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- (Magaña et al. 2007). The use of malathion is contro-
mann) (Diptera: Tephritidae), is one of the most dev- versial because of human health concerns (Flessel et
astating fruit pests worldwide. Mediterranean fruit ßy al. 1993, Marty et al. 1994) and its harmful effects on
control in Spain has primarily been based on applica- beneÞcial insects (Ehler and Endicott 1984, Urbaneja
tions of organophosphate insecticides, especially mal- et al. 2004). Furthermore, this insecticide has recently
athion, mixed with protein baits (Primo et al. 2003). In been excluded from annex one of the Directive 91/414
the Valencia region, in addition to ground applica- CEE, which lists the active ingredients allowed for
tions, aerial treatments has been performed over large pest control in the European Union.
areas as a part of a regional program against Mediter- In recent years, emphasis has been placed on im-
ranean fruit ßy (Primo et al. 2003). Although mala- plementing safer environmental measures to control
thion still shows a high rate of efÞcacy in controlling the Mediterranean fruit ßy in Spain, which include
C. capitata, pest control failures have recently been Þnding environmentally friendly insecticides. Spi-
observed in areas of the Mediterranean Basin where nosad has been put forward as one insecticide (Adan
this insecticide has been widely used. Resistant C. et al. 1996; King and Hennessey 1996; Sparks et al. 1998,
capitata populations have developed as a result of the 2001; Urbaneja et al. 2004). Compared with malathion,
intensity of insecticide treatments with malathion this insecticide has a better environmental proÞle and
has been proved less toxic on some selected beneÞ-
1 Unidad Asociada de Entomologṍa IVIA-CIB/CSIC, Centro de cials (Michaud 2003, Williams et al. 2003, Stark et al.
Protección Vegetal y Biotecnologṍa, Instituto Valenciano de Investiga- 2004, Urbaneja et al. 2004). At present, a spinosad bait
ciones Agrarias (IVIA), Ctra. Moncada-Náquera km. 4,5, 46113-
Moncada, Valencia, Spain.
treatment, Spintor Cebo (named GF-120 in the Amer-
2 Corresponding author, e-mail: aurbaneja@ivia.es. icas, Dow AgroSciencies Ibérica, Madrid, Spain), con-
3 Centro de Agroingenierṍa, Instituto Valenciano de Investigaciones taining spinosad and a mix of sugars, water, and at-
Agrarias (IVIA), Ctra. Moncada-Náquera km. 4,5, 46113-Moncada, Va- tractants (Dow AgroSciences 2002), is successfully
lencia, Spain.
4 Departamento Biologṍa de Plantas, Centro de Investigaciones being used to control different tephritid pests world-
Biológicas (CIB), Consejo Superior de Investigaciones CientṍÞcas wide (Burns et al. 2001, Barry et al. 2003, Moreno and
(CSIC), C/Ramiro de Maetzu, 9, 28040, Madrid, Spain. 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 145

Stark et al. 2004, Yee and Chapman 2005). Initial ap- reared on the citrus mealybug Planococcus citri Risso
plications of Spintor Cebo in Spain showed promising (Hemiptera: Pseudococcidae) on potato, Solanum tu-
results in controlling Mediterranean fruit ßy (Vergou- berosum (L.), sprouts. These adults were supplied in
las and Torné 2003, Chueca et al. 2007). 1.5 ml plastic vials where food, a mixture of honey and
The pyrethroid lambda-cyhalothrin and the organo- agar (50%, wt:vol), was smeared on the inner side of
phosphate phosmet are two other active ingredients the hermetic lid. Prey was obtained from the same
that have recently been recommended in Spain to source. Ten-day-old C. montrouzieri adults were used
control C. capitata in bait treatments (Generalitat Va- in the experiments.
lenciana 2005). A. colemani. Mummies of the aphid parasitoid were
To our knowledge, there is little information avail- obtained from the commercial mass rearing (Aphipar,
able regarding the nontarget effects of bait treatments. Koppert Biological Systems S.L., Águilas, Spain) in
Some previous works have been conducted with Spin- 100-ml bottles containing 500 parasitized aphids.
