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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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134 OWEN AND AMORY

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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