak value can elicit A-peak in D. melanogaster, D. malerkotliana, and D. ananassae even at mild ambient temperature. Furthermore, we show that high mid-day temperature could induce A-peak in all species even under constant light conditions suggesting that this A-peak is likely to be a stress response.     

<Emphasis Type="Italic">Drosophila</Emphasis> as models to understand the adaptive process during invasion

The last few decades have seen a growing number of species invasions globally, including many insect species. In drosophilids, there are several examples of successful invasions, i.e. Zaprionus indianus and Drosophila subobscura some decades ago, but the most recent and prominent example is the invasion of Europe and North America by the pest species, Drosophila suzukii. During the invasive process, species often encounter diverse environmental conditions that they must respond to, either through rapid genetic adaptive shifts or phenotypic plasticity, or by some combination of both. Consequently, invasive species constitute powerful models for investigating various questions related to the adaptive processes that underpin successful invasions. In this paper, we highlight how Drosophila have been and remain a valuable model group for understanding these underlying adaptive processes, and how they enable insight into key questions in invasion biology, including how quickly adaptive responses can occur when species are faced with new environmental conditions.     

hosimary: a new hAT transposon group involved in horizontal transfer

A PCR screening approach was used to search for sequences homologous to a previously described hAT transposon found in Drosophila simulans and Drosophila sechellia, named here as hosimary. In this study, 52 Drosophilidae species were analyzed and these sequences seem to be restricted to some species of the melanogaster group and Zaprionus indianus. These species present variable number of copies and most of those appear to be putatively encoding. The high hosimary sequences similarity among different species and the patchy distribution presented by this transposon strongly support the hypothesis that hosimary was horizontally transferred between the melanogaster group species and Z. indianus.     

Variability of Wing Size and Shape in Three Populations of a Recent Brazilian Invader, Zaprionus indianus (Diptera: Drosophilidae), from Different Habitats

Zaprionus indianus (Diptera: Drosophilidae) is an African species that was introduced in Brazil near the end of the 1990’s decade. To evaluate the adaptive potential of morphological traits in natural populations of this recently introduced species, we have investigated wing size and shape variation at Rio de Janeiro populations only two years after the first record of Z. indianus in Brazil. Significant genetic differences among populations from three distinct ecological habitats were detected. The heritability and evolvability estimates show that, even with the population bottleneck that should have occurred during the invasion event, an appreciable amount of additive genetic variation for wing size and shape was retained. Our results also indicated a greater influence of environmental variation on wing size than on wing shape. The importance of quantitative genetic variability and plasticity in the successful establishment and dispersal of Z. indianus in the Brazilian territory is then discussed.     

DNA barcode discovers two cryptic species and two geographical radiations in the invasive drosophilid Zaprionus indianus

Comparing introduced to ancestral populations within a phylogeographical context is crucial in any study aiming to understand the ecological genetics of an invasive species. Zaprionus indianus is a cosmopolitan drosophilid that has recently succeeded to expand its geographical range upon three continents (Africa, Asia and the Americas). We studied the distribution of mitochondrial DNA (mtDNA) haplotypes for two genes (CO‐I and CO‐II) among 23 geographical populations. mtDNA revealed the presence of two well‐supported phylogenetic lineages (phylads), with bootstrap value of 100%. Phylad I included three African populations, reinforcing the African‐origin hypothesis of the species. Within phylad II, a distinct phylogeographical pattern was discovered: Atlantic populations (from the Americas and Madeira) were closer to the ancestral African populations than to Eastern ones (from Madagascar, Middle East and India). This means that during its passage from endemism to cosmopolitanism, Z. indianus exhibited two independent radiations, the older (the Eastern) to the East, and the younger (the Atlantic) to the West. Discriminant function analysis using 13 morphometrical characters was also able to discriminate between the two molecular phylads (93.34 ± 1.67%), although detailed morphological analysis of male genitalia using scanning electron microscopy showed no significant differences. Finally, crossing experiments revealed the presence of reproductive barrier between populations from the two phylads, and further between populations within phylad I. Hence, a bona species status was assigned to two new, cryptic species: Zaprionus africanus and Zaprionus gabonicus, and both were encompassed along with Z. indianus and Zaprionus megalorchis into the indianus complex. The ecology of these two species reveals that they are forest dwellers, which explains their restricted endemic distribution, in contrast to their relative cosmopolitan Z. indianus, known to be a human‐commensal. Our results reconfirm the great utility of mtDNA at both inter‐ and intraspecific analyses within the frame of an integrated taxonomical project.     

