gorilla gorilla) to videos silverback gorillas (gorilla ... · 98 maloney, leighty, kuhar,...
Post on 10-Feb-2020
29 Views
Preview:
TRANSCRIPT
This article was downloaded by: [Dr Kenneth Shapiro]On: 09 June 2015, At: 08:58Publisher: RoutledgeInforma Ltd Registered in England and Wales Registered Number: 1072954Registered office: Mortimer House, 37-41 Mortimer Street, London W1T 3JH,UK
Journal of Applied AnimalWelfare SciencePublication details, including instructions forauthors and subscription information:http://www.tandfonline.com/loi/haaw20
Behavioral Responses ofSilverback Gorillas (Gorillagorilla gorilla) to VideosMargaret A. Maloney a , Katherine A. Leighty a ,Christopher W. Kuhar b & Tamara L. Bettinger aa Disney's Animal Kingdom® , Lake Buena Vista,Floridab Cleveland Metroparks Zoo , Cleveland, OhioPublished online: 26 Mar 2011.
To cite this article: Margaret A. Maloney , Katherine A. Leighty , Christopher W.Kuhar & Tamara L. Bettinger (2011) Behavioral Responses of Silverback Gorillas(Gorilla gorilla gorilla) to Videos, Journal of Applied Animal Welfare Science, 14:2,96-108, DOI: 10.1080/10888705.2011.551621
To link to this article: http://dx.doi.org/10.1080/10888705.2011.551621
PLEASE SCROLL DOWN FOR ARTICLE
Taylor & Francis makes every effort to ensure the accuracy of all theinformation (the “Content”) contained in the publications on our platform.However, Taylor & Francis, our agents, and our licensors make norepresentations or warranties whatsoever as to the accuracy, completeness,or suitability for any purpose of the Content. Any opinions and viewsexpressed in this publication are the opinions and views of the authors, andare not the views of or endorsed by Taylor & Francis. The accuracy of theContent should not be relied upon and should be independently verified withprimary sources of information. Taylor and Francis shall not be liable for anylosses, actions, claims, proceedings, demands, costs, expenses, damages,and other liabilities whatsoever or howsoever caused arising directly or
indirectly in connection with, in relation to or arising out of the use of theContent.
This article may be used for research, teaching, and private study purposes.Any substantial or systematic reproduction, redistribution, reselling, loan,sub-licensing, systematic supply, or distribution in any form to anyone isexpressly forbidden. Terms & Conditions of access and use can be found athttp://www.tandfonline.com/page/terms-and-conditions
Dow
nloa
ded
by [
Dr
Ken
neth
Sha
piro
] at
08:
58 0
9 Ju
ne 2
015
JOURNAL OF APPLIED ANIMAL WELFARE SCIENCE, 14:96–108, 2011
Copyright © The Walt Disney Company®
ISSN: 1088-8705 print/1532-7604 online
DOI: 10.1080/10888705.2011.551621
Behavioral Responses of SilverbackGorillas (Gorilla gorilla gorilla)
to Videos
Margaret A. Maloney,1 Katherine A. Leighty,1
Christopher W. Kuhar,2 and Tamara L. Bettinger1
1Disney’s Animal Kingdom®, Lake Buena Vista, Florida2Cleveland Metroparks Zoo, Cleveland, Ohio
This study examined the impact of video presentations on the behavior of 4 silver-
back, western lowland gorillas (Gorilla gorilla gorilla). On each of 5 occasions,
gorillas viewed 6 types of videos (blue screen, humans, an all-male or mixed-
sex group engaged in low activity, and an all-male or mixed-sex group engaged
in agonistic behavior). The study recorded behavioral responses and watching
rates. All gorillas preferred dynamic over static videos; 3 watched videos depicting
gorillas significantly more than those depicting humans. Among the gorilla videos,
the gorillas clearly preferred watching the mixed-sex group engaged in agonistic
behavior; yet, this did not lead to an increase in aggression or behavior indicating
agitation. Further, habituation to videos depicting gorillas did not occur. This
supports the effectiveness of this form of enrichment, particularly for a nonhuman
animal needing to be separated temporarily due to illness, shipment quarantine,
social restructuring, or exhibit modification.
