ECOTOXICOLOGY

Chemical Alternatives to Malathion for Controlling Ceratitis capitata

(Diptera: Tephritidae), and Their Side Effects on Natural Enemies
in Spanish Citrus Orchards
ALBERTO URBANEJA,1,2 PATRICIA CHUECA,3 HELGA MONTÓN,1 SARA PASCUAL-RUIZ,1
OSCAR DEMBILIO,1 PILAR VANACLOCHA,1 RAQUEL ABAD-MOYANO,1 TATIANA PINA,1
4
AND PEDRO CASTAÑERA

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J. Econ. Entomol. 102(1): 144Ð151 (2009)
ABSTRACT The Mediterranean fruit ßy, Ceratitis capitata (Wiedemann) (Diptera: Tephritidae), is
one of the most important fruit pests worldwide. Mediterranean fruit ßy control in Spain has been
based on organophosphate sprays, especially malathion, mixed with protein baits. However, this
insecticide has recently been excluded from annex 1 of the Directive 91/414 CEE, which lists
authorized active ingredients for pest control in the European Union. This article reports on the
efÞcacy of four alternative baited insecticides on Mediterranean fruit ßy and their side effects on three
natural enemies [Cryptolaemus montrouzieri (Mulsant), Neoseiulus californicus (McGregor), and
Aphidius colemani (Viereck)] relevant for pest control in citrus agroecosystems. A high Mediterranean
fruit ßy mortality was obtained for all baited insecticides (phosmet and spinosad) except lambda-
cyhalothrin, which caused the lowest mortality and showed a novel disabling effect on surviving
Mediterranean fruit ßy adults. Spinosad proved to be the most selective bait treatment for C.
montrouzieri and N. californicus, whereas for A. colemani the most selective bait was phosmet and
lambda-cyhalothrin. These Þndings would contribute to a sustainable chemical control of C. capitata
populations under an integrated pest management system in Spanish citrus orchards.

KEY WORDS Aphidius colemani, Cryptolaemus montrouzieri, Neoseiulus californicus, baited insec-
ticides

The Mediterranean fruit ßy, Ceratitis capitata (Wiede-
mann) (Diptera: Tephritidae), is one of the most dev-
astating fruit pests worldwide. Mediterranean fruit ßy
control in Spain has primarily been based on applica-
tions of organophosphate insecticides, especially mal-
athion, mixed with protein baits (Primo et al. 2003). In
the Valencia region, in addition to ground applica-
tions, aerial treatments has been performed over large
areas as a part of a regional program against Mediter-
ranean fruit ßy (Primo et al. 2003). Although mala-
thion still shows a high rate of efÞcacy in controlling
C. capitata, pest control failures have recently been
observed in areas of the Mediterranean Basin where
this insecticide has been widely used. Resistant C.
capitata populations have developed as a result of the
intensity of insecticide treatments with malathion
1 Unidad Asociada de Entomologṍa IVIA-CIB/CSIC, Centro de
Protección Vegetal y Biotecnologṍa, Instituto Valenciano de Investiga-
ciones Agrarias (IVIA), Ctra. Moncada-Náquera km. 4,5, 46113-
Moncada, Valencia, Spain.
2 Corresponding author, e-mail: aurbaneja@ivia.es.
3 Centro de Agroingenierṍa, Instituto Valenciano de Investigaciones
Agrarias (IVIA), Ctra. Moncada-Náquera km. 4,5, 46113-Moncada, Va-
lencia, Spain.
4 Departamento Biologṍa de Plantas, Centro de Investigaciones
Biológicas (CIB), Consejo Superior de Investigaciones CientṍÞcas
(CSIC), C/Ramiro de Maetzu, 9, 28040, Madrid, Spain.
(Magaña et al. 2007). The use of malathion is contro-
versial because of human health concerns (Flessel et
al. 1993, Marty et al. 1994) and its harmful effects on
beneÞcial insects (Ehler and Endicott 1984, Urbaneja
et al. 2004). Furthermore, this insecticide has recently
been excluded from annex one of the Directive 91/414
CEE, which lists the active ingredients allowed for
pest control in the European Union.
In recent years, emphasis has been placed on im-
plementing safer environmental measures to control
the Mediterranean fruit ßy in Spain, which include
Þnding environmentally friendly insecticides. Spi-
nosad has been put forward as one insecticide (Adan
et al. 1996; King and Hennessey 1996; Sparks et al. 1998,
2001; Urbaneja et al. 2004). Compared with malathion,
this insecticide has a better environmental proÞle and
has been proved less toxic on some selected beneÞ-
cials (Michaud 2003, Williams et al. 2003, Stark et al.
2004, Urbaneja et al. 2004). At present, a spinosad bait
treatment, Spintor Cebo (named GF-120 in the Amer-
icas, Dow AgroSciencies Ibérica, Madrid, Spain), con-
taining spinosad and a mix of sugars, water, and at-
tractants (Dow AgroSciences 2002), is successfully
being used to control different tephritid pests world-
wide (Burns et al. 2001, Barry et al. 2003, Moreno and
Mangan 2003, Prokopy et al. 2003, Revis et al. 2004,

