COMMODITY TREATMENT AND QUARANTINE ENTOMOLOGY

Attraction and Mortality of Bactrocera dorsalis (Diptera: Tephritidae)

to STATIC Spinosad ME Weathered Under Operational Conditions in
California and Florida: A Reduced-Risk Male Annihilation Treatment
ROGER I. VARGAS,1,2 STEVEN K. SOUDER,1 KEVIN HOFFMAN,3 JUAN MERCOGLIANO,3
TREVOR R. SMITH,4 JACK HAMMOND,4 BOBBIE J. DAVIS,4 MATT BRODIE,4
5
AND JAMES E. DRIPPS

J. Econ. Entomol. 107(4): 1362Ð1369 (2014); DOI: http://dx.doi.org/10.1603/EC14121

ABSTRACT Studies were conducted in 2013Ð2014 to quantify attraction, feeding, and mortality of
male oriental fruit ßies, Bactrocera dorsalis (Hendel) (Diptera: Tephritidae), to STATIC Spinosad ME
a reduced-risk male annihilation treatment (MAT) formulation consisting of an amorphous polymer
matrix in combination with methyl eugenol (ME) and spinosad compared with the standard treatment
of Min-U-Gel mixed with ME and naled (Dibrom). Our approach used a behavioral methodology for
evaluation of slow-acting reduced-risk insecticides. ME treatments were weathered for 1, 7, 14, 21, and
28 d under operational conditions in California and Florida and shipped to Hawaii for bioassays. In
Þeld tests using bucket traps to attract and capture wild males, and in toxicity studies conducted in
1-m3 cages using released males of controlled ages, STATIC Spinosad ME performed equally as well
to the standard formulation of Min-U-Gel ME with naled for material aged up to 28 d in both California
and Florida. In laboratory feeding tests in which individual males were exposed for 5 min to the
different ME treatments, mortality induced by STATIC Spinosad ME recorded at 24 h did not differ
from mortality caused by Min-U-Gel ME with naled at 1, 7, 14, and 21 d in California and was equal
to or higher for all weathered time periods in Florida during two trials. Spinosad has low contact
toxicity, and when mixed with an attractant and slow release matrix, offers a reduced-risk alternative
for eradication of B. dorsalis and related ME attracted species, without many of the potential negative
effects to humans and nontargets associated with broad-spectrum contact insecticides such as naled.

KEY WORDS Oriental fruit ßy, suppression, Min-U-Gel ME naled, MAT, alternative treatment

Oriental fruit ßy, Bactrocera dorsalis (Hendel), con-
sidered to be among the four most damaging species
of Bactrocera (Leblanc and Putoa 2000, Clarke et al.
2005, San Jose et al. 2013), is native to and widespread
throughout tropical Asia, from India, through south-
ern China, east to Taiwan and south to Vietnam and
Thailand (Drew and Hancock 1994, Leblanc et al.
2013). Included as part of the B. dorsalis complex of
⬎75 species (Drew and Hancock 1994, Clarke et al.
2005, San Jose et al. 2013) are B. dorsalis and the three
closely related sibling species, Bactrocera papayae
Drew & Hancock, Bactrocera carambolae Drew &
Hancock, and Bactrocera invadens Drew, Tsuruta &
White. The group is highly polyphagous, invasive and
adapts readily to local host conditions (Leblanc et al.
1 Daniel K. Inouye U.S. PaciÞc Basin Agricultural Research Center,
TCCPRU, USDAÐARS, 64 Nowelo St., Hilo, HI 96720.
2 Corresponding author, e-mail: roger.vargas@ars.usda.gov.
3 California Department of Food and Agriculture, 1220 N St., Sac-
ramento, CA 95814.
4 Florida Department of Agriculture and Consumer Services, Di-
2013). For example, B. dorsalis, a major fruit ßy pest
species in Hawaii, infests 173 host plant species (Met-
calf and Metcalf 1992). The four sibling species have
invaded many places around the world, including the
PaciÞc (B. papayae in Palau; B. dorsalis in Hawaii,
French Polynesia, the Mariana islands [eradicated],
and Nauru [eradicated]; and B. papayae in Australia
[eradicated]) and South America (B. carambolae in
Suriname, Guyana, French Guiana, and northern Bra-
zil; San Jose et al. 2013). Most recently, B. invadens,
considered by many to be the same species as B.
dorsalis on the basis of molecular analyses (San Jose et
al. 2013, Leblanc et al. 2013), has spread rapidly from
east to west subtropical and tropical Africa after ac-
cidental introduction into the continent (De Meyer et
al. 2010). It was Þrst detected in Kenya in 2003 and is
now recorded in 27 African countries (De Meyer et al.
2010, Geurts et al. 2014). In Africa, B. invadens has
become a very serious pest of mango and even dis-
placed the native mango fruit ßy, Ceratitis cosyra
(Walker) in many areas (Ekesi et al. 2009).

vision of Plant Industry, Gainesville, FL 32608.

