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Journal of Applied Animal Welfare Science
ISSN: 1088-8705 (Print) 1532-7604 (Online) Journal homepage: http://www.tandfonline.com/loi/haaw20
A Case Study Employing Operant Conditioning toReduce Stress of Capture for Red-Bellied Tamarins(Saguinus labiatus)
Yvonne Owen & Jonathan R. Amory
To cite this article: Yvonne Owen & Jonathan R. Amory (2011) A Case Study Employing OperantConditioning to Reduce Stress of Capture for Red-Bellied Tamarins (Saguinus labiatus), Journalof Applied Animal Welfare Science, 14:2, 124-137, DOI: 10.1080/10888705.2011.551625
To link to this article: http://dx.doi.org/10.1080/10888705.2011.551625
Published online: 26 Mar 2011.
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JOURNAL OF APPLIED ANIMAL WELFARE SCIENCE, 14:124–137, 2011
Copyright © Taylor & Francis Group, LLC
ISSN: 1088-8705 print/1532-7604 online
DOI: 10.1080/10888705.2011.551625
A Case Study Employing OperantConditioning to Reduce Stress ofCapture for Red-Bellied Tamarins
(Saguinus labiatus)
Yvonne Owen and Jonathan R. AmoryCentre for Equine and Animal Science, Writtle College, Chelmsford,
Essex, United Kingdom
Traditional techniques used to capture New World monkeys, such as net capture,
can induce high levels of acute stress detrimental to welfare. Alternatively, training
nonhuman animals via operant conditioning to voluntarily participate in husbandry
and/or veterinary practices is accepted as a humane process that can reduce stress
and improve welfare. This study details the use of operant conditioning using
positive reinforcement training (PRT) and target training to train a family of
5 captive red-bellied tamarins (Saguinus labiatus) in a wildlife park to voluntarily
enter a transportation box and remain calm for 1 min after 54 training sessions.
Observations of 2 unrelated net-capture processes provided measures of locomotion
and vocalizations as indicators of stress behavior that were compared with those
of the trained tamarins. Net-captured monkeys exhibited rapid erratic locomotion
and emitted long, high-frequency vocalizations during capture whereas the trained
tamarins exhibited minimal locomotion and emitted only 4 brief vocalizations
(root mean square 35 dB) during capture. This indicates that the use of PRT
considerably reduced potential for stress and improved welfare during the capture
and containment of the tamarins.
The impact of husbandry practices, experimental procedures, and environmental
conditions are being assessed in terms of stress and its impact on the welfare
Correspondence should be sent to Jonathan R. Amory, Centre for Equine and Animal Science,
Writtle College, Chelmsford, Essex, CM1 3RR, United Kingdom. Email: jonathan.amory@writtle.
ac.uk
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REDUCING STRESS OF CAPTURE FOR TAMARINS 125
of nonhuman animals in captivity (Bassett & Buchanan-Smith, 2006; Honess
& Marin, 2006). While recognizing that animals in the wild experience stress
as part of their struggle for existence, the Department for Environment, Food
and Rural Affairs (Defra; 2008) states that zoos, in pursuit of high standards
of animal welfare, must minimize such risks; this is particularly highlighted in
relation to transport stress.
In nonhuman primates, stress relating to human-animal interaction has been
reduced in laboratory settings using operant conditioning via positive reinforce-
ment training (PRT) for procedures such as venipuncture in rhesus macaques
(Macaca mulatta) and chimpanzees (Pan troglodytes; Coleman et al., 2008;
Reinhardt, 2003). In common marmosets (Callithrix jacchus), PRT has been
used to reduce behavioral stress indicators following urine collection (Bassett,
Buchanan-Smith, McKinley, & Smith, 2003) and to accelerate the collection
process (McKinley, Buchanan-Smith, Bassett, & Morris, 2003). Likewise, PRT
incorporating target training has been recognized as a technique for reducing
transportation stress in common marmosets (Prescott, Bowell, & Buchanan-
Smith, 2005) and has also been used to train common marmosets to participate
in homecage weighing (McKinley et al., 2003). Such use of PRT meets the
stipulations of Defra (2004), who states that training should be clearly defined
in relation to animal, keeper, and public safety and biased toward providing a
net welfare benefit to the animal.
