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

Abstract

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.

Full text

1
© The Author(s) 2018. Published by Oxford University Press on behalf of Entomological Society of America.
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 journals.permissions@oup.com
A Single Swede Midge (Diptera: Cecidomyiidae) Larva
Can Render Cauliflower Unmarketable
Chase A.Stratton,1 Elisabeth A.Hodgdon,1 Samuel G.Zuckerman,2
Anthony M.Shelton,3 and Yolanda H.Chen1,4
1Department of Plant and Soil Sciences, University of Vermont, 63 Carrigan Drive, Burlington, VT 05405, 2Rubenstein School of
Environment and Natural Resources, University of Vermont, 81 Carrigan Drive, Burlington, VT 05405, 3Department of Entomology,
Cornell University, New York State Agricultural Experiment Station, 630 West North Street, Geneva, NY 14456, and 4Corresponding
author, e-mail: yolanda.chen@uvm.edu
Subject Editor: Kris Godfrey
Received 23 February 2018; Editorial decision 24 May 2018
Abstract
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.
Key words: damage threshold, marketability threshold, invasive pest, Brassica production, Cecidomyiidae
Swede midge (Diptera: Cecidomyiidae) is an invasive pest threatening
Brassica production in the Northeastern United States and Eastern
Canada (Hallett and Heal 2001; Olfert etal. 2006; Chen etal. 2011).
Feeding by swede midge larvae results in a range of damage, from
slight swelling of plant tissue to scarring, twisting, branching, and
most severely, the complete loss of the apical bud (Chen and Shelton
2007; Chen etal. 2009). Once established in an area, swede midge is
extremely difcult to remove (Chen etal. 2011). Adecade after the
midge invaded Ontario, Canada, losses to broccoli and cauliower
(Brassica oleracea Gp. Botrytis and Gp. Italica, respectively) can exceed
85% annually (Hallett and Heal 2001). Swede midge outbreaks have
reversed previous integrated pest management (IPM) gains in cole
crops because growers often resort to calendar-based spraying (Hallett
and Sears 2013). There is a critical need for better insecticide treat-
ment thresholds (Hallett and Sears 2013) and alternative management
tactics for swede midge (Chen and Shelton 2007; Chen et al. 2009),
both of which depend on a comprehensive understanding of pest biol-
ogy and susceptibility to treatments (Kogan 1998).
Cecidomyiids are challenging insect pests because of their
ability to manipulate plant growth, resulting in galls and tumor-
ous formations (Maia etal. 2005; Vitou etal. 2008; Vijaykumar
etal. 2009; Hall etal. 2012; Stuart etal. 2012; Uechi etal. 2017).
Specifically, swede midge is difficult to control due to: 1) the
short adult life span and concealed feeding of larvae (Readshaw
1966; Hallett etal. 2009a, Chen et al. 2011); 2)multiple over-
lapping generations with irregular emergence phenotypes that
are difficult to predict (Hallett etal. 2009b); and 3)all devel-
opmental stages of susceptible Brassica hosts seem impacted by
herbivory (Hallett 2007).
Although swede midge clearly manipulates plant growth, no stud-
ies have examined the relationship between timing of larval feeding
and the emergence of market-relevant damage symptoms in Brassica
vegetables. Visible damage within an infested cauliower eld could
be due to separate infestations from different calendar days. It is
unclear whether the ultimate loss of a marketable plant is due to the
nal infestation, or a compounded effect from multiple infestations.
Effective IPM programs depend on accurate damage (the level of infes-
tation that can cause damage; Walker 1983; Hallett and Sears 2013)
and marketability thresholds (the level of infestation that renders a
plant unmarketable; Hallett and Sears 2013). Unfortunately, typi-
cal scout and spray IPM practices are impractical for swede midge
because market-relevant damage is difcult to conrm until after
Journal of Insect Science, (2018) 18(3): 24; 1–6
doi: 10.1093/jisesa/iey062
Research
Downloaded from https://academic.oup.com/jinsectscience/article-abstract/18/3/24/5040085
by Guy W Bailey Howe Library user
on 29 June 2018

larvae have left the plant (Wu etal. 2006; Chen etal. 2011). Testing
the relationship between feeding and damage relative to crop phe-
nology could allow more precision in the timing of pesticide applica-
tions rather than calendar-based sprays (Hallett etal. 2009a, Hallett
and Sears 2013).