0022-0493/09/0144Ð0151$04.00/0 䉷 2009 Entomological Society of America

February 2009 URBANEJA ET AL.: CHEMICAL ALTERNATIVES TO MALATHION FOR C. capitata
Stark et al. 2004, Yee and Chapman 2005). Initial ap-
plications of Spintor Cebo in Spain showed promising
results in controlling Mediterranean fruit ßy (Vergou-
las and Torné 2003, Chueca et al. 2007).
The pyrethroid lambda-cyhalothrin and the organo-
phosphate phosmet are two other active ingredients
that have recently been recommended in Spain to
control C. capitata in bait treatments (Generalitat Va-
lenciana 2005).
To our knowledge, there is little information avail-
able regarding the nontarget effects of bait treatments.
Some previous works have been conducted with Spin-
tor Cebo and malathion bait treatments (Michaud
2003, Medina et al. 2003, Urbaneja et al. 2004, San
Andrés et al. 2006), although no information is avail-
able for the other baited insecticides mentioned
above.
Three groups of natural enemies are key to be pre-
served in integrated pest management (IPM) pro-
grams in Spanish citrus orchards by using natural
enemy-selective pesticides. These enemies are coc-
cinellid and phytoseiid predators and hymenopterous
parasitoids (Smith et al. 1997, Jacas and Garcia-Marṍ
2002, University of California 2006, Pascual-Ruiz and
Urbaneja 2006, Urbaneja et al. 2008). Most of the
studies have focused on measuring the acute toxicity
of these pesticides. However, this may only be a partial
measure of their deleterious effects; thus, sublethal
effects on arthropod physiology and behavior also
should be considered for a complete analysis of their
impact (Desneux et al. 2007).
The aims of this study were to evaluate the efÞcacy
and the long-term effect of three alternative baited
insecticides on C. capitata under laboratory conditions
and their side effects on the adult stage of three key
natural enemies in Spanish citrus orchards: the coc-
cinelid Cryptolaemus montrouzieri Mulsant, a mealy-
bug predator; the phytoseiid Neoseiulus californicus
McGregor, a spider mite predator; and the braconid
Aphidius colemani Viereck, an aphid parasitoid. Fur-
thermore, sublethal effects were estimated on C. capi-
tata and C. montrouzieri.
Materials and Methods
Experimental Conditions. Unless otherwise stated,
environmental conditions in experiments were 25 ⫾
2⬚C, 60 ⫾ 10% RH, and a photoperiod of 16:8 (L:D) h.
C. capitata. Adults used in this assay originated from
a laboratory colony maintained at the Instituto Va-
lenciano de Investigaciones Agrarias (IVIA),
Moncada (Valencia, Spain). For each experiment, to
obtain a cohort of adults, ⬇1,000 pupae ⬍24 h old were
collected and maintained in polymethyl methacrylate
transparent cages (20 by 20 by 20 cm) until adult
emergence. Three-day-old adults were used in all the
assays. Water and a diet consisting of a mixture of
enzymatic autolyzed brewerÕs yeast (Biokar Diagnos-
tics Co., Pantin, France) and sugar (1:4, wt:wt) were
supplied to the ßies until their use.
C. montrouzieri. Adults used in this assay were ob-
tained from Silla (Valencia, Spain) where they were
145
reared on the citrus mealybug Planococcus citri Risso
(Hemiptera: Pseudococcidae) on potato, Solanum tu-
berosum (L.), sprouts. These adults were supplied in
1.5 ml plastic vials where food, a mixture of honey and
agar (50%, wt:vol), was smeared on the inner side of
the hermetic lid. Prey was obtained from the same
source. Ten-day-old C. montrouzieri adults were used
in the experiments.
A. colemani. Mummies of the aphid parasitoid were
obtained from the commercial mass rearing (Aphipar,
Koppert Biological Systems S.L., Águilas, Spain) in
100-ml bottles containing 500 parasitized aphids.
Mummies were maintained in a polymethyl methac-
rylate cage (20 by 20 by 20 cm) in a climatic chamber
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until adult emergence. Then, adults were offered a
mixture of water and honey (3:1, vol:vol). Less than
24-h-old adults were used in all the experiments.
N. californicus. Predatory mites used came from a
laboratory colony, maintained on bean, Phaseolus vul-
garis L. ÔChicoÕ, plants infested with Tetranychus ur-
ticae Koch (Acari: Tetranychidae). The laboratory
colony was initiated from individuals collected in cit-
rus orchards located in Bétera (Valencia, Spain) and
maintained in a climatic chamber. A cohort of ⬍48-
h-old adults of N. californicus was used. Likely use of
this naturally occurring predator in citrus groves
should rely on inundative releases of N. californicus
adults (A.U., R.A., and T.P., unpublished data). Be-
cause we were interested in estimating the duration of
the harmful effect before release, we decided to use
this stage instead of immature stages, as recommended
by the International Organization for Biological Con-
trol (IOBC) Working Group ÔPesticides and BeneÞcial
OrganismsÕ standards (Hassan 1994).
Bait Treatments. Three experiments were con-
ducted varying the day of insectsÕ exposure to the
residues of insecticide and bait: 1) fresh residues, 2)
3-d-old residues, and 3) 6-d-old residues. Four baited
insecticides were assayed for each experiment: 1)
Spintor Cebo at 10%; 2) Orothion at 0.5% (malathion
50% [EC] wt:vol; Quṍmicas Oro, S.A., Valencia, Spain)
⫹ Nu-lure at 0.5%; 3) Imidan 50 WP at 0.25% (phosmet
50%, wt:wt; Gowan Española Fitosanitarios S.L., Bar-
celona, Spain) ⫹ Nu-lure at 0.5%; and 4) Karate King
at 0.5% (lambda-cyhalothrin 2.5%, wt:wt; Syngenta
Agro, S.A., Madrid, Spain) ⫹ Nu-lure at 0.5%. A con-
trol with mineral water also was considered in each
experiment.
Adult Mortality. To assay the mortality an extended
laboratory method was applied to C. capitata, C. mon-
trouzieri, and A. colemani adults (Medina et al. 2004).
Clementine, Citrus clementina Hort. ex Tan. var.
Nules, leaves were collected from small trees grown in
an insecticide-free greenhouse located at the IVIA.
The petiole of each leaf was put into a 1.5-ml micro-
centrifuge tubes (NIRCO S.L., Barberá del Vallès,
Spain) containing a nutritive solution to maintain leaf
turgidity during the experiments (Moutous and Fos
1973). The petiole of the leaf was sealed to the mi-
crocentrifuge tube with plasticine (Plastilina Jovi
JOVI, S.A. Barcelona, Spain). Five droplets of 5 ␮l of
the corresponding treatment were randomly distrib-
146 JOURNAL OF ECONOMIC ENTOMOLOGY
