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1
Eects of Four Chitin Synthesis Inhibitors on Feeding and
Mortality of the Eastern Subterranean Termite, Reticulitermes
avipes Kollar (Isoptera: Rhinotermitidae).
by
Rebecca D. Vahabzadeh1, Roger E. Gold1,2 & James W. Austin1
ABSTRACT
Baiting for termite population management has shown great potential.
Studies have shown successful use of diubenzuron and hexaumuron in
commercially available baiting systems. Both are chitin synthesis inhibitors in
the benzoylphenyl urea cheimcial group. Other pesticides in this same chemi-
cal grouping have shown activity against termites, but comparative research
has been lacking. is study measured changes in feeding and mortality of
the Eastern subterranean termite Reticulitermes avipes when exposed to
paper discs treated with one of four chitin synthesis inhibitors including;
diubenzuron, hexaumuron, lufenuron, and triumuron in laboratory tests.
All were benzoylphenyl ureas, and tests included ve dierent concentra-
tions of each. Evidence of the “jackknifed” posture characteristic of chitin
synthesis inhibition during eclosion when molting, overall mean survivor-
ship, and survivorship through time were all observed. e results varied
with chemical and concentration, but all treatments caused more mortality
among termite populations than untreated controls. When presented with
choices, R. avipes did not show denitive preferences in a majority of the
tests. Lufenuron was highly acceptable to R. avipes, and caused high rates of
mortality at all concentrations tested. Hexaumuron and triumuron showed
similar acceptability and mortality at only two of the concentrations tested.
Although diubezuron was acceptable to the termites, mortality at six weeks
post-exposure was signicantly lower than with other chemicals tested.
Keywords: Subterranean termites, Reticulitermes avipes Kollar, chitin
synthesis inhibitors, insect growth regulators, termite baiting systems.
1Center for Urban & Structural Entomology, Department of Entomology, Texas A&M University,
College Station, Texas, USA 77843-2143
2corresponding author. Email:r-gold@tamu.edu.
2 Sociobiology Vol. 50, No. 3, 2007
INTRODUCTION
Because of wide distribution, Reticulitermes avipes Kollar, the Eastern
subterranean termite, causes the most economic damage of any single termite
species in North America (Austin et al. 2005; Austin et al. 2006; Cornelius
and Osbrink 2001; Grace et al. 1989; Heintschel et al. 2006; Jones and LaFage
1980; Szalanski et al. 2003). ese termites usually need contact with the soil
in order to produce a successful colony, although some, including R. avipes,
are able to form ‘aerial’ colonies with no soil contact if sucient moist condi-
tions exist (Su et al. 1989). Subterranean termites are found in virtually every
state in the United States with the exception of Alaska (Jones and LaFage
1980). Estimated costs associated with termite control and repair to urban
structures range from $2 billion (Gold et al. 1996) to $4 billion (NPMA
2004) in the United States, with global estimates exceeding $22 billion (Su
2002). Subterranean termites account for approximately 80% of this damage
(Su 1994). Reticulitermes avipes present a challenge to pest management
professionals (PMPs) and homeowners due to cryptic lifestyles. Homeown-
ers are oen only aware of the presence of these termites in their home when
the damage that they cause is signicant and the structural integrity of their
home is compromised. Most frequently, it is only aer the reproductive
caste is encountered (the alates), and then only during the swarming season
(Furman 2000). However, virtually all of the damage (to structural timbers)
is done by the foraging castes (Su 1994; Su and Scheran 2000), principally
known as workers or pseudergates.
Since the early 1940s, perimeter treatments using persistent soil-applied
pesticides have been to protect structures throughout the world. ese pe-
rimeter treatments have been eective, but when inconsistent applications
are made, even slight gaps in treatment areas may allow termites access to
vulnerable structures, especially when repellent termiticides are used (Kurica-
han and Gold 1998). A liquid chemical barrier to termites can be eective,
but concerns over environmental contamination with pesticides have raised
questions about the advisability of using this approach in the long term. For
this reason, pest management professionals (PMPs) have employed several
pre-construction options including the use of physical barriers, wood treat-
ments, and bait delivery systems which exploit the biological demands of
termites.
3
Vahabzadeh, R.D. et al.— R.Flavipes mortality to CSIs
e use of termite baiting systems as a means of preventing and controlling
subterranean termite populations was initiated in 1967, and these technologies
have been extensively researched since that time (Esenther and Gray 1968;
Pawson and Gold 1996; Su and Scherahn 1996b; Haagsma and Bean 1998;
Kistner and Sbragia 2001; Ring et al. 2001; Tsundoa et al. 2001). e theory
behind using baits to control a termite population is that an entire colony
can be aected when a slow-acting, non-repellant chemical is distributed to
the colony by social interactions with the exposed foragers (Su et al. 1987).
ese social interactions include trophallaxis (stomodeal and proctodaeal),
allogrooming, and necrophagy.
Baits using Mirex were the rst to show success in the eld. Mirex baits
were found to eectively control Reticulitermes in Southern Mississippi, but
the United States Environmental Protection Agency (EPA) banned Mirex for
use in the United States (Esenther and Beal 1974, 1978). is led entomolo-
gists to look at other chemicals that would have potential for use in baits,
including chitin synthesis inhibitors (CSIs) (Esenther and Beal 1978; Dop-
pelreiter and Korioth 1981; Pawson and Gold 1996; Jones 1984; Ahmad et
al. 1986; Su and Scherahn 1991; Su and Scherahn 1993; Su et al., 1997;
Haagsma and Bean 1998; Grace and Su 2001; Kistner and Sbragia 2001; Su
et al. 2001; Tsunoda et al. 2001).