Current conventional management recommendations for swede
midge are to use systemic neonicotinoids at transplant, followed by reg-
ular sprays of foliar insecticides for the remainder of the growing season
(Chen etal. 2011; Hodgdon etal. 2017), disrupting decades of effective
IPM in Brassica systems (Rodriguez Salamanca 2014). An alternative
approach is to use an action threshold based on the capture of ve males
per pheromone trap per day with a minimum 7-d pesticide retreat-
ment interval (Hallett and Sears 2013). This strategy reduces damage
to acceptable levels in cabbage, but not cauliower, possibly because
cabbage heartleaves protect the developing meristem from feeding lar-
vae (Andaloro etal. 1983). Also, organic growers are limited to using
large-scale crop rotations (Chen etal. 2009) and/or covering crops with
specialty insect netting (Hodgdon etal. 2017), both expensive strategies.
Swede midge damage differs across and within groups of B.
oleracea vegetables (e.g., cabbages, cauliower, broccoli, etc.) (Chen
etal. 2011). Infestations result in the lack, reduced size, or distorted
growth of the marketable portion of cauliower composed usually
of white inorescence meristem. Here, we studied the relationship
between swede midge infestation and plant damage on cauliower
to test how the timing and severity of swede midge infestation inu-
ences market-relevant damage. We applied rst-instar larvae to cauli-
ower to ask: 1)How many swede midge larvae does it take to cause
visible damage to cauliower? 2) How many larvae render cauli-
ower crowns unmarketable? and 3) Does the age of cauliower
at infestation inuence the likelihood that it will be unmarketable?
Materials and Methods
Plant Production and Colony Rearing
A laboratory-reared colony of swede midge was used for both lab-
oratory and eld trials (origin: Swiss Federal Research Station for
Horticulture, Wädenswill, Switzerland). Midges were reared on
cauliower plants, Brassica oleracea group Botrytis ‘Snow Crown’
(Harris Seeds, Rochester, NY), due to midge preference (Hallett
2007) and large bud size. Seeds were planted in 128-cell trays
lled with Fafard 3B soilless potting media (Sun Gro Horticulture,
Agawam, MA). Seedlings were transplanted into 10cm pots after
4 wk and returned to the greenhouse. Plants were grown in the
University of Vermont greenhouse under a 16:8 (L:D) h photoperiod
at ~22°C and ~30% RH until six to eight true leaves had developed.
Each day, four cauliower plants were placed into one of two ovi-
position cages (0.6 m3 wooden frame, covered in 400μm nylon mesh)
in the lab. Plants were exposed to adults for 1 d, after which they were
moved to another cage, where eggs hatched and larval development
continued. Eggs hatch ca. 1 d after oviposition in the inner folds of
meristematic tissue, and larvae feed for ~14 d until they are ready to
pupate. Fourth-instar larvae either eject from the plant or crawl down
the stem to pupate in the top 3 cm of surrounding soil. Therefore,
infested cauliower meristems were cut 3cm below the crown and
inserted back into the planting pots after ~14 d of larval development.
Pots with pupating larvae were placed back in the ovipositional cages,
where adults emerged and mated ~14 d later (Chen etal. 2011).
Artificial Infestation Procedure
Standard quantities of larvae were applied to plant buds to deter-
mine the relationship between larval density and damage intensity.
Swede midge larvae are difcult to work with because of their small
size (<2mm), feeding location within the bud, and transparent color.
Eggs are nearly invisible, so rst instars were used for trials. Most
larvae have entered the rst instar about 3 d after oviposition based
upon Readshaw (1966) and our observations. Larvae were collected
from four plants exposed to gravid females for 24h then grown for
72h in the greenhouse. All larvae and eggs were separated from the
plant by dissecting the apical bud and rinsing the fragments with
deionized water in a petridish.