uted on the upside of the leaf with the use of a mi-
cropipette. The treated leaf was transferred and Þxed
with plasticine to the bottom of a plastic cage (15 by
7 by 10 cm in depth), with a hermetic lid having a mesh
area of 12 by 8 cm for ventilation.
Ten replicates of each treatment were used per each
residual period. In the fresh residue experiment, once
droplets were dried, 10 adults per replicate were in-
troduced. In the 3- and 6-d-old experiments, until
used, treated leaves were left undisturbed in a climatic
chamber at the climatic conditions described above.
In each cage and for all species, water was offered ad
libitum in a 1.5-ml microcentrifuge tube sealed with
cotton. C. capitata adults were fed with a mixture of
yeast and sugar (1:4, wt:wt) placed on an 1.5-ml mi-
crocentrifuge tube lid Þxed to the bottom of the cage
with plasticine. A. colemani and C. montrouzieri were
fed with a mixture of honey and water (3:1, vol:vol).
Each microcentrifuge tube was sealed with cotton and
Þxed to the bottom of the cage with plasticine.
In all three experiments, mortality of C. capitata and
C. montrouzieri was evaluated daily until the Þfth day
after adultsÕ introduction. Because previous data about
the side effect of Spintor Cebo on C. montrouzieri
were already available (Medina et al. 2003) the active
ingredient spinosad was not tested. Mortality of A.
colemani was only estimated until the second day in all
three experiments following the IOBC standards
(Mead-Briggs et al. 2000).
To assay mortality in the N. californicus experi-
ments, Clementine leaves also were used. Neverthe-
less, only one droplet of 5 ␮l of the corresponding
treatment was dispensed with a micropipette onto the
middle of the upside leaf. In the fresh residue exper-
iment, once the droplet was dried, a disc surface of 2
cm in diameter containing the droplet was extracted
from the leaf. Four leaf discs per treatment were
placed downside down on hydrophilic cotton soaked
in water in a plastic cage (14.5 by 10.5 by 10 cm in
depth). The soaked cotton prevented adults from es-
caping. Ten adults of N. californicus were introduced
per leaf disc with a Þne brush. The mite T. urticae was
offered ad libitum as prey in this arena. In the 3- and
6-d-old experiments, until used, treated leaves were
left undisturbed under the above-mentioned climatic
conditions.
Sublethal Effects. Ten surviving adults from the
fresh residue treatments of C. capitata were used to
estimate the bait treatment effect on their fecundity
and fertility. Females of C. capitata were individually
placed in the same cages used to evaluate mortality. To
assess fecundity, the total number of eggs laid through
the gauze was evaluated daily over a 4-d period.
Twenty eggs per female and day were randomly taken
with a Þne brush and placed on a rectangular piece of
black cardboard, which was kept on a permanently
wet dishcloth. The number of hatched eggs was used
to calculate fertility.
Surviving females of C. montrouzieri exposed to
fresh, 3- and 6-d-old residues were used to assess the
baited insecticide effect on fecundity and fertility by
placing them individually in the same cages used for
Vol. 102, no. 1
C. capitata experiments. Prey (a mixture of all instars
of P. citri) was offered on a piece of paper (2 by 3 cm),
which was used to gather up mealybugs from infested
sprouts. These pieces of paper also were used by C.
montrouzieri females as oviposition substrate and were
replaced daily and checked under a binocular micro-
scope to ascertain fecundity and fertility. Fecundity
was estimated over a 7-d period, and fertility was
calculated as the total number of eggs laid during this
period.
Data Analysis. For each experiment, percentage
mortality, fecundity, and fertility between treatments
were compared by means of one-way variance analysis
(ANOVA) at P ⬍ 0.05 (STSC Inc. 1987). When
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needed, data were transformed to achieve homosce-
dascity and normal distribution of residues. The least
signiÞcant difference (LSD) test was applied for mean
separation at P ⬍ 0.05. When signiÞcant differences
were found (P ⬍ 0.05), mortality was corrected using
the SchneiderÐOrelli formula (Bakr 2007). Subse-
quently, for natural enemies data were interpreted
according to the IOBC standards (Sterk et al. 1999),
which include four categories: 1) harmless (mortality
below 30%), 2) slightly harmful (31Ð79% mortality),
3) moderately harmful (80% to 99% mortality), and 4)
harmful (mortality higher than 99%).
Results
Efficacy on Mediterranean Fruit Fly. Mortality
caused by malathion, Imidan 50 WP, and Spintor Cebo
was almost 100% and signiÞcantly higher than Karate
King and the control treatment at the end of all three
experiments (fresh residue: F ⫽ 203.48; df ⫽ 4, 59; P ⬍
0.0001; 3-d-old residue: F ⫽ 58.11; df ⫽ 4,58; P ⬍ 0.0001;
6-d-old residue: F ⫽ 97.39; df ⫽ 4, 59; P ⬍ 0.0001)
(Table 1). The two organophosphates, Orothion and
Imidan 50 WP, killed more ßies than the spinosad
treatment in the Þrst 2 d of the experiments for fresh
residue and 3-d-old residue experiments. Mortality
results were similar during the three residual periods
tested for all baited insecticides.
On the Þfth day of evaluation, only adults treated
with Karate King and control survived in enough num-
bers to carry out the sublethal test. A novel disabling
effect was found on adults treated with Karate King,
which could hardly ßy inside the arena and their
movements were irregular. However, under the ex-
perimental conditions, females surviving Karate King
treatment were able to lay 54.9 ⫾ 16.0 eggs for a period
of 7 d. Although this value was much lower than in the
control group, where females laid 119.4 ⫾ 30.8 eggs, no
signiÞcant differences were found (F ⫽ 3.87; df ⫽ 1,
19; P ⫽ 0.065). Egg fertility rates were 32.2 ⫾ 13.2% for
Karate King and 56.3 ⫾ 10.1% for the control, without
signiÞcant differences (F ⫽ 2.09; df ⫽ 1, 19; P ⫽ 0.165).
Side Effects on C. montrouzieri. All products yielded
signiÞcantly higher mortality values than the control
(Table 2). In all three experiments, the toxic effects of
Karate King on C. montrouzieri were faster than the
other treatments. However, by the end of the exper-
iments, the mortality caused by all treatments was
February 2009 URBANEJA ET AL.: CHEMICAL ALTERNATIVES TO MALATHION FOR C. capitata 147