tor Cebo and malathion bait treatments (Michaud Mummies were maintained in a polymethyl methac-
2003, Medina et al. 2003, Urbaneja et al. 2004, San rylate cage (20 by 20 by 20 cm) in a climatic chamber

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Andrés et al. 2006), although no information is avail- until adult emergence. Then, adults were offered a
able for the other baited insecticides mentioned mixture of water and honey (3:1, vol:vol). Less than
above. 24-h-old adults were used in all the experiments.
Three groups of natural enemies are key to be pre- N. californicus. Predatory mites used came from a
served in integrated pest management (IPM) pro- laboratory colony, maintained on bean, Phaseolus vul-
grams in Spanish citrus orchards by using natural garis L. ÔChicoÕ, plants infested with Tetranychus ur-
enemy-selective pesticides. These enemies are coc- ticae Koch (Acari: Tetranychidae). The laboratory
cinellid and phytoseiid predators and hymenopterous colony was initiated from individuals collected in cit-
parasitoids (Smith et al. 1997, Jacas and Garcia-Marṍ rus orchards located in Bétera (Valencia, Spain) and
2002, University of California 2006, Pascual-Ruiz and maintained in a climatic chamber. A cohort of ⬍48-
Urbaneja 2006, Urbaneja et al. 2008). Most of the h-old adults of N. californicus was used. Likely use of
studies have focused on measuring the acute toxicity this naturally occurring predator in citrus groves
of these pesticides. However, this may only be a partial should rely on inundative releases of N. californicus
measure of their deleterious effects; thus, sublethal adults (A.U., R.A., and T.P., unpublished data). Be-
effects on arthropod physiology and behavior also cause we were interested in estimating the duration of
should be considered for a complete analysis of their the harmful effect before release, we decided to use
impact (Desneux et al. 2007). this stage instead of immature stages, as recommended
The aims of this study were to evaluate the efÞcacy by the International Organization for Biological Con-
and the long-term effect of three alternative baited trol (IOBC) Working Group ÔPesticides and BeneÞcial
insecticides on C. capitata under laboratory conditions OrganismsÕ standards (Hassan 1994).
and their side effects on the adult stage of three key Bait Treatments. Three experiments were con-
natural enemies in Spanish citrus orchards: the coc- ducted varying the day of insectsÕ exposure to the
cinelid Cryptolaemus montrouzieri Mulsant, a mealy- residues of insecticide and bait: 1) fresh residues, 2)
bug predator; the phytoseiid Neoseiulus californicus 3-d-old residues, and 3) 6-d-old residues. Four baited
McGregor, a spider mite predator; and the braconid insecticides were assayed for each experiment: 1)
Aphidius colemani Viereck, an aphid parasitoid. Fur- Spintor Cebo at 10%; 2) Orothion at 0.5% (malathion
thermore, sublethal effects were estimated on C. capi- 50% [EC] wt:vol; Quṍmicas Oro, S.A., Valencia, Spain)
tata and C. montrouzieri. ⫹ 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
Materials and Methods
at 0.5% (lambda-cyhalothrin 2.5%, wt:wt; Syngenta
Experimental Conditions. Unless otherwise stated, Agro, S.A., Madrid, Spain) ⫹ Nu-lure at 0.5%. A con-
environmental conditions in experiments were 25 ⫾ trol with mineral water also was considered in each
2⬚C, 60 ⫾ 10% RH, and a photoperiod of 16:8 (L:D) h. experiment.
C. capitata. Adults used in this assay originated from Adult Mortality. To assay the mortality an extended
a laboratory colony maintained at the Instituto Va- laboratory method was applied to C. capitata, C. mon-
lenciano de Investigaciones Agrarias (IVIA), trouzieri, and A. colemani adults (Medina et al. 2004).