First instars were aspirated and gently applied in the tightly
folded leaves developing off the primary meristem using a 200-μl
micropipette. The same quantity of deionized water was applied to
control plants as a check for any damage caused by the procedure.
Artificial Infestation Procedure—Method Validation
To validate that larvae remained intact after applications to
treated plants, additional trials testing larval survival were per-
formed. Larvae (0, 1, 3, 5, 10, or 20)were applied to plants with
8–10 true leaves, using 20 replicate plants for each larval density.
Infested plants were grown in mesh cages (1 m × 0.7 m × 0.7 m,
BioQuip, Rancho Domingez, CA) for 10 d under rearing condi-
tions (described above). After 10 d of development, young leaves
were removed using a scalpel and larvae were gently rinsed from
the leaves using deionized water. Adissecting microscope was used
to count the number of larvae that physically responded to a gen-
tle touch with a probe. Summary statistics from these trials were
used to estimate the proportion of larvae that survived the arti-
cial infestations. We found that half the larvae survive the pro-
cedure, with 0.4±0.11, 1.5± 0.25, 2.25±0.34, 5.7 ±0.63, and
10.4 ± 0.77 (mean ± SE) moving larvae for 1, 3, 5, 10, and 20
larvae, respectively.
What Is the Damage/Marketability Threshold for
SwedeMidge?
To test the relationship between larval density and damage severity,
0, 1, 3, 5, 10, or 20 larvae were applied to uninfested cauliower
with 8–10 true leaves, replicated over 25 plants for each treatment
density. The cauliower plants tested were grown for 8wk using
the conditions described above, with the exception that they were
transplanted into 15 cm circular planting pots, rather than 7 cm
pots. Following the articial larval infestation, treated plants were
returned to the greenhouse in large pop-up cages and grown for ~21
d.To prevent larvae from completing their life cycle and reinfesting
treated plants prior to data collections, circular, at, acetate sheets
were fastened around plant stems with cotton lling the extra space
between the sheets and the stem. This design successfully restricted
larvae from reaching the soil where they pupate.
Cauliowers were evaluated using a scale adapted from Hallett
(2007), described in Table1. Cauliower plants with a score ≥1 were
unmarketable using this scale (C.A.S., personal observations). To
determine how many swede midge larvae cause damage to cauliower
(damage threshold), the frequencies of plant damage ratings across
larval treatment densities were tested using a log-linear regression. The
relationship between larval density and marketability (marketability
threshold) was tested using a binary-logistic regression. Using the
models tted from our data, the lowest numbers of larvae that cause
damage and render cauliower unmarketable were estimated.
Does the Age of Cauliflower at Infestation Influence
the Likelihood That It Will Be Marketable?
We tested if plant age and the number of larvae inuenced mar-
ket-relevant plant damage using a potted plant experiment from
2 Journal of Insect Science, 2018, Vol. 18, No. 3
Downloaded from https://academic.oup.com/jinsectscience/article-abstract/18/3/24/5040085
by Guy W Bailey Howe Library user
on 29 June 2018

July 1, 2015 to August 30, 2015 at the Bio-Research Complex at
the University of Vermont. We chose the site because it was at least
5 km away from any commercial Brassica plantings, minimizing
background midge populations that could inuence the study. The
study site was situated between outdoor hoop-house structures.
Due to the low background population of midges in this area, our
study design allowed all plants, regardless of infestation date, to
be grown outside for the entire experimental period. In order to
minimize disturbance to the study and control weeds, we covered
the study area (3×15 m) with black landscape fabric. We raised
cauliower in 15cm circular planting pots between Jackson traps
with a swede midge pheromone lure (Solida Distributions, Saint-
Ferréol-les-Neiges, Québec) to verify that midges remained absent
from theeld.
