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Control of the broad mite (Polyphagotarsonemus latus (Banks)) on organic

greenhouse sweet peppers (Capsicum annuum L.) with the predatory mite,
Neoseiulus cucumeris (Oudemans)

Article  in  Biological Control · July 2003

DOI: 10.1016/S1049-9644(03)00069-0

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 Biological Control 27 (2003) 300–309
www.elsevier.com/locate/ybcon

Control of the broad mite (Polyphagotarsonemus latus (Banks))

on organic greenhouse sweet peppers (Capsicum annuum L.) with
the predatory mite, Neoseiulus cucumeris (Oudemans)
Phyllis G. Weintraub,a,* Sophia Kleitman,a Rafi Mori,a Nurit Shapira,b and Eric Palevskyc
a
Department of Entomology, Gilat Research Center, Agricultural Research Organization, D.N. Negev 85280, Israel
b
Research and Development, Sapir Center, D.N. Arava 86825, Israel
c
Department of Entomology, Agricultural Research Organization, P.O. Box 6, Bet Dagan 50250, Israel
Received 10 May 2002; accepted 20 March 2003

Abstract

The predatory mite Neoseiulus cucumeris (Oudemans) (Acarina: Phytoseiidae) successfully controlled the broad mite Poly-
phagotarsonemus latus (Banks) (Acarina: Tarsonemidae) on two varieties of greenhouse-grown sweet peppers (Capsicum annuum L.).
A survey of pre-plant seedlings showed that nurseries were a source of infestation for the broad mite. The predatory mites were
released twice (on day 1 and 5, or 15 days later) on each plant, every second plant or every fourth plant. Broad mite populations
were evaluated by sampling young leaves from the top of the plant. The effect of the broad mite on plant height, dry mass and yield
was evaluated. Additionally, since N. cucumeris is known to control thrips, Frankliniella occidentalis (Pergande) (Thysanoptera:
Thripidae), blue sticky traps and flower sampling were used to evaluate changes in thrips populations. All three release rates of N.
cucumeris significantly (P < 0:05) controlled broad mite populations, but when the predatory mites were released only on every
fourth plant, the overall height and yield of the plants were adversely affected by broad mites. Releasing N. cucumeris on each or
every second plant was as efficacious in controlling broad mites as sulfur treatments in terms of plant height, dry mass and yield.
Plants treated with sulfur, however, had significantly higher thrips populations and fruit damage.
Ó 2003 Elsevier Science (USA). All rights reserved.

Keywords: Polyphagotarsonemus latus; Broad mite; Frankliniella occidentalis; Western flower thrips; Neoseiulus cucumeris; Biological control

1. Introduction plant can cause severe damage resulting in significantly

The broad mite, Polyphagotarsonemus latus (Banks)
(Acarina: Tarsonemidae), is a serious pest in tropical
and subtropical regions including Israel and has been
collected from about 60 different plant families (Gerson,
1992). The mite, which attacks young, growing plant
parts, is very small and difficult to detect, usually feeds
on the lower leaf surface and causes leaf edges to be-
come rigid and roll under, and causes distortion and/or
discoloration of flowers and blistering of fruits. It is an
important pest of vegetables, and peppers have a par-
ticularly low tolerance for the mite (de Coss-Romero
and Pe~ na, 1998). Less than five mites on a young pepper
*
Corresponding author. Fax: +972-8-992-6485.
E-mail address: phyllisw@volcani.agri.gov.il (P.G. Weintraub).
fewer fruit per plant and lower fruit weight (Cho et al.,
1996). Furthermore, the broad mite is known to be
distributed phoretically by whiteflies (Natarajan, 1988;
Palevsky et al., 2001; Parker and Gerson, 1994).
Therefore, once the broad mite gains entry into a
greenhouse, it can spread rapidly and have severe eco-
nomic impact.
A number of predators of the broad mite have been
reported in the literature (Gerson, 1992) including
predatory phytoseiid mite species. Fan and Petitt (1994),
and Pe~ na and Obsorne (1996) have successfully con-
trolled the broad mite in greenhouses using Neoseiulus
( ¼ Amblyseius) barkeri (Hughes) and N. californicus
(McGregor) (Acarina: Phytoseiidae), respectively.
Studies have shown that some Neoseiulus spp. are sen-
sitive to low humidity levels (Bakker et al., 1993; Croft

