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Response of the Formosan Subterranean Termites (Isoptera: Rhinotermitidae) to Baits or Nonrepellent Termiticides in Extended Foraging Arenas

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Distance effects of three treatments, noviflumuron, fipronil, and thiamethoxam, against laboratory populations of the Formosan subterranean termite, Coptotermesformosanus Shiraki, were tested in extended foraging arenas with foraging distances of 50 m. The results showed that during the 10-wk test period, all termites were killed by noviflumuron baits, whereas the nonrepellent termiticides fipronil and thiamethoxam divided the laboratory populations into two groups after causing 25-35% worker mortality. The horizontal transfer of lethal effects of fipronil was < or = 5 m. For thiamethoxam, the distance of transfer was substantially shorter. Because of their dose-dependent lethal time, the nonrepellent termiticides did not fulfill the requirements of a liquid bait model.
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HOUSEHOLD AND STRUCTURAL INSECTS
Response of the Formosan Subterranean Termites
(Isoptera: Rhinotermitidae) to Baits or Nonrepellent Termiticides
in Extended Foraging Arenas
NAN-YAO SU
Department of Entomology and Nematology, Ft. Lauderdale Research and Education Center, University of Florida,
Institute of Food and Agricultural Sciences, Ft. Lauderdale, FL 33314
J. Econ. Entomol. 98(6): 2143Ð2152 (2005)
ABSTRACT Distance effects of three treatments, novißumuron, Þpronil, and thiamethoxam, against
laboratory populations of the Formosan subterranean termite, Coptotermes formosanus Shiraki, were
tested in extended foraging arenas with foraging distances of 50 m. The results showed that during
the 10-wk test period, all termites were killed by novißumuron baits, whereas the nonrepellent
termiticides Þpronil and thiamethoxam divided the laboratory populations into two groups after
causing 25Ð35% worker mortality. The horizontal transfer of lethal effects of Þpronil was 5m.For
thiamethoxam, the distance of transfer was substantially shorter. Because of their dose-dependent
lethal time, the nonrepellent termiticides did not fulÞll the requirements of a liquid bait model.
KEY WORDS novißumuron, Þpronil, thiamethoxam, areawide population management
SOIL TREATMENTS WITH LIQUID insecticides have been the
major tool in subterranean termite control since the
1950s. In 2002, for example, soil termiticide applica-
tions accounted for 77% market share of the subter-
ranean termite control business in the United States
(Anonymous 2002). The application of soil termiti-
cides beneath a structure creates a barrier to exclude
soil-borne termites. Because of the extensive foraging
range of an underground colony, soil termiticide
treatments usually do not impact the overall pop-
ulation of subterranean termites (Su and Scheffrahn
1988a). The surviving colony continues to produce
foragers and alates that further infest nearby areas.
The termite control industryÕs reliance on soil ter-
miticide barriers is one of the contributing factors for
the continuing expansion of the Formosan subterra-
nean termite, Coptotermes formosanus Shiraki, in the
United States (Su 2003).
In recent years, nonrepellent termiticides have be-
come popular alternatives for termite control indus-
try. Approximately 60% of the termiticides used in
2002 were one of the nonrepellent termiticides
such as Þpronil (Termidor, BASF Corp., Research
Triangle Park, NC), imidacloprid (Premise, Bayer En-
vironmental Service, Montvale, NJ), or chlorfenapyr
(Phantom, BASF Corp.) (Anonymous 2002). Because
of their nonrepellency and apparent delayed action, it
has been suggested that, unlike the repellent pyre-
throid or fast-acting organic phosphate termiticides,
these new termiticides may impact the subterranean
termite populations (Kard 2001, Potter and Hillery
2002, Wagner 2003, Hu 2005). Laboratory study indi-
cated that termites exposed to sublethal doses of imi-
dacloprid did not show aversion to the subsequent
exposure and may continue to travel through the
treated soil, resulting in the colony suppression
(Thorne and Breisch 2001). Movement of exposed
termites also may spread the nonrepellent toxicants to
nestmates through trophallaxis and social grooming
(Ibrahim et al. 2003, Hu 2005). Shelton and Grace
(2003), however, reported that high concentration of
Þpronil (10 ppm) was needed for a successful trans-
fer of lethal dose to recipients, but at such dose, the
donors may be killed too fast for a substantial toxicant
transfer to occur within the population.
Laboratory evaluation for repellency, delayed ac-
tion, or horizontal transfer of these toxicants typically
uses small groups of Þeld-collected termites for testing
(Thorne and Breisch 2001, Ibrahim et al. 2003, Shelton
and Grace 2003, Hu 2005). Such protocols may be
adequate in evaluating response of individual termites
or a small group of termites to treatments, but it is
often challenging to interpret these laboratory results
for their effects against Þeld colonies with foraging
distance of 50 Ð100 m (King and Spink 1969, Su and
Scheffrahn 1988a, Grace et al. 1989, Su et al. 1993).
Laboratory bioassay with test tubes containing treated
soil (Su and Scheffrahn 1990) and the modiÞed ver-
sions (Su et al. 1995, Gahlhoff and Koehler 2001) were
designed primarily to test termiticide barrier efÞcacy,
and it is probably inappropriate to infer results of
nonrepellent termiticide tube tests for their impact
against subterranean termite populations. None of the
laboratory protocols, including those for slow-acting
baits (Su and Scheffrahn 1993, 1996), could duplicate
the distance factor of the Þeld colonies of subterra-
0022-0493/05/2143Ð2152$04.00/0 2005 Entomological Society of America
nean termites. This is especially critical in testing the
scope of transfer of nonrepellent and slow-acting tox-
icants by the nestmates over a large area, and the goal
of the control measure is aimed at the colony level.
The objective of this study was to examine the
distance effects of two nonrepellent termiticides,
Þpronil and thiamethoxam (Syngenta Crop Protec-
tion, Greensboro, NC), and one termite bait, novißu-
muron (Recruit III, Dow AgroSciences, Indianapolis,
IN), against laboratory groups of C. formosanus in a
laboratory arena with a linear foraging distance of
50 m. Thiamethoxam is a second generation neo-
nicotinoid belonging to the thianicotinyl chemical
subclass and has been under termiticide Experimental
Use Permit since 2002.
