Swede Midge Research Articles

Combining biological control approaches for managing insect crop pests in the field can generate interactive effects

Abstract With the loss of effective chemical controls of crop pests, a move towards biological controls is a way to future‐proof our agricultural system. Floral field margins have shown successes in reducing crop pests, though the effect may not be precise enough to control infestations in commercial crops. Entomopathogenic nematodes (EPNs) may provide a more species‐ and time‐specific control and combining these methods may have synergy. Three in‐field vegetation margins, divided into four plots each (two floral and two grass), were established in March 2022. Three strips of sprouting broccoli were planted parallel in April, May and June. Each strip had a split‐plot design, with eight replicates of four nematode treatments placed alongside each floral/grass plot: Steinernema carpocapsae, S. feltiae and Heterorhabditis bacteriophora and a nematode‐free control. Pest pressure was assessed using adult counts. Assessments of crop yield and crop damage associated specifically with the swede smidge (Contarinia nasturtii) were also made. It was found that utilising a combination of control measures was successful in controlling a wider range of pests, though the success of each control method was highly dependent on the time of crop plantings. Field margins had a significant influence on crop damage associated with the swede midge. The EPN H. bacteriophora was an effective control method for the cabbage stem flea beetle and the swede midge, as well as reducing crop damage and yield loss. Field margins and EPNs combined have an interactive effect on crop yield, highlighting the need for control methods to be tested in combination in future integrated pest management research to accurately understand their effects within an integrated system.

Exploring the contribution of the salivary gland and midgut to digestion in the swede midge (Contarinia nasturtii) through a genomics-guided approach.

The larvae of Contarinia nasturtii (Kieffer) (Diptera: Cecidomyiidae), the swede midge, targets the meristem of brassica crops where they induce the formation of galls and disrupt seed and vegetable production. Previously, we examined the salivary gland transcriptome of newly-hatched first instar larvae as they penetrated the host and initiated gall formation. Here we examine the salivary gland and midgut transcriptome of third instar larvae and provide evidence for cooperative nutrient acquisition beginning with secretion of enzymes and feeding facilitators followed by gastrointestinal digestion. Sucrose, presumably obtained from the phloem, appeared to be a major nutrient source as several α-glucosidases (sucrases, maltases) and β-fructofuranosidases (invertases) were identified. Genes encoding β-fructofuranosidases/invertases were among the most highly expressed in both tissues and represented two distinct gene families that may have originated via horizontal gene transfer from bacteria. The importance of the phloem as a nutrient source is underscored by the expression of genes encoding regucalcin and ARMET (arginine-rich mutated in early stages of tumor) which interfere with calcium signalling and prevent sieve tube occlusion. Lipids, proteins, and starch appear to serve as a secondary nutrient sources. Genes encoding enzymes involved in the detoxification of glucosinolates (myrosinases, arylsulfatases, and glutathione-S-transferases) were expressed indicative of Brassicaceae host specialization. The midgut expressed simple peritrophins and mucins typical of those found in Type II peritrophic matrices, the first such description for a gall midge.

Organic management of the invasive swede midge (Diptera: Cecidomyiidae) on Brassica vegetables: multiple dead ends necessitate novel approaches

Abstract The distinctive biology and ecology of the invasive swede midge, Contarinia nasturtii Kieffer (Diptera: Cecidomyiidae), render organic management in North America particularly challenging, necessitating the search for novel out-of-the box approaches to control it. Native to Eurasia, this pest was first confirmed in North America in 2000 and has since spread to several states and provinces in the United States and Canada. As a galling midge, swede midge feeding causes distorted growth in Brassica (Brassicales: Brassicaceae) vegetables, resulting in major losses of marketable produce. While conventional growers typically use systemic insecticides for plant protection early in the season, equivalent approaches for organic production do not exist. The lack of effective organic management approaches for swede midge has resulted in devastating losses for heading Brassica vegetables, which are the most sensitive to midge feeding. Here, we review over 2 decades of research focused on developing organic approaches to manage swede midge. To encourage more rapid progress on swede midge management, we believe that it is important to review the widest array of work, including recent publications as well as our unpublished research. We conclude by highlighting the most promising strategies that should be utilized on farms and explored further for organic management of swede midge in vegetable crops.

