Contextual imitation in juvenile common ravens, Corvus corax
, Richard Schuster
, Ira G. Federspiel
, Bernd Heinrich
Department of Cognitive Biology, University of Vienna, Vienna, Austria
Konrad Lorenz Research Station, Core Facility for Behaviour and Cognition, University of Vienna, Grünau Im Almtal, Austria
Department of Migration, Max Planck Institute of Animal Behavior, Radolfzell, Germany
Department of Biology, University of Konstanz, Konstanz, Germany
Department of Biology, Carleton University, Ottawa, Canada
PO Box 153, Weld, ME, 04285, U.S.A.
Received 3 May 2019
Initial acceptance 27 September 2019
Final acceptance 13 March 2020
MS number 19-00304R
Social learning is a powerful mechanism of information acquisition and can be found in various species.
According to the type of information transmitted, animals may change their motivation to perform ac-
tions, shift their perception/attention to relevant stimuli, associate other individuals' behaviours with
particular stimuli/events or learn to perform ‘novel’behaviours. The latter is referred to as imitation and
has been considered a cognitively demanding mechanism necessary for high-ﬁdelity copying, which may
or may not occur in nonhuman animals. We tested the ability of 20 juvenile ravens to imitate an action
demonstrated by a human experimenter. Birds of two test groups could observe a familiar human
executing one of two opening techniques at an artiﬁcial fruit apparatus (horizontal or vertical hand
movements directed towards the same location), whereas birds of a control group observed the human
touching but not opening the apparatus. Ravens of both test groups tended to use the same direction of
movements as observed, when they opened the apparatus themselves with their beak. Comparison with
the control group revealed that ravens had a predisposition to manipulate the apparatus by pecking.
Hence, observers of vertical hand movements most likely strengthened their initial preference for
executing peck movements towards an item enclosing food, whereas observers of horizontal hand
movements started to apply beak/head movements that hardly occur during foraging and are ‘novel’to
this context. Juvenile ravens are thus capable of imitating simple motor actions, even though they may
use a different body part to execute the behaviours than human demonstrators.
©2020 The Author(s). Published by Elsevier Ltd on behalf of The Association for the Study of Animal
Behaviour. This is an open access article under the CC BY license (http://creativecommons.org/licenses/
One of the main advantages of social life is that individuals can
make use of information provided by others, typically to improve
foraging efﬁciency and/or predator detection (Giraldeau &Caraco,
2000). Social information use can take different forms: informa-
tion may be transmitted by staying in contact with a knowledge-
able individual, like elephants, Loxodonta africana, following their
matriarch to foraging grounds and water holes (McComb, Moss,
Sayialel, &Baker, 2000); it may also be transmitted through
(repeated) exposure to the performance of a skilled individual, like
young chimpanzees, Pan troglodytes, watching older ones
manufacturing and using tools (Lonsdorf, Eberly, &Pusey, 2004;
Matsuzawa, Tomonaga, &Tanaka, 2006), and through direct
interaction between individuals, as when afﬁliated animals estab-
lish communicative conventions (McGrew, 2004; Perry et al., 2003;
Whitehead &Rendell, 2015).
Several of these cases fall into the deﬁnition of social learning
sensu Box (1984,p.213)as‘changes in the behaviour of one indi-
vidual that result partly from paying attention to the behaviour of
another’(see also Heyes, 1994, 2012 for a more reﬁned deﬁnition);
yet, the above-mentioned examples may differ with respect to (1)
which type of information is transmitted, (2) under which condi-
tions social information is used, and (3) how robust the information
transmission is over time, referring to the areas of social learning
mechanisms (Zentall &Galef, 1988) social learning strategies
(Laland, 2004; Rendell et al., 2011) and behavioural traditions and
culture (Whiten, Hinde, Laland, &Christopher, 2011), respectively.
Various social learning mechanisms have been described
(Heyes, 2012; Hoppitt &Laland, 2008; Zentall &Galef, 1988), most
*Correspondence: M-C Loretto, Department of Migration, Max Planck Institute of
Animal Behavior, Am Obstberg 1, 78315, Radolfzell, Germany.
E-mail address: firstname.lastname@example.org (M. -C. Loretto).
Contents lists available at ScienceDirect
journal homepage: www.elsevier.com/locate/anbehav
0003-3472/©2020 The Author(s). Published by Elsevier Ltd on behalf of The Association for the Study of Animal Behaviour. This is an open access article under the CC BY
Animal Behaviour 163 (2020) 127e134
of which can be well explained by learning theory (Heyes, 1994,
2012) and broadly categorized according to the type of informa-
tion processed (Zentall, 2004). While surprisingly few studies have
been designed to explicitly test for mechanisms at the motivational
level (e.g. social facilitation), perceptual level (e.g. enhancement)
and associative level (e.g. observational conditioning; Zentall,
2004), mechanisms at the ‘cognitive level’have received much
attention, from both a conceptual and a methodological point of
view (Heyes, 1994; Hoppitt &Laland, 2008; Whiten, Horner,
Litchﬁeld, &Marshall-Pescini, 2004). Speciﬁcally, action imitation,
the copying of others' behaviour, has been the focus of interest. On
the one hand, the translation of a visual input into a matching
motor output features a ‘correspondence problem’(an action looks
different from an observer's perspective than when it is performed
oneself) and thus may involve a special, and possibly more com-
plex, processing than other mechanisms of social learning (Byrne &
Whiten, 1988; Byrne, 1995; but see ; Ferrari, Bonini, &Fogassi,
2009; Huber et al., 2009). On the other hand, a faithful matching
of observed behaviour has been considered critical for the reliable
transmission of information and thus essential for cultural evolu-
tion (Boyd &Richerson, 1985, 1996; Tomasello, Kruger, &Ratner,
1993; but see Heyes, 2012).
