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Experimental and Applied Acarology ISSN 0168-8162 Exp Appl AcarolDOI 10.1007/s10493-014-9853-4
Comparison of conventional and integratedprograms for control of Tetranychusurticae (Acari: Tetranychidae)
Larissa Akemi Iwassaki, Mário Eidi Sato,Fagoni Fayer Calegario, Marcelo Poletti& Aline de Holanda Nunes Maia
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Comparison of conventional and integrated programsfor control of Tetranychus urticae (Acari: Tetranychidae)
Larissa Akemi Iwassaki • Mario Eidi Sato •
Fagoni Fayer Calegario • Marcelo Poletti •
Aline de Holanda Nunes Maia
Received: 24 March 2014 / Accepted: 18 September 2014� Springer International Publishing Switzerland 2014
Abstract The twospotted spider mite (TSSM), Tetranychus urticae Koch, is one of the
main pests on strawberry crops in Brazil. TSSM can be difficult to control due to acaricide
resistance. The objective of this work was to compare the effect of conventional and
integrated strawberry production (ISP) systems on mite abundance and acaricide resis-
tance. The control of TSSM in ISP was based on the release of Neoseiulus californicus
(McGregor) or application of a selective acaricide (propargite), when TSSM monitoring
indicated the timing for the release of predaceous mites (1–3 mites per leaflet on 30 %
leaflets) or chemical intervention ([10 mites per leaflet). Only acaricides (abamectin,
fenpyroximate) were applied in the conventional system. Integrated control of TSSM were
sufficient to maintain a significantly lower pest infestation level, resulting in a sixfold
reduction in the frequency of acaricide applications, and consequently, a lower selection
pressure for acaricide resistance. Strategies for the management of TSSM in strawberry
fields are described and discussed.
Keywords Twospotted spider mite � Strawberry � Biological control � Neoseiulus
californicus � Chemical control � Pesticide resistance
L. A. Iwassaki (&) � M. E. SatoInstituto Biologico, APTA, Rodovia Heitor Penteado km 3.5, Caixa Postal 70, Campinas,SP CEP 13001-970, Brazile-mail: [email protected]
F. F. Calegario � A. H. N. MaiaEmpresa Brasileira de Pesquisa Agropecuaria, Embrapa Meio Ambiente, Caixa Postal 69, Jaguariuna,SP CEP 13820-000, Brazil
M. PolettiPROMIP - Comercio, Pesquisa e Desenvolvimento de Agentes Biologicos Ltda. ME,Caixa Postal 111, Engenheiro Coelho, SP CEP 13165-000, Brazil
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Exp Appl AcarolDOI 10.1007/s10493-014-9853-4
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Introduction
The twospotted spider mite (TSSM), Tetranychus urticae Koch (Acari: Tetranychidae),
is a worldwide pest for many plant species, including several agricultural crops (Zhang
2003). This tetranychid mite causes significant damage to various crops in Brazil, such
as apple, peach, papaya, kidney bean, cotton and ornamental plants (de Moraes and
Flechtmann 2008). On strawberries, the spider mite feeds on the undersurface of the
leaves, causing curling and discoloration. Their rapid developmental rate and high
reproductive potential enable them to reach damaging infestation levels very rapidly
under good growing conditions (Nyoike and Liburd 2013). In Brazil, the TSSM has
been controlled almost exclusively using acaricides. However, chemical control of the
pest is becoming increasingly difficult in the field due to the development of resistance
to various acaricides (Sato et al. 2005, 2009; Nicastro et al. 2010, 2013; Tirello et al.
2012). Another problem associated with the indiscriminate use of pesticides is the
resurgence of pests due to the suppression of natural enemies (Van de Vrie et al. 1972;
Dutcher 2007).
The Brazilian production of strawberry comes mainly from the states of Minas Gerais,
Rio Grande do Sul and Sao Paulo, which account for almost 80 % of the national pro-
duction (IBGE 2006). In 2006, a project entitled the Integrated Production of Strawberry
was initiated in the State of Sao Paulo (SP; Calegario 2012; Embrapa Meio Ambiente
2013) with the aim of preserving and/or enhancing the mortality factors of the pests, using
several resources (including biological and chemical control), in an integrated manner, and
based on technical, economic, ecological, and social parameters (Tomczyk et al. 1991;
Gerson et al. 2003; Bacci et al. 2007).