1049-9644/03/$ - see front matter Ó 2003 Elsevier Science (USA). All rights reserved.
doi:10.1016/S1049-9644(03)00069-0
 P.G. Weintraub et al. / Biological Control 27 (2003) 300–309
et al., 1993; Shipp and van Houten, 1997). Because of
hairs, trichomes, domatia and other leaf depressions, the
microclimate of the surface of greenhouse plants is fa-
vorable for the survival of both broad mites and Neo-
seiulus spp.
Neoseiulus cucumeris (Oudemans) (Acarina: Phyto-
seiidae) is considered a polyphagous predatory mite,
feeding on a number of mites and insect species
(McMurtry and Croft, 1997). N. cucumeris has been
successfully used to control several mite species, e.g.
Phytonemus pallidus (Banks) (Tarsonemidae) on straw-
berry (Croft et al., 1998; Easterbrook et al., 2001),
Tetranychus urticae Koch (Tetranychidae) on straw-
berry (Easterbrook et al., 2001), and Aculops lycopersici
(Massee) (Eriophyidae) on tomatoes (Brodeur et al.,
1997); it has also controlled the thrips Thrips tabaci
Lindeman and Frankliniella occidentalis (Pergande)
(Thysanoptera: Thripidae) (Brodsgaard and Hansen,
1992; Gillespie and Quiring, 1992; de Courcy-Williams,
2001; Ramakers, 1988). Furthermore, N. cucumeris has
been shown to be compatible with plant growth regu-
lators (chlormequat, daminozide, and paclobutrazol) in
direct and residual treatments, as well as insecticidal
soap (up to 4%) (Oetting and Latimer, 1995) and neem
(Oetting and Latimer, 1995; Spollen and Isman, 1996).
To learn more about the ability of N. cucumeris to
control broad mites in organically grown greenhouse
sweet peppers in an arid climate, N. cucumeris were re-
leased at three densities and broad mite populations
were monitored. Effects of the broad mites on sweet
pepper growth and yield were assessed. Since N. cu-
cumeris is a known thrips predator, populations of F.
occidentalis were also monitored.
2. Materials and methods
All trials took place in the organic section of the Yair
Research and Development Farm in the Arava Valley
(Jordan Rift Valley below the Dead Sea) in Israel. Plants
were fertilized and watered according to standard or-
ganic agricultural practices for the area.
2.1. Pre-planting survey of pepper seedlings
Sweet pepper seedlings were obtained from an or-
ganic nursery each year for three consecutive years and
were used for transplanting into the field. In 1999, 50
seedlings of ÔFiestaÕ (yellow variety) and Ô107Õ seedlings
(red variety) were checked for the presence of broad
mites by cutting plants at ground level, followed by
washing in 80% EtOH. In the laboratory, the presence
and counts of mites in the washings were made using a
dissecting microscope at 25. In 2000 and 2001, ÔNiblaÕ
seedlings (yellow fruit,) and ÔParkerÕ seedlings (red fruit)
were used in the study, and 100 seedlings from each
301
variety were checked upon arrival at the research station
in both years. Groups of five plants were cut at soil level
and washed in 50 ml of 80% EtOH to remove any mites
or insects. Ethanol rinse was examined at 25 for
presence of mites and insects.
2.2. Pilot trial, 1999–2000
The first year, N. cucumeris was imported from Eu-
rope and released under quarantine conditions in only
one 7  15 m tunnel that was initially covered with 50-
mesh screening. There was one non-treated control
tunnel. Two varieties of organic sweet pepper seedlings
were planted on 29 August on 3 beds with 2 rows of
peppers; 90 ÔFiestaÕ seedlings were planted in the
southern half and 90 Ô107Õ seedlings were planted in the
northern half of each tunnel.
Koppert Biological Systems (Berkel en Rodenrijs,
The Netherlands) developed and supplied self-contained
breeding/food sachets of N. cucumeris, containing as a
food source, the storage mite Tyrophagus putrescentiae
(Schrank) and bran. On 9 November, 25 sachets, each
containing about 500 N. cucumeris, were distributed
about 2 m apart throughout the tunnel, and hung in the
upper third of the plants. Immediately before release of
the mite, the tunnel was covered with plastic and the
entrance was covered with a double layer of plastic. At
the end of the trial, all plant material from this tunnel
was burned.
Broad mite populations were monitored once a week
in each tunnel before N. cucumeris were released; 30
apical leaves (4–5 cm long) were placed individually in
tubes containing 25 ml of 80% EtOH. Once the N. cu-
cumeris were released, this tunnel was sampled twice a
week, one leaf from each of the plants on which a sachet
had been hung. Monitoring of the control tunnel re-
vealed that there was no natural infestation of broad
mites. Therefore, 25 plants, located midway between
plants in which the sachets were hung, were sampled and
served as the ‘‘control.’’ For the purpose of this trial
only, each plant was considered a replicate. The contents
of the alcohol from each sample were examined under a
dissecting microscope at 25 for the number of mites
present. At the end of the trial, two 20-plant samples of
each variety of peppers were harvested from both the
tunnels, graded and weighed.
2.3. Trials, 2000–2001 and 2001–2002
2.3.1. Experimental site and plants
Sixteen walk-in tunnels (7  15 m) were built in an
area designated for organic agriculture at the research
station. Each tunnel was covered with 50-mesh screening
and the entrances were covered with a double layer of
50-mesh screening. Tunnels were initially covered with