A wide variety of enrichment activities have been used to stimulate nonhuman
animals both physically and psychologically in research laboratories, zoos, and
sanctuaries (McCann et al., 2007). These activities historically include climbing
devices such as perches and objects the animals can manipulate such as toys,
puzzle-feeders, and varying edibles. More recently, the use of videos as enrich-
ment or operant rewards has been evaluated for a variety of nonhuman primate
Correspondence should be sent to Katherine A. Leighty, Disney’s Animal Kingdom®, P.O. Box
10,000, Lake Buena Vista, FL 32830. Email: Katherine.Leighty@Disney.com
96
Dow
nloa
ded
by [
Dr
Ken
neth
Sha
piro
] at
08:
58 0
9 Ju
ne 2
015
SILVERBACK GORILLA REACTIONS TO VIDEOS 97
species living in different captive conditions (Bloomsmith, Keeling, & Lambeth,
1990; Lutz & Novak 2005; Morimura, 2006). For enrichment techniques to be
effective, they must encourage species-appropriate behavior as well as provide
the animals with opportunities to make choices or otherwise exert control over
their environment (Mellen & MacPhee, 2001). Given that primates as an order
are highly visually oriented (Napier & Napier, 1985), video presentations can
potentially stimulate their innate observing responses while also allowing them
to control their exposure to video content by either turning away or relocating
to a different area of their environment.
Interest in video stimuli has been observed in several monkey species. For
example, Andrews and Rosenblum (1993) found that color video images were
as effective as banana pellets to reinforce bonnet macaques (Macaca radiata)
working on joystick tasks. Further, Platt and Novak (1997) found when video was
presented for enrichment purposes, rhesus monkeys (Macaca mulatta) watched
the monitor 25% of the time and demonstrated an overall increase in activ-
ity level. Butler (1961) discovered that the content and quality of the image
presented to the animal affects visual attention; specifically, rhesus macaques
were found to watch dynamic images preferentially over static ones and images
that were in focus rather than blurred. Further, both pigtail macaques (Macaca
nemestrina) and bonnet macaques have been observed to give socially appro-
priate responses to videos depicting threatening and nonthreatening conspecifics
(Capitanio, Boccia, & Colaiannia, 1985; Plimpton, Swartz, & Rosenblum, 1981).
Given this documented interest in video stimuli, it has been recommended
as a method of enrichment for a variety of nonhuman primate species (Lutz &
Novak, 2005; Morimura, 2006). In a study of the effectiveness and behavioral
implications of presenting video to chimpanzees in captivity (Pan troglodytes),
Bloomsmith and colleagues displayed videos of varied content including other
chimpanzees, other animals, their human caretakers, television programs, or a
blank screen as a control (Bloomsmith et al., 1990). The chimpanzees were
found to watch videos of humans and chimpanzees significantly more than the
static control, and they attended to the monitor 42% of the time during the
dynamic videos. More specifically, all subjects preferred videos of chimpanzees
engaged in agonistic behaviors (chasing, threatening, contact aggression) over
all other behavior categories including feeding, playing, and grooming. The
subjects did demonstrate some degree of habituation to the videos with repeated
presentations; however, their watching rate remained substantial.
Other than visually attending to these videos, analyses revealed no signifi-
cant deviations from subjects’ typical daily behavioral repertoire during video
presentation (Bloomsmith & Lambeth, 2000). Brent and Stone (1996) further
demonstrated the utility of televised images as an enrichment technique. They
found that a television was the most frequently utilized device by chimpanzees
when presented with an array of enrichment items over a prolonged period.
Dow
nloa
ded
by [
Dr
Ken
neth
Sha
piro
] at
08:
58 0
9 Ju
ne 2
015
98 MALONEY, LEIGHTY, KUHAR, BETTINGER
Less has been documented about the potential value of video as enrichment
for gorillas, but Maple and Hoff (1982) did present western lowland gorillas
(Gorilla gorilla gorilla) at the Sacramento Zoo with a 16-mm film depicting
gorillas copulating in an attempt to stimulate breeding. Their objective was not
achieved; however, the gorillas did attend to the video. The silverback responded
to specific content including loud noises. Building from these observations, one
aim of the present study was to determine the effectiveness of video presentation
as a form of enrichment for silverback gorillas.