One of the strategies adopted by the ISP for the control of spider mites in Brazil is the
release of predaceous mites of the species Neoseiulus californicus (McGregor) in the field.
Neoseiulus californicus is a phytoseiid mite which can provide effective biological control
of tetranychid mites on strawberry and several other cultivated plant species (Strong and
Croft 1995; McMurtry and Croft 1997; Greco et al. 2005; Sato et al. 2007; Gomez-Moya
and Ferragut 2009; Saber 2012).
This study aims to compare the strategies used for the control of T. urticae in two
strawberry production systems: an area conducted under the technical standards of ISP
(Brasil, 2008) and a commercial strawberry field using a conventional production system,
in SP.
Materials and methods
Mite strain
Neoseiulus californicus (Neomip Max�) were provided by Promip Trade, Research and
Development of Biological Agents (SP, Brazil).
Chemicals
The acaricides abamectin (Vertimec� 1.8 % EC, Syngenta Crop Protection), propargite
(Omite� 720 EC, Chemtura Chemical Industries of Brazil) and fenpyroximate (Ortus� 5 %
SC, Arysta Lifescience), were commercially available in SP and were purchased in Atibaia
County, SP.
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Field experiment
Two strawberry production fields located in Atibaia County, SP, were compared with
respect to the strategies for the control of spider mites: one field adopted the ISP system
[Sao Joao farm; Demonstration Unit for ISP System: 23�040 S, 46�400 W], whereas the
other was a commercial strawberry field using a conventional production system (Tanaka
farm: 23�050 S, 46�400 W). These fields were chosen due to the short distance between
them (B8 km), in order to reduce possible climatic differences which could affect man-
agement strategies.
Seedlings of ‘Oso Grande’ strawberry cultivar were used in both areas as follows:
• Sao Joao farm-IPA (integrated production area): 4,214 plants (0.35 9 0.35 cm),
transplanted on 9 plots (1 9 57 m), in the fourth week of March 2008.
• Tanaka farm-CPA (conventional production area): 4,000 plants (0.30 9 0.30 cm),
transplanted on 8 plots (1 9 45 m), in the third week of March 2008.
In both areas, strawberries were planted in three rows on raised beds, mulched with
black polyethylene plastic, in open-field cultivation. For the statistical analysis, the
strawberry plots were considered blocks in each production system, totaling 8–9 replicates
per treatment.
For IPA, the strategies for the control of TSSM were based on the results of the weekly
monitoring of pest abundance. The releases of predaceous mites (N. californicus) were
made when the infestation level of TSSM reached 1–3 mites per leaflet, on at least 30 % of
the leaflets. Neoseiulus californicus were released at a rate of approximately 3.0 mites per
m2, when the spider mite infestation reached the action level (1–3 mites/leaflet; 30 % of
leaflets). After the first release of N. californicus, the subsequent release was made only
when the predaceous mites were not sufficient to reduce the spider mite infestations in
3 weeks.
These N. californicus releasing rates were chosen based on the reports of Zalom (2002)
and Fraulo and Liburd (2007). Zalom (2002) considered an economic threshold level
(ETL) of 5–10 mites per mid-tier leaflet for the first 4 months following the transplant of
strawberry. Once harvest begins, strawberry plants become more tolerant of mite feeding
and treatment thresholds increase to an average of 15–20 mites per mid-tier leaflet (Zalom
2002). Fraulo and Liburd (2007) mentioned an ETL of 23–27 active mites per leaflet or
70–80 mites per leaf.
According to Greco et al. (2011), at proportions of leaflets infested with TSSM higher
than 0.30, the pest can reach the ETL [50 mites/leaflet (Wyman et al. 1979)] in less than
7 days. Previous studies in strawberry fields (Oso Grande cultivar) in the SP indicated that
when N. californicus was released at TSSM infestation levels of 1–5 mites per leaflet, the
spider mite abundance was maintained below ten mites per leaflet during all the strawberry
season (Berton et al. 2007).
In order to minimize the effect of wind on the dispersion of phytoseiid mites and favor
the establishment of the predators in the strawberry field, a fence with a plastic sheet
(1 m high) was installed on July 14, around the experimental area.
