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The proliferation of alien invasive species that rapidly colonize large areas provides an amazing opportunity to investigate the causes that allow their successful colonization (biological invasion), as well as the change they cause in already established communities. Zaprionus indianus Gupta (Diptera, Drosophilidae), also known as the African fig fly in South America and the striped vinegar fly in the USA, is a species native to the Afrotropical biogeographic region (Yassin et al., 2008). Aided by international trade and commerce (Hulme, 2009), about 30 years ago this species begun to expand its geographical distribution from its native range in Africa to other areas in the world (Vilela, 1999; van der Linde, 2006; Lavagnino et al., 2008; Commar et al., 2012; Kremmer et al., 2017). Z. indianus can be classified as a category E invasive species according to Blackburn et al. (2011), since it is fully invasive, with individuals dispersing, surviving and reproducing at multiple sites in many habitats. This species is considered a generalist and polyphagous species (Aluja & Mangan, 2007), since it can use a wide variety of decaying fruits as breeding and feeding resources (van der Linde et al., 2006; Lavagnino et al., 2008). This characteristic is perhaps one of the principal factors contributing to its rapid geographical expansion and successful colonization history. Thus, the spread of this generalist species through different habitats in North, Central and South American continents most likely involve different developmental environments, that is, different host fruits (van der Linde et al., 2006; Lavagnino et al., 2008). Zaprionus indianus is typically regarded as a secondary pest, since adult females normally oviposit in fruits that have been mechanically injured by other insects (Lasa & Tadeo, 2015;Bernardi et al., 2017) although, the presence of this species along with other insects is still concerning to soft-skinned fruits farmers. Thus, the presence of Z. indianus as well as other Drosophila species that were found in fruits injured in the first place by pest insect species as Anastrepha fraterculus Wiedemann (Diptera, Tephritidae), Ceratitis capitata Wiedemann (Diptera, Tephritidae) or Drosophila suzukii Matsumura (Diptera, Drosophilidae), can be associated with a greater release of volatiles that function as stimuli for orientation, attraction and oviposition (Bernardi et al., 2017). However, during the process of colonization to new areas Z. indianus became the north-eastern Argentina would be first pest in cultivars of strawberries (Fragaria × ananassa, Bernardi et al., 2017) and figs (Ficus carica L., Lasa et al., 2020) during geographic expansion in America. Certainly, adult females can oviposit on the fruit surface of intact ripe strawberry fruits, then larvae emerge, penetrate the epidermis and feed on the fruit pulp and yeasts (Bernardi et al., 2017). In the case of figs, females lay eggs on the bracts of the ostiole in intact fruits at the beginning of maturation and larvae enter the fruit through small natural wounds of the fruit (Lasa et al., 2020). Either as a primary or secondary pest, oviposition and subsequent larval feeding of Z. indianus on agricultural crops can contribute to decreased yields and rejected product. After the first record of this species in Argentina (Soto et al., 2006), it was determined that Z. indianus colonized different areas of Argentina (Lavagnino et al., 2008) and that the geographical expansion to north-eastern Argentina would be the consequence from a single introduction wave from Brazil (Goya et al., 2020). On the other hand, D. melanogaster and D. simulans are cosmopolitan sibling species that exploit several fermenting fruits as feeding and breeding sites. Considering that the worldwide expansion of D. simulans is more recent than its sibling species) and that D. melanogaster has a stronger association of with human activity (Keller 2007, Capy & Gilbert 2004), it would be more likely for this species to be sampled in the area evaluated. However, in a previous study, Vilela et al. (1980) detected that D. simulans was more abundant than D. melanogaster.