Despite a wealth of studies, evidence for imitation in nonhuman
animals is still debatable. Depending on the criteria used, imitation
can be found in a variety of species (Heyes, 2012; Hoppitt &Laland,
2008) or speciﬁcally in humans (Tomasello, Savage-Rumbaugh, &
Kruger, 1993) and, possibly, some great apes (Whiten et al., 2004;
but see ; Tennie, Call, &Tomasello, 2009). One of the criteria in
question is how precisely behaviours are copied. Many studies on
nonhuman primates report only low levels of precision in copying
or even no copying at all (Clay &Tennie, 2018; Tennie, Call, &
Tomasello, 2012; Tomasello, Savage-Rumbaugh, et al., 1993; Visal-
berghi &Fragaszy, 2002; Zuberbühler, Gygax, Harley, &Kummer,
1996), whereas some studies on birds report relatively high levels
of copying precision (review in Zentall, 2004). These apparent
taxonomic differences in copying precision are most likely affected
by the type of experimental task: single movements such as
pecking or stepping on a platform, as used in many bird studies, are
easier to match than a combination or sequence of behaviours, as
used in many primate studies on artiﬁcial fruits (Whiten, Custance,
Gomez, Teixidor, &Bard, 1996; but see ; Voelkl &Huber, 2000). The
level of precision in response topography has also been used as an
argument to distinguish between ‘blindly mimicking’and ‘inten-
tionally copying’, as the latter is assumed to require more degrees of
freedom with respect to matching than the former (Huber et al.,
2009). However, empirical studies testing for intentional aspects
of imitation are still scarce and the outcomes are debatable (Huber,
anyi, 2012; Kaminski, Neumann, Br€
auer, Call, &
Tomasello, 2011; see discussion on selective or ‘rational’imita-
tion: Range, Viranyi, &Huber, 2007).
Corvids are renowned for their large brains and sophisticated
sociocognitive skills, which are in manyaspects comparable to those
of primates (Emery &Clayton, 2004; Güntürkün &Bugnyar, 2016).
Despite the importance of social information use in these birds (e.g.
Bugnyar, 2013; Emery, Clayton, &Frith, 2007; Massen, Pa
Schmidt, &Bugnyar, 2014), relatively few studies have focused on
social learning mechanisms. Social facilitation has been reported for
ravens and carrion crows, Corvus corone, in investigating objects
(Miller, Schiestl, Whiten, Schwab, &Bugnyar, 2014; St€
owe et al.,
2006a, 2006b), for rooks, Corvus frugilegus, in accepting new food
(Dally, Clayton, &Emery, 2008) and, as a plausible mechanism for
American crows, Corvus brachyrhynchos, forming traditions about
artiﬁcially introduced predator types (Cornell, Marzluff, &Pecoraro,
2011; Marzluff, Walls, Cornell, Withey, &Craig, 2010). Local or
stimulus enhancement towards feeding locations, parts of feeding
apparatuses and/or speciﬁc objects have been reported for ravens
(Fritz &Kotrschal, 1999; Schwab, Bugnyar, Schloegl, &Kotrschal,
2008), jackdaws, Corvus monedula (Schwab et al., 2008) and New
Caledonian crows, Corvus moneduloides (Kenward, Rutz, Weir, &
Kacelnik, 2006). To our knowledge, there is no evidence for action
imitation, possibly because the above-mentioned mechanisms at the
motivational and perceptual levels are powerful enough to transmit
the relevant information during foraging (Federspiel, Clayton, &
Emery, 2009). Still, the apparent lack of action imitation is surpris-
ing: on the one hand, imitative abilities have been reported for other
large-brained birds such as parrots (Dawson &Foss, 1965; Moore,
1992) that resemble corvids with respect to their social life with
long-term monogamous pairs (Emery et al., 2007); on the other
hand, simple forms of action imitation have been demonstrated in
species such as pigeons, Columba livia, and quails, Coturnix japonica
(Akins, Klein, &Zentall, 2002) that hardly face a more diverse
foraging ecology than corvids, rendering a socioecological explana-
tion for a lack of imitation in corvids unlikely.
In the present study we tested common ravens, highly adaptable
food generalists that prefer feeding on carcasses (Haffer &Kirchner,
1993; Ratcliffe, 1997) and occupying a wide range of different
habitats with a great variety of potential food items (Heinrich,
1995), often of anthropogenic origin (Loretto et al., 2017; Loretto,
Schuster, &Bugnyar, 2016). Ravens are known to be sensitive to
various types of social information during foraging (Bugnyar, 2013;
Scheid, Pasteur, Range, &Bugnyar, 2007; Schwab, Bugnyar,
Schloegl, et al., 2008), including a conspeciﬁc's demonstration of
opening an apparatus containing food (Fritz &Kotrschal, 1999). We
based our study on the latter ﬁndings but adapted the methods to
explicitly test the ravens' capacity to copy the other individual's
motor action and to distinguish imitation from other social learning
mechanisms. We tested young hand-raised birds on the same
apparatus as Fritz and Kotrschal (1999) but instead of a conspeciﬁc
demonstrating a given opening technique, we used a human
experimenter demonstrating one of two alternative opening tech-
niques (vertical or horizontal hand movements) executed at exactly
the same location of the apparatus. We were therefore able to
control the motivational and perceptual information given by the
demonstrator and rule out possible effects of conspeciﬁc social
relationships between demonstrator and test subject. However,
using a human experimenter as demonstrator put the ‘correspon-
dence problem’to its extreme as it required ravens to relate the
observed hand movements to their own head/beak movements.
We compared the behaviour of the two test groups (vertical
pushing and horizontal pushing) to that of a control group, where
the individuals did not receive any demonstration of either opening
technique. However, the control birds' attention towards the
apparatus was increased in a similar way as in the two test groups,
by the human experimenter touching the opening location. We
predicted that ravens of the two test groups would need fewer
trials to solve the task than ravens of the control group and, notably,
that individuals in the test groups would match their opening
technique to the respective technique demonstrated by the
experimenter, i.e. show vertical or horizontal movements. In-
dividuals of the control group should show no preference for either
opening technique or, if one movement for manipulating the
apparatus comes more naturally to them, we predicted a predis-
position to engage in vertical ‘pecking-like’movements.
We used 20 juvenile ravens, originating from two groups. One
group (13 birds) was hand-raised in 2004 at the Konrad Lorenz
M.-C. Loretto et al. / Animal Behaviour 163 (2020) 127e134128
Research Station (KLF), Austria, and another group (seven in-
dividuals) was hand-raised in 2006 at Bernd Heinrich's laboratory
in Vermont (VT), U.S.A. All birds were taken into human care at an
early age (10e28 days, i.e. when they had hardly any feathers and
slept most of the day); they were kept in cardboard boxes in groups
of two to four birds until ﬂedging (6e7 weeks posthatch) and then
housed in one social group per site (KLF, VT). During hand raising,
all birds developed a strong attachment to their human caretakers.
