Self-recognition in an Asian elephant
Joshua M. Plotnik, Frans B. M. de Waal, and Diana Reiss
doi:10.1073/pnas.0608062103
published online Oct 30, 2006;
PNAS
This information is current as of October 2006.
Supplementary Material
www.pnas.org/cgi/content/full/0608062103/DC1
Supplementary material can be found at:
This article has been cited by other articles:
E-mail Alerts
at the top right corner of the article or
Receive free email alerts when new articles cite this article - sign up in the box
Rights & Permissions
www.pnas.org/misc/rightperm.shtml
To reproduce this article in part (figures, tables) or in entirety, see:
Reprints
www.pnas.org/misc/reprints.shtml
To order reprints, see:
Notes:
Self-recognition in an Asian elephant
Joshua M. Plotnik*
â€
, Frans B. M. de Waal*
‡
, and Diana Reiss
§¶
储
*Living Links, Yerkes National Primate Research Center, and Department of Psychology, Emory University, Atlanta, GA 30322;
§
Osborn Laboratories of
Marine Sciences, New York Aquarium, Wildlife Conservation Society, Brooklyn, NY 11224; and
¶
Department of Ecology, Evolution, and Environmental
Biology, Columbia University, New York, NY 10027
Contributed by Frans B. M. de Waal, September 13, 2006
Considered an indicator of self-awareness, mirror self-recognition
(MSR) has long seemed limited to humans and apes. In both
phylogeny and human ontogeny, MSR is thought to correlate with
higher forms of empathy and altruistic behavior. Apart from
humans and apes, dolphins and elephants are also known for such
capacities. After the recent discovery of MSR in dolphins (
Tursiops
truncatus
), elephants thus were the next logical candidate species.
We exposed three Asian elephants (
Elephas maximus
) to a large
mirror to investigate their responses. Animals that possess MSR
typically progress through four stages of behavior when facing a
mirror: (
i
) social responses, (
ii
) physical inspection (e.g., looking
behind the mirror), (
iii
) repetitive mirror-testing behavior, and (
iv
)
realization of seeing themselves. Visible marks and invisible sham-
marks were applied to the elephants’ heads to test whether they
would pass the litmus ‘‘mark test’’ for MSR in which an individual
spontaneously uses a mirror to touch an otherwise imperceptible
mark on its own body. Here, we report a successful MSR elephant
study and report striking parallels in the progression of responses
to mirrors among apes, dolphins, and elephants. These parallels
suggest convergent cognitive evolution most likely related to
complex sociality and cooperation.
cognition
å…©
mirror self-recognition
å…©
theory of mind
å…©
intelligence
å…©
empathy
M
irror self-recognition (MSR) is exceedingly rare in the
animal kingdom (1). Attempts to demonstrate MSR out-
side of the Hominoidea (i.e., humans and apes) have thus far
failed (2), with the notable exception of one report on dolphins
(
Tursiops truncatus
) (3). Animals that demonstrate MSR typi-
cally go through four stages: (
i
) social response, (
ii
) physical
mirror inspection (e.g., looking behind the mirror), (
iii
) repet-
itive mirror-testing behavior (i.e., the beginning of mirror un-
derstanding), and (
iv
) self-directed behavior (i.e., recognition of
the mirror image as self) (3, 4). The final stage is verified if a
subject passes the ‘‘mark test’’ by spontaneously using the mirror
to touch an otherwise imperceptible mark on its own body (1).
Application of the mark is recommended only if the preceding
criteria have been met (5). Animals without MSR tend to remain
at stages 1 and 2. Even if the degree to which the mirror image
is confused with a stranger is debatable for some non-MSR
species (6), these animals likely lack understanding of who is in
the mirror.
