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Crop Protection
journal homepage: www.elsevier.com/locate/cropro
How many Orius laevigatus are needed for effective western ower thrips,
Frankliniella occidentalis, management in sweet pepper?
Phyllis G. Weintraub a, *, Shimon Pivonia b, Shimon Steinberg c
a
a r t i c l e i n f o
a b s t r a c t
Article history:
Received 7 March 2011
Received in revised form
21 July 2011
Accepted 22 July 2011
Frankliniella occidentalis (Pergande) is a primary pest of greenhouse crops worldwide, in organic and
integrated pest management control practices, Orius spp. are frequently released for thrips control.
However, Orius spp. are relatively expensive to produce. More cost-efcient rearing systems and reduced
release rate might reduce the expense. In these trials, we released Orius laevigatus (Fieber) at different
rates with or without simultaneous release the predatory mite Amblyseius swirskii Athias-Henriot,
another known thrips predator, which is less expensive to rear. There was no signicant difference in
the number of O. laevigatus recovered in which either 2 or 6 individuals were released per square meter,
and there was no difference in thrips control among any of the release strategies using O. laevigatus,
suggesting that a reduced release rate can maintain effective thrips control. There was no signicant
difference in the quality or quantity of the pepper yield between treatments in which either 2 or 6 Orius/
m2 or Orius plus A. swirskii were released.
2011 Elsevier Ltd. All rights reserved.
Keywords:
Orius laevigatus
Amblyseius swirskii
Frankliniella occidentalis
Sweet pepper
1. Introduction
Thrips, especially the western ower thrips (WFT) Frankliniella
occidentalis (Pergande), are the primary pests of greenhouse crops
worldwide due to their polyphagous diet and their ability to rapidly
develop resistance to insecticides. WFT generally prefers enclosed
areas such as the owers, under the calyx of fruit and in newly opening
leaves, which makes them difcult to reach with insecticides but
controllable by small predatory arthropods. The generalist anthocorid
predator Orius laevigatus (Fieber) has been used as an effective biological control agent for WFT, preying on both larvae and adults
(Dissevelt et al., 1995; Frescata and Mexia, 1996), but it will also
consume other small arthropods found in owers (Shakya et al., 2009
and references therein), as well as pollen (Coll, 1998). Although Orius
spp. are effective thrips predators, they are relatively expensive to
mass-rear and this expense must be borne in-part by the growers. For
that reason there have been a number of investigations on the development of cost-effective factitious hosts for rearing Orius spp. (Lee and
Lee, 2004, and references therein; De Clercq et al., 2005; Mendes et al.,
2005; Ferkovich et al., 2007). Another means of reducing the cost to
growers would be to release fewer individual predators.
* Corresponding author. Tel.: 972 506 220 170; fax: 972 8 992 6485.
E-mail addresses: phyllisw@volcani.agri.gov.il (P.G. Weintraub), shimonp@arava.
co.il (S. Pivonia), s_stein@biobee.com (S. Steinberg).
0261-2194/$ e see front matter 2011 Elsevier Ltd. All rights reserved.
doi:10.1016/j.cropro.2011.07.015
1444
Table 1
Effect of predator treatments on the number of Polyphagotarsonemus latus
collected weekly on upper Capsicum leaf-samples (n 2000 leaves/treatment)
from 9 September to 11 December 2007.
Treatment
Total S.E.
Control
100 A. swirskii
6 O. laevigatus
2 O. laevigatus
6 O. laevigatus, 100 A. swirskii
2 O. laevigatus, 100 A. swirskii
P 0.0023, F 5.815, df 5, 18
421.3 159.5 A
44.5 19.73 B
266.0 54.31 AB
187.3 83.2 AB
15.0 11.5 B
8.8 3.9 B
Columns with the same letters are not signicantly different (a 0.05).
2.4. Monitoring
Twenty leaves from the upper stratum, 20 middle leaves from
the middle portion and 20 fully open owers per tunnel were
harvested randomly every week and placed separately in
containers with about 150e200 ml of 80% EtOH with 0.5% NaClO (to
dissolve spider mite webbing if necessary). Upon returning to the
2.2. Predators
A. swirskii and O. laevigatus were obtained from a commercial
insectary, Bio-Bee Sde Eliyahu Ltd., Israel. A. swirskii was reared and
packaged for release in wheat bran containing a non-phytophagous
mite (Carpoglyphus lactis L.) as prey. O. laevigatus was released as
a population of adults and 5th instar nymphs from vials containing
vermiculite.