We used this attachment to familiar persons to test the ravens'
responses to the demonstration by a human experimenter. We took
special care that the human experimenter was treating the birds as
similarly as possible, for example by hand feeding every bird each
day. Ravens of the KLF group were tested 11e15 weeks post-
hatching and those of the VT group 16e19 weeks posthatching. At
the time of testing, all birds were group housed in large natural-
istically designed outdoor enclosures (KLF: 230 m
; VT: 2x 50 m
containing perches, vegetation cover and natural soil. The aviaries
were built so that individuals could be visually but not acoustically
separated. The ravens were marked with coloured leg rings for
individual identiﬁcation. All individuals were fully habituated to
close contact with humans including the experimenter and to short
separations from the group during the experiments.
All 20 individuals were hand-raised under similar conditions
(see above) and participated in experiments voluntarily. The birds
were never deprived of food, and water was available ad libitum for
drinking and bathing. This study adheres to the ASAB/ABS Guide-
lines for the Use of Animals in Research, the Austrian and local
government guidelines, the US law on animal research and treat-
ment, the institutional guidelines of the Konrad Lorenz Research
Station, University of Vienna and the University of Vermont. Some
of the raven nestlings were provided by zoos (four from Munich,
three from Wuppertal); the others were taken from the wild in
Germany (six) with permission from the Ministerium für Land-
witschaft, Umweltschutz und Raumordnung des Landes Branden-
burg on 25 February 2004 and in Vermont (seven) with permits
from the US Federal Fish and Wildlife Permit Number MB689376-0,
State of Maine Department of Inland Fisheries and Wildlife Permit
22077, and Vermont Fish and Wildlife Department Scientiﬁc Col-
lecting Permit. The study subjects in Austria remained in captivity
at the Cumberland Wildpark after the completion of this study for
further research, while subjects in Vermont were released from the
aviary in the year after the study.
Procedure and Analysis
We used the same test apparatus as Fritz and Kotrschal (1999),
which was a box that consisted of a wooden frame (30 x 30 cm and
10 cm high) with a cover and bottom of white polystyrene (Fig. 1).
The cover was movable and consisted of two lids which could slide
in opposite directions, either by directing force at the gap between
the lids on the top of the apparatus or by pulling on one side from a
lateral position next to the box. Unlike in the original study by Fritz
and Kotrschal (1999), we did not provide lashes on the lids to
facilitate pulling from the side and we demonstrated both opening
techniques at the top of the apparatus exclusively (i.e. at the gap
between the lids). In Fritz and Kotrschal's (1999) study, pecks
directed towards the lids were vertical head/beak movements
performed by the ravens when sitting on top of the apparatus. We
thus modelled this pecking behaviour with vertical hand move-
ments performed by the experimenter. The alternative horizontal
movements demonstrated by the experimenter resembled the
horizontal head movements ravens perform for cleaning their
beak; this behaviour may occur during foraging but, to our
knowledge, is not used for extracting food; we thus considered it to
be ‘novel’in the context of food acquisition. Before starting the
experiment, we presented the apparatus to the birds in the aviary
without lids for habituation. After 1e2 weeks, all birds were used to
taking small pieces of reward out of the opened box.
The 13 individuals kept at KLF were randomly assigned to one of
two test groups (six birds in group A, seven in group B). One bird of
group A had to be excluded from the tests due to severe illness
during the study period and was replaced by one raven raised in VT.
The other six ravens in VT were assigned to the control group C,
whereas again one bird could not be tested as it showed much
higher levels of neophobia. Note that the study was conducted
stepwise because we were initially not sure of getting a second
group of hand-raised ravens in VT; we therefore did not randomly
allocate birds to all three conditions (group A, B and control C)
across the two sites, but focused on the two test conditions in
Austria ﬁrst. However, we took special care that the ravens at both
sites were raised and kept as similarly as possible. The same person
(M.L.) acted as experimenter for all birds. For an experimental
session, he visually separated one of the birds from the others,
presented the opened box and ﬁlled it with a small but highly
preferred food reward (dry dog food). After closing the box with the
lids, he performed one of three behaviours: (1) with birds from
group A, he performed vertical hand movements into the small gap
between the lids, making the lids slide open; (2) with birds from
group B, he performed horizontal hand movements by moving the
hand from the small gap between the lids towards the edge of the
lids, making them slide open; (3) with birds from control group C,
he put his hands on top of the lids, but did not perform any hand
movements to open them. Note that all three behaviours were
directed towards the same location at the apparatus and the two
opening techniques were executed at the same starting point
(where the two lids met; Fig. 1). We thus provided information
about the relevant part of the box (local enhancement) and about
the fact that it was safe to manipulate the apparatus (social facili-
tation) in all three conditions. The only difference between the
conditions was what the hands of the experimenter were doing,
that is, resting on the lids (control) or pushing the lids via vertical or
horizontal movements. The demonstrations were conducted only
when the birds showed no signs of arousal (feather/body position,
vocalization) and their head and eyes were oriented towards the
experimenter (which could take up to 10 min). The demonstrations
of vertical and horizontal movements were repeated three times in
a row; the touching of the lids in the control group lasted
approximately as long as these movement demonstrations (3 s).
Before the birds got access to the test apparatus themselves for
5 min, it was turned 90
to control for any orientation on envi-
ronmental cues in the test compartment (e.g. left or right wall). We
videotaped the ravens during the trials (examples are available in
the video in the Supplementary Material), and we categorized and
scored every contact of the birds with the box, until they could
obtain the food by opening the lids. We considered trials as ‘un-
successful’when the birds did not approach the apparatus in 5 min
and/or disturbances like background noise caused the birds to
panic in the experimental room. These trials were excluded from
the analysis. For each bird, we thus analysed the ﬁrst three trials in
which it touched the box and eventually opened the box success-
fully. The contacts with the box were classiﬁed as follows: (1)
vertical push: the individual showed a pecking-like action by
moving the head in a vertical direction, often inserting the beak at
the gap between the two lids of the box, which led to a partial
opening without any horizontal movement of the head; (2) hori-
zontal push: after inserting the beak in the gap between the lids,
the individual moved its head horizontally and thus pushed one of
M.-C. Loretto et al. / Animal Behaviour 163 (2020) 127e134 129
the lids to the side, or it took one lid with the beak and pushed it to
the side; (3) every other beak contact with the cover or parts of the
box was categorized as ‘other box contacts’. A typical example was
pecking at the wooden frame or poking with the beak underneath
the apparatus. Importantly, none of these ‘other box contacts’
caused any movement of the lids.