Table 1. Percentage mortality (mean ⴞ SE) of C. capitata adults exposed to either fresh, 3- or 6-d-old residues of different baited
insecticides plus a water-treated control

Day of evaluation
Residual age Treatment
1 2 3 4 5
Fresh residue Orothion 0.5% ⫹ Nu-lure 0.5% 63.4 ⫾ 6.3a 93.0 ⫾ 3.0a 97.0 ⫾ 2.1a 98.0 ⫾ 1.3a 98.0 ⫾ 1.3a
Imidan 50 WP 0.25% ⫹ Nu-lure 0.5% 57.6 ⫾ 5.5a 93.0 ⫾ 2.6a 99.0 ⫾ 1.0a 99.0 ⫾ 1.0a 100 ⫾ 0.0a
Karate King 0.5% ⫹ Nu-lure 0.5% 20.7 ⫾ 3.6b 32.1 ⫾ 5.7c 38.9 ⫾ 6.1c 41.9 ⫾ 6.9b 42.8 ⫾ 7.1b
Spintor Cebo 10% 18.1 ⫾ 2.5b 59.8 ⫾ 5.1b 82.9 ⫾ 5.6b 93.9 ⫾ 2.7a 95.9 ⫾ 1.7a
Control 2.5 ⫾ 1.2c 3.0 ⫾ 1.3d 3.0 ⫾ 1.3d 3.5 ⫾ 1.5c 6.0 ⫾ 2.3c
3-d-old Orothion 0.5% ⫹ Nu-lure 0.5% 56.1 ⫾ 6.8a 83.9 ⫾ 5.8a 83.9 ⫾ 5.8a 86.9 ⫾ 5.2a 92.0 ⫾ 4.2a
Imidan 50 WP 0.25% ⫹ Nu-lure 0.5% 59.2 ⫾ 6.2a 80.0 ⫾ 5.5a 88.9 ⫾ 4.8a 90.0 ⫾ 4.4a 93.3 ⫾ 4.4a
Karate King 0.5% ⫹ Nu-lure 0.5% 14.1 ⫾ 3.8c 19.2 ⫾ 4.7c 28.1 ⫾ 7.3b 34.4 ⫾ 8.7b 39.4 ⫾ 8.9b
Spintor Cebo 10% 32.8 ⫾ 3.7b 62.3 ⫾ 4.0b 85.2 ⫾ 2.7a 91.1 ⫾ 2.8a 95.1 ⫾ 2.2a
Control 0.0 ⫾ 0.0d 1.0 ⫾ 0.7d 2.0 ⫾ 1.2c 5.5 ⫾ 1.8c 15.7 ⫾ 4.3c
6-d-old Orothion 0.5% ⫹ Nu-lure 0.5% 44.1 ⫾ 10.7a 74.6 ⫾ 8.7a 80.9 ⫾ 7.4b 83.9 ⫾ 6.7b 88.9 ⫾ 4.3a

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Imidan 50 WP 0.25% ⫹ Nu-lure 0.5% 55.1 ⫾ 8.7a 83.9 ⫾ 2.6a 91.0 ⫾ 2.3b 98.0 ⫾ 1.3a 98.0 ⫾ 1.3a
Karate King 0.5% ⫹ Nu-lure 0.5% 16.6 ⫾ 4.4b 22.7 ⫾ 6.0b 32.0 ⫾ 5.7c 42.8 ⫾ 6.4c 45.0 ⫾ 6.6b
Spintor Cebo 10% 39.7 ⫾ 4.9a 73.9 ⫾ 4.0a 96.3 ⫾ 2.0a 100.0 ⫾ 0.0a 100.0 ⫾ 0.0a
Control 1.0 ⫾ 0.7c 1.5 ⫾ 0.8c 1.5 ⫾ 0.8d 4.9 ⫾ 2.0d 14.3 ⫾ 3.9c

In each residual age, within each column, mean values followed by a different letter are signiÞcantly different (P ⬍ 0.05; LSD test).

similar (⬇60%) and signiÞcantly different from the
control (fresh residue: F ⫽ 8.135; df ⫽ 3, 39; P ⬍ 0.0001;
3-d-old residue: F ⫽ 13.578; df ⫽ 3, 98; P ⬍ 0.0001;
6-d-old residue: F ⫽ 7.680; df ⫽ 3, 39; P ⬍ 0.0001).
These values represent corrected mortality of be-
tween 36 and 71%, which gives an IOBC category 2.
Fecundity of surviving females was not affected in
any case compared with the control (fresh residue:
F ⫽ 4.33; df ⫽ 3, 39; P ⫽ 0.010; 3-d-old residue: F ⫽ 2.72;
df ⫽ 3, 39; P ⫽ 0.097; 6-d-old residue: F ⫽ 1.19; df ⫽
3, 39; P ⫽ 0.150). Mean fecundity values were 28.9 ⫾
7.5, 25.5 ⫾ 5.0, and 42.5 ⫾ 3.9 eggs for fresh, 3-d-old
residues, and 6-d-old residues, respectively. Nor was
fertility affected (fresh residue: F ⫽ 1.23; df ⫽ 3, 29; P ⫽
0.319; 3-d-old residue: F ⫽ 0.468; df ⫽ 3, 26; P ⫽ 0.708;
6-d-old residue: F ⫽ 0.146; df ⫽ 3, 32; P ⫽ 0.743). Mean
fertility values were 62.7 ⫾ 7.1, 69.3 ⫾ 2.1, and 66.9 ⫾
1.3 for fresh, 3-d-old residues, and 6-d old residues,
respectively.
Side Effects on A. colemani. In the three residual
experiments, no signiÞcant differences were found
when Imidan and Karate King bait treatments were
compared with the control, irrespective of the residual
age (Table 3). Hence, both products were classed as
IOBC category 1 (harmless). However, Orothion
caused the highest mortality of A. colemani (94%),
reaching an IOBC category 3. Although the spinosad
bait treatment also yielded higher mortalities than the
control, it had a lower impact on this parasitoid (IOBC
category 2) (fresh residue: F ⫽ 24.69; df ⫽ 4, 34; P ⬍
0.0001; 3-d-old residue: F ⫽ 20.28; df ⫽ 4, 34; P ⬍ 0.0001;
6-d-old residue: F ⫽ 12.11; df ⫽ 4, 34; P ⬍ 0.0001).
Side Effects on N. californicus. At the end of the
experiments, statistically signiÞcant differences were
found between the control and all the baited insecti-
cides for the fresh residue (fresh residue: F ⫽ 37.63;
df ⫽ 4, 27; P ⬍ 0.0001; 3-d-old residue: F ⫽ 31.88; df ⫽
4, 27; P ⬍ 0.0001); 6-d-old residue: F ⫽ 15.31; df ⫽ 4,
27; P ⬍ 0.0001). The spinosad bait treatment caused
70% mortality on N. californicus, representing an IOBC
category 2, whereas Orothion and Imidan 50 WP
caused ⬇85% mortality, corresponding to an IOBC
category 3. Karate King was the most harmful insec-

Table 2. Percentage mortality (mean ⴞ SE) of C. montrouzieri adults exposed to either fresh, 3- or 6-d-old residues of different baited
insecticides plus a water-treated control

