Commercial orchards, ornamental nurseries, and residential horticulture in North Carolina experience economic losses due to pine vole (Microtus pinetorum) depredation. Predator odors and the herbicide Casoron were tested as potential repellents for pine voles. To test for avoidance behavior, animals were allowed to build a nest in one of two chambers attached to each arm of a Y-maze. The cage containing the nest was treated with either a test repellent compound, methylene chloride (solvent control), or left unmanipulated (control). Animals were categorized as either maintaining or changing nest cage preference between pre-test and test periods. The number of animals that changed cage preference in the control group was compared to the treatment groups. Only the Casoron treatments were significantly different, with approximately 50% of the animals changing preference. The difference in time spent in the nest cage during the pre-test and test periods for the treatment groups were compared to control groups. The Casoron and DTT treatments resulted in significant time differences. These results indicate that Casoron has repellent potential and warrants further investigation into its effectiveness in the field. The predator odors tested showed little promise as repellents

Salatti, Christopher J.

Vandenbergh, John G.

Woolhouse, Anthony D.

English

DigitalCommons@University of Nebraska

University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln 6 - Sixth Eastern Wildlife Damage Control Conference (1993) Eastern Wildlife Damage Control Conferences October 1993 THE USE OF ODOR TO INDUCE AVOIDANCE BEHAVIOR IN PINE VOLES Christopher J. Salatti North Carolina State University Anthony D. Woolhouse Institute for Industrial Research and Development, Lower Hut, New Zealand John G. Vandenbergh North Carolina State University Follow this and additional works at: https://digitalcommons.unl.edu/ewdcc6  Part of the Environmental Health and Protection Commons Salatti, Christopher J.; Woolhouse, Anthony D.; and Vandenbergh, John G., "THE USE OF ODOR TO INDUCE AVOIDANCE BEHAVIOR IN PINE VOLES" (1993). 6 - Sixth Eastern Wildlife Damage Control Conference (1993). 29. https://digitalcommons.unl.edu/ewdcc6/29 This Article is brought to you for free and open access by the Eastern Wildlife Damage Control Conferences at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in 6 - Sixth Eastern Wildlife Damage Control Conference (1993) by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. THE USE OF ODOR TO INDUCE AVOIDANCE BEHAVIOR IN PINE VOLESCHRISTOPHER J. SALATTI, Dept. of Zoology, NCSU, Raleigh, NC 27695-7617, USAANTHONY D. WOOLHOUSE, Institute for Industrial Research and Development, P.O. Box 31,310. Lower Hut, New ZealandJOHN G. VANDENBERGH, Dept. of Zoology, NCSU, Raleigh, NC 27695-7617, USAABSTRACT: Commercial orchards, ornamental nurseries, and residential horticulture in North Carolina experience economiclosses due to pine vole (Microtus pinetorum) depredation. Predator odors and the herbicide Casoron were tested as potentialrepellents for pine voles. To test for avoidance behavior, animals were allowed to build a nest in one of two chambers attached toeach arm of a Y-maze. The cage containing the nest was treated with either a test repellent compound, methylene chloride (solventcontrol), or left unmanipulated (control). Animals were categorized as either maintaining or changing nest cage preference betweenpre-test and test periods. The number of animals that changed cage preference in the control group was compared to the treatmentgroups. Only the Casoron treatments were significantly different, with approximately 50% of the animals changing preference. Thedifference in time spent in the nest cage during the pre-test and test periods for the treatment groups were compared to controlgroups. The Casoron and DTT treatments resulted in significant time differences. These results indicate that Casoron has repellentpotential and warrants further investigation into its effectiveness in the field. The predator odors tested showed little promise asrepellents.Key words: Repellent, pine vole, Microtus pinetorum, North Carolina, orchardProc. East. Wildl. Damage Control Conf. 6:149-151. 