FPirstroceedings report :of A ftheric aHnawaiian fig E onntomological Maui Society (2018) 50:55–65 55

First Report of African Fig Fly, indianus Gupta (Diptera: ), on the Island of Maui, , USA, in 2017 and Potential Impacts to the Hawaiian Entomofauna

Brittany Willbrand,1 Douglas Pfeiffer,1 Luc Leblanc,2 and Amir Yassin3 1Virginia Tech Department of Entomology, Price Hall, Blacksburg, VA 24601 2University of Idaho, Department of Entomology, Plant Pathology and Nematology, 875 Pe- rimeter Drive MS 2329, Moscow, ID 83844-2329 3Sorbonne Universites, Museum National d’Histoire Naturelle, 12 rue Buffon, CP 39, Paris 75005, France

Abstract. This report confirms the first reported observation ofZaprionus india- nus Gupta (Diptera: Drosophilidae), commonly known as African fig fly, on Maui (new island record). Adult specimens were collected in October and November 2017 while surveying for populations of suzukii (Matsumura) (Dip- tera: Drosophilidae). Specimens were retrieved from four localities in Haiku and Kula among traps positioned at fruiting height in six host plant environments (orange, lemon, starfruit, banana, strawberry, and cherimoya). Historically, the earliest records of Z. indianus in the state were recorded on Oahu in 2013 (new state record, new island record), on Kauai in 2015 (new island record), and on the Big Island (Hawaii) in 2017 (new island record). Including this report, there are currently at least 33 introduced Drosophilidae species established in the state of Hawaii. Furthermore, it is the second member belonging to Zaprionus that has been identified on the Hawaiian Islands. Specimens were not only retrieved from farms and subdivisions but also within mountain ranges and state forest reserves, suggesting that further research is needed to evaluate potential impacts to endemic entomofauna.

Key words: Invasive drosophilids, , African fig fly, new island record, Maui

The African fig fly, Zaprionus in- nus Anaprionus have an odd number of dianus Gupta (Diptera: Drosophilidae), white stripes whereas members of sub- is a red-brown vinegar fly with distinctive genus Zaprionus, including Z. indianus, secondary coloring that is native to the have an even number of white stripes (van Afrotropics (Gupta 1970). As illustrated der Linde 2010). Furthermore, the black in Figure 1, members of genus Zaprionus and white stripes on Z. indianus are of have longitudinal white stripes on the equal size with the stripe width main- dorsal regions of the head and thorax (Yas- tained the full length of the head to the sin and David 2010). Genus Zaprionus thorax (van der Linde 2010). The vittiger contains two subgenera, Anaprionus and species group, of which Z. indianus is a Zaprionus, which can be differentiated member, is characterized by a row of com- through examination of external morphol- posite spines fused with long bristles at the ogy. While both groups have longitudinal base of the forefemur (Yassin and David white stripes, species belonging to subge- 2010). Once considered cryptic species, 56 Willbrand et al.

