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Optimizing Trap Design and Trapping Protocols for Drosophila
suzukii (Diptera: Drosophilidae)
Author(s): Justin M. Renkema, Rosemarije Buitenhuis, and Rebecca H. Hallett
Source: Journal of Economic Entomology, 107(6):2107-2118. 2014.
Published By: Entomological Society of America
URL: http://www.bioone.org/doi/full/10.1603/EC14254
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HORTICULTURAL ENTOMOLOGY
Optimizing Trap Design and Trapping Protocols for Drosophila suzukii
(Diptera: Drosophilidae)
JUSTIN M. RENKEMA,
1,2
ROSEMARIJE BUITENHUIS,
3
AND REBECCA H. HALLETT
1
J. Econ. Entomol. 107(6): 2107Ð2118 (2014); DOI: http://dx.doi.org/10.1603/EC14254
ABSTRACT Drosophila suzukii Matsumura (Diptera: Drosophilidae) is a recent invasive pest of fruit
crops in North America and Europe. Carpophagous larvae render fruit unmarketable and may promote
secondary rot-causing organisms. To monitor spread and develop programs to time application of
controls, further work is needed to optimize trap design and trapping protocols for adult D. suzukii.
We compared commercial traps and developed a new, easy-to-use plastic jar trap that performed well
compared with other designs. For some trap types, increasing the entry area led to increased D. suzukii
captures and improved selectivity for D. suzukii when populations were low. However, progressive
entry area enlargement had diminishing returns, particularly for commercial traps. Unlike previous
studies, we found putting holes in trap lids under a close-Þtting cover improved captures compared
with holes on sides of traps. Also, red and black traps outperformed yellow and clear traps when traps
of all colors were positioned 10Ð15 cm apart above crop foliage. In smaller traps, attractant surface
area and entry area, but not other trap features (e.g., headspace volume), appeared to affect D. suzukii
captures. In the new, plastic jar trap, tripling attractant volume (360 vs 120 ml) and weekly attractant
replacement resulted in the highest D. suzukii captures, but in the larger commercial trap these
measures only increased by-catch of large-bodied Diptera. Overall, the plastic jar trap with large entry
area is affordable, durable, and can hold high attractant volumes to maximize D. suzukii capture and
selectivity.
KEY WORDS spotted wing drosophila, trap design, attractant, color
Drosophila suzukii Matsumura (Diptera: Drosophili-
dae), commonly called spotted wing drosophila, was
Þrst described in Japan and is recorded from other
Asian countries; it was found in California and Spain
in 2008 and has since spread across mainland North
America and Europe (Kanzawa 1935, Hauser 2011,
Calabria et al. 2012, Cini et al. 2012). Female D. suzukii
ßies have a serrated ovipositor that allows them to lay
eggs in ripe and ripening soft-skinned temperate fruit
crops (Mitsui et al. 2006, Walsh et al. 2011). Devel-
oping larvae cause softening of fruit tissues, rendering
fruit unmarketable and may promote rot-causing or-
ganisms, accelerating decomposition (Louis et al.
1996, Walsh et al. 2011). Under heavy infestations, up
to 80% yield loss can occur (Lee et al. 2011); 20 and
37% losses in revenue were estimated in untreated
California strawberries and raspberries, respectively
(Goodhue et al. 2011), and over $26 million in crop
losses were reported in the eastern United States in
2013 (Burrack 2014).
As a response to the rapid spread and high economic
impact of D. suzukii, considerable efforts are being
made to develop monitoring and management pro-
grams. A number of insecticide classes are effective
against D. suzukii, but application frequencies (5Ð14 d;
Bruck et al. 2011) may increase both the risk that
maximum insecticide residue limits are exceeded and
the potential for resistance development. Cultural
control methods such as removal of dropped or over-
ripe fruit, removal of wild hosts from Þeld margins, and
exclusion netting are recommended currently (Ka-
wase et al. 2007, Walsh et al. 2011, Cini et al. 2012,
Ontario Ministry of Agriculture, Food, and Rural Af-
fairs [OMAFRA] 2014a), and biological control agents
are under investigation (Chabert et al. 2012). To mon-
itor D. suzukii, ßies can be easily trapped in homemade
containers with entry holes and baited with afford-
able, moderately attractive liquids, such as apple cider
vinegar, a yeastÐsugar solution, or whole wheat bread
dough (e.g., Dreves and Langellotto-Rhodaback 2011,
Eaton 2014, OMAFRA 2014b). However, trap designs
and captures vary widely, with little standardization
and utility for making management decisions. With
the identiÞcation of a highly attractive lure (Cha et al.
2012, 2014), optimizing trap physical design, and de-
veloping trapping protocols, trapping should become
more useful for monitoring and possibly for popula-
tion reduction.
Recently, a large, multi-state project was conducted
to evaluate several trap types and designs and identify
trap features that improved captures of and selectivity
1
School of Environmental Sciences, University of Guelph, 50 Stone
Rd. E., Guelph, Ontario, Canada N1G 2W1.
2
Corresponding author, e-mail: renkemaj@uoguelph.ca.
3
Vineland Research and Innovation Centre, 4890 Victoria Ave. N.,
Box 4000, Vineland Station, Ontario, Canada L0R 2E0.
0022-0493/14/2107Ð2118$04.00/0 䉷2014 Entomological Society of America
for D. suzukii (Lee et al. 2012, 2013). It showed that
trap types affect D. suzukii captures but not selectivity;
traps with larger entry area captured more ßies than
those with smaller entry areas (Landolt et al. 2011, Lee
et al. 2012). However, entry area modiÞcations were
not evaluated between traps of the same design. Sur-
face area of liquid attractants within traps also appears
to be an important trap feature, as increasing the
surface area improved ßy captures (Lee et al. 2013).
Keeping entry area and attractant surface area equal
between different trap types will provide useful in-
formation on whether differences in other trap fea-
tures (e.g., headspace, trap volume) affect D. suzukii
captures. Color appears to be an important visual cue
for D. suzukii, but the most attractive color for traps
has not been established (Basoalto et al. 2013, Lee et
al. 2013). Finally, mass trapping has been suggested for
D. suzukii control (e.g., Cini et al. 2012). Effects of
variables, such as attractant volume and replacement
frequency, have not been assessed on D. suzukii cap-
tures but should provide useful information for de-
veloping mass trapping protocols.