Nevertheless, in a survey of over half of UK laboratory and breeding es-
tablishments that use and breed primates, Prescott and Buchanan-Smith (2007)
found that training programs were not widely adopted. To date, most studies have
involved laboratory-housed nonhuman primates (McKinley et al., 2003; Prescott
et al., 2005; Prescott & Buchanan-Smith, 2007) with far fewer published zoo-
based studies (Colahan & Breder, 2003; Savastano, Hanson, & McCann, 2003).
This study was inspired by a real need in Paradise Wildlife Park (PWP) in
Hertfordshire, United Kingdom, where the plan was to transport a family of five
red-bellied tamarins, including a pregnant female, to a different enclosure in
September 2008. The tamarins had previously been moved from their enclosure
on three separate occasions. Each move had involved prolonged net-capture
procedures resulting in stress indicators of atypical and frequent high-pitched
“screaming,” rapid and erratic locomotion, and aggression from the dominant
male. Therefore, training the tamarins to voluntarily enter and remain calm for
1 min in a locked transportation box would avoid (to the benefit of their welfare)
the stress of net capture. Activities included observational studies followed by
the design, implementation, and evaluation of a PRT plan, including individual
target training.
To ascertain whether PRT can reduce stress, physiological and/or behavioral
measures of stress are required (Maestripieri, Hoffman, Anderson, Carter, &
Higley, 2009). However, when studying timid animals, a sample collection of
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126 OWEN AND AMORY
physiological indicators of stress may itself induce stress and thus confound
results, making behavioral measures of stress a requirement. Behavioral indi-
cators such as quantitative measures of stress-induced vocalizations in rodents
and animals on the farm (Moura et al., 2008; Sánchez, 2003) and increased
locomotion in callitrichids (Barros, de Souza-Silva, Huston, & Tomaz, 2004;
Bassett et al., 2003) have both been identified as noninvasive measures of stress.
Nevertheless, analysis of vocalizations as an indicator of stress is relatively
novel, particularly so within zoo collections. Indeed, Defra’s (2008) analysis
of vocalizations is not listed as an assessment tool. Due to the timid nature
of red-bellied tamarins, this study applied behavioral measures of stress. These
included analysis of vocalizations during capture: the number, nature, intensity,
and frequency of vocalizations as well as locomotion observations. Data were
compared with the same measures taken for monkeys captured using traditional
net-capture techniques.
METHOD
Behavioral observations were made by a single observer (Y.O.) using instanta-
neous scan sampling. Training was conducted using operant conditioning via
positive reinforcement and target training. This study was approved by the
Writtle College Ethics Committee and complies with guidelines for ethical
treatment of animals in applied animal behavior and welfare research prepared
by the International Society for Applied Ethology Ethics Committee (2002).
Study Tamarins
The animals in the study were a family of 5 red-bellied tamarins including
Keira, a breeding female (5 years, 11 months old) believed to be 2 months
pregnant, and 4 males. Bruce (4 years old) was the dominant male, followed by
adolescent offspring Tucker and Chan (1 year, 7 months old) and Dominic, a
juvenile (7 months old). All tamarins were captive, mother reared, and had not
experienced any form of training prior to this study.
Housing
The tamarins were housed in an enclosure with both indoor and outdoor access.
The indoor enclosure (house) was approximately 0.91 m � 1.22 m � 1.22 m
positioned approximately 1.22 m from ground level, containing a substrate of
wood shavings, one heat lamp, two tube radiators, two shelves, and a nest box.
The outdoor enclosure had an irregular shape and was approximately 3 m �
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REDUCING STRESS OF CAPTURE FOR TAMARINS 127
2.74 m; the height was 3.35 m with glass panels up to 2.13 m and wire mesh
for the remaining height. Access between the house and outdoor enclosures was
via an opening with PVC strip curtains.