B. dorsalis detections have occurred in California
5 Dow AgroSciences, LLC, Crop Protection R & D, 9330 Zionsville every year since 1966 (California Department of Food
Road, Indianapolis, IN 46268. and Agriculture [CDFA] 2008), and Florida has had
August 2014 VARGAS ET AL.: REDUCED-RISK MALE ANNIHILATION TREATMENT
twelve B. dorsalis detections since 1999 (in seven
separate years) with the last occurring in 2010
(FDACS 2010; Steck, personal commnication 2014).
Although the source and ecology of these ßies has
been contentious (Liebhold et al. 2006, Papadoupolos
et al. 2013), these detections have often triggered
expensive eradication programs and quarantines. The
nationÕs largest fruit-producing states are California
and Florida. California accounts for over half of the
harvested fruit acreage, while Florida ⬇20% (CDFA
2013). Potential hosts of signiÞcant economic concern
in California and Florida include citrus (combined
⬇96% of all citrus produced in the United States),
tomato, peach, pear, and bell pepper. In California, the
combined 2005 gross value of the commercial hosts
potentially affected was ⬎US$9.8 billion (CDFA
2008). In 2011, the economic value of grapefruit, or-
ange, tomato, and bell peppers combined in Florida
was US$2.3 billion (Florida Department of Agriculture
and Consumer Services [FDACS] 2012).
Numerous eradication efforts undertaken by the
California Department of Food and Agriculture
(CDFA), Florida Department of Agriculture and Con-
sumer Services (FDACS), and U.S. Department of
Agriculture (USDA) over the years have prevented
the establishment of B. dorsalis in the continental
United States and have allowed for movement of ag-
ricultural commodities from these states. The primary
method used in California and Florida for eradication
of accidental introductions of ME-attracted fruit ßies
includes the application of large numbers of gel-like
“bait stations” of Min-U-Gel 400 (Active Minerals In-
ternational, Hunt Valley, MD) mixed with methyl
eugenol (ME) and naled to utility poles and street
trees at a height of 1.8 Ð2.4 m. Male annihilation treat-
ments (MAT) are conducted in a 2.1 km (1.5 mile)
radius from each ßy Þnd site for a minimum of 23.3
km2. The technique is repeated every 2 wk for a min-
imum of four applications, or one to two life cycles,
depending on the severity of the infestation (CDFA
2008). A quarantined area is declared fruit-ßy-free
when no ßies have been detected for a time period
corresponding to three generations after the last ßy
Þnd (CDFA 2008, 2010).
Min-U-Gel is a Þne grade of attapulgite clay (an-
hydrous magnesium aluminum silicate) that was de-
veloped for spot applications in male annihilation
programs in California for eradication of B. dorsalis
(Chambers et al. 1974, Cunningham and Suda 1985).
One disadvantage of Min-U-Gel and similar thickened
formulations is that they are short-lived when used in
areas subject to high temperatures and high rainfall
(Cunningham et al. 1975a,b; Cunningham and Suda
1985; Vargas et al. 2000). Furthermore, use of naled in
residential areas has met increasing opposition from
utility companies, home-owners and environmental
groups. Recent research has addressed replacement of
organophosphate insecticides with moderately toxic
insecticides, such as Þpronil (Vargas et al. 2005), or
reduced-risk insecticides, such as spinosad (Vargas et
al. 2003, 2008b), as well as traps, with novel dispensers
such as SPLAT (Specialized Pheromone and Lure
1363
Application Technology, ISCA Technologies) that
slows release of lure and allows for treatments to be
sprayed (Vargas et al. 2008a). Safer and more conve-
nient treatments would allow for the application of
more uniform and possibly fewer treatment points
within an area with little environmental impact. This
would allow for the treatment of environmentally
sensitive areas as well. The formulation containing
SPLAT, spinosad, and ME registered by Dow Agro-
Sciences in the United States and South Africa is called
“STATIC Spinosad ME;” the same formulation regis-
tered by ISCA Technologies in Brazil is called
“SPLAT-MAT Spinosad ME.” In small-scale trials in
Hawaii, Vargas et al. (2008a) Þrst demonstrated that
attraction of male B. dorsalis to the SPLAT-MAT-
Spinosad ME treatments equaled or outperformed
Min-U-Gel ME with naled. In addition, results indi-
cated excellent killing power of SPLAT-MAT-Spi-
nosad ME weathered for 8 wk when compared with
Min-U-Gel ME with naled. Spinosad has low contact
toxicity and when mixed with this amorphous polymer
matrix offers a reduced-risk alternative without many
of the negative impacts to humans and nontargets that
come with broad-spectrum contact insecticides. Its
versatility allows for various application methods
ranging from small-scale manual applications to large-
scale mechanical applications (Stelinski et al. 2007,
Piñero et al. 2011).
The objective of the current study was to compare
performance of STATIC Spinosad ME (at two appli-
cation amounts, 5 and 10 ml) with Min-U-Gel-naled
ME weathered under operational conditions under
California and Florida climatic conditions, at attract-
ing and killing male B. dorsalis through bioassays done
in Hawaii. In local attraction experiments conducted
using bucket traps, and in toxicity tests involving Þeld
cages and feeding tests in the laboratory, we compared
the STATIC Spinosad ME formulation to the standard
Min-U-Gel formulation with naled currently used in
eradication programs in California and Florida.
Materials and Methods
Insects. B. dorsalis were obtained from a colony
established from infested papaya and reared for no
more than two generations at the U.S. Department of
AgricultureÐAgricultural Research Service (USDAÐ
ARS), Daniel K. Inouye United States PaciÞc Basin
Agricultural Research Center (DKIUSPBARC) in
Hilo, HI, following the methods described in Vargas
(1989). Adult ßies were allowed to emerge inside
cubical screen cages (30 cm3) with a 3:1 mixture of
sucrose and USB enzymatic yeast hydrolysate (United
States Biochemical, Cleveland, OH) as a food source
and water ad libitum. All experimental ßies were held
in a laboratory maintained at 22 ⫾ 3⬚C and 60 Ð 80%
relative humidity (RH), and a photoperiod of 12:12
(L:D) h. All male ßies were tested after they reached
an age of 28 d to allow them to become sexually
mature.
Weathering in California and Florida. Three ME
treatments were evaluated: 1) 5 ml by volume of
1364 JOURNAL OF ECONOMIC ENTOMOLOGY
