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Racemic Pheromone Blends Disrupt Mate Location in the Invasive Swede Midge, Contarinia nasturtii

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Swede midge, Contarinia nasturtii Kieffer, is an invasive cecidomyiid pest that causes serious losses of Brassica oilseed and vegetable crops in the Northeastern U.S. and Canada. Currently, few alternatives to systemic insecticides exist for its management. Because a single feeding larva can render heading Brassica crops unmarketable, management strategies that prevent oviposition are needed urgently. Pheromone-mediated mating disruption is a promising management approach for swede midge because it prevents mating and subsequent crop damage. While the swede midge pheromone has been identified, one of the major barriers to using it in mating disruption is the high cost of synthesis. Racemic blends, consisting of natural and non-natural stereoisomers, could be useful for mating disruption because they are cheaper to produce. However, it is not clear whether racemic pheromone blends attract males and/or prevent them from locating and mating with females. Here, we studied the behavior of male swede midge in Y-tube and wind tunnel bioassays to pheromone blends. Specifically, we tested whether males: (1) are attracted to different doses of pheromone, (2) discriminate between blends comprising natural stereospecific or racemic components, or a combination thereof, and (3) are able to locate and copulate with females in pheromone-permeated olfactometers. We found that picogram amounts of pheromone attracted males and prevented them from locating females in y-tube olfactometers. While males were more attracted to stereospecific blends, compared to racemic blends, all blends tested prevented nearly all males mating with females. Therefore, low dose racemic blends may be promising for pheromone-mediated mating disruption.
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Racemic Pheromone Blends Disrupt Mate Location in the Invasive
Swede Midge, Contarinia nasturtii
Elisabeth A. Hodgdon
1
&Rebecca H. Hallett
2
&Kimberly F. Wallin
3,4
&Chase A. Stratton
1
&Yolanda H. Chen
1
Received: 5 February 2019 /Revised: 4 May 2019 /Accepted: 28 May 2019 /Published online: 22 June 2019
#Springer Science+Business Media, LLC, part of Springer Nature 2019
Abstract
Swede midge, Contarinia nasturtii Kieffer, is an invasive cecidomyiid pest that causes serious losses of Brassica oilseed and
vegetable crops in the Northeastern U.S. and Canada. Currently, few alternatives to systemic insecticides exist for its manage-
ment. Because a single feeding larva can render heading Brassica crops unmarketable, management strategies that prevent
oviposition are needed urgently. Pheromone-mediated mating disruption is a promising management approach for swede midge
because it prevents mating and subsequent crop damage.While the swede midge pheromone has been identified, one of the major
barriers to using it in mating disruption is the high cost of synthesis. Racemic blends, consisting of natural and non-natural
stereoisomers, could be useful for mating disruption because they are cheaper to produce. However, it is not clear whether
racemic pheromone blends attract males and/or prevent them from locating and mating with females. Here, we studied the
behavior of male swede midge in Y-tube and wind tunnel bioassays to pheromone blends. Specifically, we tested whether males:
(1) are attracted to different doses of pheromone, (2) discriminate between blends comprising natural stereospecific or racemic
components, or a combination thereof, and (3) are able to locate and copulate with females in pheromone-permeated olfactom-
eters. We found that picogram amounts of pheromone attracted males and prevented them from locating females in y-tube
olfactometers. While males were more attracted to stereospecific blends, compared to racemic blends, all blends tested prevented
nearly all males mating with females. Therefore, low dose racemic blends may be promising for pheromone-mediated mating
disruption.
Keywords Pheromone .Mating disruption .Vegetable pest management .Reproduction .Swede midge .Cecidomyiidae
Introduction
Contarinia nasturtii Kieffer (swede midge; Diptera:
Cecidomyiidae) is a small galling fly that is a serious pest of
Brassica spp. (Brassicaceae) vegetable and oilseed crops in
Europe, Eastern Canada and the Northeastern USA (Chen et al.
2011; Hallett and Heal 2001). Larvae feed within the plant mer-
istem, causing deformed and scarred leaves and stems and, in
severe cases, can cause complete loss of heads of broccoli, cau-
liflower, cabbage, and other related Brassica crops. Recently,
vegetable growers in the US states of New York and Vermont
reported up to 100% yield loss of organic kale and broccoli (Y.
Chen, C. Hoepting, pers. comm.). No insecticides that are ap-
proved for certified-organic production are effective in control-
ling the midge (Evans and Hallett 2016;Seamanetal.2014).
Due to the severe economic losses inflicted by this pest, some
small, diversified organic growers in the region now avoid
Brassica production entirely (Y. Chen, pers. obs.).