Day of evaluation IOBC

Residual age Treatment
1 4 6 categorya

Fresh residue Orothion 0.5% ⫹ Nu-lure 0.5% 7.0 ⫾ 2.6b 18.0 ⫾ 3.3bc 51.0 ⫾ 7.4a 2
Imidan 50 WP 0.25% ⫹ Nu-lure 0.5% 5.0 ⫾ 2.2b 26.0 ⫾ 8.8ab 43.0 ⫾ 10.3a 2
Karate King 0.5% ⫹ Nu-lure 0.5% 18.8 ⫾ 4.8a 43.7 ⫾ 9.6a 61.8 ⫾ 9.4a 2
Control 1.1 ⫾ 1.1b 3.3 ⫾ 1.7c 10.0 ⫾ 2.4b
3-d-old Orothion 0.5% ⫹ Nu-lure 0.5% 10.3 ⫾ 4.0b 51.1 ⫾ 7.2a 74.9 ⫾ 9.1a 2
Imidan 50 WP 0.25% ⫹ Nu-lure 0.5% 12.0 ⫾ 3.9b 45.0 ⫾ 9.0a 65.0 ⫾ 9.1a 2
Karate King 0.5% ⫹ Nu-lure 0.5% 33.2 ⫾ 7.0a 55.6 ⫾ 7.2a 66.7 ⫾ 7.0a 2
Control 5.0 ⫾ 2.2b 8.0 ⫾ 2.9b 13.0 ⫾ 4.5b
6-d-old Orothion 0.5% ⫹ Nu-lure 0.5% 3.0 ⫾ 1.5b 29.3 ⫾ 4.4ab 42.7 ⫾ 4.8a 2
Imidan 50 WP 0.25% ⫹ Nu-lure 0.5% 9.3 ⫾ 4.3b 46.7 ⫾ 10.7a 52.9 ⫾ 11.8a 2
Karate King 0.5% ⫹ Nu-lure 0.5% 38.1 ⫾ 8.8a 47.2 ⫾ 8.4a 60.2 ⫾ 10.1a 2
Control 1.1 ⫾ 1.1b 9.2 ⫾ 3.6b 8.2 ⫾ 3.4b

In each residual age, within each column, mean values followed by a different letter are signiÞcantly different (P ⬍ 0.05, LSD test).
a
IOBC standards: 1, harmless; 2, slightly harmful; 3, moderately harmful; and 4, harmful corresponding to the mortality observed for the sixth
day of evaluation.
148 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 102, no. 1

Table 3. Percentage mortality (mean ⴞ SE) of A. colemani adults exposed to either fresh, 3- or 6 d-old residues of different baited
insecticides plus a water-treated control

Day of evaluation IOBC

Residual age Treatment
1 2 category*

Fresh residues Orothion 0.5% ⫹ Nu-lure 0.5% 66.0 ⫾ 13.2a 89.4 ⫾ 7.0a 3
Imidan 50 WP 0.25% ⫹ Nu-lure 0.5% 4.9 ⫾ 3.6b 6.2 ⫾ 4.1b 1
Karate King 0.5% ⫹ Nu-lure 0.5% 1.4 ⫾ 1.4b 17.4 ⫾ 8.3b 1
Spintor Cebo 10% 13.7 ⫾ 6.5b 20.8 ⫾ 10.0b 1
Control 3.4 ⫾ 2.2b 7.9 ⫾ 3.2b
3-d-old Orothion 0.5% ⫹ Nu-lure 0.5% 74.8 ⫾ 6.4a 94.0 ⫾ 3.9a 3
Imidan 50 WP 0.25% ⫹ Nu-lure 0.5% 26.3 ⫾ 9.5b 34.4 ⫾ 9.5bc 1
Karate King 0.5% ⫹ Nu-lure 0.5% 16.5 ⫾ 3.6b 32.0 ⫾ 5.5bc 1
Spintor Cebo 10% 16.8 ⫾ 5.0b 46.1 ⫾ 6.3b 1
Control 12.9 ⫾ 3.6b 25.4 ⫾ 3.7c
6-d-old Orothion 0.5% ⫹ Nu-lure 0.5% 54.3 ⫾ 6.9a 82.9 ⫾ 4.7a 2

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Imidan 50 WP 0.25% ⫹ Nu-lure 0.5% 7.5 ⫾ 3.8b 21.1 ⫾ 1.5c 1
Karate King 0.5% ⫹ Nu-lure 0.5% 7.1 ⫾ 2.9b 22.9 ⫾ 5.2c 1
Spintor Cebo 10% 14.4 ⫾ 4.3b 47.9 ⫾ 9.8b 2
Control 13.3 ⫾ 5.0b 21.9 ⫾ 6.5c

In each residual age, within each column, mean values followed by a different letter are signiÞcantly different (P ⬍ 0.05; LSD test).
a
IOBC standards: 1, harmless; 2, slightly harmful; 3, moderately harmful; and 4, harmful corresponding to the mortality corrected observed
for second day of evaluation.

ticide, reaching 100% mortality in the 6-d-old residue,
corresponding to an IOBC category 4 (Table 4).
Discussion
The two organophosphates Orothion and Imidan 50
WP and also Spintor Cebo were highly effective in
killing C. capitata, with a mortality rate of ⬇100%.
Karate King produced lower Mediterranean fruit ßy
mortality rates, with values of ⬇40%. However, it
caused a disabling effect on adults, which could not ßy
and displayed irregular movements. A reduction in
Mediterranean fruit ßy fecundity and fertility also
were observed for this insecticide, although differ-
ences were not signiÞcant. This pyrethroid was
sprayed in certain citrus-growing areas of the Valencia
region in 2007 and gave good results in controlling C.
capitata. An explanation for these differences could be
related to the disabling effect under Þeld conditions,
because females fed on this pyrethroid might not have
been able to reach the fruits to oviposit and, conse-
quently, no damage was found. Nevertheless, further
research is needed to clarify this issue.
The baited insecticide treatments are considered
generally harmless on nontarget organisms (Roessler
1989), although the use of a nonspeciÞc C. capitata bait
also could attract natural enemies. In this study, the
natural enemies behaved differently depending on the
arthropod species and the insecticide bait treatment.
Spinosad-baited treatment turned out to be the most
selective for C. montrouzieri and N. californicus,
whereas for A. colemani the most selective were phos-
met and lambda-cyhalothrin. To our knowledge, this
is the Þrst time reporting on the side effects of the
baited organophosphate phosmet and the pyrethroid
lambda-cyhalothrin. The effect of lambda-cyhalothrin

Table 4. Percentage mortality (mean ⴞ SE) of N. californicus adults exposed to either fresh, 3- or 6-d-old residues of different baited
insecticides plus a water-treated control