Field studies were conducted in 2012 and 2013 to
improve trap design and trapping protocols for D.
suzukii. Suggestions and issues arising from previous
work (Lee et al. 2012, 2013; Basoalto et al. 2013) were
used to address speciÞc trapping questions and pro-
vide new information for trap development. We tested
whether increasing entry area in all traps would ubiq-
uitously improve D. suzukii captures or selectivity
(experiment A), whether other trap features affected
D. suzukii captures when entry area and attractant
surface area were equivalent (experiment B), and
whether entry area position on traps affected D. su-
zukii captures (experiment C). Effect of trap color was
tested in the Þeld, but traps were positioned close
together so ßies were presented with all colors simul-
taneously (experiment D). Trap attractant volume
and replacement frequency were altered to determine
effects on D. suzukii captures and selectivity (exper-
iment E).
Materials and Methods
Experiment A: Trap Type and Entry Area. Home-
made deli-cup traps and 2012 models of commercially
available Contech Fruit Fly Traps (Contech Enter-
prises Inc., Victoria, BC, Canada) and Biobest Droso
Traps (Biobest Canada Ltd., Leamington, ON, Can-
ada) in 2012 and a homemade plastic jar trap in 2013
with modiÞed entry areas were evaluated (Table 1;
Fig. 1). Clear deli-cups (Twinpak, Plastipak Industries
Inc., Boucherville, QC, Canada) and plastic jars (Rich-
ards Packaging, Mississauga, ON, Canada) were
wrapped with red tape (Cantech Industries Inc., John-
son City, TN), and plastic jars had a red plastic plate
(22 cm in diameter) as a rain cover over the jar lid.
Entry areas of different sizes were made with single
hole punches in Deli-cup and modiÞed Contech traps
(small holes: 0.3, 0.8 cm) or with hot metal punches
(large holes: 1.8 cm), along sides of traps near the top.
Metal hardware mesh (3 by 3 mm
2
openings) in 2012
and Þberglass drywall tape (2.5 by 2.5 mm
2
openings;
Sheetrock, CGC Corp., Chicago, IL) in 2013 were
glued over large holes. In modiÞed Biobest traps, the
plastic inserts in holes (that reduced the entry area of
each hole) were removed and mesh was glued over
the holes. In modiÞed Contech traps, the red tubes
inside the traps were removed.
Traps were partially Þlled with 100 ml of apple cider
vinegar (ACV; H.J. Heinz Co., Leamington, ON, Can-
ada) and hung using plastic ties 2Ð3 m above the
ground on tree branches in sweet cherry (Prunus
avium L. ÔHeldenÞngenÕ and ÔLapinsÕ) and peach
(Prunus persica (L.) Stokes ÔRedstarÕ) orchards near
Niagara-on-the-Lake, Ontario (43⬚14⬘1⬙N, 79⬚9⬘51⬙
W), and from bamboo garden stakes pushed into the
ground at an angle so that traps were ⬍0.5 m above
foliage of day-neutral strawberries (Fragaria x anan-
assa Duchesne ÔAlbionÕ) near Vineland, Ontario
(2012: 43⬚10⬘1⬙N, 79⬚20⬘29⬙W; 2013: 43⬚10⬘17⬙N, 79⬚
21⬘38⬙W). All crops were postharvest in 2012, and in
2013, cherries were postharvest, peaches were har-
vested a few days after traps were placed, and straw-
berries were being harvested. Unscented dish deter-
gent (Selection, Metro Brands, Toronto, ON, Canada)
was added to ACV (1 ml/liter) to reduce surface
tension. Within each crop, traps were placed in a
randomized complete block design (RCBD) with Þve
blocks at least 25 m from each other. Within blocks,
traps were 5 m apart (one trap per tree) ina4by2row
grid in 2012 anda3by3rowgrid in 2013. Traps were
Table 1. Physical parameters and details of entry area modifications made to traps used for capturing D. suzukii
Trap type Trap entry area
(mm
2
)
Vol
(ml)
Surface area of
ACV (cm
2
)
Ht above
ACV (cm)
Headspace above
ACV (ml)
a
Entry points (on side) Exp.
Deli-cup 64 500 72 5.5 400 Nine 0.3-cm holes A, B
128 Eighteen 0.3-cm holes A, B, D
2036 Eight 1.8-cm holes A, B
Contech 57 210 17 7.2 120 Two 0.6-cm holes A, B, C
157 Two 0.6-cm ⫹two 0.8-cm holes A, B
2,036 Eight 1.8-cm holes A, B
50 Four 0.4-cm holes (in lid) E
Biobest 340 1100 83 14.5 1,520 Three 1.2-cm holes A, E
2010 Three 1.2-cm ⫹three 1.8-cm holes A
Plastic jar 2036 1000 80 11.5 920 Eight 1.8-cm holes A
b
,C, E
a
Calculated for experiment A; traps with 100 ml ACV.
b
Evaluated in 2013 only.
2108 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 107, no. 6
in place 6Ð19 September 2012 and 19 AugustÐ7 Sep-
tember 2013 and serviced every 4 Ð5 d by emptying the
contents, adding new ACV, and rerandomizing within
blocks.
Experiment B: Trap Type and Entry Area With
Equivalent Attractant Surface Area. Two trap types
with small (64 or 57 mm
2
), medium (128 or 157 mm
2
),
or large (2036 mm
2
) entry areas (Table 1) and equiv-
alent ACV surface area were evaluated in 2012. Small
plastic cups (30 ml; Solo Cup Company, Lake Forest,
IL) were held in place on bottoms of traps with small
pieces of mounting putty (Lepage, Henkel Canada
Corp., Mississauga, ON, Canada) and partially Þlled
with 25 ml ACV (surface area ⫽12.6 cm
2
). Water (60
ml) with dish detergent was added to the trap sur-
rounding the small plastic cup.
Traps were hung on trellising string ⬇1 m above the
ground in red raspberries (Rubus sp. ÔNovaÕ) near
Waterloo, Ontario (43⬚29⬘57⬙N, 80⬚38⬘14⬙W) in an
RCBD with seven blocks that were at least 15 m apart.
Traps were 5 m apart within blocks ina3by2rowgrid.
Traps were in place 5Ð13 October and serviced every
4Ð5 d; ßies that drowned in ACV and water were
collected.