2.3. Trials
Each tunnel constituted a replicate and there were four replicates of each treatment in each year. In commercial greenhouses,
O. laevigatus is released gradually, X individuals per week, over
consecutive weeks until the desired release rate is achieved;
a practice that we followed in these trials. Producers of biological
control agents often recommend the gradual release to avoid the
consequences of an accidental insecticide application killing all of
the released predators. Therefore, to achieve a nal density of 6
O. laevigatus/m2, 2 individuals/m2 were release for three consecutive weeks. Similarly, A. swirskii was released in groups of 50
individuals/m2 (ca. 10/plant) per week for two consecutive weeks,
until the desired release rate was achieved. Predator releases started 3 weeks after transplanting. A treatment of 1% liquid sulfur was
applied to foliage for broad mite control 2 weeks after transplanting. Sweet pepper is susceptible to powdery mildew (Leveillula taurica (Lv.) G. Arnaud); therefore, from the end of October
all tunnels were treated biweekly with 1% liquid sulfur, as
commonly practiced in the area (Elad et al., 2007).
Six treatments were randomly assigned to the tunnels in the
rst year (2007): non-treated control, 100 A. swirskii/m2, 6
O. laevigatus/m2, 2 O. laevigatus/m2, 6 O. laevigatus/m2 plus 100
A. swirskii/m2, and 2 O. laevigatus/m2 plus 100 A. swirskii/m2. Due to
the results of the rst year in which 100 A. swirskii/m2 did not
control thrips this treatment was eliminated in the second year.
Additionally the treatment of 6 O. laevigatus/m2 plus 100 A. swirskii/
m2 was deemed unnecessary because the lower release rate
controlled the thrips. Therefore the second year served a validation
Fig. 1. Total number of Frankliniella occidentalis (larvae and adults) and Orius laevigatus
(nymphs and adults) in 20 owers averaged over the 4 replicated tunnels during the
2007 season. Standard error bars are indicated. Arrows indicate predator release dates;
see text for further explanation.
1445
In the rst year, despite the sulfur treatment, there were still
populations of broad mites, and they were only signicantly
reduced in treatments that included A. swirskii (Table 1). It is
notable that the lowest populations of broad mites were seen in the
tunnels that also had O. laevigatus although this difference was not
statistically signicant. This may indicate that there was some
feeding on the broad mites by Orius. In the second year, broad mites
were adequately controlled with the liquid sulfur application early
in the season.
Orius spp. were found to have invaded tunnels where it was not
released about two months after transplanting the seedlings (Figs. 1
and 2), possibly being carried passively by workers or through
active invasion by local populations. Because of this movement we
Table 2
Cumulative total (S.E.) number of Frankliniella occidentalis (WFT) adults and larvae, Orius laevigatus (O.l.) adults and nymphs, and Amblyseius swirskii (A.s.) per replicate from
weekly counts of Capsicum owers (n 2600 owers/treatment) from 9 September to 6 November 2007.
Treat-ment
A. swirskii
WFT adults
WFT larvae
Orius adults
Orius nymphs
Control
100 A. s.
6 O. l.
2 O. l.
6 O. l., 100 A. s.
2 O. l., 100 A. s.
1.0 0.4 C
24.3 5.4 A
0C
1.0 0.4 C
9.3 1.9 B
6.3 2.5 BC
P < 0.0001
F 16.145
df 5, 18
1206.5 228.3 A
315.3 97.5 B
118.3 35.2 B
123.8 13.0 B
88.8 22.1 B
66.0 14.2 B
P < 0.0001
F 22.520
df 5,18
311.8 48.9 A
106.0 15.5 B
31.3 8.5 C
42.5 9.9 BC
43.5 13.5 BC
29.3 7.6 C
P < 0.0001
F 25.521
df 5, 18
2.5 1.9 B
1.0 0.7 B
43.5 3.1 A
54.0 6.7 A
73.0 11.4 A
60.3 8.5 A
P < 0.0001
F 65.343
df 5, 18
3.7 3.4 B
1.5 0.6 B
101.0 7.5 A
128.0 26.9 A
142.5 22.7 A
116.3 15.5 A
P < 0.0001
F 51.156
df 5, 18
Individual columns with the same letters are not signicantly different (a 0.05).
1446
Table 3
Cumulative total (S.E.) number of F. occidentalis (WFT) adults and larvae, O. laevigatus (O.l.) adults and nymphs, and A. swirskii (A.s.) per replicate from weekly counts of
Capsicum owers (n 2200 owers/treatment) from 16 September to 4 November 2008.