Transport-Box Habituation
As the tamarins had previous negative experience with transportation cages, a
transportation box was constructed for the purpose of the training. The box
was made from marine wood (2400� 2400, 61 cm � 61 cm) with wire-mesh
windows on two end doors and a steel handle for carrying. All tamarins could
be transported as a group in the box or, using a divider, they could be separated
during transport if necessary.
At the end of Training Session 9, the box was placed on a shelf containing
a small handful of Trio Munch (Special Diets Services) to allow the tamarins
to habituate to the box prior to its use. The box was modified after Training
Session 31 to include two windows on one side, as shown in Figure 1, to facilitate
training.
Shaping Plan
The goal behavior was to have the tamarins voluntarily enter a transportation
box and remain calm while confined for 1 min. A shaping plan was developed
FIGURE 1 Modified transportation box.
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TABLE 1
Shaping Plan Showing Approximation Goals and the
Number of Training Sessions Required for All Five Tamarins to
Achieve Each Goal Together With the Cumulative Number of
Training Sessions Toward the Training Goal
No. Training Approximation Goal
No. of Training
Sessions Required
Cumulative Number
of Training Sessions
1 Accept hand-feeding with use of clicker and
stating name of tamarin
7 7
2 Hand-feeding with 3 s delay before reward 1 8
3 Move to and touch target with reward behind
target
4 12
4 Move and touch target with reward from
other hand
4 16
5 Touch target with reward delay of 3 s 1 17
6 Touch target inside box 9 26
7 Establish reward zones outside of box (failed) 3 29
8 Reestablish approximation goal six 2 31
9 Touch target inside box with doors half shut 3 34
10 Touch target inside box with doors three
quarters shut
6 40
11 Touch target inside box with side doors
closed
13 53
12 Remain calm within locked transportation
box for 30 s
4 57
Goal Remain calm within locked transportation
box for 1 min
3 60
Extended training until actual transportation
date
5 65
based on best practice training recommendations by Prescott and Buchanan-
Smith (2007) and incorporating Colahan and Breder’s (2003) planning stages; it
included 12 behavioral approximations toward the goal behavior (Laule, Bloom-
smith, & Shapiro, 2003) as shown in Table 1.
TRAINING SESSIONS
Training sessions were less than 10 min in duration. Twenty-five days were
available to train the tamarins; however, without advance knowledge of how long
the training goal would take to achieve, training sessions were initially scheduled
three times a day (Session A at 08:15, Session B at 09:45, and Session C at
11:15) Mondays through Fridays. On occasion, some flexibility of rewards or
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materials was necessary. Where session goals were not met, regression to a
previous session goal was required (Prescott et al., 2005).
At the beginning of each training session, notices were posted requesting
silence of zoo visitors; an Olympus DM-20 digital voice recorder was secured
to the enclosure door and activated. A commercial “clicker” was used as the
primary bridge. Individual targets were constructed of wood in different shapes;
where appropriate, holes were drilled to enable the tamarins to hold the targets.
Food as a Training Reward
Behavioral observations were conducted to determine which of the foods in
the animals’ normal diets were consumed first. These foods were assumed to
be highly preferred foods and were used during training sessions. The most
commonly used food rewards during training were apple or Mini Marex (Special
Diets Services) soaked in apple juice and refrigerated overnight. Other food
rewards used on occasion included melon, grape, pear, and Mini Marex dipped
in marmoset gum.
Data Collection
During training, individual tamarins were required to achieve the appropriate
approximation goal four consecutive times in a training session to achieve a
maximum session score of 100%. When a session goal was not achieved, a
score of 0% was given, and when goals were performed once, twice, or three
consecutive times, scores of 25%, 50%, and 75%, respectively, were given. Each
training session was documented and evaluated.
In addition to data collection from training sessions, observations were made
of the net capture and containment of a single, unrelated female red-bellied
tamarin (housed separately) for transportation to a zoo and of the net capture and
containment of 5 common marmosets (Callithrix jacchus) for transportation to
another site. Capture duration was timed, locomotion activity was observed, and
vocalizations were recorded for analysis as indicators of stress. Vocalizations
emitted during the capture processes were recorded on an Olympus DM-20
digital voice recorder, set at 44,100 Hz, 16 bit mono. The number and nature of
vocalizations emitted during all capture processes were quantitatively evaluated
to compare stress levels.