black shade screening (30% light exclusion), which was
302 P.G. Weintraub et al. / Biological Control 27 (2003) 300–309
later removed. Two varieties of organically grown pep-
per seedlings, ÔNiblaÕ seedlings and ÔParkerÕ seedlings
were planted in three double row beds in each tunnel on
17 September 2000 and 2 September 2001. Ninety ÔNi-
blaÕ were planted in the northern half of each tunnel and
90 ÔParkerÕ in the southern half.
2.3.2. Release of N. cucumeris
Neoseiulus cucumeris was obtained from Bio-Bee Bi-
ological Systems (Kibbutz SÕdeh Eliyahu, Israel). Re-
lease rates were as follows: every plant, every second
plant, every fourth plant, and no-release (control). In
the 2001–2002 season, a positive control (sulfur spray)
for broad mites was added to the trials. There were four
different tunnels for each treatment, and treatments were
randomly assigned to the 16 tunnels. Predator releases
were performed by placing 3 spoons of a mixture of N.
cucumeris, T. putrescentiae (at a ratio of 1:3, equivalent
of 575–600 predators/plant) on the upper-most leaves of
the plants. Release dates were 29 September and 4 Oc-
tober in 2000, and 25 September and 10 October in
2001.
2.3.3. Effect of predator releases on broad mite popula-
tions and vegetative and yield parameters of peppers
Mites were sampled once a week from designated
plants; six plants of each pepper variety were sampled
per bed. For release rates of every second plant and
every fourth plant, a middle (non-treated) plant was
sampled. One leaf (a young leaf from the top of the
plant, 5–6 cm long) from each of these six plants was
placed in a 200 ml plastic container containing 50 ml of
80% EtOH; this constituted one replicate. Each bed in
the tunnel was similarly sampled, for a total of three
replicated samples per tunnel. In the laboratory, the
leaves were removed and the contents of each container
were examined under a dissecting microscope at 25 for
presence of mites.
To measure the effect of broad mites on the pepper
plants, after broad mite populations in the treated tun-
nels were reduced to near zero, the designated sampling
plants (18 plants per variety per tunnel) were removed at
soil level. In 2000 there were severe problems with
powdery mildew (Leveillula taurica (Lev.) Arn.) and the
trial was terminated on 27 November. The height of
each plant was measured, the number of peppers greater
than 4 cm long were counted and weighed as a group,
after which the plants (without peppers) were placed in
paper bags and dried at 70 °C for at least 48 h. The dry
weight of each plant was recorded. In the 2001–2002
season, two sets of 12 plants from each variety in each
tunnel were harvested. Peppers were harvested every 10–
14 days, weighed, and graded for marketability. At the
end of the harvest, plants designated for sampling were
cut at soil level, then measured for height and dry weight
as described above.
2.3.4. Effect of N. cucumeris on thrips
Thrips (F. occidentalis) were monitored weekly with
2 blue sticky traps per tunnel and by collecting 5
flowers randomly from each bed. The flowers were
placed in a plastic container in which the bottom
consisted of loose weave screening, to support the
flowers, and a glue-coated petri dish beneath, to collect
thrips. The container was closed and a few drops of
turpentine were applied to cotton on the lid to drive the
thrips out of the flowers. A total of 15 flowers (three
replicates of 5 flowers) from each variety were collected
weekly.
2.4. Statistical analysis
Statistical analysis of the first year and yield data
were performed using CoStat Statistical Software
(Minneapolis, MN, USA). Before ANOVA was run, a
pretest to determine the homogeneity of variances
(homoscedasticity) was performed. Analysis of repli-
cates was done by completely randomized one-way
ANOVA. Means were separated by Tukey-Kramer at
a ¼ 0:05. Analysis of data from the second and third
year was performed using SAS version 8.1 software
(SAS Institute Inc. Cary, NC, USA). Data were
initially transformed (x2 ) then analyzed using
nested GLM procedure. Means were separated by
Student–Newman–Keuls test at a ¼ 0:05. Broad mite
population Ômite daysÕ were calculated as adult female
cumulative mite days (ACMDs) per sample, by accu-
mulating mite days at each sampling date as:
ACMDs ¼ ½0:5 ðmplp þ mplc Þ  dcp , where mplp was
the number of mites per leaf at the prior sampling date,
mplc was the current number of mites per leaf and dcp
was the interval of days between sampling dates (Beers
and Hull, 1990).
3. Results
3.1. Pre-planting survey of seedlings
From the first year (1999), a total of 100 seedlings
were examined before planting, and 1 broad mite and 3
thrips were found. In the second year (2000), 15 broad
mites were found on ÔParkerÕ seedlings and none on the
ÔNibla,Õ but both varieties had thrips. During planting,
broad mites were probably distributed to all ÔNiblaÕ
seedlings since, within 10 days of planting, some plants
were starting to show evidence of mite damage. We were
concerned about this large initial population; therefore,
all tunnels were sprayed with liquid sulfur 2 days before
the first N. cucumeris release to reduce populations to
more normal levels for the time of year. In the third year
(2001), no broad mites or thrips were found during the
pre-plant examination.
 P.G. Weintraub et al. / Biological Control 27 (2003) 300–309 303