For more than 10 years, Disney’s Animal Kingdom® has maintained two
social groupings of western lowland gorillas: a mixed-sex troop currently con-
sisting of one silverback and three adult females and an all-male troop of four
adult silverback males. During the day, these two social groups are housed
in separate naturalistic outdoor habitats (1765.16 m2 and 2601.29 m2) that
face each other. This allows visual, olfactory, and auditory access between
groups. Previous research has suggested that exhibit designs such as this may
affect the dynamics of all-male groups by increasing noncontact aggression
(Stoinski, Kuhar, Lukas, & Maple, 2004). Therefore, a second focus of this
study was to determine whether the silverbacks of the all-male troop would
respond differently to video of the mixed-sex troop compared with their own.
Modeling the work of Bloomsmith et al. (1990), we presented these animals
with an array of videos and documented their attention and other behavioral
responses.
METHOD
Subjects and Housing
Four silverback western lowland gorillas at Disney’s Animal Kingdom®, ages
15 to 27 years, served as subjects for this study (see Table 1). Testing sessions
were conducted in the mornings while the gorillas were individually housed in
their overnight sleeping quarters. These holding areas vary in size from 51 to
76.5 m3 and have front panels made of 5 � 5 cm galvanized mesh. Each area
TABLE 1
Gorilla Demographics
Name Age at Start of Study Relevant Rearing History
G 27 Hand reared in absence of gorillas
K 17 Mother reared
Z 17 Mixed rearing
S 15 Mixed rearing
Dow
nloa
ded
by [
Dr
Ken
neth
Sha
piro
] at
08:
58 0
9 Ju
ne 2
015
SILVERBACK GORILLA REACTIONS TO VIDEOS 99
contains a skylight to let in fresh air with a galvanized mesh barrier from which
enrichment items are attached to encourage climbing and foraging behaviors.
Situated throughout the room are benches of varying heights and stainless steel
platforms that provide elevated resting areas and locations on which the gorillas
can build nests from bedding materials. Prior to each session the gorillas were
fed their normal morning portion of primate chow. At the completion of data
collection and the remainder of the morning’s husbandry routine, all subjects
were given access to their shared outdoor naturalistic yard.
Materials
A cart containing a 21-in. (53.3-cm) color television (Sony Trinitron) was
wheeled in front of the gorilla and one of six 10-min videos was played (Table 2).
All videos were played without sound to control for this potential confound. Each
10-min gorilla video showed a collection of short video clips edited together of
either the all-male group or the mixed-sex group at Disney’s Animal Kingdom®.
For each of the four gorilla videos, each member of the group depicted was
presented on screen for equal amounts of time to control for differential response
to specific individuals. Behavioral observations of the gorillas were conducted
using the Observer® XT (Noldus, Leesburg, VA) program on an iPAQ (Hewlett-
Packard, #HX2495B, Palo Alto, CA).
