HoRTICU LTURAL ENTONtOLU)GY
Toxicity of Imidacloprid-Treated Spheres to Caribbean fruit fly,
Anastrepha suspense (Diptera: Tephritidae) and Its Parasitoid
DiM s -l m im.lt rpl longicaudata (Hymenoptera: Braconidae)
in the Laboratory
OSCAR E. LIBURD,1 TIMOTHY C. HOLLER,2 AND AMY L. MOSES"
Department of Entomology and Nematology, Natural Area Dr., University of Florida, Gainesville, FL 32611
J. Econ. Entomol. 97(2): 525 529 (2004)
ABSTRACT No-choice cage tests were used to study the toxicity of imidacloprid-treated spheres to
Caribbean fruit fly, Anastrepha suspensa (Loew), and its associated parasitoid, Diachasmimorpha
longicaudata (Ashmead), in the laboratory. Three imidacloprid sphere treatments (2,4, and 8% active
ingredient [AI] Provado 1.6 F) and an untreated control sphere (no toxicant) were evaluated against
A. suspense. Throughout the observation period (2-72 h), all concentrations of imidacloprid-treated
spheres I .. I significantly more A. suspense compared with control spheres. After 4 h of exposure to
imidacloprid-treated spheres, significantly more A. suspense were killed on spheres treated with 8%
compared with 2% (AI). At 48 and 72 h, there were no significant differences in the mean number
ofA. stuspensa killed at 2, 4, and 8% (AI), potentially indicating that a period of 24 h was sufficient for
flies to ingest a lethal dose of the pesticide. Overall, ,.i; ...i-, more A. suspense males were killed
after 72 h of exposure to imidacloprid-treated spheres compared with females. For D. longicaudata,
only two imidacloprid sphere treatments, 2 and 4% (AI), and an untreated sphere (control) were
evaluated for .. 1 :iJi in cage tests. There were no significant i1-. ... in mortality of D. longi-
caudata between the 2 and 4% (AI) imidacloprid-treated spheres. Both rates killed .', il .
D. longicaudata compared with the con trol. However, after 24,48, and 72 h of exposure to imidacloprid-
treated spheres, significantly more ). longicaudata were killed in cages containing 4% compared with
2% (AI) and untreated control spheres. The study demonstrates the potential use of imidacloprid-
treated spheres for control ofA. suspensa in areas where it may be difficult to apply broad-spectrum
KEY WORDS Caribbean fruit fly, Diachasmimorpha longicaudata, imidacloprid-treated spheres
INCREASINGLY, APPLICATION OF PESTICIDES by air and oc-
c .ii by ground for fruit fly control is meeting
resistance from environmentalist and the general
public. Access to. .: .. .:i sensitive areas such as hos-
pitals, bodies of water, and school zones is becoming
increasingly problematic for fruit fly eradication pro-
grams that emphasize broad-spectrum insecticides
(Clark et al. 1996). The situation is further compli-
cated because biological (Baranowski et al. 1993) and
cultural methods of control do not yield immediate
results necessary for successful eradication programs
(AliNiazee and Croft 1999). To prevent fruit flies from
harboring in these areas and reinfesting surrounding
areas, alternative strategies for managing these criti-
cally sensitive areas must be developed.
Several types of traps, as well as trap-lure combi-
nations and baits specifically designed to improve
1 E-mail: email@example.com.
2 SDA APHIS PPQ CPHST, 1913 SW 34th St., Cainesville, Fl.
monitoring capabilities through increased trap cap-
tures while minimizing environmental impacts and
decreasing chemical residues on fruit crops, have been
tested for control of Caribbean fruit fly, Anastrepha
suspense (Loew) (Greany et al. 1978, Burditt 1982).
Thomas et al. (2001) evaluated trap-lure combinations
against populations of A. suspense and Mexican fruit
fly, Ancastreppha ludens (Loew), as substitutes for the
glass McPhail trap and found that open-bottom, plastic
traps baited with a two-component synthetic lure
ammoniumm acetate and putrescine) caught as many
or more fruit flies than McPhail traps baited with
torula yeast. In their study, fruit fly captures varied
among seasons and locations, but more females and
fewer nontarget insects were captured with synthetic
Several opiine brachonid parasitoid species, includ-
ing F '* .,. ., longicaudata (Ashmead) and
Doryctobracon areolatus ( -.1,l i ), were intro-
duced into the United States for biological control of
A. suspensa (Lawrence et al. 1978, Baranowski et al.
0022-0493/04/0525-0529$04.00/0 2004 Entomological Society of America
JOURNAL OF ECONOMIC ENTOMOLOGY
1993). Baranowski et al. (1993) reported a 40% decline
in trap catches of A. suspense 5 yr postrelease of D.