Several aspects of swede midge biology create difficulty man-
aging this pest. The presence of multiple overlapping generations
and prolonged crop susceptibility to damage necessitates protec-
tion throughout the growing season (Hallett et al. 2009; Stratton
et al. 2018). Further, larvae are protected from foliar insecticides
within the meristem (Wu et al. 2006). Compounding these chal-
lenges is an extremely low damage threshold for vegetables. For
example, Stratton et al. (2018) found that a single larva can
render a cauliflower plant unmarketable. While some growers
use calendar sprays of conventional insecticides to manage
*Elisabeth A. Hodgdon
elisabeth.hodgdon@gmail.com
1
Department of Plant and Soil Science, University of Vermont, 63
Carrigan Dr., Burlington, VT 05405, USA
2
School of Environmental Sciences, University of Guelph, 50 Stone
Rd. East, Guelph, Ontario N1G 2W1, Canada
3
Rubenstein School of Environment and Natural Resources, 81
Carrigan Dr., Burlington, VT 05405, USA
4
United States Department of Agriculture Forest Service, Northern
Research Station, 707 Spear St., South Burlington, VT 05403, USA
Journal of Chemical Ecology (2019) 45:549558
https://doi.org/10.1007/s10886-019-01078-0
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
... mixture of (2S,9S)-diacetoxyundecane, (2S,10S)-diacetoxyundecane, and (S)-2-acetoxyundecane, 43,44 successfully disrupted male behavior and reduced midge damage to Brassica vegetable crops in European and North American studies. 43,45 Mating disruption may not be economically feasible at a commercial scale, however, due to the structural complexity (chirality) and high cost of swede midge pheromone synthesis. 43,44 To reduce the costs of pheromone inputs in a swede midge mating disruption system, racemic blends containing non-natural stereoisomers, as well as single-component pheromones, present opportunities for cost reduction by simplifying the chemical synthesis required (C. ...
... Although complete racemic blends and single components are unattractive to male swede midges, 46,47 they can disorient males and prevent mating. 45,47 Therefore, understanding how females respond to blends deviating from their natural three-component mixture may help inform pheromone blend selection in future mating disruption systems. ...
... italica)at the University of Guelph Elora Research Station in Ariss, Ontario, Canada. As part of a separate study, 45 Each plot contained 80 mating disruption dispensers, spaced in a 2 × 2 m grid pattern hanging from wire stakes 25 cm from the ground. We used reservoir-type semipermeable polyethylene bag dispensers (ChemTica Internacional S.A., Heredia, Costa Rica). ...
Article
Full-text available
BACKGROUND Pheromone‐mediated mating disruption, which uses large amounts of synthetic female pheromones to interrupt insect reproductive behavior, has been successful for managing important agricultural pests. While multiple mechanisms have been discovered explaining how synthetic pheromone treatments prevent males from finding females, it is less clear how unnaturally large doses of synthetic sex pheromone impact the behavior of female insects, particularly nonlepidopteran females. In some species, ‘autodetecting’ females possess pheromone receptors and respond to ambient pheromones by altering their mating behavior. Here, we test whether exposure to stereospecific and racemic synthetic pheromones influences calling and subsequent propensity to mate in female swede midge (Contarinia nasturtii Kieffer; Diptera: Cecidomyiidae), a pest of Brassica crops. RESULTS In both laboratory and field settings, females exposed to stereospecific and racemic three‐component pheromone blends called significantly more frequently and for longer durations than midges in control treatments. In the field, midges were twice as likely to call in pheromone‐treated plots versus nontreated plots. Additionally, pheromone pre‐exposure reduced subsequent mating: while 68% of female midges mated following control conditions, only 42% and 35% of females pre‐exposed to stereospecific and racemic three‐component blends mated, respectively. CONCLUSION While more frequent calling within pheromone‐treated backgrounds may increase the likelihood that females are detected by males, a reduction in female propensity to mate would increase the efficacy of a pheromone‐mediated mating disruption system. Our work presents the first known investigation of autodetection behavior in Cecidomyiidae. Additional research is necessary to understand the implications of female autodetection for swede midge management.
... Racemic pheromone compounds, or mixtures of all possible stereoisomers of the pheromone compounds, are typically less costly to produce and may present a more economical mating disruption system for swede midge. Although unnatural stereoisomers of the "main" (most abundant) swede midge pheromone component in the blend, (2S,10S)-diacetoxyundecane, inhibit male attraction (Boddum et al. 2009;Hodgdon et al. 2019a), they may still be useful for mating disruption. Unattractive compounds may camouflage calling females, adulterate attractive pheromone plumes, desensitise males, and otherwise prevent males from locating females (Miller et al. 2006;Miller and Gut 2015). ...
... Unattractive compounds may camouflage calling females, adulterate attractive pheromone plumes, desensitise males, and otherwise prevent males from locating females (Miller et al. 2006;Miller and Gut 2015). We previously found that racemic pheromone blends prevented male midges from mating with calling females in a mating disruption simulation trial in the laboratory (Hodgdon et al. 2019a). ...