Gallup was the first to hypothesize about a phylogenetic
connection between MSR and empathy (7), a connection sup-
ported by evidence for consolation behavior in apes but not
monkeys (8, 9). A possible ontogenetic connection between
MSR and empathy is reflected in the coemergence of MSR and
‘‘sympathetic concern’’ during child development (10, 11). Dol-
phins and elephants represent interesting additions to MSR tests
because, like the hominoids (8, 12), they are highly empathic
animals known for so-called ‘‘targeted helping’’ [i.e., helping that
takes the specific needs of others into account (8)] aimed at both
conspecifics and humans. As in dolphins (13, 14), there are
numerous reports of elephants physically supporting or trying to
lift up injured or incapacitated conspecifics (15–17). In view of
the aforementioned hypothetical connection with empathy, the
elephant’s known social complexity (15, 16, 18) and its relatively
large and complex brain (19, 20), we introduced three adult
female Asian elephants (
Elephas maximus
) at the Bronx Zoo in
New York City to a jumbo-size mirror (244
â«»
244 cm) in a variant
of the classical mark test (1) using both visual and ‘‘sham’’
marks (3).
Elephants have the advantage that they can touch most of their
own body with their trunks, thus permitting an unequivocal mark
test. A previous failed attempt to demonstrate MSR in two Asian
elephants presented the animals with a relatively small mirror
that was kept at a distance, well out of trunk-reach (21).
Assuming that physical exploration of the mirror surface should
be part of the learning process (5) and that mirror size matters,
we built an almost 2.5-m-tall elephant-resistant mirror to allow
close-up inspection of the reflective surface (Fig. 1). Here we
demonstrate that all three subjects reached the aforementioned
third and fourth stages of MSR progression and that one subject
passed the mark test.
Results and Discussion
Baseline, Controls, and Initial Mirror Exposure.
There were five
experimental phases: baseline (T1), covered mirror (T2), open
mirror (T3), covered-mirror sham (T4), and the mark test (T5).
Happy, Maxine, and Patty all spent far more time close to the
mirror during 3 days of open vs. covered mirror (i.e., T3 vs. T2;
Happy, 19.4 vs. 0.2%; Maxine, 37.9 vs. 1.3%; and Patty, 49.7 vs.
3.3%), indicating that time spent at the mirror was due to its
reflective qualities rather than to the novelty of the apparatus.
During T3, all three subjects showed investigative behavior of the
mirror surface and frame including touching and probable
sniffing. For Maxine and Patty, trunk-over-wall exploration (i.e.,
the swinging of the trunk over and behind the wall on which the
mirror was mounted) declined from the first through the fourth
day of mirror exposure (Maxine, 10 to 0 times; Patty, 13 to 4
times). Happy never put her trunk over the mirror wall. Maxine
and Patty also attempted to physically climb the mirror wall to
look over and behind it (see Movie 1, which is published as
supporting information on the PNAS web site), and both, on
separate occasions, seemed to try to get their trunks underneath
and behind the mirror by kneeling down in front of it. Their
behavior was highly unusual (i.e., animal-care staff had rarely
observed similar attempts by the elephants to look over or
underneath enclosure walls). Remarkably, all three subjects
showed a total absence of social interaction with their mirror
image, such as species-typical visual, vocal, or agonistic displays
(15, 16, 18, 22).
Author contributions: J.M.P., F.B.M.d.W., and D.R. designed research; J.M.P. and D.R.
performed research; J.M.P., F.B.M.d.W., and D.R. analyzed data; and J.M.P., F.B.M.d.W.,
and D.R. wrote the paper.
The authors declare no conflict of interest.
Abbreviation: MSR, mirror self-recognition.
â€
To whom correspondence may be addressed at: Department of Psychology, 532 North
Kilgo Circle, Emory University, Atlanta, GA 30322. E-mail: jplotni@emory.edu.
‡
To whom correspondence may be addressed. E-mail: dewaal@emory.edu.
储
To whom correspondence may be addressed at: Osborn Laboratories of Marine Sciences,
New York Aquarium, Boardwalk and West 8th Street, Brooklyn, NY 11224. E-mail:
dlr28@columbia.edu.
© 2006 by The National Academy of Sciences of the USA
www.pnas.org
å…¾
cgi
å…¾
doi
å…¾
10.1073
å…¾
pnas.0608062103
PNAS
å…©
November 7, 2006
å…©
vol. 103
å…©
no. 45
å…©
17053–17057
PSYCHOLOGY
All three elephants displayed behavior consistent with mirror-
testing and self-directed behavior during T3 (open mirror) and
T5 (mark test), such as bringing food to and eating right in front
of the mirror (a rare location for such activity), repetitive,
nonstereotypic trunk and body movements (both vertically and
horizontally) in front of the mirror, and rhythmic head move-
ments in and out of mirror view; such behavior was not observed
in the absence of the mirror (see Movie 2, which is published as
supporting information on the PNAS web site, for an example).