CSIs are a category of insect growth regulators that interfere with the
assembly of chitin aer a molt (Pedigo 1996). e four chemicals that
were used in this study belong to the chemical group called benzoylphenyl
ureas (BPUs) (Fig. 1). We use BPUs and chitin synthesis inhibitors (CSIs)
interchangeably throughout the paper, but their subtle dierences should
be noted, as described herein. e exact mode of action of BPUs is not fully
understood; however, it is known that BPUs do not inhibit chitin synthetase,
the enzyme controlling the last step of the process, but rather seem to interfere
with the assembly of chitin chains and microbrils. When immature stages
of insects are exposed to BPUs, they are incapable of completing ecdysis. As a
consequence, termites die during the molting process (Graf 1999). BPUs are
highly lipophilic molecules, and when administered to the host, they tend to
deposit in the body fat, where they are slowly released into the blood stream.
is mechanism is complemented by the fact that only a small amount of the
molecule is metabolized. A high percentage of the excretion of these chemicals
4 Sociobiology Vol. 50, No. 3, 2007
occurs in the form of the unchanged parent molecule. Because of this trait,
a natural slow release occurs that prolongs the bioavailability of these com-
pounds (Graf 1999). is slow action makes BPUs very good candidates for
Fig. 1. BPUs: A) Diubenzuron, B) Hexaumuron, C) Lufenuron, and D) Triumuron.
5
Vahabzadeh, R.D. et al.— R.Flavipes mortality to CSIs
use in baits. Currently in the United States, hexaumuron, novaumuron and
diubenzuron are incorporated into commercially available baiting systems,
while triumuron is still being developed for use against termites. Lufenuron
is approved for use, but ecacy testing for termite control is still underway.
Of the four benzoylphenyl ureas tested in this project (Fig 1), the rst to
be introduced was diubenzuron [1-(4-cholorophenyl)-3-(2,6-diubenzoyl)
urea)]. Diubenzuron was rst reported in the literature by J.J. van Daalen
in 1972, and is now produced by Solvay Duphar B.V. (Tomlin 2000). It is
currently the active ingredient in Exterra™ Termite Interception and Baiting
System marketed by Ensystex Inc., and Advance Termite Bait System TM
by Whitmire Micro-Gen. Doppelreiter and Korioth (1981) reported that
diubenzuron caused mortality in R. avipes at between 10 and 1000 ppm
with the concentration dierence being insignicant. Ahmad et al. (1986)
showed that diubenzuron not only caused mortality in termites, but also
reduced fecundity of female termites, and eected viability of eggs. Su and
Scheran (1993) reported that R. avipes showed high mortality (80 %)
when exposed to diubenzuron in treated diet. While Ahmad et al. (1986)
showed that termites would accept the diet at up to 1000 ppm diubenzuron,
Su and Scheran (1993) stated that termites were deterred from feeding on
diubenzuron when concentrations were above 31.3 ppm.
Triumuron [1-(2-cholorobenzoyl)-3-(4-triuoromethoxyphenyl) urea]
was rst reported in the literature by G. Zoebelein et al. in 1979 and is produced
by Bayer Environmental Science® (Tomlin 2000). Triumuron has been used
on a variety of dierent pests and has both larvicidal and ovicidal activity. It
has shown eects on stored product beetles (Blumberg et al. 1985; Elek and
Longsta 1994), rice weevils (Smith and Grigarick 1989), ies (Broce and
Gonzaga 1987; Knapp and Cilek 1988), spiny bollworm (Meisner 1987),
cockroaches (Demark and Bennett 1989), scale insects (Eisa et al. 1991),
and locusts (Wilps and Diop 1997). It is currently registered for use in crop
protection, public health and animal health usage. At the present time, it is
reportedly registered for termite control in Australia.
Hexaumuron (1[3,5-dichloro-4-(1,1,2,2-tetrauoroethoxy) phenyl]-3-
(2,6-diurobenzoyl) urea) was rst reported in the literature by R.J. Sbragia
et al. in 1983 and introduced by Dow Elanco (now DowAgroSciences) in
1987 (Tomlin 2000). It is currently the active ingredient in Sentricon® Bait-
Reference not in bibliography
6 Sociobiology Vol. 50, No. 3, 2007
ing Systems. Hexaumuron has been shown to have eects on subterranean
termites both in the laboratory and in the eld (Pawson and Gold 1996;
Haagsma and Bean 1998; Peters and Fitzgerald 1999; Prabhakaran 2001;
Su 1994; Su et al. 1997, 2001). Hexaumuron has also been shown to have
potential to control fungus growing ants (Peppuy et al.1998). Hexaumuron
has been reported to be a superior to lufenuron and diubenzuron by Su and
Scheran (1993, 1996a) for use in termite baiting systems.
Lufenuron [(RS)-1-[2,5-dichloro-4-(1,1,2,3,3,3-hexauroropropoxy)
phenyl]-3-(2,6-diurorobenzoyl) urea] was rst reported in 1989 and intro-
duced by Ciba-Geigy (now Syngenta Crop Protection, Inc.) in 1990 (Tomlin
2000). Lufenuron has been shown to greatly reduced egg hatch in cat eas
by eecting the composition of the chorion of the egg (Meola et al. 1999).
Lufenuron is also used to control Lepidoptera and Coleoptera larvae on cot-
ton, maize, and vegetables, as well as citrus whiteies and rust mites on citrus
fruit (Tomlin 2000). It has been registered as Zyrox® for termite control.
MATERIALS AND METHODS
Termite Collection
All Reticulitermes avipes used for these experiments were collected
from colonies in College Station, Texas. ey were collected using traps of
moistened corrugated cardboard housed in polyvinylchloride (PVC) pipes
that were12.5 cm tall with a 10 cm diameter. Aer being sorted in the labo-
ratory, the termites were maintained in Falcon 150 x 25mm sterile plastic
petri dishes and supplied with Fisher brand tongue depressors for food and
shelter. Termites used in the experiments were held in the laboratory for less
than one month.