Experiment C: Entry Area Position. ModiÞed
Contech traps, with holes in the lid and a larger,
7-cm-diameter red lid as a cover, were evaluated in
2013 and compared with unmodiÞed Contech and
plastic jar traps (Table 1; Fig. 1). Traps were partially
Þlled with ACV (100 ml) and hung from trellising
string ⬇1 m above the ground in fall red raspberries
(Rubus sp. ÔAutumn BrittenÕ) at two locations: Milton
(43⬚34⬘37⬙N, 79⬚57⬘22⬙W) and Vineland, Ontario
(43⬚9⬘56⬙N, 79⬚22⬘48⬙W) in an RCBD with six
replications at each site. Blocks were at least 15 m
apart, and traps were 5 m apart along a single raspberry
row within blocks. Traps were in place 24 Septem-
berÐ 8 or 9 October (Milton or Vineland, respectively)
and serviced every 4Ð6 d. Other Drosophila spp. in
traps were not counted in this experiment.
Experiment D: Trap Color. Four trap colors were
evaluated in 2012 by spray painting deli-cups and lids
(Table 1) red, black, or yellow (Rust-Oleum Corp.,
Vernon Hills, IL) or leaving them unsprayed (clear).
Traps were partially Þlled with 120 ml ACV and
hung 25 cm apart from 90 cm bamboo stakes that
were secured horizontally on fence posts above
foliage of fall red raspberries (Rubus sp. ÔAutumn
BrittenÕ) near Milton, Ontario (43⬚34⬘37⬙N, 79⬚
57⬘22⬙W). Each stake had one trap of each color.
Trap color order was randomized along each stake
and rerandomized each time traps were serviced.
There were six replications with stakes spaced at
least 25 m apart in randomly chosen locations
throughout the Þeld. Traps were in place 24 Octo-
berÐ7 November and serviced weekly. Trap color
was characterized with a colorimeter (CR Ð 400,
Konica-Minolta, Ramsey, NJ) using the L*a*b*in-
Fig. 1. Homemade deli-cup (a, b) and plastic jar (g) and commercial Contech (c, d, e, f) and Biobest (h, i) traps with
modiÞed entry areas (see Table 1 for entry areas) used to capture D. suzukii.
December 2014 RENKEMA ET AL.: TRAP DESIGNS FOR D. suzukii 2109
dices, where the L*value is 0 for black and 100 for
white, a*is positive for red-purple and negative for
bluish-green, and b*is positive for yellow and neg-
ative for blue (McGuire 1992). L*a*b*indices
wereÑyellow traps, 86.11, ⫺6.27, 65.02; red traps,
41.89, 48.79, 29.53; and black traps, 24.62, 0.18, ⫺0.36.
Experiment E: Trap Type and Attractant Volume
and Replacement Frequency. Two trap types (Table
1) were evaluated in 2013 for effects of ACV volume
and frequency of ACV replacement on numbers of
D. suzukii and total by-catch. Traps were partially
Þlled with either 120 or 360 ml ACV, and those with
360 ml were either serviced weekly or only at the
end of the experiment. Traps were hung in fall red
raspberries (Rubus sp. ÔPolanaÕ and ÔAutumn Brit-
tenÕ) near Mt. Albert, Ontario (44⬚8⬘17⬙N, 79⬚
17⬘15⬙W) from 24 SeptemberÐ15 October in an
RCBD with Þve replications. Arrangement and ser-
vicing of traps was as described in experiment C;
traps with 360 ml that were only emptied at the end
of the experiment were rerandomized with the
other traps within blocks each week. The by-catch
(all non-D. suzukii individuals) was identiÞed to
family and categorized by size as small, medium, or
large (see Table 5 for details).
Data Analysis. Captures over the entire trapping
period were analyzed for experiments B, D, and E.
Captures of D. suzukii were calculated per day for
experiment C where the trapping period varied be-
tween sites and for experiment A where the trapping
period varied year-to-year and because a few traps fell
during certain trapping periods.
Captures of male, female, total D. suzukii ßies, the
proportion of D. suzukii out of total Drosophila by-
catch (experiment A), and total by-catch sorted by
size (experiment E) were analyzed using the standard
least squares platform in JMP software (SAS Institute
2012;
␣
⫽0.05) with Þxed and random effects. Fixed
effects wereÑtrap type, crop, and trap type ⫻crop
(years analyzed separately) for experiment A; trap
type, entry area, and trap type ⫻entry area for ex-
periment B; trap type, location, and trap type ⫻lo-
cation for experiment C; and trap type, attractant
amount and replacement frequency, and trap type ⫻
amount and replacement frequency for experiment E.
Blocks or blocks nested within crops or sites were
random effects. Where trap type and crop or site
interactions were signiÞcant, trap performance was
subsequently analyzed for each crop or site. Resid-
uals were checked for normality of error variance,
and data were log (x) or square-root (x) trans-
formed where necessary. Back-transformed lsmeans
are shown; TukeyÕs honestly signiÞcant difference
(HSD) tests were used to separate lsmeans or trans-
formed lsmeans.
For experiment D, numbers of D. suzukii in traps of
different colors were compared using goodness-of-Þt
Gtests. The pooled G-test statistic is presented, as
results were consistent between replicates (hetero-
geneity G-test, P⬎0.05; McDonald 2009).
Results
Experiment A: Trap Type and Entry Area. Num-
bers of D. suzukii ßies captured in traps with varying
entry areas differed signiÞcantly in both 2012 and 2013
(Fig. 2). More ßies were captured in deli-cup traps
with the largest entry area than any other trap type in
2012. In 2013, plastic jar traps and deli-cup traps with
largest entry area captured more ßies than other traps.
In both years, captures in Contech traps were im-
proved by increasing the entry area from 57 to 157
mm
2
, but not by a further increase from 157 to 2036
mm
2
. Increasing the entry area of Biobest traps did not
improve ßy captures in either year. In 2012, the pro-
portion of Drosophila spp. caught that were D. suzukii
did not differ by trap type, but in 2013 higher propor-
tions were generally found in traps with larger entry
areas (Fig. 3).