3.2. Effects of N. cucumeris on broad mites
The results of the release of N. cucumeris for con-
trolling broad mites on sweet peppers for the 3 years of
these trials are shown in Figs. 1–3, respectively. In the
first year (Fig. 1) immediately after the sachets con-
taining the N. cucumeris were distributed, there was a
reduction in the number of broad mites, and by the
second sampling date (18 November) after release, there
was a significantly lower (ÔFiestaÕ P ¼ 0:0004, F ¼ 16:85,
df ¼ 1; 26; Ô107,Õ P < 0:0001, F ¼ 26:82, df ¼ 1; 24)
density of broad mites. This trend continued until the
end of the trial. Broad mites peaked at a higher density
on the yellow ÔFiestaÕ variety of sweet pepper than on the
red 107 variety.
In the second year (Fig. 2), due to high densities of
broad mites coming from the nursery, sulfur was
sprayed on all plants 2 days before the first release. N.
cucumeris was released twice (27 September and 4 Oc-
tober) at three rates. The sulfur treatment caused a rapid
decline in broad mite density. For both varieties, the
treatment in which N. cucumeris were released on every
fourth plant took the longest time to control the broad
mites. On 25 October, there were significant differences
between the control and all release rates for ÔNiblaÕ
(P < 0:0001, F ¼ 18:91, df ¼ 3; 12); the situation re-
mained the same until the end of the trial. On 1 No-
vember there were significant differences between the
control and all release rates for ÔParkerÕ (P < 0:0001,
F ¼ 31:44, df ¼ 3; 12); the situation remained the same

