First Detections of Zaprionus indianus (Diptera: Drosophilidae) in Minnesota
Zaprionus indianus Gupta (Diptera: Drosophilidae), also known as the African fig fly, is native to the tropical regions of Africa (Renkema et al. 2013, J. Entomol. Soc. Ont. 144: 125–130). Zaprionus indianus can be identified by the even number of conspicuous silvery stripes outlined in black on the dorsal side of the head and thorax (Renkema et al. 2013; van der Linde et al. 2006, Florida Entomol. 89: 402–404). Specimen coloration on the head and thorax can range from yellow (van der Linde et al. 2006) to a darker reddish-brown (Renkema et al. 2013), with the anterior femora having 4–6 distinct composite spines, each with a second short branch (van der Linde et al. 2006). Zaprionus indianus spread to South America in 1998, with the first detection in Brazil (David et al. 2006, Heredity 96: 53–62). In North America, Z. indianus was first detected in Florida in 2005 (van der Linde et al. 2006). As of 2012, detections of Z. indianus in the United States were confirmed as far west as California and as far north as Wisconsin, Michigan, Connecticut, and New York, with a total of 14 states reporting detections between 2006 and 2012 (van der Linde, 2012, http://www.kimvdlinde.com/professional/Zaprionus%20distribution%20US.php). In Canada, Z. indianus was confirmed in Ontario and Quebec in 2013 (Renkema et al. 2013). As analyzed by Lichtenberg and Olson (2018, PLoS One 13(2): e0192280), the recent expansion of international trade has greatly increased the risk of introducing nonnative pest species and contributing to deleterious ecological and agricultural impacts, particularly for fruit and vegetable crops. The high volume of international trade, thus, provides one plausible explanation as to how Z. indianus entered North America.
Despite its common name, Z. indianus will colonize and oviposit on damaged or decaying fruit of a variety of plant species (van der Linde et al. 2006). In its native range of Africa, 74 species of fruit are known to be suitable hosts; additionally, 17 more species have tested positive as hosts in Florida such as pond apple, Annona glabra L., and grapefruit, Citrus×paradisi Macfadyen (van der Linde et al. 2006). In Brazil, Z. indianus rapidly became a pest of fig fruit, Ficus carica L. In a study by Gomes et al. (2002, Braz. J. Microbiol. 34: 5–7), the yeast, Candida tropicalis (Castellani ) Berkhout, was found in all figs damaged by Z. indianus, suggesting that this insect is a carrier of the yeast, which can contribute to fruit decomposition. Although Z. indianus is a generalist, its interaction with fig is unique in that females will oviposit eggs near the ostiole prior to maturation of the fruit, which also infects the fruit with C. tropicalis (Matevelli et al. 2015, J. Insect Physiol. 82: 66–74). This behavior may have contributed to its pest status. Within the first year of detection in Brazil (1998), exports of figs from São Paulo were reduced by 50%, resulting in estimated annual losses of $767,000 USD due to Z. indianus damage (Oliviera et al. 2013, J. Appl. Entomol. 137: 1–15). Interestingly, C. tropicalis is also known to be a human pathogen that is implicated as one of the more important Candida species for epidemiology and virulence (Zuza-Alves et al. 2017, Front. Microbiol. 8: 1927)
In this report, we provide confirmation of the first detections of Z. indianus adults in Minnesota via a trapping network for the invasive, drosophila, Drosophila suzukii (Matsumura). From 2013 to 2016, apple-cider vinegar traps were deployed to monitor D. suzukii populations (Asplen et al. 2015, J. Pest Sci. 88: 469–494). Traps were placed at various farms surrounding the Minneapolis–St. Paul metropolitan area and in southeast Minnesota, including a vineyard located 8.1 km south of Hastings, MN and the Rosemount Research and Outreach Center near Rosemount, MN, which is 23.5 km west of the vineyard. Traps were checked weekly, from late May to September. In 2017, commercially available Scentry® traps (Great Lakes IPM, Vestaburg, MI) developed for D. suzukii and baited with a fourcomponent lure (Cha et al. 2017, Environ. Entomol. 46: 907–915) were used for monitoring D. suzukii. Scentry traps contain a lure that consists of a blend of acetic acid, ethanol, acetoin, and methionol (Cha et al. 2017) and 100 ml of water in the bottom of the trap mixed with a drop of dish soap to break the surface tension. One advantage of the Scentry traps (with water) and the four-component lure is that it minimizes the number of nontarget insects collected (Cha et al. 2017), especially compared to apple-cider vinegar or other fermenting bait traps designed for D. suzukii (Asplen et al. 2015). Scentry traps were deployed at the Rosemount Research and Outreach Center near Rosemount, MN, and the vineyard near Hastings, MN, in addition to locations that were part of the ongoing trapping network throughout the Minneapolis–St. Paul metropolitan area with data posted to the FruitEdge™ website (https://www.fruitedge.umn.edu/swdtrap). Traps at the vineyard were removed in mid-September following the completion of grape harvest. However, three traps for D. suzukii were monitored until mid-December at the Rosemount Research and Outreach Center.