Procedure
To allow for acclimation, the gorillas were introduced to the cart, television,
and human observer several times before the study began. Testing sessions were
conducted 5 days per week from September through December 2008 between
TABLE 2
Video Types and Content
Videos Description
Blue screen Control video
Humans Depicting park guests
All-male group, low activity Members of the all-male troop exhibiting behaviors such
as eating, walking, and being inactive
Mixed-sex group, low activity Members of the mixed-sex troop exhibiting behaviors such
as eating, walking, and being inactive
All-male group, agonistic Members of the all-male troop exhibiting behaviors such
as chest beating, standing in a stiff stance, and chasing
Mixed-sex group, agonistic Members of the mixed-sex troop exhibiting behaviors such
as chest beating, standing in a stiff stance, and chasing
Dow
nloa
ded
by [
Dr
Ken
neth
Sha
piro
] at
08:
58 0
9 Ju
ne 2
015
100 MALONEY, LEIGHTY, KUHAR, BETTINGER
TABLE 3
Ethogram Used During Gorilla Observations
Behaviors Definition
Charge Run in a swift and aggressive manner
Chest beating Rapid striking of the chest/abdomen using the hands
Eat/Forage Consume or search for food, drink water
Flee Rapid distancing from monitor
Locomote Movement from one area to another by walking
Pacing Repetitive locomotion occurring at least two times in a row
Play Use of enrichment device in enclosure
Pursed lips Puffed out upper and lower lip areas
Self-groom Visually inspect, lick, or scratch own body
Slap/Bang Body contacts part of the enclosure aggressively
Stiff stance Rigid body with forearms stiff and close together, hands formed tightly
with fingers curled in, standing on knuckles
Throw object Launch object into the air
Undesirable Coprophagy, regurgitate and reingest
Vocalize Emit audible vocal sound
Watching Gaze is directed at the monitor
Not visible behavior Gorilla is out of the observer’s view
Other Behavior observed is not defined in the ethogram
the hours of 0730 and 0800. Each morning, 2 of the 4 gorillas were randomly
selected to participate one at a time in the study. The order of video presentation
was randomized such that each gorilla viewed each of the six videos on five
separate occasions, resulting in 30 testing sessions with each gorilla. During all
of the sessions, the observer stood out of direct view of the gorillas and did not
interact with them at any point. While the video played, the observer recorded
the frequency and duration of behavioral responses (Table 3).
Analyses
To examine all behaviors exhibited during video presentation (with the exception
of “watching”), the time spent engaged in each behavior was calculated as
a proportion of the time the animal was visible to the observer. The time
spent “watching” the video was calculated as a proportion of the 10-min video
duration. The mean of these values was calculated for each subject for each of
the six video types.
A dependent t test was used to determine if subjects differed in the pro-
portion of time spent (a) watching dynamic videos (all video types except
the blue screen) compared with the static ones (blue screen) and (b) watching
videos depicting gorillas (four gorilla videos) compared with humans. For these
Dow
nloa
ded
by [
Dr
Ken
neth
Sha
piro
] at
08:
58 0
9 Ju
ne 2
015
SILVERBACK GORILLA REACTIONS TO VIDEOS 101
analyses, the parametric test was selected because it is not possible to obtain
a significant result with the corresponding nonparametric test given that only
4 subjects contributed data (lowest possible p value with 4 subjects is .068
for this test). This fact will be considered when drawing conclusions from this
data. A 2 � 2 Factorial ANOVA was used to examine the impact of social
group depicted (all-male vs. mixed-sex) and behavioral content (low activity vs.
agonistic) on time spent watching gorilla videos.
To control for individual differences in overall video-watching time in this
analysis, the z score of each individual’s mean proportion of video watching for
each video type was used in the analysis. This transformation had the additional
outcome of increasing normality within the data set. Visual inspection of the
time spent watching videos over repeated presentations was used to determine
whether habituation took place. All statistical tests were two-tailed with alpha
set at 0.05 and conducted with SPSS 15.0 (Chicago, IL).
Activity During Video Presentation
The proportion of time engaged in each behavior category during video presen-
tation is displayed in Figure 1. Of all behaviors, subjects spent the most time
FIGURE 1 Proportion of time each gorilla spent engaged in the recorded behaviors when
shown the static blue screen, human, and gorilla videos.
Dow
nloa
ded
by [
Dr
Ken
neth
Sha
piro
] at
08:
58 0
9 Ju
ne 2
015
102 MALONEY, LEIGHTY, KUHAR, BETTINGER
watching the television monitor, with the exception of the blue-screen control
condition in which subjects spent less time watching the monitor than they did
eating/foraging. For ease of presentation, all behaviors in the ethogram reflecting
agonistic or agitated responses to the videos were grouped into a single category
entitled “agonistic/agitation.” The category included charge, chest beating, flee,
pacing, pursed lips, slap/bang, stiff stance, and throw object. These behaviors
were not demonstrated at a substantial rate to any of the video types. Visual
inspection of the behavioral data revealed that no behaviors were remarkably
altered between the static video control condition and the videos depicting human
or gorilla content with the exception of the degree to which the video was
watched by the subject.