Moncada (Valencia, Spain). For each experiment, to Clementine, Citrus clementina Hort. ex Tan. var.
obtain a cohort of adults, ⬇1,000 pupae ⬍24 h old were Nules, leaves were collected from small trees grown in
collected and maintained in polymethyl methacrylate an insecticide-free greenhouse located at the IVIA.
transparent cages (20 by 20 by 20 cm) until adult The petiole of each leaf was put into a 1.5-ml micro-
emergence. Three-day-old adults were used in all the centrifuge tubes (NIRCO S.L., Barberá del Vallès,
assays. Water and a diet consisting of a mixture of Spain) containing a nutritive solution to maintain leaf
enzymatic autolyzed brewerÕs yeast (Biokar Diagnos- turgidity during the experiments (Moutous and Fos
tics Co., Pantin, France) and sugar (1:4, wt:wt) were 1973). The petiole of the leaf was sealed to the mi-
supplied to the ßies until their use. crocentrifuge tube with plasticine (Plastilina Jovi
C. montrouzieri. Adults used in this assay were ob- JOVI, S.A. Barcelona, Spain). Five droplets of 5 ␮l of
tained from Silla (Valencia, Spain) where they were the corresponding treatment were randomly distrib-
146 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 102, no. 1

uted on the upside of the leaf with the use of a mi- C. capitata experiments. Prey (a mixture of all instars
cropipette. The treated leaf was transferred and Þxed of P. citri) was offered on a piece of paper (2 by 3 cm),
with plasticine to the bottom of a plastic cage (15 by which was used to gather up mealybugs from infested
7 by 10 cm in depth), with a hermetic lid having a mesh sprouts. These pieces of paper also were used by C.
area of 12 by 8 cm for ventilation. montrouzieri females as oviposition substrate and were
Ten replicates of each treatment were used per each replaced daily and checked under a binocular micro-
residual period. In the fresh residue experiment, once scope to ascertain fecundity and fertility. Fecundity
droplets were dried, 10 adults per replicate were in- was estimated over a 7-d period, and fertility was
troduced. In the 3- and 6-d-old experiments, until calculated as the total number of eggs laid during this
used, treated leaves were left undisturbed in a climatic period.
chamber at the climatic conditions described above. Data Analysis. For each experiment, percentage
In each cage and for all species, water was offered ad mortality, fecundity, and fertility between treatments
libitum in a 1.5-ml microcentrifuge tube sealed with were compared by means of one-way variance analysis
cotton. C. capitata adults were fed with a mixture of (ANOVA) at P ⬍ 0.05 (STSC Inc. 1987). When

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yeast and sugar (1:4, wt:wt) placed on an 1.5-ml mi- needed, data were transformed to achieve homosce-
crocentrifuge tube lid Þxed to the bottom of the cage dascity and normal distribution of residues. The least
with plasticine. A. colemani and C. montrouzieri were signiÞcant difference (LSD) test was applied for mean
fed with a mixture of honey and water (3:1, vol:vol). separation at P ⬍ 0.05. When signiÞcant differences
Each microcentrifuge tube was sealed with cotton and were found (P ⬍ 0.05), mortality was corrected using
Þxed to the bottom of the cage with plasticine. the SchneiderÐOrelli formula (Bakr 2007). Subse-
In all three experiments, mortality of C. capitata and quently, for natural enemies data were interpreted
C. montrouzieri was evaluated daily until the Þfth day according to the IOBC standards (Sterk et al. 1999),
after adultsÕ introduction. Because previous data about which include four categories: 1) harmless (mortality
the side effect of Spintor Cebo on C. montrouzieri below 30%), 2) slightly harmful (31Ð79% mortality),
were already available (Medina et al. 2003) the active 3) moderately harmful (80% to 99% mortality), and 4)
ingredient spinosad was not tested. Mortality of A. harmful (mortality higher than 99%).
colemani was only estimated until the second day in all
three experiments following the IOBC standards
Results
(Mead-Briggs et al. 2000).