Treat-ment
A. swirskii
WFT adults
WFT larvae
Orius adults
Orius nymphs
Control
6 O. l.
2 O. l.
2 O. l., 100 A. s.
0.5 0.5 AB
0B
0B
8.0 4.3 A
P < 0.018
F 4.950
df 3, 12
286.5 20.3 A
12.8 2.8 B
23.3 3.1 B
16.3 4.2 B
P < 0.0001
F 62.350
df 3, 12
95.8 10.5 A
4.0 0.8 B
7.8 2.8 B
5.5 1.9 B
P < 0.0001
F 37.370
df 3, 12
2.5 0.9 B
59.8 8.7 A
58.5 7.6 A
58.8 4.9 A
P < 0.0001
F 45.342
df 3, 12
0.5 0.2 B
108.3 8.6 A
101.0 3.5 A
75.8 11.6 A
P < 0.0001
F 68.238
df 3, 12
Individual columns with the same letters are not signicantly different (a 0.05).
A. swirskii
F. occidentalis
O. laevigatus
Control
100 A. swirskii
6 O. laevigatus
2 O. laevigatus
6 O. l, 100 A. s.
2 O. l., 100 A. s.
0.5 0.5 C
54.0 7.2 A
2.0 2.0 BC
1.8 1.0 BC
12.3 5.8 B
11.8 2.4 B
P < 0.0001
F 24.574
df 5, 18
134.0 27.4 A
2.0 0.9 B
12.3 7.1 B
8.0 2.9 B
2.7 1.6 B
1.8 0.6 B
P < 0.0001
F 24.993
df 5, 18
1.3 0.8
1.5 0.9
6.5 1.9
6.3 3.0
4.8 0.7
4.3 1.1
P 0.175
F 1.746
df 5, 18
Individual columns with the same letters are not signicantly different (a 0.05).
Table 5
Cumulative total (S.E.) number of F. occidentalis (adults and larvae), O. laevigatus
(O.l.) (adults and nymphs) and A. swirskii (A.s.) per replicate from weekly counts of
Capsicum mid-leaves (n 2200 leaves/treatment) from 16 September to 4
November 2008.
Treatment
A. swirskii
F. occidentalis
O. laevigatus
Control
6 O. laevigatus
2 O. laevigatus
2 O. l., 100 A. s.
00 B
00 B
00 B
5.3 3.1 A
P 0.0237
F 4.556
df 3, 12
17.0 10.3 A
0.3 0.3 B
0.5 0.5 B
0.5 0.5 B
P 0.0145
F 5.329
df 3, 12
0.8 0.84
5.8 1.1
2.8 1.6
2.8 1.1
P 0.086
F 2.797
df 3, 12
Individual columns with the same letters are not signicantly different (a 0.05).
1447
Table 6
Percent of pepper yield (S.E.) without blemish and of export quality (which includes blemish-free peppers) for 2007e2008 and 2008e2009.
Treatment
2007e2008 % blemish-free
2008e2009 % blemish-free
Control
100 A. swirskii
6 O. laevigatus
2 O. laevigatus
6 O. l, 100 A. s.
2 O.l., 100 A. s.
0B
21.49 4.73
72.19 3.72
69.95 3.88
59.15 6.48
64.88 3.68
P < 0.0001
F 39.869
df 5, 90
3.47 2.15
64.09 7.48
98.75 6.67
99.44 3.20
85.58 8.35
96.84 9.66
P < 0.0001
F 65.540
df 5, 90
45.04 11.24 B
51.84 12.02 B
99.75 0.25 A
93.29 4.30 A
100.0 A
97.84 1.44 A
96.15 2.33 A
P < 0.0001
F 30.577
df 3, 44
99.8 0.17 A
P < 0.0001
F 27.399
df 3, 44
B
A
A
A
A
D
C
AB
A
B
AB
Individual columns with the same letters are not signicantly different (a 0.05).
at the time of the rst release (see Table 7 for subsequent releases
and for the ratios in the second year). At no time did the prey:predator ratio exceed 7.5:1 in tunnels where O. laevigatus was
released. Natural invasion or movement by workers of Orius into
the non-treated control tunnels reached cumulative prey:predator
ratios of 17 and 6.7 for the years 2007 and 2008, respectively. Bosco
et al. (2008) also found in general that prey:predator ratios were
lower in greenhouses where they released O. laevigatus as
compared to greenhouses where natural invasion occurred.