a b

Figure 1. Thorax (a) and front tibia (b) of Zaprionus indianus collected on Maui. The lack of a white spot on the scutellum, and the presence of tibial spines, separates this species from Zaprionus ghesquierei. members of the indianus species complex, mis, and consume pulp and yeast vital for including Z. africanus, Z. gabonicus, and development (Bernardi et al. 2017). Unlike Z. indianus, can be reliably distinguished Drosophila simulans Sturtevant and other by spermatheca shape with Z. africanus drosophilids that oviposit on decaying figs, possessing a narrower spermatheca and an adult Z. indianus females can oviposit apically serrated aedeagal flap,Z. gaboni- on ripening figs, increasing economic cus with a basally smooth aedeagal flap damage incurred by farmers (Matavelli and Z. indianus with a basally serrated et al. 2015). As a secondary pest, adult Z. aedeagal flap (Yassin and David 2010). indianus females can oviposit into fruits Though morphologically similar, species that have mechanical injury from other belonging to the indianus species complex , including oviposition injury by display a variety of ecological behaviors Drosophila suzukii (Matsumura) (Ber- resulting in differences in pest status and nardi et al. 2017) making the presence of invasive potential. both drosophilids particularly concerning As a polyphagous drosophilid, Z. in- to farmers of any soft-skinned fruit. dianus uses a wide range of host plants Aided by international trade and com- for opportunistic feeding and breeding merce, Z. indianus has been introduced to (Lavagnino et al. 2008). This results in a wide variety of localities outside of its damage to agricultural crops as well as native range including North and South making eradication of the drosophilid America, Europe, and Asia (Westphal et challenging once established. Even though al. 2008, Hulme 2009). Invasive range ex- Z. indianus is typically regarded as a pansion for Z. indianus has been reported secondary pest, it has demonstrated the on the Asian continent in India (Gupta potential to cause direct injury to select 1970, Fartyal et al. 2014), Saudi Arabia cultivars of both fig (Matavelli et al. 2015) (Amoudi et al. 1991), Egypt (Yassin and and strawberry (Bernardi et al. 2017) Abou-Youssef 2004), Iraq (Al T’Oma et al. fruits. Oviposition and subsequent larval 2010), and Jordan (Al-Jboory and Katbeh- feeding on agricultural crops can contrib- Bader 2012). In Europe, specimens have ute to decreased yields and rejected prod- been reported in France (Kremmer, et al. uct. On intact ripe strawberry fruit, adult 2017) and Madeira archipelago (Rego et females can oviposit on the fruit surface al. 2017). In , Z. indianus where larvae emerge, penetrate the epider- has invaded Brazil (Vilela 1999), Uru- First report: African fig fly on Maui 57 guay (Goñi et al. 2001), and Argentina composed of a 236 ml Mason jar and a (Soto et al. 2006). In Central America, Z. 473 ml red Solo cup and assembled with indianus was confirmed in Panama (van epoxy, sandpaper, an unfolded paperclip, der Linde et al. 2006). In , and a soldering tool (Cold-Heat®). The reports of Z. indianus were published in first 2.5 cm of the Solo cup interior was Mexico (Lasa and Tadeo 2015), Canada