Bait Preparation
e chemical solutions containing the benzoylphenyl ureas were all pre-
pared with high performance liquid chromatograph grade acetone from EM
Science. A solution of each of the four BPUs at 1000 ppm were prepared,
and then serial (1:10) dilutions were made to yield 100, 10, 1, and 0.1 ppm
solutions, respectively. Hexaumuron, diubenzuron and triumuron were
all obtained from Chem Services (West Chester, PA) and were 99% pure.
Lufenuron was obtained from Sigma Chemical (St. Louis, MO) and was
7
Vahabzadeh, R.D. et al.— R.Flavipes mortality to CSIs
99.7% pure.
Termite Feeding Substrates.
A 4 x 6 cm piece of one-ply BayWest 1002 paper was soaked in the treated
solution in a 100 x 20mm Kimax® dish. Non-treated controls were prepared
with the same paper stock which was either soaked in pure acetone, to test
for acetone eects (acetone controls), or put into the dish without any treat-
ment (untreated controls). e treated papers were then held horizontally
and sequentially rotated until dry to minimize a dierential concentration
gradient of the chemical from one end of the paper. e paper was then placed
in the lid portion of a Fisher brand 100 x 15mm sterile plastic petri dish and
placed in a ‘humidity dish’. Humidity dishes were constructed to keep the
environment at 100% RH to optimize feeding by the termites. e humidity
chambers were made of a Falcon 150 x 25mm sterile plastic petri dishes in which
approximately 40 g of sand was spread evenly on the bottom and moistened
thoroughly. e dishes containing the paper were then put on the sand and
the lid of the larger dish was put in place. is procedure was repeated three
times for each concentration of the four chemicals in evaluation.
Termite Feeding Trials.
To initiate a feeding trial, 300 worker termites were aspirated and placed
in a 100 x 15 mm sterile plastic petri dish and held in the humidity dish.
A dish of 300 termites was prepared for each of the concentrations of the
BPUs to be tested. Both of the dishes containing the paper and the termites
were allowed to sit for 24 h prior to testing. is allowed the treated paper
to moisten in the humid environment without direct application of water,
making it more acceptable to feeding termites, and to prevent dierential
concentration gradients of the chemical to the edges of the paper. During this
period, the termites were also starved. Aer 24 h, the termites were split into
groups of 100 and placed into the dishes with the treated papers or controls.
Each concentration-chemical group had termites from the same colony. e
termites were allowed to feed on the paper for 5 d, aer which time they were
removed and placed into clean petri dishes for evaluation of survivorship.
e treated paper was le in the dish, and the bottom portion of the dish
was placed on it to keep the paper in place. e area of the papers remaining
were then determined. Area loss measurements were done by analyzing digital
8 Sociobiology Vol. 50, No. 3, 2007
images taken of each paper before and aer testing, similar to the procedures
of Su and Messenger (2000), Vahabzadeh (2002) and Heintschel et al. (2007)
Photographs were taken with a digital camera (Nikon Coolpix® 4300, Tokyo,
Japan). All images were incorporated into Adobe Photoshop (Adobe Systems
Inc. 2001) where they were converted to a black-and-white color scheme to
increase measurement accuracy. is required translating the images’ color
to grayscale and setting the contrast to a maximum level. An electronic paint
tool was used to correct small blemishes that remained inside the perimeter
of the paper aer the color conversion with Adobe Photoshop soware
(Adobe Systems, San Jose, California). e amended images were analyzed
using SigmaScan® Pro 5 (SPSS Inc. 1999) to determine the area remaining
of each paper. is area remaining following feeding was then subtracted
from the original known area of the paper to estimate the amount of paper
consumed by the termites.
Survivorship Experiments.
Aer being removed from the treatment dishes, 100 termites were placed
in a 100 x 15 mm petri dish with a smaller version of the tongue depressor
structure used to house freshly collected termites in our laboratory. Su and
Scheran (1993) reported the “symptoms of ecdysis inhibition” as cannibal-
ization of appendages and antennae by nest mates, as well as the “jackknifed”
position. In this study, both the number of surviving termites, and the number
that showed the jackknifed pose were recorded as evidence of chitin synthesis
inhibition. e numbers of surviving termites were recorded on a weekly
basis for six wks beginning at 1 wk aer placement on non-treated food (12
d post-exposure). Experimental units were maintained in an Elliot-Williams
Environmental chamber held at 24 ± 2°C and 24h D:D. A Hobo Pro Series
monitor was placed in the chamber to record temperature and humidity.
Choice Tests.
Choice tests were carried out in Falcon 150 x 25 mm sterile plastic petri
dishes. e cellulose sources used were discs (7 mm dia.) of Fisherbrand
Qualitative P5 Filter paper cut with a standard hole-punch out. Past projects
done in our laboratory showed that R. avipes would feed on this paper. e
discs were soaked in either 0.1, 1, 10, 100, or 1000 ppm solutions of diuben-
zuron, hexaumuron, lufenuron or triumeron, respectively. e control
9
Vahabzadeh, R.D. et al.— R.Flavipes mortality to CSIs
discs were not treated, but were handled just as the treated discs. For each
test, two discs, each treated with a dierent BPU of the same concentration,
or a non-treated control were place at equal distance from the center of the
dish. e termites were given only two choices based on preliminary experi-
ments that found that termites seemed to be ‘overwhelmed’ when presented
more than two choices, and hovering in the center of the dish, not visiting
any of the choices. e clear dishes were labeled on the bottom so that the
circles could be identied through the translucent dish without marking on
the actual paper disc. e discs were moistened with 25µl of water and 50
R. avipes workers were aspirated and placed in the center of the dish. Aer
giving the termites at least one hour to ‘acclimate’, the number of termites
at each disc were counted every hour for 6 h on the rst day (24 h). On the
second day, the termites were counted once in the morning and once in
the late aernoon. e termites were counted once in the aernoon of the
third day. Aer the initial day, the paper circles were moistened twice a day.