For IPA, when the TSSM infestations reached levels above ten mites per leaflet for
more than 1 week, the decision of chemical intervention was taken to prevent possible
serious damages caused by the spider mites (Wyman et al. 1979; Chiavegato and Mischan
1981). In this case, when the acaricide applications were made on the strawberry field (July
28 and August 18), TSSM abundances were of 35–59 mites per leaflet, with more than
80 % of infested leaflets. These infestation levels (C35 mites/leaflet) were similar to the
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ETL (40 mites/leaflet) adopted by Sato et al. (2007) for the acaricide application against
TSSM, in strawberry fields where N. californicus had been released.
The selective acaricide propargite (Sato et al. 2002) was applied at the recommended
concentration [216 (AI) mg/l] for the control of TSSM in strawberry fields in Brazil
(AGROFIT 2014). In the conventional production area (CPA), the control of TSSM was
performed by the farm owner, using only chemical acaricides, without considering any pest
abundance monitoring. The acaricide applications were made almost every week,
according to the owner, from June to September 2008.
Assessments of abundances of phytophagous and predaceous mites were made weekly
(for 32 weeks) in both areas, from the seedling transplanting period to the end of the
strawberry harvest (April–November). The leaflet sampling method was similar to that
proposed by Greco et al. (2011), collecting one leaflet from a mature leaf in each row at
10-m intervals (ten footsteps, each of approximately 1 m).
On each sampling date, 80 (n = 10 leaflets/plot 9 8 plots for CPA) or 81 (n = 9
leaflets/plot 9 9 plots for IPA) strawberry leaflets were collected and placed in paper bags,
in Styrofoam boxes with ice, and taken to the laboratory in Campinas City. Mites (T.
urticae and N. californicus) on each leaflet were counted under a dissecting microscope
within 24 h. The phytoseiid mites collected from leaves were mounted in Hoyer’s medium
on microscope slides for subsequent identification. Samples of TSSM (males) were also
mounted on slides for identification.
Data on the meteorological (temperature and rainfall) conditions in Atibaia County
along the field experiment period were provided by Integrated Agrometeorological
Information Center (CIIAGRO) of Instituto Agronomico de Campinas (IAC; CIIAGRO
2008).
Acaricide resistance monitoring in Tetranychus urticae
Samples of TSSM mites were taken from both strawberry fields at the beginning of the
spider mite infestation (March for IPA; May for CPA) in each area and at the peak of the
strawberry harvesting period (August for IPA; September for CPA) for the monitoring of
acaricide resistance in TSSM. The study was carried out for the acaricides abamectin,
propargite and fenpyroximate. After collection, the mites were transferred to jack bean
plants (Canavalia ensiformis L.) and maintained for a period of 17–25 days under labo-
ratory conditions (at 25 ± 2 �C) before performing the toxicity tests.
These tests were based on the method described by Knight et al. (1990). Sixty female
TSSM adults were placed on a bean leaf disc (4 cm diameter) on water-soaked cotton in a
Petri dish (9 cm diameter). A prepared suspension of acaricide (2 ml) was sprayed onto the
leaf disc mites using a Potter spray tower (Burkard Manufacturing, Uxbridge, UK) at
68.9 kPa. Preliminary tests indicated that 1.6 ± 0.1 mg/cm2 of distilled water was sprayed
on the leaf disc with this volume and pressure.
Only one concentration [in mg/l of AI (active ingredient)] was used for each acaricide,
which was equivalent to the discriminating concentration [abamectin (4.79); fenpyroxi-
mate (46.3); propargite (40.3)] of each acaricide (Sato et al. 2004, 2005). Only distilled
water was applied for the control. Thereafter, the mites on the leaf disc were kept at
25 ± 1 �C with a 14 h photoperiod for 48 h (for abamectin and fenpyroximate) or 72 h
(for propargite) after treatment.
Individual mite survival was determined by touching each mite with a fine brush. Mites
that were unable to walk at least a distance equivalent to their body length were considered
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dead. Tests in which control mortality was equal to or higher than 10 % were not con-
sidered in this study. Each experiment was replicated four times.
Statistical analyses
For the field experiment, repeated measures ANOVA was used to analyze and compare the
numbers of mites (T. urticae and N. californicus) between the treatments (IPA and CPA)
and evaluation dates (periods). For comparison of treatments the post hoc Tukey’s multi-
comparison test was applied. Profile Analysis was used for comparisons among evaluation
dates (periods).