1995.Each year the commercial orchards, ornamental nurseriesand residential horticulture of North Carolina experiencesignificant economic losses due to pine vole (Microtuspinetorum) depredation. Problems in apple orchards havereceived the most attention. Approximately 50% of the treedeath within apple orchards is attributed to vole damage,resulting in an estimated annual loss of $2.5 million (Bromleyet al. 1992). Damage in apple orchards occurs when pine volesfeed on the roots and the sub-surface portion of the trunk oftrees (Byer 1976).Recent advances in the field of inter-specific chemicalcommunication suggest that predator odors can be used asrepellents of pest species (Schumake 1977). Sullivan et al.(1988) isolated the most volatile components of severalpredator odors and tested these compounds for their repellentpotential. Traps treated with a red fox (Vulpes fulva) fecalcomponent, 2,5-dihydro-2,4,5,-trimethylthizoline (DTT),caught significantly fewer Montane voles (M. montanus).Treatment with a mixture of 2-n-propylthietane and 3-n-propyl-1,2-dithiolane (stoat, Mustela spp., anal glandcomponent) also reduced the number of voles trapped. Thesetreatments also significantly reduced the number of apple treesthat were damaged.This preliminary report describes tests of 2-n-propylthietane and DTT to induce avoidance behavior in pinevoles. In addition, anecdotal observations by horticulturistsindicate that orchardists using the herbicide Casoron to controlweeds have fewer vole problems. Casoron (Dichlobenil,Uniroyal) 4G and 10G (4% and 10% active ingredients) wasalso tested for its repellent potential. A more detailed reporton the effectiveness of Casoron is in preparation.This research was supported by North CarolinaAgricultural Research Project 05460. We thank P.T. Bromley,W.T. Sullivan and W.A. Skroch for helpful suggestions duringthe course of this research.METHODSWild stock, laboratory reared pine voles were weaned atapproximately 28 days of age and housed individually for 3weeks prior to testing. Animals were tested when 5 to 12months old and had no prior experience with the apparatus.Each vole was tested only once. Y-maze apparatuses fittedwith infrared sensors to monitor movements were used.Voles were allowed to establish a nest in one arm of theY-maze for 24 hrs. The animal was returned to the holdingchamber and the location of its nest was recorded. The cagecontaining the nest was then either treated with a potentialrepellent compound, or treated as a control. The animal wasgiven access to the Y-tube for an additional 6 hours and itsposition within the apparatus was recorded. The duration oftime in minutes spent in the cages and the stem of the Y-tubewas determined using the event recorder printout. In addition,trials were taped using a time-lapse video recorder. The tapeswere used to determine the position of the voles when theevent recorder printout was inconclusive. After every trial,the apparatuses were cleaned with a 50% alcohol in watersolution. The bedding, nest material and food were discardedand replaced with fresh material.For each trial, cage preference was determined duringthe pre-test and test periods. Cage preference was categorizedusing two criteria: (1) the presence of a nest in a cage and atleast 50% of the time spent in that nest cage during the pretestperiod or (2) the presence of a nest or 60% of the time spentin a cage or the stem during the test period. The differences intime spent in the nest cage between the pretest and the testperiods was also recorded for each trial. These differenceswere analyzed using a Mann-Whitney test.RESULTSChi-square analysis comparing the Control 1 and thesolvent treatment did not differ (chi-square = 0.32, p = 0.57,df = 1; Table 1), so these values were pooled as a controlgroup. Neither stoat odor nor fox feces odor (DTT) causedsignificant changes in preference (stoat: chi-square = 0.24, P= 0.62 fox: chi-square = 1.17, P = 0.28), but the percentage ofvoles that changed preference when subjected to DTT suggeststhat more extensive testing might show a statisticallysignificant effect for this treatment. Casoron 4G treatmentcaused significant changes in cage preference (chi-square =9.14, P = 0.0025). Control 1 and control 2 treatments did notdiffer (chi-square = 0.046, P = 0.83) so these values werepooled and compared to the Casoron 10G treatment. TheCasoron 10G caused a significant change in cage preference(chi-square 6.99, P 0.008).Measurements of the mean difference in time spent inthe nest cage during the pre-test and test periods showed thatthe control 1 and solvent treatments did not differ Mann-Whitney test-Z = -0.28 P = 