Data Analysis
Because this case study did not include a control group, inferential statistics
could not be applied; thus, descriptive statistics (counts, percentages, mean, and
mode) were used. The vocalization-sound files were computer analyzed using
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Sound Forge 6.0 set to a standard Blackman-Harris algorithm over a dB range of
�100 to 0 and a frequency range of 20 to 20,000 Hz. The intensity and frequency
of calls emitted during 20 s of actual containment in a net and, for the trained
tamarins, in the transportation box, were analyzed in terms of minimum and
maximum recordings of amplitude (decibels) and frequency (Hertz). In addition,
the root mean square (RMS) power of each recording was compared to provide
a measure of sound intensity over time corresponding to the loudness of the
sound perceived by human hearing (Sony, 2006).
RESULTS
Transport-Box Habituation
When the transportation box was placed in the outdoor enclosure, all 5 tamarins
immediately investigated, located the food inside, and were observed feeding
and playing in and around the box.
Training
The training goal was first achieved for all 5 tamarins during Training Session 54
after a total of 9 hr of training, although training continued for 65 sessions to
meet the needs of PWP’s actual transportation date. Overall scores for all the
training sessions combined ranged from 64% achieved by Bruce (dominant male)
to 90% achieved by Dominic (juvenile male).
Training using individual targets enabled each tamarin to be positioned in the
enclosure and in different sides of the transportation box. Vocalizations during
training sessions were described as “chirps,” “chirrups,” and “whistles” lasting
an average of 0.1 s and “trills” lasting an average 1.2 s. The RMS power for all
calls during training was �29.2 dB.
Capture Duration
The duration of each capture process, and the average capture duration time for
each monkey, is provided in Table 2.
Vocalizations During Capture
An overview of the nature, number, and duration of vocalizations emitted per
capture process is provided in Table 3. During net capture, the single net-captured
tamarin emitted both long calls �1 s (“screams”) and short calls <1 s (“cheets”).
The 5 marmosets emitted short calls (“tsiks” and “chatters”), whereas the trained
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REDUCING STRESS OF CAPTURE FOR TAMARINS 131
TABLE 2
Duration of Capture Processes
Capture Group
Total Duration
of Capture
(Seconds)
Average Capture Time
per Monkey
(Seconds)
Net capture of single S. labiatus (0.1.0) 263 263.0
Net capture of five C. jacchus (2.1.2) 217 43.4
Voluntary capture of five S. labiatus (3.1.1) 170 34.0
TABLE 3
Vocalizations Emitted From Monkeys During Capture Process
Capture Process
Number of
Long Calls
(�1 s)
Number of
Short Calls
(<1 s)
Average Number
of Short Calls
per Monkey
Average Number
of Calls When
Captured
Net capture of single
S. labiatus (0.1.0)
51 27 27 22
Net capture of five
C. jacchus (2.1.2)
0 237 49.4 10
Voluntary capture of five
S. labiatus (3.1.1)
0 176 36.0 4
tamarins emitted short calls (“chips”) lasting 0.1 s. During actual transportation
to a new enclosure, the trained tamarins did not emit any vocalizations; once
released, the tamarins were observed eating within 60 s.
The single net-captured tamarin struggled in the net for 20 s, emitting long
calls throughout, whereas each of the marmosets was contained in the net
for an average of 2 s, emitting short calls. Conversely, the trained tamarins
voluntarily entered the transportation box, emitting only four short calls over
6.5 s. Waveforms of these vocalizations are provided in Figure 2. Spectrum
analysis of vocalizations recorded for each capture process are provided in
Table 4, which illustrates that net-captured monkeys emitted more intense and
higher frequency calls.