Pheromone trap monitoring reveals the continued absence of swede midge in the Northern Great Plains

Abstract The swede midge, Contarinia nasturtii (Kieffer) (Diptera: Cecidomyiidae), is invasive to North America, where it was first reported in Ontario, Canada. It is now established in eastern Canada and from eastern Minnesota in the Midwest to the northeastern seaboard of the United States of America. Swede midge is a serious pest of brassicaceous plants, including vegetable and oilseed crops. To ensure its early detection in the Northern Great Plains, a monitoring programme was established using pheromone traps located primarily along the edges of canola fields from North Dakota, United States of America, northwest to the Peace River region, in Alberta and British Columbia, Canada. In North Dakota, 117 trap sites were monitored between 2015 and 2021. In western Canada, monitoring occurred on a small scale from 2006 to 2011, and 521 trap sites were monitored from 2013 to 2021. Swede midge was not detected in canola grown in the Northern Great Plains between 2006 and 2021. Partners in North Dakota and western Canada intend to maintain the monitoring programme to support early detection of swede midge if it does continue to disperse northwestwards. The monitoring programme contributes to outreach activities and fosters farmer and agronomist participation in pest management (i.e., community science) in the Northern Great Plains.

Characterization of the swede midge, Contarinia nasturtii, first instar larval salivary gland transcriptome

Proteins in saliva of gall-forming insect larvae govern insect-host plant interactions. Contarinia nasturtii, the swede midge, is a pest of brassicaceous vegetables (cabbage, cauliflower, broccoli) and canola. We examined the salivary gland (SG) transcriptome of first instar larvae reared on Brassica napus and catalogued genes encoding secreted proteins that may contribute to the initial stages of larval establishment, the synthesis of plant growth hormones, extra-oral digestion and evasion of host defenses. A significant portion of the secreted proteins with unknown functions were unique to C. nasturtii and were often members of larger gene families organized in genomic clusters with conservation patterns suggesting that they are undergoing selection.

Farm-level Losses and Grower Willingness to Try Management Strategies for Swede Midge in Vegetable Crops

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.

A chromosome-level genome assembly of the orange wheat blossom midge, Sitodiplosis mosellana Géhin (Diptera: Cecidomyiidae) provides insights into the evolution of a detoxification system.

The orange wheat blossom midge Sitodiplosis mosellana Géhin (Diptera: Cecidomyiidae), an economically important pest, has caused serious yield losses in most wheat-growing areas worldwide in the past half-century. A high-quality chromosome-level genome for S. mosellana was assembled using PacBio long read, Illumina short read, and Hi-C sequencing technologies. The final genome assembly was 180.69 Mb, with contig and scaffold N50 sizes of 998.71 kb and 44.56 Mb, respectively. Hi-C scaffolding reliably anchored 4 pseudochromosomes, accounting for 99.67% of the assembled genome. In total, 12,269 protein-coding genes were predicted, of which 91% were functionally annotated. Phylogenetic analysis indicated that S. mosellana and its close relative, the swede midge Contarinia nasturtii, diverged about 32.7 MYA. The S. mosellana genome showed high chromosomal synteny with the genome of Drosophila melanogaster and Anopheles gambiae. The key gene families involved in the detoxification of plant secondary chemistry were analyzed. The high-quality S. mosellana genome data will provide an invaluable resource for research in a broad range of areas, including the biology, ecology, genetics, and evolution of midges, as well as insect–plant interactions and coevolution.