On more than one occasion, the elephants stuck their trunks into
their mouths in front of the mirror or slowly and methodically
moved their trunks from the top of the mirror surface downward.
In one instance, Maxine put her trunk tip-first into her mouth at
the mirror, as if inspecting the interior of her oral cavity, and in
another instance, she used her trunk to pull her ear slowly
forward toward the mirror. Because these behaviors were never
observed in T1 or T2 (the initial, ‘‘no mirror’’ control condi-
tions), or at any other time, they indicate the elephants’ tendency
to use the mirror as a tool to investigate their own bodies. Apes
are known for very similar self-investigation in front of the
mirror, such as picking with their fingers at their teeth (1, 23),
which is considered a precondition for the mark test (5). Similar
to the time frame observed in chimpanzees (1), Happy reached
this criterion for the mark test within 3 days, and Maxine and
Patty reached this criterion within 4 days.
The Mark Test.
On the first day of the mark test (T5), a visible
mark (Fig. 2) was applied to the right side of each elephant’s
head, and an invisible sham-mark was applied to the left side of
the head. The sham-mark controlled for both olfactory and
tactile cues (i.e., texture), leaving only a visual component to
differentiate between mark and sham-mark (see
Supporting Text
,
which is published as supporting information on the PNAS web
site, for the chemical composition of the marking substances).
Lone sham-marks had been used previously in T4 to test this
control while avoiding habituation by the other elephant to the
visual component of the mark. The elephants never touched the
sham-mark under this previous condition, suggesting the pre-
dicted absence of odor or tactile cues. A controlled-mark
condition similar to T4, but using the visual mark instead of the
sham-mark in a covered-mirror condition, would have been an
ideal addition to our testing procedure but could not be imple-
mented because of the presence of the elephant’s partner.
Husbandry concerns prevented us from isolating each elephant
during testing; hence any visual mark might have attracted the
partner’s attention and risked the loss of mark salience by the
time actual mark tests were conducted in front of the open
mirror.
One elephant, Happy, passed the mark test on the first day of
marking. Caretakers did not notice her touching either the mark
or sham-mark before being released into the elephant yard.
After being released into the yard, she walked straight to the
mirror where she spent 10 seconds, then walked away. Seven
minutes later she returned to the mirror, and over the course of
the next minute she moved in and out of view of the mirror a
couple of times, until she moved away again. In the following 90
seconds, out of view of the mirror, she repeatedly touched the
visible mark but not the sham-mark. She then returned to the
mirror, and while standing directly in front of it, repeatedly
touched and further investigated the visible mark with her trunk
(see Movie 3, which is published as supporting information on
the PNAS web site).
Combining all experimental phases (T1–T5), Happy touched
her own head with her trunk a total of 47 times. Comparing the
frequency distribution of head touches across three aggregate
conditions [i.e., (
i
) the first mark test, (
ii
) the open-mirror tests
Fig. 1.
Elephant yard with open mirror. A drawing of a typical open-mirror
session (drawing by F. Plotnik from a still taken from the rooftop camera). One
elephant stands at the mirror, while another stands off to the side. The
elephant yard in which the mirror was installed is not visible to the public.
Fig. 2.
Mark and mark-touching. (
A
) Happy with a visual X-shaped mark on
her head, (
B
) Happy at the mirror touching the mark with the tip of her trunk.
This still image was captured from a video camera embedded in the mirror.
The locations of the mark and the sham-mark were counterbalanced on the
left and right side of the elephant’s head on consecutive mark days. Also see
Movies 1–3.
17054
å…©
www.pnas.org
å…¾
cgi
å…¾
doi
å…¾
10.1073
å…¾
pnas.0608062103
Plotnik
et al.
before marking, and (
iii
) all nonmirror conditions combined]
with the expected frequency distribution based on Happy’s
observation time under those three conditions, a significant
difference was found (
â¹
2
⫽
130.83, df
⫽
2,
P
â¬
0.001). On the
mark day itself, Happy showed dramatically increased head
touching early in the session, most of which (i.e., 12 of 14 times;
Fig. 3; measured as rate per minute) occurred during or within
90 seconds after proximity to the mirror. All 12 touches during
or right after mirror exposure came in contact with or close to
(within 20 cm) the visible mark on the right side of Happy’s head.
