Erythritol, an Artificial Sweetener, Is Acaricidal Against Pest Mites and Minimally Harmful to a Predatory Mite
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Journal of Economic Entomology, 114(4), 2021, 1701–1708
doi: 10.1093/jee/toab101
Advance Access Publication Date 3 June 2021
Research
Horticultural Entomology
Erythritol, an Artificial Sweetener, Is Acaricidal Against
Pest Mites and Minimally Harmful to a Predatory Mite
Rebecca A. Schmidt-Jeffris,1,3, Elizabeth H. Beers,2 Peter Smytheman,2, and
Downloaded from https://academic.oup.com/jee/article/114/4/1701/6291425 by guest on 17 October 2021
Linda Rehfield-Ray1
1
USDA-ARS, Temperate Tree Fruit and Vegetable Crop Research Unit, 5230 Konnowac Pass Road, Wapato, WA 98951, USA,
2
Washington State University, Tree Fruit Research and Extension Center, 1100 N Western Ave, Wenatchee, WA 98801, USA, and
3
Corresponding author, e-mail: rebecca.schmidt@usda.gov
Subject Editor: Surendra Dara
Received 9 February 2021; Editorial decision 27 April 2021
Abstract
Erythritol, an artificial sweetener, has shown promise as an organic, human-safe insecticide. Recently, erythritol
applications were shown to be successful at controlling pear psylla (Cacopsylla pyricola (Förster)) (Hempitera:
Psyllidae), the most important pest of pear in the Pacific Northwest, USA. Twospotted spider mite (Tetranychus
urticae Koch) (Trombidiformes: Tetranychidae) and pear rust mite (Epitrimerus pyri (Nalepa)) (Trombidiformes:
Eriophyidae) can also be highly damaging pear pests. Their common natural enemy, Galendromus occidentalis
(Nesbitt) (Mesostigmata: Phytoseiidae), can provide biological control if selective pesticides are used for
managing other pests. Through a series of bioassays, we sought to determine whether erythritol could also be
used for controlling either species of pest mite. We also examined whether erythritol had acute or sublethal
impacts on G. occidentalis, through a variety of exposure methods. Effects examined included mortality, fe-
cundity, prey consumption, and locomotion. We determined that a high concentration of erythritol (30%) had
efficacy against both pest mite species and caused arresting behavior in twospotted spider mite. Erythritol
caused little acute mortality in G. occidentalis, but did reduce fecundity and prey consumption through some
exposure methods. Through motion-capture software, we determined that this is primarily due to reduced
movement, likely caused by difficulty walking on residues and excessive grooming behavior. Because the
predatory mite non-target effects were less acute than those for the two pest mites, we concluded that eryth-
ritol could likely be integrated into pear IPM with little or no disruption of mite biological control.
Key words: erythritol, twospotted spider mite, pear rust mite, western predatory mite, pear
Erythritol is a sugar alcohol sweetener that is safe for human con- Geden 2018), and a tephritid (Anastrepha ludens) (Diaz-Fleischer
sumption (Munroe et al. 1998) and available as a certified organic et al. 2019). Recent work has demonstrated its potential for con-
food product. Erythritol has insecticidal properties and has been trolling social insects, like ants and termites (Barrett et al. 2020,
shown to cause larval and adult mortality and to decrease fecundity Caponera et al. 2020).
in Drosophila melanogaster (Baudier et al. 2014, O’Donnell et al. Consumption of erythritol may increase osmotic pressure within
2016, Sampson et al. 2017a, O’Donnell et al. 2018) and the agricul- insects, resulting in disruption of cellular processes (Choi et al.
tural pest D. suzukii (Matsumara) (Diptera: Drosophilidae) (Choi 2017, Tang et al. 2017). In a mosquito, it was found to reduce
et al. 2017, Goffin et al. 2017, Sampson et al. 2017a, b, Tang et al. stored glycogen and lipid levels, alter gene expression, and impact
2017, Choi et al. 2019). It may also act as a D. suzukii oviposition protein glycosylation (Sharma et al. 2020). Erythritol consumption
repellent (Goffin et al. 2017). A field study found that erythritol by insects can also cause excessive regurgitation (Diaz-Fleischer et al.
reduced D. suzukii larval populations by 75% in blueberry and 2019) and reduced motor coordination (Baudier et al. 2014, Wentz
blackberry (Sampson et al. 2017b). Erythritol is toxic to mosquitoes et al. 2020).
(Gilkey et al. 2018, Sharma et al. 2020), filth flies (Musca domestica A recent study demonstrated that erythritol is also toxic to pear
and Stomoxys calcitrans) (Burgess and King 2017, Burgess and psylla (Cacopsylla pyricola (Förster)) (Hempitera: Psyllidae), a
Published by Oxford University Press on behalf of Entomological Society of America 2021. 1701
This work is written by (a) US Government employee(s) and is in the public domain in the US.1702 Journal of Economic Entomology, 2021, Vol. 114, No. 4
piercing-sucking, phloem-feeding pest (Wentz et al. 2020). Toxicity oc- This is the first study to document the efficacy of erythritol
curred when erythritol was provided in a liquid diet and when adults against a non-insect arthropod and the first to examine potential
or nymphs were placed on treated leaves. Erythritol applications to non-target effects on a natural enemy. Through a series of laboratory
pear trees reduced pear psylla nymph populations to one-third the level bioassays, we sought to determine if erythritol could be an effective
of the control (Wentz et al. 2020). This is promising, as new tactics option for either twospotted spider mite or pear rust mite manage-
are needed for managing pear psylla, the most important pest of pear ment. Because biological control is a critical component of mite
in the Pacific Northwest. Pear psylla cause fruit russet (small brown management in tree fruit, we also examined whether erythritol was
spots), defoliation, stunting, and even tree death (Alston and Murray harmful to G. occidentalis and if so, by which routes of exposure.
2007). Half of all pear pest management costs are due to pear psylla Because previous work with erythritol indicates intoxication occurs
control efforts (Gallardo et al. 2016). Pear psylla are also known to rap- through feeding, we hypothesized that the two pest mite species
idly develop insecticide resistance (Madsen and Morgan 1970, Alston would have increased mortality following erythritol treatments, and
and Murray 2007, Thompson et al. 2019) and all currently registered that mortality in G. occidentalis would be confined to treatments
pear psylla control materials are limited in efficacy (Courtney 2017). where they were fed erythritol-contaminated prey.