The relationship between the time series of the number of spider mites and predators
was analyzed using cross-correlation function analysis, estimating the coefficient of cor-
relation (r) and lag between the temporal series. If the lag is zero, it means that the highest
correlation (between mite species) was observed for the same evaluation dates. For lag 0,
the data of abundance streams in real-time. If the lag is 1, for instance [for the species T.
urticae (A) and N. californicus (B)], the fluctuation of mites of the species B is correlated
with the fluctuation of mites of the species A in lag 1, or 1 week (interval between
evaluations) after the evaluation period for the species A. Lag 3 correspond to a 3-week
interval, and lag 5 to a 5-week interval. Data were square-root-transformed for homoge-
neity of variance (homoscedasticity) and normal distribution.
For the monitoring of acaricide resistance in TSSM, the percentage of acaricide-resis-
tant mites was estimated using weighted least squares (Stokes et al. 2000), considering that
the number of alive individuals in each treatment was a random variable with binomial
distribution. Comparisons between pairs of treatments were made via v2 test (Wald 1943),
using the PROC CATMOD of SAS System (SAS Institute 2008).
Results
Significant differences were observed for the two treatments (IPA and CPA)
[F1,151 = 331.79; P \ 0.001], evaluation dates (periods) [F31,4681 = 206.53; P \ 0.001]
and interactions (treatments 9 periods) [F31,4681 = 48.49; P \ 0.001], indicating that the
abundance of TSSM were different between treatments (conventional vs. integrated pro-
duction systems) during this period. The abundance of TSSM in IPA was lower than in
CPA from week 22 to 32 after the strawberry transplanting. The highest abundance in CPA
was 140.9 mites (active stages) per leaflet in week 23, whereas the highest abundance for
IPA was in week 21, with 59 mites per leaflet (Fig. 1). The average abundance of TSSM
(33.0 mites/leaflet) in CPA was 2.29 higher than for IPA.
The TSSM infestation in the strawberry integrated production area (IPA) was observed
from the first sampling date, on 1 April. Four releases of the N. californicus were neces-
sary, based on the infestation levels of the spider mite. For IPA, the predaceous mites were
released at rates of 29–3.5 mites per m2, on 11 April (week 3), 21 May (week 8), 29 July
(week 18) and 19 August (week 21), when the TSSM infestations were above the action
level (1–3 mites/leaflet; 30 % of leaflets). The last two releases (July and August) were
carried out 24 h after spraying of the selective acaricide (propargite) on the strawberry
field.
The two acaricide applications (weeks 18 and 21) were performed when TSSM
abundance reached levels above ten mites per leaflet for more than 1 week. The appli-
cations of the acaricide propargite significantly reduced (P \ 0.05) the abundance of
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TSSM (weeks 19 and 22) without causing any significant negative effect on the abun-
dance of N. californicus.
Additional acaricide treatments or N. californicus releases were not necessary due to the
gradual reduction of TSSM infestation in the field after the end of August. In the second
0
20
40
60
80
100
120
140
160
180
0
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20
30
40
50
60
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100
Apr Mai Jun Jul Aug Sep Oct Nov
Rainfall (mm)
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Tetranychus ur�cae
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ites p
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umbe
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s per
leafl
et
Fig. 1 Number of active forms of Tetranychus urticae and Neoseiulus californicus per leaflet on strawberryplants, in integrated production (IPA) and conventional production areas (CPA); rainfall and temperatureconditions in Atibaia County, state of Sao Paulo (SP), in 2008
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half of October, the infestation of spider mites reduced to zero on the strawberry plants of
IPA (Fig. 1).
For CPA, the beginning of the TSSM infestation was registered in the second half of
May (week 8); however, the grower only initiated pest control 1 month later, when he
started applying acaricides. According to him, the acaricide applications were done on an
almost weekly basis between the months of June and September. Altogether, 12 sprays
were used, ten of abamectin and two of fenpyroximate. Even with those applications, the
TSSM infestation increased in the field, reaching 100 % of infested leaflets and up to 140.9
mites per leaflet in September (week 23; Fig. 1).