Termites on the edge of the disc were counted as feeding on the paper. Every
possible pair-wise combination of the four CSIs and the non-treated control
were tested. Between observations, the dishes were kept in large sealed plastic
containers with moist sand in the bottom so as to maintain 100% RH.
Voucher Information.
Vouchers of the termites used in these studies were placed in the Depart-
ment of Entomology, Texas A&M University Insect Collection, in the Minnie
Belle Heep Building, College Station, TX.
RESULTS
Subterranean Termite Feeding.
Tests for signicant dierences and interaction eects were conducted
applying an analysis of variance (ANOVA) (SPSS 2001). Signicant dier-
ences among survivors were detected for day (F = 129.44, df =5, p < 0.001),
Treatment (F = 48.907, df =4, p < 0.001), Concentration (F = 31.815, df
=4, p < 0.001), Treatment x Concentration (F = 20.565, df =12, p < 0.001),
and Day x Treatment (F = 3.014, df =25, p < 0.001). Post Hoc tests for means
comparisons were performed applying Tukey’s highly signicant dierence
(HSD) at the α = 0.05 level. Reticulitermes avipes fed on all of the treated
10 Sociobiology Vol. 50, No. 3, 2007
and control papers, and the amount of feeding varied depending on chemical
and concentration used in the treatments. Termites consumed signicantly
(p< 0.001) more of the paper treated with diubenzuron at concentrations
ranging from 0.1-100 ppm (39.92-52.38 % of the paper consumed) than at
1000 ppm (29.58%) (Table 1). e lower concentrations (0.1-100 ppm) were
also favored over either control (15.99 and 14.52% for acetone and untreated
paper control, respectively, versus 10.55 to 14.42% of the mean area remain-
ing), implicating a non deterrence for the chemical treatments.
e consumption of triumuron-treated paper showed a similar trend to
diubenzuron. Of the concentrations tested, the termites consumed more
of the paper treated with 10 and 100 ppm solutions (53.92 and 55.00%,
respectively), but signicantly less (p<0.001) in controls (33.38 acetone and
39.50% paper control, respectively). ere is a direct relationship between
the mean area remaining (cm2) and the percent of paper consumed with
increased consumption and increased dosage up to 100 ppm. e percent
paper consumed ranged from 44.54 to 55.00%. e mean area remaining
ranged from 10.80 to14.52 cm2, whereas the highest dosage of 1000 ppm
was only 41.12% paper consumed and 14.13 cm2 area remaining. e results
from the hexaumuron trials are summarized in Table 1. ere was a sig-
nicant (p<0.001) dierence in the amount of treated paper consumed at
concentrations of 1-1000 ppm as compared to the two control and the 0.1
ppm treatments. e most preferred concentration was 1 ppm where 60.25
% of the test papers were consumed within 5 d.
Lufenuron at concentrations of 0.1-1000 were signicantly (p<0.001) dif-
ferent, in terms of consumption of treated papers by R. avipes as compared
to either control (Table 1). Of the concentrations evaluated, 0.1 and 1.0 ppm
were favored over the other concentrations, results support the attractiveness
of lufenuron to foraging termites.
Survivorship - Mean Survivorship.
All of the test populations of R. avipes showed mortality through the six
weeks of observations. e mean survivorship at the end of the six week period
was compared between the groups over time and was evaluated by ANOVA
(SPSS, 2001). Termites were counted each week for six weeks in order to
calculate the slope of the percentage of survivors for each active ingredient
11
Vahabzadeh, R.D. et al.— R.Flavipes mortality to CSIs
Table 1. Mean percent of test papers (24 cm2) treated with diubenzuron, triumuron, hexaumuron and lufenuron consumed by Reticulitermes avipes
at the concentrations indicated using digital analysis of the mean areas remaining following feeding for 5 days.
Concentration (ppm) Diubenzuron Triubenzuron Hexaumuron Lufenuron
Mean Area1 % of paper Mean Area1 % of paper Mean Area1 % of paper Mean Area1 % of paper
Remaining (cm2) consumed Remaining (cm2) consumed Remaining (cm2) consumed Remaining (cm2) consumed
Acetone control 15.99+ 0.68 a 33.38 15.99+0.68 a 33.38 15.99+0.68 a 33.38 15.99+0.68 a 33.38
paper control 14.52+1.19 ab 39.50 14.52+1.19 ab 39.50 14.52+1.19 ab 39.50 14.52+1.19 ab 39.50
0.1 11.43+2.80 c 52.38 13.31+0.40 bc 44.54 15.72+0.97 ab 34.50 5.74+0.75 c 76.08
1 10.55+2.36 c 56.04 12.56+0.50 bc 47.67 9.54+0.92 c 60.25 5.99+0.94 c 75.04
10 12.29+1.11 bcd 48.79 11.06+0.72 cde 53.92 12.78+2.22 b 46.75 9.65+1.48 d 59.79
100 14.42+2.26 abd 39.92 10.80+0.77 de 55.00 10.19+1.74 c 57.54 9.81+0.39 d 59.13
1000 16.90+0.13 e 29.58 14.13+0.61 abc 41.12 12.02+2.99 b 49.92 11.91+0.88 e 50.38
1Means within columns followed by the same letter were not signicantly dierent from each other applying Tukey’s HSD at the α = 0.05 level (SPSS, 2001).
12 Sociobiology Vol. 50, No. 3, 2007
and concentration. is was performed by calculating the slope of the best t
line of the means of survivors using linear regression and comparing means
by ANOVA (SPSS 2001).
Diubenzuron - e slopes of the percentage of survivors for the termites
fed on diubenzuron-treated paper were variable. e termites fed on paper
treated with 10 ppm diubenzuron solution died signicantly (p<0.001)
slower than the termites fed on the other treated papers (Figure 2).