To assay mortality in the N. californicus experi- Efficacy on Mediterranean Fruit Fly. Mortality
ments, Clementine leaves also were used. Neverthe- caused by malathion, Imidan 50 WP, and Spintor Cebo
less, only one droplet of 5 ␮l of the corresponding was almost 100% and signiÞcantly higher than Karate
treatment was dispensed with a micropipette onto the King and the control treatment at the end of all three
middle of the upside leaf. In the fresh residue exper- experiments (fresh residue: F ⫽ 203.48; df ⫽ 4, 59; P ⬍
iment, once the droplet was dried, a disc surface of 2 0.0001; 3-d-old residue: F ⫽ 58.11; df ⫽ 4,58; P ⬍ 0.0001;
cm in diameter containing the droplet was extracted 6-d-old residue: F ⫽ 97.39; df ⫽ 4, 59; P ⬍ 0.0001)
from the leaf. Four leaf discs per treatment were (Table 1). The two organophosphates, Orothion and
placed downside down on hydrophilic cotton soaked Imidan 50 WP, killed more ßies than the spinosad
in water in a plastic cage (14.5 by 10.5 by 10 cm in treatment in the Þrst 2 d of the experiments for fresh
depth). The soaked cotton prevented adults from es- residue and 3-d-old residue experiments. Mortality
caping. Ten adults of N. californicus were introduced results were similar during the three residual periods
per leaf disc with a Þne brush. The mite T. urticae was tested for all baited insecticides.
offered ad libitum as prey in this arena. In the 3- and On the Þfth day of evaluation, only adults treated
6-d-old experiments, until used, treated leaves were with Karate King and control survived in enough num-
left undisturbed under the above-mentioned climatic bers to carry out the sublethal test. A novel disabling
conditions. effect was found on adults treated with Karate King,
Sublethal Effects. Ten surviving adults from the which could hardly ßy inside the arena and their
fresh residue treatments of C. capitata were used to movements were irregular. However, under the ex-
estimate the bait treatment effect on their fecundity perimental conditions, females surviving Karate King
and fertility. Females of C. capitata were individually treatment were able to lay 54.9 ⫾ 16.0 eggs for a period
placed in the same cages used to evaluate mortality. To of 7 d. Although this value was much lower than in the
assess fecundity, the total number of eggs laid through control group, where females laid 119.4 ⫾ 30.8 eggs, no
the gauze was evaluated daily over a 4-d period. signiÞcant differences were found (F ⫽ 3.87; df ⫽ 1,
Twenty eggs per female and day were randomly taken 19; P ⫽ 0.065). Egg fertility rates were 32.2 ⫾ 13.2% for
with a Þne brush and placed on a rectangular piece of Karate King and 56.3 ⫾ 10.1% for the control, without
black cardboard, which was kept on a permanently signiÞcant differences (F ⫽ 2.09; df ⫽ 1, 19; P ⫽ 0.165).
wet dishcloth. The number of hatched eggs was used Side Effects on C. montrouzieri. All products yielded
to calculate fertility. signiÞcantly higher mortality values than the control
Surviving females of C. montrouzieri exposed to (Table 2). In all three experiments, the toxic effects of
fresh, 3- and 6-d-old residues were used to assess the Karate King on C. montrouzieri were faster than the
baited insecticide effect on fecundity and fertility by other treatments. However, by the end of the exper-
placing them individually in the same cages used for 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 compared with the control, irrespective of the residual
control (fresh residue: F ⫽ 8.135; df ⫽ 3, 39; P ⬍ 0.0001; age (Table 3). Hence, both products were classed as
3-d-old residue: F ⫽ 13.578; df ⫽ 3, 98; P ⬍ 0.0001; IOBC category 1 (harmless). However, Orothion
6-d-old residue: F ⫽ 7.680; df ⫽ 3, 39; P ⬍ 0.0001). caused the highest mortality of A. colemani (94%),
These values represent corrected mortality of be- reaching an IOBC category 3. Although the spinosad
tween 36 and 71%, which gives an IOBC category 2. bait treatment also yielded higher mortalities than the
Fecundity of surviving females was not affected in control, it had a lower impact on this parasitoid (IOBC
any case compared with the control (fresh residue: category 2) (fresh residue: F ⫽ 24.69; df ⫽ 4, 34; P ⬍
F ⫽ 4.33; df ⫽ 3, 39; P ⫽ 0.010; 3-d-old residue: F ⫽ 2.72; 0.0001; 3-d-old residue: F ⫽ 20.28; df ⫽ 4, 34; P ⬍ 0.0001;
df ⫽ 3, 39; P ⫽ 0.097; 6-d-old residue: F ⫽ 1.19; df ⫽
6-d-old residue: F ⫽ 12.11; df ⫽ 4, 34; P ⬍ 0.0001).