Materials and Methods
The extended foraging arena was composed of 11
small arenas (24 by 24 cm and 1.4 cm in thickness)
connected in linear series with each other by a 5-m-
long coiled Tygon tubing (0.6 cm in diameter) to form
a 50-m (excluding the length of the small arenas)
foraging distance from one end to the other (Fig. 1A).
The small arena was composed of two sheets of trans-
parent Plexiglas (24 by 24 by 0.6 cm in thickness)
separated from each other by Plexiglas laminates
(2 cm in width and 0.2 cm in thickness on three sides,
and 7 cm in width and 0.2 cm in thickness on one side)
placed between the outer margins to form a 0.2-cm gap
of 20 by 15 cm (Fig. 1B). Two pieces of 0.2-cm-thick
transparent Plexiglas (7 by 1.5 cm) were bolted be-
tween the 0.6-cm-thick Plexiglas sheets at 3.5 cm from
each other near the arena center to maintain the
0.2-cm gap of the arena. Approximately 60 g of sifted
sand (150Ð500-
m sieves) was poured in the 0.2-cm
gap and moistened with 15 ml of deionized water.
The upper sheet had an access hole (0.5 cm in diam-
eter) near one corner, onto which a Plexiglas cup
(4.5 cm in diameter and 3 cm in height) with lid was
Þtted to form a termite release chamber (Fig. 1B).
Three transparent plastic tubes (4.5 cm in diameter
and 3 cm in length) containing moistened wood pieces
(Spruce, Picea spp., 2.5 cm in length and 0.5 cm in
diameter) were inserted in the Tygon tubing at three
positions, one at the center and the others near the
Þrst and last small arenas (Fig. 1A).
Termites were collected from three Þeld colonies of
C. formosanus by using the method described by Su
and Scheffrahn (1986). Ten thousand workers (un-
differentiated larvae of at least the third instar) and
1,500 soldiers were divided roughly into 11 groups and
placed in the arena through each release chamber,
after which more moistened wood pieces were placed
into chamber to provide additional food sources. The
arena was placed in the dark at 25 2Cfor1wkto
allow termite movement throughout the 50-m arena,
after which a treatment chamber (4.5 cm in diameter
Fig. 1. The extended foraging arena was composed of 11 small arenas (24 by 24 cm and 1.4 cm in thickness) connected
to each other by a 5-m-long Tygon tubing (0.6 cm in diameter) to form a 50-m foraging distance (A). The small arena was
composed of two sheets of transparent Plexiglas (24 by 24 by 0.6 cm in thickness) with the 0.2-cm gap Þlled with moistened
sand (B). After placing termites through the release chambers, the treatment chamber was inserted near 0-m arena.
2144 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 98, no. 6
and 3 cm in length) was inserted at one section of
Tygon tubing 30 cm from the second arena from one
end (Fig. 1A). The small arena nearest to the treat-
ment chamber was referred to as the 0-m arena, the
arena at the left end was referred to as the 5-m
arena, and other small arenas were similarly referred
to by their distance from the treatment chamber,
namely, 45-m arenas (Fig. 1A). For novißumuron,
the treatment chamber was Þlled with a roll of cellu-
lose bait containing 0.5% novißumuron, or Recruit III.
For Þpronil or thiamethoxam, the chamber contained
a segment of 2-cm-thick sand treated with either ter-
miticide sandwiched between two segments of 1-cm-
thick untreated sand. Water emulsions of Termidor SC
(at 0.06%) or ACTAW 25 WG (0.1%) (Syngenta Crop
Protection) were applied in sand to yield 80.8 ppm
(wt:wt) Þpronil or 135.8 ppm thiamethoxam. The
treated sand was left overnight to dry before use. The
yielded rate was equivalent to applying 4.07 liters/m
2
sand for preconstruction termiticide treatments
(NPCA 1985), assuming the penetration of the liquid
termiticide onto 2-cm-thick sand. Extended arenas
with treatment chambers Þlled with untreated sand
also were prepared as the control.
After the installation of treatments, digital images of
the small arenas were taken weekly for 10 wk, and the
numbers of live or dead workers were counted from
the images on the computer monitor. Because some,
but not all, corpses decomposed quickly and became
invisible from the digital images, the weekly dead
termite counts included freshly dead individuals as
well as some of those present in previous week. The
weekly data thus represented the observed mortality
for each small arena at the time when the digital image
was taken. The experiments were replicated three
times by using termites of three colony origins. At the
end of the 10-wk period, the arenas were disassembled
to count the numbers of surviving workers and soldiers
and their positions in the arenas. The square-root of
percentage of mortality was arcsine-transformed and
subjected to analysis of variance (ANOVA). SigniÞ-
cant differences (
0.05) among treatments were
separated by least signiÞcant difference (LSD) test
(SAS Institute 1985).
Results
Noviflumuron Baits. Termites entered the treat-
ment chamber containing novißumuron bait immedi-
ately after it was inserted in tubing between 0- and 5-m
arenas and began feeding (Fig. 2A). After 1 wk of
feeding, motionless workers enclosed with exuviae
(Fig. 2B) were observed throughout most of the 11
small arenas, with the highest number (approximately
nine workers) found in the 5-m arena (Fig. 3). A
small number of exuviae-wrapped workers, possibly
during their routine molting, were occasionally found
in control arenas (Fig. 3), but the substantially larger
number of such workers in novißumuron arenas im-
plied its chitin synthesis inhibitory (CSI) effects on
termites. The jack-knife posture was akin to the
symptom of termites exposed to another chitin syn-
thesis inhibitor, hexaßumuron (Su and Scheffrahn
1993). The affected workers remained alive but mo-
tionless and were extensively groomed by healthy
workers. No dead termites were found in any of the 11
small arenas with novißumuron at 1 wk (Fig. 4). More
termites with CSI effects were found throughout the
50-m arenas at 2 wk (Fig. 3), and some began to die
after developing dark necrotic lesions, resulting in
5Ð30% mortalities at 2 and 3 wk mostly in small arenas
5 m from novißumuron baits (Fig. 4). At 3 wk, the
number of workers with CSI effects declined, and the
peak seemed to shift from 5-m arena at 1 wk to 5-m
arena at 2 wk and further away from baits toward
25-mÐ30-m arenas at 3 wk (Fig. 3). As the mortality
increased at 4 wk, fewer termites with CSI effects were
observed. Even at 4 wk when 50 Ð90% mortality was
recorded from 5- to 50-m arenas, feeding of baits
continued. Akin to the distance pattern of chitin syn-
thesis inhibitory effects, initial mortality peak also was
observed near the treatment chamber (5-mÑ5-m
arenas), but then mortality began to occur near 25Ð
30-m arenas at 4 to 5 wk (Fig. 4). As the mortality levels
at arenas 5Ð10 m reached near 100% at 6 to 7 wk,
mortality in arenas 20 m also increased. Only at 7 wk
when all termites were dead between 5- and 10-m
arenas (including bait chamber), feeding of novißu-
muron baits stopped. This was probably because of the
avoidance of decomposed corpses near the treatment
chamber. No termites were found feeding the baits
after 7 wk, but by then termites throughout the arenas
apparently have had ingested lethal doses of novißu-
muron, either directly or through trophallaxis, as ev-
idenced by the increasing mortality that rippled
through arenas 20 m between 6 and 10 wk (Fig. 4).