Recordings were independently coded by two observers (M.L.
and T.B.) with very high interobserver agreement (Cohen's
kappa ¼0.852, P<0.001, 95% conﬁdence interval ¼0.714, 0.989;
Landis &Koch, 1977). The coding of T.B. was mostly blind to the test
condition, as we tried to avoid ﬁlming the hand movements of the
experimenter). Since some individuals were much more active than
others (see also St€
owe et al., 2006a, 2006b), we calculated the
proportion of each category (vertical push, horizontal push and
other box contacts) over the ﬁrst three successful trials together
and compared these values between test groups A and B and the
control group C. We used nonparametric tests, i.e. KruskaleWallis
rank sum tests for differences between all groups and the
ManneWhitney test for pairwise comparisons between groups and
adjusted the Pvalue following the Benjamini and Hochberg (1995)
correction. Since nonparametric tests are not very powerful, espe-
cially with a relatively low sample size, we additionally followed a
generalized linear model (beta distribution) approach employing a
Markov chain Monte Carlo algorithm to investigate the posterior
distribution of the treatment effects. This allowed us to directly
draw inference about the difference between treatments based on
the calculated credible intervals (Baldwin &Fellingham, 2013). The
advantage of this Bayesian approach is that the analysis does not
suffer the dependencies in the researcher's intentions like classical
hypothesis testing using Pvalues does (Kruschke, 2010). Instead it
allowed us to calculate the believability of candidate values given
the data we observed and thus yielded a natural way to assess the
credibility of null values and the probability of achieving research
goals (Kruschke, 2010). All analyses were conducted with the sta-
tistical software R, version 3.5.3 (R Development Core Team, 2019)
and connected to OpenBUGS v.3.2.3 (Lunn, Spiegelhalter, Thomas,
&Best, 2009) via package R2OpenBUGS v.3.2e2.2 (Sturtz, Ligges,
Against our expectation, there was no clear difference between
groups in the number of trials individuals needed to successfully
open the box (group A: 9e15 trials, mean ¼12, SD ¼2.683; group B:
3e39 trials, mean ¼26, SD ¼18.565; group C: 15e45 trials,
mean ¼31.2, SD ¼11.145; KruskaleWallis test:
P¼0.072). Thus, we did not ﬁnd that the opportunity for social
learning affected the ravens’efﬁciency in solving the task. However,
groups differed with respect to the relative proportion of vertical
push movements (KruskaleWallis test:
¼9.353, P¼0.009) and
horizontal push movements (KruskaleWallis test:
P¼0.015), respectively. As expected, post hoc tests revealed a sig-
niﬁcant difference between the two test groups A and B (pairwise
comparisons ManneWhitney test: vertical pushing: W¼41, N
¼0.016; horizontal pushing: W¼3, N
¼0.024; Fig. 2). Interestingly, there was no signiﬁcant dif-
ference between test group A and control group C (ManneWhitney
test: vertical pushing: W¼10, N
horizontal pushing: W¼30, N
there was a signiﬁcant difference between test group B and control
group C for vertical pushing (ManneWhitney test: W¼8.5, N
¼0.045) and a marginally nonsigniﬁcant difference
for horizontal pushing (W¼30, N
There was no difference between the three groups regarding the
Figure 1. ‘Artiﬁcial fruit’used in experiments: black arrow (A) and grey arrow (B) indicate hand movement of the demonstrator for group A and group B, respectively. Thin black
arrows show direction of opening of the two sliding lids.
Push movements (%)
Figure 2. Box plots show the percentages of vertical and horizontal pushing for each of
the three groups (A, B and C) with median (thick line), quartiles (box limits), 5th and
95th percentiles (error bars) and outliers (open circles). Birds in group A saw a human
make vertical hand movements, birds in group B saw a human make horizontal hand
movements and birds in group C were not shown any hand movements. Percentages
refer to the total number of box contacts over the ﬁrst three successful trials. Asterisks
indicate signiﬁcant differences between groups (P<0.05).
M.-C. Loretto et al. / Animal Behaviour 163 (2020) 127e134130
category of other box contacts (KruskaleWallis test: (
For vertical pushing the estimated means of the beta distribu-
tion back-transformed to probabilities were 0.44 for group A (95%
credible interval, CI ¼0.36 e0.52), 0.24 for group B
(CI ¼0.17 e0.34) and 0.50 for control group C (CI ¼0.32 e0.69).
The posterior distributions of these estimates are shown in Fig. 3a.
The mean estimated probabilities for horizontal pushing were 0.07
for group A (CI ¼0.02 e0.24), 0.25 for group B (CI ¼0.16 e0.36)
and 0.12 for control group C (CI ¼0.04 e0.37). The posterior dis-
tributions of these estimates are shown in Fig. 3b. For vertical and
horizontal pushing the posterior distributions of the estimates are
very similar for groups A and C with smaller credible intervals for
group A. This indicates a predisposition for vertical pushing (group
C), which was strengthened by the demonstrations for group A and
it suggests that the difference between test groups is mainly driven
by the modiﬁed preference of ravens in group B.
After observing a familiar human experimenter opening an
artiﬁcial fruit apparatus with horizontal or vertical hand move-
ments, juvenile ravens that witnessed horizontal hand movements
increased the relative frequency of horizontal beak movements in
comparison to juveniles that witnessed vertical movements. The
comparison with birds of the control group, which observed the
experimenter touching but not opening the apparatus, revealed
that ravens have a predisposition to manipulate the lids by pecking,
which resembles the demonstrated vertical movements. Hence,
ravens that had observed vertical hand movements most likely
strengthened their initial preference for executing peck move-
ments towards an item enclosing food, whereas ravens that had
observed horizontal hand movements did not show any preference
for vertical pecking but tended to exhibit more horizontal push
movements towards the apparatus. Note that ravens may show
horizontal head movements during foraging, but typically for
wiping/cleaning their beak and not for extracting food.