Fig. 1. Population dynamics of P. latus on ÔFiestaÕ (A) and Ô107Õ (B) sweet peppers after one release of N. cucumeris (arrow) in sachets, 1999. Data
points are the means from 25 leaves SEM. Solid line represents plants without sachets, dashed line represents plants with sachets.

Fig. 2. Population dynamics of P. latus on ÔNiblaÕ (A) and ÔParkerÕ (B) sweet peppers during the 2000 season after two releases of N. cucumeris
(arrows). Data points are the means of 12 6-leaf samples SEM. Nc 1 (N. cucumeris released on every plant), Nc 2 (N. cucumeris released on every
second plant), Nc 4 (N. cucumeris released on every fourth plant), and Con (non-treated control).
304 P.G. Weintraub et al. / Biological Control 27 (2003) 300–309
Fig. 3. Population dynamics of P. latus on ÔNiblaÕ (A) and ÔParkerÕ (B) sweet peppers during the 2001 season after two releases of N. cucumeris
(arrows). Data points are the means of 12 6-leaf samples SEM. Nc 1 (N. cucumeris released on every plant), Nc 2 (N. cucumeris released on every
second plant), Nc 4 (N. cucumeris released on every fourth plant), and Con (non-treated control).
until the end of the trial. At the end of the trial, the
broad mite densities in the control tunnels reached an
average of 51.3 mites/6-leaf sample on the red ÔParkerÕ
variety and 38.4 mites/6-leaf sample (populations
peaked the week before at 46.3 mites/6-leaf sample) on
the yellow ÔNiblaÕ variety. The broad mite population
on ÔParkerÕ was still increasing, while the population on
ÔNiblaÕ had started to decline.
Results from the third year (Fig. 3) show that after the
first release of N. cucumeris in all three release rates, there
was a substantial reduction in the density of broad mites
as compared to the control. In ÔNiblaÕ (Fig. 3A) 8 days
after the first release (7 October), there was a significant
difference between the control and all other treatments
(P ¼ 0:0001, F ¼ 12:38, df ¼ 3; 12). In ÔNiblaÕ 4 days
after the second release (14 October), there was a sig-
nificant difference between the control and N. cucumeris
released on every fourth plant versus N. cucumeris
released on every plant and every second plant
(P < 0:0001, F ¼ 31:72, df ¼ 3; 12); this situation re-
mained the same until the end of the trial. The density of
broad mites on ÔNiblaÕ control plants peaked on 5 No-
vember and gradually declined thereafter. On the last
sampling date (3 December), there was no significant
difference between the treatments (P ¼ 0:25). A similar
situation was seen in the ÔParkerÕ variety (Fig. 3B). In
ÔParkerÕ 4 days after the second release (14 October),
there was a significant difference between the control and
N. cucumeris released on every fourth plant versus N.
cucumeris released on every plant and every second plant
(P < 0:0001, F ¼ 42:91, df ¼ 3; 12); this situation re-
mained the same until the end of the trial. The density of
broad mites on ÔParkerÕ control plants peaked earlier, on
14 October. On the last sampling date (3 December),
there was a significant difference between the control and
all other treatments (P ¼ 0:0001, F ¼ 13:72, df ¼ 3; 12).
3.3. Effect of predator releases on broad mite populations
and vegetative and yield parameters of peppers
The parameters of plant height and dry mass were
measured to determine how the release of N. cucumeris
reduced the effects of the broad mites on pepper plants.
In the first year (1999–2000), peppers were harvested
once, and then because of quarantine restrictions, plants
were destroyed in the tunnel in which N. cucumeris were
released. Plants in the control tunnel did not have sig-
nificant broad mite populations and were not treated
against any insects; therefore, the difference in yield per
plant and weight of each fruit is attributable to factors
other than broad mite damage.
In the second year (2000–2001) (Table 1), due to se-
vere powdery mildew problems, the trials had to be
terminated early. Release of N. cucumeris on every plant
reduced the broad mite populations such that plant
height in ÔNiblaÕ increased significantly as compared to
control plants (P < 0:05). There were no differences in
the numbers of peppers produced by either variety of
pepper under any treatment regime. There were no dif-
ferences in the weights of peppers from ÔParkerÕ plants.
Height, dry weight, and yield in 2001–2002 are shown
in Table 2. For both ÔNiblaÕ and ÔParkerÕ sweet peppers,
release of N. cucumeris on every plant or every second
plant caused a decrease in broad mites and allowed
a significant increase in plant height as compared to
non-treated control plants (P < 0:001, F ¼ 77:78,
df ¼ 4; 355). ÔNiblaÕ and ÔParkerÕ plants treated with N.
cucumeris on every fourth plant were significantly
shorter than the other treatments with N. cucumeris and
the sulfur-treated control, but there was no significant
difference in the dry weight. There was no significant
difference in the amount of exportable fruit among the
treatments for either variety, although the percent of
 P.G. Weintraub et al. / Biological Control 27 (2003) 300–309 305

Table 1
Effects of broad mites on sweet pepper plants in 2000–2001a
Treatment Mite-days Height (cm) Dry wt. (g) Yield
#Peppers Pepper wt. (g)
ÔNiblaÕ
Nc 1 82.3 75.3 a 44.6 a 8.1 a 89.0 a
Nc 2 83.2 74.6 a 44.6 a 8.7 a 87.1 a
Nc 4 154.9 69.5 b 40.0 a 8.1 a 84.7 a
Control 901.8 69.7 b 43.5 a 7.8 a 79.6 a
ÔParkerÕ
Nc 1 40.4 57.2 ab 33.5 ab 7.1 a 75.7 a
Nc 2 93.3 61.5 a 36.6 a 7.4 a 81.4 a
Nc 4 101.5 52.3 b 29.7 b 7.7 a 71.7 a
Control 972.1 57.9 ab 35.4 ab 7.6 a 80.7 a
Means (based on 72 plants) within a column group followed by different letters are significantly different (P < 0:05).
a
Neoseiulus cucumeris released on every plant (Nc 1), N. cucumeris released on every second plant (Nc 2), N. cucumeris released on every fourth
plant (Nc 4), and non-treated control plants.