scoured with sandpaper, then coated with (Renkema et al. 2013), and in the United a thin layer of epoxy. The silver band from States including Florida (van der Linde et the Mason jar lid was then firmly pressed al. 2006), Virginia (Pfeiffer et al. 2012), down into the cup interior. The Solo cup Michigan (Van Timmeren and Isaacs was allowed to cure for 24 hours. An un- 2014), and Pennsylvania (Joshi et al. 2014). folded paperclip was pressed against the We report here an additional range expan- ceramic tip of the soldering tool to conduct sion to the island of Maui, Hawaii, USA heat. Then, the ceramic tip was used to in 2017, discovered during a survey to pierce the solo cup in eight places (two on identify whether populations of the inva- each side) to create 5 mm diameter entry sive drosophilid D. suzukii were present holes. Nylon rope was strung through the within several localities and host plants. top two holes of the Solo cup to enable trap installation (Figure 2). Materials and Methods Attractants. Attractants were selected Survey localities and host plants. based on drosophilids innate attraction Four locations on Maui were selected for to fermentation volatiles (Stensmyr et the qualitative survey: a private estate in al. 2003, Stökyl et al. 2010, Faucher et Haiku, HI (20.899859°N, –156.283533°W, al. 2013) and historical success in field elevation 302 m), Kula Agricultural capture using vinegars and wine as ol- Park (20.797167°N, –156.368971°W, 341 factory baits (Landoldt et al. 2012, Cha m), Kula Country Farms (20.747138°N, et al. 2015). The five attractants used in –156.337140°W, 889 m), and University this survey were: apple cider vinegar of Hawaii at Manoa Kula Research Station (ACV, supplied by Marukan Vinegar (20.757534°N; –156.319755°W, 980 m). Co. Ltd.), brown rice vinegar (BRV, sup- Seven host plants were selected to survey plied by Marukan Vinegar Co. Ltd.), red including fruiting trees (orange, lemon, wine (RW, Oak Leaf Vineyards, Merlot), starfruit, banana, cherimoya) and fruits ACV+RW, and BRV+RW. The latter and vegetables (strawberry, pumpkin). two attractant blends were prepared at a Orange, lemon, and starfruit were surveyed 60:40% concentration of vinegar to wine. at the Haiku estate. Bananas were surveyed Acetic acid (AcOH) concentrations were at Kula Agricultural Park. Strawberries, quantified by Dr. Naoki Akasaka with pumpkin, and lemon were surveyed at Kula high-performance liquid chromatography Country Farms. Cherimoya was surveyed (HPLC, Organic Acid Analysis System at Kula Research Station. Prominence, Shimadzu) as previously Trap assembly. The trapping device described in Akasaka et al. (2017). The used in this experiment was a novel AcOH concentrations of undiluted BRV variation of the traditional deli cup design and ACV were 4.23% and 4.37% (% wt/ where a Mason jar, serving as a removable vol), respectively. Once diluted with red trap base, houses the drowning solution wine, the AcOH concentrations of 60% while a Solo cup permits entry and pas- BRV and 60% ACV were 2.54% and sive diffusion of the attractant within 2.62% (% wt/vol), respectively. Attractants the headspace of the trap. Each trap was were aliquoted (40 ml per trap) into Mason 58 Willbrand et al.