Triumuron - All but one concentration had a signicantly dierent slope
than the acetone control (Table 2); however none were signicantly dierent
from the untreated control group (Figure 2).
Hexaumuron - ere was no signicant dierence between the treated
groups and those fed on untreated paper (Figure 2). ere was a signicant
dierence (p<0.001) among two of the groups and the acetone control. Of
the treated groups, the termites fed on paper treated with 0.1 ppm solution
Fig. 2. Survival of R. avipes to controls (acetone and paper) and four BPUs: Diubenzeron,
Hexaumuron, Lufenuron, and Triumuron at A) 12 DAT, B) 17 DAT, C) 24 DAT, D) 31 DAT,
E) 38 DAT, and F) 45 DAT. e x-axis denotes BPU concentrations ranging from 0.1 to 1000
ppm, y-axis denotes active ingredient and/or control, and z-axis denotes percent survival (n=100),
respectively.
13
Vahabzadeh, R.D. et al.— R.Flavipes mortality to CSIs
died the slowest.
Lufenuron - All of the termites fed on
paper treated with lufenuron died sig-
nicantly (p<0.001) faster than termites
fed on either controls. ese results are
summarized in Figure 2.
DISCUSSION
e rst objective of this study was to
determine the concentration of each of
the four BPUs that was the most accept-
able to Reticulitermes avipes. Although
a specic ‘threshold’ concentration was
not observed, it is apparent that R. avipes
will adjust to the amount of feeding on
a treated food source depending on the
concentration of the treatments. ere
were signicant dierences in amount of
feeding not only among the four BPUs,
but also among dierent concentrations
of the same BPU. Lufenuron was highly
acceptable to R. avipes at four of the ve
concentrations tested. is BPU treated
disc was the most consumed by R. avi-
pes in this portion of the experiment. Su
and Scheran (1996a) report lufenuron
to be less acceptable to R. avipes than
hexaumuron. In their study, lufenuron
was found deterrent at 0.4% of the con-
centration at which hexaumuron was
found deterrent. In the present study,
hexaumuron at 1 and 100 ppm had
similar acceptability to lufenuron, while
the other four concentrations tested were
generally less acceptable (to R. avipes).
Table 2. Mean slopes of the percentage of survivors over a six week period challenged to various active ingredients.
Chitin Synthesis Inhibitor
Concentration Diubenzuron Triubenzuron Hexaumuron lufenuron
(ppm) Slope/intercept R2 Slope/intercept R2 Slope/intercept R2 Slope/intercept R2
Acetone control y = -1.2893x + 107.94a 0.9407 y = -1.2893x + 107.94a 0.9407 y = -1.2893x + 107.94a 0.9407 y = -1.2893x + 107.94a 0.9407
paper control y = -1.6974x + 109.52ab 0.9356 y = -1.6974x + 109.52ab 0.9356 y = -1.6974x + 109.52ab 0.9356 y = -1.6974x + 109.52ab 0.9356
0.1 y = -2.2143x + 104.5c 0.9433 y = -1.5854x + 70.349bc 0.9479 y = -1.8493x + 102.60bc 0.9502 y = -2.5255x + 121.02c 0.9909
1 y = -1.7175x + 98.193bc 0.9571 y = -1.2253x + 73.771abcd 0.8960 y = -2.4513x + 116.01cd 0.9725 y = -2.5770x + 120.06cd 0.9856
10 y = -0.9147x + 100.07ad 0.9503 y = -1.3666x + 68.593bcde 0.8886 y = -2.5664x + 110.82cde 0.9345 y = -2.2408x + 106.92cde 0.9659
100 y = -1.4943x + 97.481abd 0.9743 y = -1.6974x + 109.52abdf 0.9356 y = -2.2786x + 102.42df 0.9342 y = -2.0650x + 82.586cdef 0.9157
1000 y = -1.4540x + 86.302abc 0.7226 y = -1.7415x + 76.222bcde 0.9306 y = -2.4912x + 100.56cde 0.8957 y = -0.0133x + 0.4826ab 0.3804
1Means within columns followed by the same letter were not signicantly dierent from each other applying Tukey’s HSD at the α = 0.05 level (SPSS, 2001).
14 Sociobiology Vol. 50, No. 3, 2007
Diubenzuron at 0.1 and 1 ppm and triumuron at 10 and 100 ppm also
had similar acceptability to those of hexaumuron at 100 ppm for R. avi-
pes. ese dierences may be attributed to subtle dierences among colony
preference for either a cellulose food source or the active ingredients applied
to them in the present study or in the study by Su and Scherahn (1996a).
Acceptance of diubenzuron and hexaumuron bait products from eld
studies have been comparable for both rhinotermitid groups in Texas (JWA,
personal observation).
Feeding: Amount of Paper Consumed
e amount of treated material that R. avipes will consume is an indication
of how acceptable that treated material is to the test termite population. e
results of this test indicate that R. avipes will feed on BPU-treated material
depending on the CSI and the concentration at which it was treated.
Survivorship: Mean percentage of survivors
e goal of any termite baiting treatment is to ultimately reduce the colony
to a point where it is not causing signicant damage to a structure or to elimi-
nate it completely. Observing the mean percentage of survivors of R. avipes
45 d aer being exposed to four CSIs at ve dierent concentrations allowed
us to conclude that these chemicals have an adverse eect on termite survival.
ese results were concentration dependent and quite variable (Fig. 2).
e optimal CSI concentration incorporated into a bait would kill slowly
enough for the foragers to transfer the treated material to its colony mates.
us it is not only important to look at overall mean percentage of survivors,
but also the rate at which the termites died. A chemical that kills too quickly
would not be eective as a termite bait tool; however, in these tests even low
concentrations produced eects in one to two weeks. Although this should
be sucient time for termites to move the CSI into the colony, the rate of
transfer can depend largely on the size, age, and nesting structure of a colony.