To test whether plant age has an effect on plant damage and the
likelihood of marketability, 0, 1, 5, 10, or 20 larvae were applied to
plants of three age groups (30 [2 true leaves], 55 [4–6 true leaves],
and 80 [6–8 true leaves] d after seeding [DAS]), replicated across
30 cauliower plants in a randomized complete block design. After
hardening off 4 wk old seedlings for 2 d, we placed randomly
assigned plants to the different treatments at the start of the study,
so each plant remained in the same location for the entire experi-
ment. Each block consisted of two trays (0.3×0.5 m) that hold
six pots each in a 2× 3 grid. We placed six plants randomized by
treatment date and larval density in a zig-zag pattern in the trays. We
were concerned that the circular acetate sheets may constrict cauli-
ower stems through the course of this trial, so instead we loosely
fastened ne mesh around the base of the stem to restrict larvae from
reaching thesoil.
We inoculated midge larvae on the treatment plants at 30, 55,
and 80 DAS. On each inoculation date, we brought the subset of
pre-assigned plants into an onsite hoop-house. Under a dissecting
microscope, we infested cauliower using the same micropipette
method, but the outermost layer of the waxy cuticle was also gently
abraded using Kimwipes (Uline, Pleasant Prairie, WI), so the water
droplets could adhere to the small meristems of the youngest plants.
In order to control for any damage this may have caused, we also
abraded older plants.
After the larval inoculations, we assessed the treatment plants
for damage every 4 wk. Plants infested at 30 DAS were assessed
4, 8, and 12wk after transplanting (WAT), plants infested at 55
DAS were assessed at 8 and 12 WAT, and plants infested at 80 DAS
were evaluated 12 WAT. We were able to visually differentiate swede
midge damage from other herbivores including diamondback moth
(Plutella xylostella L.) (Lepidoptera: Plutellidae) and imported
cabbageworm (Pieris rapae L.) (Lepidoptera: Pieridae) that feed on
foliage rather than the developing meristem (see Table1 for swede
midge damage descriptions). We recorded plant marketability at the
end of these trials using standards developed from discussions with a
local vegetable grower (A.J., personal communication). Cauliowers
with scarring or twisting within the inner petioles of the crown were
unmarketable.
We used a log-linear and binary-logistic regression to test how
larval density, plant age, and their interaction inuenced damage and
marketability, respectively. We used the model output to predict the
larval density and plant age that had the highest impact on dam-
age and marketability. All statistics were performed using R version
Table1. Damage scale and associated symptoms used to assess
cauliflower artificially infested with 0, 1, 3, 5, 10, or 20 swede midge
larvae
Damage value Cauliower symptoms
0 No damage
1 Mild twisting to 1 leaf or orets
2 Mild twisting of stem, 2–3 leaves, or orets and/or mild
swelling of petioles
3 Severe twisting of 2–3 leaves or orets and/or
severe swelling of petioles
4 Severe twisting and/or crumpling of stem,
3+ leaves, or orets; severe swelling and/or
scarring of petioles and/or orets
5 Severe twisting of stem, leaves, and orets; severe
scarring of stem, leaves, petioles, and orets
6 Death of apical meristem and/or multiple
compensatory shoots
Fig.1. (a) Counts for cauliflower damage scores of different larval densities applied to plants in the laboratory. Twenty plants per treatment were assessed for
damage at 10 d postlarval infestation using a modified scale from Hallett (2007) (described in Table1). Larval density was positively correlated with plant damage
(z=4.16; P<0.001). (b) Binomial logistic regression testing the effect of larval density on the likelihood that infested cauliflower will be marketable. Histograms
indicating the number (n) of marketable (P=1) and unmarketable (P=0) cauliflower are also reported for each treatment density. Larval density was negatively
correlated with marketability (z=−3.40; P<0.001).