In 2012, captures of females differed due to the trap
type and entry area ⫻crop interaction (F
14,84
⫽2.7,
P⫽0.002), but captures of males did not (F
14,84
⫽1.5,
P⫽0.146). In 2013, captures differed signiÞcantly for
both females (F
16,96
⫽3.6, P⬍0.0001) and males
(F
16,96
⫽5.7, P⬍0.0001) due to the trap type and entry
area ⫻crop interaction. Main differences in male and
female trap captures between crops in both years were
due to efÞciency of Contech 156 mm
2
compared with
Contech 2,036 mm
2
, and magnitude of differences
between the best traps (deli-cup 2,036 mm
2
and plastic
jar traps) compared with less effective traps (Tables
2Ð4).
Experiment B: Trap Type and Entry Area With
Equivalent Attractant Surface Area. When attractant
surface areas were equivalent, neither trap type nor
the trap type ⫻entry area interaction affected trap
captures (Fig. 4). For female and total ßies, but not
male ßies, D. suzukii captures increased with increas-
ing entry area. There were signiÞcantly higher cap-
tures in traps with largest (2,036 mm
2
) compared with
smallest (57 or 64 mm
2
) entry areas. Proportion of D.
suzukii out of all Drosophila spp. (71Ð83%) was not
signiÞcantly affected by trap type (F
1,29
⫽1.6, P⫽
0.212), entry area (F
2,29
⫽0.1, P⫽0.941), or their
interaction (F
2,30
⫽0.2, P⫽0.842).
Experiment C: Entry Area Position. Numbers of
male, female, and total D. suzukii ßies captured dif-
fered signiÞcantly between trap types and locations,
but the trap type ⫻location interaction was only
signiÞcant for total ßies (Fig. 5). About eight times
more total ßies were captured in modiÞed (four holes
in lids) than unmodiÞed Contech traps, and about
double the number of ßies was captured in plastic jar
traps than modiÞed Contech traps. When male and
female ßies were analyzed separately, plastic jar traps
did not capture more ßies than modiÞed Contech
traps (Fig. 5). More total ßies were captured at Milton
(33.9 ⫾6.7/8.2) than at Vineland (7.3 ⫾1.4/1.7;
lsmeans ⫾95% CI). The signiÞcant trap type ⫻loca-
tion interaction was due to more total ßies captured in
plastic jar traps than modiÞed Contech traps at Milton,
but not at Vineland.
2110 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 107, no. 6
Experiment D: Trap Color. Male, female, and total
D. suzukii ßy captures varied signiÞcantly due to trap
color (Fig. 6). Red and black traps captured more ßies
than clear or yellow traps. The proportion of Drosoph-
ila spp. caught that were D. suzukii was not signiÞ-
cantly affected by trap color (
2
⫽1.5, df ⫽3, P⫽
0.684), although percent D. suzukii in red and black
(86 and 84%) traps was ⬇10% greater than that in
yellow and clear traps (74 and 75%).
Experiment E: Trap Type and Attractant Volume
and Replacement Frequency. Trap type and attract-
ant amount and replacement frequency signiÞcantly
affected numbers of and percent D. suzukii captured
(Fig. 7). More D. suzukii were captured in plastic jar
traps with 360 ml of ACV replaced weekly than in all
other trap and amount and replacement frequency
combinations. Plastic jar traps captured a higher per-
centage of D. suzukii than Biobest traps. Plastic jar
traps with 360 ml ACV replaced weekly had a higher
proportion of D. suzukii out of the total by-catch than
those with 120 ml replaced weekly or 360 ml not
replaced.
The by-catch in traps consisted mainly of beetles
(Coleoptera) and ßies (Diptera). The large majority
of beetle by-catch was sap beetles (Nitidulidae), and
plastic jar traps with 360 ml ACV replaced weekly
captured more nitidulids than most other trap types
and amount and replacement frequency combinations
(Table 5). Large-sized by-catch was dominated by
blow ßies (Calliphoridae) that were almost exclu-
sively captured in Biobest traps and in higher numbers
when 360 ml ACV was replaced weekly in Biobest
traps compared with 360 ml that was not replaced. The
by-catch of medium-sized Diptera was more than dou-
ble in Biobest than plastic jar traps and more than two
to three times greater in traps with 360 ml ACV re-
placed weekly than others. Small-sized by-catch in
plastic jar traps was nearly double that of Biobest traps
Fig. 2. Mean (⫾95% CI) numbers of D. suzukii captured in four trap types with varying entry areas (mm
2
) in three crops
(cherries, peaches, and strawberries) in the Niagara region, Ontario, experiment A in (a) 2012 (trap F
7,84
⫽36.3, P⬍0.0001;
crop F
2,12
⫽12.2, P⫽0.001; trap ⫻crop F
14,84
⫽2.3, P⫽0.009) and (b) 2013 (trap F
8,96
⫽37.3, P⬍0.0001; crop F
2,12
⫽88.4,
P⬍0.0001; trap ⫻crop F
16,96
⫽5.7, P⬍0.0001). Plastic jar traps tested only in 2013. Arrows indicate unmodiÞed commercial
traps. Back-transformed lsmeans are shown; bars with the same letter in each panel are not signiÞcantly different (TukeyÕs
HSD test,
␣
⫽0.05).
December 2014 RENKEMA ET AL.: TRAP DESIGNS FOR D. suzukii 2111
and was greater in traps with 360 ml ACV replaced
weekly than others.
Discussion
Improving trap design and trapping protocol, along
with other methods and developments (e.g., detection
of larvae in ripe fruit, highly attractive lures), will
increase the utility of trap capture data for monitoring
the range expansion of D. suzukii and making man-
agement decisions where this pest severely impacts
soft-skinned fruit. Here we show that trap entry area
size and placement, liquid attractant surface area, at-
tractant volume and replacement frequency, and trap
color affect D. suzukii captures. Our results differ from
those of previous D. suzukii trapping studies (Lee et
al. 2012, 2013; Basoalto et al. 2013) by showing that
entry area enlargement has diminishing returns, traps
with entry holes on lids capture more ßies, and that red
and black traps improve captures compared with yel-
low traps. We have developed an easy-to-use home-
made trap that with increased volume and frequent
Fig. 3. Mean (⫾95% CI) percent D. suzukii of all Drosophila spp. captured in four trap types with varying entry areas
(mm
2
) in three crops (cherries, peaches, and strawberries) in the Niagara region, Ontario, experiment A in (a) 2012 (trap
F
7,84
⫽2.0, P⫽0.067; crop F
2,12
⫽89.7, P⬍0.0001; trap ⫻crop F
14,84
⫽0.6, P⫽0.844) and (b) 2013 (trap F
8,96
⫽7.1, P⬍
0.0001; crop F
2,12
⫽55.4, P⬍0.0001; trap ⫻crop F
16,96
⫽1.6, P⫽0.083). Plastic jar traps tested only in 2013. Arrows indicate
unmodiÞed commercial traps. Back-transformed lsmeans are shown; bars with the same letter in each panel are not
signiÞcantly different (TukeyÕs HSD test,
␣
⫽0.05).