0.78), so these values were pooledas a control group. The stoat odor differences were notsignificantly different from the control group (p = 0.53), whichconcurs with the chi-square analysis. The difference in timespent in the nest cage for the Casoron 4G and 10G treatmentswas significantly different from the control (p = 0.068 and P= 0.027 respectively), which also concurs with the analysis ofchange in cage preference for this treatment. DTT significantlyaffected the difference in time spent in the nest cage (P =0.025). This result does not agree with the analysis of changein cage preference for this treatment.Table 1. The percentage of animals that changed cagepreference between the pre-test and test periods in eachtreatment.Treatment n % ChangedControl 1 19 5.3Control 2 15 13.3Solvent 15 6.7Casoron 4G 12 50.0Casoron 10G 15 46.7Stoat Odor 14 7.1Fox Odor 14 21.4DISCUSSIONOf the four compounds tested, only Casoron was foundto induce avoidance behavior. 2-Propylthietane did not appearto repel pine voles or effect their behavior. The fox odor (DTT)did not result in a significant number of voles changing cagepreference, but it did effect the voles’ behavior. The timedifferences for nest occupation for the fox odor weresignificantly less than for the control treatments. This indicatesthat the voles behaved differently when the fox odor waspresent. DTT produces a stress response in laboratory raisedalbino rats, as measured by behavioral and biochemical assays(Vernet-Maury et al. 1984). The pine vole’s response to DTTexposure within the Y-tube suggests that pine voles, like rats,detect the fox odor. Unfortunately, the DTT does not appearto induce an avoidance response in pine voles, but it may alterbehavior In a way that would be useful for vole management.By using DTT to manipulate the stress response of voles, itmay be possible to disrupt feeding or reproductive behaviorand indirectly result in smaller vole populations. Furtherexperiments determine how fox odor affects vole behaviorneed to be conducted.The results indicated that Casoron 4G and 10G havepromising repellent potential. Both treatments repelledapproximately 50% of the voles from their nest cages. Thefact that only some of the voles were repelled may be due totwo aspects of the experimental design. First, the stress andanxiety of being tested in a strange, “unnatural” environmentmay have overridden the repellent effects of Casoron for someanimals. Second, a very conservative bioassay was used toindicate repelled behavior. The experiment was designed todetermine whether a vole could be prevented from re-enteringa nest cage. Casoron’s ability to force 50% of the animals togive up the security of their nests, where all the food cubeswere often cached, provides strong evidence for its repellentpotential.If Casoron proves to be an effective repellent it would bea very useful and environmentally safe vole control too. UsingCasoron as a repellent could reduce the quantity ofrodenticides used and frequency of applications. Problemswith secondary poisoning of non-target species anddevelopment of rodenticide resistant vole population couldbe reduced because of fewer rodenticide applications. SinceCasoron has a low toxicity (oral toxicity: LD50 in rats is >3.2 g/kg), there would not be any serious threat to non-targetspecies. From a practical perspective, may orchardists arealready familiar with Casoron and would likely be receptiveto learning new applications for an existing chemical to repelvoles. In addition, herbicides are already part of the integratedpest management program in orchards so Casoron applicationcould control weeds as well as repel pine voles.LITERATURE CITEDBromley, P. T., M. L. Parker, W. T. Sullivan. 1992. Controllingvole damage in commercial orchards and ornamentalnurseries. North Carolina Cooperative Extension ServiceBulletin AGI-472-1:1-4.Byers, R.E. 1976. Review of pine vole control methods. Va.Fruit, 64: 20-32.Schumake, S.A. 1977. The search for applications of chemicalsignals in wildlife management. Pp. 357-376, in ChemicalSignals in Vertebrates (D. M ller-Schwarze and M. M.Mozell, eds.) Plenum Press, N.Y.Sullivan, T. P., D. R. Crump, and D. S. Sullivan. 1988. Use ofpredator odors as repellents to reduce feeding damageby herbivores. J. Chem. Ecol., 14:363-377.Vernet-Manry, E., E. H. Polak, and A. Demel. 1984. Structure-activity relationship of stress-inducing odorants in the rat.Chem. Ecol., 10:1007-1018.