A newly invasive species may promote dissimilarity of pest populations between organic and conventional farming systems

Insect taxa vary in their phenology across space creating dissimilar patterns of species abundance over time. The role of human disturbances and invasive species in these patterns of temporal dissimilarity (phenological differences) across space, however, remain largely unexplored. To dissect these patterns, we evaluated four common pests and one newly invasive species (Contarinia nasturtii; Swede midge) at 220 time points across 2 years on organic and conventional farms. We first summarized across time and evaluated differences in pest abundance between farm management (organic and conventional). We then used generalized additive models to describe temporal patterns of abundance, disentangling phenological differences across management systems. Last, we conducted a temporal beta diversity analysis to identify which species and management practices contribute most to dissimilarity. We found that aggregating pest abundance across time and species masked differences in pest phenology across management systems and concealed variation in pest abundance that was strongly driven by an invasive species, respectively. Overall, our results suggest that organic and conventional farms may be only superficially similar in pest abundance. Rather, by accounting for time, we demonstrate a more nuanced understanding of pest communities moving beyond abundance that may be particularly important for management of newly invasive species.

Field tests of candidate pheromone blends show promise for mating disruption of the invasive swede midge (Diptera: Cecidomyiidae)

Abstract 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.

Horizontal Transfer of Microbial Toxin Genes to Gall Midge Genomes.

A growing body of evidence has underscored the role of horizontal gene transfer (HGT) in animal evolution. Previously, we discovered the horizontal transfer of the gene encoding the eukaryotic genotoxin cytolethal distending toxin B (cdtB) from the pea aphid Acyrthosiphon pisum secondary endosymbiont (APSE) phages to drosophilid and aphid nuclear genomes. Here, we report cdtB in the nuclear genome of the gall-forming “swede midge” Contarinia nasturtii (Diptera: Cecidomyiidae) via HGT. We searched all available gall midge genome sequences for evidence of APSE-to-insect HGT events and found five toxin genes (aip56, cdtB, lysozyme, rhs, and sltxB) transferred horizontally to cecidomyiid nuclear genomes. Surprisingly, phylogenetic analyses of HGT candidates indicated APSE phages were often not the ancestral donor lineage of the toxin gene to cecidomyiids. We used a phylogenetic signal statistic to test a transfer-by-proximity hypothesis for animal HGT, which suggested that microbe-to-insect HGT was more likely between taxa that share environments than those from different environments. Many of the toxins we found in midge genomes target eukaryotic cells, and catalytic residues important for toxin function are conserved in insect copies. This class of horizontally transferred, eukaryotic cell-targeting genes is potentially important in insect adaptation.

De Novo Whole-Genome Assembly of the Swede Midge (Contarinia nasturtii), a Specialist of Brassicaceae, Using Linked-Read Sequencing.

The swede midge, Contarinia nasturtii, is a cecidomyiid fly that feeds specifically on plants within the Brassicaceae. Plants in this family employ a glucosinolate-myrosinase defense system, which can be highly toxic to nonspecialist feeders. Feeding by C. nasturtii larvae induces gall formation, which can cause substantial yield losses thus making it a significant agricultural pest. A lack of genomic resources, in particular a reference genome, has limited deciphering the mechanisms underlying glucosinolate tolerance in C. nasturtii, which is of particular importance for managing this species. Here, we present an annotated, scaffolded reference genome of C. nasturtii using linked-read sequencing from a single individual and explore systems involved in glucosinolate detoxification. The C. nasturtii genome is similar in size and annotation completeness to that of the Hessian fly, Mayetiola destructor, but has greater contiguity. Several genes encoding enzymes involved in glucosinolate detoxification in other insect pests, including myrosinases, sulfatases, and glutathione S-transferases, were found, suggesting that C. nasturtii has developed similar strategies for feeding on Brassicaceae. The C. nasturtii genome will, therefore, be integral to continued research on plant-insect interactions in this system and contribute to effective pest management strategies.

Compensatory Abilities of Canola in Response to Swede Midge (Diptera: Cecidomyiidae) Damage.