The WFT dynamics at the predator:prey ratios we observed did
not conform to the predictions of Sabelis and van Rijns (1997)
model; we observed a type-2 pest dynamics (which predicts
a delayed decrease in WFT populations) in which it took 4e5 weeks
for the WFT population to reach near zero. For predator:prey ratios
of less than 1:50 they predicted a type 1 pest dynamics (which
predicts an immediate decline in pest population within approximately 1 week). They noted that some eld research results supported their model, but that other research did not. No clear
explanation can be offered for a delayed decrease in WFT populations; there is an element of physical protection in the owers,
perhaps pollen feeding by Orius reduces their thrips-feeding rate,
or as Chow et al. (2010) suggested, Orius will switch to feeding on
whatever food (WFT or broad mites) is most abundant. Indeed, we
found lower population densities of broad mites in tunnels where
both A. swirskii and O. laevigatus were released (Table 1.) e
circumstantial evidence that Orius feeds on broad mites.
WFT populations in tunnels in which only A. swirskii was
released were signicantly lower than the non-treated control, but
control was insufcient in terms of practical WFT management.
Similarly to the case with our release of O. laevigatus, A. swirskii did
not t the Sabelis and van Rijn (1997) model of type 1 dynamics
with predator:prey ratios of 1:9 or greater in owers. Predator:prey
ratios, although hard to estimate, were closer to 1:1 (as mites were
released before thrips were captured); however, WFT demonstrated a type-2 dynamics, gradually increasing in population size
Table 7
Predator:prey estimates at time of O. laevigatus releases and ratio based on cumulative total numbers of O. laevigatus and F. occidentalis found in owers in 2007 and
2008. Additionally the estimates for 2 O. laevigatus and 100 A. swirskii (O. l. A.s.) are
given.
Cumulative number
of O. laevigatus
released
1st release
2nd release
3rd release
Natural
invasiona
O. l. A.s.
2/m
4/m2
6/m2
2007 ratio
2008 ratio
Initial
Cumulative
Initial
Cumulative
1:4
1:7.5
1:6
1:140
1:0.27
1:0.22
1:0.28
1:17
1:1
1:1.25
1:1.25
1:30
1:0.09
1:6.7
1:4
1:0.14
1:1
1:0.07
a
This may have been due to workers moving O. laevigatus among tunnels or
natural invasion of O. albidipennis.
before declining to near zero after almost two months (Fig. 1).
However, Sabelis and van Rijn (1997) also noted that for phytoseiid
mites the model predictions tend to be more qualitative (predicting
the rate of decline in prey populations) rather than quantitative.
Quantitative predictions would require knowing the specics of the
predatory mite species the ability to attack rst or second instar
thrips, predation rate, oviposition rate, etc.
When A. swirskii was combined in a release strategy with
O. laevigatus, a signicant improvement in thrips control over the
non-treated control or over A. swirskii alone was observed. There
was circumstantial evidence of IGP (O. laevigatus is the intraguild
predator); fewer A. swirskii were found in owers in tunnels where
O. laevigatus was released. While Urbaneja et al. (2003) concluded
that N. cucumeris (Oudemans) helped the establishment of Orius by
being a supplemental food source, and that indirectly enhanced
thrips control, we found that A. swirskii contributed directly to
thrips control. Additionally, there is no evidence from these trials
that O. laevigatus established faster or in larger numbers in the
presence of A. swirskii (Figs. 1 and 2).
The results from this study strongly suggest that fewer
O. laevigatus individuals could be released and still maintain
effective WFT control, thus reducing the costs to growers. Recommended Orius release rates, according to major companies on
internet websites vary according to crop and location, but with the
recommended 2e4 sequential releases, the total number of Orius
per square meter is often between 4 and 8/m2 and up to 10/m2 for
hot spots (US$400e1000 per 1000 m2 greenhouse); therefore
a reduction of even a few individuals would represent a substantial
saving to the growers. Application rates of A. swirskii are usually 50/
m2, sequentially for 2 weeks (approximately $220 for bulk release
per 1000 m2 greenhouse). As shown in both years, a reduction in
the number of Orius released for WFT control does not adversely
affect the quality or quantity of pepper fruit. Early release of Orius is
an important factor in effective thrips management. More research
on the timing and number of releases of different Orius species
should be conducted to determine if our observations with
O. laevigatus are in accord with other species.
Acknowledgements
The authors would like to thank Marilyn Steiner for insightful
comments on the manuscript, Sophia Kleitman, Danit Parker, and
Talya Samany for technical assistance. This paper is a contribution
from the Agricultural Research Organization, Institute of Plant
Protection, Bet Dagan, Israel.