The first detection of Z. indianus in Minnesota occurred in September 2013, at the vineyard near Hastings, MN (N 44.685345; W –92.871799), where one female fly was found in an apple cider vinegar trap in wine grapes (e.g., Frotenac, Vitis vinifera × riparia (data not shown) (African Fig Fly, 2014, FruitEdge. https://www.fruitedge.umn.edu/affalert); this specimen was confirmed by Allen L. Norrbom of the Systematic Entomology Laboratory, Agricultural Research Service, USDA (Washington, DC). No subsequent detections of Z. indianus were observed in Minnesota until October 2017, when several adult flies were found in Scentry traps near Rosemount, MN (Table 1). Specimens of Z. indianus were placed in the Insect Museum, Department of Entomology, University of Minnesota. Zaprionus indianus were found in traps collected from 13 October until 2 November 2017, with a peak mean catch of 31.67 ± 8.5 adults per trap per week on 19 October. Traps positive for Z. indianus were located on the edge of a tree line, within 10 m of an adjacent raspberry planting used for research purposes (N 44.728363; W –93.097024). Despite the reduction of nontarget flies caught in the Scentry trap with the improved four-component lure (Cha et al. 2017), the substantial numbers of Z. indianus trapped in 2017 indicates that this trap/lure could serve as a potential monitoring tool for Z. indianus as well as for D. suzukii.
In Minnesota, D. suzukii has been an opportunistic and economic pest of all small berry crops since 2012 (Asplen et al. 2015). The possible addition of Z. indianus as an additional species within the pest complex could be problematic. Bernardi et al. (2017, Neotrop. Entomol. 46: 1–7) demonstrated that in strawberry, Fragaria×ananassa Duch., prior feeding damage by D. suzukii can create a habitat that is significantly more suitable for Z. indianus oviposition and adult development. The coexistence of D. suzukii with Z. indianus, which causes primary damage in ripening fruit and accelerates decay and secondary damage, could lead to potential increases in damage for Minnesota fruit crops. The detections of Z. indianus in temperate northern states suggests either long-distance migration could be involved, given the potential for long-distance movement observed with many other fruit fly species (Asplen et al. 2015; Chapman et al. 2005, Bull. Entomol. Res. 94: 123–136), or the capacity to adapt to conditions outside of its original tropical environment, which has also been observed in other fruit fly species (da Mata et al. 2008, Biol. Invasions 12: 1231–1241).
After spreading to the northern United States, Z. indianus was documented in Ontario and Quebec, Canada, in apple cider vinegar traps used for surveying D. suzukii. The Z. indianus specimens were collected from peach (Prunus persica L.), blueberry (Vaccinium spp. L.), raspberry (Rubus idaeus L.), strawberry (Fragaria× ananassa (Weston) Duchesne ex Rozier (pro sp.)), cherry (Prunus spp. L.), and plums (Prunus spp. L.) during pre- and postharvest (Renkema et al. 2013). Many of these crops are specialty crops also grown in Minnesota and face pest pressure from D. suzukii. The generalist behavior in crop choice by Z. indianus (Renkema et al. 2013), in addition to physiological elasticity in a variety of climates, provides a basis for a niche shift in this species (de Mata et al. 2008) and, thus, the potential for Z. indianus to colonize Minnesota fruit crops. However, in 2013 and 2017, despite early season monitoring, Z. indianus was not found until September and October, respectively, which suggests that early season crops may not be at risk for damage by Z. indianus. Additional research, including more extensive monitoring studies, will be required to determine if Z. indianus consistently occurs in Minnesota and, if so, how the season long phenology of Z. indianus will overlap with crop phenology. Moreover, additional information on the biology, phenology, and host preferences of Z. indianus and D. suzukii will be needed to better understand what crops may be most at risk in Minnesota and the upper Midwest region.
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