By 10 wk, no live termites were found in any of the 11
small arenas in the novißumuron treatment.
Sand Treated with Fipronil. One to 2 d after the
treatment chamber was inserted, dead termites were
found in Þpronil-treated sand (Fig. 5A). At 1 wk when
decomposition of some corpses became evident, no
live termite entered the treated sand. Almost all ter-
mites in 0-m arena for Þpronil at 1 wk were either dead
or moribund (Fig. 6). Moribund termites typically laid
on the side or back with all appendages folded to-
gether (Fig. 5B). Dead termites were often covered
with sand. Some exposed termites, either directly or
through social contact, moved to 5-m arena before
dying, indicating the horizontal transfer of Þpronil.
With a few occasions of dead termites found in 30-m
arena, most dead termites were observed in arenas
5 m from treated sand throughout the 10-wk test
period (Fig. 6). Termites stopped entering treated
sand after 1 wk, and no additional mortality was ob-
served in arenas 5 m from treatment. Consequently,
the initial population of 10,000 workers (plus 1,500
soldiers) was divided into two isolated groups.
Sand Treated with Thiamethoxam. As with Þpronil
treatment, dead termites were found in thiame-
thoxam-treated sand a few days into the experiment,
and no live termites were entering the treated sand
after 1 wk, when corpse decomposition became evi-
dent. Approximately 30% mortality was recorded in
December 2005 S
U:EXTENDED FORAGING ARENA 2145
the 0-m arena at 1 wk, and with the exception of
5% mortality observed in 20- and 25-m arenas at
2 wk, dead termites (30Ð50% mortality) were found
mostly in 0-m arenas during initial 8-wk period
(Fig. 6). At 9 wk, 30% mortality also was recorded
in 5- and 5-m arenas, but at the 10 wk, dead termites
were found only at the 0-m arena. Between 1 and
10 wk, a few live termites were found in 0-m arena,
whereas many dead termites were buried in sand and
isolated from the live termites (Fig. 5C). Live termites
seemed to travel into the Tygon tube connecting to
the treated chamber, but none entered the treated
sand after the second week. No or very few dead
termites were found in arenas 5 m from treated sand
throughout the 10-wk test period (Fig. 6). As with the
Þpronil test, the surviving termites in the extended
arenas were divided into two isolated groups.
Final Mortality and Positions of Surviving Ter-
mites. Almost no dead termites were observed in any
of the control arenas throughout the 10-wk experi-
ment (Fig. 4), but the Þnal count revealed a mean
worker mortality of 17.6% (Table 1). The lack of ap-
parent termite corpses in any of the small arenas for
untreated control suggested that dead workers may
have been cannibalized or removed, or some may have
molted into soldier caste. Indeed, more soldiers (1,505
and 1,537) were found in the Þnal count of two rep-
licates of control arenas than initially placed (1,500) in
Fig. 2. Termites fed on novißumuron baits up until 7 wk when 100% mortality was recorded in small arenas 10 m from
treatment (A), and workers with chitin synthesis inhibitory effects were found through out the 11 small arenas during 1Ð4 wk
(B).
2146 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 98, no. 6
the arenas, suggesting the workerÐsoldier transforma-
tion. As expected from the weekly digital image counts
of novißumuron arenas, no live termites were found in
any parts of the extended arena, resulting in 100%
mortality for both castes of all replicates (Table 1).
The Þnal mean worker mortalities for arenas contain-
ing sand treated with nonrepellent termiticides were
signiÞcantly higher (43.0 and 48.4% for Þpronil and
thiamethoxam, respectively) than untreated control
(17.6%), indicating 25Ð30% of the 10,000 workers
were killed by the termiticides (Table 1). There was
no signiÞcant difference in solider mortalities be-
tween control and Þpronil or thiamethoxam treat-
ment.
The isolated group of 200 workers in the 5-m
arena, wood chamber, and tubing leading to 0-m arena
contained 40% soldiers at 10 wk for both Þpronil and
thiamethoxam (Fig. 7). The other groups of 5,000 Ð
5,500 workers were found in 5-m arenas (plus tubing
and wood chambers). Soldier proportion for Þpronil
arenas ranged 10 Ð30% for arenas 5 m away from
treated sand, with the largest number (600) found in
the 10-m arena and tubing leading to the 15-m arena.
For thiamethoxam arenas, 25 workers plus 17 sol-
Fig. 3. Numbers of workers enclosed in exuviae recorded in 5Ð45-m arenas for control and novißumuron treatment
during the 10-wk test.
December 2005 SU:EXTENDED FORAGING ARENA 2147
diers ( 40% soldier) were found in 0-m arenas, but
they were in tunnels isolated from dead termites bur-
ied in arena sand (Fig. 5C). The remaining termites
were found in arenas 5 m with more workers further
away from the treatment, but proportionally more
solders were presented near thiamethoxam-treated
sand and dead termites were in 0-m arena (Fig. 7).