THE USE OF ODOR TO INDUCE AVOIDANCE BEHAVIOR IN PINE VOLES

UNL | Libraries

University of Nebraska - Lincoln 
DigitalCommons@University of Nebraska - Lincoln 
6 - Sixth Eastern Wildlife Damage Control 
Conference (1993) Eastern Wildlife Damage Control Conferences 
October 1993 
THE USE OF ODOR TO INDUCE AVOIDANCE BEHAVIOR IN PINE 
VOLES 
Christopher J. Salatti 
North Carolina State University 
Anthony D. Woolhouse 
Institute for Industrial Research and Development, Lower Hut, New Zealand 
John G. Vandenbergh 
North Carolina State University 
Follow this and additional works at: https://digitalcommons.unl.edu/ewdcc6 
 Part of the Environmental Health and Protection Commons 
Salatti, Christopher J.; Woolhouse, Anthony D.; and Vandenbergh, John G., "THE USE OF ODOR TO INDUCE 
AVOIDANCE BEHAVIOR IN PINE VOLES" (1993). 6 - Sixth Eastern Wildlife Damage Control Conference 
(1993). 29. 
https://digitalcommons.unl.edu/ewdcc6/29 
This Article is brought to you for free and open access by the Eastern Wildlife Damage Control Conferences at 
DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in 6 - Sixth Eastern Wildlife 
Damage Control Conference (1993) by an authorized administrator of DigitalCommons@University of Nebraska - 
Lincoln. 
THE USE OF ODOR TO INDUCE AVOIDANCE BEHAVIOR IN PINE VOLES
CHRISTOPHER J. SALATTI, Dept. of Zoology, NCSU, Raleigh, NC 27695-7617, USA
ANTHONY D. WOOLHOUSE, Institute for Industrial Research and Development, P.O. Box 31,310. Lower Hut, New Zealand
JOHN G. VANDENBERGH, Dept. of Zoology, NCSU, Raleigh, NC 27695-7617, USA
ABSTRACT: Commercial orchards, ornamental nurseries, and residential horticulture in North Carolina experience economic
losses due to pine vole (Microtus pinetorum) depredation. Predator odors and the herbicide Casoron were tested as potential
repellents for pine voles. To test for avoidance behavior, animals were allowed to build a nest in one of two chambers attached to
each arm of a Y-maze. The cage containing the nest was treated with either a test repellent compound, methylene chloride (solvent
control), or left unmanipulated (control). Animals were categorized as either maintaining or changing nest cage preference between
pre-test and test periods. The number of animals that changed cage preference in the control group was compared to the treatment
groups. Only the Casoron treatments were significantly different, with approximately 50% of the animals changing preference. The
difference in time spent in the nest cage during the pre-test and test periods for the treatment groups were compared to control
groups. The Casoron and DTT treatments resulted in significant time differences. These results indicate that Casoron has repellent
potential and warrants further investigation into its effectiveness in the field. The predator odors tested showed little promise as
repellents.
Key words: Repellent, pine vole, Microtus pinetorum, North Carolina, orchard
Proc. East. Wildl. Damage Control Conf. 6:149-151. 1995.
Each year the commercial orchards, ornamental nurseries
and residential horticulture of North Carolina experience
significant economic losses due to pine vole (Microtus
pinetorum) depredation. Problems in apple orchards have
received the most attention. Approximately 50% of the tree
death within apple orchards is attributed to vole damage,
resulting in an estimated annual loss of $2.5 million (Bromley
et al. 1992). Damage in apple orchards occurs when pine voles
feed on the roots and the sub-surface portion of the trunk of
trees (Byer 1976).
Recent advances in the field of inter-specific chemical
communication suggest that predator odors can be used as
repellents of pest species (Schumake 1977). Sullivan et al.
(1988) isolated the most volatile components of several
predator odors and tested these compounds for their repellent
potential. Traps treated with a red fox (Vulpes fulva) fecal
component, 2,5-dihydro-2,4,5,-trimethylthizoline (DTT),
caught significantly fewer Montane voles (M. montanus).
Treatment with a mixture of 2-n-propylthietane and 3-n-
propyl-1,2-dithiolane (stoat, Mustela spp., anal gland
component) also reduced the number of voles trapped. These
