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Sublethal effects of neuroactive compounds on pheromone response thresholds in male oriental fruit moths.

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Archives of Insect Biochemistry and Physiology 1:331-344 (1984)
Sublethal Effects of Neuroactive Compounds
on Pheromone Response Thresholds in Male
Oriental Fruit Moths
C.E. Linn, Jr., and W.L. Roelofs
Department of Entomology, New York State Agricultural Experiment Station, Genma
The pheromone-mediated flight behavior of male Oriental fruit moths in a
sustained-flight tunnel was observed after males were treated topically with
sublethal concentrations of permethrin, carbaryl, chlordimeform, dieldrin,
octopamine, serotonin, yohimbine, and cyproheptadine. With the exception
of serotonin all compounds were found to disrupt one or more specific
elements of the male precopulatory flight sequence. Among the insecticides,
dieldrin was least active, whereas permethrin, carbaryl, and chlordimeform
induced unique effects at specific phases of the sequence. Octopamine
induced a hypersensitivity to the olfactory signal and mimicked one of the
effects observed with chlordimeform. Yohimbine and cyproheptadine
significantly decreased moth activation t o the chemical signal but did not
alter flight performance in responding moths. Yohimbine and cyproheptadine
also reversed the effects induced by octopamine. The results of our study
show that the complex precopulatory sequence of behaviors exhibited by
males is very sensitive to sublethal concentrations of a range of neuroactive
Key words: sex pheromone, Oriental fruit moth, sublethal effects, permethrin, carbaryl,
chlordimeforrn, dieldrin, octopamine, serotonin, yohimbine, cyproheptadine
The sex pheromone-mediated flight behavior of male moths is a complex
response that involves integration of visual and chemical inputs with a
Acknowledgments: We gratefully acknowledge Kathy Poole, Marlene Campbell, and Laura
Child for rearing the OFM. We thank Dr R.M. Hollingworth and Dr D. Soderlund for the
generous gifts of test compounds, and also Dr Soderlund for his comments on the manuscript. We also thank Joe Ogrodnick, Rose McMillan-Sticht, and Bernadine Aldwinkle for the
figures. This research was supported by National Science Foundation grant BNS 82-16752.
Received February 27,1984; accepted April 13,1984.
Address reprint requests to Dr C.E. Linn, Jr, Department of Entomology, NYS Agricultural
Experiment Station, Geneva, NY 14456.
0 1984 Alan R. Liss, Inc.
Linn and Roelofs
circadian rhythm that also regulates normal flight activity [l]. Females typically release a specific blend of compounds to which males respond optimally
[2].In the case of the Oriental fruit moth,* Gvupholithu molesfa (Busck), the
sex pheromone blend comprises three components: (Z)-8-dodecenyl acetate
plus 6% (E)S-dodecenyl acetate and 3-30% (Z)-8-dodecenol [ 3 ] . We have
been conducting studies using the OFM as a model organism to understand
the factors that control or influence the response specificity of males to the
chemical signal. One approach has been to analyze the behavior of males in
a flight tunnel to a large number of blend-dosage combinations. In these tests
male OFM responded in peak numbers to a narrow range of treatments
around the blend and release rate produced by females. Analysis of the male
response to suboptimal treatments showed evidence for several threshold
effects on flight behavior, each associated with specific changes in blend or
release rate [4-61.
We report here a series of exploratory experiments to determine the efficacy of another approach to understanding how thresholds that control
response specificity are regulated-that is, to observe the effects of sublethal
concentrations of neuroactive compounds on male behavior. These compounds include insecticides with specific modes of action affecting various
pathways in the nervous system, and neurotransmitters and neuromodulators that may affect the circadian rhythmicity of locomotory activity, as well
as specific motor patterns. The results show that both the pheromonestimulated behavior and the thresholds for activation in male OFM can be
dramatically altered with sublethal concentrations of a variety of compounds,
and that different compounds influence male behavior in specific ways.
Male OF34 were reared on small green apples at 2 5 T , 16:8 L:D photoperiod. Adult males were segregated daily by age and kept under similar
conditions in a room separated from females.
For all experiments the pheromone source was 10 pg of the optimal blend:
Z8-12:Ac with 6% E8-12:Ac and 10% Z8-12:OH added [6]. A stock solution of
the three compounds (0.1 pglpl) was prepared in distilled Skelly €3 (principally hexanes). The ratio of compounds was checked by capillary GLC (45m
Carbowax 20 M column). The stock solution (100 111) was applied to a rubber
septum (red 5 x 9 mm, Arthur H. Thomas Co, Philadelphia), using a
disposable capillary pipette.