Day of evaluation IOBC

Residual age Treatment
1 4 6 categorya

Fresh residues Orothion 0.5% ⫹ Nu-lure 0.5% 25.1 ⫾ 9.4ab 72.1 ⫾ 7.8ab 87.4 ⫾ 4.1ab 3
Imidan 50 WP 0.25% ⫹ Nu-lure 0.5% 22.5 ⫾ 6.3abc 82.5 ⫾ 2.5a 95.0 ⫾ 5.0ab 3
Karate King 0.5% ⫹ Nu-lure 0.5% 47.5 ⫾ 8.5a 87.5 ⫾ 6.3a 97.5 ⫾ 2.5a 3
Spintor Cebo 10% 7.5 ⫾ 4.8bc 52.5 ⫾ 4.8b 77.5 ⫾ 4.8b 2
Control 6.3 ⫾ 3.3c 26.3 ⫾ 6.0c 26.3 ⫾ 6.0c
3-d-old Orothion 0.5% ⫹ Nu-lure 0.5% 0.0 ⫾ 0.0b 51.3 ⫾ 5.2b 86.3 ⫾ 4.2ab 2
Imidan 50 WP 0.25% ⫹ Nu-lure 0.5% 5.0 ⫾ 2.9b 30.0 ⫾ 5.8cd 80.0 ⫾ 13.5ab 2
Karate King 0.5% ⫹ Nu-lure 0.5% 7.5 ⫾ 4.1a 77.5 ⫾ 2.5a 97.5 ⫾ 2.5a 3
Spintor Cebo 10% 0.0 ⫾ 0.0b 45.0 ⫾ 2.9bc 70.0 ⫾ 5.8b 2
Control 6.3 ⫾ 1.8b 21.3 ⫾ 3.5c 21.3 ⫾ 3.5c
6-d-old Orothion 0.5% ⫹ Nu-lure 0.5% 5.0 ⫾ 1.9c 60.0 ⫾ 9.1b 85.0 ⫾ 4.6a 2
Imidan 50 WP 0.25% ⫹ Nu-lure 0.5% 7.5 ⫾ 2.5c 87.5 ⫾ 4.8a 87.5 ⫾ 4.8a 3
Karate King 0.5% ⫹ Nu-lure 0.5% 37.5 ⫾ 7.5a 95.0 ⫾ 5.0a 100 ⫾ 0.0a 4
Spintor Cebo 10% 22.5 ⫾ 4.8b 45.0 ⫾ 5.0b 82.5 ⫾ 6.3a 2
Control 3.8 ⫾ 2.6c 11.3 ⫾ 4.4c 32.5 ⫾ 9.4b