2112 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 107, no. 6
replacement of liquid attractant captures more D. su-
zukii and fewer nontarget organisms than a commer-
cial trap.
Based on results of Lee et al. (2012), we expected
improved trap captures of D. suzukii with increased
entry area of the three trap types examined in this
study. Indeed we found that increasing the entry area
from 64 to 2,036 mm
2
in deli-cup traps resulted in a
fourfold and over threefold increase in captures in
2012 and 2013, respectively. However, increasing the
entry area from 340 to 2,010 mm
2
in Biobest traps
resulted in a small, nonsigniÞcant gain in captures. It
is likely that there is a diminishing rate of increasing
captures with increased entry area (Lee et al. 2012),
as increasing Contech trap entry area from 57 to 156
mm
2
(and removing the red tube) signiÞcantly im-
proved captures, but a further increase to 2,036 mm
2
had no effect in 2012 and little effect in 2013. A di-
minishing rate of increase may also depend on initial
(unmodiÞed) trap entry area and other trap charac-
teristics (e.g., attractant surface area, trap size).
The position of entry holes affected D. suzukii cap-
tures, as four holes (50 mm
2
) in the lid of Contech
traps resulted in D. suzukii captures that were approx-
imately eight times higher than those in unmodiÞed
Contech traps with two holes (57 mm
2
) on the trap
sides. This result is opposite to what Lee et al. (2013)
found, where side-entry traps captured four to seven
times more ßies than traps with covered top entries.
The trap entry area and the distance between the lid
and the cover were larger in the Lee et al. (2013) study
than this experiment. A larger distance between cover
and trap may have allowed rain to enter traps, thus
diluting the attractant and reducing attractiveness
compared with side-entry traps. The proximity and
larger diameters of Contech covers relative to the trap
lids likely prevented any rain from entering traps.
However, in this study plastic jar traps with side en-
tries and covers still captured twice as many D. suzukii
ßies than Contech traps with holes in lids.
The surface area of liquid attractants in traps can
affect D. suzukii captures, as increasing ACV surface
area from 40 to 90 cm
2
resulted in 12% more captures
(Lee et al. 2013). In the current study, when surface
area was equivalent between two trap types, deli-cups
and Contech, differences in D. suzukii captures de-
pended only on entry area. Other trap features that
differ between deli-cup and Contech designs, such as
height above attractant and headspace, did not appear
to affect captures. Therefore, fewer captures in Con-
tech than deli-cup traps when both had entry areas of
2,036 mm
2
(experiment A), may be explained by the
larger attractant surface area in deli-cup than Contech
traps (72 vs 17 cm
2
). However, despite having large
entry and attractant surface areas, Biobest traps per-
formed poorly in experiment A, meaning too large
headspace or height above attractant could negatively
affect D. suzukii captures. Due to the design of the
2012 Biobest trap, which did not have a ßat bottom, it
was not possible to manipulate the attractant surface
area.
Improved trap sensitivity is required for accurate
monitoring of D. suzukii at low population levels to
time control measures. We found the same trends in
D. suzukii capture rates among trap types and entry
areas in 2013 (earlier in the season, lower captures) as
in 2012 (later in the season, higher captures). In straw-
Table 4. Mean (95% CI) numbers of female D. suzukii cap-
tured per trap per day in four trap types with varying entry areas
in three fruit crops, Niagara region, Ontario, 19 August–7 Sep-
tember 2013, experiment A
Trap type Entry area
(mm2)CherriesaPeachesbStrawberriesc
Deli-cup 64 0.6 (0.4Ð1.0)c 0.2 (0.1Ð0.4)bc 0.000c
128 0.8 (0.5Ð1.2)c 0.2 (0.1Ð0.4)bc 0.002 (0.006Ð0.029)bc
2,036 2.9 (2.3Ð3.6)a 0.8 (0.5Ð1.1)a 0.120 (0.050Ð0.221)a
Contech 57 0.5 (0.2Ð0.8)c 0.1 (0.0Ð0.3)c 0.002 (0.006Ð0.029)bc
157 1.9 (1.4Ð2.5)ab 0.3 (0.1Ð0.5)bc 0.025 (0.001Ð0.078)abc
2,036 1.8 (1.3Ð2.4)ab 0.5 (0.3Ð0.8)ab 0.066 (0.018Ð0.144)ab
Biobest 340 0.6 (0.4Ð1.0)c 0.1 (0.0Ð0.3)c 0.002 (0.006Ð0.029)bc
2,010 1.0 (0.7Ð1.5)bc 0.1 (0.0Ð0.3)c 0.036 (0.005Ð0.098)abc
Plastic jar 2036 3.0 (2.3Ð3.7)a 0.9 (0.6Ð1.3)a 0.042 (0.007Ð0.107)abc
F8,32 P22.8 ⬍0.0001 12.9 ⬍0.0001 4.9 0.0005
Means in the same column with the same letter are not signiÞcantly
different, TukeyÕs HSD test,
␣
⫽0.05.
a
Postharvest.
b
Harvest to postharvest.
c
During harvest.
Table 2. Mean (95% CI) numbers of female D. suzukii cap-
tured per trap per day in three trap types with varying entry areas
in three postharvest fruit crops, Niagara region, Ontario, 6 –19
September 2012, experiment A
Trap
type
Entry area
(mm
2
)Cherries Peaches Strawberries
Deli-cup 64 1.0 (0.6Ð1.7)c 0.8 (0.6Ð1.1)b 0.4 (0.3Ð0.7)de
128 2.2 (1.3Ð3.5)bc 0.9 (0.6Ð1.2)b 1.1 (0.7Ð1.7)bc
2,036 5.0 (3.1Ð8.2)a 2.8 (2.0Ð3.8)a 3.1 (2.0Ð4.6)a
Contech 57 1.1 (0.7Ð1.8)c 0.8 (0.6Ð1.1)b 0.3 (0.2Ð0.5)e
157 3.7 (2.3Ð5.9)ab 2.7 (2.0Ð3.8)a 1.1 (0.7Ð1.6)bc
2,036 2.9 (1.8Ð4.7)ab 1.5 (1.1Ð2.0)ab 2.1 (1.4Ð3.1)ab
Biobest 340 1.8 (1.1Ð2.9)bc 1.1 (0.8Ð1.6)b 0.8 (0.5Ð1.1)cd
2,010 2.2 (1.4Ð3.6)bc 1.1 (0.8Ð1.5)b 1.3 (0.9Ð2.0)abc
F
7,28
P10.5 ⬍0.0001 10.4 ⬍0.0001 17.5 ⬍0.0001
Means in the same column with the same letter are not signiÞcantly
different, TukeyÕs HSD test,
␣
⫽0.05.