Swede midge (Contarinia nasturtii Kieffer) is an invasive, economic pest of canola (Brassica napus L.) that threatens production throughout Canada. Swede midge has up to four overlapping generations, placing canola at risk of multiple infestations in the field. The relationship between single and multiple swede midge infestations at different canola stages, and the resulting impacts on yield, are unknown. Laboratory experiments were conducted to evaluate the impact of single and multiple infestations of swede midge on four plant stages of canola: three-leaf, seven-leaf, primary bud, and secondary bud. Previously, the seven-leaf and primary bud stages were considered vulnerable to swede midge, but we determined that the secondary bud stage is also vulnerable. Evidence of compensation by canola in response to herbivory by swede midge was discovered. Compensation occurred mainly through increased production of tertiary racemes and pods and was maximized with exposure of 4.5-6.5 female midges per plant. Although compensation may increase potential yield, it also results in uneven crop maturation resulting in delayed harvest and yield loss. Consequently, to prevent delays in maturation and harvest, insecticides should be applied before these densities are reached.

Synthetic pheromone exposure increases calling and reduces subsequent mating in female Contarinia nasturtii (Diptera: Cecidomyiidae).

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. 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. 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.

Odors from phylogenetically-distant plants to Brassicaceae repel an herbivorous Brassica specialist

Specialist insect herbivores are constrained by highly specific odor recognition systems to accept suitable host plants. Given that odor recognition leads specialist insects to accept a limited range of plants, we hypothesized that phylogenetically distant plants produce odors that are physicochemically different from host odors and would be less attractive or even repellent to a specialist herbivore. We tested this hypothesis by examining behavioral and ovipositional responses of swede midge (Contarinia nasturtii, Diptera: Cecidomyiidae), a specialist of brassicas, to broccoli sprayed with non-host essential oils. Specifically, we asked: (1) How do essential oils from different plant species influence host-seeking and oviposition behaviors of swede midge? (2) Do odors from non-host plants that are not phylogenetically related or physicochemically similar to host plants affect host-seeking or ovipositional behavior of swede midge? In oviposition assays, we found that non-host odors varied in their ability to modify female midge behavior and that phylogenetic relatedness was negatively correlated with larval density. In y-tube assays, we found that female midges most frequently avoided non-host odors that were more similar to brassica odors. Females were less likely to oviposit on or choose any treated host plants, but particularly avoided garlic, spearmint, thyme, eucalyptus lemon, and cinnamon bark treatments. Overall, we found that plant phylogenetic relatedness and odor similarity are related to repellency. Therefore, altering the diversity of plant odors by explicitly accounting for plant phylogenetic distance and odor similarity, relative to host plants, may be an important, underexploited tactic for sustainably managing challenging pests.

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

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.

Diel patterns of emergence and reproductive behaviour in the invasive swede midge (Diptera: Cecidomyiidae)

AbstractSwede midge (Contarinia nasturtii (Kieffer); Diptera: Cecidomyiidae) is a serious invasive pest of Brassica Linnaeus (Brassicaceae) oilseed and vegetable crops in Canada and the United States of America. Pheromone mating disruption is a promising new tactic for managing this difficult pest, but research is needed to determine how pheromone delivery can be optimised. With an understanding of swede midge diel mating patterns, pest managers could limit pheromone release to periods when midges are sexually active. We conducted a series of 24-hour trials to test whether swede midge exhibit diel periodicity of emergence, female calling, and male capture in pheromone traps. We found that females began releasing pheromones almost immediately following emergence within the first five hours after dawn. In the field, we found that males were most active from dawn until late morning, indicating that midges mate primarily during the first five hours of photophase. Low levels of reproductive activity during midday and nighttime hours present opportunities to turn off dispensers and reduce the cost of pheromone inputs in a swede midge mating disruption system.