3, 39; P ⫽ 0.150). Mean fecundity values were 28.9 ⫾
Side Effects on N. californicus. At the end of the
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 experiments, statistically signiÞcant differences were
fertility affected (fresh residue: F ⫽ 1.23; df ⫽ 3, 29; P ⫽ found between the control and all the baited insecti-
0.319; 3-d-old residue: F ⫽ 0.468; df ⫽ 3, 26; P ⫽ 0.708; cides for the fresh residue (fresh residue: F ⫽ 37.63;
6-d-old residue: F ⫽ 0.146; df ⫽ 3, 32; P ⫽ 0.743). Mean df ⫽ 4, 27; P ⬍ 0.0001; 3-d-old residue: F ⫽ 31.88; df ⫽
fertility values were 62.7 ⫾ 7.1, 69.3 ⫾ 2.1, and 66.9 ⫾ 4, 27; P ⬍ 0.0001); 6-d-old residue: F ⫽ 15.31; df ⫽ 4,
1.3 for fresh, 3-d-old residues, and 6-d old residues, 27; P ⬍ 0.0001). The spinosad bait treatment caused
respectively. 70% mortality on N. californicus, representing an IOBC
Side Effects on A. colemani. In the three residual category 2, whereas Orothion and Imidan 50 WP
experiments, no signiÞcant differences were found caused ⬇85% mortality, corresponding to an IOBC
when Imidan and Karate King bait treatments were 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, related to the disabling effect under Þeld conditions,
corresponding to an IOBC category 4 (Table 4). 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
Discussion
research is needed to clarify this issue.
The two organophosphates Orothion and Imidan 50 The baited insecticide treatments are considered
WP and also Spintor Cebo were highly effective in generally harmless on nontarget organisms (Roessler
killing C. capitata, with a mortality rate of ⬇100%. 1989), although the use of a nonspeciÞc C. capitata bait
Karate King produced lower Mediterranean fruit ßy also could attract natural enemies. In this study, the
mortality rates, with values of ⬇40%. However, it natural enemies behaved differently depending on the
caused a disabling effect on adults, which could not ßy arthropod species and the insecticide bait treatment.