While a slow-acting chemical is optimal, it must cause mortality within the
population within a reasonable period of time in order to prevent extensive
damage to the structure.
e second object was to determine if feeding on diet treated with these
four BPUs would have an eect on R. avipes. Termites exposed to diets
treated with all four BPUs exhibited characteristic jackknifed postures as-
15
Vahabzadeh, R.D. et al.— R.Flavipes mortality to CSIs
sociated with death from chitin synthesis inhibition. Many also showed
dierent survivorship and rates of mortality from untreated control groups.
Once again, there was variation among the four BPUs, and within dier-
ent concentrations of the same BPUs; however lufenuron caused the most
mortality in the test period under the constraints of this experiment. Four
of the ve lufenuron concentrations tested caused at least 90% mortality in
approximately 7 weeks of this experiment (Fig. 2). Similarly, hexaumuron
elicited at least 90% mortality with three of its concentrations, followed by
triumuron with two of the concentrations tested. ese results dier from Su
and Scheran’s 1996 ndings that non-deterrent concentrations of lufenuron
caused less than 80% mortality even aer 9 weeks. e reason for these dif-
ferences remains unknown. One can only speculate that subtle dierences
among various natural populations of termites collected from the eld would
likely inuence their respective susceptibilities to these BPUs.
Eects of Benzoylphenyl Ureas: Jackkning
Although a specic mode of action for chitin synthesis inhibitors in un-
known, their eects can be observed. Termites fed on all four of the BPUs
used in this experiment showed the jackknifed posture, which indicated that
death would occur due to BPU exposure. e frequency of jackkning, like
the other observations in these experiments, was dependent on the chemical
and concentration.
e third objective of this study was to determine if R. avipes would
exhibit a preference for dierent treatments of BPUs or untreated controls.
ere were some preferences evident. e majority of the choice tests showed
no preference between the four BPUs represented. When compared to con-
trols, diubenzuron was the only BPU chosen more oen than an untreated
control, and that was in only one concentration tested. is would indicate
that in a setting in which BPUs are incorporated into termite baits and placed
around a structure, there is an equal chance that R. avipes would visit an
untreated food source as there is a chance that it would visit the bait. Even
though colonies of R. avipes can be highly localized in conned urban settings
where the frequency of interaction between adjacent foraging populations
would be expected high, the directed foraging of termites to bait stations
can be relatively low (Vargo 2003). Many variables, such as seasonal weather
16 Sociobiology Vol. 50, No. 3, 2007
patterns, predation, competition between nearby colonies, size or age of a
colony, and the number of alternative food sources available can aect the
viability of a termite colony and confound the interpretation of the action
of the bait (Forschler and Ryder 1996a, 1996b).
Choice Tests
Both choice and no-choice tests were conducted with R. avipes to treated
paper. When the treated materials were presented to groups of termites, the
termites oen showed no preference, when observing the number of termites
visiting discs at set intervals. But also observed were the number of discs that
were completely consumed at the end of the experiment. In only seven of the
30 choice tests between treated discs did R. avipes show a preference for
one treatment over another.
Around a structure R. avipes will probably not be given a choice between
two dierent commercial baits. ey will however be presented with the choice
of feeding on a treated bait and untreated materials, namely the structure
that is supposedly being protected by the bait. In the choice tests in which
the termites had a choice between a treated disc and an untreated control
R. avipes showed a preference in eight of 20, respectively. A breakdown of
their feeding preferences follows:
Diubenzuron
Reticulitermes avipes consumed more of the paper treated with lower
concentrations (0.1 - 10 ppm), with the 1 ppm solution being the most
acceptable. At the higher concentrations, 100 and 1000 ppm, feeding was
inhibited. It is apparent that there might be slight attractiveness at concentra-
tions between 1 and 10 ppm. ere was a signicant dierence in percentage
of survivors depending on concentration. is is contrary to the ndings of
Dopplereiter and Korith (1981) who observed no signicant concentration
related dierences in production of mortality in R. avipes.
R. avipes fed on diubenzuron-treated paper had some of the highest
percentages of survivors in the portion of the experiment. Four of the ve
concentrations had similar survivorship percentages as the untreated controls.
Termite feeding on 10 ppm treated discs with diubenzuron had the highest
mean percentage of survivors in the entire experiment (~ 61%), even outnum-
bering the survivors in the controls, 44 and 26 % for acetone and untreated
17
Vahabzadeh, R.D. et al.— R.Flavipes mortality to CSIs
paper controls, respectively. R. avipes fed on diubenzuron-treated paper had
some of the slowest mortality, similar to the untreated controls; however, the
eects of diubenzuron may take longer to observe than 6 weeks as suggested
by Dopplereiter and Korioth (1981). ey observed 100% aer 14 weeks of
observation. Although jackknifed termites were observed, diubenzuron had
fewer jackknifed termites when compared to lufenuron and triumuron at
the same concentrations and time. e majority of this jackkning occurred
at the higher concentrations; however, feeding decreased above 10 ppm. is
suggests a threshold of preference which is concentration-dependent.
Diubenzuron was preferred over triumuron at 10 ppm while the opposite
was true at 100 ppm. Interestingly enough, in the 10 ppm choice test, more
triumuron discs were consumed and the opposite was true in the 100 ppm
choice test. Although there was no signicant dierence in the number of
termites visiting the discs treated with 1000 ppm dilutions, there were two
discs of diubenzuron completely consumed while no visible consumption
of triumuron discs were observed. is would imply that R avipes, given
a choice, prefers diubenzuron to triumuron at 10, 100 and 1000 ppm.
ere was no dierence in preference for diubenzuron when compared to
lufenuron; with about the same number of discs completely consumed of
each (Figure 2).