Despite psylla spray budgets that have doubled in recent years ($1,000
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to $2,000/acre), growers are seeing the highest psylla pressure in over a
decade (Dupont 2019). Materials and Methods
After pear psylla, spider mites (primarily Tetranychus urticae
Erythritol
Koch, Trombidiformes: Tetranychidae) and pear rust mite
In all assays described below, food-grade erythritol (Pyure Brands,
(Epitrimerus pyri (Nalepa)) (Trombidiformes: Eriophyidae) are the
LLC, Naples, FL) was mixed with water to make the appropriate
next most challenging pear pests in the Pacific Northwest. Mite
concentration solution (% w/v). Concentrations tested (5%, 15%,
feeding removes cellular contents, including chlorophyll, resulting in
and 30%) are those examined in previous literature working with
decreased tree vigor and yield (Beers and Hoyt 1993, Oldfield et al.
orchard pests (Wentz et al. 2020).
1993). Pears can be particularly sensitive to spider mite damage;
feeding can result in pre-mature leaf drop, reduced fruit size, and
poor fruit set, resulting in reduced yield (Westigard et al. 1966, Beers Tetranychus urticae Assays
and Hoyt 1993). Spider mite outbreaks in pear are often due to non- Female T. urticae were taken from a colony originating from Cornell
target effects of insecticide applications for pear psylla management University, which has been maintained in culture for >20 yr. Mites
on mite natural enemies (Westigard 1971, Burts 1983, Riedl and were reared on potted lima bean plants (Phaseolus lunatus L.) at
Hoying 1983, Westigard et al. 1986). Spider mites are notorious for 23°C and a 16:8 L:D photoperiod. Bioassay arenas consisted of a
developing resistance to pesticides; resistance of T. urticae to 96 ac- 3.8 cm diameter bean leaf disk placed with the lower surface fa-
tive ingredients has been reported (Mota-Sanchez and Wise 2021). In cing up in a 100 ml plastic cup partially filled with moist cotton.
Pacific Northwest pear, T. urticae pesticide resistance has reached ex- Two types of assays were conducted: contact+residue and residue
treme levels (Courtney 2017), with documented resistance to many only. For the contact+residue bioassay, 10 T. urticae females were
active ingredients, including abamectin, bifenazate, etoxazole, and transferred to each leaf disk with a fine brush. Then, treatments
hexythiazox (Beers, unpublished data). Pear rust mite feeds on both were made by spraying arenas with 2 ml of the appropriate solution
the foliage and fruit; feeding on fruits results in fruit russet, causing (or water) using a laboratory sprayer (Potter Spray Tower, Burkard
fruit downgrading and yield loss (Herbert 1979, Easterbrook 1996). Scientific, London, UK) at ~45 kPA. This resulted in 2.31 mg/cm2 of
Natural enemies do not provide consistent control of pear rust wet solution. For the residue bioassay, arenas were sprayed first and
mites (Oldfield et al. 1993, Murray and DeFrancesco 2014) and or- allowed to dry for ~1 h prior to adding the 10 females. Both assays
ganic pesticide options are limited and considered fairly ineffective, tested three concentrations of erythritol (30%, 15%, and 5%) and
making organic pear rust mite management exceptionally difficult a water control and each treatment consisted of five replications of
(Murray and DeFrancesco 2014). Because of these issues, additional 10 individuals. After treatment, assays were held at 23°C and a 16:8
options for management of spider mites or rust mites, especially or- L:D photoperiod. In each assay, at 24 and 48 h after treatment, the
ganic options, are needed (Murray and DeFrancesco 2014). number of live, dead, and runoff (drowned in cotton) spider mites
The western predatory mite, Galendromus occidentalis (Nesbitt) were counted. Mites were considered dead if they were unable to
(Mesostigmata: Phytoseiidae), is the most important natural enemy move one body length forward after gentle prodding with a brush.
of pest mites in Northwest tree fruit (Schmidt-Jeffris et al. 2015, In the residue assay, the total number of T. urticae eggs laid was also
Schmidt-Jeffris et al. 2019). The key principle of integrated mite man- counted during each evaluation.
agement in apple is the conservation of G. occidentalis by limiting Impacts of erythritol residues on spider mite locomotion were
use of pesticides with non-target effects to this predator (Hoyt 1969, also assessed. Three treatments were tested: 30% erythritol, 5%
Hoy 2011). In pear, G. occidentalis tends to be present in lower erythritol, and an untreated control. Circular glass cover slips
numbers (Easterbrook 1996, Horton et al. 2002) due to the use of (1 cm diameter) were used as arenas. To improve the spread of
broad-spectrum pesticides for pear psylla management (Westigard erythritol solution on the glass surface, a non-ionic surfactant
1971). However, when selective pesticides are used, G. occidentalis is (Regulaid, KALO, Overland Park, KS) was added to erythritol so-
capable of controlling spider mites (Westigard 1971). Less is known lutions at a rate of 0.1% (w/v). Erythritol solutions or water were
about the natural enemies of pear rust mite and the role of predation applied using a fine mist spray bottle (Premium Vials, Tullytown,
in its population dynamics (Easterbrook 1996), but G. occidentalis PA). Sprays resulted in ~0.2 mg of wet residue per cover slip
can in some cases maintain populations below economic thresholds (0.05 mg/cm2). Cover slips were air dried (~1 h) after applica-
(Proverbs et al. 1975). Ideally, new pesticides adopted for pear psylla tion. In each trial, 12 cover slips were placed near each other in
or mite control would be minimally harmful to G. occidentalis, or a 4 × 3 grid on a piece of moistened filter paper in a Petri dish.
at least more harmful to pest mites than to their predator (Schmidt- The moistened filter paper was used to discourage mites from
Jeffris and Beers 2018). leaving arenas. In each trial, four cover slips from each treatmentJournal of Economic Entomology, 2021, Vol. 114, No. 4 1703
were added to the grid in a randomly assigned location. Then, arenas. The location of each egg was marked with a felt pen. One
one T. urticae female was added to each cover slip. The Petri dish female G. occidentalis was then added to each arena.
containing the coverslips was placed under a camera (GigE, Basler In all single route exposure assays, arenas were held at ~22°C,
AG, Ahrenburg, Germany) and the movement of the mites was 16:8 L:D. Female G. occidentalis were evaluated at 24 and 48 h after
recorded for 30 min. EthoVision XT 14 software (Noldus Inc., treatment for mortality, runoff, and fecundity. In the contaminated
Leesburg, VA) was used to track mite movement and determine prey assays, the number of T. urticae eggs consumed at each time
total distance traveled by each individual. Individual observations point was also recorded.