Our results indicate that young ravens are capable of simple
forms of action imitation, corroborating similar ﬁndings from other
birds such as pigeons (Klein &Zentall, 2003), quails (Akins &
Zentall, 1996), starlings, Sturnus vulgaris (Campbell, Heyes, &
Goldsmith, 1999), budgerigars, Melopsittacus undulatus (Mui,
Haselgrove, Pearce, &Heyes, 2008) and tits (Aplin et al., 2015). In
particular the ravens' tendency to copy horizontal movements is in
line with the idea of a speciﬁc category of action imitation, that is,
contextual imitation (Hoppitt &Laland, 2008), as ravens seemingly
learned to execute a behaviour that is within the species' repertoire
(e.g. for cleaning the beak) in a novel context, extracting food.
Whether their imitative skills are based on ‘blindly mimicking’
other individuals' actions (as demonstrated in pigeons, McGregor,
Saggerson, Pearce, &Heyes, 2006) or guided by observational
learning about outcomes needs to be addressed in future studies.
Note that in contrast to most other avian imitation studies, ra-
vens were not exposed to a trained conspeciﬁc, but had to copy the
motor patterns of a human experimenter. Copying of human
behaviour has so far only been reported for chimpanzees (Custance,
Whiten, &Bard, 1995; Tomasello, Savage-Rumbaugh, et al., 1993),
orang-utans, Pongo pygmaeus (Call, 2001), bottlenose dolphins,
Tursiops truncatus (Jaakkola, Guarino, Rodriguez, &Hecksher, 2013;
Tayler &Saayman, 1973), pet dogs, Canis lupus familiaris (Range,
Huber, &Heyes, 2011; Top
al, Byrne, Mikl
anyi, 2006), and
a grey parrot, Psittacus erithacus (Moore, 1992). Such an ability is
striking with respect to the ‘correspondence problem’(Nehaniv &
Dautenhahn, 2002), as what an animal sees being executed (in
this case, hand movements) is very different to the action it sub-
sequently performs itself (in this case, head movement). However,
regardless of the topography of the actions, that is, how given body
parts move, the effects on the environment are similar (in this case,
lids are slid open). This functional matching of observed behaviours
with different body parts leads to interesting questions at the
neuronal level, as these results may be difﬁcult to explain solely on
the basis of mirror neurons (Di Pellegrino, Fadiga, Fogassi, Gallese,
&Rizzolatti, 1992; Gallese, Fadiga, Fogassi, &Rizzolatti, 1996).
Several of the above-mentioned imitation studies involved an-
imals that had been raised and/or kept in close contact with
humans and thus may be regarded as ‘enculturated’(Tomasello,
Savage-Rumbaugh, et al., 1993). In great apes, for example, exten-
sive human training and human contact has been identiﬁed as a
critical driver of imitation (Call, 2001); consequently, it has been
suggested that the performance of these ‘enculturated’subjects is
not representative of great apes in general (Henrich &Tennie, 2017;
but see Byrne &Russon, 1998 for studies under naturalistic con-
ditions). The same argument may apply to species of other taxo-
nomic groups, whereby different individuals and/or species may
experience different degrees of ‘enculturation’and its effects. Our
ravens received intensive human care as chicks which certainly
affected their behaviour towards humans later in life. Yet, we
suggest that their upbringing concerned mainly their behaviour
0 0.25 0.5 0.75 1
0 0.25 0.5 0.75 1
Figure 3. Posterior distributions based on 90 000 draws from the joint posterior distribution of each model's parameters are shown for (a) vertical and (b) horizontal push
movements over the three trials combined. Birds in group A saw a human make vertical hand movements, birds in group B saw a human make horizontal hand movements and
birds in group C were not shown any hand movements.
M.-C. Loretto et al. / Animal Behaviour 163 (2020) 127e134 131
towards humans (e.g. the amount of attention they paid to humans)
rather than their cognitive abilities. The fact that budgerigars and
pigeons kept under laboratory conditions can discriminate natural
movements of humans and dogs (walking forwards versus back-
wards) indicates that enculturation is not necessary for animals to
discriminate between human dynamic cues (Mui et al., 2007).
Could any social learning mechanism other than imitation ac-
count for the behavioural biases towards the method demonstrated
by the human model? In the study by Fritz and Kotrschal (1999),it
was difﬁcult to distinguish between stimulus enhancement and
action imitation because the two actions were executed at two
different locations of the apparatus. Here, we controlled for this
possibility by directing all demonstrated actions towards the same
location at the apparatus. Furthermore, we controlled for the pos-
sibility that birds associate the direction of lid movements with
particular features in the environment by turning the box by 90
before testing (compare Heyes, 1994). It might be possible that
ravens tried to emulate the end or outcome of an action sequence
(Whiten et al., 2004), but in this case birds of the two test groups
should not have differed in their directions of head movements.
Because a human model was used, motivational factors in terms of
biases towards a certain model should also be more comparable
between the groups than if there had been two or more conspeciﬁc
models used with different social relationships to the observers
(Coussi-Korbel &Fragaszy, 1995; Laland, 2004). We therefore
conclude that the current results can be best explained by a form of
action imitation. Note that this interpretation refers solely to the
capacity of copying other individuals' behaviour (Box, 1984; Heyes,
1994) and does not make any assumptions about the ravens’
intentionality of copying.
Against our expectation, individuals from the two test groups
did not always open the box more quickly or successfully than birds
from the control group. This ﬁnding indicates that although
imitation alters the ravens' propensity to perform particular be-
haviours, it does not necessarily affect their efﬁciency in solving the
task, at least not in our set-up. Future studies should thus address
not only whether imitation can be used but also under which
conditions it pays off, relative to other social learning mechanisms.
We propose that ravens, and possibly other corvids, employ
imitation in situations when it is crucial to learn about using certain
types of behaviour. Young ravens might apply this skill during
extractive foraging, when they are confronted with novel problems
(as in our current study); older birds that already have ample
experience with foraging techniques might employ it in other do-
mains, such as in self-aggrandizing or joint displays in the context
of pair formation and during play. Another interesting question for
futures studies concerns the ravens' capacity to selectively imitate
(Buttelmann, Zmyj, Daum, &Carpenter, 2013; Range et al., 2007).
So far, we only know that ravens are highly selective in choosing
whom to learn from, both in dyadic and in group settings (Kulahci
et al., 2016; Schwab, Bugnyar, Schloegl, et al., 2008). Future studies
need to test whether they ‘blindly’mimic every behaviour
demonstrated or selectively copy only those components that
‘make sense’in a given situation (Gergely, Bekkering, &Kir
2002). Using a human experimenter as demonstrator seems to be
a promising way to proceed along these lines.