Head touches never came in contact with or close to the
sham-mark on the left side of Happy’s head (binomial test 12 vs.
0,
z
⫽
3.18,
P
⫽
0.0008). Happy’s right-side vs. left-side bias on
the first mark day differed significantly from that for head
touches on nonmark days (Fisher’s exact test,
P
⫽
0.025). In
other words, Happy’s touching of the right side of her head
(particularly the mark itself) on the first mark day deviated from
her general head touching during all previous conditions in both
its higher frequency and its bias toward the side with the visible
mark. In addition, although female African elephants (
Lox-
odonta africana
) often touch their heads because of temporal
gland secretion (15), female Asian elephants do not; their
temporal gland is bilateral, vestigial, and nonsecretory (24), thus
eliminating concerns about their propensity to touch this area.
Passing and Failing the Mark Test.
In contrast to Happy, Maxine
and Patty failed to show increased self-touching of either the
mark or sham-mark. Maxine and Patty were marked twice;
Happy was marked three times. On the second day of marking,
Happy never approached the mirror nor did she touch either the
mark or sham-mark. She was re-marked on a third day during
which time she stationed herself at the mirror but touched
neither the mark nor the sham-mark. We repeated the marking
procedure on all three elephants after 2 months; none of them
touched either the mark or sham-mark during this second phase
of marking, although all of them continued to show self-directed
behavior at the mirror.
The fact that one elephant passed the mark test but two did not
is not inconsistent with data recorded for other species because
even in the most extensively tested species with MSR, the chim-
panzee (
Pan troglodytes
), fewer than half of the individuals may pass
the test according to some studies (23, 25). Similarly, absence of
responses to the mark after multiple exposures resembles the
reaction of MSR-capable apes, which generally lose interest in the
mark within minutes of mirror exposure, apparently realizing that
the mark is inconsequential (26). For this reason, multiple mark
tests on a single individual are considered to compromise mark
salience and are therefore uninterpretable (5).
Happy, Maxine, and Patty all continued to show self-directed
behavior at the mirror, indicating that they may have only lost
interest in the mark but not in their own reflection. Although we
encourage further testing of Asian elephants, because of the
overexposure of our three elephants to the marking materials
and the descriptions of elephants’ extraordinary memory (15,
16), we would not expect these three elephants to pass during
further rounds of testing.
According to the manufacturer, the ingredients of the mark and
sham-mark material (both face paints) are identical except for the
pigmentation components (see
Supporting Text
); the titanium di-
oxide, which is used to make the mark paint ‘‘white,’’ is odorless
according to its Material Safety Data Sheet (MSDS). The zinc
sulfide, which is used to make the sham-mark paint luminescent,
may have a slight odor, but we would expect that if the zinc sulfide
odor in the sham-mark paint was detectable and differentiated from
the mark by the elephants, they would have been attracted to the
sham-mark rather than the visual mark. However, as our data show,
no such attraction was evident. Therefore, we conclude that the
odor and tactile components of the mark and the sham-mark are
either equal or negligible and that any differential touching of the
mark should be due to its visual component.
The later negative outcomes in all three subjects seem to
confirm the absence of tactile and odor clues of the marks. One
would further suspect a lack of ‘‘concern’’ about bodily appear-
ance and cleanliness in elephants compared with primates.
Whereas primates often groom specific spots on their bodies (27,
28), elephants rarely autogroom with their trunks (29, 30).
Rather, they ‘‘substrate groom,’’ which includes dust-throwing
and mud-bathing (30, 31). This manner of ‘‘grooming’’ actually
adds debris to the body. It may very well be that because of an
elephant’s large body-surface area (29) and the mud and sand it
often carries around on its body, attention to detail is not a
priority. A small paint mark may be trivial to them.