Male OFM were treated with the following compounds: the insecticides
chlordimeform (as the free base), permethrin (5050 &:trans), carbaryl (ana-
*Abbreviations: CNS = central nervous system; DMSO = dimethyl sulfoxide; E8-12Ac = (E)8-dodecenyl acetate; GLC = gas-liquid chromatography; OFM = Oriental fruit moth; 2812:Ac = (Z)-8-dodecenyl acetate; Z8-12:OH = (Z)-8-dodecenol.
Neuroactive Compounds and Moth Pheromone Response
lytical standard), dieldrin (analytical standard); the biogenic amines DLoctopamine (Sigma Chemical Co, St. Louis, as the hydrochloride) and serotonin (5-hydroxytryptamine, as the hydrochloride, Sigma); and two known
antagonists of octopamine-the alkaloid yohimbine (as the free base) and
cyproheptadine. Chlordimeform, yohimbine, and cyproheptadine were gifts
of Dr R.M. Hollingworth, Purdue University, and permethrin, carbaryl, and
dieldrin were gfts of Dr D. Soderlund, NYS Agricultural Experiment Station.
For each compound a dilution series was prepared and for all compounds
except octopamine and serotonin, acetone was the solvent. For the latter two
DMSO was utilized, as they are soluble in DMSO and we had hypothesized
from previous studies [7Jthat this solvent might serve as a suitable carrier
for the compounds across the cuticle.
Procedure for Treating Insects
Four-day-old males were treated 5 h prior to the normal period of testing
in the flight tunnel (2 hr prior to initiation of scotophase). Males were first
immobilized by placing them individually into 4-dram vials and then into a
freezer ( - l 0 T ) for 10 min. Upon removal 1 p1 of solution was applied
topically to the ventral thoracic region using a syringe. On each test day a
series of concentrations were tested in addition to a control group receiving
no treatment, one receiving the cold treatment alone, and one receiving cold
exposure plus 1 pl of solvent. The solvent control group was treated first,
followed by the series of concentrations in ascending order. Each compound
was tested separately, with ten males treated per test day for each concentration and control. Prior to any treatment the syringe was cleaned and repeatedly rinsed with distilled acetone.
Flight Tunnel Procedures
The flight behavior of individual male OFM to the synthetic pheromone
lure was observed in the flight tunnel of Miller and Roelofs [8]. Treated and
control groups were placed in the room housing the flight tunnel for 1h of
acclimation prior to testing. For all tests the flight tunnel conditions were:
2 1 T , 350 lux, 50-70% RH, 35 cmlsec air velocity. The procedures and apparatus for handling and testing males were as previously described [5,6].
Males were scored for each behavior performed in the flight sequence [5]:
taking flight, stationary hovering flight near the release point, upwind anemotactic flight over a 1.5-m distance, landing at the source followed by a
hairpencil display to the septum [9]. For the present study a single extrusion
of the hairpencils was scored as a display. Analysis was made of the number
of males exhibiting each behavior based on the total number tested for all
days (n = 70 for each concentration and control). For each treatment, behaviors were analyzed using the method of adjusted significance levels for
proportions, P < 0.05 [lo]. For each compound control groups were also
analyzed to v e d y that no significant effects had occurred in the cold- or
solvent-treated insects. In the results to follow, all comparisons are between
treated insects and untreated controls, as there were no significant effects
observed between untreated, cold-treated, or solvent-treated controls in any
Linn and Roelofs
of the tests. For the temporal data cited below the mean and standard
deviation are indicated, based on the number of males exhibiting the behavior in question.
Evaluation of the percentage mortality for each compound (Fig. 1) was
based on the number of males exhibiting no activity, even when prodded or
touched, 24 h after treatment. For our experiments we arbitrarily defined a
sublethal concentration as one resulting in <25% mortality 24 h after treatment. For the four insecticides tested, males were most sensitive to permethrin, followed by carbaryl, chlordimeform, and dieldrin. No lethal effects were
observed for octopamine, serotonin, yohimbine, or cyproheptadine over the
concentration range tested.
Effects of Insecticides
Significant effects on male behavior following exposure to sublethal concentrations were observed with all four insecticides tested. Treatment with
permethrin resulted in a significant decrease in the number of males that
oriented to the odor plume or initiated upwind flight (Fig. 2a). Following
Fig. 1. Percentage mortality for each test compound recorded 24 h after treatment for a range
of concentrations (pg) applied in 1 pl of solvent to male OFM. Clear area at the bottom of the
figure shows the range of concentrations below 25% mortality and considered sublethal.