Although predaceous mites were not released in CPA, N. californicus were found on
strawberry plants from week 24 (September 2008) of the experiment (Fig. 1). In both
strawberry fields, significant differences in N. californicus abundances were also observed
for treatments (IPA vs. CPA) [F1,151 = 80.87; P \ 0.001], periods [F31,4681 = 37.06;
P \ 0.001] and their interaction [F31,4681 = 35.27; P \ 0.001]. Neoseiulus californicus
mites were observed in IPA from April to November with higher abundances than in CPA
in week 3 and weeks 15–28 after transplanting. The highest abundance of N. californicus
was observed on 22 September (week 26), with 4.1 mites per leaflet in IPA (Fig. 1).
Significant correlations were observed between TSSM and N. californicus on straw-
berry plants for IPA (r = 0.792, df = 30, P \ 0.05; in lag 3) and for CPA (r = 0.818,
df = 30, P \ 0.05; in lag 5). The correlation between TSSM and N. californicus in lag 3
indicates that the abundances of N. californicus followed variations in TSSM infestations
in the strawberry field (IPA), but with a lag of 3 weeks.
Acaricide resistance monitoring
In the CPA, the percentage of abamectin-resistant TSSM increased significantly
(P B 0.0001) from May to September, varying from 7.1 to 69.0 %. For fenpyroximate-
resistant mites, the increase was from 24.2 to 68.3 % in the same period. For propargite,
which was not used by the grower during the evaluated period, a decrease in the percentage
of resistant mites was observed (Table 1). In the case of IPA, no significant change was
Table 1 Mean (±SE; n = 4) percentage of resistant mites for the acaricides abamectin, fenpyroximate andpropargite, in populations of Tetranychus urticae collected at the beginning and at the peak of infestation instrawberry conventional production (CPA) and integrated production areas (IPA) and P values associatedwith the v2 Wald test for comparisons between periods of tests with each acaricide, and for each productionsystem, in Atibaia County, SP, in 2008
Productionsystem (Area)
Acaricide Resistant mites (%) v2 (df = 1) P
May September
CPA Abamectin 7.1 ± 0.02 69.0 ± 0.03 388.33 \0.0001
Fenpyroximate 24.2 ± 0.03 68.3 ± 0.03 131.37 \0.0001
Propargite 51.2 ± 0.03 14.6 ± 0.02 86.18 \0.0001
March August
IPA Abamectin 21.7 ± 0.03 16.2 ± 0.02 2.30 0.13
Fenpyroximate 17.9 ± 0.02 20.0 ± 0.03 0.34 0.56
Propargite 10.0 ± 0.02 10.8 ± 0.02 0.09 0.77
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observed (P C 0.13) in the percentage of acaricide-resistant mites during the strawberry
growing season (Table 1).
Discussion
Considering the abundance of TSSM in CPA, high infestation levels (80–140 mites/leaflet)
were observed from 25 August (week 22) to 6 October (week 28), causing severe damage
to the strawberry plants during this period. According to Chiavegato and Mischan (1981),
high infestation levels of TSSM can significantly affect strawberry production (up to 80 %
loss), leading to the death of plants if high infestation levels are maintained for long
periods in the field.
For IPA, the maximum infestation level of TSSM was 59 mites per leaflet, with an
average abundance of 14.9 mites per leaflet, which did not cause any visual damage to the
strawberry plants. The presence of N. californicus mites in IPA may have affected the
abundance and the behavior of TSSM, reducing the damage caused by the pest mite. The
TSSM can recognize infochemicals (kairomones) from its predators (phytoseiid mites) or
cues from injured spider mites and consequently avoid feeding or ovipositing in areas
exposed to these cues (Grostal and Dicke 1999).
The potential of N. californicus as a biological control agent has been documented
widely (Sabelis and Janssen 1994; Rhodes and Liburd 2006; Greco et al. 2005, 2011; Sato
et al. 2007; Kim et al. 2013). The results of management adopted in IPA are congruent with
those reported by Sato et al. (2007) and Greco et al. (2011), which indicate that this
predator is capable of maintaining low TSSM densities at appropriate relative prey–
predator ratios.