Journal of Insect Science, 2018, Vol. 18, No. 3 3
Downloaded from https://academic.oup.com/jinsectscience/article-abstract/18/3/24/5040085
by Guy W Bailey Howe Library user
on 29 June 2018

Fig.2. (a) Counts for cauliflower damage scores of different larval densities applied to plants at 30 DAS. Thirty plants per treatment were assessed for damage at
4, 8, and 12wk postlarval infestation using a categorical damage scale described in Table1. Damage at 12wk is shown. Larval density was positively correlated
with plant damage (z=3.418; P<0.001). (b) Binomial logistic regression testing the effect of larval density on the likelihood that cauliflower infested 30 DAS
will be marketable. Histograms indicating the number of marketable (P=1) and unmarketable (P=0) cauliflower are reported for each treatment density. Larval
density was negatively correlated with marketability (z=−3.364; P<0.001). (c) Counts for cauliflower damage scores of different larval densities applied to plants
at 55 DAS. Thirty plants per larval density were assessed for damage at 4 and 8wk postlarval infestation. Damage at 8wk is shown. Larval density was positively
correlated with plant damage (z=5.455; P<0.001). (d) Binomial logistic regression testing the effect of larval density on the likelihood that cauliflower infested 55
DAS will be marketable. Histograms reporting marketable and unmarketable cauliflower are reported for each treatment density. Larval density was negatively
correlated with marketability (z=−5.032; P<0.001). (e) Counts for cauliflower damage scores of different larval densities applied to plants at 80 DAS. Thirty plants
per larval treatment were assessed for damage at 4wk postlarval infestation. Larval density was positively correlated with plant damage (z=5.907; P<0.001).
(f) Binomial logistic regression testing the effect of larval density on the likelihood that cauliflower infested 80 DAS will be marketable. Histograms indicating
the number of marketable (P=1) and unmark etable (P=0) cauliflower are reported for each treatment density. Larval density was negatively correlated with
marketability (z=−5.852; P<0.001).
4 Journal of Insect Science, 2018, Vol. 18, No. 3
Downloaded from https://academic.oup.com/jinsectscience/article-abstract/18/3/24/5040085
by Guy W Bailey Howe Library user
on 29 June 2018

3.2.2 (RStudio Team 2016). Bar plots were built using ggplot2 ver-
sion 2.2.1 (Wickham 2009) and negative binomial regressions were
plotted using popbio version 2.4.3 (Stubben and Milligan 2007).
Results
Plants treated with more larvae experienced more severe damage
(Fig.1a; log-linear regression, z= 4.158, P<0.001) and a reduced
likelihood that the plant would be marketable (Fig.1b; binary-logis-
tic regression, z=−3.400, P<0.001). We found that the single larva
treatment most often caused minor twisting to leaf stems and o-
rets, rendering cauliower unmarketable52% of the time. Ten lar-
vae resulted in a range of damage from mild twisting of leaves to
severe swelling and scarring of orets, rendering 68% of the plants
unmarketable. Damage from the 20 larvae treatment also varied, but
most often resulted in severe swelling and scarring in the developing
crown, rendering 82% of the plants unmarketable.
The same trend held in the eld potted plant trials, with more
larvae causing more cauliower damage (Fig.2a, c, and e; log-linear
regression, z=3.689, P< 0.001) and a lower likelihood of mar-
ketability (Fig.2b, d, and f; binary-logistic regression, z= −2.894,
P<0.001). Larval density and plant age at infestation did not have
a signicant interaction for damage (z=−0.540, NS) or marketa-
bility (z = −0.213, NS), meaning that similar patterns of damage
and marketable losses were present across larval treatments for the
different cauliower age groups. Cauliower age alone also did not
directly inuence damage or marketability (z= 1.464, −0.572; NS,
NS). Altogether, our data suggest that midge larvae cause signicant
damage and marketable losses regardless of cauliowerage.
Discussion
Our results contribute important ndings about swede midge:
1) half of the larvae perish following our inoculation procedure
(see Materials and Methods); 2)any quantity of larval feeding can
cause noticeable damage on cauliower (Fig.1a); 3) a single larva
can render cauliower unmarketable52% of the time (Fig.1b); and
4)damage and marketable losses occur regardless of cauliower age
at infestation (Fig.2).