Behavior During Captures
During net capture of the single tamarin, brief periods of stationary locomotion
were observed when she hid in the enclosure furniture. When the net approached,
tamarin locomotion was erratic, involving bouts of rapid locomotion at speeds
difficult to track visually. Several collisions with enclosure glass and furniture
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FIGURE 2 Waveforms of vocalizations during actual capture. 1 D Net capture of single
S. labiatus. 2 D Net capture of single C. jacchus. 3 D Voluntary capture of five S. labiatus.
TABLE 4
Spectrum Analysis of Vocalizations During Capture in Net and Voluntary Capture in
Box Showing Decibels (Db) at Frequency (Hz) and Root Mean Square (RMS) Power
Capture Process
Minimum Recording
(dB at Hz)
Maximum Recording
(dB at Hz) RMS Power
Net capture of single
S. labiatus (0.1.0)
�84 dB at 8,542 Hz �26 dB at 4,246 Hz �12.5 dB
Net capture of five
C. jacchus (2.1.2)
�100 dB at 8,895 Hz �37 dB at 6,186 Hz �17.4 dB
Voluntary capture of five
S. labiatus (3.1.1)
�88 dB at 2,213 Hz �48 dB at 905 Hz �35.0 dB
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REDUCING STRESS OF CAPTURE FOR TAMARINS 133
were observed. During net capture of the 5 marmosets, individuals were observed
running, leaping, and changing direction almost effortlessly, only pausing briefly
when the net was not near. Fleeing locomotion was difficult to track visually.
Marmosets not targeted with the net exhibited huddling behavior or hid. During
evasive locomotion, multiple collisions occurred against the enclosure glass
and furniture, and falling from heights was observed. During capture of the
trained tamarins, individuals were observed leaping between branches to access
the transportation box, followed by minimal location in the box (walking or
stationary).
DISCUSSION
This study demonstrated that operant conditioning could be used to train the
study animals to voluntarily enter a transportation box and remain calm while
confined for 1 min. As a result, the trained tamarins did not undergo net capture
when relocated to their new enclosure. Data comparison indicated that training
did reduce the study animals’ potential for stress during capture compared with
the traditional net-capture process.
During capture, marked differences in vocalizations between the trained
tamarins and the net-captured monkeys were identified. Vocalizations from net-
captured monkeys were louder and of higher frequency than those of the trained
tamarins. Although no data exist to link higher frequency vocalizations of red-
bellied tamarins with stress and no direct comparison can be made between
species, high-frequency vocalizations have been established as reliable indicators
of mental or physical distress in pigs (Sus scrofa; Dupjan, Schon, Puppe,
Tuchscherer, & Manteuffel, 2008; Puppe, Schon, Tuchscherer, & Manteuffel,
2005) and have been documented as an indicator of bovine stress during branding
(Watts & Stookey, 1999).
The long “scream” calls (Figure 3) emitted from the single tamarin during
net capture were comparable in frequency to calls recorded in a laboratory
FIGURE 3 Spectrogram of tamarin “scream” call. a D Coates and Poole (1983). b D
This study.
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experiment by Coates and Poole (1983). They observed that screams were
emitted only in stressful situations and directed at humans. The similarity of
vocalizations recorded in this study suggests that the net capture was a stressful
experience.
Vocalizations of the common marmosets also indicated that their net capture
was a stressful experience. Their loud series of brief, descending “tsik” calls
emitted during capture are comparable to the fear response for their species
(Lazaro-Perea, 2001). Conversely, vocalizations of the trained tamarins enclosed
in the box indicated that they did not experience the same levels of stress ex-
perienced by net-captured monkeys. Their vocalizations most closely resembled
unidirectional “seep” calls in response to mildly disturbing stimuli (Coates &
Poole, 1983). Their vocalizations, however, were of lower frequency; further
research is required to ascertain whether they are indeed comparable “seep”
calls or to identify the implications of this difference (Figure 4).
Unlike the net-captured monkeys, the trained tamarins did not display in-
creased locomotive stress behavior, nor did they collide with enclosure furniture
or fall from height. Conversely, the rapid and erratic locomotion of monkeys
undergoing net capture indicated a stress response and is believed to have had
potential to negatively impact on their welfare.