Article
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Swede midge, Contarinia nasturtii (Kieffer) (Diptera: Cecidomyiidae), causes severe economic losses in Brassica Linnaeus (Brassicaceae) crops in its invasive range in North America. Larvae feed within the meristem of their host plants, causing deformed heads, stems, and leaves. Pheromone-mediated mating disruption is particularly promising for swede midge management in high-value vegetable crops because its use is allowed in organic production. However, a major challenge to developing economically viable mating disruption is that the stereospecific three-component swede midge pheromone is costly to synthesise. In broccoli ( Brassica oleracea Linnaeus var. italica ) field plots, we tested whether stereospecific, lower-cost racemic, and single-component pheromone blends resulted in trap shutdown and reduced crop damage compared to nontreated controls. We found a significant reduction in males caught in three-component stereospecific and racemic pheromone–treated plots but not in the single-component treatments. Although marketable broccoli yields were not higher overall in the pheromone-treated plots compared with those in the controls, yields were significantly higher in the three-component stereospecific treatment in year 2. Therefore, the three-component stereospecific blend shows promise as a pheromone blend for swede midge mating disruption. However, due to high cost and levels of crop damage across all treatments, additional research is necessary to optimise swede midge mating disruption.
... There are currently no swede midge-resistant crop varieties, although variation in swede midge crop preference has been observed on farms (Hoepting and Vande Brake 2020). Growers expressed an interest in mating disruption, a strategy currently in the research and development phase that may become commercially viable in the future (Hodgdon 2019). Growers ranked intercropping, trap cropping, and ground barriers the lowest. ...
Article
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Since its introduction to North America in the 1990s, the invasive swede midge ( Contarinia nasturtii ) has become an important pest of cruciferous (Brassicaceae) vegetables in the northeast and Great Lakes regions of the United States and the Canadian provinces of Québec and Ontario. Swede midge reduces yield in cruciferous vegetables through larval feeding that distorts growth. Overlapping generations, cryptic larval feeding, and lack of effective biopesticides pose challenges for managing swede midge effectively using current tools. In 2018, we distributed an online survey for commercial vegetable growers in the United States and Canada to measure farm-level economic impacts of swede midge and grower perspectives on new management strategies for this pest. Growers reported losing $3808 US ($4890 Canadian) on average per acre per year due to swede midge–related vegetable crop losses. Both organic and conventional growers expressed an interest in paying more for nonchemical swede midge management vs. insecticides and were interested in trying new management strategies, particularly biological control.
... The stereospecific sex pheromone (4a) at 0.5 mg per septum exhibited more effective attractiveness to OWBMs in comparison with the 0.5 mg racemic sex pheromone (4b). This result is consistent with the findings of Hodgdon et al. 36 Thus, the reported sex pheromones had distinct attractiveness on OWBMs. The pheromones synthesized via the modular synthesis were biologically active and can be used in the management and control of gall midges. ...
Article
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BACKGROUND Sudden outbreaks of the orange wheat blossom midge, Sitodiplosis mosellana (Géhin) cause huge wheat yield losses. Use of sex pheromones is more efficient than laborious egg counting to monitor these hidden‐concealed insects. Quick synthesis of the sex pheromones is therefore required to meet the sudden outbreak needs. RESULTS A synthetic approach of stereospecific and racemic S. mosellana pheromones was presented. This method afforded the stereospecific and racemic S. mosellana pheromones in three steps and high enantioselectivity (> 98% ee for (2S,7S)‐2,7‐nonanediyl dibutyrate) in less than 1 day with 74% and 73% overall yields, respectively, whereas most conventional methods require longer synthesis time with less than 40% yield. The synthesis routes could quickly and economically afford the pheromones, starting from synthon (S)‐but‐3‐yn‐2‐ol (1a) or but‐3‐yn‐2‐ol (1b), through the same three‐step processes of coupling, reduction, and esterification. The Y‐tube olfactometer results showed significant attractiveness of the synthetic stereospecific and racemic sex pheromones to S. mosellana males relative to the blank control (P < 0.001). Field trials also demonstrated significant attractiveness of the synthetic stereospecific and racemic sex pheromones relative to the blank control (P < 0.001). CONCLUSION This modular approach is conducive to the deployment of field traps and timely responses to S. mosellana outbreaks and can be a time‐saving and cost‐effective tool to manage S. mosellana. © 2022 Society of Chemical Industry.
... Therefore, turning off the dispensers during mid-day and night-time hours could reduce the pheromone consumption and associated costs in a mating disruption system. 23 The sex pheromone emitted from apple leaf midge females (Table S2, entry 6) was identified as (13R,8Z)-13-acetoxy-8-heptadecen-2-one. 24 Boundary traps baited with a rubber septum dispenser containing 2 mg (13R,8Z)-13-acetoxy-8-heptadecen-2one were very effective at preventing midges from moving into mass-trapped plots. ...
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In 1996, damage symptoms typical of the swede midge, Contarinia nasturtii (Keiffer), were observed on broccoli, Brassica oleracea L. var. italica (Brassicaceae), crops east of Toronto, Ontario. Early attempts to identify an associated insect larva were unsuccessful, and damage symptoms became mistakenly attributed to nutrient deficiencies (T Clarke, personal communication). Between 1996 and 1999, damaged plants were seen by growers regularly, and resulted in up to 85% loss of marketable yield (T Clarke, personal communication). In June 2000, we initiated investigations at two sites 12 km apart to determine the causal organism of this damage. Both sites were located at farms where cole crops are primarily -gown and from where the first damage reports originated.