longicaudata. Later, Sivinski et al. (1999) showed that
A. suspensa larvae and their brachonid parasitoids,
including D. longicaudata, were evenly distributed
within the canopy of host trees, suggesting that height
above ground or distance from canopy edge of trees
did i- .._.-i.. .i.-' affect oviposition preferences for
A. suspense. The development of effective pest man-
agement strategies for A. suspensa without negatively
impacting parasitoid populations is essential to main-
taining long-term control of A. suspense in a produc-
Recently, the strategy of using imidacloprid-treated
spheres for management of key fruit 11 pests, Rhago-
letis .: .. (Walsh) and Rhagoletis mendax Cur-
ran, have been given much attention in northeastern
United States (Liburd et al. 1999, Prokopy et al. 2000,
Stelinski and Liburd 2001, Hamill et al. 2003). This
strategy may also .,i II : other fruit fly species,
including A. suspense, a key pest of tropical fruit in
Florida and the Caribbean region (Norrbom and Kim
1988). Although efforts are underway to develop bait
stations (Sivinski, personal communication), there are
no studies in the literature that have investigated the
potential of using imidacloprid-treated spheres for
control ofA. suispensa. In addition, there are no reports
(for any fruit fly species) on how imidacloprid-treated
spheres may impact fruit fly parasitoid densities. Nev-
ertheless, before any large-scale trials are developed,
laboratory assays must be performed to determine the
response of A. suspense and its natural enemies to
imidacloprid-treated sphere tactics.
The objective of this study was to conduct labora-
tory assays to investigate the toxicity of A. suspense to
imidacloprid-treated spheres and to explore the po-
tential nontarget effects of using imidacloprid-treated
spheres on D. longicaudata, a key parasitoid of A.
Materials and Methods
Experiments to evaluate the toxicity of imidaclo-
prid-treated spheres to A. suspeonsa and D. loigicaudata
were conducted at APHIS-Plant Protection and Quar-
antine, Center for Plant Health Science and Technol-
ogy (CPHST) Laboratory in Gainesville, FL, and the
Fruit and Vegetable Integrated Pest Management
Laboratory, University of Florida, Gainesville, FL. The
unit used was a starch/sugar 9-cm-diameter sphere
composed of gelatinized c( :i corn syrup, sugar,
cayenne pepper, and sorbic acid (Liburd et al. 1999,
Stelinski and liburd 2001). The sugar/starch sphere
was coated with a mixture of 70% k- :1. :, orange
florescent paint ([4CI-3 Behr Flat Y i: Cluster],
Home Depot, ( :.. I: FL), 20% sucrose solution
(wt:vol), and varying amounts of toxicant (imidaclo-
prid) and water, depending on the treatment.
Experimental design was a randomized complete
block with five replicates per treatment. Each cage
contained 25 male and 25 female fruit flies or parasi-
toids, totaling 250 individuals per treatment. Four
treatments were evaluated: 1) spheres brush painted
with mixture of2% ([AI]) imidacloprid (Provado 1.6
F, Bayer Cropscience, Kansas City, MO) and wa-
ter; 2) same as 1 except 4% imidacloprid and 6% water;
3) same as 1 except 8% imidacloprid and 2% water, and
4) control 10% water, no toxicant. Each sphere was
placed on an inverted 236.8-ml plastic cup (Solo Cup
Co., Urbana, IL), pedestal equidistant from the top,
sides, and bottom of a 30 by 30-crn cubed Plexiglas
cage. Before the start of the experiment, each sphere
was misted with water to simulate "morning dew" and
again at 24 and 48 h.
Source of Insects. A. s&uspensa pupae were obtained
from colonies maintained at the Florida Department
of Agriculture and Consumer Service's Division of
Plant Industry in Gainesville, FL (Burns 1995). Adults
were maintained on a diet of sugar (sucrose), protein
(yeast hydrolysate), and water. Flies were protein-
sugar starved 24 h before commencement of assays to
increase their responsiveness. Only water was pro-
vided in two souffles cups (59.2 ml). Each cup with
water had a dental wick protruding through its lid to
.I1 :I, ,1 .:... treatment cages easy access to water.
The only other moisture source came from misting the
spheres. .. i mature 7-10-d-old i were tested.