were discarded if the mite left the cover slip arena. Trials were
run until there were ≥30 valid observations per treatment. New Galendromus occidentalis Locomotion
T. urticae were used in every trial. Locomotion assays were carried out similarly to those testing
T. urticae. Here, trials consisted of four arenas tested simultaneously,
Epitrimerus pyri Assay again with the location of individual treatments randomized in each
This assay examined erythritol contact+residue exposure on pear trial. To increase contrast between the light-colored predatory mites
rust mites. Pear cv. ‘Bartlett’ leaves were collected from a research and the background, the detached head of a black foam brush (Tool
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pear orchard (Wenatchee, WA) and washed with water to remove Bench Hardware, Dollar Tree, Chesapeake, VA) was used instead of
any pesticide residues or arthropods. Leaf disks (18 mm diameter) filter paper. Trials continued until there were ≥20 valid observations
were cut from the leaves and placed on Petri dishes partially filled per treatment. New G. occidentalis were used in every trial. All other
with agar gel to help preserve leaf turgor. Pear rust mite infested aspects of the assay were identical to the T. urticae locomotion assay.
leaves were field-collected from the same orchard. Pear rust mites
were transferred individually to the leaf disks (10 mites/disk) with a Galendromus occidentalis Multiple
single bristle brush. This experiment tested three erythritol concen-
Exposure Routes
trations (30%, 15%, and 5%) and a water control. Each treatment
In this final assay, G. occidentalis were exposed to erythritol
had five replicate disks. Applications were made in the same manner
via direct contact, residues, and contaminated prey. Predatory
as the twospotted spider mite contact+residue assay. After treatment,
mites were ordered from a commercial insectary (Biotactics Inc.,
assays were held at 23°C and a 16:8 L:D photoperiod. Pear rust mite
Romoland, CA) and used upon arrival. Three concentrations of
mortality was evaluated 48 h after treatment.
erythritol (30%, 15%, and 5%) were compared to a water control,
with 30 leaf disk arenas/replicates (2.2 cm diameter) per treatment.
Galendromus occidentalis Single Exposure Routes Eight female T. urticae were added to each leaf disk and allowed to
Predators used in this experiment series were collected from an ex- oviposit for 48 h. The positions of 30 T. urticae eggs were marked
perimental apple orchard (Rock Island, WA) in August 2019 and with a felt pen and any additional eggs and all T. urticae females
kept in colony on lima bean plants infested with T. urticae. Assays were removed from the arenas. A single G. occidentalis female was
were conducted in March–April 2020. Leaf disks (2.2 cm diameter) added to each arena. At 24 and 48 h, the number of live, dead, and
were cut from lima bean leaves and placed lower-side up on water- runoff G. occidentalis and the number of eggs laid and prey con-
saturated cotton within a 14.7 ml plastic cup. In all assays, a single sumed per female was recorded. When all G. occidentalis eggs in the
G. occidentalis female was added to each arena (one replicate), with control had hatched (6 d after treatment), the numbers of hatched
20 replicates per treatment. There was a total of six experiments, and unhatched eggs were recorded.
testing three exposure routes for two concentrations (5% and 30%)
of erythritol. The three exposure routes were the following: direct
Data Analyses
contact only, residue only, and contaminated prey only. For each
All data were analyzed in SAS 9.4 (SAS Institute, Cary, NC). For
exposure method experiment, a single erythritol concentration was
all analyses except the locomotion assays, data were analyzed
tested against a water control.
using a completely randomized, generalized linear model (PROC
In the direct contact exposure assays, ~30 predatory mite fe-
GENMOD), specifying a binomial distribution for mortality, runoff,
males were added to a 3.5 cm leaf disk placed on water saturated
prey consumption, and egg hatch data (dead/total, runoff/total, and
cotton within a plastic cup (14.7 ml). Galendromus occidentalis
eggs consumed/total eggs, respectively) and a Poisson distribution for
were sprayed with the appropriate solution of erythritol or water
oviposition data (eggs laid/live female). For the locomotion assays,
using a cooking oil sprayer (Fox Run, Bucks County, PA). This re-
data were analyzed using a generalized linear mixed model (PROC
sulted in ~10 mg of solution per leaf disk. Predatory mites were
GLIMMIX), with treatment as the fixed effect and trial number as
examined for spray droplets under a dissecting microscope; indi-
the random effect. To meet model assumptions, total distance trav-
viduals with observable residue on their bodies were transferred
elled was square root transformed. For all analyses, when the overall
individually to untreated arenas until all 20 replicates contained a
model was significant (P < 0.05) and there were more than two treat-
G. occidentalis female.
ments being compared, means were separated using least-squares
In the residue only exposure assays, 20 of the 2.2 cm diameter
means with a Tukey–Kramer adjustment (P < 0.05).
leaf disk arenas were created and sprayed with the appropriate solu-
tion of erythritol with the oil sprayer. Residues were air dried for ~4
h. Then, a single female G. occidentalis was added to each leaf disk.
Results
In the assays with contaminated prey, ~50 female T. urticae were
added to a 3.5 cm bean leaf disk arena and allowed to oviposit for Tetranychus urticae Assays
3 d. Then, female T. urticae were removed from the disk. The leaf There was a significant difference in mortality between treatments in
disk was then dipped in the appropriate concentration of erythritol T. urticae mortality when exposed to erythritol via contact+residues
or water. Before residues were dry, 10 T. urticae eggs of the appro- at 24 (χ2 = 32.59; df = 3; P < 0.0001) and 48 h (χ2 = 45.66; df = 3;
priate treatment were added to each of 20 untreated 2.2 cm leaf disk P < 0.0001). At both 24 and 48 h, T. urticae mortality was higher1704 Journal of Economic Entomology, 2021, Vol. 114, No. 4
in the 30% erythritol treatment than the two lower concentrations, or residue treatments at either concentration tested. However, there
which did not differ from the control or each other (Fig. 1). Mortality was a trend for twofold higher fecundity in the control in both the
reached 60% in the 30% erythritol treatment at 48 h. Only one in- 30% contact and 30% residue assays at 48 h (Table 1). In the 5%
dividual was documented as ‘runoff’ during this assay, and there- erythritol exposure via contaminated prey assay, fecundity was sig-
fore, treatment was not significant at 24 or 48 h (χ2 = 2.79; df = 3; nificantly higher (2–3×) in the control versus the treatment on both
P = 0.4255; statistical results were the same on both evaluations). evaluation dates (Table 1). Fecundity did not differ between the
There was not a significant difference in mortality between treat- treatment and control in the 30% erythritol exposure via contamin-
ments in T. urticae mortality when exposed to erythritol via residues ated prey assay. There were no differences in the percent prey con-
only at 24 (χ2 = 2.79; df = 3; P = 0.4247) or 48 h (χ2 = 3.47; df = 3; sumption in either contaminated prey assay at 24 or 48 h.