Table 3. Mean (95% CI) numbers of male D. suzukii captured
per trap per day in four trap types with varying entry areas in three
fruit crops, Niagara region, Ontario, 19 August–7 September
2013, experiment A
Trap type Entry area
(mm2)CherriesaPeachesbStrawberriesc
Deli-cup 64 0.4 (0.2Ð0.6)cd 0.1 (0.0Ð0.4)abc 0.000
128 0.4 (0.2Ð0.6)cd 0.2 (0.0Ð0.5)abc 0.000
2036 1.7 (1.3Ð2.1)a 0.6 (0.2Ð1.0)a 0.012 (0.001Ð0.039)
Contech 57 0.2 (0.1Ð0.4)d 0.0 (0.0Ð0.2)c 0.000
157 0.8 (0.6Ð1.1)bc 0.1 (0.0Ð0.2)bc 0.000
2036 1.0 (0.7Ð1.3)ab 0.4 (0.1Ð0.8)ab 0.004 (0.000Ð0.023)
Biobest 340 0.4 (0.2Ð0.6)cd 0.1 (0.0Ð0.4)abc 0.000
2010 0.4 (0.2Ð0.6)d 0.1 (0.0Ð0.3)abc 0.004 (0.000Ð0.023)
Plastic jar 2036 1.3 (1.0Ð1.7)ab 0.4 (0.2Ð0.9)ab 0.008 (0.000Ð0.032)
F8,32 P20.2 ⬍0.0001 22.8 ⬍0.0001 1.2 0.357
Means in the same column with the same letter are not signiÞcantly
different, TukeyÕs HSD test,
␣
⫽0.05.
a
Postharvest.
b
Harvest to postharvest.
c
During harvest.
December 2014 RENKEMA ET AL.: TRAP DESIGNS FOR D. suzukii 2113
berries in 2013, no or very low male and female cap-
tures in traps with small entry areas would have re-
sulted in a recommendation for no D. suzukii
management, whereas higher captures in traps with
larger entry areas would have supported a decision to
control for D. suzukii at that time. SigniÞcant trap type
and entry area differences among sites or crops for
captures of males or female ßies appeared to be due
largely to differences in captures between modiÞed
Contech traps (156 vs 2036 mm
2
). Therefore, regard-
less of crop (postharvest peaches or cherries versus
ripening strawberries) or hanging method (tree
branches in shade versus bamboo stakes in an open
strawberry Þeld), deli-cup or plastic jar traps with
large entry areas performed best.
Trap selectivity is also important for early season
monitoring and ease of sorting samples. We found
little difference in trap selectivity in 2012, when all
traps captured 20Ð30% D. suzukii out of total Dro-
sophila spp., but in 2013 when D. suzukii proportions
were only 0.5Ð2.5%, traps that captured more Dro-
sophila spp. also captured higher proportions of D.
suzukii. To our knowledge, this is the Þrst report of a
difference in trap design affecting selectivity, as pre-
vious studies found equal proportions of D. suzukii
among trap types with 10Ð70% D. suzukii (Lee et al.
2012, 2103; Basoalto et al. 2013). In experiment E with
plastic jar and Biobest traps, a similar pattern was
observed, with fewer captures and lower selectivity in
Biobest than in plastic jar traps. Plastic jar traps with
mesh over the holes prevented captures of large- and
many medium-sized Diptera, including almost all Cal-
liphoridae that were abundant, as this site was adja-
cent to pasture. Use of mesh over holes shifted the
distribution of the by-catch to small Diptera, as almost
twice as many small Diptera were captured in plastic
jar traps than Biobest traps. The time it took to process
samples was not recorded, but we noted it was less
Fig. 4. Mean (⫾95% CI) numbers of D. suzukii captured in two trap types (deli-cups, Contech; data pooled) with varying
entry area sizes (small: 57 or 64 mm
2
; medium: 128 or 156 mm
2
; large: 2036 mm
2
) and equal attractant surface area per trap
(12.6 cm
2
) in fall red raspberries near Waterloo, Ontario, experiment B. Comparisons for Males: trap type F
1,29
⫽0.39, P⫽
0.535; entry area F
2,29
⫽0.50, P⫽0.615; trap ⫻area F
2,29
⫽1.06, P⫽0.359; Females: trap type F
1,29
⫽2.02, P⫽0.166; entry
area F
2,29
⫽7.49, P⫽0.002; trap ⫻area F
2,29
⫽0.98, P⫽0.388; Total ßies: trap type F
1,29
⫽0.64, P⫽0.429; entry area F
2,29
⫽
4.29, P⫽0.023; trap ⫻area F
2,29
⫽0.10, P⫽0.909. Back-transformed lsmeans are shown; bars with the same letter of the
same case are not signiÞcantly different (TukeyÕs HSD test,
␣
⫽0.05).
Fig. 5. Mean (⫾95% CI) numbers of D. suzukii captured in three trap types 24 SeptemberÐ8 or 9 October 2013 in fall
red raspberries near Milton and Vineland, Ontario, experiment C. Comparisons for Males: trap type F
1,20
⫽56.9, P⬍0.0001;
site F
1,10
⫽50.7, P⬍0.0001; trap ⫻site F
2,20
⫽2.6, P⫽0.096; Females: trap type F
1,20
⫽36.3, P⬍0.0001; site F
1,10
⫽171.1,
P⬍0.0001; trap ⫻site F
2,20
⫽0.9, P⫽0.443; Total ßies: trap type F
2,20
⫽3.7, P⫽0.043; site F
1,10
⫽149.5, P⬍0.0001; trap ⫻
site F
2,20
⫽121.6, P⬍0.0001. Back-transformed lsmeans are shown; bars with the same letter of the same case in the same
font style are not signiÞcantly different (TukeyÕs HSD test,
␣
⫽0.05).