The behavior of the elephants was strikingly similar to that of
other animals who have demonstrated MSR. Although none of the
elephants aimed social behavior at the mirror, they all, like the apes
and dolphins, exhibited exploratory and mirror-testing behavior
before more explicitly self-directed activities. Further studies on
elephants of different ages, gender, and personal history will be
needed to confirm and further elucidate the capacity for MSR in
these animals. Our study suggests that mirror size and access to the
mirror surface should be considered in replication attempts.
The mark-touching by one elephant is compelling evidence
that this species has the capacity to recognize itself in a mirror.
Finding strong parallels among apes, dolphins, and elephants in
both the progression of behavioral stages and actual responses
to a mirror provides compelling evidence for convergent cog-
nitive evolution. Perhaps MSR indexes an increased self–other
distinction that also underlies the social complexity and altruistic
tendencies shared among these large-brained animals.
Materials and Methods
Subjects.
Subjects were adult female Asian elephants housed and
observed in pairs (Happy
å…¾
Samuel R. and Maxine
å…¾
Patty) at the
Fig. 3.
Rate of head touching by Happy across four conditions. For mark tests
and open-mirror tests, the black bars show the rate per minute of self-
touching by Happy while at the mirror or within 90 seconds of having stepped
away from the mirror. Gray bars show the rate of touching before mirror
exposure or
⬎
90 seconds after having left the mirror location. For comparison,
the self-touching rate during covered mirror and baseline is provided (‘‘no
mirror’’), which is the combined data for the mirror-closed (T2) and mirror-
absent (T1) conditions.
Plotnik
et al.
PNAS
å…©
November 7, 2006
å…©
vol. 103
å…©
no. 45
å…©
17055
PSYCHOLOGY
Bronx Zoo, located in New York City. The youngest elephant
(Samuel R.) was not included in the study. Maxine (35 years of age),
Patty (35 years of age), and possibly Happy (34 years of age) had
infrequent but previous exposure to a small mirror that was leaned
against a tree beyond their reach as part of their enrichment
program. They were not exposed to any mirrors in the year before
the present study; however, like all animals at the zoo, they had
experience with reflective surfaces, such as pools of water.
Procedures.
Maxine and Patty were shifted from their holding
area to the outdoor elephant yard for 1 h (
⬇
0915–1015 h) each
morning for observation and then shifted into a zoo exhibit no
later than 1030 h. From 1115 to 1215 h, Happy and Samuel R.
were also given access to the same elephant yard for observation,
but in contrast to Maxine and Patty, they were not restricted to
the yard. For husbandry reasons, they retained access to the
holding area.
There were five experimental phases, during which each pair
of elephants was videotaped from a roof above the exhibit yard:
baseline (T1; 1 h per day for 4 days), covered mirror (T2; 1 h per
day for 3 days), open mirror (T3; 1 h per day for 4 days),
covered-mirror sham (T4; 1 h for 1 day), and the mark test (T5;
1 h per day, see
Results and Discussion
). A low-frequency
sensitive microphone was installed behind the wall adjacent to
the mirror to record elephant vocalizations (these data were not
analyzed for this study). The mirror was built and installed over
a period of 2 weeks but remained covered during T2 (covered
mirror). For T3 (open mirror), three camera angles were used,
one of which, as described previously, was operated from the
roof above the elephant yard [using a Sony (Tokyo, Japan)
PDF-150 digital video (miniDV) camera]. A second camera
(Optura Xi miniDV camera; Canon, Lake Success, NY) with a
side view of the mirror location was installed on a tripod located
outside of the elephant yard at ground level. The third camera
was a 3-mm-diameter charge-coupled device Elmo (Plainview,
NY) lipstick color camera embedded in the mirror and inter-
faced with an external miniDV camera behind the mirror wall.
Although the elephants were always videotaped for a period of
⬇
1 h per day, because the elephants had access to areas of the
yard and building that were not visible, actual observation time
varied depending on how much time each subject spent in
camera view.
On the first day of mirror exposure for each pair, the holding area
door was slightly opened for a period of 10 min to allow the subjects
time to habituate to the mirror. The door was then fully opened to
allow the elephants entrance into the yard. The elephants were
observed for a previously undetermined number of days (but for the
same length of daily observation time) until they reached behavioral
criteria. Before the mark test, we conducted T4 (i.e., 1 day of
sham-marking in a covered-mirror condition). The elephant was
sham-marked in the center of her forehead and observed for 1 h.