Discussion
Results of this study showed that the CSI novißu-
muron eliminated 10,000 C. formosanus works (plus
1,500 soldiers) within the 50-m arena in 10 wk,
whereas the nonrepellent termiticides divided the
populations into two isolated groups after killing 25Ð
30% of the workers. The results indicated that termites
exposed to Þpronil, either directly or through social
interaction with contaminated individuals, moved
5 m, and those exposed to thiamethoxam moved
5 m before the onset of death. Once dead and de-
composed corpses accumulated near treatments,
healthy termites no longer came in contact with treat-
ment and survived. Because termites entered sand
treated with Þpronil (80.8 ppm) or thiamethoxam
(135.8 ppm) initially, neither termiticide at the tested
concentrations was repellent, and the avoidance was
probably a response to dead termites or decomposed
corpses. It seemed that the horizontal transfer of Þpro-
nil did occur as suggested previously (Kard 2001, Pot-
ter and Hillery 2002, Ibrahim et a. 2003, Wagner 2003,
Fig. 4. Percentage of worker mortality recorded in 5Ð45-m arenas for control and novißumuron treatment during the
10-wk test.
2148 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 98, no. 6
Hu 2005), but the distance of transfer was 5m.As
reported by Shelton and Grace (2003), those exposed
to high doses of Þpronil may be able to transfer lethal
doses to others, but apparently they could not move
too far away from treatment before being immobi-
lized. For thiamethoxam at 135.8 ppm, the distance of
transfer was substantially shorter.
Potter and Hillery (2002), who used in-ground
bucket stations to measure activity of the eastern
subterranean termite, Reticulitermes flavipes (Kollar),
reported elimination of termite activity in six of eight
sites after soil application of Þpronil. The stations
that remained active at two sites in their report were
5 m away from treated soil. Their results thus do
not contradict with results of this study. A Þeld study
reported that soil application of the nonrepellent
termiticide imidacloprid did not measurably impact
nearby populations of C. formosanus (Osbrink et al.,
2005). Another Þeld study to compare termite control
measures against the invasive R. flavipes in Chile also
showed that applications of Þpronil in soil did not
affect colony activities in the vicinity of treatments
(R. Ripa, personal communication).
Numerous studies have demonstrated the elimina-
tion of all detectable subterranean termite activity by
hexaßumuron or novißumuron baits at a variety of
locations with many termite species, to the point
where citations to the published literature are super-
ßuous (Grace and Su 2001). Results of this laboratory
test conÞrmed previous Þeld studies that the lethal
effects of novißumuron can affect a population with a
foraging distance of 50 m, leading to colony elimina-
tion.
The main difference between the nonrepellent ter-
miticides and CSIs such as novißumuron is their lethal
time, i.e., time required to death after exposure to
lethal doses (Su and Scheffrahn 1988b). Unlike novi-
ßumuron, lethal times of Þpronil and thiamethoxam
are dose-dependent (Remmen and Su 2005). Individ-
uals contaminated (either directly or through con-
tact) with lower but lethal doses were able to move
away from treatment as evidenced by the dead ter-
mites found in arenas 5 m away from Þpronil-treated
sand. But those exposed to higher lethal doses, either
by repeatedly entering or continuously tunneling
treated sand, may die rather quickly in or near the
treatment. The large number of dead or decomposed
corpses in areas near the treatment probably acted as
the repellent to healthy termites. The avoidance of
dead and decomposed corpses (necrophobic behav-
ior) was well documented in termites such as C. for-
mosanus (Su 1982) and Pseudacanthotermes spiniger
Sjo¨ stedt (Chouvenc 2003). The effect of nonrepellent
termiticides when acquired by termites at higher
doses, therefore, is similar to that of fast-acting ter-
miticides such as chlorpyrifos, and their barrier efÞ-
cacy is because of secondary repellency (Su et al.
1982).
It remains possible that soil treatments with non-
repellent termiticides may eliminate a colony whose
entire foraging range is within 5 m (or less for thia-
methoxam) of treatment, but the treated soil must
contain the ideal (active ingredient) concentration(s)
that is both lethal and slow-acting. Treated sand used
in this study contained a homogeneous concentration,
but it is unlikely that applications of liquid termiticides
in the Þeld, either by trenching, rodding, or drilling
and injection, can produce a homogeneously lethal
and slow-acting concentration that allows contami-
Fig. 5. Dead termites were found in Þpronil-treated sand
1 to 2 d after it was inserted in the arena (A), and moribund
(those laying on the side or back with all appendages folded
together) and dead termites (covered with sand particles)
were observed in 0 m arena at 1 wk (B). Throughout the
10-wk experiment for thiamethoxam, live termites were
found in 0-m arena where corpses were buried in sand and
well isolated from live termites (C).
December 2005 SU:EXTENDED FORAGING ARENA 2149
nated termites to move away from treated soil at any
substantial distance before being immobilized. Ter-
mites exposed to soil with higher concentrations
would be killed rather quickly, those exposed to lower
nonlethal doses would survive, and only those exposed
to the intermediate range of both lethal and slow-
acting doses may move away from treated soil before
dying. Because foraging galleries of a colony may ori-
ent toward any direction; not necessary only toward
treated soil, some termites would survive and the col-
ony may be divided into more than one disconnected
populations as shown in this study.
To manage populations of subterranean termites in
a large area, especially the invasive species such as
C. formosanus, the ability of a control agent to elimi-
nate or kill the entire colony is vital. Because the
surviving colony would continue to produce alates
that further infest nearby areas, use of a soil termiti-
cide, be it nonrepellent or otherwise, would allow
Fig. 6. Percentage of worker mortality recorded in 5Ð45-m arenas for Þpronil and thiamethoxam treatment during the
10-wk test.
Table 1. Mortality (% SE) of C. formosanus workers and
soldiers in the extended foraging arenas containing noviflumuron
bait or sand treated with fipronil or thiamethoxam during a 10-wk
experiment
Treatment Worker Soldier
Control 17.6 2.1a 13.8 13.8a
Novißumuron 100.0 100.0b 100.0 100.0b
Fipronil 43.0 0.4c 27.6 4.4a
Thiamethoxam 48.4 7.0c 20.4 6.1a
Means followed by the same letter within a column are not signiÞ-
cantly different (
0.05) according to LSD test (SAS Institute 1985).