In each residual age, within each column, mean values followed by a different letter are signiÞcantly different (P ⬍ 0.05; LSD test).
a
IOBC standards: 1, harmless; 2, slightly harmful; 3, moderately harmful; and 4, harmful corresponding to the mortality corrected observed
for the sixth day of evaluation.
February 2009 URBANEJA ET AL.: CHEMICAL ALTERNATIVES TO MALATHION FOR C. capitata
on N. californicus was the only effect to yield an IOBC
category 4 in this study. The harmful effects of con-
ventionally spraying of this pyrethroid onto the most
common predatory mite in Spanish citrus orchards,
Euseius stipulatus Athias-Henriot, were already known
(Jacas and Garcia-Marṍ 2002). This was not the case for
Spintor Cebo at 10% and Orothion at 0.5% ⫹ Nu-lure
at 0.5%, both of which proved harmless against E.
stipulatus in a Þeld experiment (San Andrés et al.
2006).
Some previous results on the side effects of spi-
nosad- and malathion-baited treatments also are avail-
able. The effects of these pesticides were studied on
C. cryptolaemus and on vedalia, Rodolia cardinalis
(Mulsant) (Coleoptera: Coccinellidae), under labo-
ratory (Medina et al. 2003) and semiÞeld conditions
(Medina et al. 2004). The results of these studies
showed that Spintor Cebo was harmless for both pred-
ators, whereas malathion plus the proteinaceous bait
proved moderately harmful (IOBC category 3). Sim-
ilar results for both baited insecticides have been ob-
tained for several key citrus predators in Florida
(Michaud 2003). In the study conducted in Florida,
both malathion and spinosad proved toxic for two
parasitoids that are already abundant in Spanish citrus
orchards, the aphid parasitoid Lysiphlebus testaceipes
Cresson (Hymenoptera: Braconidae) and the ar-
mored scale parasitoid Aphytis melinus DeBach (Hy-
menoptera: Aphelinidae).
The sublethal effects of both malathion and spi-
nosad baited treatments also have been studied in four
other parasitoids (Urbaneja et al. 2004). Following the
same methodology described in the current study,
both insecticides killed ⬇60% of adults in Citrostichus
phyllocnistoides Narayan (Hymenoptera: Eulophi-
dae), the most important citrus leafminer parasitoid in
the Mediterranean Basin. However, malathion was
classiÞed as harmful on C. phyllocnistoides due to re-
duced fecundity and fertility of surviving females,
whereas Spintor Cebo did not show any sublethal
effect. In the same study, malathion also proved harm-
ful against the Mediterranean fruit ßy parasitoid Dia-
chasmimorpha tryoni (Cameron) (Hymenoptera:
Braconidae), the mealybug parasitoid Anagyrus
pseudococci (Girault) (Hymenoptera: Encyrtidae),
and the leafminer parasitoid Diglyphus isaea (Walter)
(Hymenoptera: Eulophidae), whereas Spintor Cebo
yielded harmless.
Most studies on the side effects of spinosad empha-
size that this insecticide is generally selective for pred-
ators but not for parasitoids (Williams et al. 2003).
However, in the case of baited treatments, it seems
that different side effects can be obtained depending
on the parasitoid species. Indeed, the integration of
baited spinosad and parasitoid releases is possible
(Vargas et al. 2001). In coffee plantations in Hawaii a
study was made to assess the possibility of integrating
Spintor Cebo or malathion bait treatments with con-
servation of the parasitoid Fopius arisanus (Sonan)
(Hymenoptera: Braconidae), concluding that the
Þelds treated with spinosad were more easily colo-
nized by the parasitoids than those treated with mal-
149
athion (Vargas et al. 2001). Based on these results, in
Hawaii and other American areas where C. capitata
and other tephritids are key pests, the guidelines for
areawide integrated strategies combine environmen-
tally safe bait treatments with the release and conser-
vation of natural enemies. In recent years, emphasis
has been placed on implementing these measures to
control the Mediterranean fruit ßy in Spain. To this
end, two different approaches to biological control are
currently being considered. The Þrst is a classical bi-
ological control program introducing two exotic para-
sitoids, F. arisanus and D. tryoni (Santiago et al. 2006,
Pérez-Hinarejos et al. 2006), whereas the second ap-
proach involves identifying and conserving both
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polyphagous predators and indigenous parasitoids of
the Mediterranean fruit ßy (Falcó et al. 2006, Urbaneja
et al. 2006).
In summary, our results could help to integrate
biological and chemical control of Mediterranean fruit
ßy in citrus orchards. A bait-formulation containing
spinosad seem to be the best option when considering
pest control efÞcacy together with the side effects on
the three beneÞcial arthropods chosen for this study
and on the others available. However, the negative
effects on some parasitoid species should not be ne-
glected. Special attention should be paid when aug-
mentative biological control strategies are imple-
mented that based on parasitoid releases [as could be
the case with A. melinus against the California red
scale, Aonidiella aurantii (Maskell) (Hemiptera: Di-
aspididae)].
Acknowledgments
We thank J. Calvo and J. E. Belda (Koppert Biological
System S. L., Águilas, Spain) for the A. colemani supply; I.
Boix, R. Aparici, and J. L. Porcuna for the C. montrouzieri
supply, and F. Barraclough for correcting the English. This
research was partially funded by the Instituto Nacional de
Investigación y Tecnologṍa Agraria (RTA03-103C601), by
the Conselleria dÕAgricultura, Pesca i Alimentació de la Gen-
eralitat Valenciana, and FEOGA COOPERACIÓN. R.A. and
P.C. were recipients of a grant from IVIA.
References Cited
Adan, A., P. del Estal, F. Budia, M. González, and E. Viñuela.
1996. Laboratory evaluation of the novel naturally de-
rived compound spinosad against Ceratitis capitata. Pes-
tic. Sci. 48: 261Ð268.
Bakr, E. 2007. LdP Line. (http://embakr.tripod.com/ldpline/
index.htm).
Barry, J. D., R. I. Vargas, N. W. Miller, and J. G. Morse. 2003.
Feeding and foraging of wild and sterile Mediterranean
fruit ßies (Diptera: Tephritidae) in the presence of spi-
nosad bait. J. Econ. Entomol. 96: 1405Ð1411.
Burns, R. E., D. L. Harris, D. S. Moreno, and J. E. Eger. 2001.
EfÞcacy of spinosad bait sprays to control Mediterranean
and Caribbean fruit ßies (Diptera: Tephritidae) in com-
mercial citrus in Florida. Fla. Entomol. 84: 672Ð 678.
Chueca, P., H. Montón, J. L. Ripollés, P. Castañera, E. Moltó,
and A. Urbaneja. 2007. Spinosad bait treatments as al-
ternative to malathion to control the Mediterranean fruit
150 JOURNAL OF ECONOMIC ENTOMOLOGY
ßy Ceratitis capitata (Diptera: Tephritidae) in the Med-
iterranean Basin. J. Pestic. Sci. 32: 407Ð 411.
Desneux, N., A. Decourtye, and J. M. Delpuech. 2007. The
sublethal effects of pesticides on beneÞcial arthropods.
Annu. Rev. Entomol. 52: 81Ð106.
Dow AgroSciences. 2002. GF-120 Naturalyte. Fruit ßy bait. In-
secticidal bait. (http://www.cdms.net/ldat/ld62A001.pdf).
Ehler, L. E., and P. C. Endicott. 1984. Effect of malathion
bait sprays on biological control of insect pest of olive,
citrus, and walnut. Hilgardia 52: 1Ð 47.
Falcó, J. V., I. Tarazona, M. Pérez-Hinarejos, E. Garzón-
Luque, J. Malagón, and F. Beitia. 2006. Two native pupal
parasitoids of Ceratitis capitata (Diptera, Tephritidae)
found in Spain. IOBC/WPRS Bull. 29: 71Ð75.
Flessel, P., P.J.E. Quintana, and K. Hooper. 1993. Genetic
toxicity of malathion: a review. Environ. Mol. Mutagen.
22: 7Ð17.