P = 0.3252). Mortality remained low in all treatments throughout
the assay, with 0–2% mortality at 24 h and 0–4% mortality at 48 h Galendromus occidentalis Locomotion
(data not shown). Similarly, there were no differences in runoff at Distance travelled by G. occidentalis in 30 min significantly differed
either time point h (χ2 = 2.79; df = 3; P = 0.4255; statistical results between the three treatments (F2,42 = 16.10; P < 0.0001). Individuals
were the same on both dates). Again, only one individual was ob- in the control traveled five times the distance as those in either the
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served as runoff. Fecundity also did not differ between treatments at 30% or 5% erythritol treatments, which did not differ from each
either 24 (χ2 = 2.02; df = 3; P = 0.5684) or 48 h (χ2 = 5.05; df = 3; other (Fig. 4).
P = 0.1682). Across treatments, females laid 3.6 ± 0.4 eggs per day.
Distance travelled by T. urticae in 30 min significantly differed
Galendromus occidentalis Multiple
between the three treatments (F2,63 = 15.29; P < 0.0001). The control
Exposure Routes
treatment T. urticae travelled the greatest distance, 30% erythritol
Mortality did not differ between any of the treatments at 24
treatment spider mites the least distance, and the 5% erythritol treat-
(χ2 = 5.98; df = 3; P = 0.1124) or 48 h (χ2 = 6.51; df = 3; P = 0.0891).
ment was intermediate (Fig. 2).
There was a trend for higher mortality in the erythritol treatments
Epitrimerus pyri Assay
There was a significant difference in mortality between treatments in
E. pyri mortality (χ2 = 57.39; df = 3; P < 0.0001). The 30% treatment
had the highest mortality (~80%) and did not significantly differ
from the 15% treatment (Fig. 3). Mortality was significantly lower
in the 5% treatment than the 30% treatment, but did not differ from
the 15% treatment. Control E. pyri mortality was significantly lower
than all of the erythritol treatments (Fig. 3).
Galendromus occidentalis Single Exposure Route
There were no significant differences in mortality or runoff at either
concentration tested via the three exposure routes compared to their
appropriate controls (Table 1). Mortality was 0–5% in all assays.
There was a trend for higher runoff in the control compared to the
direct contact and residue treatments, but this difference was never
statistically significant (Table 1). There were no differences in fe-
cundity between the treatments and the control in the direct contact Fig. 2. Mean (± SE) distance traveled (cm) by T. urticae in 30 min while
walking on two concentrations of dried erythritol residues or an untreated
control. Treatments marked with the same letter were not statistically
different (P < 0.05).
Fig. 1. Mean (± SE) percent mortality of T. urticae exposed to three
concentrations of erythritol or a water control by contact+residue. Treatments Fig. 3. Mean (± SE) percent mortality of E. pyri exposed to three concentrations
marked with the same letter within an evaluation period were not statistically of erythritol or a water control by contact+residue. Treatments marked with
different (P < 0.05). the same letter were not statistically different (P < 0.05).Journal of Economic Entomology, 2021, Vol. 114, No. 4 1705
Table 1. Percent mortality, runoff, fecundity (eggs/live female), and percent T. urticae prey consumed for G. occidentalis females exposed
to two concentrations of erythritol via three different routes, at 24 and 48 h after exposure
24 h 48 h
Eggs/live % Prey Eggs/live % Prey
Treatment n % Mortality % Runoff female consumed n % Mortality % Runoff female consumed
5% Direct 20 0 5 0.79 ± 0.22 - 20 5 25 0.71 ± 0.27 -
Control 20 0 5 0.69 ± 0.20 - 20 0 25 1.00 ± 0.29 -
χ2 0.00 2.18 0.12 1.41 0.00 0.69
P 1.0000 0.1394 0.7267 0.2347 1.0000 0.4056
5% Residue 20 0 5 0.74 ± 0.20 - 20 0 10 0.78 ± 0.22 -
Control 20 0 15 0.71 ± 0.21 - 20 0 15 0.76 ± 0.22 -
χ2 0.00 1.16 0.01 0.00 0.23 0
P 1.0000 0.2820 0.9131 1.0000 0.6316 0.9646
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5% Contam- 19 0 5 0.28 ± 0.14 37 ± 5 20 0 10 0.67 ± 0.28 57 ± 8
inated prey
Control 20 0 0 0.85 ± 0.23 43 ± 5 20 0 10 1.61 ± 0.46 60 ± 8
χ2 0.00 1.47 5.23 1.32 0.00 0.00 7.27 0.29
P 1.0000 0.2260 0.0222 0.2512 1.0000 1.0000 0.0070 0.5926
30% Direct 19 0 11 0.25 ± 0.10 - 19 0 16 0.30 ± 0.13
Control 20 0 20 0.44 ± 0.17 - 20 0 20 0.65 ± 0.21
χ2 0.00 0.68 1.05 0.00 0.12 2.42
P 1.0000 0.4081 0.3053 1.0000 0.7315 0.1200
30% Residue 20 0 0 0.24 ± 0.16 - 20 0 0 0.25 ± 0.17 -
Control 20 0 10 0.31 ± 12 - 19 0 11 0.69 ± 0.22 -
χ2 0.00 2.88 0.18 0.00 2.99 3.4
P 1.0000 0.0898 0.6712 1.0000 0.0838 0.0653
30% Contam- 20 0 5 0.89 ± 0.20 42 ± 7 20 0 15 1.53 ± 0.33 56 ± 9
inated prey
Control 20 0 15 0.76 ± 0.25 32 ± 5 20 0 15 1.47 ± 0.45 53 ± 7
χ2 0.00 1.16 0.18 3.26 0.00 0.02 0.02 0.30
P 1.0000 0.2820 0.669 0.0801 1.0000 0.8886 0.8886 0.5861
Each route and concentration combination was tested against its own control. Degrees of freedom = 1 in all tests.
(χ2 = 1,286; df = 3; P < 0.0001) and 48 h (χ2 = 1,400; df = 3;
P < 0.0001; Fig. 5B). Fecundity was also significantly higher in
the control than the three erythritol treatments at 24 (χ2 = 24.50;
df = 3; P < 0.0001) and 48 h (χ2 = 68.99; df = 3; P < 0.0001; Fig.
5C). Egg hatch was 100% in all treatments.