We then conducted 2 more days of covered-mirror observation
(T2) immediately followed by 1 day of open-mirror observation
(T3) before proceeding to the first mark test (T5). On marking days,
one elephant per pair was marked and sham-marked by an elephant
keeper in the holding area. Using three fingers, the X-shaped mark
and same-shaped sham-mark (
⬇
12 cm diagonal length and
⬇
4 cm
wide) were applied to opposite sides of the elephant’s head in the
area diagonally above the eye and in front of the ear and counter-
balanced on subsequent days of marking. Any touching of the mark
and sham by the elephant before being released into the yard (a
period that never exceeded 5 minutes) was noted by the keepers.
After the elephants were released into the yard, all procedures were
identical to those of the open-mirror condition (T3). The mark test
was repeated on each of the three subjects after a 2-month break
with a differently shaped mark following the aforementioned
procedure. No two elephants in the same pair were ever marked on
the same day, and all paint was removed after each mark test.
Mirror.
Two 0.6-cm-thick pieces of 122
â«»
244-cm acrylic (Plas-
kolite, Columbus, OH) mirror were glued to plywood to produce
a full 244
â«»
244-cm mirror with a negligible yet fully braced seam
down the middle. The mirror was then framed with steel support
and bolted to the yard wall
⬇
30 cm off the ground. The mirror
cover (i.e., a metal door painted with flat, nonreflective brown
paint) was then installed with a reinforced hinge and back-
supported with steel on the adjacent wall. The door was locked
in either the open or the closed position depending on the
experimental procedure.
Mirror Location.
The elephants were considered ‘‘at the mirror’’
if they were within 4 m of the mirror apparatus as judged by their
position relative to a visible grating in the wall to the left of the
mirror.
Coding Procedure.
While coding sessions where all three cameras
were used (T3–T5), two tape decks and monitors were used to
code behaviors while at the mirror. All sessions (T1–T5) were
coded by using as many of the three tapes as was necessary to
verify accuracy. In general, the roof camera tapes were coded,
with the mirror camera and the side-view camera tapes used to
verify the elephants’ behaviors when facing the mirror (and thus
when their backs were to the roof camera).
Data were coded by using a behavioral ethogram developed
during baseline (T1) observations. All data were then organized
and analyzed by using Excel PivotTables (Microsoft, Redmond,
WA). All data were coded by J.M.P.; however, 100% agreement
was reached on the frequency and location of all mark touches
during T5 (the mark test) by J.M.P. and D.R., who coded
Happy’s first mark session independently.
We thank Gordon Gallup, Jr., and Joyce Poole for their helpful
comments on the study and manuscript. We are grateful to J. Mahoney,
P. Thomas, P. Kalk, K. Theis, G. Stark, G. Gordian, G. Fergason, W.
Canino, C. Vitale, and M. Medina of the Bronx Zoo Mammal Depart-
ment for their assistance in conducting the study. We also thank R. Lattis
and J. Breheny for supporting this project; the Bronx Zoo Machine and
Carpentry Shops for construction of the mirror apparatus; T. Veltre, L.
Groskin, J. Deveney, and D. Mulewski for audio
å…¾
visual support; D.
Moore, K. Payne, A. Murray, H. Lyn, and M. Maust for their assistance
in this study; and J. McDowell and N. Bliwise for statistical advice.
Finally, we thank Palmer Paint Products, Inc. for providing advice on the
marking material. This project was conducted at the Wildlife Conser-
vation Society (WCS)’s Bronx Zoo and was supported by WCS’s Living
Institutions Animal Enrichment Program, the Living Links Center at the
Yerkes National Primate Research Center, and the Department of
Psychology at Emory University.
1. Gallup GG, Jr (1970)
Science
167:86–87.
2. Anderson JR, Gallup GG, Jr (1999) in
Animal Models of Human Emotion and
Cognition
, eds Haug M, Whalen RE (American Psychological Association,
Washington, DC), pp 175–194.
3. Reiss D, Marino L (2001)
Proc Natl Acad Sci USA
98:5937–5942.
4. Keenan JP, Gallup GG, Jr, Falk D (2003)
The Face in the Mirror: The Search
for the Origins of Consciousness
(HarperCollins, New York).