Each value represents the mean and SD for 50 individuals tested.
Neuroactive compounds and Moth Pheromone Response
i c
Fig. 2. Flight response of male OFM to a synthetic sex pheromone source 5 h after topical
application of permethrin (a), carbaryl (b), chlordimeform (c), dieldrin (d), octopamine (e),
yohirnbine (f), and cyroheptadine (g). Behaviors are: taking flight (TF), plume orientation (OR),
upwind flight (UP),and hairpencil display (HP) (at least one extrusion of the hairpencils).
Values shown for 10 cm distance indicate males that landed on the 15 x 15 cm platform
where source was located. N = 70 for each concentration. Dashed line indicates response of
untreated controls. Within each behavior response values with different letters are significantly different, P < 0.05. Concentrations are pg applied in 1 PI of solvent to each moth;
values in parentheses indicate percent mortality.
Linn and Roelofs
Figure 2 c and d.
Neuroactive Compounds and Moth Pheromone Response
2 60
$ 1
Figure 2 e and f.
Linn and Roelofs
flight initiation, males that did not orient to the plume typically flew a short
distance and settled on the floor or side of the tunnel and became quiescent.
Males that oriented to the plume but did not initiate upwind flight typically
exhibited stationary flight for less than 3 s, thereafter settling on the floor of
the tunnel. Males treated with 10P7toloP5 pg that flew to the source also
took significantly longer to do so than did control insects (with
pg flight
initiation took 7.3 f 1.4s, n = 36, vs 1.1f 0.1 s, n = 64,and the time to fly
upwind 1.5m took 11.3 4.8 s, n = 36, vs 3.1 k 1.1s, n = 64).
Male response after treatment with carbaryl was not affected during the
early orientation phase, but rather males were unable to initiate and sustain
upwind flight (Fig. 2b). With loP5 to lo-' pg, for increasing percentages of
males, the initial stage of the flight response was characterized by wide
lateral excursions in the horizontal plane, often in excess of 40 cm (in control
moths zigzag turns typically were 10-15 cm in lateral displacement across the
center line of the plume). These excursions eventually resulted in the male
losing contact with the plume and flying to the side of the tunnel. In addition,
to loP2 pg significant proportions of moths that initiated upwind
flight failed to reach the source, leaving the plume space at varying distances
from the source after exhibiting wide and apparently uncontrolled lateral
casting patterns. Males that flew upwind to the source at loP5 pg took
_---__ ------- -- g,,, -------- - ---------
-0 --a
10.' (0)
100 (0)
oi 40
10' (0)
1 0 2 (0)
Figure 2 g.
;O 6
Neuroactive Compounds and Moth Pheromone Response
significantly longer than did control insects (15.7 f 4.9 s, n = 47, vs 2.8 f
1.1s, n = 65), with the males displaying stationary hovering flight several
times along the flight path.
Male response after treatment with chlordimeform was affected at all
phases of the behavioral response (Fig. 2c). With 0.01 pg fewer males reached
the source than initiated upwind flight, and the time taken to reach the
source was 11.3 f 3.7 s (n = 41), vs 3.1 k 0.8 s (n = 63), for controls. In
addition, the hairpencil display was significantly disrupted, with males exhibiting convulsive spasms upon reaching the platform and attempting to
exert the hairpencil structures. In some cases these spasms lasted for up to 1
min (38.6 k 17.2 s, n = 41, for 0.01 pg), after which the male became
quiescient and had to be removed from the platform. With 1pg chlordimeform, significantly fewer males oriented to the odor plume; those that did so
spent significantly longer in this behavior than did controls (71.4 k 14.5 s, n
= 37, vs 1.2 f 0.6 s, n = 66) and were unable to initiate upwind flight,
instead flying vertically out of the odor plume.
Male response was relatively unaffected by dieldrin (Fig. 2d) compared to
permethrin, carbaryl, and chlordimeform. Male response appeared to be
affected only in the early orientation phase, and no obvious adverse effects
on flight performance (time to reach the source) or the hairpencil display
were observed.
Casual observations were also made of male activity during the period
between treatment with insecticides and testing in the flight tunnel. These
observations indicated that chlordimeform-treated males exhibited increased
levels of spontaneous motor activity (walking andlor rapid bursts of wingfanning) and that the amount of activity appeared to be dose-related. The
increased activity was observed within 30 min of application and was not
observed with any of the other insecticides tested.