When the termites had a choice between hexaumuron and diubenzuron,
they showed a preference in two of the tests. At 1 ppm, the termites visited the
hexaumuron discs more oen, which was supported by the fact that two of
the hexaumuron discs were completely consumed while only one diuben-
zuron disc was completely consumed. At 10 ppm the diubenzuron-treated
discs were visited more oen and both chemicals had one disc completely
gone. Although at 100 ppm, the number of termites visiting discs of each
BPU were exactly the same, at two hexaumuron discs.
Diubenzuron-treated discs were visited more oen than the control at
both 1 and 10 ppm. When the disc was treated with 1000 ppm, the termites
visited the control disc more oen. is was the only test in which the number
of discs consumed were noticeably dierent, with seven diubenzuron discs
completely consumed as compared to four of the controls were completely
consumed.
Diubenzuron had a moderately positive correlation between concentra-
18 Sociobiology Vol. 50, No. 3, 2007
tion and amount of feeding (R2 = 0.764). is implies a general trend for
R.avipes to be less attracted to treated discs as concentration or diuben-
zuron increased. is could be a disadvantage to this CSI when attempting
to formulate an active concentration range that would be amenable to most
target termite species.
Triumuron
When fed to R. avipes, triumuron treated disc preference were dierent
to diubenzuron treatments. Ten and 100 ppm solutions of triumuron were
the most acceptable to R. avipes, while the other three concentrations of
triumuron were less attractive. Termites fed on triumuron-treated paper
exhibited variability in mean percentage of survivors (ranging from 0.50 –
37.33%). Termites fed on paper treated with 0.1 and 1000 ppm solutions
of triumuron had very low mean percentage of survivors (5.0 and 0.50%,
respectively), while termites fed on 100 ppm solution had a high percentage
of survivors (37.33%). It is unclear if these results simply demonstrate the
lack of preference to this active ingredient-concentration in terms of feeding
or possible aversion, which subsequently resulted with the higher percentage
of survivors.
In the triumuron trials, most of the concentrations showed a slope for
mortality that was signicantly dierent from controls (Table 2), indicating
some level of eectiveness. Triumuron at 0.1 ppm showed mortality, but
the mean percentage of survivors at the beginning of the experiment was ~
40% while the three remaining concentrations had initial survivorship ~
60%. A higher initial survivorship could allow more foragers to return to
the colony and potentially transfer the treated material to other termites.
Conversely, a higher survivorship may reect greater aversion to the various
treatment combinations. Reticulitermes avipes that were fed on paper treated
with triumuron exhibited the most jackkning compared to the other three
BPUs in this experiment. e majority of this jackkning was observed in
termites feeding on paper treated with 1 and 10 ppm solutions. is implies
that this chemical may be an eective bait active ingredient at low to moder-
ate concentrations. R. avipes showed a preference for hexaumuron paper
discs treated at1000 ppm when given a choice between hexaumuron and
triumuron. It was observed that overall eight hexaumuron discs were
19
Vahabzadeh, R.D. et al.— R.Flavipes mortality to CSIs
consumed while only one triumuron disc was completely consumed for the
same concentration (1000 ppm).
Only one choice test between triumuron and lufenuron showed a dif-
ference in the number of termites visiting discs. At 100 ppm, the termites
visited the lufenuron-treated disc more oen. Seven discs of triumuron
were completely consumed at the end of the experiment while only three of
lufenuron were completely consumed. ree tests were signicantly dierent
(p < 0.0001) in the choice between triumuron and the untreated control:
Triumuron was preferred at 1 and 100 ppm while the control was more read-
ily frequented at 10 ppm. Although inconclusive, these results suggest that
triumuron at 1 and 100 ppm could be good candidates to further evaluate
for use in termite baiting situations around structures. Other than the strong
positive correlations between mean percentage of survivors and the slope
(R2=0.979), triumuron showed no specic trends among the measured
factors in this experiment.
Hexaumuron
e results of the hexaumuron trials were variable and did not show
a denite pattern with relation to the amount of feeding. e most ac-
ceptable concentrations of hexaumuron were at 1 and 100 ppm. Overall,
hexaumuron caused mortality that was signicantly dierent (p < 0.0001)
than the untreated control groups at 10, 100 and 1000 ppm. Termites fed
on hexaumuron-treated paper had high initial percentages of survivors (~
80%), and all but one concentration (0.1 ppm) showed a slope signicantly
more negative than that of the controls (Table 2). Similar to our ndings,
Sheets et al. (2000) demonstrated that the rate of uptake, level of maximum
uptake, and amount of insect-to-insect transfer were concentration depen-
dent for hexaumuron, and that even aer 40 d exposure it was not further
metabolized, thus demonstrating the ability to spread throughout a termite
colony in an ecacious manner.
R. avipes challenged with hexaumuron treated paper were observed
to exhibit jackkning trends similar to diubenzuron; however, there was
less jackkning than in the termites fed on triumuron or lufenuron at the
same concentrations over the same period of time (Fig. 2). e majority of
the jackkning observed in hexaumuron baited termites were observed
20 Sociobiology Vol. 50, No. 3, 2007
among the higher concentrations. ere was only one choice test in which
the termites showed a preference between hexaumuron and lufenuron. At
1000 ppm, more termites were observed at the hexaumuron-treated discs.
is suggests that even at high concentrations of hexaumuron, termites
will continue to feed and consume treated cellulose materials, one possible
explanation as to why it was selected as the BPU of choice among the earli-
est bait systems on the market. Further evaluation of this BPU with other
active ingredients resulted with an equal number of discs being consumed.
In only one test between hexaumuron and the untreated control did the
termites exhibit any preference. At 10 ppm, the control was preferred to the
hexaumuron-treated disc. As with triumuron, the only strong correlation
(R2=0.962) in hexaumuron was between the mean percent of survivors and
its slope (Table 2).