In this study, we report the distribution, relative abundance and use of feeding and breeding resources by Z. indianus, D. melanogaster and D. simulans in different localities of Argentina (Table I). We analyzed only males, since females of D. simulans and D. melanogaster are indistinguishable (Markow & O’Grady, 2006). D. simulans and D. melanogaster were classified to species by the inspection of their genitalia (Markow & O’Grady, 2006) whereas we identified Z. indianus by its phenotype (van der Linde, 2006; Commar et al., 2012). Two different collection techniques were performed to quantify numbers of individuals and the relative abundance of D. melanogaster, D. simulans and Z. indianus: adult collections in the wild and emerged flies in the laboratory. We collected adults in the wild by net sweeping over: a) baits wherein flies were collected by means of 10 bucket (20 cm of diameter) with fermenting banana baits randomly distributed throughout each collecting sites and b) rotten fruits that were found on the ground (the number of resources utilized as natural attractant is indicated in Table I). In the case of emerged flies in the laboratory, the collections consisted in gathering rotten fruits from the same locations, of adult collection. Fruits were isolated in closed containers with two pieces (10 cm x 10 cm, each) of paper towel and taken to the laboratory. Emerged adult flies from each container were identified by species for 15 days to ensure that all emerged flies were offspring of flies that laid eggs in those fruits in their respective natural environments. Adult collection using fermented banana baits was ineffective to attract Z. indianus (see also Castrezana, 2011) although this specie has emerged from banana (Table II and Willbrand et al., 2018). Taking into account this result, we decided to exclude the adult sample collected on banana bait of the evaluation and use only the flies collected on fruits laying on the ground. We only analyzed Z. indianus, D. melanogaster and D. simulans even though other species as A. fraterculus, C. capitata and Drosophila mercatorum Patterson & Wheeler (Diptera, Drosophilidae; data not shown) were sampled. Taking both adult and emerged flies sampled together, a total of 4.412 flies were collected from 11 localities (Table II). More than half of the flies collected (51,4%, 2266 flies) were identified as D. melanogaster, whereas 1.917 (43,4%) and 229 (5,2%) of the total flies collected were Z. indianus and D. simulans, respectively. We observed that Z. indianus was absent in the locality of Ing. Juarez population (Table II) as was observed previously (Lavagnino et al., 2008). It is important to note that the resource available in Ing. Juarez is guava, which has been reported as host of Z. indianus, in this study (Table II, Fig.1) and others (Lavagnino et al., 2008; Lasa et al., 2017). Besides, Ing Juarez exhibits similar climatic parameters than the other localities where Z. indianus is present. Thus, neither the lack of breeding and feeding sites nor climatic factors would be the cause of the absence of Z. indianus in Ing. Juarez. This gap in the distribution of Z. indianus in northern Argentina is strange considering that Ing Juarez is 160 km away from Las Lomitas, where this species is found. Our results revealed (Table II) that D. melanogaster (59,0%, 2009 flies) was the most abundant species in adult collections in the wild (3407 flies), while the relative abundance of the other two species were 36,5% for Z. indianus (1243 flies) and 4,5% for D. simulans (155 flies). On the other hand, for emerged flies in the laboratory, our records showed (Table II) a change in the relative abundance pattern compared to adult collections in the wild, since Z. indianus represented 67,0% (674 flies) of the total emerged flies’ sample while D. melanogaster constituted the 25,6% with 257 flies and D. simulans has the 7,4% (74 flies). The emergence record in the laboratory was significantly different respect to adult collection in the wild (Χ.= 349,9, d.f.= 2, p < 0,0001), since we detected an excess of emerged flies corresponding to Z. indianus respect to Drosophila species, suggesting a decoupling between the proportions of the species analyzed that were attracted to and emerged from the feeding and breeding sites evaluated. There is niche overlap between the fly species studied, since flies of Drosophila species and Z. indianus emerged from most of the resources evaluated (Fig. 1, Table II). However, emergence data indicate (Fig. 1) that the percentage of Drosophila species respect to Z. indianus varied from 100% (orange) to 6% (mango). The result on orange should be explained: on the one hand, orange resource was sampled in Ituzaingo, wherein Z. indianus was found using other resources (Mango and Guava) as breeding sites (Table II). On the other hand, Z. indianus exhibited a good performance when it developed in orange as breeding resource in laboratory experiments (Lavagnino et al., 2020). Thus, the absence of Z. indianus in orange could be the consequence of chance since there is no biological explanation to the absence of this species from both orange samples (adult and emerged collections). Finally, the proportions of Drosophila species and Z. indianus collected and emerged were significantly different (p<0.05) for all fruit resources evaluated (excluding orange). The fact that the percentages of emerged flies is different from the ones collected around fruit resources in the wild could be accounted by differences in oviposition preferences between species, and/or by interspecific competition (Fanara et al., 1999; Rodrigues et al., 2016). In this sense, Galego & Carareto (2005) demonstrated that Z. indianus residues significantly reduced the viability of D. simulans reared under lab conditions. In summary, our study indicates that the pattern of the relative abundance of Drosophila species and Z. indianus is variable depending on the locality, the fruit resource and the sample evaluated.

Acknowledgments

ACKNOWLEDGMENTS

We would like to thank Estación Experimental Egropecuaria (INTA): Bella Vista, (Corrientes), Montecarlo (Misiones) and Yuto (Jujuy) for invaluable help during collecting trips. This work was supported by a grant from Agencia Nacional de Promoción Científica y Técnica (Argentina). NJL and JJF are members of Carrera del Investigador Científico of CONICET (Argentina).

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