Given that there is essentially no larval threshold for swede
midge on cauliower, we suggest plants be protected for the entire
season. Our trials tested larval densities that are much lower than
would be experienced in an infested eld where females oviposit
clusters of 5–20 eggs on host plants (Readshaw 1966). Traditional
scout and spray IPM approaches remain inappropriate for manag-
ing swede midge in cauliower because market-relevant damage can
result from any larval feeding and adults can emerge throughout the
growing season (Hallett etal. 2009a, Chen etal. 2011; Samietz etal.
2012; Hallett and Sears 2013; Des Marteaux etal. 2015).
Other Cecidomyiid species have been shown to excrete digestive
enzymes that disrupt growth and development on their host (Tooker
and De Moraes 2007, 2010; Tooker 2012). The same has been pre-
sumed but not tested in swede midge. The fact that our single larva
treatment rendered half of the cauliower unmarketable yet half
of the larvae die following our procedure is troubling. However, it
would be interesting to specically test if damage is caused from sal-
ivary excretions or physical injury caused by larvae. If larval excre-
tions distort cauliower growth independent of physical damage,
then a more accurate damage or marketability threshold could be
determined by applying known volumes of extracted saliva to plants.
These additional trials could also lead toward a more complete
understanding of how, so few larvae are able to cause such signif-
icant losses in cauliower.
In addition, we tested how cauliower damage varies following
a single oviposition event. Swede midge has a short life cycle and
multiple generations occur in infested elds (Hallett etal. 2009b).
How damage and marketability vary in response to multiple infesta-
tions remains untested. Our results suggest that multiple infestations
would further reduce the likelihood that plants are marketable, but
swede midge damage varies across and within different Brassica cul-
tivars (Chen etal. 2011). Further work testing how multiple infes-
tations inuence cauliower damage and how single infestations
inuence damage to other Brassica crops are warranted.
Heading brassicas, like cauliower, may also be more susceptible
to swede midge herbivory than those with multiple meristems. As
mentioned, we still do not know whether larval excretions impact
development throughout the plant or only within the infested mer-
istem. If swede midge damage is localized to the developing meris-
tem, plants with multiple growing points, like canola and brussels
sprouts, may only lose a portion of marketable growth. That said,
whether the number or severity of infested meristems on crops with
multiple growing points inuences ultimate damage or marketability
has not been tested.
Swede midge poses a major threat to Brassica production in
their introduced range (Hallett and Heal 2001; Chen et al. 2011;
Hallett and Sears 2013). While systemic insecticides and calen-
dar-based foliar sprays effectively manage swede midge conven-
tionally (Hallett etal. 2009a), regular spraying reverses previous
gains in IPM programs developed for other Brassica pests (Hallett
and Sears 2013; Rodriguez Salamanca 2014), like diamondback
moth and imported white cabbage worm (Furlong et al. 2013).
Furthermore, large-scale crop rotations can provide control for
organic producers (Chen and Shelton 2009) but only temporarily
on farms with limited acreage because a portion of pupae remain
dormant in the soil (Readshaw 1966; Hallett 2007; Stuart etal.
2012). To avoid dormant populations, growers are recommended
to rotate at least 2 km away from previous Brassica plantings for
at least 3 yr. Tactics that prevent mated females from nding and
ovipositing on host plants (e.g., repellents), males from nding and
mating with females (e.g., pheromone mating disruption), and/or
physically block midges from contacting Brassica crops (e.g., exclu-
sion netting) will be more effective long-term solutions to manage
swede midge organically.
Acknowledgments
We thank City Market in Burlington, VT, and their co-op members for donat-
ing their patronage dividends that comprised our Co-op Seedling Patronage
Grant, which funded our project. We also thank Colleen Armstrong, David
Heleba, and Tom Doubleday from the University of Vermont greenhouses for
assisting with plant production, and Ross Pillischer for assisting with data
collection. USDA National Institute of Food and Agriculture (grant number:
2013-34103-21431) and the Vermont Specialty Crop Block Grant Program
(grant number: 02200-SCBGP-9-1) provided support for the graduate assist-
antship to C.A.S.