Effects of Biogenic Amines
Treatment with octopamine resulted in an increase in the number of males
taking flight and orienting to the odor plume followed by a significant
decrease in the number of males initiating upwind flight (Fig. 2e). Although
the increase in male flight and plume orientation was not statistically significant, it was associated with a marked change in behavior exhibited by males
upon being introduced into the tunnel. Males did not exhibit the typical
wing-fanning andlor walking activation response; instead, upon being placed
in the odor stream, males took flight immediately from a stationary position
in the release cage. This apparent increase in sensitivity to the chemical
signal was not reflected in increased levels of spontaneous activity prior to
testing, as was observed with chlordimeform-treated males. Increasing the
concentration of octopamine resulted not only in more males taking flight
and orienting to the plume, but also significantly longer times spent in this
phase of the response (47.2 k 16.2 s, n = 36, at 10 pg vs 1.1k 0.4 s, n = 61,
for controls). Octopamine-treated insects that did fly upwind did not appear
to be affected during flight, and completed this behavior in the same time as
did controls (4.2 f 1.1s, n = 30, at 10 pg vs 3.6 k 1.3 s, n = 61). However,
Linn and Roelofs
treated insects exhibited decreased levels of hairpencil displays at the source
compared to controls. With 10 pg, males exhibited either no display or at
most two displays, thereafter becoming quiescent on the platform. Control
males typically exhibited several bouts of 3-5 displays covering a period of
In contrast to octopamine, serotonin (0.1-100 pg) did not significantly affect
male behavior at any phase of the response, either in number of responding
individuals or with respect to temporal factors.
Effects of Antagonists
Treatment of male OFM with yohimbine or cyproheptadine resulted in a
significant decrease in the number of males initiating a flight response to the
pheromone (Fig. 2 f,g). With the exception of two individuals, males that did
not respond to the sex pheromone were capable of flight when touched with
a blunt probe. In addition, no effects on flight performance were observed
for males that completed the flight sequence, and there did not appear to be
any effect on the duration or intensity of the hairpencil display.
Yohimbine and cyproheptadine were also found to block the effect of
octopamine on male behavior (Fig. 3). Application of 100 pg yohimbine or 1
pg cyproheptadine following 10 pg octopamine resulted in a reversal of the
observed effects with each separate compound, and normal flight behavior
was observed compared to control insects.
The results of our exploratory study indicate that the pheromone-mediated
precopulatory flight and courtship behavior of male OFM is very sensitive to
10' Octoparnine t 10'Cyproheptadine
80 -
10' Octoparnine
lo2 Yohirnbine
Fig. 3. Flight response of male OFM to a synthetic sex pheromone source after topical
application of octopamine followed by application of yohimbine or cyproheptadine. Symbols
and analysis as in Figure 2. N = 70 for each concentration.
Neuroactive Compounds and Moth Pheromone Response
a variety of neuroactive compounds. In general the insecticides we tested at
sublethal concentrations did not affect the males’ ability to detect and respond to the signal, but they significantly disrupted the males’ ability to
execute the oriented flight response upwind to the source. This disruption
occurred in several ways, suggesting that different sites in the nervous
system or levels of integration and motor control were being affected. We
recognize, however, the difficulty in such extrapolations [ll], as our results
do not provide direct evidence of central versus peripheral action of the
compounds, their mode of entry, or their metabolic fate.
The dominant effect observed in moths treated with permethrin was on
the ability of males to sustain flight after detecting the pheromone signal.
Permethrin is a synthetic pyrethroid, a group of compounds that block axonal
conduction and transmission [El.A characteristic effect of these compounds
is increased spontaneous bursting in neurons, leading eventually to suppression of activity in the neural pathway [E,13].The results of our study suggest
that permethrin disrupted basic motor units involved in executing normal
flight behavior. In another study [14] permethrin was found to decrease the
activation response of male Pectinophoru gossypiellu (Saunders). The observed
difference in results could be due to the difference in time between treatment
and testing (5 h in the present study, 96 h in [14]), reflecting differing degrees
of impact of the compound on the nervous system over time.
In contrast to permethrin, carbaryl significantly disrupted the ability of
males to execute the oriented upwind flight response. This is a more complex
activity involving integration of visual and chemical imput with a guidance
mechanism that influences the basic motor pattern controlling flight. Carbaryl is an inhibitor of acetylcholinesterase and thus is active in the CNS [El.
Our results suggest that this compound affected CNS centers involved in
integrating sensory stimuli and the guidance mechanism rather than specific
motor pathways controlling flight coordination.