The first release of N. californicus carried out in the third week (April) was not suffi-
cient for a rapid establishment of the predaceous mite in IPA. One of the possible problems
associated with the establishment of the phytoseiid mites on the strawberry plants was the
presence of winds (C10 km/h) on the area of the beds, in conditions of low abundance
(0.19 mites/leaflet) of the spider mite. The influence of winds on the aerial dispersal of
phytoseiid mites was reported by several authors (Tixier et al. 1998; Jung and Croft 2001).
The aerial dispersal is mainly passive and by wind, but some active take-off behaviors have
been reported (Sabelis and Afman 1994). As prey food levels decline, with starvation and
the presence of wind, aerial take-off of phytoseiids occurs (Jung and Croft 2001).
The fence with a plastic sheet installed on 14 July around the experimental area in IPA,
in order to protect the plants from the wind, may have influenced the establishment of N.
californicus in the field. The abundance of N. californicus increased very slowly
(0.01–0.07 mites/leaflet in 14 weeks) from April to the beginning of July on the strawberry
plants in IPA; however, a relatively rapid increase (0.15–0.37 mites/leaflets in 2 weeks) in
its abundance was noticed in the second half of July (weeks 16–18), after the installation of
the fence. This fortnight interval was one of the driest periods of the year in Atibaia County
(CIIAGRO 2008).
Abundance of N. californicus equal to or above 1.0 mites per leaflet was observed in
IPA from 18 August (week 21), coinciding with the period of the highest rates of rainfall
(40–80 mm/month) and consequently higher humidity. The positive effect of higher
humidity on the establishment of phytoseiid mites was also reported by several authors
(Gerson et al. 2003; de Vis et al. 2006).
The applications of the acaricide propargite did not affect the abundance of N. cali-
fornicus. The low toxicity of propargite to this strain of N. californicus has already been
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reported by Sato et al. (2002). The median lethal concentration (LC50) of propargite in
adults of N. californicus was 2 g AI/l, under laboratory conditions (Sato et al. 2002), which
is almost 109 higher than the recommended concentration of this acaricide for the control
of TSSM in strawberry fields in Brazil (AGROFIT 2014). This strain of N. californicus has
been shown to be resistant or tolerant to pesticides from several chemical classes (e.g.
pyrethroids, organophosphates, spiromesifen) (Poletti and Omoto 2005; Sato et al. 2007,
2011), facilitating the integration of the use of this natural enemy with pesticide appli-
cations for insect pest control in strawberry fields.
The use of pesticide-resistant predaceous mites for the control of spider mites has also
been reported for several species of phytoseiid mites [e.g. Amblyseius fallacis (Garman),
Metaseiulus occidentalis (Nesbitt), Typhlodromus pyri Scheuten, Phytoseiulus persimilis
Athias-Henriot] in different crops (Hoy 1990; Blommers 1994; Hardman et al. 2000; Lee
et al. 2001).
Although propargite has been used as the selective acaricide for the control of TSSM,
several other acaricides have low toxicity to N. californicus (Sato et al. 2002; Castagnoli
et al. 2005; Liburd et al. 2007) and may be useful for the management of the spider mite in
strawberry fields. Bifenazate, for instance, presents low toxicity towards the predaceous
mite, and has been recommended for use in combination with N. californicus for the
control of TSSM on strawberries (Rhodes and Liburd 2006; Liburd et al. 2007; Greco et al.
2011).
The presence of phytoseiid mites in the area of the conventional production (CPA)
was only observed on 8 September (week 24), probably due to the interruption of the
acaricide applications, which was associated with an increase in the rainfall frequency.
Abamectin, which was the most frequently applied acaricide on the strawberry plants in
CPA, was classified as slightly harmful (Meyer et al. 2009; da Silva et al. 2012) or
harmful (Kaplan et al. 2012) to N. californicus. This acaricide caused significant mor-
talities (C60 %) to the active forms of the phytoseiid mite, especially on the first day
after treatment (Sato et al. 2002; da Silva et al. 2012). The other acaricide used by the
grower (fenpyroximate) was considered to be less toxic to N. californicus than abamectin
(Sato et al. 2002).