Discussion
This is the first study to document pesticidal activity of erythritol
to any non-insect arthropod. Our bioassay results suggest that this
may be effective as a method for controlling plant-feeding mites, but
the physiological mechanism of toxicity is unknown. Erythritol may
be absorbed by plant cells (Collander 1937) and spider mites and
rust mites feed on plant cell contents (Schmidt-Jeffris et al. 2019).
However, there was virtually no T. urticae mortality when solely
Fig. 4. Mean (± SE) distance traveled (cm) by G. occidentalis in 30 min while exposed to dry erythritol residues; all mortality occurred in the
walking on two concentrations of dried erythritol residues or an untreated ‘contact+residue’ assay, where pest mites had the ability to directly
control. Treatments marked with the same letter were not statistically ingest erythritol or absorb it through their cuticle. Effects on spider
different (P < 0.05). mite locomotion were even observed in a short period of time on
glass disks with dried residues. It is unlikely that mites were able
than the control (Fig. 5A). Runoff did not differ between any to feed on erythritol in this situation. This suggests that impacts on
of the treatments at 24 (χ2 = 2.84; df = 3; P = 0.4197) or 48 h mites may also be due to inert effects of residues, as opposed to
(χ2 = 2.88; df = 3; P = 0.4106) and only two runoff individ- chemical activity. Particle films, such as kaolin, can reduce spider
uals were observed. Percent prey consumption was significantly mite populations on plants and cause difficulty moving (Glenn et al.
higher in the control than the three erythritol treatments at 24 1999); it is possible that the dried erythritol residues caused similar1706 Journal of Economic Entomology, 2021, Vol. 114, No. 4
prey, and this was the only treatment where the predator was con-
fined to an arena with fresh, undried residues. Indeed, the few dead
individuals observed in this assay seemed to have gotten stuck in
wet residues while walking. Therefore, there is little evidence that
acute mortality would occur in a field application, where there are
likely to be untreated surfaces.
The negative sublethal effects of erythritol to G. occidentalis ap-
peared to stem from reduced movement. G. occidentalis movement
was five times lower in the erythritol treatments than the control in
the locomotion study. Runoff in the residue-only and direct contact-
only assays was notably high, likely due to the lack of prey, but in
the residue-only assays, runoff tended to be higher in the control.
This provides further evidence that G. occidentalis decrease move-
ment on erythritol residues. Reduced movement may have also re-
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sulted in decreased prey consumption and oviposition in the multiple
exposure route assay. In the single exposure route assays, sublethal
effects primarily occurred when G. occidentalis were provided with
T. urticae eggs contaminated with 5% erythritol, resulting in >50%
reduction in fecundity. However, this trend was not seen in the assay
testing 30% erythritol. We speculate that it may have been easier for
G. occidentalis to avoid the erythritol residues on the eggs treated
with 30% erythritol; the crystals left on the dried eggs were larger
and more clumped together in that treatment. However, further in-
vestigation would be needed to adequately test this. These results
indicate consumption of contaminated prey may be a potential
route of erythritol sublethal toxicity for G. occidentalis, but more
long-term studies and field trials should be conducted to determine
if this would significantly impact biological control. There was also
a >60% decrease in fecundity when G. occidentalis were exposed
to dried residues of 30% erythritol, which was marginally signifi-
cant. This may be due to reduced movement to search for ovipos-
ition sites. Because no prey were provided in this assay, differences
between fecundity in the control and the erythritol treatment cannot
be explained by reduced prey-finding or consumption due to eryth-
ritol applications. Despite these potential sublethal effects, the low
level of G. occidentalis mortality following erythritol exposure, com-
pared to the much higher levels of T. urticae and E. pyri mortality,
indicates that erythritol may be favorable for maintaining mite bio-
logical control (Schmidt-Jeffris and Beers 2018). Given that these
trials were conducted on small arenas, and in most cases, not on pear
foliage, field studies will be needed to determine how both efficacy
and non-target effects of erythritol scale up to a level relevant for
Fig. 5. Response of G. occidentalis females to exposure to three pest management.
concentrations of erythritol or a water control through contact+residue Erythritol may also be much less likely to cause a pest mite out-
exposure and feeding on contaminated prey at 24 and 48 h after treatment. break than the pesticides most commonly used for pear psylla and
(A) percent mortality, (B) mean (± SE) percent prey consumed by live females,
rust mite management. Currently, pear psylla management relies pri-
(C) mean (± SE) eggs laid by live females. Treatments marked with the same
marily on malathion, chlorpyrifos, lambda-cyhalothrin, spinetoram,
letter within an evaluation period were not statistically different (P < 0.05).
and novaluron (DuPont and Strohm 2020, Nottingham and Beers
2020). Malathion and chlorpyrifos are organophosphates, a chem-
effects. Further work is needed to both ascertain the mechanism of ical class toxic to a variety of natural enemies (Bartlett 1968, Hassan
erythritol toxicity in plant-feeding mites and to determine if eryth- et al. 1988, Theiling and Croft 1988). Pyrethroids, including lambda-
ritol solutions are an effective control method in the field. cyhalothrin, are well known for causing high levels of acute mor-
This is also the first study to examine the non-target effects of tality in G. occidentalis and other natural enemies, and disrupting
erythritol on a natural enemy. The only other non-pest species that orchard biological control (Croft 1990, Hamby et al. 2013, Beers
has been tested is the honey bee (Apis mellifera L.) (Choi et al. and Schmidt 2014, Shearer et al. 2016). Spinetoram is not only
2019). This study found no decrease in worker bee longevity when toxic to G. occidentalis (Lefebvre et al. 2011, Beers and Schmidt
fed erythritol solutions for 9 h, compared to water only or su- 2014, Schmidt-Jeffris and Beers 2015), but also reduces popula-
crose solutions. Erythritol also appears to be minimally harmful to tions of Trechnites spp., the key parasitoid of pear psylla (Shearer
G. occidentalis. None of the single methods of exposure (direct con- et al. 2016). Although novaluron does not cause substantial mor-
tact, dry residues, or contaminated prey), resulted in any mortality. tality in G. occidentalis adults (Schmidt-Jeffris and Beers 2015), it
There was a numerical (nonsignificant) increase in mortality when does cause juvenile mortality and reductions in oviposition and egg
G. occidentalis were exposed by contact+residues+contaminated hatch (Lefebvre et al. 2011, Beers and Schmidt 2014), and can resultJournal of Economic Entomology, 2021, Vol. 114, No. 4 1707
in pest mite outbreaks (Martinez-Rocha et al. 2008). Novaluron is Baudier, K. M., S. D. Kaschock-Marenda, N. Patel, K. L. Diangelus,
also harmful to key pear psylla natural enemies, such as Chrysoperla S. O’Donnell, and D. R. Marenda. 2014. Erythritol, a non-nutritive sugar
carnea and Deraeocoris brevis (Mills et al. 2016). While some acari- alcohol sweetener and the main component of Truvia®, is a palatable in-
gested insecticide. PLoS One. 9: e98949.