Taken together, with the present study we have shown an in-
formation transfer via social learning between a human demon-
strator and observing ravens. Our controlled set-up and speciﬁcities
of the results (i.e. the matching of movement directions) allows us
to conclude that action imitation is the underlying social learning
mechanism. As the actions in question wereprobably already in the
species’repertoire, we argue that the imitation is contextual, that is,
the ravens have learned to perform a given behaviour in a novel
context. Birds in the imitation groups were not quicker in solving
the task than birds in the control group, raising the question under
which conditions imitation pays off.
Data and R code for the Bayesian analysis are available at https://
We are thankful to KurtKotrschal, Christian Schl€
ogl and Mareike
owe for their help at the KLF, Rachel Smolker, Jodi Boos-Blaszyk
and Hagen Blaszyk for their help in Vermont, the Herzog von
Cumberland Stiftung for cooperation in keeping ravens, the ‘Verein
orderer KLF’for permanent support, Paul S€
ommer, the Zoos
München and Wuppertal for help in accessing the young ravens
and ﬁnally Johannes Fritz for sharing his artiﬁcial fruit apparatuses.
The study was funded by a ‘KUWI Stipendium’of the Karl-Franzens-
University of Graz and the FWF projects R31-B03, P16939eB03 and
P29705. M.L. is currently supported by the European Union's Ho-
rizon 2020 research and innovation programme under the Marie
Sklodowska-Curie grant agreement No 798091.
Supplementary material associated with this article is available
Akins, C. K., Klein, E. D., & Zentall, T. R. (2002). Imitative learning in Japanese quail
(Coturnix japonica) using the bidirectional control procedure. Animal Learning &
Behavior, 30(3), 275e281.
Akins, C. K., & Zentall, T. R. (1996). Imitative learning in male Japanese quail
(Coturnix japonica) using the two-action method. Journal of Comparative Psy-
chology, 110(3), 316.
Aplin, L. M., Farine, D. R., Morand-Ferron, J., Cockburn, A., Thornton, A., &
Sheldon, B. C. (2015). Experimentally induced innovations lead to persistent
culture via conformity in wild birds. Nature, 518(7540), 538e541. https://
Baldwin, S. A., & Fellingham, G. W. (2013). Bayesian methods for the analysis of
small sample multilevel data with a complex variance structure. Psychological
Methods, 18(2), 151.
Benjamini, Y., & Hochberg, Y. (1995). Controlling the false discovery rate: A practical
and powerful approach to multiple testing. Journal of the Royal Statistical So-
ciety: Series B, 57(1), 289e300. Retrieved from http://www.jstor.org/stable/
Box, H. O. (1984). Primate behaviour and social ecology. London, U.K.: Chapman &
Boyd, R., & Richerson, P. J. (1985). Culture and the evolutionary process. Chicago, IL:
The University of Chicago Press.
Boyd, R., & Richerson, P. J. (1996). Why culture is common, but cultural evolution is
rare. Proceedings of the British Academy, 88,77e94.
Bugnyar, T. (2013). Social cognition in ravens. Comparative Cognition &Behavior
Reviews, 8,1e12. https://doi.org/10.3819/ccbr.2013.80001.
Buttelmann, D., Zmyj, N., Daum, M., & Carpenter, M. (2013). Selective imitation of
in-group over out-group members in 14-month-old infants. Child Development,
84(2), 422e428. https://doi.org/10.1111/j.1467-8624.2012.01860.x.
Byrne, R. W. (1995). The thinking ape: Evolutionary origins of intelligence. Oxford,
U.K.: Oxford University Press.
Byrne, R. W., & Russon, A. E. (1998). Learning by imitation: A hierarchical approach.
Behavioral and Brain Sciences, 21(5), 667e684. https://doi.org/10.1017/
Byrne, R. W., & Whiten, A. (1988). Machiavellian intelligence: Social expertise and the
evolution of intellect in monkeys, apes and humans. Oxford, U.K.: Oxford Uni-
Call, J. (2001). Body imitation in an enculturated orangutan (Pongo pygmaeus).
Cybernetics &Systems, 32(1e2), 97e119.
Campbell, F. M., Heyes, C. M., & Goldsmith, A. R. (1999). Stimulus learning and
response learning by observation in the European starling, in a two-object/two-
action test. Animal Behaviour, 58(1), 151e158.
Clay, Z., & Tennie, C. (2018). Is overimitation a uniquely human phenomenon? In-
sights from human children as compared to bonobos. Child Development, 89(5),
1535e154 4. https://doi.org/10.1111/cdev.12857.
M.-C. Loretto et al. / Animal Behaviour 163 (2020) 127e134132
Cornell, H. N., Marzluff, J. M., & Pecoraro, S. (2011). Social learning spreads
knowledge about dangerous humans among American crows. Proceedings of the
Royal Society of Biological Sciences, 279(1728). Retrieved from http://rspb.
Coussi-Korbel, S., & Fragaszy, D. M. (1995). On the relation between social dynamics
and social learning. Animal Behaviour, 50,1441e1453.
Custance, D. M., Whiten, A., & Bard, K. A. (1995). Can young chimpanzees (Pan
troglodytes) imitate arbitrary actions? Hayes &hayes (1952) revisited. Behav-
iour, 132(11), 837e859.
Dally, J. M., Clayton, N. S., & Emery, N. J. (2008). Social inﬂuences on foraging by
rooks (Corvus frugilegus). Behaviour, 145(8), 1101e1124. Retrieved from http://
Dawson, B. V., & Foss, B. M. (1965). Observational learning in budgerigars. Animal
Behaviour, 13(4), 470e474.
Di Pellegrino, G., Fadiga, L., Fogassi, L., Gallese, V., & Rizzolatti, G. (1992). Under-
standing motor events: A neurophysiological study. Experimental Brain
Research, 91(1), 176e180 .
Emery, N. J., & Clayton, N. S. (2004). The mentality of crows: Convergent evolution
of intelligence in corvids and apes. Science, 306, 1903e1907.
Emery, N. J., Clayton, N. S., & Frith, C. D. (2007a). Introduction. Social intelligence:
From brain to culture. Philosophical Transactions of the Royal Society of London B
Biological Sciences, 362(1480), 485e488. Retrieved from http://rstb.