Swede midge (Diptera: Cecidomyiidae) diapause initiation under stable conditions: not a family affair

AbstractLarvae of the swede midge,Contarinia nasturtii(Kieffer) (Diptera: Cecidomyiidae), rely on environmental cues to initiate the diapause programme. This facultative diapause strategy, which provides opportunities for both bet hedging and multivoltinism, likely contributed to the successful colonisation and spread of this invasive pest in North America. Population diapause incidence is variable even under relatively stable conditions (especially at the critical day length), yet the mechanisms influencing the developmental trajectory of individuals under such conditions are unknown. Here we approach the non-environmental (i.e., heritable) controls of this variation by comparing diapause frequencies within and among full-sibling swede midge families reared in one of two stable environments. Under warm, long-day conditions > 99% of swede midges pupated directly, while 86% of swede midges entered diapause under cool, short-day conditions. In the latter condition, most families exhibited mixed developmental trajectories (ranging from 36% to 96% diapause). This developmental variation among siblings indicates that the diapause induction threshold does not follow simple Mendelian inheritance with complete dominance for a particular allele, but may follow incomplete dominance or a more complex heredity. Alternatively, within-family diapause variation may result from maternal bet hedging or factors such as maternal age or larval nutrition.

Determining Temperature-Dependent Development and Mortality Parameters of the Swede Midge (Diptera: Cecidomyiidae).

The swede midge (Contarinia nasturtii Kieffer) is an invasive insect in North America whose feeding has caused a decline of over 60% of total canola acreage in Ontario, Canada since 2011. Temperature-dependent development and mortality information are important to develop an effective pest management strategy for this insect; as the most comprehensive study on C. nasturtii development was completed on populations from the United Kingdom in the 1960s, new geographically relevant information is needed. Contarinia nasturtii eggs, larvae, pupae, and adults were reared from wild populations collected from Elora, Ontario, and allowed to develop at different temperatures. Resulting development rates were fit to a series of growth models and the model with the best relative goodness-of-fit was selected to represent the given life stage. Eggs from Ontario populations developed more quickly than their UK counterparts at temperatures below approximately 17°C, but more slowly at temperatures above 17°C. The same phenomenon was observed in larvae at 20°C. Pupae from both populations had similar development rates, and adult longevity was similar as well. This information will inform the management of C. nasturtii, and may help prevent its spread to other canola-producing regions of North America.

A new species of Contarinia Rondani (Diptera: Cecidomyiidae) that induces flower galls on canola (Brassicaceae) in the Canadian prairies

AbstractA new species, Contarinia brassicola Sinclair (Diptera: Cecidomyiidae), which induces flower galls on canola (Brassica napus Linnaeus and Brassica rapa Linnaeus (Brassicaceae)), is described from Saskatchewan and Alberta, Canada. Larvae develop in the flowers of canola, which causes swelling and prevents opening, pod formation, and seed set. Mature larvae exit the galls, fall to the soil, and form cocoons. Depending on conditions, larvae will either pupate and eclose in the same calendar year or enter facultative diapause and emerge the following year. At least two generations of C. brassicola occur each year. Adults emerge from overwintering cocoons in the spring and lay eggs on developing canola flower buds. The galls produced by C. brassicola were previously attributed to the swede midge, Contarinia nasturtii (Kieffer) in Saskatchewan; here, we compare and list several characters to differentiate the two species.

A Single Swede Midge (Diptera: Cecidomyiidae) Larva Can Render Cauliflower Unmarketable.

Swede midge, Contarinia nasturtii Kieffer (Diptera: Cecidomyiidae), is an invasive pest causing significant damage on Brassica crops in the Northeastern United States and Eastern Canada. Heading brassicas, like cauliflower, appear to be particularly susceptible. Swede midge is difficult to control because larvae feed concealed inside meristematic tissues of the plant. In order to develop damage and marketability thresholds necessary for integrated pest management, it is important to determine how many larvae render plants unmarketable and whether the timing of infestation affects the severity of damage. We manipulated larval density (0, 1, 3, 5, 10, or 20) per plant and the timing of infestation (30, 55, and 80 d after seeding) on cauliflower in the lab and field to answer the following questions: 1) What is the swede midge damage threshold? 2) How many swede midge larvae can render cauliflower crowns unmarketable? and 3) Does the age of cauliflower at infestation influence the severity of damage and marketability? We found that even a single larva can cause mild twisting and scarring in the crown rendering cauliflower unmarketable 52% of the time, with more larvae causing more severe damage and additional losses, regardless of cauliflower age at infestation.