D. longicaudata were obtained from Division of
Plant Industry (Biocontrol Rearing Facility) and were
tested when 5 8 d old. Before placing D. longicaudata
into test cages, they were fed honey, presented in a
gelatinous form (i.e., agar/water/honey block) in an
open petri dish on the bottom of the cage. Water was
....1.. .1 as described above for A. suspense by using
two souffles cups with dental wicks placed inside the
cages. D. longicaudata were subjected to two and 4%
imidacloprid treatments. Temperature and humidity
best suited for responsiveness were maintained where
-. l1.i. 25.6-30C and 60 78% RH. A photoperiod of
12:12 (L:D) h was provided with florescent lamps with
the aid of a timer.
Sampling. A. susspensa and D. longicaudata visits to
the spheres to attempt feeding were recorded at the
following intervals: 2, 4, 24, 48, and 72 h. Data were
recorded according to sex by counting the number of
males and females that were killed after contact (feed-
ing or alighting) with the sphere.
Statistical Analysis. Male and female data were ini-
tially pooled to examine the overall effects of imida-
cloprid-treated spheres on A. suspense and D. longi-
caudata. i ... II data were separated according to sex
to determine the toxicity of imidacloprid-treated
spheres to males and females independently. Data
from all experiments were square root transformed (x
+ 0.5) to stabilize variances and subjected to a re-
peated measures analysis of variance (ANOVA) fol-
lowed by mean separation by using the least significant
difference (LSD) test (SAS Institute 2001). The re-
sultswere considered statistically .' i .. .. i<
0.05. Data are presented as untransformed means and
Vol. 97, no. 2
LIBURD ET AL.: Toxic SPHERES TO CONTROL A. Saspensa
Table 1. Mean SEM percentage of A. suspense killed on spheres treated with different concentrations of inidacloprid
% Hours posttreatment
Imidacloprid 2 4 24 48 72
0 0.1 0.1b 0.1 0.1c 0.1 0.ce 0.4 0.b 7.7 1.3b
2 5.7 0.9a 7.6 1.2b 17.4 + 1.5b 53.4 + 2.2a 87.6 + 1.0a
4 6.6 1.2a 8.2 1.0ab 21.4 1 1.0a 56.2 3.0a 88.1 1 2.1a
8 7.3 + 1.0a 10.2 0.8a 2-.8 + 1.1a 58.2 3.4a 86.5 3.3a
Means within column followed by the same letter .. ... ... I : ..' (F < 0.05, LSD test; SAS Institute Inc. 2001). Analyses were
performed on square root-transformed data, but means shown are backtransformed data. For 2 h, F= 71 2: df = 3, 12; P < 0.01; for 4 h, F
155.3; df 3,12; P < 0.01; for 24 h, F 357.8; df 3,12; P < 0.01; for 48 h, F 313.3; df 3,12; P < 0.01; and for 72 h, F 516.9; df = 3, 12;
P < 0.01. For all treatments, n = 250
Laboratory Assays for A. suspense. Throughout the
observation period (2 72 hi all concentrations (2, 4,
and 8% [AI]) of imidacloprid-treated spheres killed
significantly more A. suspense compared with control
spheres (Table 1). After 2 h, there was no significant
difference in the mean number ofA. suspense killed at
2, 4, and 8% (AI). After 4 h of exposure to treated
spheres, .. '. n more A. suspense were killed at
8% compared with 2% (AI). There was no significant
difference in the number of A. suslpensa killed by the
2 and 4% imidacloprid-treated spheres.
Results from the 24-h observation period differed
from those at 4 h i, .... --i. greater number of A.
suspensa were killed at 4 and 8% (AI) compared with
flies exposed to 2% (AI) imidacloprid-treated spheres.
At 48 and 72 h, there were no significant differences
in the mean number of : dII. -I A. suspensa when ex-
posed to imidacloprid-treated spheres at 2, 4, and 8%
(AI). All treatments (2, 4, and 8% [AIl) killed -12
times as many A. suspense compared with untreated
imidacloprid spheres. All treatments with imidaclo-
prid killed significantly more A. suspensa compared
with the control over time (F = 590.8; df = 1, 38; P <
0.0001). There were no significant 1.~... .. .. among
imidacloprid sphere treatments over time (F = 0.02;
df = 2, 29; P = 0.98).
i ic.1ilili f-: of Male and Female A. suspense to
Imidacloprid-Treated Spheres. Overall, A. sus-pensa
males were on average 1.2 times more susceptible to
imidacloprid-treated spheres compared with females.