treatments also significantly reduced the number of apple trees
that were damaged.
This preliminary report describes tests of 2-n-
propylthietane and DTT to induce avoidance behavior in pine
voles. In addition, anecdotal observations by horticulturists
indicate that orchardists using the herbicide Casoron to control
weeds have fewer vole problems. Casoron (Dichlobenil,
Uniroyal) 4G and 10G (4% and 10% active ingredients) was
also tested for its repellent potential. A more detailed report
on the effectiveness of Casoron is in preparation.
This research was supported by North Carolina
Agricultural Research Project 05460. We thank P.T. Bromley,
W.T. Sullivan and W.A. Skroch for helpful suggestions during
the course of this research.
METHODS
Wild stock, laboratory reared pine voles were weaned at
approximately 28 days of age and housed individually for 3
weeks prior to testing. Animals were tested when 5 to 12
months old and had no prior experience with the apparatus.
Each vole was tested only once. Y-maze apparatuses fitted
with infrared sensors to monitor movements were used.
Voles were allowed to establish a nest in one arm of the
Y-maze for 24 hrs. The animal was returned to the holding
chamber and the location of its nest was recorded. The cage
containing the nest was then either treated with a potential
repellent compound, or treated as a control. The animal was
given access to the Y-tube for an additional 6 hours and its
position within the apparatus was recorded. The duration of
time in minutes spent in the cages and the stem of the Y-tube
was determined using the event recorder printout. In addition,
trials were taped using a time-lapse video recorder. The tapes
were used to determine the position of the voles when the
event recorder printout was inconclusive. After every trial,
the apparatuses were cleaned with a 50% alcohol in water
solution. The bedding, nest material and food were discarded
and replaced with fresh material.
For each trial, cage preference was determined during
the pre-test and test periods. Cage preference was categorized
using two criteria: (1) the presence of a nest in a cage and at
least 50% of the time spent in that nest cage during the pretest
period or (2) the presence of a nest or 60% of the time spent
in a cage or the stem during the test period. The differences in
time spent in the nest cage between the pretest and the test
periods was also recorded for each trial. These differences
were analyzed using a Mann-Whitney test.
RESULTS
Chi-square analysis comparing the Control 1 and the
solvent treatment did not differ (chi-square = 0.32, p = 0.57,
df = 1; Table 1), so these values were pooled as a control
group. Neither stoat odor nor fox feces odor (DTT) caused
significant changes in preference (stoat: chi-square = 0.24, P
= 0.62 fox: chi-square = 1.17, P = 0.28), but the percentage of
voles that changed preference when subjected to DTT suggests
that more extensive testing might show a statistically
significant effect for this treatment. Casoron 4G treatment
caused significant changes in cage preference (chi-square =
9.14, P = 0.0025). Control 1 and control 2 treatments did not
differ (chi-square = 0.046, P = 0.83) so these values were
pooled and compared to the Casoron 10G treatment. The
Casoron 10G caused a significant change in cage preference
(chi-square 6.99, P 0.008).
Measurements of the mean difference in time spent in
the nest cage during the pre-test and test periods showed that
the control 1 and solvent treatments did not differ Mann-
Whitney test-Z = -0.28 P = 0.78), so these values were pooled
as a control group. The stoat odor differences were not
significantly different from the control group (p = 0.53), which
concurs with the chi-square analysis. The difference in time
spent in the nest cage for the Casoron 4G and 10G treatments
was significantly different from the control (p = 0.068 and P
= 0.027 respectively), which also concurs with the analysis of
change in cage preference for this treatment. DTT significantly
affected the difference in time spent in the nest cage (P =
0.025). This result does not agree with the analysis of change