STATICÐSpinosad (2% active ingredient [a.i.])ÐME;
2) 10 ml by volume of STATICÐSpinosadÐME; and 3)
5 ml Min-U-Gel ME with naled (5% a.i.) (Dibrom
Concentrate; Valent USA, Walnut Creek, CA), cur-
rently in use in California and Florida (standard).
Treatments were applied by CDFA and FDACS staff
that normally execute eradication application proto-
cols in their state. All samples were weathered out-
doors in locations representative of the single areas in
California (Van Nuys) and Florida (Winter Haven)
where fruit ßy eradication applications have been or
are expected to be made. A metering gun (30 Gunjet
with Meterjet 23600, Spraying Systems Co, Wheaton,
IL) was attached to a pressurized gas cylinder back-
pack sprayer (model T, R & D Sprayers, Opelousas,
LA) and used to apply treatment amounts to the sur-
face of untreated quarter-inch plywood, measuring 15
by 15 cm, with a hole drilled near one corner, 2.5 cm
from each side. Plywood panels were hung on a weath-
ering tower oriented in one of the four cardinal di-
rections (North, South, East, and West) in direct sun-
light. Mean (⫾SEM) daily air temperature, RH, and
cumulative rainfall values based on Hobo data record-
ers (Onset Computer Corporation, Pocasset, MA)
maintained at the weathering site were: 24.8 ⫾ 1.8⬚C
(range: 14.4 Ð39.4⬚C), 55.4% ⫾ 2.8 (24.0 Ð 84.0%), and
0.0 mm for Van Nuys, CA; and 26.8 ⫾ 0.4⬚C (23.9 Ð
28.4⬚C), 82.2% ⫾ 1.2 (73.0⫺95.0%), and 254.3 mm for
Winter Haven, FL. Each of the three different treat-
ments were weathered and tested for each of Þve
aging periods (1, 7, 14, 21, and 28 d) from 10 June to
8 July 2013. Rainfall at the Winter Haven, FL, weath-
ering site washed off some of the Min-U-Gel from the
plywood boards. Consequently, these tests were done
a second time from 26 August to 23 September 2013.
Mean (⫾SEM) daily air temperature, RH, and cumu-
lative rainfall values at the weathering site were:
26.6 ⫾ 0.3⬚C (21.3Ð34.7⬚C), 82.8% ⫾ 1.0 (75.0 Ð94.0%),
and 72.1 mm for Winter Haven, FL. At the prescribed
intervals, each panel was wrapped in tin foil, placed
inside a 1-gallon Ziploc bag (3.8 liters), and then in-
dividually placed in a bubble envelope. Treatment
replicates were grouped and sealed inside a container
(4-liter polyethylene, Rubbermaid, Fairlawn, OH),
and all samples were then boxed and sent overnight
express. Once received in Hawaii, samples were
placed in a freezer held at 0⬚C until deployed in a
designated test.
Field Attraction in Hawaii. Field attraction exper-
iments were conducted on 2 August 2013 using a
randomized complete block design. For this experi-
ment, we used plastic bucket traps. Each trap was
constructed from a plastic container (LT-804-165,
Highland Plastics, Mira Loma, CA; 20 cm in height and
21.5 cm in diameter), which was drilled on the sides
to create four entry points. For STATIC treatments, a
plastic 1.5-ml microcentrifuge tube (Fisher, Hampton,
NH) that had the tip cut off (diameter of the resulting
hole: 6 mm) was inserted in a 1-cm hole to permit
responding males to enter but not exit. For Min-U-Gel
treatments, entry holes were larger (2.5 cm in diam-
eter) without centrifuge tubes to ensure ßies did not
Vol. 107, no. 4
die inside centrifuge tubes and block entry holes ow-
ing to the fumigant killing effect of naled. Each trap
had a plastic lid through which a 30-cm steel wire was
placed and secured with a drop of glue. In Þeld tests
all treatments were deployed simultaneously in four
separate 3 acre (1.2 ha) commercial papaya orchards
(19⬚ 37⬘15⬙ N, 155⬚ 04⬘22⬙ W, elevation 685 feet),
Keaau, Hawaii Island, HI, to quantify the relative at-
tractiveness of each ME formulation to wild male B.
dorsalis. Starting at 0900 hours, traps were hung from
a papaya tree with a plastic tie at eye level for a 4-h
period, allowing wild B. dorsalis males to enter traps.
Traps for each of the Þve time periods and for all three
treatments (for Florida and California) were placed in
one of the four orchards at 10-m intervals (three treat-
ments ⫻ four replicates ⫻ two locations ⫻ 5 wk ⫽ 120
traps). Four persons were needed to deploy and ser-
vice the trap sets simultaneously. At the end of Þeld
tests, microcentrifuge tube caps were closed for
STATIC treatments and masking tape was applied to
the 2.5 cm (1 inch) holes for Min-U-Gel treatments.
All traps were brought back to the laboratory where
numbers of males captured were counted.
Cage Attraction and Mortality. Relative attraction
and toxicity of ME treatments associated with each
toxicant, spinosad or naled, were measured in 1-m3
screen cages deployed from 17 June to 18 July 2013 at
the DKIUSPBARC in Hilo, HI, using laboratory-
reared male B. dorsalis. For each of the Þve aging
periods on each test day, one treated wood panel was
hung inside each screen cage containing a Þberglass
tray with food (3:1 sucrose/yeast hydrolysate), water,
and a guava plant (Psidium guajava L.) in a 1-gallon
(3.8 liter) pot held inside an open air covered head-
house. Twenty laboratory-reared males were released
per cage between 0800 and 0900 hours. After the ßies
were released, an observer recorded the number of
dead males after 4 and 24 h exposure to panels. One
replicate from each location (one per day) was done
for each treatment. For each of the Þve aging periods,
four replicates of each of the three ME treatments
were tested. In total, 480 males was tested for each
aging period (2,400 males in all) or four replicates for
each substance-combination within an age category
(three treatments ⫻ four replicates ⫻ two locations ⫻
20 ßies ⫻ 5 wk).
Feeding and Mortality. The relative toxicity of the
three ME formulations described above was assessed
under laboratory conditions (PBARC) maintained at
22.0 ⫾ 2.0⬚C, 50 Ð 60% RH, and a photoperiod of 12:12
(L:D) h using laboratory-reared males. Feeding tests
were conducted from 17 June to 18 July 2013. Indi-
vidual males were introduced into an experimental
cage (30 cm3) containing a particular treatment and
gently placed onto the test material. Each male was
allowed to feed for at least 1 min and up to 5 min
(maximum time). Given the compulsive feeding be-
havior exhibited by male B. dorsalis when in contact
with ME (Steiner 1952), males commonly fed for 5
min. After the 5-min feeding period, each male was
placed in an inverted small plastic cup (labeled) con-
taining a small cotton wick saturated with water. Mor-
August 2014 VARGAS ET AL.: REDUCED-RISK MALE ANNIHILATION TREATMENT 1365