cides for T. urticae control are minimally harmful to G. occidentalis
Beers, E. H., and S. C. Hoyt. 1993. Twospotted spider mite, pp. 130–132. In
(Irigaray and Zalom 2007, Schmidt-Jeffris and Beers 2015,
E. H. Beers, J. F. Brunner, M. J. Willett and G. M. Warner (eds.), Orchard
Schmidt-Jeffris et al. 2015), those that control rust mites (sulfur,
Pest Management: A Resource Book for the Pacific Northwest. Good Fruit
abamectin, fenpyroximate, pyridaben, fenbutatin oxide) are known Grower, Yakima, WA.
to be harmful to predatory mites (Asselbergs et al. 1998, Irigaray Beers, E. H., and R. A. Schmidt. 2014. Impacts of orchard pesticides on
and Zalom 2006, Irigaray et al. 2007, Park et al. 2011, Beers and Galendromus occidentalis: lethal and sublethal effects. Crop Prot. 56:
Schmidt 2014, Bergeron and Schmidt-Jeffris 2020). Future studies 16–24.
should compare erythritol efficacy to conventional insecticides and Bergeron, P. E., and R. A. Schmidt-Jeffris. 2020. Not all predators are equal:
acaricides in the field and not only examine impacts on pear psylla miticide non-target effects and differential selectivity. Pest Manag. Sci. 76:
and pest mite populations, but also natural enemies. The lack of re- 2170–2179.
Burgess, E. R. I., and C. J. Geden. 2018. Larvicidal potential of the polyol
ported pest mite outbreaks in erythritol field trials testing efficacy on
sweeteners erythritol and xylitol in two filth fly species. J. Vector Ecol.
Downloaded from https://academic.oup.com/jee/article/114/4/1701/6291425 by guest on 17 October 2021
pear psylla (Wentz et al. 2020) provides good preliminary evidence
44: 11–17.
that this product does not disrupt biological control.
Burgess, E. R., 4th, and B. H. King. 2017. Insecticidal potential of two sugar
Many other crops besides pear also have spider mite outbreaks alcohols to Musca domestica (Diptera: Muscidae). J. Econ. Entomol. 110:
when chemical applications for control of key pests harm predatory 2252–2258.
mite populations. Erythritol may provide pest control that is less dis- Burts, E. C. 1983. Effectiveness of a soft-pesticide program on pear pests. J.
ruptive to mite biological control than current practices. For instance, Econ. Entomol. 76: 936–941.
erythritol is effective against the invasive D. suzukii (Sampson et al. Caponera, V., M. Barrett, D. R. Marenda, and S. O’donnell. 2020. Erythritol
2017b), which attacks soft fruit crops. Pesticides currently recom- ingestion causes concentration-dependent mortality in eastern subter-
mended for D. suzukii control are broad-spectrum: spinosyns, or- ranean termites (Blattodea: Rhinotermitidae). J. Econ. Entomol. 113:
348–352.
ganophosphates, pyrethroids, and neonicotinoids (Walsh et al. 2011,
Choi, M. Y., S. B. Tang, S. J. Ahn, K. G. Amarasekare, P. Shearer, and J. C. Lee.
Haviland and Beers 2012), all of which are known for non-target
2017. Effect of non-nutritive sugars to decrease the survivorship of spotted
effects on natural enemies. Use of these insecticides has disrupted
wing drosophila, Drosophila suzukii. J. Insect Physiol. 99: 86–94.
the previously existing pest management programs in soft fruit crops Choi, M. Y., H. Lucas, R. Sagili, D. H. Cha, and J. C. Lee. 2019. Effect of
where D. suzukii has established (Lee et al. 2019, Stockton et al. erythritol on Drosophila suzukii (Diptera: Drosophilidae) in the presence
2021). If erythritol applications can be successfully incorporated of naturally-occurring sugar sources, and on the survival of Apis mellifera
into D. suzukii pest management, outbreaks of mites might decrease. (Hymenoptera: Apidae). J. Econ. Entomol. 112: 981–985.
In cropping systems where mites are secondary pests, efficacy of Collander, R. 1937. The permeability of plant protoplasts to non-electrolytes.
erythritol against key pests and the non-target effects on important Trans. Faraday Soc. 33: 985–990.
predatory mites should be explored. Research on other natural en- Courtney, R. 2017. Pear psylla, just like spider mites, showing resist-
ance to pesticides Good Fruit Grower. https://www.goodfruit.com/
emies and pollinators will be crucial to integrating erythritol into
pear-psylla-just-like-spider-mites-showing-resistance-to-pesticides/.
integrated pest management.
Croft, B. A. 1990. Pesticide selectivity: pyrethroids, pp. 335–353. Arthropod
biological control agents and pesticides. John Wiley & Sons, New York,
NY.
Acknowledgments Diaz-Fleischer, F., J. Arredondo, R. Lasa, C. Bonilla, D. Debernardi, D. Perez-
The authors gratefully acknowledge the technical support of Staples, and T. Williams. 2019. Sickly sweet: insecticidal polyols induce
P. Bergeron, E. Moretti, and K. Thomsen-Archer. We also thank lethal regurgitation in dipteran pests. Insects 10: 53.
Dupont, S. T. 2019. Moving toward bio-based IPM in
W.R. Cooper and L. Nottingham for helpful comments on an
pears. Good Fruit Grower. https://www.goodfruit.com/
earlier draft of the manuscript. This work was supported by
dupont-moving-toward-bio-based-ipm-in-pears/.
funding from the Fresh and Processed Pear Research Committees.
DuPont, S. T., and C. J. Strohm. 2020. Integrated pest management pro-
The use of trade, firm, or corporation names in this publication is grammes increase natural enemies of pear psylla in Central Washington
for the information and convenience of the reader. Such use does pear orchards. J. Appl. Entomol. 144: 109–122.
not constitute an official endorsement or approval by the United Easterbrook, M. A. 1996. 3.2.2 Damage and control of eriophyoid mites in
States Department of Agriculture or the Agricultural Research apple and pear, pp. 527–541. In E. E. Lindquist, M. W. Sabelis and J. Bruin
Service of any product or service to the exclusion of others that (eds.), Eriophyid mites—their biology, natural enemies and control, vol. 6.
may be suitable. Elsevier Science, Amsterdam, Netherlands.