The introduction of the transportation box within the enclosure at the end of
Training Session 9 resulted in instant interest by the entire group who rapidly
(<10 s) investigated and played in and around the box. This supports research
by Hardie and Buchanan-Smith (2000), who identified that, in 51.2% of trials,
S. labiatus touched nonthreatening novel items in <1 min when placed >1 m
from the enclosure floor.
A number of practical challenges were encountered and addressed throughout
the training. For example, additional doors were added to the front of the trans-
portation box to accommodate the trainer’s hand and the targets. As food rewards
were taken from the tamarins’ daily diet, on occasion, a highly preferred food
was used, which resulted in tamarins squabbling and stealing the food reward
of others. In addition, as only heterozygous female tamarins are trichromats
(Osorio, Smith, Vorobyev, & Buchanan-Smith, 2004), distinctive, individually
FIGURE 4 Spectrogram of tamarin “seep” call. a D Coates and Poole (1983). b D This
study.
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REDUCING STRESS OF CAPTURE FOR TAMARINS 135
shaped targets were used instead of color-coded targets. Although individual
target training was not necessary to train the tamarins to voluntarily participate
in their capture, the decision to include this was one of “future-proofing” for
welfare reasons where individuals could be separated out, or captured/contained,
for future veterinary and/or husbandry purposes.
Shapiro, Bloomsmith, and Laule (2003) emphasize that in assessing the
benefits of training, potential trainers want to know how long it takes to shape a
behavior and what effects are experienced by the primates. The training goal for
this case study was achieved in 54 training sessions, equating to 9 hr of training
for 5 tamarins. To our knowledge, there are no published articles documenting
the use of operant conditioning on S. labiatus; consequently, direct comparison
of results cannot be made. However, Savastano et al. (2003) describe PRT of
6 other Saguinus spp. within 10 single-species groups to establish less invasive
husbandry techniques. The number of training sessions required to establish
hand-feeding varied considerably across the groups, taking from 1 to 20 sessions
to complete. This indicates marked differences in training time investment re-
quired between different groups of tamarins and across species. Similarly, in this
study, there were clear differences between the training scores achieved between
individuals, the reasons for which are not known. As all 5 tamarins were required
to achieve approximation goals four consecutive times in a training session
prior to progression, this affected the total number of training sessions required.
Furthermore, individual target training added complexity where tamarins were
required to recognize and respond to their unique target. This is also believed
to have increased the number of training sessions required.
It is possible that a different trainer and/or group of tamarins may realize
a difference in time investment toward their training goal, as demonstrated by
Savastano et al. (2003). It can also be argued that net captures are relatively
quick and in no way compare with the time investment needed to train nonhuman
primates. However, as highlighted by McKinley et al. (2003), Reinhardt (2003),
Prescott and Buchanan-Smith (2007), and others, PRT can be employed to
facilitate a range of husbandry, welfare, and veterinary procedures for captive,
nonhuman primates to whom we have a duty of care.
The results from this study indicate that using operant conditioning with PRT
considerably reduced potential for stress during capture for the trained tamarins,
indicating a net welfare benefit—perhaps especially so for Keira, the breeding
female who was pregnant at the time of capture.
CONCLUSION
Operant conditioning using PRT is recognized as a humane and valuable tool
that can be used to reduce anxiety, distress, and fear in primates and can
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facilitate husbandry, veterinary, and laboratory procedures over more traditional,
stressful methods. This case study demonstrated that it was possible to use
operant conditioning to train a family of five S. labiatus to voluntarily enter
a transportation box and remain calm for 1 min. Where net-captured monkeys
exhibited rapid and erratic locomotion and emitted long, high-frequency calls
during capture, the trained tamarins exhibited minimal locomotion and emitted
only four, brief, low-frequency vocalizations. The tamarins’ calls indicated a
reduction in their perceived stress and, therefore, an improvement in their welfare
while undergoing a relocation process.
ACKNOWLEDGMENTS
We thank the staff at Paradise Wildlife Park who enabled this research, in
particular Lynn Whitnall (Director), Gary Watts (Head Keeper of Primates),
and Steve Goodwin (Deputy Head Keeper of Primates).
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