Figure 2. Trap installation: example of trap positioning on a lemon tree jars, a drop of unscented dish soap was Agricultural Park. On 2 Nov 2017, 15 traps added to each jar to break the surface ten- were deployed on the strawberry, pump- sion, and the lids and bands were affixed kin, and lemon at Kula Country Farms. for transport. After one week, traps were removed and Trap installation and retrieval. Five the specimens collected. Specimens were traps were used (one of each attractant strained by pouring the attractant solution type) for each host plant at each location over a fine mesh filter (1 mm) and were for a total of 40 traps. Once trap locations stored in 70% isopropyl alcohol for three were delineated, the traps were installed days prior to examination. at fruiting height, which varied by crop Identification and voucher specimens. type. For fruiting trees (orange, lemon, Though the original objective of the sur- banana, cherimoya, and starfruit), traps vey was to identify whether D. suzukii were hung at a ca. 1 m height. For fruit and populations were present (Yes/No) in vegetable crops (strawberry and pumpkin), the localities and host-plants surveyed, traps were tied to a gardening stake that this objective was expanded to include Z. was secured in the ground at fruit height. indianus after the first specimen was rec- After nylon rope was used to hang the trap ognized. Specimens were identified asD. to fruiting height, a Mason jar containing suzukii, Z. indianus, or non-target. Once attractant solution was screwed on to the D. suzukii and Z. indianus specimens were bottom of the Solo cup. On October 23rd identified for a particular attractant type 2017, 15 traps were deployed on orange, and host plant combination, no further lemon, and starfruit trees at the Haiku quantification was performed. Identifica- estate. On 31 Oct 2017, 5 traps were de- tion as Z. indianus was confirmed through ployed at the cherimoya grove at Kula examination of external morphology by Research Station. On 1 Nov 2017, 5 traps BW, using standard keys (van der Linde were deployed on the bananas at Kula 2010, Yassin and David 2010). Voucher First report: African fig fly on Maui 59 specimens were submitted to DP and LL, suzukii specimens were retrieved. At Kula for imaging, identification, and collection Country Farms, both Z. indianus and D. submission. Taxonomic confirmation was suzukii specimens were retrieved from all provided by LL and AY. Specimens were attractant types used in the lemon grove. deposited at the Systemic Entomology In the strawberry fields, no target droso- Lab, USDA ARS (Beltsville, MD), the De- philids were captured when RW was used partment of Entomology at Virginia Tech, as an attractant. However, BRV and ACV, the Muséum d’Histoire Naturelle de Paris, alone and blended with RW, were effective the Hawaii Department of Agriculture, the in the field capture of both target droso- Bishop Museum, and the Museum philids. For the pumpkin traps, D. suzukii at the University of Hawaii at Manoa. specimens were captured using ACV+RW or BRV+RW attractants. No Z. indianus Results specimens were retrieved, regardless of Adult Z. indianus specimens were attractant used. At Kula Research Sta- captured within traps installed in six of tion, every attractant used was effective in the seven host plant fruits surveyed (ba- capturing D. suzukii, whereas Z. indianus nana, cherimoya, lemon, orange, starfruit, specimens were retrieved only in RW, and strawberry) and at all four localities ACV+RW, and BRV+RW baited traps. It is surveyed. Survey results are presented noteworthy that BRV and BRV+RW were (Table 1) simply to show that Z. indianus effective at field captures of both target was attracted to the various baits and in drosophilids, as previous research has different fruit systems, each with a differ- established BRV as an effective attractant ent olfactory environment. At the private to D. suzukii in laboratory trapping experi- estate in Haiku, all three host plants ments (Akasaka et al. 2017). The attrac- surveyed including lemon, orange, and tants used in this survey and the resulting starfruit contained both Z. indianus and captures were reported simply to provide a D. suzukii specimens. At Kula Agriculture detailed record of the circumstances from Park, only Z. indianus specimens were re- which target specimens were attracted. trieved from the traps placed in the banana Whether an attractant resulted in captures grove. At Kula Country Farms, D. suzukii in this survey, does not provide evidence specimens were retrieved from all three that these results would be applicable to host plants surveyed, while Z. indianus other surveys or experiments. Further specimens were retrieved from the lemon research would be needed to discern any and strawberry, but not the pumpkin traps. trends comparing attractant efficacy with At Kula Research Station, the traps posi- confidence, as the lack of replicates and tioned in the Cherimoya grove contained quantification limit the extrapolation of both D. suzukii and Z. indianus. trends outside of this survey. Five attractants were used (ACV, BRV, RW, ACV+RW, BRV+RW) in the field Discussion capture of two exotic drosophilids (Z. This report established a new island indianus, D. suzukii) with results that record for Z. indianus on Maui, compiled varied by host plant and locality. At the collection data throughout the state (Table private estate in Haiku, every attractant 2), and provided an update for introduced examined resulted in captures of Z. india- Drosophilidae established in Hawaii. nus and D. suzukii. At Kula Agricultural Historically, the earliest Z. indianus Park, every attractant was effective in specimens in the state were collected on capturing Z. indianus adults, but no D. Oahu in 2013 (new state record, new island 60 Willbrand et al. – + + + + + + + AFF BRV+RW – + + + + + + + SWD – + + + + + + + AFF ACV+RW – + + + + + + + SWD – – + + + + + + AFF RW – – – + + + + + SWD – – + + + + + + AFF BRV Zaprionus indianus (AFF) and attractant, by and host-plant. survey locality, – – + + + + + + SWD (SWD) and (SWD) – – + + + + + + AFF ACV