Treatments 2 and 4% (AI) killed -_,.: -11i more
males than females (Table 2). There were no signif-
icant differences between males and females for 0 and
8% (AI). I..: .., i more males (F= 160; df = 3,12;
P < 0.0001) and females (F = 124.5; df = 3, 12; P <
0.0001) were killed with imidacloprid treatments com-
pared with the control (Table 2).
i, ,inhii, of D. longicaudata to Imidaeloprid-
Treated Spheres. There was no significant difference
in mortality of D. longicaudata exposed to 2 and 4%
(AI) imidacloprid-treated spheres at 2 or 4 h (Table
3). However, 2% (AI) killed significantly more D.
longicaudata compared with the control after 24 h.
After 24-, 48-, and 72-h exposures to imidacloprid-
treated spheres, .,,i, ,..i more D. longicaudata
were killed with 4% compared with 2% (AI) and the
control (Table 3).
There were no significant differences among imi-
dacloprid sphere treatments for D. longicaudata over
time (F = 1.4; df = 1, 87; P = 0.25). However, both
imidacloprid sphere treatments (2 and 4% [AI]) killed
significantly more D. longicaudata compared with the
control [ (F = 47.4; df = 1, 82; P < 0.001) and (F =
101.5; df = 1,87; P <0.001) for 2 and 4%, respectively]
These results demonstrate that imidacloprid-
treated spheres were effective in killing A. suspensa at
all rates of imidacloprid (2, 4, or 8%) evaluated. The
*.. : ..!.! of A. s&spensa to imidacloprid-treated
spheres is not surprising considering ti, Hi.. not
given an option to alight or forage on other nontreated
surfaces and because these spheres have been re-
ported to be highly toxic to other tephritids (Liburd
et al. 1999). Nevertheless, if it is possible to induce fly
mortality as early as 2 h after setting on a treated
sphere (in the field), residual effectiveness may not be
critical, although certainly desirable, from a replace-
ment standpoint (Hamill et al. 2003). However, it is
unlikely that all the flies in the field would be exposed
to a toxic dose of the pesticide during a 2-h period;
therefore, it would be important for spheres to remain
effective for a fairly long period after they are de-
ployed in the 1;. I.1
After 4-h exposure to imidacloprid-treated spheres,
significantly greater numbers ii .. .. killed by 8%
Table 2. Mean SEM percentage male and female A. suspense
killed on spheres treated with different concentrations of
% .Male Female
0 10.4 + 5.3b 4.6 + 2.8b
2 95.0 + 1.6a* 79.0 + 2.2a
4 95.0 1.5a* 78.2 2.3a
8 96.7 2.7a 82.2 4.3a
Means within column followed by the same letter are not signifi-
cantly different (P < 0.05. LSD test; SAS Institute Inc. 2001). Analysis
was performed on square root-transformed data, but means shown are
The number of killed males in imidacloprid treatments at 2 and
4% is significantly higher than females. For 0% (AI), F = 1.0; df = 1,4;
P = 0.34: for 2% (AI), F = 34.5; df 1,4; P < 0.01: for 4% (AI), F
34.1: df 1,4; P < 0.01; and for 8% (AI), F 2.8; df 1,4, P 0.1.
For all treatments, n = 125.
JOURNAL OF ECONOMIC ENTOMOLOGY
Table 3. Mean SEM percentage D. longicaudata killed on spheres treated with different concentrations of inidaeloprid
% Hours posttreatment
Imidacloprid 2 4 24 48 72
4.4 = 1.8a
22 1 0.4c
1.1 1 1.5c
77.0 1 6.2a
Means within column followed by the same letter are not significantly different (P < 0.05, LSD test; SAS Institute Inc. 2001). Analyses were
performed on square root-transformed data, but means shown are backtransformed data. For 2 h, F = 9.00; df = 2,8; P < 0.01; for 4 h, F = 7.97;
df 2,8; P 0 013: for 2 h, F 1743; df = 2,8; P < 0.01; for 48 h, F 68.29; df 2,8; P < 001; and for 72 h, F 105.40: df 2,8: P <0.01.