and displayed irregular movements. A reduction in Spinosad-baited treatment turned out to be the most
Mediterranean fruit ßy fecundity and fertility also selective for C. montrouzieri and N. californicus,
were observed for this insecticide, although differ- whereas for A. colemani the most selective were phos-
ences were not signiÞcant. This pyrethroid was met and lambda-cyhalothrin. To our knowledge, this
sprayed in certain citrus-growing areas of the Valencia is the Þrst time reporting on the side effects of the
region in 2007 and gave good results in controlling C. baited organophosphate phosmet and the pyrethroid
capitata. An explanation for these differences could be 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 149

on N. californicus was the only effect to yield an IOBC athion (Vargas et al. 2001). Based on these results, in
category 4 in this study. The harmful effects of con- Hawaii and other American areas where C. capitata
ventionally spraying of this pyrethroid onto the most and other tephritids are key pests, the guidelines for
common predatory mite in Spanish citrus orchards, areawide integrated strategies combine environmen-
Euseius stipulatus Athias-Henriot, were already known tally safe bait treatments with the release and conser-
(Jacas and Garcia-Marṍ 2002). This was not the case for vation of natural enemies. In recent years, emphasis
Spintor Cebo at 10% and Orothion at 0.5% ⫹ Nu-lure has been placed on implementing these measures to
at 0.5%, both of which proved harmless against E. control the Mediterranean fruit ßy in Spain. To this
stipulatus in a Þeld experiment (San Andrés et al. end, two different approaches to biological control are
2006). currently being considered. The Þrst is a classical bi-
Some previous results on the side effects of spi- ological control program introducing two exotic para-
nosad- and malathion-baited treatments also are avail- sitoids, F. arisanus and D. tryoni (Santiago et al. 2006,
able. The effects of these pesticides were studied on Pérez-Hinarejos et al. 2006), whereas the second ap-
C. cryptolaemus and on vedalia, Rodolia cardinalis proach involves identifying and conserving both

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(Mulsant) (Coleoptera: Coccinellidae), under labo- polyphagous predators and indigenous parasitoids of
ratory (Medina et al. 2003) and semiÞeld conditions the Mediterranean fruit ßy (Falcó et al. 2006, Urbaneja
(Medina et al. 2004). The results of these studies et al. 2006).
showed that Spintor Cebo was harmless for both pred- In summary, our results could help to integrate
ators, whereas malathion plus the proteinaceous bait biological and chemical control of Mediterranean fruit
proved moderately harmful (IOBC category 3). Sim- ßy in citrus orchards. A bait-formulation containing
ilar results for both baited insecticides have been ob- spinosad seem to be the best option when considering
tained for several key citrus predators in Florida pest control efÞcacy together with the side effects on
(Michaud 2003). In the study conducted in Florida, the three beneÞcial arthropods chosen for this study
both malathion and spinosad proved toxic for two and on the others available. However, the negative
parasitoids that are already abundant in Spanish citrus effects on some parasitoid species should not be ne-
orchards, the aphid parasitoid Lysiphlebus testaceipes glected. Special attention should be paid when aug-
Cresson (Hymenoptera: Braconidae) and the ar- mentative biological control strategies are imple-
mored scale parasitoid Aphytis melinus DeBach (Hy- mented that based on parasitoid releases [as could be
menoptera: Aphelinidae). the case with A. melinus against the California red
The sublethal effects of both malathion and spi- scale, Aonidiella aurantii (Maskell) (Hemiptera: Di-
nosad baited treatments also have been studied in four aspididae)].
other parasitoids (Urbaneja et al. 2004). Following the
same methodology described in the current study,
both insecticides killed ⬇60% of adults in Citrostichus Acknowledgments
phyllocnistoides Narayan (Hymenoptera: Eulophi-
dae), the most important citrus leafminer parasitoid in We thank J. Calvo and J. E. Belda (Koppert Biological
the Mediterranean Basin. However, malathion was System S. L., Águilas, Spain) for the A. colemani supply; I.
Boix, R. Aparici, and J. L. Porcuna for the C. montrouzieri
classiÞed as harmful on C. phyllocnistoides due to re-
supply, and F. Barraclough for correcting the English. This
duced fecundity and fertility of surviving females, research was partially funded by the Instituto Nacional de
whereas Spintor Cebo did not show any sublethal Investigación y Tecnologṍa Agraria (RTA03-103C601), by
effect. In the same study, malathion also proved harm- the Conselleria dÕAgricultura, Pesca i Alimentació de la Gen-
ful against the Mediterranean fruit ßy parasitoid Dia- eralitat Valenciana, and FEOGA COOPERACIÓN. R.A. and
chasmimorpha tryoni (Cameron) (Hymenoptera: P.C. were recipients of a grant from IVIA.
Braconidae), the mealybug parasitoid Anagyrus
pseudococci (Girault) (Hymenoptera: Encyrtidae),
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