2150 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 98, no. 6
further establishment and spread of C. formosanus. As
reported by Osbrink et al. (2005), the nonrepellent
termiticides apparently did not fulÞll the require-
ments of a liquid bait model. If C. formosanus popu-
lations are to be managed, there is a need to use a
control measure that can kill the entire colony.
Acknowledgments
I thank R. Pepin (University of Florida) and A. Mullins
(New Orleans Mosquito and Termite Control Board) for
technical assistance, and R. H. Scheffrahn and B. Cabrera
(University of Florida) for review of the manuscript. This
research was supported by the Florida Agricultural Experi-
ment Station and a grant from USDAÐARS under the grant
agreement no. 58-6435-2Ð 0023. Additional funding was pro-
vided by Syngenta Crop Protection. This article was ap-
proved for publication as Journal Series No. R-10895.
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Received 27 May 2005; accepted 9 August 2005.
2152 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 98, no. 6
... After termites are killed by liquid termiticides, large quantities of corpses may accumulate in the treated zone and trigger tunnelclogging or avoidance behaviors of live termites (Gautam et al. 2014). This phenomenon, namely 'secondary repellency', may reduce the transfer efficiency of liquid termiticides, especially when distance is taken into account (Osbrink and Lax 2003, Remmen and Su 2005, Su 2005, Yeoh and Lee 2007, Chouvenc 2018, Baker and Miguelena 2020. For example, Su (2005) reported that transfer of fipronil or thiamethoxam among C. formosanus did not occur beyond 3-5 m because these insecticides triggered secondary repellency and prevented further transfer of the toxicant far away from treatment. ...
... This phenomenon, namely 'secondary repellency', may reduce the transfer efficiency of liquid termiticides, especially when distance is taken into account (Osbrink and Lax 2003, Remmen and Su 2005, Su 2005, Yeoh and Lee 2007, Chouvenc 2018, Baker and Miguelena 2020. For example, Su (2005) reported that transfer of fipronil or thiamethoxam among C. formosanus did not occur beyond 3-5 m because these insecticides triggered secondary repellency and prevented further transfer of the toxicant far away from treatment. Likewise, Baker and Miguelena (2020) reported significant reductions of the desert subterranean termite, Heterotermes aureus (Snyder) (Blattodea: Rhinotermitidae), in monitoring stations adjacent to soil treated with fipronil, but no evidence of termite reductions was found in stations further away from the treated soil. ...
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... Baits containing CSIs have provided a viable option for homeowners and the pest control industry because, unlike traditional liquid termiticide barrier systems, complete colony elimination is possible and bait systems are more sustainable and environmentally friendly as CSI baits employed 600-fold less insecticides than the liquid termiticide [2,32]. Furthermore, the liquid termiticide can kill only termites that contacted the treatment and few meters away from the treatment as it is fact acting and dose-dependent insecti-cide [33][34][35][36]. On the other hand, CSI baits are slow-acting and lethal time dose-independent insecticide, which allows to eliminate colonies of subterranean termite near the structures regardless of distances from the treatment [2,33,36,37]. ...
... Furthermore, the liquid termiticide can kill only termites that contacted the treatment and few meters away from the treatment as it is fact acting and dose-dependent insecti-cide [33][34][35][36]. On the other hand, CSI baits are slow-acting and lethal time dose-independent insecticide, which allows to eliminate colonies of subterranean termite near the structures regardless of distances from the treatment [2,33,36,37]. Despite of baits' sustainability and usefulness in termite control, the relatively long duration of time required to achieve colony elimination of subterranean termites is considered the least appealing aspect of baiting systems [2]. ...
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Effective active ingredients in toxicant bait formulations must be non-deterrent to insect feeding behavior at lethal concentrations. This study evaluated feeding deterrence for Coptotermes formosanus Shiraki, C. gestroi (Wasmann), and Reticulitermes flavipes (Kollar) when provided access to cellulose impregnated with various concentrations of the insect molting hormone, 20-hydroxyecdysone (20E). Termites were exposed to 20E concentrations of 200, 500, 1000 and 2000 ppm and to noviflumuron at 5000 ppm in a 24 h choice-test, and the mass of substrate consumption from treated and untreated media pads was compared for each treatment. 20E feeding deterrence was detected at 500, 1000 and 2000 ppm for C. gestroi, and at 2000 ppm for C. formosanus. No significant differences in consumption of treated and untreated substrate was detected at any concentration for R. flavipes. Potential methods for reducing deterrence are discussed.
... Those prosecutions take tested the impactiveness of imidacloprid-remedy -muds by experience to extra than 20 types of termites, with Allodontermes, Amitermes, Coptotermes, Heterotermes, Macrotermes, Mastotermes, Microcerotermes, Microtermes, Nasutitermes, Reticulitermes, and Schedorhinotermes. Imidacloprid, take mainly substituted pyrethroids and organophosphate termiticides by way of the vigorous elements of optimal in termite loam handlings 7 . Single suggestion suggests that termites resolve remain to fodder obsessed by handlings of sluggish-substitute, no nauseating termiticide, subsequent in exclusion of termite inhabitants in extents together to the actions 8 . ...
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Termites reason deep commercial fatalities international. Microcerotermes diversus (Silvestri) reasons marvelous indemnities to timber effort in the constructions and woodland plants. Diverse kinds of fly spray have been utilized to dominate this underground termite. In the present research, efficacy of imidacloprid and Spinosad against Microcerotermes diversus (Silvestri) was studied. The results showed that the direct spray of different concentration (200, 400 and 600 ppm) for both Spinosad and imidacloprid on the stems of Olive trees and soil surrounding a diameter of 20 cm was high impactive in termite infestation reduction which decreasing the tunnels length and the quantity of workforces gradually and absence the termite infestation after the time. The duration of absence of termite infestation refinish on concentrations of the both termiticides. It is noted in concentrations 200 and 400 ppm for the pesticide imidacloprid, the infestation was continuous during the year and the termite infestation did not stop, as for the concentration of 600 ppm, it prevented the infestation for a period of 3 months, and then the infestation resumed in the months of April, May and June, after which the infestation was stopped. As for the pesticide Spinosad at all its concentrations, it prevented the infestation with different periods, the best and most efficient, the concentration of 600 ppm, the infestation was prevented after two months of spraying, and the infestation continued for all concentrations until the assumption of the investigate period, besides the impact of spinosad reduced and prevent the quantity of workforces visiting the stem of Olive trees gradually till the infestation was absence.