References Cited
Andaloro, J. T., K. B.Rose, A. M.Shelton, C. W.Hoy, and R. F.Becker. 1983.
Cabbage growth stages. N. Y.Food Life Sci. Bull. 101: 1–4.
Chen, M., and A. M.Shelton. 2007. Impact of soil type, moisture, and depth
on swede midge (Diptera: Cecidomyiidae) pupation and emergence.
Environ. Entomol. 36: 1349–1355.
Chen, M., and A. M.Shelton. 2009. Simulated crop rotation systems control
swede midge, Contarinia nasturtii. Entomol. Exp. Appl. 133: 84–91.
Journal of Insect Science, 2018, Vol. 18, No. 3 5
Downloaded from https://academic.oup.com/jinsectscience/article-abstract/18/3/24/5040085
by Guy W Bailey Howe Library user
on 29 June 2018

Chen, M., A.M. Shelton, P. Wang, C. A. Hoepting, W. C. Kain, and D. C.Brainard.
2009. Occurrence of the new invasive insect Contarinia nasturtii (Diptera:
Cecidomyiidae) on cruciferous weeds. J. Econ. Entomol. 102: 115–120.
Chen, M., A.M. Shelton, R. H. Hallett, C. A. Hoepting, J. R. Kikkert, and
P.Wang. 2011. Swede midge (Diptera: Cecidomyiidae), ten years of inva-
sion of crucifer crops in North America. J. Econ. Entomol. 104: 709–716.
Des Marteaux, L. E., J. M.Schmidt, M. B.Habash, and R. H.Hallett. 2015.
Patterns of diapause frequency and emergence in swede midges of south-
ern Ontario. Agric. For. Entomol. 17: 77–89.
Furlong, M. J., D.J. Wright, and L. M.Dosdall. 2013. Diamondback moth
ecology and management: problems, progress, and prospects. Annu. Rev.
Entomol. 58: 517–541.
Hall, D. R., L. Amarawardana, J. V. Cross, W. Francke, T. Boddum, and
Y.Hillbur. 2012. The chemical ecology of Cecidomyiid midges (Diptera:
Cecidomyiidae). J. Chem. Ecol. 38: 2–22.
Hallett, R. H. 2007. Host plant susceptibility to the swede midge (Diptera:
Cecidomyiidae). J. Econ. Entomol. 100: 1335–1343.
Hallett, R., and J. Heal. 2001. First Nearctic record of the swede midge
(Diptera: Cecidomyiidae), a pest of cruciferous crops from Europe. Can.
Entomol. 133: 713–715.
Hallett, R. H., and M. K.Sears. 2013. Pheromone-based action thresholds for con-
trol of the swede midge, Contarinia nasturtii (Diptera: Cecidomyiidae), and
residual insecticide efcacy in cole crops. J. Econ. Entomol. 106: 267–276.
Hallett, R. H., M.Chen, M. K.Sears, and A. M.Shelton. 2009a. Insecticide man-
agement strategies for control of swede midge (Diptera: Cecidomyiidae)
on cole crops. J. Econ. Entomol. 102: 2241–2254.
Hallett, R. H., S. A. Goodfellow, R. M. Weiss, and O. Olfert. 2009b.
MidgEmerge, a new predictive tool, indicates the presence of multiple
emergence phenotypes of the overwintered generation of swede midge.
Entomol. Exp. Appl. 130: 81–97.
Hodgdon, E. A., Y. H.Chen, C. A.Hoepting, and R.Hallett. 2017. Organic
management of Swede midge. New York State IPM. https://ecommons.
cornell.edu/handle/1813/55087
Kogan, M. 1998. Integrated pest management: historical perspectives and con-
temporary developments. Annu. Rev. Entomol. 43: 243–270.
Maia, V. C., P. D. A. L.Constantino, and R. F. Monteiro. 2005. New gall
midges (Diptera, Cecidomyiidae) associated with two species of Eugenia
(Myrtaceae). Rev. Bras. Entomol. 49: 347–352.