Lufenuron
Lufenuron was the most palatable of the chemicals evaluated. Four of
the six most highly consumed disc areas remaining were lufenuron treated
papers. Results suggested by the quantity of paper consumed by R. avipes
in this portion of the experiment imply that lufenuron was a highly accept-
able BPU at most concentrations tested. Termites that fed on paper treated
with 1000 ppm dilutions of lufenuron had no survivors within the rst two
weeks of the six week observation period, while most of the other CSIs and
controls had surviving termites well into the six week observation period. It is
unclear if rapid death was due to direct toxicity or if chitin inhibition played
a more signicant role, particularly in instances where internal gut morphol-
ogy may have been aected. e other three concentrations of lufenuron
had similar mean percentages of survivors; these being fairly low relative to
other CSIs. e slopes of survivors for termites that fed on lufenuron-treated
paper exhibited some variability. Termites fed on 0.1, 1 and 10 ppm dilutions
of lufenuron had initial survivorship ~ 90%, and had consistently negative
slopes for survivorship (Table 2), indicating that most termites would likely
die between 55 and 60 days, just a few days aer the hexaumuron treated
termites. Termites that were fed on lufenuron treated discs at 100 ppm had
a lower initial survivorship (~ 60%), and were all dead aer four weeks of
observations. As stated before, most termites exposed to lufenuron at 1000
21
Vahabzadeh, R.D. et al.— R.Flavipes mortality to CSIs
ppm were dead upon the initial observation period. R. avipes that fed on
paper treated with lufenuron exhibited jackkning postures, although not as
frequently as with triumuron. Like triumuron, their jackkning postures
were observed in termites which fed more readily at lower concentrations,
which ate more, and died more slowly than the two highest concentrations
applied. Some death without observable jackning postures may be due to
internal damage elicited by BPUs.
Chitin synthesis inhibitors have been demonstrated to aect the produc-
tion of the peritrophic membrane of locust Locusta migratoria (L.) (Clarke
et al. 1977), blow y Calliphora erythrocephala Meigen (Becker 1978), and
both the pupal integument of yellow mealworm, Tenebrio molitor L. (Soltani
1987) and its developing peritrophic membrane (Soltani 1984). It may also
be that R. avipes possess a less sensitive target site for lufenuron’s mode of
action (Bogwitz et al. 2005), resulting in more rapid toxicity and death. It
is well established that dierent organisms possess variable proportions of
muscarinergic receptors, which invariably inuence insects dierently when
challenged to dierent insecticides (Liu & Casida 1993) and likely with
most BPUs. Even when overt jackning is not observed, internal damage to
various sights is occurring. Morales-Ramos et al. (2006) support this notion
and have demonstrated that BPUs consumed by termites damage peritrophic
matrices, sometimes preventing their full development.
In only one test between lufenuron and the untreated controls did ter-
mites demonstrate a preference. At 100 ppm, the control was preferred to
lufenuron-treated discs, indicating that lufenuron may not elicit attractant
properties at this concentration. Lufenuron expressed a strong correlation
between concentration and slope of the mean % of survivors (R2 =0.899).
As treatment concentrations increased, their slopes increased (or became less
negative). Lufenuron also exhibited a strong negative correlation between
mean area remaining and mean % of survivors (R2 =0.713). A strong linear
relationship between the amount of treated material consumed and the num-
ber of termites that died was observed, and lufenuron was the only BPU that
showed the relationship between the amount of treated material consumed
and mortality so clearly (see Figure 2). Previously, lack of mortality has been
attributed to the deterrence of feeding at higher concentrations for other
chemicals. Interestingly, lufenuron was the only BPU that did not show a
22 Sociobiology Vol. 50, No. 3, 2007
strong correlation (R2 =0.195) between the mean percent of survivors and
the slope. is was due to the rapid mortality observed at higher concentra-
tions (e.g., the slope at 1000 ppm) (Table 2). One concern from these results
might be that lufenuron may have a more direct dose-response relationship,
whereby a greater number of termites may die before they are capable of dis-
seminating the active ingredient throughout the colony (or before deleterious
chitin inhibition occurs); a broader number of concentrations should be
used to determine where the threshold is and subsequent eld evaluations
should be considered.
When evaluating the impact of CSIs on the survival and egg viability of
another rhinotermitid termite, Coptotermes formosanus, Rojas & Morales-
Ramos (2004) observed no statistical dierences in egg viability as all CSIs
prevented larva from hatching, and with rst instars failing to eclose; no
dierences were observed in the mortality of queens and kings exposed to
diubenzuron and hexaumuron treatments and controls. Only lufenuron
treatments showed signicantly increased mortality rates within a month of
exposure to the active ingredient. Furthermore, Rojas and Morales-Ramos
(2004) also observed that the estimated number of eggs oviposited during the
rst 100 d was signicantly lower in the lufenuron treatment group compared
to hexaumuron, diubenzuron, and controls. ey suggest that lufenuron
appeared to be the most potent of the CSIs tested against primary queens
and kings of C. formosanus and that hexaumuron was the least potent,
showing no dierence in adult mortality between treatments and controls
aer 6 mo of exposure.
Based on this preliminary investigation, lufenuron, particularly at low
concentrations, has great promise for termite control if incorporated into
a termite bait matrix. In general, most of the benzoylphenyl ureas exhibit a
lot of variability in their palatability and acceptance by R. avipes, but show
potential for use in remedial termite baiting systems at some concentrations.
Diubenzuron, although acceptable to feeding by these termites, lagged behind
the other three BPUs in the level of mortality exacted to R. avipes under these
experimental constraints. With the demonstrated success of several CSIs for
remedial termite control, results of this study suggest that lufenuron should
be given careful future consideration for potential evaluation as another active
23
Vahabzadeh, R.D. et al.— R.Flavipes mortality to CSIs
ingredient which may reliably control unwanted termite populations.
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