The specific effects observed with permethrin and carbaryl contrast further
with chlordimeform in which a number of concentration-dependent effects
were observed. Increasing concentrations of chlordimeform disrupted upwind flight, the courtship display, plume orientation, and initiation of upwind flight. In addition, chlordimeform appeared to cause a concentrationrelated increase in spontaneous motor activity observed very soon after
treatment and extending through the test period. This observation supports
a number of other studies with insects, and lepidoptera specifically, showing
that sublethal concentrations of chlordimeform induce in the early stages of
toxicity a hyperactive state, effectively disrupting a number of behaviors
[16,17J, including normal flight activity [18].
No significant effects of behavior were observed with sublethal concentrations of the cyclodiene dieldrin. It is possible that this was due to an insufficient time for the material to exert an effect on the target tissues given the
experimental protocol [15].
The biogenic amines octopamine and serotonin were chosen for testing
because of suspected roles in modulating CNS functions [19-261, and because
direct effects of octopamine and serotonin on olfactory discrimination have
been demonstrated in the honey bee, Apis melliferu [22]. In the present study
Linn and Roelofs
treatment with octopamine induced a marked increase in sensitivity to the
pheromone signal, suggesting that the threshold for upwind flight had been
shifted. We make this judgment based on the similarity of male response
after treatment with octopamine to that observed to a higher than optimal
concentration of the appropriate pheromone blend, where males typically
take flight and remain in a stationary hovering flight near the release point
for extended periods, thereafter leaving the odor plume by flying in a vertical
pathway [5,23].
The absence of any observable effects in serotonin-treated insects does not
eliminate this compound from consideration as a potential modulator of
pheromone behavior. Serotonin has also been implicated in modulating
circadian locomotor rhythms in the moth Agvotis ipsilon [24], in Peripluneta
umericanu [25], and in Drosophilu melunogustev [26]. Further testing with OFM
at different times in the diurnal cycle might be necessary to observe an effect.
It is also possible that topical applicaltion was not an effective means of
introducing this compound into the hemolymph and neural tissues.
A number of studies have demonstrated that chlordimeform interacts
directly with octopaminergic receptor sites [19,27-331. In the present study
octopamine and chlordimeform influenced male behavior in similar ways but
also displayed distinct differences. Both compounds appeared to induce a
state of hypersensitivity, but while that observed with octopamine was exclusive to the olfactory stimulus, chlordimeform induced a more general excitatory state [MI. The effect on plume orientation and initiation of upwind flight
observed with all concentrations of octopamine was very similar to that
observed with the 1pg concentration of chlordimeform. However, at other
concentrations chlordimeform also disrupted the upwind flight performance
of males and dramatically affected the hairpencil display, inducing spasms
and loss of motor control. The hairpencil display was also disrupted by
octopamine but in this case the effect was a lowering of the intensity of the
display. If chlordimeform exerts its effects on the insect nervous system by
interacting exclusively with octopaminergic sites, then the results suggest
that chlorimeform had access to more of these sites than did octopamine.
The observed sensitivity of octopamine-treated males to the chemical signal was effectively reversed by yohimbine and cyproheptadine, both known
antagonists of one type of octopamineregic receptor [19,32]. In addition,
yohimbine and cyproheptadine also exerted pronounced effects on male
activation when presented alone, effectively eliminating male response to
pheromone without significantly affecting the male’s ability to fly. These
results, along with those from tests with chlordimeform, suggest that octopamine may be involved in modulating thresholds for pheromone-mediated
behavior. However, further tests would be needed to confirm this, since it is
known that chlordimeform, yohimbine, and cyproheptadine can interact at
other sites [21,30,32].
The results of our study also have implications for two practical goals.
First, it is clear that insecticides can exert significant sublethal effects on
mating behavior and could thus have an important influence on pheromone
field-trapping studies. It is also clear that sublethal effects of insecticides can
contribute to reduced mating success in populations and thus contribute
Neuroactive Compounds and Moth Pheromone Response
significantly to control of populations treated in conventional ways [14].
Second, our flight tunnel assay allows for detailed analysis of a complex
behavioral pattern that is critical for the organism’s survival. The oriented
flight response of male OFM is essentially the same as that observed for
numerous other species and presumably is under similar neural control. The
results of our study suggest that this sensitive assay can provide useful
information concerning subtle effects of compounds to a degree not matched
by other assay systems. We believe this technique can provide a new, rapid,
and effective tool for screening compounds.
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