Olfert, O., R. Hallett, R. M. Weiss, J. Soroka, and S. Goodfellow. 2006.
Potential distribution and relative abundance of swede midge, Contarinia
nasturtii, an invasive pest in Canada. Entomol. Exp. Appl. 120: 221–228.
Readshaw, J. L. 1966. The ecology of the swede midge, Contarinia nasturtii
(Kieff.) (Diptera, Cecidomyiidae). I.--Life history and inuence of temper-
ature and moisture on development. Bull. Entomol. Res. 56: 685–700.
Rodriguez Salamanca, L. M. 2014. Cole crops integrated pest management.
Michigan State Univ. Ext.
RStudio Team. 2016. RStudio: Integrated Development Environment for
R. R Foundation for Statistical Computing, Vienna, Austria. https://
www.R-project.org/
Samietz, J., R. Baur, and Y.Hillbur. 2012. Potential of synthetic sex phero-
mone blend for mating disruption of the swede midge, Contarinia nastur-
tii. J. Chem. Ecol. 38: 1171–1177.
Stuart, J. J., M.S. Chen, R. Shukle, and M. O.Harris. 2012. Gall midges
(Hessian ies) as plant pathogens. Annu. Rev. Phytopathol. 50:
339–357.
Stubben, C. J., and B. G.Milligan. 2007. Estimating and analyzing demo-
graphic models using the popbio package in R. J. Stat. Softw. 22:
1–23.
Tooker, J. 2012. Hessian y on wheat. Penn State Coop. Ext. ento.psu.edu/
extension/factsheets/pdf/pdf-version-of-hessian-y-on-wheat (accessed 8
June 2018).
Tooker, J., and C.De Moraes. 2007. Feeding by Hessian y larvae does not
induce plant indirect defences. Ecol. Entomol. 32: 153–161.
Tooker, J., and C.De Moraes. 2010. Feeding by hessian y (Mayetiola destruc-
tor [Say]) larvae on wheat increases levels of fatty acids and indole-3-
acetic acid but not hormones involved in plant-defense signaling. J. Plant
Growth Regul. 30: 158–165.
Uechi, N., J. Yukawa, M.Tokuda, and N.Maryana. 2017. Description of
the Asian chili pod gall midge, Asphondylia capsicicola sp. n., with com-
parative notes on Asphondylia gennadii (Diptera : Cecidomyiidae) that
induces the same sort of pod gall on the same host plant species in the
Mediterranean region. Appl. Entomol. Zool. 52: 113–123.
Vijaykumar, L., A. K. Chakravarthy, S. U. Patil, and D. Rajanna. 2009.
Resistance mechanism in rice to the midge Orseolia oryzae (Diptera:
Cecidomyiidae). J. Econ. Entomol. 102: 1628–1639.
Vitou, J., M.Skuhravá, V.Skuhravý, J. K.Scott, and A. W.Sheppard. 2008. The
role of plant phenology in the host specicity of Gephyraulus raphanistri
(Diptera: Cecidomyiidae) associated with Raphanus spp. (brassicaceae).
Eur. J.Entomol. 105: 113–119.
Walker, P. T. 1983. Crop losses: the need to quantify the effects of pests,
diseases and weeds on agricultural production. Agric. Ecosyst. Environ.
9: 119–158.
Wickham, H. 2009. ggplot2: elegant graphics for data analysis. Springer-
Verlag, New York, New York. http://ggplot2.org
Wu, Q. J., J.Z. Zhao, A. G. Taylor, and A. M.Shelton. 2006. Evaluation of
insecticides and application methods against Contarinia nasturtii (Diptera:
Cecidomyiidae), a new invasive insect pest in the United States. J. Econ.
Entomol. 99: 117–122.
6 Journal of Insect Science, 2018, Vol. 18, No. 3
Downloaded from https://academic.oup.com/jinsectscience/article-abstract/18/3/24/5040085
by Guy W Bailey Howe Library user
on 29 June 2018