Table 2
Effects of the broad mite, P. latus, and thrips on sweet pepper plants in 2001–2002a
Treatment Mite-days Height Dry wt. Total days Export P. latus damage Thrips damage
(cm) (g) harvest b
No. Wt. (kg) % No. Wt. (kg) No. Wt. (kg)
ÔNiblaÕ
Nc 1 28.6 115.7 a 55.8 b 73 407 a 76.4 a 92.4 5b 1.0 b 9b 1.8 b
Nc 2 32.3 111.1 a 56.3 b 73 503 a 94.0 a 94.9 5b 1.1 b 2b 0.4 b
Nc 4 664.7 99.5 b 59.7 b 73 419 a 82.9 a 91.7 54 ab 6.8 ab 3b 0.7 b
N-t Con 1667.4 72.6 c 49.4 b 53 149 a 27.3 a 69.4 130 a 21.0 a 55 b 10.0 ab
T Con 7.3 112.1 a 179.9 a 93 525 a 101.6 a 67.9 10 b 1.9 b 155 a 32.3 a
ÔParkerÕ
Nc 1 12.5 91.7 a 44.3 b 73 556 a 98.3 a 80.3 2b 0.2 b 6b 1.1 b
Nc 2 17.6 91.0 a 41.1 b 53 545 a 93.5 a 78.4 7b 1.1 b 4b 0.7 b
Nc 4 520.2 81.4 b 38.9 b 73 549 a 101.8 a 86.3 25 b 4.1 b 14 b 2.6 b
N-t Con 1438.8 62.9 c 41.7 b 53 196 a 33.0 a 68.3 139 a 20.0 a 43 b 7.1 b
T Con 3.3 91.9 a 150.7 a 93 593 a 112.8 a 65.2 13 b 2.4 b 167 a 30.7 a
Means (height and dry weight based on 72 plants, yield based on 8 groups of 12 plants) within a column group followed by different letters are
significantly different (P < 0:05).
a
Neoseiulus cucumeris released on every plant (Nc 1), N. cucumeris released on every second plant (Nc 2), N. cucumeris released on every fourth
plant (Nc 4), non-treated control plants (N-t Con), and sulfur treated control plants (T Con).
b
Average percent of exportable peppers; mechanical or other damage not shown on table.

exportable fruit from the N. cucumeris treatments was
80–95% while that of the two controls was 65–70%.
Sweet peppers from sulfur-treated control plants were
picked for 93 days, from N. cucumeris-treated plants for
73 days, and from non-treated control plants for 53
days. In both varieties, there was significantly more fruit
damaged by broad mites in the non-treated controls
versus all other treatments, except from ÔNiblaÕ plants in
which N. cucumeris were released on every fourth plant.
3.4. Effect of N. cucumeris on thrips
The effect of N. cucumeris on thrips as observed by
blue sticky trap catches is shown in Fig. 4. In the second
year (2000–2001) (Fig. 4A), there were no significant
differences between thrips caught in tunnels from the
three release rates and the control until the week of
15–22 November. From this week until the week ending
on 10 January 2001, there were significant differences
between the number of thrips trapped in the tunnels of
the three release rates versus the control (P 6 0:001,
F ¼ 5:264–29:491, df ¼ 3; 56). There were no significant
differences between thrips trapped in the three release
rates. In the third year (2001–2002) (Fig. 4B), there were
no significant differences between thrips caught in any of
the tunnels.
The effects of N. cucumeris on thrips populations in
sweet pepper flowers are shown in Fig. 5. In 2000–2001
(Fig. 5A), there were no significant differences in the
thrips densities in flowers between the two varieties
(P ¼ 0:677). The density of thrips in all three release
rates was significantly lower than in the control from
the second sampling date (25 October, P ¼ 0:014,
F ¼ 3:661, df ¼ 3; 178) until the end of flowering. In
306 P.G. Weintraub et al. / Biological Control 27 (2003) 300–309

Fig. 4. Population dynamics of F. occidentalis from blue sticky trap catches in 2000 (A) and 2001 (B) on sweet peppers after two releases of N.
cucumeris (arrows). Data points are the means of 8 blue sticky traps per treatment or control SEM. Nc 1 (N. cucumeris released on every plant), Nc
2 (N. cucumeris released on every second plant), Nc 4 (N. cucumeris released on every fourth plant), N-t Con (non-treated control), and T Con
(sulfur–treated control).