Table 1. Captures (mean ⴞ SEM) of wild male B. dorsalis in bucket traps baited with various ME treatments that were weathered in
CA and FL for 1, 7, 14, 21, and 28 d and shipped to Hawaii for bioassays

Time period (d)

Location ME treatment
1 7 14 21 28
California 5 ml STATIC 132.5 ⫾ 109.3 43.0 ⫾ 19.2 34.8 ⫾ 14.3 19.8 ⫾ 3.1 21.0 ⫾ 7.6
10 ml STATIC 82.0 ⫾ 30.4 76.8 ⫾ 49.8 49.5 ⫾ 25.9 51.0 ⫾ 27.4 30.8 ⫾ 20.4
Min-U-Gel 155.3 ⫾ 73.8 128.8 ⫾ 57.6 52.3 ⫾ 17.5 41.0 ⫾ 17.5 48.0 ⫾ 31.2
Florida 5 ml STATIC 59.3 ⫾ 30.7 20.3 ⫾ 9.4 16.5 ⫾ 12.3 5.5 ⫾ 1.6 0.8 ⫾ 0.5
10 ml STATIC 93.3 ⫾ 31.7 23.8 ⫾ 8.3 14.5 ⫾ 5.8 14.5 ⫾ 7.4 1.0 ⫾ 0.6
Min-U-Gel 89.8 ⫾ 41.4 30.5 ⫾ 9.3 3.3 ⫾ 2.6 3.3 ⫾ 2.3 0.0 ⫾ 0.0

Traps were hung from papaya trees in four separate 1.21-ha orchards for 4 h. Studies were conducted on 2 Aug. 2013 (randomized complete
block design). For each location and within each weathered time category, values in a different column followed by different letters are
signiÞcantly different according to ANOVA at the P ⫽ 0.05 level LSD Test (StatSoft Inc. 2011; California: 1 d: F2,9 ⫽ 0.23, P ⫽ 0.799; 7 d: F2,9 ⫽
0.91, P ⫽ 0.438; 14 d: F2,9 ⫽ 0.23, P ⫽ 0.803; 21 d: F2,9 ⫽ 0.38, P ⫽ 0.695; 28 d: F2,9 ⫽ 0.39, P ⫽ 0.689; Florida: 1 d: F2,9 ⫽ 0.29, P ⫽ 0.757; 7 d:
F2,9 ⫽ 0.34, P ⫽ 0.724; 14 d: F2,9 ⫽ 0.80, P ⫽ 0.478; 21 d: F2,9 ⫽ 1.80, P ⫽ 0.223; 28 d: F2,9 ⫽ 1.44, P ⫽ 0.286).

tality was recorded after 4 and 24 h. Because 10 males Results

were exposed in sequence to the same material, mor-
tality was calculated as a proportion (number of males
dead by 10 males that fed on a given treatment). For
each of the Þve aging periods, four replicates of each
of the three ME treatments were evaluated. In all,
1,200 males were individually tested.
Statistical Analysis. For the Þeld attraction study
with bucket traps, captures of male B. dorsalis with the
three ME treatments were compared using a one-way
analysis of variance (ANOVA), data were transformed
[sqrt(x ⫹ 0.5)] when needed to stabilize variances.
Means were compared using the Fisher-protected
least signiÞcant difference test with P ⫽ 0.05. For cage
and feeding studies, mortality induced by STATIC
with spinosad was compared, for every time period,
against that of Min-U-Gel-ME with naled using a one-
way ANOVA. Proportion data were arcsine-trans-
formed before analysis. For data that did not meet the
assumptions of normality, a nonparametric KruskalÐ
Wallis Test was done. Untransformed means are pre-
sented in all tables. Because two different work crews
applied test materials, and rainfall varied at the two
weathering sites, noticeably affecting the amount of
Min-U-Gel on the plywood boards shipped from Flor-
ida, we decided to present results for California and
Florida separately. In another article, we will present
models of ME, spinosad, and naled degradation over
time. All statistical analyses were conducted using
STATISTICA 10.0 (StatSoft Inc. 2011, Tulsa, OK).
Field Attraction in Hawaii. With the California and
Florida weathered samples, B. dorsalis captures were
not signiÞcantly different for the three ME treatments
within each weathered time category of 1, 7, 14, 21,
and 28 d (Table 1) for Þeld tests. In the second Florida
trial, STATIC (10 ml) was signiÞcantly more attractive
than the other two treatments (STATIC [5 ml] and
Min-U-Gel) at 14 and 21 d (Table 2).
Cage Attraction and Mortality. In the cage test
with California weathered samples, mortality at 4 h
was signiÞcantly different for 5 and 10 ml STATIC
treatments and Min-U-Gel at 7, 14, 21, and 28 d (Table
3). In contrast, no signiÞcant differences were ob-
served in mortality after 24 h for any of the time
periods. In cage tests with Florida weathered samples,
signiÞcant differences were only observed at 1 and 7 d
for 4 h mortality between STATIC and Min-U-Gel
treatments. However, no signiÞcant differences were
observed in 24 h mortality trials for any of the time
periods. In the second Florida trial, mortality at 4 h was
signiÞcantly higher for the Min-U-Gel treatments than
for the STATIC treatments at 7 d (Table 4). However,
mortality at 24 h was signiÞcantly higher with STATIC
(5 and 10 ml) treatments compared with mortality for
Min-U-Gel at 14 and 21 d.
Feeding and Mortality. In the 5-min feeding tests
with California weathered samples, mortality at 4 h was
signiÞcantly different for 5 and 10 ml STATIC treatments
and Min-U-Gel for all time periods (Table 5). No sig-