2114 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 107, no. 6
time consuming to separate D. suzukii from other small
ßies than searching for and removing them when they
adhered to the bodies of large ßies.
We hypothesized that captures in large traps
(Biobest, plastic jar) could be improved by adding
more attractant, in this case ACV, and that with in-
Fig. 6. Total numbers of D. suzukii captured in deli-cup traps that were unpainted (clear) or painted (yellow, black, or
red) and hung in groups with one trap of each color above foliage of fall red raspberries near Milton, Ontario, experiment
D. Comparisons for Males:
2
⫽1378.8, df ⫽3, P⬍0.0001; Females:
2
⫽1107.3, df ⫽3, P⬍0.0001; Total ßies:
2
⫽2466.7,
df ⫽3, P⬍0.0001. Percent D. suzukii captures out of total D. suzukii captures is above each bar.
Fig. 7. Mean (⫾SE) (a) numbers and (b) percent D. suzukii out of all by-catch in two trap types (Biobest, Plastic jar)
24 SeptemberÐ15 October in fall red raspberries near Mt. Albert, Ontario, experiment E. Apple cider vinegar in traps (120
or 360 ml) was replaced weekly or not replaced (360 ml) for 3 wk. Comparisons for D. suzukii captures: trap type F
1,20
⫽
38.9, P⬍0.0001; amount and replacement frequency F
2,20
⫽17.5, P⬍0.0001; trap type ⫻amount and replacement frequency
F
1,20
⫽12.0, P⫽0.0004, and for percent D. suzukii: trap type F
2,20
⫽124.9, P⬍0.0001; amount and replacement frequency
F
2,20
⫽2.4, P⫽0.12; trap type ⫻amount and replacement frequency F
2,20
⫽7.8, P⫽0.003. Bars with the same letter in each
panel are not signiÞcantly different (TukeyÕs HSD test,
␣
⫽0.05.
December 2014 RENKEMA ET AL.: TRAP DESIGNS FOR D. suzukii 2115
creased volume, replacement frequency could be re-
duced without compromising D. suzukii captures. Tri-
pling the amount of ACV in plastic jar traps (360 vs 120
ml) improved D. suzukii captures by about three times
and selectivity by ⬇5% with weekly replacement;
however, the same increase in ACV volume did not
improve D. suzukii captures in Biobest traps. We ob-
served that the large by-catch of large- and medium-
sized Diptera ßoated on the ACV and suspect that as
a result, D. suzukii were less likely to drown and more
likely able to escape from Biobest traps through the
large unscreened entry holes. Not replacing 360 ml
ACV for 3 wk resulted in much lower captures in
plastic jar traps than with weekly replacement of 360
ml of ACV, but less of an effect was detected in Biobest
traps. Before placing traps at this location (24 Sep-
temberÐ15 October), D. suzukii was managed with
Delegate (spinetoram) on 2 and 8 September and
malathion on 16 September at recommended rates. As
a result, captures were low the Þrst week (24 Sep-
temberÐ1 October) and four to Þve times higher in the
third and second weeks, respectively (data not
shown). Therefore, as D. suzukii numbers increased,
ACV aged and likely became a less potent attractant.
However, traps without replacement of 360 ml of ACV
captured almost as many D. suzukii as those with 120
ml replaced weekly; therefore, time required for ser-
vicing traps was reduced without compromising cap-
tures.
There was a signiÞcant difference in both male and
female D. suzukii captures among traps of different
colors. As in laboratory choice experiments (Basoalto
et al. 2013), ßies appear to be attracted to red and black
more than yellow when given a choice of trap color in
the Þeld. Lee et al. (2013) reported that when traps
were hung in shady spots and spaced 2Ð3 m apart,
yellow traps captured more D. suzukii ßies than other
colors; captures were 1.5 times higher in yellow than
clear traps that had the fewest captures of all colors.
Differences in color hues may help explain capture
efÞciency differences. Our yellow traps were lighter
in hue (L*a*b*⫽86.11, ⫺6.27, 65.02) than those used
by Lee et al. (2013) (74.23, ⫺2.21, 64.01), and our red
traps (41.89, 48.79, 29.53) had a greater a*value (in-
creased red-purple intensity) than theirs (38.03, 35.15,
19.06). As with other fruit-infesting ßies (Diptera:
Tephritidae, Rhagoletis spp.), attractiveness to trap
colors may be inßuenced by crop type or change with
fruit maturity (Liburd et al. 1998, Henneman and
Papaj 1999, Mayer et al. 2000) or be related to trap age,
as colors may fade throughout the trapping season.
Dark colors, red and black, may be more attractive to
D. suzukii in Þelds with ripe, similarly colored fruit, as
was the case in this experiment. At a few locations with
ripe fruit or postharvest, red traps captured more ßies
than yellow or traps of other colors (Lee et al. 2013).
However, we suspect that differences in our results
and those of Lee et al. (2013) are mainly due to how
traps were positioned. Trap color may not be as im-
portant as the attractant for capturing D. suzukii. Flies
will enter traps with ACV at relatively similar rates
when they do not perceive various colors simultane-
ously (traps spaced 2Ð3 m apart, Lee et al. 2013). When
traps containing the same attractant are near each
other (25 cm apart, this experiment) color becomes a
signiÞcant factor, resulting in captures in red traps that
were seven times higher than in yellow traps. Traps in
our experiment were placed above raspberry foliage,
where colors may contrast more sharply with back-
ground colors (blue sky, white or gray clouds), chang-
ing their relative attractiveness to ßies that are below
in foliage, than colors in shady crop areas where lower
contrasts with background colors may occur. There-
fore, further investigation is needed to determine
whether ßy captures are greater in red or dark colored
Table 5. Mean (95% CI) numbers of non-D.suzukii individuals captured over 3 wk in two trap types with differing amounts and
replacement frequency of apple cider vinegar in fall red raspberries, Mt. Albert, Ontario, 24-September–15 October, experiment E
Trap type Amount (ml) and replace.
