Diptera: Ulidiidae)

Journal of Insect Science (2017) 17(1): 29; 1–9 doi: 10.1093/jisesa/iew123 Research article Aggregation Behavior and a Putative Aggregation Pheromone in Sugar Beet Root Maggot Flies (Diptera: Ulidiidae) Erik J. Wenninger,1,2 Susan Y. Emmert,3 Kelly Tindall,4 Hongjian Ding,3,5 Mark A. Boetel,6 D. Rajabaskar,3,7 and Sanford D. Eigenbrode3 1Department of Plant, Soil, and Entomological Sciences, University of Idaho, Kimberly Research & Extension Center, Kimberly, ID 83341, 2Corresponding author, e-mail: [email protected], 3Department of Plant, Soil, and Entomological Sciences, University of Idaho, Moscow, ID 83844, 4Twin Falls County Cooperative Extension, 246 3rd Ave. East, Twin Falls, ID 83301, 5Current address: Food and Drug Administration, Jefferson, AR 72079, 6Department of Entomology, North Dakota State University, NDSU Dept. 7650, P.O. Box 6050, Fargo, ND 58108, and 7Current address: Department of Agricultural Entomology, Tamil Nadu Agricultural University, Coimbatore 641 003, India Subject Editor: Stephen Lapointe Received 21 September 2016; Editorial decision 8 December 2016 Abstract Male-biased aggregations of sugar beet root maggot, Tetanops myopaeformis (Ro¨ der) (Diptera: Ulidiidae), flies were observed on utility poles near sugar beet (Beta vulgaris L. [Chenopodiaceae]) fields in southern Idaho; this contrasts with the approximately equal sex ratio typically observed within fields. Peak observation of mating pairs coincided with peak diurnal abundance of flies. Volatiles released by individual male and female flies were sampled from 08:00 to 24:00 hours in the laboratory using solid-phase microextraction and analyzed using gas chromatog- raphy/mass spectrometry (GC/MS). Eleven compounds were uniquely detected from males. Three of these compounds (2-undecanol, 2-decanol, and sec-nonyl acetate) were detected in greater quantities during 12:00– 24:00 hours than during 08:00–12:00 hours. The remaining eight compounds uniquely detected from males did not exhibit temporal trends in release. Both sexes produced 2-nonanol, but males produced substantially higher (ca. 80-fold) concentrations of this compound than females, again peaking after 12:00 hours. The temporal synchrony among male aggregation behavior, peak mating rates, and release of certain volatile compounds by males suggest that T. myopaeformis flies exhibit lekking behavior and produce an associated pheromone. Field assays using synthetic blends of the putative aggregation pheromone showed evidence of attraction in both females and males. Key words: Tetanops myopaeformis, sex pheromone, sugar beet root maggot fly, lekking, Beta vulgaris The sugar beet root maggot, Tetanops myopaeformis (Ro¨ der) (Diptera: Possible pheromone-based options for improving T. myopaefor- Ulidiidae), is an important pest of sugar beet, Beta vulgaris L. mis management methodology could include the development of (Chenopodiaceae), in the United States and Canada. Larvae feed on attract-and-kill strategies and more effective monitoring tools to op- roots and root hairs, causing damage that can lead to significant losses timize the timing and efficacy of conventional and alternative con- in yield of sugar beet roots and allow for secondary infections by trol tools. Aggregations of T. myopaeformis flies often are observed pathogens (Hawley 1922, Harper 1962, Bechinski et al. 1993). on utility poles and other vertical surfaces near sugar beet fields dur- Management of T. myopaeformis primarily targets larvae in the soil, ing the afternoon hours; this phenomenon is familiar to both sugar relying heavily upon the use of carbamate and organophosphate in- beet producers and scientists studying T. myopaeformis (personal secticides, both of which have worker safety issues and environmental observations; Anderson et al. 1994, Chirumamilla et al. 2008), but risks (Gupta 2006). Moreover, the carbamate insecticide that has been its underlying mechanisms have not been studied. While collecting widely used in Idaho for root maggot management (i.e., aldicarb) is flies in large numbers from such aggregations on utility poles in scheduled to be phased out of use by 2018 (Anonymous 2010), and Minidoka County, Idaho, we noted that the flies produced an odor the remaining organophosphates may be at high risk of removal from that was detectable to the human observer, prompting an investiga- registration in relation to ongoing enforcement of the Food Quality tion into the possible existence of sex or aggregation pheromones Protection Act of 1996. As such, there exists an urgent need to develop produced by these flies. Neither aggregation behavior nor phero- alternative strategies to manage this pest. mone production have been studied for any member of the family VC The Authors 2017. Published by Oxford University Press on behalf of Entomological Society of America. 