Table 2. Captures (mean ⴞ SEM) of wild male B. dorsalis in bucket traps baited with various ME treatments that were weathered in
FL for 1, 7, 14, 21, and 28 d and shipped to Hawaii for bioassays

Time period (d)

Location ME treatment
1 7 14 21 28
Florida 5 ml STATIC 472.8 ⫾ 57.2 221.5 ⫾ 34.3 276.8 ⫾ 32.4b 162.5 ⫾ 39.4b 101.8 ⫾ 9.5
10 ml STATIC 657.8 ⫾ 130.1 386.3 ⫾ 35.6 430.8 ⫾ 48.8a 321.3 ⫾ 25.0a 220.8 ⫾ 64.0
Min-U-Gel 865.5 ⫾ 115.3 248.8 ⫾ 75.8 50.3 ⫾ 11.4c 92.0 ⫾ 13.1b 101.3 ⫾ 19.0

Traps were hung from papaya trees in four separate 1.21 ha orchards for 4 h. Studies were conducted on 10 Jan. 2014 (randomized complete
block design). For each location and within each weathered time category, values in a different column followed by different letters are
signiÞcantly different according to ANOVA at the P ⫽ 0.05 level LSD Test (StatSoft Inc. 2011; Florida: 1 d: F2,9 ⫽ 3.46, P ⫽ 0.077; 7 d: F2,9 ⫽
2.86, P ⫽ 0.109; 14 d: F2,9 ⫽ 30.84, P ⱕ 0.001; 21 d: F2,9 ⫽ 17.59, P ⱕ 0.001; 28 d: F2,9 ⫽ 3.72, P ⫽ 0.067).
1366 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 107, no. 4

Table 3. Mortality (mean % ⴞ SEM) of laboratory-reared male B. dorsalis induced by three ME treatments associated with a toxicant
(either spinosad or naled)

Time period (d)

Location Mortality ME treatment
1 7 14 21 28
California 4h 5 ml STATIC 91.3 ⫾ 4.3 80.0 ⫾ 7.4b 30.0 ⫾ 4.6b 26.3 ⫾ 10.7b 15.0 ⫾ 10.2b
10 ml STATIC 71.3 ⫾ 11.3 70.0 ⫾ 2.9b 40.0 ⫾ 14.3b 46.3 ⫾ 10.1b 6.3 ⫾ 3.1b
Min-U-Gel 88.8 ⫾ 5.2 97.5 ⫾ 2.5a 91.3 ⫾ 4.3a 87.5 ⫾ 3.2a 92.5 ⫾ 4.3a
24 h 5 ml STATIC 95.0 ⫾ 2.9 98.8 ⫾ 1.3 97.5 ⫾ 1.4 96.3 ⫾ 1.3 92.5 ⫾ 3.2
10 ml STATIC 96.3 ⫾ 1.3 100.0 ⫾ 0.0 96.3 ⫾ 2.4 95.0 ⫾ 2.0 97.5 ⫾ 1.4
Min-U-Gel 97.5 ⫾ 2.5 100.0 ⫾ 0.0 95.0 ⫾ 2.9 95.0 ⫾ 2.0 97.5 ⫾ 2.5
Florida 4h 5 ml STATIC 82.5 ⫾ 7.2ab 32.5 ⫾ 7.5b 15.0 ⫾ 11.9 18.8 ⫾ 15.6 10.0 ⫾ 8.4
10 ml STATIC 78.8 ⫾ 5.2b 68.8 ⫾ 15.3ab 25.0 ⫾ 15.5 13.8 ⫾ 6.3 5.0 ⫾ 3.5
Min-U-Gel 97.5 ⫾ 2.5a 83.8 ⫾ 10.1a 31.3 ⫾ 14.0 35.0 ⫾ 7.4 37.5 ⫾ 17.6
24 h 5 ml STATIC 95.0 ⫾ 3.5 88.8 ⫾ 1.3 68.8 ⫾ 21.3 92.5 ⫾ 2.5 78.8 ⫾ 8.3
10 ml STATIC 95.0 ⫾ 2.0 92.5 ⫾ 7.5 81.3 ⫾ 8.3 86.3 ⫾ 7.5 76.3 ⫾ 11.4
Min-U-Gel 97.5 ⫾ 2.5 88.8 ⫾ 9.7 58.8 ⫾ 8.3 83.8 ⫾ 8.0 77.5 ⫾ 14.5

Materials were weathered in CA and FL for 1, 7, 14, 21, and 28 d and shipped to HI for bioassays. For each test day, groups of 20 males were
released inside 1-m3 cages with one ME treatment, food and water. Studies were conducted from 17 June to 18 July 2013 at USDA-ARS-
USPBARC, Hilo, HI. For each location and within each mortality period, values in a different column followed by different letters are
signiÞcantly different according to ANOVA at the P ⫽ 0.05 level LSD Test (StatSoft Inc. 2011)(CA: mortality 4 h: 1 d: F2,9 ⫽ 1.84, P ⫽ 0.214;
7 d: F2,9 ⫽ 11.66, P ⫽ 0.003; 14 d: F2,9 ⫽ 15.4, P ⫽ 0.001; 21 d: F2,9 ⫽ 16.12, P ⫽ 0.001; 28 d: F2,9 ⫽ 37.19, P ⫽ 0.001; mortality 24 h: 1 d: F2,9 ⫽
0.40, P ⫽ 0.683; 7 d: F2,9 ⫽ 1.00, P ⫽ 0.405; 14 d F2,9 ⫽ 0.09, P ⫽ 0.917; 21 d: F2,9 ⫽ 0.05, P ⫽ 0.956; 28 d: F2,9 ⫽ 1.11, P ⫽ 0.370; FL: mortality
4 h: 1 d: F2,9 ⫽ 4.38, P ⫽ 0.047; 7 d: F2,9 ⫽ 5.30, P ⫽ 0.030; 14 d: F2,9 ⫽ 0.34, P ⫽ 0.721; 21 d: F2,9 ⫽ 1.00, P ⫽ 0.405; 28 d: F2,9 ⫽ 2.33, P ⫽ 0.153;
mortality 24 h: 1 d: F2,9 ⫽ 0.49, P ⫽ 0.629; 7 d: F2,9 ⫽ 0.09, P ⫽ 0.912; 14 d: F2,9 ⫽ 0.34, P ⫽ 0.721; 21 d: F2,9 ⫽ 0.37, P ⫽ 0.701; 28 d: F2,9 ⫽ 0.03,
P ⫽ 0.975).