5. Gallup GG, Jr (1994) in
Self-Awareness in Animals and Humans: Developmental
Perspectives
, eds Parker ST, Mitchell RW, Boccia ML (Cambridge Univ Press,
Cambridge, UK), pp 35–50.
6. de Waal FBM, Dindo M, Freeman CA, Hall M (2005)
Proc Natl Acad Sci USA
102:11140–11147.
7. Gallup GG, Jr (1982)
Am J Primatol
2:237–248.
8. de Waal FBM (2003) in
Feelings & Emotions: The Amsterdam Symposium
, eds
Manstead T, Frijda N, Fischer A (Cambridge Univ Press, Cambridge, UK), pp
379–399.
9. de Waal FBM, Aureli F (1996) in
Reaching Into Thought: The Minds of the Great
Apes
, eds Russon AE, Bard KA, Parker ST (Cambridge Univ Press, Cambridge,
UK), pp 80–110.
10. Bischof-Ko
¨hler D (1988)
Schweiz Z Psychol
47:147–159.
17056
å…©
www.pnas.org
å…¾
cgi
å…¾
doi
å…¾
10.1073
å…¾
pnas.0608062103
Plotnik
et al.
11. Zahn-Waxler C, Radke-Yarrow M, Wagner E, Chapman M (1992)
Dev Psychol
28:126–136.
12. de Waal FBM (1996)
Good Natured: The Origins of Right and Wrong in Humans
and Other Animals
(Harvard Univ Press, Cambridge, MA).
13. Caldwell MC, Caldwell DK (1966) in
Whales, Dolphins, and Porpoises
, ed Norris
KS (Univ of California Press, Berkeley, CA), pp 755–789.
14. Connor RC, Norris KS (1982)
Am Nat
119:358–372.
15. Moss C (1988)
Elephant Memories: Thirteen Years in the Life of an Elephant
Family
(Fawcett Columbine, New York).
16. Poole J (1996)
Coming of Age With Elephants: A Memoir
(Hyperion Books, New
York).
17. Hamilton-Douglas I, Bhalla S, Wittemyer G, Vollrath F (2006)
App Anim Behav
Sci
, 100:87–102.
18. Payne K (2003) in
Animal Social Complexity: Intelligence, Culture, and Indi-
vidualized Societies
, eds de Waal FBM, Tyack PL (Harvard Univ Press,
Cambridge, MA), pp 57–85.
19. Shoshani J (1998)
TREE
13:480–487.
20. Shoshani J, Kupsky WJ, Marchant GH (2006)
Brain Res Bull
70:124–157.
21. Povinelli DJ (1989)
J Comp Psychol
103:122–131.
22. Olson D, ed (2004)
Elephant Husbandry Resource Guide
(Allen Press, Law-
rence, KS).
23. Povinelli DJ, Rulf AB, Landau KR, Bierschwale DT (1993)
J Comp Psychol
107:347–372.
24. Brown RE (1985) in
Social Odours in Mammals
, eds Brown RE, Macdonald
DW (Oxford Univ Press, New York), Vol 1, pp 235–244.
25. Swartz KB, Evans S (1991)
Primates
32:483–496.
26. Povinelli DJ, Gallup GG, Jr, Eddy TJ, Bierschwale DT, Engstrom MC,
Perilloux HK, Toxopeus IB (1997)
Anim Behav
53:1083–1088.
27. van Lawick-Goodall J (1968)
Anim Behav Monogr
1:161–311.
28. de Waal FBM (1982)
Chimpanzee Politics: Power and Sex Among Apes
(Harper
& Row, New York).
29. Mooring MS, Benjamin JE, Harte CR, Herzog NB (2000)
Anim Behav
60:35–45.
30. Leuthold W (1977)
African Ungulates: A Comparative Review of Their Ethology
and Behavioral Ecology
(Springer-Verlag, New York).
31. Estes R (1991)
The Behavior Guide to African Mammals: Including Hoofed
Mammals, Carnivores, Primates
(Univ of California Press, Berkeley, CA).
Plotnik
et al.
PNAS
å…©
November 7, 2006
å…©
vol. 103
å…©
no. 45
å…©
17057
PSYCHOLOGY