Fig. 5. Population dynamics of F. occidentalis from flowers in 2000 (A) and 2001 (B) on sweet peppers after two releases of N. cucumeris (arrows).
Data points are the means of 12 sets of 5 flowers per treatment or control SEM. Nc 1 (N. cucumeris released on every plant), Nc 2 (N. cucumeris
released on every second plant), Nc 4 (N. cucumeris released on every fourth plant), N-t Con (non-treated control), and T Con (sulfur–treated
control).

2001–2002 (Fig. 5B), there were no significant differ-
ences in the thrips densities in flowers between the two
varieties (P ¼ 0:527). From the second through the
fourth sampling dates, there were significant differences
among the three release rates and control (P < 0:001,
F ¼ 5:67–10:985, df ¼ 3; 176–188). By the end of the
trial (the last two sampling dates), the quality and
quantity of the flowers from the control tunnels fell se-
verely as compared to the tunnels in which N. cucumeris
were released.
The number of thrips trapped on blue sticky traps
from the sulfur–treated tunnels was higher than other
treatment but not significantly so (Fig. 4B). However,
the density of thrips in flowers from the sulfur-treated
control tunnels was significantly higher ðP < 0:001;
F ¼ 38:656, df ¼ 4; 233) than all other treatments or the
non-treated control (Fig. 5B). This translated to signif-
icantly more thrips-damaged fruit than all other treat-
ments (Table 2).
4. Discussion
The use of insect predators and parasitoids is an in-
tegral component of biological control, and often re-
quires importation from another country or continent.
Although the predatory mite, N. cucumeris, used in these
trials occurs naturally in Israel, it was not being
 P.G. Weintraub et al. / Biological Control 27 (2003) 300–309
cultivated and thus had to be imported from Europe.
Standard Israeli importation procedures mandate a
quarantine period, usually at the Ministry of Agriculture
quarantine laboratory in Bet Dagan, for at least one
generation. Once the imported organism has been
shown to be free of disease or other organisms, it can be
cultured and used in field trials. Due to the isolated
nature of the Arava Valley, some of the sachets of N.
cucumeris that were imported from Europe were held in
the quarantine laboratory; the remainder were used in a
field trial under quarantine procedures, as described in
the materials and methods. Results were sufficiently
encouraging to warrant commercial production under
the auspices of BioBee Biological Systems (Kibbutz
SÕdeh Eliyahu, Israel), and thus provided for research in
subsequent years. In these trials, we examined different
levels of release of N. cucumeris, for controlling the
broad mite, P. latus, and examined the effects of broad
mites on pepper plants.
Over the course of the 3 years of these trials, broad
mites were found twice on plants arriving from organic
nurseries. Even though there are organic acaricide
treatments available, such as sulfur powders and sprays,
pepper seedlings arrived infested with broad mites sug-
gesting that this is a major source of contamination. The
broad mite could be easily moved from infested seed-
lings to clean ones by one of two ways. As farm workers
plant seedlings, broad mites could be quickly spread to
non-infested plants. Additionally, in the late summer
and early autumn, whiteflies are still abundant; the
phoretic relationship with broad mites is well established
(Palevsky et al., 2001) and could lead to effective dis-
tribution of the broad mite within the greenhouse.
The slow release delivery system (Thripex, Koppert,
Holland) used in the first preliminary trial provides
optimum conditions for predatory mites (average ratio
of one N. cucumeris to 8 T. putrescentiae) when pest
populations are still low; initial populations of about
500 predatory mites/sachet will increase to between 4000
and 8000 in 6 weeks. Unfortunately this system was not
available for our trials in the second and third year.
Instead we released the mite twice to insure predator
establishment and pest control early in the season.
Placing the bran—T. putrescentiae—N. cucumeris mix
(average ratio of one N. cucumeris to 3 T. putrescentiae)
exposed on the upper-most pepper leaves did allow the
predatory mites to disperse. As soon as the bran dried
out, the T. putrescentiae died and were no longer a food
source for the N. cucumeris. Using the sachets instead of
this protocol would allow one release instead of two,
and perhaps would provide better broad mite control
than phytoseiids such as N. californicus and N. barkeri
which can only be released on plants when the pest is
present (Pe~ na and Obsorne, 1996). This is particularly
important because very low broad mite populations se-
riously affect pepper plants. Furthermore, N. cucumeris
307
is very easy and inexpensive to mass-produce, whereas
N. californicus is much more difficult and expensive.
In both sweet pepper varieties, there was significantly
more fruit damaged by broad mites in the non-treated