niÞcant differences were observed in mortality after
24 h until 28 d. In the 5-min feeding tests with
Florida weathered samples, signiÞcant differences
were only observed at the 7-d time period for 4 h
mortality between STATIC and Min-U-Gel treat-
ments. No signiÞcant differences were observed in
the 24 h mortality with treatments for any of the
time periods. In the second Florida test, mortality at
4 h was signiÞcantly different for 5 and 10 ml
STATIC treatments and Min-U-Gel for only the 7-d
period (Table 6). No signiÞcant differences were
observed in the 24 h mortality with treatments for
any of the time periods.
Discussion
In initial small-scale trials in Hawaii and subsequent
weathering trials in California, Vargas et al. (2008a,b,
2009) provided evidence that reduced-risk formula-
tions of SPLAT with ME and spinosad (SPLAT-MAT-
spinosad-ME) performed equally as well or better
than standard Min-U-Gel with naled (Cunningham
and Suda 1985). In small-scale trials conducted in
Tahiti, applications of SPLAT-MAT-spinosad-ME un-
der various weathering conditions were equal to fresh
material for up to 4 wk (Leblanc et al. 2011). In
addition, demonstration trials in fruit orchards under
various climatic conditions and crops indicated sig-
niÞcant population reductions of B. carambolae, car-
ambola fruit ßy, in Brazil and B. dorsalis, in Hawaii,
respectively, with application of SPLAT-MAT-Spi-
nosad ME (Vargas et al. 2014). In the current study
done under operational conditions in California and
Florida, the relative attractiveness and toxicity of
STATIC Spinosad ME (aka SPLAT-MAT-Spinosad-
ME) to male B. dorsalis were compared with Min-U-
Gel ME and naled currently used in California and
Florida during eradications of accidental introduc-
tions of Bactrocera fruit ßies. In Þeld tests involving
bucket traps to attract and capture wild males and in

Table 4. Mortality (mean % ⴞ SEM) of laboratory-reared male B. dorsalis induced by three ME treatments associated with a toxicant
(either spinosad or naled)

Time Period (d)

Location Mortality ME treatment
1 7 14 21 28
Florida 4h 5 ml STATIC 85.0 ⫾ 8.7 67.5 ⫾ 8.5b 57.5 ⫾ 7.5 27.5 ⫾ 11.8 25.0 ⫾ 11.9
10 ml STATIC 92.5 ⫾ 4.8 65.0 ⫾ 15b 67.5 ⫾ 13.8 45.0 ⫾ 20.6 15.0 ⫾ 6.4
Min-U-Gel 100 100a 62.5 ⫾ 9.5 15.0 ⫾ 5.0 60.0 ⫾ 19.1
24 h 5 ml STATIC 100 95.0 ⫾ 2.8 100a 95.0 ⫾ 5.0a 97.5 ⫾ 2.5
10 ml STATIC 100 95.0 ⫾ 5.0 100a 97.5 ⫾ 2.5a 100
Min-U-Gel 100 100.0 ⫾ 0.0 85.0 ⫾ 6.4b 77.5 ⫾ 4.8b 90.0 ⫾ 7.1

Materials were weathered in FL for 1, 7, 14, 21, and 28 d and shipped to HI for bioassays. For each test day, groups of 20 males were released
inside a 1-m3 cages with one ME treatment, food, and water. Studies were conducted from 3 Sept. to 30 Oct. 2013 at USDA-ARS-PBARC, Hilo,
HI. For each location and within each mortality period, values in a different column followed by different letters are signiÞcantly different
according to ANOVA at the 0.05 level LSD (Florida: mortality 4 h: 1 d: F2,9 ⫽ 2.55, P ⫽ 0.133; 7 d: F2,9 ⫽ 10.77, P ⫽ 0.004; 14 d: F2,9 ⫽ 0.45,
P ⫽ 0.653; 21 d: F2,9 ⫽ 1.18, P ⫽ 0.350; 28 d: F2,9 ⫽ 3.24, P ⫽ 0.087; mortality 24 h: 7 d: F2,9 ⫽ 0.86, P ⫽ 0.456; 14 d: F2,9 ⫽ 0.7.50, P ⫽ 0.012; 21 d:
F2,9 ⫽ 6.35, P ⫽ 0.019; 28 d: F2,9 ⫽ 1.49, P ⫽ 0.275).
August 2014 VARGAS ET AL.: REDUCED-RISK MALE ANNIHILATION TREATMENT 1367

Table 5. Mortality (mean % ⴞ SEM) of laboratory-reared male B. dorsalis in feeding studies in the laboratory

Time period (d)