... Fipronil-sulfone was also detected in the termite body fraction of workers collected from monitoring stations 1, 5, and 6 at collection three weeks after the discontinuous soil treatment (Table 6). These results showed that workers of C. formosanus moved at least 28 m and that workers of R. speratus moved at least 6 m after contacting fipronil-treated soil around the stations, although termites exposed to fipronil had been reported to never move more than 5 m [33]. ...
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We assessed the efficacy of a discontinuous soil treatment using a diluent of fipronil suspension concentrate in controlling colonies of Coptotermes formosanus and Reticulitermes speratus. In-ground monitoring stations were installed at Isogi Park and Kindai University, and individual termites inhabiting the stations were collected for four or six years to determine the numbers and locations of colonies present in test areas before and after the discontinuous soil treatment. Microsatellite genotyping indicated that two C. formosanus and two R. speratus colonies in the test area at Isogi Park and five R. speratus colonies in the test area at Kindai University were active and that their territories fluctuated every year. One of the two C. formosanus colonies at Isogi Park and one of the five R. speratus colonies at Kindai University were subjected to discontinuous soil treatments with fipronil and were strongly affected by the treatment at the colony level, resulting in the suppression and possible elimination of colonies. Termite activity of the fipronil-treated colony of C. formosanus was detected within one week after the discontinuous soil treatment and was not found for more than two years (28 months), while termite activity of the fipronil-treated colony of R. speratus was detected within four days and three weeks after the discontinuous soil treatment and was not detected thereafter for three years. Fipronil residue analysis showed that workers of C. formosanus moved at least 28 m and that workers of R. speratus moved 6 m from the treated soil locations for up to three weeks.
... At a global level, although studies of this type were conducted on pest species of subterranean termites (Rhinotermitidae), the current study provides preliminary information on optimal experimental and rearing conditions in the laboratory for C. testaceus. As previously shown, the importance of the biological relevancy of a bioassay when testing control method against subterranean termites in laboratory conditions is critical (Su, 2005;Chouvenc, 2018), to study the applicability of such approach in a field situation. The current study therefore provides initial guidelines for the manipulation of C. testaceus in the laboratory, thus being able to carry out future studies aimed at testing control approach for this species. ...
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Coptotermes testaceus (L.) (Rhinotermitidae) is a subterranean termite species that cause damage in urban and agricultural areas in the neotropics. Despite its economic importance, there are no studies on its basic biological aspects for laboratory management and the development of strategies for its control. The objective of the present study was to evaluate the relative humidity, temperature, substrate moisture and preference to different wood substrates for the best C. testaceus survival under laboratory conditions. For this, a range of eight relative humidity (from 9 to 100%), three temperatures (20, 25 and 30 °C), six substrates (Pinus sp, Cedrela odorata (L.), Cocos nucifera (L.), Eucalyptus urophylla (S. T. Blake), Haematoxylum campechianum (L.) and Tabebuia rosea [Bertol.] DC) and four substrate moistures, (0 to 60%) were tested. The results of this study indicated a significant effect of all factors on termite survival or termite preference. When tested independently, the highest survival percentage of C. testaceus was obtained with humidity of 100%, temperature of 20 °C, substrate moisture of 60% and the Eucalyptus urophylla substrate, reaching 83.33% survival at 21 days of observation. With these preliminary assays on small termite groups, it is concluded that with the appropriate percentages of humidity, temperature and substrate and the interaction of these three factors, further research can be conducted using larger termite groups in biologically relevant conditions, in order to study various aspects of C. testaceus biology.
... Most ant species, such as Solenopsis invicta, Acromyrmex versicolor and Linepithema humile, dispose of dead colony members in special chambers or refuse piles (Howard and Tschinkel, 1976;Julian and Cahan, 1999;Choe et al., 2009), Temnothorax lichtensteini has been to bury alien corpses, while Formica polyctena and S. invicta practice cannibalism (Driessen et al., 1984;Renucci et al., 2011). In termites, corpses can be buried, cannibalized, abandoned or avoided (Rosengaus and Traniello, 2001;Su, 2005;Neoh et al., 2012;Ulyshen and Shelton, 2012;. ...
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Social insects display a range of sophisticated behaviors to deal with cadavers, which together act to guarantee the health and social homeostasis of their colonies. In termites, cadaver management involves an entire repertoire of activities, such as antennation, grooming, retreat, alarm and agonistic behaviors. We performed different bioassays to evaluate whether postmortem-age, origin and caste of a cadaver influence the behavior of Coptotermes gestroi. Quantitative analyses of corpse management behaviors indicated that C. gestroi is able to discriminate the origin and caste of cadavers. Cadavers of worker nestmates were preferentially cannibalized while corpses of alien workers were buried. In addition, soldiers that had been dead for 24hours were buried while freshly dead soldiers were either buried, consumed or ignored, indicating a plastic behavioral response that depends on postmortem age. Corpse consumption is an important component of corpse management repertoire because this process eliminates contaminant and enables nutrient recycling. The physical isolation of the termite corpse through burial after grooming also helps to prevent other colony members from contacting the cadaver, further mitigating against the potential spread of disease.
... They showed that due to multilevel disease resistance mechanisms, the incidence of an epizootic within a group of termites is unlikely: the three major mechanisms were grooming, cellular encapsulation, and gut antifungal activity. Similarly, in extensive laboratory work, Su [67] and Chouvenc [58] showed that Coptotermes formosanus Shiraki and Coptotermes gestroi (Wasmann), respectively, avoided or sealed off areas treated with fipronil. Our fieldwork had similar results in that whilst the bait toxicants were relocated into some of the mounds, colony elimination did not occur. ...