References
Bosco, L., Giacometto, E., Tavella, L., 2008. Colonization and predation of thrips
(Thysanoptera; Thripidae) by Orius spp. (Heteroptera; Anthocoridae) in sweet
pepper greenhouses in Northwest Italy. Biol. Cont. 44, 331e340.
Buitenhuis, R., Shipp, L., Scott-Dupree, C., 2009. Intra-guild vs. extra-guild prey:
effect on predator tness and preference of Amblyseius swirskii (Athias-Henriot)
1448
Lee, K.-S., Lee, J.-H., 2004. Rearing of Orius strigicollis (Heteroptera: Anthocoridae)
on articial diet. Entomol. Res. 34, 299e303.
Mendes, S.M., Bueno, V.H.P., Carvalho, L.M., Reis, R.P., 2005. Production cost of Orius
insidiosus as biological control agent. Pesq. Agropec. Bras. 40, 441e446.
Messelink, G., van Steenpaal, S.E.F., Ramakers, P.M.J., 2006. Evaluation of phytoseiid
predators for control of western owers thrips on greenhouse cucumber.
BioControl 51, 753e768.
Ramakers, P.M.J., van Lieburg, M.J., 1982. Start of commercial production and
introduction of Amblyseius mckenziei Sch. And Pr. (Acarina: Phytoseiidae) for
the control of Thrips tabaci Lind. (Thysanoptera: Thripidae) in glasshouses. Med.
Fac. Landbouww. Rijksuniv. Gent. 47, 541e545.
Sabelis, M.W., van Rijn, P.C.J., 1997. Predation by insects and mites. In: Lewis, T. (Ed.),
Thrips as Crop Pests. CAB, Wallingford, UK, pp. 259e354.
Shakya, S., Weintraub, P.G., Coll, M., 2009. Effect of pollen supplement on intraguild
predatory interactions between two omnivores: the importance of spatial
dynamics. Biol. Cont. 50, 281e287.
Shipp, J.L., Zariffa, N., 1991. Spatial patterns of and sampling methods for western
ower thirps (Thysanopera, Thripidae) on greenhouse sweet-pepper. Can.
Entomol. 123, 989e1000.
Shipp, J.L., Zariffa, N., Ferguson, G., 1992. Spatial patterns of and sampling methods
for Orius spp. (Hemiptera, Anthocoridae) on greenhouse sweet-pepper. Can.
Entomol. 124, 887e894.
Tal, C., Coll, M., Weintraub, P.G., 2007. Biological control of Polyphagotarsonemus
latus (Acari: Tarsonemidae) by the predaceous mite Amblyseius swirskii (Acari:
Phytoseiidae). Bull. IOBC/WPRS 30 (5), 111e115.
Tavella, L., Alma, A., Conti, A., Arzone, A., 1996. Evaluation of the effectiveness
of Orius spp. in controlling Frankliniella occidentalis. Acta Hort. 431,
499e506.
Teich, Y., 1966. Mites of the family of Phytoseiidae as predators of the tobacco
whitey, Bemisia tabaci Gennadius. Israel J. Agric. Res. 16, 141e142.
Ucko, O., Cohen, S., Ben-Joseph, R., 1998. Prevention of virus epidemics by a cropfree period in the Arava region of Israel. Phytoparasitica 26, 313e321.
Urbaneja, A., Leon, F.J., Gimenez, A., Aran, E., van der Blom, J., 2003. The interaction
of Neoseiulus (Amblyseius) cucumeris (Oudemans) (Aca.: Phytoseiidae) on the
installation of Orius laevigatus (Fieber) (Hem.: Anthocoridae) in sweet pepper
crops. Bol. San Veg. Plagas 29, 1e12.
Van Maanen, R., Vila, E., Sabelis, M.W., Janssen, A., 2010. Biological control of broad
mites (Polyphagotarsonemus latus) with the generalist predator Amblyseius
swirskii. Exp. Appl. Acarol. 52, 29e34.
Van Rijn, P.D.J., Tanigoshi, L.K., 1999. Pollen as food for the predatory mites Iphiseius
degenerans and Neoseiulus cucumeris (Acari: Phytoseiidae): dietary range and
life history. Exp. Appl. Acarol. 23, 785e802.
Weintraub, P.G., Kleitman, S., Palevsky, E., 2005. Diel movement of predatory mites
(Neoseiulus cucumeris), reared in light or dark, on greenhouse sweet pepper.
Bull. IOBC/WPRS 28 (1), 313e316.