Emery, N. J., Seed, A. M., Von Bayern, A. M. P., & Clayton, N. S. (2007b). Cognitive
adaptations of social bonding in birds. Philosophical Transactions of the Royal
Society B: Biological Sciences, 362(1480), 489e505. https://doi.org/10.1098/
Federspiel, I. G., Clayton, N. S., & Emery, N. J. (2009). The 3E's approach to social
information use in birds: Ecology, ethology and evolutionary history. In
R. Dukas, & J. M. Ratcliffe (Eds.), Cognitive ecology II (pp. 272e297). Chicago, IL:
University of Chicago Press.
Ferrari, P. F., Bonini, L., & Fogassi, L. (2009). From monkey mirror neurons to primate
behaviours: Possible ‘direct’and ‘indirect’pathways. Philosophical Transactions of
the Royal Society B: Biological Sciences, 364(1528), 2311e2323.
Fritz, J., & Kotrschal, K. (1999). Social learning in common ravens, Corvus corax.
Animal Behaviour, 57, 785e793.
Gallese, V., Fadiga, L., Fogassi, L., & Rizzolatti, G. (1996). Action recognition in the
premotor cortex. Brain, 119(2), 593e610.
Gergely, G., Bekkering, H., & Kir
aly, I. (2002). Rational imitation in preverbal infants.
Nature, 415(6873). https://doi.org/10.1038/415755a, 755e755.
Giraldeau, L.-A., & Caraco, T. (2000). Social foraging theory. Princeton, NJ: Princeton
University Press. https://doi.org/10.2307/j.ctv36zrk6.
Güntürkün, O., & Bugnyar, T. (2016). Cognition without cortex. Trends in Cognitive
Sciences, 20(4), 291e303. https://doi.org/10.1016/J.TICS.2016.02.001.
Haffer, J., & Kirchner, H. (1993). Corvus coraxeKolkrabe. In U. N. Glutz von Blotz-
heim, & K. M. Bauer (Eds.), Handbuch der V€
ogel Mitteleuropas, 13/III pp.
1947 e2022). Wiesbaden, Germany: AULA-Verlag.
Heinrich, B. (1995). Neophilia and exploration in juvenile common ravens, Corvus
corax.Animal Behaviour, 50, 695e704.
Henrich, J., & Tennie, C. (2017). Cultural evolution in chimpanzees and humans. In
M. N. Muller, R. W. Wrangham, & D. R. Pilbeam (Eds.), Chimpanzees and human
evolution (pp. 645e702). Cambridge, MA: Harvard University Press.
Heyes, C. M. (1994). Social learning in animals: Categories and mechanisms. Bio-
logical Reviews, 69(2), 207e231.
Heyes, C. M. (2012). What's social about social learning? Journal of Comparative
Psychology, 126(2), 193e202. https://doi.org/10.1037/a0025180.
Hoppitt, W., & Laland, K. N. (2008). Social processes inﬂuencing learning in animals:
A review of the evidence. Advances in the Study of Behavior, 38,105e165.
Huber, L., Range, F., & Vir
anyi, Z. (2012). Dogs imitate selectively, not necessarily
rationally: Reply to. Animal Behaviour, 83(6), e1. https://doi.org/10.1016/
Huber, L., Range, F., Voelkl, B., Szucsich, A., Vir
anyi, Z., & Miklosi, A. (2009). The
evolution of imitation: What do the capacities of non-human animals tell us
about the mechanisms of imitation? Philosophical Transactions of the Royal So-
ciety of London. Series B, Biological Sciences, 364(1528), 2299e2309. https://
Jaakkola, K., Guarino, E., Rodriguez, M., & Hecksher, J. (2013). Switching strategies: A
dolphin's use of passive and active acoustics to imitate motor actions. Animal
Cognition, 16(5), 701e709. https://doi.org/10.1007/s10071-013-0605-3.
Kaminski, J., Neumann, M., Br€
auer, J., Call, J., & Tomasello, M. (2011). Dogs, Canis
familiaris, communicate with humans to request but not to inform. Animal
Behaviour, 82(4), 651e658. https://doi.org/10.1016/J.ANBEHAV.2011.06.015.
Kenward, B., Rutz, C., Weir, A. A. S., & Kacelnik, A. (2006). Development of tool use in
new caledonian crows: Inherited action patterns and social inﬂuences. Animal
Behaviour, 72(6), 1329e1343. https://doi.org/10.1016/J.ANBEHAV.2006.04.007.
Klein, E. D., & Zentall, T. R. (2003). Imitation and affordance learning by pigeons
(Columba livia). Journal of Comparative Psychology, 117(4), 414.
Kruschke, J. K. (2010). Bayesian data analysis. Wiley Interdisciplinary Reviews:
Cognitive Science, 1(5), 658e676.
Kulahci, I. G., Rubenstein, D. I., Bugnyar, T., Hoppitt, W., Mikus, N., & Schwab, C.
(2016). Social networks predict selective observation and information spread in
ravens. Royal Society Open Science, 3(7). https://doi.org/10.1098/rsos.160256.
Laland, K. N. (2004). Social learning strategies. Animal Learning &Behavior, 32(1),
Landis, J. R., & Koch, G. G. (1977). The measurement of observer agreement for
categorical data. Biometrics, 33,159e174 .
Lonsdorf, E. V., Eberly, L. E., & Pusey, A. E. (2004). Sex differences in learning in
chimpanzees. Nature, 428(6984), 715e716. https://doi.org/10.1038/428715a.
Loretto, M.-C., Schuster, R., & Bugnyar, T. (2016). GPS tracking of non-breeding ra-
vens reveals the importance of anthropogenic food sources during their
dispersal in the Eastern Alps. Current Zoology, 62(4). https://doi.org/10.1093/cz/
Loretto, M.-C., Schuster, R., Itty, C., Marchand, P., Genero, F., & Bugnyar, T. (2017).
Fission-fusion dynamics over large distances in raven non-breeders. Scientiﬁc
Reports, 7(1), 380. https://doi.org/10.1038/s41598-017-00404-4.
Lunn, D., Spiegelhalter, D., Thomas, A., & Best, N. (2009). The BUGS project: Evo-
lution, critique and future directions. Statistics in Medicine, 28(25), 3049e3067.