freq. Coleoptera
a
Diptera, Hymenoptera, and Lepidoptera
Large
b
Medium
c
Small
d
Biobest 29.4 (16.7Ð45.6) 89.7 (65.0Ð118.5)a 77.1 (60.7Ð95.5)a 151.1 (105.7Ð204.5)b
Plastic jar 37.5 (23.0Ð55.5) 0.5 (0.5Ð4.6)b 32.5 (22.2Ð44.8)b 280.3 (217.1Ð351.5)a
120 weekly 30.0 (16.6Ð47.2) 30.6 (15.7Ð50.5)ab 45.9 (31.3Ð63.2)b 203.1 (144.9Ð271.0)b
360 weekly 40.6 (24.8Ð60.3) 40.0 (22.8Ð62.4)a 94.8 (75.2Ð119.1)a 325.2 (250.3Ð409.9)a
360 not replaced 29.9 (16.6Ð47.1) 11.8 (3.5Ð25.1)b 27.3 (16.4Ð41.0)b 126.9 (81.9Ð181.6)b
Biobest 120 weekly 36.2 (18.9Ð59.1)ab 102.4 (64.9Ð148.4)ab 78.6 (52.0Ð110.7) 161.5 (97.1Ð242.2)
360 weekly 24.4 (10.7Ð43.6)b 151.5 (104.9Ð206.5)a 134.2 (98.6Ð175.3) 223.9 (146.7Ð317.4)
360 not replaced 28.1 (13.2Ð48.6)b 35.9 (15.4Ð64.9)b 34.8 (18.0Ð57.0) 84.7 (40.3Ð145.3)
Plastic jar 120 weekly 24.3 (10.6Ð43.5)b 0.9 (1.2Ð9.1)c 21.9 (9.1Ð40.1) 249.4 (167.4Ð347Ð6)
360 weekly 60.9 (37.7Ð89.7)a 0.1 (3.0Ð5.8)c 62.2 (38.8Ð91.0) 177.7 (333.1Ð573.9)
360 not replaced 31.7 (15.7Ð53.3)b 0.8 (1.4Ð8.7)c 20.7 (8.4Ð38.5) 445.4 (109.8Ð261.9)
Trap type F
1,20
P1.6 0.226 127.9 ⬍0.0001 21.9 0.0001 17.9 0.0004
Amount F
2,20
P1.1 0.339 5.0 0.018 16.2 ⬍0.0001 13.8 0.0002
Trap ⫻amt F
2,20
P4.2 0.029 6.6 0.006 1.8 0.1935 0.7 0.495
Means in the same column with the same letter are not signiÞcantly different, TukeyÕs HSD test,
␣
⫽0.05.
a
NitidulidaeÑ96.6%; Other ColeopteraÑ3.4%.
b
Large: CalliphoridaeÑ91.6%; ApidaeÑ1.8%; LepidopteraÑ0.8%; Other DipteraÑ5.8%.
c
Medium: Muscidae and AnthomyiidaeÑ55.2%; AnisopodidaeÑ44.8%.
d
Small: Drosophila spp.Ñ49.6%; ChloropidaeÑ25.4%; ScatopsidaeÑ9.8%; SciaridaeÑ8.0%; Proctotrupidae and BraconidaeÑ2.3%; Other
DipteraÑ4.9%.
2116 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 107, no. 6
traps placed above foliage compared with yellow or
other colored traps placed within the crop canopy.
An ideal trap should also be cost-effective, easy-to-
use, and durable. The commercial traps cost more
(Contech Fruit Fly Trap: $5 CDN, Biobest Droso
Trap: $6.50 CDN) than the materials plus labor costs
for our homemade traps (materials for deli-cup trap
with large holes and mesh: $0.40 CDN, plastic jar trap:
$2 CDN; labor is $0.17 CDN per trap for both types at
20 traps made per hour and $10 per hour). Despite
being cost-efÞcient, deli-cup traps with two plastic ties
were not as easy to hang from branches or stakes than
traps with a single plastic tie. Plastic deli-cups also
become brittle, and traps are not reusable after a
season, unlike commercial traps. The homemade, plas-
tic jar traps are durable, except red plastic plates used
as covers cracked and red tape faded, thus requiring
replacement each season. ModiÞcation to some com-
mercial traps have been made since these experiments
were conducted, which may have improved trap ef-
Þciency. However, we recommend that the plastic jar
trap or very similar designs be used for future D.
suzukii trapping, based on its performance in 2013
experiments, ease-of-use (to service trap, jar can be
unscrewed from lid without removing plastic tie from
branch or stake), relative durability, ability to hold a
large volume of attractant, and moderate price. Fur-
thermore, the relative efÞcacy of these traps at low D.
suzukii levels suggests that they may be suitable for use
in early detection of D. suzukii as well as for population
monitoring to time pest management actions.
In conclusion, traps for D. suzukii should maximize
entry area, although designs with large containers and
large entry areas (⬇350 mm
2
) will likely not be im-
proved by further increasing the entry area. Attractant
surface area should also be maximized (Lee et al.
2013) and is likely more important than other trap
features (e.g., headspace volume) in affecting D. su-
zukii captures, at least in smaller traps like those tested
in this study. Larger traps are advantageous, as they
can hold more liquid attractant, resulting in greater
captures, reduced servicing time, or both, but large
holes in large traps should be covered with mesh to
exclude larger-bodied by-catch. However, certain fea-
tures of large traps, particularly the large headspace
volume in the Biobest traps evaluated herein, may
facilitate D. suzukii survival in and eventual escape
from traps. Captures of D. suzukii were greater in red
or black compared with yellow or clear traps and in
traps with holes in lids compared with those with holes
on trap sides, but these Þndings are not consistent with
previous studies and require further testing.
Acknowledgments
We thank Contech Enterprises Inc. and Biobest Canada
Ltd. for providing traps; Scott MacSween, Jeff Tigchelaar,
Bert Andrews, Alvin Brooks, Louis Rotierre, and Anne Nau-
man for access to Þelds; Jordan Hazell, Zachariah Telfer,
Emily Anderson, Caitlyn Schwenker, Taylor LaPlante, Chris
House, Karen Heal, Angela Brommit, Kevin Reeh, and Erfan
Vafaie for technical assistance; and John Cline (University of
Guelph) for use of colorimeter. This research was funded by
the University of GuelphÐOntario Ministry of Agriculture,
Food and Rural Affairs Sustainable Production Program
awarded to R.H.H. and R.B. and a Webster Postdoctoral
Fellowship, School of Environmental Sciences, University of
Guelph, awarded to J.M.R.
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