- – + + + + + + SWD Drosophila suzukii Species: Attractant: Lemon Starfruit Orange Banana Cherimoya Lemon Strawberry Pumpkin

Qualitative 1. reportingTable of Attractant Abbreviations: ACV (Apple cider vinegar), BRV (Brown rice vinegar), RW (Red wine). Minus sign denotes zero captures; Plus sign sign zerocaptures;denotesPlus Minus sign (Redwine). RW rice vinegar), (Brown BRV vinegar), cider (Apple AttractantACV Abbreviations: denotes more or captures. one Private Haiku Estate

Kula Agricultural Park Kula Research Station Kula Country Farms

First report: African fig fly on Maui 61 1 HDOA IM-UH HDOA HDOA MNH-P BM BM HDOA VT-ENT, USDA-SEL, BM USDA-SEL, VT-ENT, HDOA, USDA-SEL HDOA, BM Personal BM Personal Collection Personal BM 2 B. WillbrandB. al. et. B. WillbrandB. al. et. N. Evenhuis et. al. et. Evenhuis N. K. Adachi;K. Ruabora, A. CurtissR. al. et. B. WillbrandB. al. et. C. ImadaC. N. Evenhuis et. al. et. Evenhuis N. L. Ishii WillbrandB. al. et. B. AzamaB. N. Evenhuis et. al. et. Evenhuis N.

K. MagnaccaK. N. Evenhuis et. al. et. Evenhuis N. K. MagnaccaK. Collector K. MagnaccaK.

Cherimoya Strawberry, lemon Surinam cherry Orange, lemon, Banana Litchi starfruit Jaboticaba

Unknown* Unknown* environment Unknown*

Host plant Research station Farm Mountains Forest reserve Farm Residence Farm Mountains Mountains Residence Residence Mountains Mountains Mountains Gulch Habitat Gulch 980 889 1356 905.3 302 341 1342 1387

1397 610 1383

(m)

Elev. –156.33714 –156.33714 –158.10284 –159.69015 –156.28353 –156.33690 –158.10302 –158.10370 –158.10357 –158.10360 GPS W (K. Magnacca, personal communication, 2018). (K. Magnacca, personal communication, 2018). 2 20.75753 20.74714 21.42582 22.09820 20.89986 20.79717 21.42582 21.42480

21.42457 21.42475 GPS N

Kula Kula Lualualei Kokee Kokee State Park Kainaliu Haiku Kula Lualualei Lualualei Lihue Kaneohe Lualualei Peahinaia Trail Lualualei Central Kaluaa Gulch Locality Pahole Gulch (Evenhuis et al., 2017). 2017). al., et (Evenhuis 1 records in the State of Hawaii. N.S. = new state record; N.I. = new island record. Collection abbreviations: HDOA HDOA abbreviations: Collection record. island new = N.I. record;state new = N.S. ZaprionusHawaii. of indianusState the inrecords

N.I. N.I. N.I.