Watching of Static Versus Dynamic Videos
The mean proportion of the video watched for the static blue-screen control video
ranged from 0.008 (S) to 0.172 (G) with a mean across subjects of 0.060 ˙
.038. For the dynamic videos, subjects ranged from 0.296 (G) to 0.711 (S) with
a mean proportion of the video watched of 0.547 ˙ .089. Thus, the subjects
spent significantly more time watching videos containing dynamic images than
the static blue control screen (t (3) D �3.859, p D .031; see Figure 2).
FIGURE 2 Proportion of time each gorilla was visible to the observer that was spent
watching the static and dynamic videos.
Dow
nloa
ded
by [
Dr
Ken
neth
Sha
piro
] at
08:
58 0
9 Ju
ne 2
015
SILVERBACK GORILLA REACTIONS TO VIDEOS 103
RESULTS
Watching of Human Versus Gorilla Videos
When shown the video depicting humans, the mean proportion of the video
watched ranged across subjects from 0.339 (G) to 0.504 (S) with a mean of
0.405 ˙ .035. For the videos depicting gorillas, subjects ranged from 0.286 (G)
to 0.763 (S) with a mean proportion of the video spent watching of 0.583 ˙ .104.
When analyzing across all subjects, the proportion of the video watched was
not significantly different across the human and gorilla videos (t (3) D �2.234,
p D .122); yet, 3 of the 4 subjects did watch significantly more of the gorilla
videos than the human video (t (2) D �8.710, p D .013; see Figure 3).
Impact of Gorilla Video Content on Watching Rate
To examine the impact of the behavioral content and social group depicted
on the gorilla videos, the mean proportion of the video watched was cal-
culated for each subject for each of the four gorilla-video types. A 2 � 2
Factorial ANOVA (gorilla social group by behavioral content) of the z scores
of these values revealed a significant main effect for gorilla social group de-
FIGURE 3 Proportion of time each gorilla was visible to the observer that was spent
watching the human and gorilla videos.
Dow
nloa
ded
by [
Dr
Ken
neth
Sha
piro
] at
08:
58 0
9 Ju
ne 2
015
104 MALONEY, LEIGHTY, KUHAR, BETTINGER
FIGURE 4 Proportion of time all gorillas spent watching the video as a function of social
group depicted (all-male or mixed-sex) and behavioral content (low activity or agonistic).
picted (F(1) D 4.916, p D .047) with the subjects watching videos of the
family group (nontransformed M D 0.623, SE D 0.090) over those of the
bachelor group (nontransformed M D 0.543, SE D .077). A significant main
effect was also present for the behavioral content of the gorilla videos (F(1)
D 21.582, p D .001) with the subjects watching videos of agonistic behavior
(nontransformed M D 0.673, SE D 0.092) over those depicting low-activity
behavior (nontransformed M D 0.492, SE D 0.061). A significant interaction
was present between social group depicted and behavioral content (F(1) D
6.626, p D .024) with the video depicting the family group engaged in agonistic
behavior to be the most attended to (nontransformed M D 0.757, SE D 0.138;
see Figure 4).
Habituation to Videos
Visual inspection of the time spent watching the videos over repeated presen-
tations revealed marked habituation to the human videos over time, such that
there was a 74% decrease in time spent watching between the first and fifth
presentation of the human video. Habituation was not evident in the subjects’
watching of gorilla videos (Figure 5).
Dow
nloa
ded
by [
Dr
Ken
neth
Sha
piro
] at
08:
58 0
9 Ju
ne 2
015
SILVERBACK GORILLA REACTIONS TO VIDEOS 105
FIGURE 5 Mean number of seconds all gorillas spent watching the 10-min human and
gorilla videos across five presentations.
DISCUSSION
As seen in other primate species, these silverback gorillas demonstrated a high
level of interest in video presentations. This novel change to their environment
appeared to be engaging for these animals as they spent a large proportion of
their time visually focused on the video. Dynamic videos displaying human and
gorilla content resulted in significantly higher watching rates compared with
the static blue-screen control video, demonstrating that the gorillas were clearly
attending to the content of the videos (Figure 2). This preference for dynamic
images reinforces similar findings in chimpanzees (Bloomsmith et al., 1990) and
rhesus macaques (Butler, 1961).