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Various pesticide nanocarriers have been developed. However, their pest-control applications remain limited in laboratories. Herein, we developed silica nanocapsules encapsulating fipronil (SNC) and their engineered form, poly(ethyleneimine)-coated SNC (SNC-PEI), based on recombinant catalytic modular protein D4S2 and used them against termite colonies Coptotermes lacteus in fields. To achieve this, an integrated biomolecular bioprocess was developed to produce D4S2 for manufacturing SNC containing fipronil with high encapsulation efficiency of approximately 97% at benign reaction conditions and at scales sufficient for the field applications. PEI coating was achieved via electrostatic interactions to yield SNC-PEI with a slower release of fipronil than SNC without coating. As a proof-of-concept, bait toxicants containing varied fipronil concentrations were formulated and exposed to nine termite mounds, aiming to prolong fipronil release hence allowing sufficient time for termites to relocate the baits into and distribute throughout the colony, and to eliminate that colony. Some baits were relocated into the mounds, but colonies were not eliminated due to several reasons. We caution others interested in producing bait toxicants to be aware of the multilevel resistance mechanisms of the Coptotermes spp. “superorganism”.
... To observe the behavior of subterranean termites in laboratory conditions, a planar arena has been widely used to study a variety of topics, such as tunneling behaviors (Su 2005a;Lee et al. 2008;Yang et al. 2009;Bardunias and Su 2010a,b), foraging behaviors , agonistic behaviors (Li et al. 2010), insecticide assays (Su 2005b, Chouvenc 2018, molting site fidelity (Kakkar et al. 2018), and polyethism (Du et al. 2017b, Yanagihara et al. 2018). The planar arena has several advantages in that the assay provides the termites with foraging distances and a soil environment while allowing for high visibility at all times with low disturbance, high survivorship, and possibility for experimental manipulations (see details in Chouvenc et al. (2011), Chouvenc (2018). ...
Article
As a social insect, termites have different castes and division of labor in a colony. Investigating the social behavior of subterranean termites is a challenge due to the cryptic nature and large colony size. Planar arenas are commonly used to study these termites under laboratory conditions, and have provided several advantages. However, there is no means to designate areas such as a royal chamber or central nest from foraging sites because reproductives can move freely across arenas. In this study, we examined the minimum passing size of different castes of Coptotermes formosanus Shiraki (Blattodea: Rhinotermitidae), in order to develop a reproductive excluder and correlated minimum passing size with head widths and heights. We found that workers and soldiers of C. formosanus were able to pass through a gap greater than or equal to 0.7 mm. Our results showed that there are significant differences in the head width and height based on castes and head height was more critical than head width to determine passing size. We further confirmed feasibilities of the reproductive excluders using incipient colonies of C. formosanus. Confining reproductives using the excluder in laboratory experiments will provide more chances to study the royal chamber and central nest independently of foraging sites.
... (Lee et al., 2001). 이중 토양처리법은 1930년대 이전부터 흰개미 방제를 위해 제안되던 방법으 로 (Kofoid and Termite investigations committee, 1934), 건 물 주변 토양에 살충물질을 희석한 용액을 처리하여 지중 에서 생활하는 지중 흰개미가 목조 건축물에 접근하지 못 하도록 보호하는 역할을 수행한다 (Su and Scheffrahn, 1990;Bläske et al., 2003;Su, 2005). ...
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A Termiticide that is applied to the soil treatment method, one of the methods for preventing termites in Korea’s wooden cultural properties, will be subjected to the leaching of the effective ingredient in treated soil by the moisture behavior of rain. As a result, termiticide is deteriorated and needs to be reprocessed, but the standards and evaluation methods are nonexistent in korea. Accordingly, a basic indoor evaluation measure was proposed for the evaluation of the effectiveness of the termiticide chamber and the calculation of the reprocessing period. First, avoidance and contact toxicity were assessed at two concentrations of the same termiticide as a method for assessing termiticide suitability. The evaluation of mortality revealed that the soil termiticide used in this experiment was non-repellent, and that death from contact was confirmed. Afterwards, artificial rainfall and soil penetration tests were conducted to determine efficacy of termiticide in soil and the approximate reprocessing period was calculated by comparing the weather data. Persistence evaluation revealed perforation by termites after continuous water exposure of more than about 160 to 170mm of water injection condition. Based on the results, compared with weather data for the last five years, the termiticide of concentration used in this experiment is expected to remain effective for about one year if treated after September. The purpose of this study was to provide basic data for the establishment of a manual for the selection of termiticide for soil treatment by calculating the efficacy for termite mortality and the duration of the leaching effectiveness by water behavior in soil.
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In the United States, the number of areas infested with the Formosan subterranean termite has increased in recent years, but its worldwide distribution remains primarily in areas between ca. 35degrees north and south of the equator. Soil termiticide applications that have been in widespread use by the pest control industry for the half-century are intended for exclusion of soilborne termites from the structures, but their inability to kill vast colonies in soil may have allowed the establishment and increase of Coptotermes formosanus populations in many introduced areas. With the development of baits that can be used to eliminate termite colonies, there is hope that C. formosanus populations may be substantially reduced if area-wide programs are implemented.
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A mark-release-recapture study was conducted with dye-marked eastern subterranean termites, Reticulitermes flavipes (Kollar), at two sites in metropolitan Toronto. Inter-connected termite galleries were found to extend up to 79 m and to cover areas of 266 and I 091 m 2 • Colony foraging populations at the two sites were estimated at 2 .I and 3.2 million termites. These foraging distances and population estimates exceed those reported for R. flavipes in other regions.
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The efficacy of the Sentricon™ Colony Elimination System containing Recruit™ II termite bait (Dow AgroSciences LLC, 0.5% hexaflumuron) in controlling active subterranean termite infestations has been demonstrated in numerous studies. This baiting system and other termite baiting systems are now widely used, and generally accepted tools for remedial termite control in North America, Hawaii, and other parts of the world. The role of baiting systems in prevention of termite damages and long-term structural protection, however, is more controversial than their use in remedial control. We discuss three lines of evidence in support of the use of baits for long-term structural protection: (1) successful control of termite populations with baits in remedial studies allows a conceptual leap to preventative efficacy, since baits target colonies and populations and cannot be evaluated directly for prevention in the manner of soil insecticide barriers; (2) field and laboratory studies demonstrate that termite colonies feed on multiple resources and continue to radiate outward from each of those resources in search of additional food, increasing the likelihood of rapid bait discovery; and (3) results of our long-term field studies over the past decade demonstrate that newly invading termites will reuse existing galleries in the soil left by earlier colonies that lead to monitoring stations, were detected in monitoring stations, and were subsequently eliminated without any noticeable evidence of structural infestation or damage.