controls versus all other treatments. Although the dif-
ferences were not significant, there was more broad
mite-damaged fruit from the tunnels in which N. cu-
cumeris was released on every fourth plant followed by
sulfur-treated control tunnels, and the least amount of
damaged fruit was found in tunnels in which N. cu-
cumeris was released on every or every second plant.
Sulfur has been considered the single most effective
treatment for broad mites, but these trials clearly dem-
onstrate that release of about 600 N. cucumeris on every
plant or every second plant is equally effective.
Neoseiulus cucumeris (protonymph, deutonymph or
adult) has been shown, in laboratory trials, to kill 0–1
first instar thrips (F. occidentalis) per 24 h on cucumber
leaf discs (Shipp and Whitfield, 1991). Release rates for
the control of F. occidentalis have varied widely from
one introduction of 25 females per pepper plant (van
Houten and van Stratum, 1995), three introductions of
350 mites/m2 per week in cyclamen (de Courcy-Wil-
liams, 2001) to six introductions of 60–100 mites/plant
distributed evenly on cucumbers (Steiner, 1990).
Although the purpose of our trials was to determine
the efficacy of N. cucumeris against broad mites, mea-
surements of F. occidentalis populations were also made.
In both years, two releases of N. cucumeris kept popu-
lations of thrips in flowers significantly below thrips
populations in untreated control flowers. However, re-
sults from sticky traps data are equivocal, since during
the third year of the trial, thrips populations were more
than double the previous year. Additionally, evaluation
of yield showed that the amount of damage to fruit was
less in N. cucumeris release tunnels as compared to non-
treated control tunnels. An unexpected result was the
observation that the population of thrips in sulfur-
treated tunnels was higher than in any other treatment
or control. This was reflected in significantly more
thrips-damaged fruit; yet, the total yield from sulfur-
treated plants was larger than any other treatment.
These results are difficult to interpret. Burleigh et al.
(1998) reported that sulfur was one of two insecticides
that significantly reduced thrips populations on pepper
(C. annuum) but did not result in an increase in yield. It
is possible that, in our trials, sulfur improved the plant
quality (primarily by killing powdery mildew) and
therefore the thrips populations were higher. Since rig-
orous positive controls, such as release of Orius spp. or
chemical control measures were not employed, it is dif-
ficult to evaluate the relative efficacy of N. cucumeris in
the suppression of thrips from our trials.
Trials to evaluate the efficacy of N. cucumeris to
control thrips also included monitoring and distribution
of both species. By sampling apical, middle and basal
308 P.G. Weintraub et al. / Biological Control 27 (2003) 300–309
cucumber leaves, Steiner (1990) showed that N. cu-
cumeris was most numerous on middle and basal leaves.
She commented that, whereas P. persimilis were fre-
quently found associated with colonies of T. urticae, the
opposite was true of N. cucumeris and thrips; they were
not observed together. Higgins (1992), sampling flowers
and middle leaves of bell peppers and long English cu-
cumbers, rarely found N. cucumeris in the flowers where
western flower thrips are predominantly found. He at-
tributed N. cucumerisÕ inability to control the pest to the
fact that they were not found in the flowers. Our results
support these studies because we found very few N.
cucumeris on the apical leaves that we sampled to de-
termine broad mite densities, and none in the flowers. In
neither study did the researchers mention the time of
day that samples were taken. Our samples were always
taken in the morning hours, although not at a specific
time. Because N. cucumeris effectively controls broad
mites, it is possible that the predator moves up and
down the plant as light intensity and temperature
changes throughout the day.
In all 3 years, N. cucumeris proved to be an effective
control agent for the broad mite and became established
on the pepper plants. When the effect of the broad mite
on plant morphological parameters (height and dry
mass) and yield are taken into account, the most effec-
tive release rates were releasing about 600 mites on every
or every second plant twice, early in the season.
Acknowledgments
We thank Mr. Rami Golan at Ben Gurion University
of the Negev for evaluating yield in the third year of this
trial, Dr. Ruth Marcus for assistance with statistical
analysis, and Janis Joseph for editorial comments. This
research was funded in part by a grant from the Chief
Scientist of the Ministry of Agriculture, the Israeli
Vegetable Board and the Jewish National Fund. This
paper is a contribution from the Agricultural Research
Organization, Institute of Plant Protection, Bet Dagan,
Israel, No. 509/02.
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