The species depicted in the dynamic videos also had a significant impact
on the engagement of the gorillas. Three of the 4 subjects had a significant
preference for watching videos of gorillas over humans (Figure 3). This may in-
dicate the potential for gorillas to selectively attend to their own species. Similar
selective attention within species has been seen in facial recognition processing
of both humans and nonhuman primates (Neiworth, Hassett, & Sylvester, 2007;
Dow
nloa
ded
by [
Dr
Ken
neth
Sha
piro
] at
08:
58 0
9 Ju
ne 2
015
106 MALONEY, LEIGHTY, KUHAR, BETTINGER
Pascalis & Bachevalier, 1988). It is interesting that the 1 animal in this study who
did not prefer the gorilla videos, G, has a rearing history unique from the other
subjects (Table 1). G was rejected by his mother soon after birth and required
hand rearing. Because of husbandry demands, this hand rearing was conducted
out of visual contact with other gorillas. Thus, his response to these videos may
reflect his early exposure to humans and lack of early experience to gorillas.
Further, G was also the oldest of the 4 subjects in this study, and his watching
rates across all video types were lower than those of the other animals. On the
other hand, S, the youngest animal observed, had the highest watching rates.
This may suggest a negative relationship between age and attention to videos,
with older animals having a reduced attention span to this form of media. Further
investigation, including a larger sample of animals from a variety of facilities,
will be needed to tease out the impacts of age and early rearing history on
interest in video stimuli in nonhuman primates.
Among the videos depicting gorillas, analyses revealed a significant inter-
action between social group depicted and behavioral content of the video on
the time spent watching. That is, subjects showed a significant preference for
watching gorillas engaged in agonistic behaviors such as chest beating and
charging, particularly when it involved the mixed-sex troop housed in the facing
enclosure (Figure 4). Although this video type did cause more engagement
with the video, it did not lead to the production of agonistic behaviors or
behaviors reflecting agitation, such as fleeing or pacing during the observation
period (Figure 1). Thus, it appears that the subjects recognize alteration in
behavioral and social content; however, they do not respond to it in any way other
than adjusting their level of visual attention. Recent studies with chimpanzees
have shown that they are able to comprehend the representational relationship
between 2D video images and the 3D world without confusing the two (Leighty,
Menzel, & Fragaszy, 2008; Menzel, 2005). That is, they do not react to video
presentations as if they were actual 3D events; rather, they are able to use them
as a tool to gain information about their 3D environment such as the location
of a hidden food item. It is likely the case here that the gorillas comprehend
that the images they are viewing on the 2D monitor are only representations
of real-world events and that they are not actually occurring in the present
time.
There was no apparent decline in the subject’s watching rates to the four
gorilla videos with repeated presentation. Thus, there was no evidence of these
subjects habituating to the content of these videos over five viewings. On the
other hand, a clear habituation effect was seen to the video depicting humans,
with a particularly sharp decline following the third presentation (Figure 5).
Taken together, these findings reiterate the notion that these animals are stimu-
lated by watching video of their own species. We therefore conclude that video
depicting gorilla behavior is a valuable and cost-effective enrichment tool that
Dow
nloa
ded
by [
Dr
Ken
neth
Sha
piro
] at
08:
58 0
9 Ju
ne 2
015
SILVERBACK GORILLA REACTIONS TO VIDEOS 107
promotes positive welfare. We feel it would be particularly useful in cases when
animals must be temporarily separated due to illness, shipment quarantine, social
restructuring, and/or exhibit modification, and can be a useful component of a
comprehensive enrichment program.
ACKNOWLEDGMENTS
This research would not have been possible without the support and assistance
of the keepers and managers of the Primate Husbandry Team at Disney’s Animal
Kingdom®. We thank James Gash for his assistance with video editing.
REFERENCES
Andrews, M. W., & Rosenblum, L. A. (1993). Live-social video reward maintains joystick task
performance in bonnet macaques. Perceptual and Motor Skills, 77, 755–763.