Susceptibility and Interactions of <Emphasis Type="Italic">Drosophila suzukii</Emphasis> and <Emphasis Type="Italic">Zaprionus indianus</Emphasis> (Diptera: Drosophilidae) in Damaging Strawberry

Drosophila suzukii (Matsumura) has been recently detected causing damage to strawberries in Brazil. Infestation in strawberry culture has often been observed jointly with the presence of Zaprionus indianus Gupta. This study investigated the susceptibility of strawberries at three ripening stages to infestation of D. suzukii and Z. indianus and their interaction. In the laboratory, strawberries cv. Albion at different ripening stages (green, semi-ripe and ripe) were exposed to D. suzukii and Z. indianus for 24 h in choice and no-choice bioassays. Additionally, we evaluated the effects of mechanical damage incurred artificially or by D. suzukii oviposition on Z. indianus infestation. In no-choice bioassay, there were no significant differences in fruit susceptibility to D. suzukii infestation at different ripening stages. However, in choice bioassay, D. suzukii adults preferred to oviposit on R fruit. The presence of mechanical damage did not increase susceptibility of fruit to D. suzukii oviposition. For Z. indianus, there was greater susceptibility of R fruit in relation to SR and G fruit in both the choice and no-choice bioassays. There was a significant and positive interaction of mechanical damage and damage caused by D. suzukii to R fruit and infestation by Z. indianus, which was not observed in SR and G fruit. Although infestation of Z. indianus is related to attack damaged or decaying fruit, this work shows that this species has the ability to oviposit and develop in healthy strawberry fruit with and increased infestation level when the fruit has damage to its epidermis.     

From a non‐target to a target: identification of a fermentation volatile blend attractive to Zaprionus indianus

The African fig fly, Zaprionus indianus Gupta, is rapidly spreading through the New World and is a new potential pest for numerous fruit crops. Methods are needed to detect and monitor Z. indianus. A recent study shows that Z. indianus can be attracted with a mixture of wine and vinegar, but there are no chemical attractants yet identified. This fly was captured incidentally as a non‐target insect in experiments to develop chemical lures, based on wine and vinegar fermentation volatiles, for Drosophila suzukii Matsumura and Drosophila melanogaster Meigen. We then generated testable hypotheses on what combination of these volatiles was involved in Z. indianus attraction to wine and vinegar. We determined through a series of trapping experiments that the blend of ethanol, acetic acid, acetoin, isoamyl acetate, methionol and ethyl hexanoate constitutes a strong attractant for Z. indianus and accounts for its attraction to the combination of wine and vinegar. These results and findings provide the first opportunity to develop a long‐lasting and consistent chemical lure for trapping of Z. indianus. Such a lure in a suitable trap should provide a good means to document the spread of the fly and determine its seasonality and abundance in new areas and crops.     

Scenario of the spread of the invasive species Zaprionus indianus Gupta, 1970 (Diptera, Drosophilidae) in Brazil

Zaprionus indianus was first recorded in Brazil in 1999 and rapidly spread throughout the country. We have obtained data on esterase loci polymorphisms (Est2 and Est3), and analyzed them, using Landscape Shape Interpolation and the Monmonier Maximum Difference Algorithm to discover how regional invasion occurred. Hence, it was apparent that Z. indianus, after first arriving in São Paulo state, spread throughout the country, probably together with the transportation of commercial fruits by way of the two main Brazilian freeways, BR 153, to the south and the surrounding countryside, and the BR 116 along the coast and throughout the north-east.     