Gallardo, R. K., J. F. Brunner, and S. Castagnoli. 2016. Capturing the eco-
nomic value of biological control in western tree fruit. Biol. Control. 102:
93–100.
References Cited
Gilkey, P. L., D. T. Bolshakov, J. G. Kowala, L. A. Taylor, S. O’Donnell,
Alston, D. G., and M. Murray. 2007. Pear psylla (Cacopsylla pyricola), Utah D. R. Marenda, and L. K. Sirot. 2018. Lethal effects of erythritol on the
Pests Fact Sheets. Utah State University. ENT-62-07. mosquito Aedes aegypti Linnaeus (Diptera: Culicidae). J. Appl. Entomol.
Asselbergs, D. J. M., S. van Nierop, P. A. Oomen, and P. F. J. Oostelbos. 1998. 142: 873–881.
Effects of active substances of plant protection products on biological con- Glenn, D. M., G. J. Puterka, T. Vanderzwet, R. E. Byers, and C. Feldhake.
trol agents used in glasshouses. OEPP/EPPO Bullentin 28: 425–431. 1999. Hydrophobic particle films: a new paradigm for suppression of
Barrett, M., V. Caponera, C. McNair, S. O’Donnell, and D. R. Marenda. 2020. arthropod pests and plant diseases. J. Econ. Entomol. 92: 759–771.
Potential for use of erythritol as a socially transferrable ingested insecticide Goffin, J., N. Gallace, N. Berkvens, H. Casteels, M. De Ro, D. Bylemans, and
for ants (Hymenoptera: Formicidae). J. Econ. Entomol. 113: 1382–1388. T. Beliën. 2017. Toxicity of erythritol, a sugar alcohol and food additive,
Bartlett, B. R. 1968. Outbreaks of two-spotted spider-mites and cotton aphids to Drosophila suzukii (Matsumara). Acta Hort. 1156: 843–848.
following pesticide treatment. I. Pest stimulation vs natural enemy destruc- Hamby, K. A., J. A. Alifano, and F. G. Zalom. 2013. Total effects of contact
tion as the cause of outbreaks. J. Econ. Entomol. 61: 297–303. and residual exposure of bifenthrin and λ-cyhalothrin on the predatory1708 Journal of Economic Entomology, 2021, Vol. 114, No. 4
mite Galendromus occidentalis (Acari: Phytoseiidae). Exp. Appl. Acarol. G. M. Warner (eds.), Orchard pest management: a resource book for the
61: 183–193. Pacific Northwest. Good Fruit Grower, Yakima, WA.
Hassan, S. A., F. Bigler, H. Bogenschutz, E. Boller, J. Brun, P. Chiverton, Park, J. J., M. Kim, J. H. Lee, K. I. Shin, S. E. Lee, J. G. Kim, and K. Cho.
P. Edwards, F. Mansour, E. Naton, P. A. Oomen, et al. 1988. Results of the 2011. Sublethal effects of fenpyroximate and pyridaben on two predatory
fourth joint pesticide testing programme carried out by the IOBC/WPRS- mite species, Neoseiulus womersleyi and Phytoseiulus persimilis (Acari,
Working Group “Pesticides and Beneficial Organisms”. J. Appl. Entomol. Phytoseiidae). Exp. Appl. Acarol. 54: 243–259.
105: 321–329. Proverbs, M. D., J. R. Newton, D. M. Logan, and F. E. Brinton. 1975. Codling
Haviland, D. R., and E. H. Beers. 2012. Chemical control programs for moth control by release of radiation-sterilized moths in a pome fruit or-
Drosophila suzukii that comply with international limitations on pesticide chard and observations of other pests. J. Econ. Entomol. 68: 555–560.
residues for exported sweet cherries. J. Integr. Pest Manag. 3: 1–6. Riedl, H., and S. A. Hoying. 1983. Toxicity and residual activity of fenvalerate to
Herbert, H. J. 1979. Population trends and behavior of the pear rust mite, Typhlodromus occidentalis (Acari: Phytoseiidae) and its prey Tetranychus
Epitrimerus pyri (Prostigmata: Eryiophyoidea), on pears in Nova Scotia. urticae (Acari: Tetranychidae) on pear. Can. Entomol. 115: 807–813.
Can. Entomol. 111: 955–957. Sampson, B. J., C. T. Werle, S. J. Stringer, and J. J. Adamczyk. 2017a. Ingestible
Horton, D. R., D. A. Broers, T. Hinojosa, T. M. Lewis, E. R. Miliczky, and insecticides for spotted wing Drosophila control: a polyol, Erythritol, and
R. R. Lewis. 2002. Diversity and phenology of predatory arthropods an insect growth regulator, Lufenuron. J. Appl. Entomol. 141: 8–18.
overwintering in cardboard bands placed in pear and apple orchards of Sampson, B. J., D. A. Marshall, B. J. Smith, S. J. Stringer, C. T. Werle,
Downloaded from https://academic.oup.com/jee/article/114/4/1701/6291425 by guest on 17 October 2021
Central Washington State. Ann. Entomol. Soc. Am. 95: 469–480. D. J. Magee, and J. J. Adamczyk. 2017b. Erythritol and Lufenuron det-
Hoy, M. A. 2011. Integrated mite management in Washington apple orchards, rimentally alter age structure of wild Drosophila suzukii (Diptera:
pp. 237–242. Agricultural Acarology: Introduction to Integrated Mite Drosophilidae) populations in blueberry and blackberry. J. Econ. Entomol.
Management. Taylor and Francis Group, LLC, Boca Raton, FL. 110: 530–534.
Hoyt, S. C. 1969. Integrated chemical control of insects and biological control Schmidt-Jeffris, R. A., and E. H. Beers. 2015. Comparative biology and
of mites on apple in Washington. J. Econ. Entomol. 62: 74–86. pesticide susceptibility of Amblydromella caudiglans and Galendromus
Irigaray, F. J. S., and F. Zalom. 2006. Side effects of five new acaricides on occidentalis as spider mite predators in apple orchards. Exp. Appl. Acarol.
the predator Galendromus occidentalis (Acari, Phytoseiidae). Exp. Appl. 67: 35–47.
Acarol. 38: 299–305. Schmidt-Jeffris, R. A., and E. H. Beers. 2018. Potential impacts of orchard
Irigaray, F. J. S. D. C., and F. G. Zalom. 2007. Selectivity of acaricide exposure pesticides on Tetranychus urticae: a predator-prey perspective. Crop Prot.
on Galendromus occidentalis reproductive potential. Bicontrol Sci. Techn. 103: 56–64.