For all treatments, n = 250
compared with 2% (AI), suggesting that higher con-
centrations of insecticide may be required over time
to ensure greater efficacy. Stelinski et al. (2001) re-
ported that the effectiveness of imidacloprid-treated
spheres against R. pomonella flies decreased .':
cantly after 12 wk i :. 1 i exposure when treated with
2% (AI) imidacloprid, but .... i ., was not affected
after 12 wk on spheres treated with 4 and 8% (AI)
imidacloprid. In our study, the importance of higher
insecticide concentration over time became more ap-
parent after 24 h, when greater numbers of A. suispensa
succumbed to the 4 and -- compared with 2% (AI)
treatments. Apparently, a 24-h exposure period was
sufficient, because results were similar at the 48- and
72-h observations. However, these studies should be
tested either in field cages or a commercial citrus
grove to determine whether the results observed in
the laboratory can be duplicated in the field.
The:. l. t :orange 1 **u. used in our
study is believed to be visually attractive to both males
and females (Greany et al. 1978). It is not clear why
male A. suspense were 1.2 times more susceptible than
females to imidacloprid, a neonicotinoid insecticide,
that has both contact and systemic mode of action
(Liburd et al. 2003). It is possible that males landed on
spheres more often than females to feed, or perhaps
with the intent to mate, and as a result were more
likely to come into contact with a toxic dose of imi-
dacloprid. Imidacloprid has been shown to have lethal
and sublethal effects on other tephritids (Hu and
The benefits of using imidacloprid-treated spheres
include a reduction in pesticide residues on crops, as
well as reduced environmental and worker hazards
(Hamill et al. 2003). In addition, unlike sticky spheres,
insects killed from feeding on pesticide-treated
spheres do not accumulate on spheres and reduce
Before using imidacloprid-treated spheres in an ag-
ricultural or environmentally sensitive ecosystem, a
measure of their effects on beneficials (,.... ..1 ....1
predators) must be assessed. Our study measured the
effects of imidacloprid-treated spheres on an opiine
parasitoid used throughout the world in tephritid fruit
fly biological control programs (Sivinski et al. 2000).
Although higher mortality of D. longicaudata was re-
corded with 4% compared with 2% (AI) after 24 h it
is believed that the seasonal population dynamics of
fruit fly parasitoids inhabiting various A. suspensa
niches (for feeding) are so limited that populations
would not be ..,: .... I reduced (Sivinski et al.
1998). Vargas etal. (2001,2002) reported that spinosad
or phloxine B bait sprays had little or no effect on
Fopius arisanus (Sonan), the major parasitoids of Med-
iterranean fruit fly, Cer ., .. .; (Wiedemann),in
Hawaii. Nevertheless, further research using field
plots would be necessary to determine susceptibility
ofD. longicaudata to imidacloprid-treated spheres un-
der natural conditions.
Fruit fly control in some sensitive areas in the U.S.
and internationally preclude the use of .. i ap-
plied bait-sprays, or the ., : ... of sterile fruit flies
due to topography (Burns et al. 2001). For instance,
the use of bait sprays is a concern in potentially sen-
sitive areas (e.g., due to water, hospitals) in Texas and
California where Mexican fruit fly is of economic im-
portance. Florida has also experienced a problem with
the occurrence of oriental fruit il Bactrocera donsalis
Hendel, and guava fruit fly, Bactrocera correct
Presently, the insecticide imidacloprid is registered
for soil and foliar treatment in field crops, vegetables
and selected fruits. The sugar/starch sphere evaluated
in this study has been reported to be susceptible to
rodent feeding (Stelinski and Liburd 2001). A new
plastic version of spheres with sucrose cap is targeting
Rhagoletis spp. (Hamill et al. 2003). The data derived
from the current study and future field studies 11
:., .*1. :.,l lead to commercialization of insecticide-
treated spheres in citrus as well as other crops cur-
rently threatened by A. suspense. However, field tests
will be necessary because of the ambiguities inherent
in laboratory cage studies. The potential danger of
using imidacloprid-treated spheres to nontarget or-
ganisms, including people and birds, also remains to be
We thank Rajya Shukla for help analyzing some of the
data. We also thank Jon Hamill and Gisette Seferina for
conducting some of the laboratory assays. We -1:
thank John Sivinski (USDA-ARS-CMAVE. Gainesville FL),
and Norm Leppla for critically reviewing the manuscript.
: 1, thanks to George Schneider (Director of FDACS-
DPI, Biocontrol Rearing Facility) for providing the Carib-
bean fruit flies for this study. This research was supported by
Vol. 97, no. 2
LIBURD ET AL.: Toxic SPHERES TO CONTROL A. Srspensa
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Received 13 May 2003; accepted 24 November 2003.