Location Mortality ME treatment
1 7 14 21 28
California 4h 5 ml STATIC 75.0 ⫾ 8.7b 57.5 ⫾ 7.5b 57.5 ⫾ 11.1b 67.5 ⫾ 4.8b 45.0 ⫾ 13.2b
10 ml STATIC 55.0 ⫾ 11.9b 50.0 ⫾ 9.1b 55.0 ⫾ 13.2b 55.0 ⫾ 11.9b 17.5 ⫾ 4.8c
Min-U-Gel 100.0 ⫾ 0.0a 100.0 ⫾ 0.0a 100.0 ⫾ 0.0a 100.0 ⫾ 0.0a 100.0 ⫾ 0.0a
24 h 5 ml STATIC 100.0 ⫾ 0.0 100.0 ⫾ 0.0 97.5 ⫾ 2.5 95.0 ⫾ 2.9 60.0 ⫾ 9.1b
10 ml STATIC 100.0 ⫾ 0.0 100.0 ⫾ 0.0 92.5 ⫾ 4.8 100.0 ⫾ 0.0 72.5 ⫾ 8.5b
Min-U-Gel 100.0 ⫾ 0.0 100.0 ⫾ 0.0 100.0 ⫾ 0.0 100.0 ⫾ 0.0 100.0 ⫾ 0.0a
Florida 4h 5 ml STATIC 70.0 ⫾ 14.7 17.5 ⫾ 2.5b 17.5 ⫾ 11.1 12.5 ⫾ 4.8 5.0 ⫾ 5.0
10 ml STATIC 72.5 ⫾ 11.1 40.0 ⫾ 16.3b 5.0 ⫾ 2.9 5.0 ⫾ 5.0 0.0 ⫾ 0.0
Min-U-Gel 100.0 ⫾ 0.0 85.0 ⫾ 8.7a 45.0 ⫾ 20.2 50.0 ⫾ 18.3 10.0 ⫾ 10.0
24 h 5 ml STATIC 100.0 ⫾ 0.0 57.5 ⫾ 2.5 55.0 ⫾ 17.1 40.0 ⫾ 10.8 15.0 ⫾ 6.5
10 ml STATIC 100.0 ⫾ 0.0 72.5 ⫾ 21.0 55.0 ⫾ 6.5 37.5 ⫾ 7.5 12.5 ⫾ 6.3
Min-U-Gel 100.0 ⫾ 0.0 92.5 ⫾ 4.8 90.0 ⫾ 7.1 55.0 ⫾ 20.6 25.0 ⫾ 11.9

Individual males (10 per replicate) were allowed to feed for 5 min (except for Min-U-Gel treatment that resulted in mortality prior to time
limit) on one of three ME treatments (toxicant either spinosad or naled) that were weathered in CA and FL and sent to HI for bioassays.
Materials were weathered for 1, 7, 14, 21, and 28 d. A single male was gently placed on one ME treatment inside a 30-cm3 cage. Feeding studies
were conducted from 17 June to 18 July 2013 at USDA-ARS-USPBARC, Hilo, HI. For each location, and within each mortality period, values
in a different column followed by different letters are signiÞcantly different according to ANOVA at the P ⫽ 0.05 level, LSD Test (StatSoft
Inc. 2011) (CA: mortality 4 h:1 d: F2,9 ⫽ 10.81, P ⫽ 0.004; 7 d: F2,9 ⫽ 49.84, P ⫽ 0.001; 14 d: F2,9 ⫽ 20.52, P ⫽ 0.001; 21 d: F2,9 ⫽ 24.04, P ⫽ 0.001;
28 d: F2,9 ⫽ 66.28, P ⫽ 0.001; mortality 24 h: 14 d: F2,9 ⫽ 1.45, P ⫽ 0.285; 21 d: F2,9 ⫽ 3.00, P ⫽ 0.100; 28 d: F2,9 ⫽ 23.66, P ⫽ 0.001; FL: mortality
4 h: 1 d: F2,9 ⫽ 3.60, P ⫽ 0.071; 7 d: F2,9 ⫽ 9.68, P ⫽ 0.006; 14 d: F2,9 ⫽ 1.93, P ⫽ 0.200; 21 d: H(2, N ⫽ 12), ⫽ 5.50, P ⫽ 0.064; 28 d: F2,9 ⫽ 0.61,
P ⫽ 0.567; mortality 24 h: 7 d: F2,9 ⫽ 2.83, P ⫽ 0.112; 14 d: F2,9 ⫽ 2.86, P ⫽ 0.109; 21 d: F2,9 ⫽ 7.00, P ⫽ 0.520; 28 d: F2,9 ⫽ 0.62, P ⫽ 0.558).

toxicity studies conducted in 1-m3 cages using released
males of controlled ages, STATIC Spinosad ME per-
formed equally as well as the standard formulation of
Min-U-Gel ME with naled for material aged up to 28 d
in both California and Florida. In laboratory feeding
tests in which individual males were exposed for 5 min
to the different ME treatments, mortality induced by
STATIC Spinosad ME recorded at 24 h did not differ
from that caused by Min-U-Gel ME with naled at 1, 7,
14, and 21 d in California and all weathered time
periods in Florida. Our results with STATIC Spinosad
ME in operational trials are consistent with previous
small-scale trials (Vargas et al. 2008a, 2009) and fall
within the 14 d application schedule recommended in
eradication protocols in California and Florida. Ap-
plication of 10 ml of STATIC Spinosad ME produced
more consistent results than 5 ml of STATIC Spinosad
ME. Rain in Florida washed away Min-U-Gel rapidly;
however, there was still attraction and mortality to
ßies landing on blank plywood squares owing to the
ME and naled that was absorbed.
The frequency of fruit ßy detections in California
requires annual applications of MAT with naled.
Ninety percent of the eradication projects (243 of
274) initiated in California between 1982 and 2007
were directed against tropical fruit ßies (Papadopou-
los et al. 2013), many of these in urban areas. In the
summer and fall of 2013, California had delimitations
in Þve counties (Alameda, Los Angeles, Orange, San
Diego, and Santa Clara), eradications in six counties
(Alameda, Los Angeles, Orange, San Bernardino,
Solano, and Santa Clara), and quarantine in one
county (OrangeÐLos Angeles County) for three sep-
arate ME responding species B. dorsalis (seven de-
limitations, six eradications, one quarantine), peach
fruit ßy, Bactrocera zonata (Saunders) (one delimita-
tion, three eradications), and guava fruit ßy, Bactro-
cera correcta (Bezzi) (three delimitations, one erad-
ication), and Florida initiated a delimitation zone for
a single detection of B. correcta during that time. The
need to reduce the use of organophosphates in resi-
dential and commercial areas has become a priority.