Drosophila suzukii in Michigan vineyards,and the first report of Zaprionus indianus from this region

Drosophila suzukii is a new invasive pest that in recent years has become established in the Great Lakes region of the United States. Understanding the level of infestation in potentially susceptible crops is an important first step for planning appropriate management responses. This study was conducted in 2010–2012 to determine the infestation potential of this pest in native Vitis labrusca, French hybrid and V. vinifera grape cultivars grown in Michigan vineyards. Drosophila suzukii adults were reared out of collected grape samples in all 3 years, comprising a low proportion of all emerged drosophilids in each of the years. This trend was also found in vacuum sampling, conducted in 2011, with the majority of flies collected being non‐D. suzukii drosophilids. Another recently introduced invasive fly species, Zaprionus indianus, was also reared out of grape samples collected in 2012. While the results of this study indicate no immediate threats to commercial grape production from D. suzukii, further research is needed to elucidate possible secondary effects that this species may have on vineyards, such as the introduction of diseases to the fruit.     

Colonizing potential of Drosophilidae (Insecta,Diptera) in environments with different grades of urbanization

Modern environmental destruction through human action has had a big impact on biological diversity. In the Brazilian Cerrado, the second largest South American biome, more than 60% of the native vegetation has been devastated mainly due to anthropic activities. One of the consequences of these activities is the distinct dispersion patterns of endemic and colonizer species in urban environments. In this report we assess the colonizing potential of drosophilids in environments with different grades of urbanization, defined according to the vegetation cover, edifications and demographic density. We performed 12 monthly collections in the city of Brasília, the capital of Brazil, which is located in the core region of the Cerrado. Although we identified 16 species, 90% of the 22,509 captured specimens were Zaprionus indianus, a species recently introduced in Brazil, and the cosmopolitan D. simulans. We captured all the exotic species that occur in the Biome, with the exception of D. kikkawai, but only 8 from the 25 endemic species that occur in natural sites around Brasília. The abundance of four endemic species (D. nebulosa, D. sturtevanti, D. cardini and D. prosaltans) decreased as the grade of urbanization increased. D. immigrans, an exotic species, showed the opposite pattern. We concluded that most endemic species of Drosophilidae are not able to colonize the new environment represented by the city, and that some species of this family may detect not only environmental alteration, by their presence or absence, but also the grade of environmental disturbance, by their relative abundance.     

Newly invading species exploiting native host-plants: the case of the African Zaprionus indianus (Gupta) in the Brazilian Cerrado (Diptera,Drosophilidae)

The African Zaprionus indianus (Diptera, Drosophilidae) was introduced into the Neotropical Region by the end of the 1990’s, and it became abundant in several types of altered and natural environments. In the Cerrado, the second South American biome in extension, it has been found mainly in open vegetation and during the rainy season. In the current work, we showed that Z. indianus utilizes a major native fruit of the Brazilian Cerrado (Solanum lycocarpum) primarily, all over the fructification period and states of fruit’s decay, confirming the adaptative versatility of this invading fly in new environments.     

Effects of exotic annual grass litter and local environmental gradients on annual plant community structure

Exotic annual grasses have been introduced into many semi-arid ecosystems worldwide, often to the detriment of native plant communities. The accumulation of litter from these grasses (i.e. residual dry biomass) has been demonstrated to negatively impact native plant communities and promote positive feedbacks to exotic grass persistence. More targeted experiments are needed, however, to determine the relative impact of exotic grass litter on plant community structure across local environmental gradients. We experimentally added exotic grass litter to annual forb-dominated open woodland communities positioned along natural canopy cover gradients in southwest Western Australia. These communities are an important component of this region’s plant biodiversity hotspot and are documented to be under threat from exotic annual grasses. After a one-year treatment period, we measured the effects of exotic grass litter, soil properties, and canopy cover on native and exotic species richness and abundance, as well as common species’ biomass and abundances. Plant community structure was more strongly influenced by soil properties and canopy cover than by grass litter. Total plant abundances per plot, however, were significantly lower in litter addition plots than control plots, a trend driven by native species. Exotic grass litter was also associated with lower abundances of one very common native species: Waitzia acuminata. Our results suggest that exotic grass litter limits the establishment of some native species in this system. Over multiple years, these subtle impacts may contribute substantially to the successful advancement of exotic species into this system, particularly in certain microenvironments.