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Two chitin synthesis inhibitors, hexaflumuron and diflubenzuron, were evaluated in a laboratory choice test for their potential as bait toxicants against the Formosan subterranean termite, Coptotermes formosanus Shiraki, and the eastern subterranean termite, Reticulitermes flavipes (Kollar).Concentrations of hexaflumuron that elicited feeding deterrence were >125 ppm for C. formosanus and >62.5 ppm for R. flavipes, whereas concentrations required to cause >90% mortality at 9 wk were > 15.6 ppm and >2 ppm for C. formosanus and R. flavipes, respectively. Diflubenzuron deterred feeding of C. formosanus at such low concentrations (>2 ppm) that the highest recorded mortality was only 50% and is not likely to be effective in a bait against this termite species. More than 80% of R. flavipes workers died after feeding on diflubenzuron at >7.8 ppm, whereas feeding deterrence was recorded at >31.3 ppm. We conclude that hexaflumuron is superior to diflubenzuron as a bait toxicant because it is effective over a concentration range of 15.6-62.5 ppm. This concentration range is lethal and nondeterrent for both C. formosanus and R. flavipes. Diflubenzuron is efficacious against R. flavipes over a fairly narrow range of concentrations (7.8-31.3 ppm) and does not appear to be useful as a bait toxicant against C. formosanus.
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Lethality, molting inhibitory effects, and feeding deterrence of 2 chitin synthesis inhibitors, hexaflumuron and lufenuron, were studied in a laboratory choice test using wood sawdust as feeding medium. Feeding deterrence of hexaflumuron in sawdust medium was lower than that observed in a previous study in which hexaflumuron-impregnated wooden blocks were used. The concentration threshold of hexaflumuron for feeding deterrence is high [>8,000 ppm for Coptotemes formosanus Shiraki, and >4,000 ppm for Reticulitermes flavipes (Kollar)], whereas ≍100% mortality was recorded 9 wk after exposure even at the lowest concentrations tested (125 ppm for C. formosanus and 31.3 ppm for R. flavipes). Feeding deterrence of lufenuron was observed at lower concentration intervals (1,000-2,000 ppm and 50-100 ppm for C. formosanus and R. flavipes, respectively) than hexaflumuron, but baits treated with the nondeterrent concentrations of lufenuron caused only 50-80% mortality. even after 9 wk of exposure. The overall potential of lufenuron as a bait toxicant is less than that of hexaflumuron.
Conference Paper
The U.S. Forest Service has been testing chemicals for termite control since 1939. Today its termiticide testing program is nationally recognized for providing unbiased efficacy data for product registration using standardized tests, sites, and evaluation procedures. Virtually all termiticides undergo Forest Service testing before being registered by EPA. Termiticides undergo 18-24 months of laboratory screening before going to the field. Based on the concrete slab test, termiticides are considered effective in the field at the lowest concentration(s) that prevent termites from penetrating treated soil in 10 plots at each site for at least five years. Sites are located in Arizona, Mississippi, Florida, and South Carolina. Results provide a benchmark to compare and assess new and existing products. Because termite control is no longer limited to repellent or contact chemical barriers, tests are also performed on non-repellent delayed-action termiticides, barriers, and wood products. Some of the new products have novel effects on termite biology, ecology, and behavior that require new evaluation procedures. The Forest Service presently has 26 funded agreements with industry involving laboratory screening of three termiticides and field evaluations of 20 termiticides and four impregnated barriers. We also continued to monitor plots on five termiticides and two physical barriers from past (expired) agreements. Marketed termiticides being tested by the Forest Service include bifenthrin (Biflex(R)), chlorpyrifos, cypermethrin, fenvalerate, permethrin (Dragnet(R) and Torpedo(R)), imidacloprid (Premise(R)), and fipronil (Termidor(R)). Candidate termiticides include chlorfenapyr, cyfluthrin (Tempo(R)), and deltamethrin(2).
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Data presented herein indicate that subterranean termite infestations can be eliminated by applying non-repellent liquid termiticides solely around the exterior perimeter of buildings. Foraging activity was extensively monitored on the interior and exterior of 12 structures heavily infested with the eastern subterranean termite, Reticulitermes flavipes (Kollar). Monitoring methods before and after an exterior-only application of either Termidor® (fipronil) or Premise® (imidacloprid) were similar to those used to assess the effects of baits on termite populations. Substantial, and often rapid reductions in termite foraging activity were observed, particularly with Termidor. Of the eight structures treated with Termidor, 40 of 43 infested monitoring stations within 0.3 to 4.0 m of the exterior treated trench were inactive within three months. Dead and decaying termites were found in several monitored locations, further suggesting that effects extend inward and well beyond the exterior site of application. Termite activity within monitoring stations was less affected by exterior Premise applications, although visible activity involving structural components eventually ceased. Potential implications and benefits of exterior-targeted liquid applications relative to the future of termite control are discussed.
Article
Subterranean foraging galleries of a colony of C. formosanus Shiraki (Isoptera: Rhinotermitidae) were excavated in a filled, swampy area about 2 miles west of Lake Charles. Branches from 3 main galleries radiating from a dead baldcypress tree ramified over about 1.4 acres. These galleries were connected with food sources more than 200 feet from the original starting point. Species of trees attacked included dead baldcypress, dead pine, live wax myrtle, and live Chinese tallow. Live pine was not attacked by this termite. Most of the galleries were lined with carton material that varied in thickness and the galleries ranged from 2 to 46 inches deep. Vertical galleries branched from horizontal galleries and extended to the water table. A subterranean carton nest that contained 6 supplementary queens was found 19 inches below the soil surface and 25 feet from the nearest food source. Based on the date the swampy area was filled, it was apparent that this gallery system was less than 10 years old.