17: 541–546. Schmidt-Jeffris, R. A., E. H. Beers, and D. W. Crowder. 2015. Phytoseiids in
Irigaray, F. J. S., F. Zalom, and P. B. Thompson. 2007. Residual toxicity of Washington commercial apple orchards: biodiversity and factors affecting
acaricides to Galendromus occidentalis and Phytoseiulus persimilis repro- abundance. Exp. Appl. Acarol. 67: 21–34.
ductive potential. Biol. Control. 40: 153–159. Schmidt-Jeffris, R. A., E. H. Beers, and C. Duso. 2019. Insect pests of fruit:
Lee, J. C., X. Wang, K. M. Daane, K. A. Hoelmer, R. Isaacs, A. A. Sial, mites, pp. 425–451. In X. Xu and M. Fountain (eds.), Integrated man-
and V. M. Walton. 2019. Biological control of spotted-wing drosophila agement of insect pests and diseases of tree fruit. Burleigh Dodds Science
(Diptera: Drosophilidae)—current and pending tactics. J. Integr. Pest Publishing, Cambridge, UK.
Manag. 10: 13. Sharma, A., J. Reyes, D. Borgmeyer, C. Ayala-Chavez, K. Snow, F. Arshad,
Lefebvre, M., N. J. Bostanian, H. M. Thistlewood, Y. Mauffette, and A. Nuss, and M. Gulia-Nuss. 2020. The sugar substitute erythritol
G. Racette. 2011. A laboratory assessment of the toxic attributes of six ‘re- shortens the lifespan of Aedes aegypti potentially by N-linked protein
duced risk insecticides’ on Galendromus occidentalis (Acari: Phytoseiidae). glycosylation. Sci. Rep. 10: 6195.
Chemosphere. 84: 25–30. Shearer, P. W., K. G. Amarasekare, S. P. Castagnoli, E. H. Beers, V. P. Jones,
Madsen, H. F., and C. V. G. Morgan. 1970. Pome fruit pests and their control. and N. J. Mills. 2016. Large-plot field studies to assess impacts of newer
Annu. Rev. Entomol. 15: 295–320. insecticides on non-target arthropods in Western U.S. orchards. Biol.
Martinez-Rocha, L., E. H. Beers, and J. E. Dunley. 2008. Effect of pesticides Control 102: 26–34.
on integrated mite management in Washington State. J. Entomol. Soc. B.C. Stockton, D. G., A. K. Wallingford, D. H. Cha, and G. M. Loeb. 2021.
105: 1–12. Automated aerosol puffers effectively deliver 1-OCTEN-3-OL, an ovipos-
Mills, N. J., E. H. Beers, P. W. Shearer, T. R. Unruh, and K. G. Amarasekare. ition antagonist useful against spotted-wing drosophila. Pest Manag. Sci.
2016. Comparative analysis of pesticide effects on natural enemies in 77: 389–396.
western orchards: A synthesis of laboratory bioassay data. Biol. Control Tang, S. B., J. C. Lee, J. K. Jung, and M. Y. Choi. 2017. Effect of erythritol
102: 17–25. formulation on the mortality, fecundity and physiological excretion in
Mota-Sanchez, D., and J. C. Wise. 2021. The Arthropod Pesticide Resistance Drosophila suzukii. J. Insect Physiol. 101: 178–184.
Database. Michigan State University. http://www.pesticideresistance.org. Theiling, K. M., and B. A. Croft. 1988. Pesticide side-effects on arthropod nat-
Munroe, I. C., W. O. Bernt, J. F. Borzelleca, G. Flamm, B. S. Lynch, ural enemies: a database summary. Agric. Ecosyst. Environ. 21: 191–218.
E. Kennepohl, E. A. Bar, and J. Modderman. 1998. Erythritol: an inter- Thompson, A., R. Hilton, A. Kc, J. W. Pscheidt, and D. Rendon. 2019. 2019
pretive summary of biochemical, metabolic, toxicological and clinical Pest Management Guide for Tree Fruits in the Mid-Columbia Area. EM
data. Food Chem. Toxicol. 36: 1139–1174. 8203. Oregon State University.
Murray, K., and J. DeFrancesco. 2014. Pest management strategic plan for Walsh, D. B., M. P. Bolda, R. E. Goodhue, A. J. Dreves, J. Lee, D. J. Bruck,
pears in Oregon and Washington. https://ipmdata.ipmcenters.org/source_ V. M. Walton, S. D. O’Neal, and F. G. Zalom. 2011. Drosophila suzukii
list.cfm?sourcetypeid=4. (Diptera: Drosophilidae): invasive pest of ripening soft fruit expanding
Nottingham, L. B., and E. H. Beers. 2020. Management of pear psylla its geographic range and damage potential. J. Integr. Pest Manag. 2:
(Hemiptera: Psyllidae) using reflective plastic mulch. J. Econ. Entomol. G1–G7.
113: 2840–2849. Wentz, K., W. R. Cooper, D. R. Horton, R. Kao, and L. B. Nottingham. 2020.
O’Donnell, S., K. Baudier, and D. R. Marenda. 2016. Non-nutritive polyol The artificial sweetener, erythritol, has insecticidal properties against pear
sweeteners differ in insecticidal activity when ingested by adult Drosophila psylla (Hemiptera: Psyllidae). J. Econ. Entomol. 113: 2293–2299.
melanogaster (Diptera: Drosophilidae). J. Insect Sci. 16: 47. Westigard, P. H. 1971. Integrated control of spider mites on pear. J. Econ.
O’Donnell, S., K. Baudier, K. Fiocca, and D. R. Marenda. 2018. Erythritol Entomol. 64: 496–501.
ingestion impairs adult reproduction and causes larval mortality in Westigard, P. H., L. J. Gut, and W. J. Liss. 1986. Selective control program for
Drosophila melanogaster fruit flies (Diptera: Drosophilidae). J. Appl. the pear pest complex in southern Oregon. J. Econ. Entomol. 79: 250–257.
Entomol. 142: 37–42. Westigard, P. H., P. B. Lombard, and J. H. Grim. 1966. Preliminary investiga-
Oldfield, G. N., P. H. Westigard, M. Smirle, and J. E. Dunley. 1993. Pear tions of the effect of feeding of various levels of two-spotted spider mite on
rust mite, pp. 147–149. In E. H. Beers, J. F. Brunner, M. J. Willett and its Anjou pear host. Proc. Am. Soc. Hort. Sci. 89: 117–122.You can also read