Generalitat Valenciana. 2005. Bulletṍ dÕAvisos de la Gener-
alitat Valenciana, Juny. 87: 17Ð20.
Hassan, S. A. 1994. Activities of the IOBC/WPRS working
group pesticides and beneÞcial organisms. IOBC/WPRS
Bull. 17: 1Ð5.
Jacas, J. A., and F. Garcia-Marı́. 2002. Side-effects of pesti-
cides on selected natural enemies occurring in citrus in
Spain. IOBC Bull. 24: 103Ð112.
King, J. R., and M. H. Hennessey. 1996. Spinosad bait for the
Caribbean fruit ßy (Diptera: Tephritidae). Fla. Entomol.
79: 526 Ð531.
Magaña, C., P. Hernández-Crespo, F. Ortego, and P. Castañ-
era. 2007. Resistance to malathion in Þeld populations of
Ceratitis capitata. J. Econ. Entomol. 100: 1836 Ð1843.
Marty, M. A., S. V. Dawson, M. A. Bradman, M. E. Harnly, and
M. J. Dibartolomeis. 1994. Assessment of exposure to
malathion and maloxon due to aerial application over
urban areas of southern California. J. Exp. Anal. Environ.
Epidemiol. 4: 65Ð 81.
Mead-Briggs, M. A., K. Brown, M. P. Candolfi, M.J.M. Coul-
son, M. Miles, M. Moll, K. Nienstedt, M. Schuld, A. Ufer,
and E. McIndoe. 2000. A laboratory test for evaluating
the effects of plant protecting products on the parasitic
wasp, Aphidius rhopalosiphi (DeStephani-Perez) (Hy-
menoptera: Braconidae). In M. P. e. al. CandolÞ [ed.],
Guidelines to evaluate side-effects of plant protection
products to non-target arthropods. IOBC, BART and
EPPO Joint Initiative. WPRS/SROP, Dijon, France.
Medina, P., A. Adán, F. Budia, P. Del Estal, and E. Viñuela.
2003. Estudios de laboratorio extendido de la actividad
de Spinosad GF-120 en Ceratitis capitata (Wiedemann)
(Diptera: Tephritidae) y en fauna auxiliar de los cṍtricos.
III Congreso Nacional de Entomologṍa Aplicada, IX Jor-
nadas CientṍÞcas de la Sociedad Española de Entomologṍa
Aplicada 188.
Medina, P., I. López, F. Budia, A. Adán, and E. Viñuela. 2004.
Development of an extended-laboratory method to test
bait treatments. IOBC/WPRS Bull. 27: 59 Ð 66.
Michaud, J. P. 2003. Toxicity of fruit ßy baits to beneÞcial
insects in citrus. J. Insect Sci. 3: 8.
Moreno, D. S., and R. L. Mangan. 2003. Bait matrix for novel
toxicants for use in control of fruit ßies (Diptera: Te-
phritidae), pp. 333Ð362. In C. Schwalbe [ed.], Invasive
arthropods in agriculture. Science Publishers, Inc., En-
Þeld, NH.
Moutous, G., and A. Fos. 1973. Essais de rhizogénèse chez la
feuille de vigne isolée. Rev. Zool. Agric. Pathol. Veg.
Premier Trimestre: 27Ð28.
Pascual-Ruiz, S., and A. Urbaneja. 2006. Lista de efectos
secundarios de plaguicidas sobre fauna útil en cṍtricos.
Levante Agrṍcola 380: 186 Ð191.
Vol. 102, no. 1
Pérez-Hinarejos, M., S. Santiago, J. V. Falcó, and F. Beitia.
2006. Laboratory experiments with Fopius arisanus, an
exotic egg-pupal parasitoid of Ceratitis capitata. IOBC/
WPRS Bull. 29: 209 Ð214.
Primo, E., F. Alfaro, and R. Argilés. 2003. Plan de actuación
contra la mosca de las frutas (Ceratitis capitata) en la
Comunidad Valenciana. Phytoma España 153: 127Ð130.
Prokopy, R. J., N. W. Miller, J. C. Piñero, J. D. Barry, L. C.
Tran, L. Oride, and R. I. Vargas. 2003. Effectiveness of
GF-120 fruit ßy bait spray applied to border area plants
for control of melon ßies (Diptera: Tephritidae). J. Econ.
Entomol. 96: 1485Ð1493.
Revis, H. C., N. W. Miller, and R. I. Vargas. 2004. Effects of
aging and dilution on attraction and toxicity of GF-120
fruit ßy bait spray for melon ßy control in Hawaii. J. Econ.
Downloaded from https://academic.oup.com/jee/article/102/1/144/2199105 by guest on 06 June 2023
Entomol. 97: 1659 Ð1665.
Roessler, Y. 1989. Insecticidal bait and cover sprays, pp.
329 Ð335. In A. S. Robinson and G. Hopper [eds.], Fruit
ßies, their biology, natural enemies and control. Elsevier,
Amsterdam, The Netherlands.
San Andrés, V., R. Abad, T. Ansaloni, S. Aucejo, B. Belliure,
O. Dembilio, J. A. Jacas, J. Mora, S. Pascual-Ruiz, T. Pina,
et al. 2006. Efectos secundarios sobre Euseius stipulatus
de tratamientos cebo dirigidos al control de Ceratitis
capitata. Phytoma España 180: 38 Ð 45.
Santiago, S., M. Pérez-Hinarejos, E. Garzón-Luque, F. Beitia,
and J. V. Falcó. 2006. Parasitism of Diachasmimorpha
tryoni on Mediterranean fruits infested with Ceratitis
capitata larvae in laboratory. IOBC/WPRS Bull. 29: 205Ð
208.
Smith, D., G.A.C. Beattie, and R. Broadley. 1997. Citrus
pests and their natural enemies. Integrated pest manage-
ment in Australia. State of Queensland, DPI & HRDC,
Brisbane, Australia.
Sparks, T. C., G. D. Thompson, H. A. Kirst, M. B. Herlein,
L. L. Larson, T. V. Worden, and S. T. Thibault. 1998.
Biological activity of the spinosyns, new fermentation
derived insect control agents on tobacco budworm (Lep-
idoptera: Noctuidae) larvae. J. Econ. Entomol. 91: 1277Ð
1283.
Sparks, T. C., G. D. Crouse, and G. Durst. 2001. Natural
products as insecticides: the biology, biochemistry and
quantitative structure-activity relationships of spinosyns
and spinosoids. Pest Manag. Sci. 57: 896 Ð905.
Stark, J. D., R. Vargas, and N. Miller. 2004. Toxicity of spi-
nosad in protein bait to three economically important
tephritid fruit ßy species (Diptera: Tephritidae) and their
parasitoids (Hymenoptera: Braconidae). J. Econ. Ento-
mol. 97: 911Ð915.
Sterk, G., S. A. Hassan, M. Baillod, F. Bakker, F. Bigler, S.
Blümel, H. Bogenschütz, E. Boller, B. Bromand, J. Brun,
et al. 1999. Results of the seventh joint pesticide testing
programme carried out by the IOBC/WPRS-Working
Group “Pesticides and BeneÞcial Organisms”. Biocontrol
44: 99 Ð117.
STSC Inc. 1987. Statgraphics userÕs guide, version 5.0.
Graphic software system. STSC Inc., Rockville, MD.
University of California. 2006. IPM pest management
guidelines: citrus. (http://www.ipm.ucdavis.edu/PDF/
PMG/pmgcitrus.pdf).
Urbaneja, A., O. Dembilio, D. Tortosa, E. Viñuela, and P.
Castañera. 2004. Efectos secundarios de tratamientos
cebo usados para el control de Ceratitis capitata, sobre
fauna útil. Phytoma España 160: 28 Ð 40.
Urbaneja, A., F. G. Mari, D. Tortosa, C. Navarro, P. Vana-
clocha, L. Bargues, and P. Castanera. 2006. Inßuence of
ground predators on the survival of the Mediterranean
February 2009 URBANEJA ET AL.: CHEMICAL ALTERNATIVES TO MALATHION FOR C. capitata
fruit ßy pupae, Ceratitis capitata, in Spanish citrus or-
chards. Biocontrol 51: 611Ð 626.
Urbaneja, A., S. Pascual-Ruiz, T. Pina, R. Abad-Moyano, H.
Montón, P. Castañera, and J. A. Jacas. 2008. EfÞcacy of
some acaricides against Tetranychus urticae (Acari: Tet-
ranychidae) and their side-effects on selected natural
enemies occurring in citrus orchards. Pest Manag. Sci. 64:
834 Ð 842.
Vargas, R. I., S. L. Peck, G. T. McQuate, C. G. Jackson, J. D.
Stark, and J. W. Armstrong. 2001. Potential for areawide
integrated management of Mediterranean fruit ßy
(Diptera: Tephritidae) with a braconid parasitoid and a
novel bait spray. J. Econ. Entomol. 94: 817Ð 825.
151
Vergoulas, P., and M. Torné. 2003. SPINOSAD CEBO*: un
sistema innovador para el control de la mosca del medi-
terráneo. Phytoma España 153: 134 Ð138.
Williams, T., J. Valle, and E. Viñuela. 2003. Is the naturally
derived insecticide Spinosad compatible with insect nat-
ural enemies? Biol. Sci. Technol. 13: 459 Ð 475.
Yee, L. Y., and P. S. Chapman. 2005. Effects of GF-120 fruit
ßy bait concentrations on attraction, feeding, mortal., and
control of Rhagoletis indifferens (Diptera: Tephritidae). J.
Econ. Entomol. 98: 1654 Ð1663.
Received 14 March 2008; accepted 25 June 2008.
Downloaded from https://academic.oup.com/jee/article/102/1/144/2199105 by guest on 06 June 2023