1 This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact [email protected] 2 Journal of Insect Science, 2017, Vol. 17, No. 1 Ulidiidae, but sex or aggregation pheromones have been described observer continued walking the transect until another fly was and exploited in attract-and-kill and mass trapping tactics for some located. In 2001, observations were taken hourly from 09:00 to Tephritidae (flies within the superfamily Tephritoidea, which also 17:00 hours, and in 2003, observations were taken every two hours includes Ulidiidae). For example, a blend of male-specific phero- from 09:00 to 15:00 hours. Each row observed was selected mones that is attractive to females in laboratory bioassays and field randomly. trials has been identified for the Mediterranean fruit fly, Ceratitis In 2003 and 2006, T. myopaeformis flies were observed on util- capitata (Wiedemann) (Diptera: Tephritidae) (Baker et al. 1990, ity poles bordering sugar beet fields. In 2003, observations were Heath et al. 1991, Jang et al. 1994, Howse and Knapp 1996, Jang made on 31 May, 1 June, and 2 June—the days of peak fly activity and Light 1996). In addition, a male-produced pheromone of the pa- that year. In 2006, observations were made on 24 and 31 May, and paya fruit fly, Toxotrypana curvicauda Gerstaecker (Diptera: 13 and 23 June; these observations were timed to encompass the T. Tephritidae), is attractive to conspecific females in the field (Landolt myopaeformis mating period in order to determine if there was a et al. 1988, 1991), and male-produced pheromones have been inves- seasonal trend in aggregation behavior. On each observation date, tigated for use in attract-and-kill or mass trapping control of the we recorded the number of individual males and females observed Caribbean fruit fly, Anastrepha suspense (Loew) (Diptera: and the number of mating pairs observed every 2 h from 08:00 (in Tephritidae) (Nation 1989, Heath et al. 1993). Moreover, a male 2003) or 10:00 (in 2006) to 20:00 hours. In 2003, observations were sex pheromone in combination with a female aggregation phero- made on seven utility poles spaced at approximately 100-m intervals mone plus a food attractant and phagostimulant has been effective along the perimeter of a single sugar beet field. In 2006, observa- in mass trapping the olive fruit fly, Bactrocera oleae (Rossi) (for- tions were expanded to include five beet fields, with six utility poles merly Dacus oleae) (Diptera: Tephritidae), in Greece (Haniotakis sampled in one field and seven in the other four fields (i.e., a total of et al. 1991). 34 poles). In 2006, the poles from one field were not sampled at The goals of this study included describing aggregation and mat- 20:00 on 13 June due to a technical issue. Poles were similarly ing behavior of T. myopaeformis in the field, identifying potential spaced, and all fields were within an approximate radius of 4 km. pheromones produced by male and female flies, and testing the at- tractiveness of a synthetic putative pheromone blend in the field. Collection of Maggots and Rearing of Adult Flies Over 3 years, we performed observations in commercial sugar beet Third-instar T. myopaeformis were collected from sugar beet fields fields in southern Idaho to document the aggregation and mating be- in Minidoka County, Idaho during July and August of 2001 and havior of T. myopaeformis adults, including the sex ratios and tim- March 2002 for the use in the laboratory during the spring and the ing of aggregations as well as the onset of mating during the day. summer of 2002. By mid-July, T. myopaeformis larvae reach matur- Subsequent laboratory experiments focused on identifying the vola- ity, cease feeding, and enter diapause (Bechinski et al. 1993). Larvae tile compounds released by both male and female flies and charac- were collected by digging to a depth of approximately 0.5 m and terizing the timing of their release. Finally, we evaluated responses separating them from the excavated soil. During the mid- and late- of female and male flies to synthetic lures containing blends of the summer collections, it was often possible to pull up individual stand- putative male-produced pheromone in commercial sugar beet fields ing beet plants and collect larvae from the roots and adjacent soil. in Idaho and North Dakota. After transfer to the laboratory, larvae were cleaned with distilled water and placed onto moist cotton pads in Petri dishes. Larvae were stored in dishes in total darkness at 4 C until they could be Materials and Methods reared to the adult stage for the bioassay. Larvae collected during Field Observations the summer were stored for a minimum of 6 months to allow for Field observations were conducted during 2001, 2003, and 2006 in completion of diapause (Callenbach et al. 1957). Larvae collected commercial sugar beet fields in Minidoka County, Idaho. This area during the spring were stored for a minimum of one week and up to historically has experienced the greatest pressure from T.

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