Bloomsmith, M. A., Keeling, M. E., & Lambeth, S. P (1990). Videotapes: Environmental enrichment
for singly housed chimpanzees. Lab Animal, 19, 42–46.
Bloomsmith, M. A., & Lambeth, S. P. (2000). Videotapes as enrichment for captive chimpanzees.
Zoo Biology, 19, 541–551.
Brent, L., & Stone, A. M. (1996). Long-term use of televisions, balls, and mirrors as enrichment
for paired and singly caged chimpanzees. American Journal of Primatology, 39, 139–145.
Butler, R. A. (1961). The responsiveness of rhesus monkeys to motion pictures. The Journal of
Genetic Psychology, 98, 239–245.
Capitanio, J. P., Boccia, M. L., & Colaiannia, D. J. (1985). The influence of rank on affect perception
by pigtailed macaques (Macaca nemestrina). The American Journal of Primatology, 8, 53–59.
Leighty, K. A., Menzel, C. R., & Fragaszy, D. M. (2008). How young children and chimpanzees (Pan
troglodytes) perceive objects in a 2D display: Putting an assumption to the test. Developmental
Science, 11, 778–792.
Lutz, C. K., & Novak, M. A. (2005). Environmental enrichment for nonhuman primates: Theory
and application. Institute for Laboratory Animal Research, 46, 178–191.
Maple, T. L., & Hoff, M. P. (1982). Gorilla behavior. New York, NY: Van Nostrand Reinhold.
McCann, C., Buchanan-Smith, H., Jones-Engel, L., Farmer, K., Prescott, M., Fitch-Snyder, H., &
Taylor, S. (2007). IPS international guidelines for the acquisition, care, and breeding of nonhu-
man primates. International Primatological Society, Second Edition. Retrieved from http://www.
internationalprimatologicalsociety.org/docs/IPS_International_Guidelines_for_the_Acquisition_
Care_and_Breeding_of_Nonhuman_Primates_Second_Edition_2007.pdf
Mellen, J., & MacPhee, M. S. (2001). Philosophy of environmental enrichment: Past, present, and
future. Zoo Biology, 20, 211–226.
Menzel, C. R. (2005). Progress in the study of chimpanzee recall and episodic memory. In H.
Terrace & J. Metcalfe (Eds.), The missing link in cognition: Origins of self-reflective consciousness
(pp. 188–224). New York, NY: Oxford University Press.
Morimura, N. (2006). Cognitive enrichment in chimpanzees: An approach of welfare entailing
an animal’s entire resources. In T. Matsuzawa, M. Tomonaga, & M. Tanaka (Eds.), Cognitive
development in chimpanzees, (pp. 368–391). Tokyo, Japan: Springer-Verlag.
Napier, J. R. & Napier, P. H. (1985). The natural history of primates. Cambridge, MA: MIT Press.
Dow
nloa
ded
by [
Dr
Ken
neth
Sha
piro
] at
08:
58 0
9 Ju
ne 2
015
108 MALONEY, LEIGHTY, KUHAR, BETTINGER
Neiworth, J. J., Hassett, J. M., & Sylvester, C. J. (2007). Face processing in humans and new world
monkeys: The influence of experimental and ecological factors. Animal Cognition, 10, 125–134.
Pascalis, O., & Bachevalier, J. (1988). Face recognition in primates: A cross-species study. Be-
havioural Processes, 43, 87–96.
Platt, D. M., & Novak, M. A. (1997). Video stimulation as enrichment for captive rhesus monkeys
(Macaca mulatto). Applied Animal Behaviour Science, 52, 139–155.
Plimpton, E. H., Swartz, K. B., & Rosenblum, L. A. (1981). Responses of juvenile bonnet macaques
to social stimuli presented through color videotapes. Developmental Psychobiology, 14, 109–115.
Stoinski, T. S., Kuhar, C. W., Lukas, K. E., & Maple, T. L. (2004). Social dynamics of captive
western lowland gorillas living in all-male groups. Behaviour, 141, 169–195.
Dow
nloa
ded
by [
Dr
Ken
neth
Sha
piro
] at
08:
58 0
9 Ju
ne 2
015
top related