Record N.I. N.S., * captured with banana bait 2017 Hawaii Maui 2017 2017 Kauai 2018 2017 2017 2017 2016 2017 2015 2014 2017 2013 Oahu 2017 2013 Table 2. Table Year (Hawaii Department of Agriculture), USDA-SEL (United States Department of Agriculture – Systemic Entomology Lab), BM (Bishop Museum), Museum), (Bishop BM Lab), Entomology Systemic – Agriculture of Department States (United USDA-SEL Agriculture), of Department (Hawaii VT-ENT (Virginia – Entomology Department), Tech MNH-P (Muséum d’Histoire Naturelle de IM-UHParis), (Insect Museum – University Hawaii). of 2013 62 Willbrand et al. record), on Kauai in 2015 (new island re- attractants used were unsuitable for the cord), and on the Big Island in 2017 (new given combination of target species and island record). Adding to the detailed list host plant environment. However, other of introduced Drosophilidae compiled by factors such as climate, elevation, fruiting Leblanc et al. (2009), there can now be stage, and population dispersal may have considered at least 33 introduced Droso- contributed to the results. The absence of philidae species established in the state of Z. indianus in the pumpkin fields of Kula Hawaii. Country Farms may be attributed to popu- This is the second member of genus lation dispersal to preferred hosts, such as Zaprionus that has been identified on the the adjacent lemon grove. Even though Z. Hawaiian Islands. In 2005, Z. ghesquierei indianus specimens were retrieved from Collart was identified on the island of the majority of host plant environments Hawaii and a year later specimens were surveyed (lemon, orange, starfruit, ba- identified throughout Kula, Maui (Leblanc nana, cherimoya, strawberry), the presence et al. 2009). Zaprionus ghesquierei can be of an insect is not sufficient evidence of easily distinguished from Z. indianus, as economically significant damage. Further specimens have a white spot on the tip of research is needed to determine economic the scutellum of Z. ghesquierei (lacking in thresholds by crop and to characterize Z. indianus (Figure 1a) and the presence ecological impacts to endemic species. of spurs on the foretibiae of Z. indianus Unfortunately, the discovery of Z. (Figure 1b) (Yassin and David 2010). Fol- indianus at four localities throughout lowing this report of Z. indianus, earlier Maui provokes more questions than an- Zaprionus captured in Kula in 2006 swers—Is the range expansion limited to were re-examined by L.L., and their iden- agricultural ecosystems, or are they also tity as Z. ghesquierei was re-confirmed. present in native forests? Throughout Furthermore, four Z. ghesquierei vouchers the state, specimens have not only been at the University of Hawaii Insect Museum retrieved from farms and subdivisions were re-identified by Camiel Doorenweerd but also within mountain ranges and state to confirm the identification. No Z. ghes- forest reserves, which suggests that the quierei specimens were identified in this species is able to thrive in a wide variety survey. of environments. Based on our results, it The effectiveness of a given compound appears that further surveying on Maui is to elicit an attraction response is influ- needed in regions producing soft-skinned enced by environmental cues (Faucher fruit and berries, native forest reserves, et al. 2013) and physiological adaptations and within diverse microclimates. Will the (Matavelli et al. 2015, Nguyen et al. 2016). combined presence of D. suzukii and Z. in- Thus, attractant efficacy is mediated not dianus have deleterious impacts for Maui only by the species unique preferences, farmers? Considering that Z. indianus can but also by environmental co-factors, cause direct injury to fig and strawberry such as olfactory and visual cues, that (Matavelli et al. 2015, Bernardi et al. vary between host plant environments. 2017), and that these crops are produced In this survey, no D. suzukii specimens by Maui farmers, the pest potential of this were retrieved from the banana grove introduced species should be examined at Kula Agricultural Park and no Z. in- and economic thresholds defined. Are dianus specimens were retrieved in the there any adverse impacts to endemic pumpkin field at Kula Country Farms. drosophilids? Zaprionus indianus has In both instances, it is possible that the led to declines of native drosophilids in First report: African fig fly on Maui 63 other locations (Castro and Vilente 2001, thank Chauncy and Teena Monden at Tidon et al. 2003, da Silva et al. 2005b, Kula Country Farms, Sylvester Tumbaga da Silva et al. 2005a) and the Hawaiian at Kula Agricultural Park, and Pamela Islands are already struggling to cope with Shingaki at Kula Research Station for the appearance of many invasive species, permitting and assisting with trap instal- including insects. On Hawaii and Maui, lation and retrieval. Special thanks to even though researchers found a strong as- Dr. Devin Ridgley, Scorpio-V division of sociation between exotic drosophilids with HNu Photonics, and Mary Liang, National introduced host plant environments and Solar Observatory (NSO) at the Daniel endemic drosophilids with native plant K. Inouye Solar Telescope (DKIST), for species, invasive drosophilids were still reviewing this manuscript. We would encountered in native forests and endemic like to thank Dr. Mark G. Wright and the drosophilids in disturbed or nonnative two anonymous reviewers that provided environments (Leblanc et al. 2013). critical feedback to greatly enhance this This finding not only suggests eco- report. We would also like to thank Janis logical interactions between endemic and Matsunaga, Hawaii Department of Agri- introduced species but also adaptations culture, Camiel Doorenweerd, University within a dynamic environment, both of of Hawaii Insect Museum, Dr. Allen Norr- which warrant characterization. Addi- bom, USDA-SEL, and Dr. Karl Magnacca tional research is needed to quantify the for their support in providing collection economic and ecological significance of details. this finding and to examine whether eradi- cation efforts are necessary and feasible. 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