Table 6. Mortality (mean % ⴞ SEM) of laboratory-reared male B. dorsalis in feeding studies in the laboratory

Time Period (d)

Location Mortality ME treatment
1 7 14 21 28
Florida 4h 5 ml STATIC 72.5 ⫾ 24.3 55.0 ⫾ 15.0b 40.0 ⫾ 12.2 15.0 ⫾ 9.6 2.5 ⫾ 2.5
10 ml STATIC 72.5 ⫾ 18.9 60.0 ⫾ 12.9b 35.0 ⫾ 8.7 15.0 ⫾ 5.0 27.5 ⫾ 11.8
Min-U-Gel 97.5 ⫾ 2.5 100a 50.0 ⫾ 26.1 7.5 ⫾ 7.5 27.5 ⫾ 24.3
24 h 5 ml STATIC 100 85.0 ⫾ 8.7 72.5 ⫾ 11.8 70.0 ⫾ 17.8 70.0 ⫾ 9.1
10 ml STATIC 100 95.0 ⫾ 5.0 90.0 ⫾ 10.0 75.0 ⫾ 13.2 87.5 ⫾ 6.3
Min-U-Gel 100 100 55.0 ⫾ 24.0 35.0 ⫾ 15.0 60.0 ⫾ 15.8

Individual males (10 per replicate) were allowed to feed for 5 min (except for Min-U-Gel treatment that resulted in mortality prior to time
limit) on one of three ME treatments (toxicant either spinosad or naled) that were weathered in FL and sent to HI for bioassays. Materials
were weathered for 1, 7, 14, 21, and 28 d. A single male was gently placed on one ME treatment inside a 30-cm3 cages. Feeding studies were
conducted from 3 Sept. to 30 Oct. 2013 at USDA-ARS-PBARC, Hilo HI. For each location, and within each mortality period, values in a different
column followed by different letters are signiÞcantly different according to ANOVA at the P ⫽ 0.05 level LSD (Florida: mortality 4 h: 1 d: F2,9 ⫽
0.65, P ⫽ 0.546; 7 d: F2,9 ⫽ 12.05, P ⫽ 0.003; 14 d: F2,9 ⫽ 0.55, P ⫽ 0.597; 21 d: F2,9 ⫽ 0.32, P ⫽ 0.734; 28 d: H(2, N ⫽ 12) ⫽ 4.09, P ⫽ 0.1292; mortality
24 h: 7 d: F2,9 ⫽ 1.53, P ⫽ 0.268; 14 d: F2,9 ⫽ 1.03, P ⫽ 0.396; 21 d: F2,9 ⫽ 1.922, P ⫽ 0.202; 28 d: F2,9 ⫽ 1.039, P ⫽ 0.393).
1368 JOURNAL OF ECONOMIC ENTOMOLOGY
STATIC spinosad ME offers a novel and convenient
ready-to-use MAT formulation that is safer than the
current use of organophosphates that may pose po-
tential negative effects on human and environmental
health. Also, even though the program pesticides are
not persistent, their temporary presence could con-
tribute to the overall pesticide load of an area (USDA
2001), particularly, with multiple delimitation, eradi-
cation, and quarantine efforts running simultaneously.
From a homeowner perspective, the use of a reduced-
risk treatment would be more appealing and reduce
the reluctance to allow property access. About one
half of households in California maintain at least one
fruit tree that is a fruit ßy host (CDFA 1993). For
ground crews, the ready-to-use STATIC formulations
would eliminate the process of handling and mixing
liquid formulations of Min-U-Gel and naled. Given the
frequency of detection over the last two decades, the
opportunity to implement an additional option for
fruit ßy eradication protocol seems reasonable.
Acknowledgments
We thank Russell Ijima, Jordan “Kama” Lee Loy, and Daisy
L. Willis (PaciÞc Basin Agricultural Research Center, USDAÐ
ARS, Hilo, HI) for experimental setup and data collection
throughout these trials. We thank James Mueller and Ale-
jandro Calixto (DowAgroSciences) for technical advice and
assistance in applying the treatments. In addition, we thank
Synda Boulahia-Kheder (National Institute of Agronomy,
Cité Mahrajène, Tunisia) and Ming-Yi Chou (University of
Hawaii at Manoa, Honolulu, HI) for coordinating feeding
trials. We thank W.H. Shipman Limited, A & B Properties,
and Kauai Coffee Plantation, and in particular, Randall S.
Akao, Greg Williams, and various papaya growers for allow-
ing access to Þeld sites for Þeld attraction evaluations. We
also thank Patrick J. Gomes and John C. Stewart of the Animal
and Plant Health Inspection Service (APHIS) for their sup-
port and guidance. We appreciate the advice and input of
Earl Andress (APHIS, Los Alamitos, CA) for the Þeld trials.
Without the Þnancial support of CDFA (Sacramento, CA)
these trials could not have been completed. We also recog-
nize the contributions of Agenor Mafra-Neto in formulating
and manufacturing the spinosad test product (ISCA Tech-
nologies, Riverside, CA). IR-4 funds were essential for plan-
ning and completing this research. Finally, we appreciate the
comments by John Stark, Luc Leblanc, Robert Dowell, and
Nicholas Manoukis on an earlier version of this manuscript.
Mention of a proprietary product does not constitute an
endorsement or a recommendation by the USDA for its use.
USDA is an equal opportunity provider and employer.
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