In the case of CPA, although the grower used ten applications of the acaricide aba-
mectin and two of fenpyroximate on the strawberry beds, the TSSM abundance was not
satisfactorily controlled, due to the evolution of resistance to these acaricides, as confirmed
in the study of acaricide resistance monitoring. Abamectin and fenpyroximate resistance in
TSSM was also reported by several authors (Campos et al. 1995; Stumpf and Nauen 2002;
Suh et al. 2006; Yorulmaz and Ay 2009; Ay and Kara 2011), including cases of popula-
tions found in commercial strawberry fields in SP (Sato et al. 2009; Nicastro et al. 2010).
The initial frequency of abamectin resistance in TSSM from CPA was relatively low
(7.1 %), in spite of the fact that this compound has been used on strawberries for more than
20 years in Atibaia County. This result is probably due to the instability of abamectin
resistance (Sato et al. 2005; Nicastro et al. 2010) associated with the strawberry cultivation
system in this county. Sato et al. (2005) mentioned a decrease in abamectin resistance
frequency from 75 to \15 % in 6 months under laboratory conditions. The strawberry
cultivation period in Atibaia is normally from April to November. During the other period
of the year (5–6 months), there was no acaricide application in the field. In this aspect, the
interval from one season of strawberry to another may contribute significantly to the
reestablishment of susceptibility in TSSM. The immigration of susceptible (or resistant)
mites from other host plants may also affect the reestablishment of susceptibility in field
conditions (Miller et al. 1985).
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For fenpyroximate, the resistance was shown to be more stable in TSSM under labo-
ratory conditions. In a population with an initial resistance frequency of 75 %, the per-
centage of resistant mites decreased to 49.6 % within 1 year (Sato et al. 2004). This
stability is one of the factors that may have influenced the reestablishment of susceptibility
in the field, leading to a higher initial resistance frequency (24.2 %) for fenpyroximate in
TSSM in CPA.
Considering the evolution of acaricide resistance along the cultivation period, a similar
frequency of resistance of TSSM to fenpyroximate and abamectin (about 69 %) was
observed in September, 4 months after the first sampling, despite the fact that abamectin
was sprayed 59 more often than fenpyroximate in this period (May–September). One
possible explanation for the rapid evolution of fenpyroximate resistance is the dominance
of resistance. Studies of the genetics of fenpyroximate resistance in a strain of TSSM
collected from a commercial strawberry field in SP indicated that the fenpyroximate
resistance was controlled by one major, incompletely dominant factor (Sato et al. 2004).
The stability of fenpyroximate resistance may have also contributed to the rapid evolution
of resistance in the field.
For the acaricide propargite, although the grower did not apply this chemical in CPA
during the studied period, the compound had been used for many years in this area. The
high initial percentage (51.2 %) of propargite-resistant mites in CPA is probably due to the
migration of resistant mites from other host plants (Miller et al. 1985), such as roses and
other ornamental crops, cultivated in several commercial fields in Atibaia. The reduction in
the percentage of resistant mites from May to September was probably related to the
instability of propargite resistance in the absence of selection pressure (Grafton-Cardwell
et al. 1987).
In the case of IPA, although the number of acaricide applications was 69 lower than in
CPA, the TSSM infestations were significantly lower on the strawberry plants. This
reduction in TSSM abubdance was probably due to the release of the predaceous mite N.
californicus on the strawberry beds (Greco et al. 2004, 2005; Sato et al. 2007).
The strategies used in the area of integrated production of strawberry, including mon-
itoring the abundance of TSSM and use of the predaceous mite N. californicus in asso-
ciation with the selective acaricide propargite, were efficient to keep the TSSM infestation
levels lower than in the area of conventional production, allowing a reduction in the use of
acaricides by 69 in comparison with CPA. Another advantage associated with the use of
predaceous mites was the reduction in selection pressure for the evolution of pesticide (e.g.
abamectin and fenpyroximate) resistance in TSSM and other target pests [e.g. broad mite,
Polyphagotarsonemus latus (Banks; Acari: Tarsonemidae)] in IPA.
Acknowledgments The authors are thankful to the FAPESP (Sao Paulo Research Foundation) for fundingthis research (Processes # 2007/08612-4 and 2012/17972-2) and for the scholarship to the first author(Process # 2008/02103-3). We would also like to thank CNPq-Brazil (The National Council for Scientificand Technological Development) for the research fellowship provided to the second author, to Dr. HelymarMachado (UNICAMP) for the assistance in the statistical analysis, and to the growers for providing theexperimental areas.
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