in cage preference for this treatment.
Table 1. The percentage of animals that changed cage
preference between the pre-test and test periods in each
treatment.
Treatment n % Changed
Control 1 19 5.3
Control 2 15 13.3
Solvent 15 6.7
Casoron 4G 12 50.0
Casoron 10G 15 46.7
Stoat Odor 14 7.1
Fox Odor 14 21.4
DISCUSSION
Of the four compounds tested, only Casoron was found
to induce avoidance behavior. 2-Propylthietane did not appear
to repel pine voles or effect their behavior. The fox odor (DTT)
did not result in a significant number of voles changing cage
preference, but it did effect the voles’ behavior. The time
differences for nest occupation for the fox odor were
significantly less than for the control treatments. This indicates
that the voles behaved differently when the fox odor was
present. DTT produces a stress response in laboratory raised
albino rats, as measured by behavioral and biochemical assays
(Vernet-Maury et al. 1984). The pine vole’s response to DTT
exposure within the Y-tube suggests that pine voles, like rats,
detect the fox odor. Unfortunately, the DTT does not appear
to induce an avoidance response in pine voles, but it may alter
behavior In a way that would be useful for vole management.
By using DTT to manipulate the stress response of voles, it
may be possible to disrupt feeding or reproductive behavior
and indirectly result in smaller vole populations. Further
experiments determine how fox odor affects vole behavior
need to be conducted.
The results indicated that Casoron 4G and 10G have
promising repellent potential. Both treatments repelled
approximately 50% of the voles from their nest cages. The
fact that only some of the voles were repelled may be due to
two aspects of the experimental design. First, the stress and
anxiety of being tested in a strange, “unnatural” environment
may have overridden the repellent effects of Casoron for some
animals. Second, a very conservative bioassay was used to
indicate repelled behavior. The experiment was designed to
determine whether a vole could be prevented from re-entering
a nest cage. Casoron’s ability to force 50% of the animals to
give up the security of their nests, where all the food cubes
were often cached, provides strong evidence for its repellent
potential.
If Casoron proves to be an effective repellent it would be
a very useful and environmentally safe vole control too. Using
Casoron as a repellent could reduce the quantity of
rodenticides used and frequency of applications. Problems
with secondary poisoning of non-target species and
development of rodenticide resistant vole population could
be reduced because of fewer rodenticide applications. Since
Casoron has a low toxicity (oral toxicity: LD50 in rats is >
3.2 g/kg), there would not be any serious threat to non-target
species. From a practical perspective, may orchardists are
already familiar with Casoron and would likely be receptive
to learning new applications for an existing chemical to repel
voles. In addition, herbicides are already part of the integrated
pest management program in orchards so Casoron application
could control weeds as well as repel pine voles.
LITERATURE CITED
Bromley, P. T., M. L. Parker, W. T. Sullivan. 1992. Controlling
vole damage in commercial orchards and ornamental
nurseries. North Carolina Cooperative Extension Service
Bulletin AGI-472-1:1-4.
Byers, R.E. 1976. Review of pine vole control methods. Va.
Fruit, 64: 20-32.
Schumake, S.A. 1977. The search for applications of chemical
signals in wildlife management. Pp. 357-376, in Chemical
Signals in Vertebrates (D. M ller-Schwarze and M. M.
Mozell, eds.) Plenum Press, N.Y.
Sullivan, T. P., D. R. Crump, and D. S. Sullivan. 1988. Use of
predator odors as repellents to reduce feeding damage
by herbivores. J. Chem. Ecol., 14:363-377.
Vernet-Manry, E., E. H. Polak, and A. Demel. 1984. Structure-
activity relationship of stress-inducing odorants in the rat.
Chem. Ecol., 10:1007-1018.


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THE USE OF ODOR TO INDUCE AVOIDANCE BEHAVIOR IN PINE VOLES

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