Marzluff, J. M., Walls, J., Cornell, H. N., Withey, J. C., & Craig, D. P. (2010). Lasting
recognition of threatening people by wild American crows. Animal Behaviour,
79(3), 699e707. https://doi.org/10.1016/j.anbehav.2009.12.022.
Massen, J. J. M., Pa
sukonis, A., Schmidt, J., & Bugnyar, T. (2014). Ravens notice
dominance reversals among conspeciﬁcs within and outside their social group.
Nature Communications, 5, 3679. https://doi.org/10.1038/ncomms4679.
Matsuzawa, T., Tomonaga, M., & Tanaka, M. (2006). Cognitive Development in
Chimpanzees. Tokyo, Japan: Springer-Verlag. https://doi.org/10.1007/4-431-
McComb, K., Moss, C., Sayialel, S., & Baker, L. (2000). Unusually extensive networks
of vocal recognition in African elephants. Animal Behaviour, 59(6), 1103e1109.
McGregor, A., Saggerson, A., Pearce, J., & Heyes, C.(2006). Blind imitation in pigeons,
Columba livia.Animal Behaviour, 72(2), 287e296. https://doi.org/10.1016/
McGrew, W. (2004). The cultured chimpanzee: Reﬂections on cultural primatology.
Cambridge, U.K.: Cambridge University Press.
Miller, R., Schiestl, M., Whiten, A., Schwab, C., & Bugnyar, T. (2014). Tolerance and
social facilitation in the foraging behaviour of free-ranging crows (Corvus cor-
one corone; C. c. cornix). Ethology, 120,1e8. https://doi.org/10.1111/eth.12298.
Moore, B. R. (1992). Avian movement imitation and a new form of mimicry: Tracing
the evolution of a complex form of learning. Behaviour, 122(3), 231e263.
Mui, R., Haselgrove, M., McGregor, A., Futter, J., Heyes, C., & Pearce, J. M. (2007). The
discrimination of natural movement by budgerigars (Melopsittacus undulatus)
and pigeons (Columba livia). Journal of Experimental Psychology: Animal Behavior
Processes, 33(4), 371e380. https://doi.org/10.1037/0097-7403.33.4.371.
Mui, R., Haselgrove, M., Pearce, J., & Heyes, C. (2008). Automatic imitation in bud-
gerigars. Proceedings of the Royal Society of Biological Sciences, 275(1651),
Nehaniv, C. L., & Dautenhahn, K. (2002). The correspondence problem. In
K. Dautenhahn, & C. L. Nehaniv (Eds.), Complex adaptive systems. Imitation in
animals and artifacts (pp. 41e61). Cambridge, MA: MIT Press.
Perry, S., Baker, M., Fedigan, L., Gros-Louis, J., Jack, K., MacKinnon, K. C., et al. (2003).
Social conventions in wild white-faced capuchin monkeys. Current Anthropol-
ogy, 44(2), 241e268. https://doi.org/10.1086/345825.
R Core Team. (2019). R: A Language and Environment for Statistical Computing.
Vienna, Austria: R Foundation for Statistical Computing. https://www.R-project.
Range, F., Huber, L., & Heyes, C. (2011). Automatic imitation in dogs. Proceedings of
the Royal Society B: Biological Sciences, 278(1703), 211e217. https://doi.org/
Range, F., Viranyi, Z., & Huber, L. (2007). Selective imitation in domestic dogs.
Current Biology, 17(10), 868e872.
Ratcliffe, D. (1997). The raven. A natural history in Britain and Ireland. London, U.K.:
Rendell, L., Fogarty, L., Hoppitt, W. J. E., Morgan, T. J. H., Webster, M. M., &
Laland, K. N. (2011). Cognitive culture: Theoretical and empirical insights into
social learning strategies. Trends in Cognitive Sciences, 15(2), 68e76.
Scheid, C., Pasteur, L., Range, F., & Bugnyar, T. (2007). When , what , and whom to
Watch? Quantifying Attention in Ravens (Corvus corax) and Jackdaws (Corvus
monedula), 121(4), 380e386. https://doi.org/10.1037/0735-7036.121.4.380.
Schwab, C., Bugnyar, T., & Kotrschal, K. (2008a). Preferential learning from non-
afﬁliated individuals in jackdaws. Corvus monedula), 79,148e155. https://
Schwab, C., Bugnyar, T., Schloegl, C., & Kotrschal, K. (2008b). Enhanced social
learning between siblings in common ravens, Corvus corax.Animal Behaviour,
75(2), 501e508. https://doi.org/10.1016/j.anbehav.2007.06.006.
owe, M., Bugnyar, T., Loretto, M.-C., Schloegl, C., Range, F., & Kotrschal, K. (2006a).
Novel object exploration in ravens (Corvus corax): Effects of social relationships.
Behavioural Processes, 73(1). https://doi.org/10.1016/j.beproc.2006.03.015.
owe, M., Bugnyar, T., Loretto, M.-C., Schloegl, C., Range, F., & Kotrschal, K. (2006b).
Novel object exploration in ravens (Corvus corax): Effects of social relationships.
Behavioural Processes, 73(1), 68e75. https://doi.org/10.1016/
Sturtz, S., Ligges, U., & Gelman, A. E. (2005). R2WinBUGS: A Package for Running
WinBUGS from R. 12 pp. 1e16). https://doi.org/10.7916/D80C55HH,3.
Tayler, C. K., & Saayman, G. S. (1973). Imitative behaviour by indian ocean bottlenose
dolphins (Tursiops aduncus) in captivity. Behaviour, 44(3), 286e298.
Tennie, C., Call, J., & Tomasello, M. (20 09). Ratcheting up the ratchet: On the evo-
lution of cumulative culture. Philosophical Transactions of the Royal Society B:
Biological Sciences, 364(1528), 2405e2415.
M.-C. Loretto et al. / Animal Behaviour 163 (2020) 127e134 133
Tennie, C., Call, J., & Tomasello, M. (2012). Untrained chimpanzees (Pan troglodytes
schweinfurthii) fail to imitate novel actions. PloS One, 7(8). https://doi.org/
Tomasello, M., Kruger, A. C., & Ratner, H. H. (1993a). Cultural learning. Behavioral
and Brain Sciences, 16(3), 495e511.
Tomasello, M., Savage-Rumbaugh, S., & Kruger, A. C. (1993b). Imitative learning of
actions on objects by children, chimpanzees, and enculturated chimpanzees.
Child Development, 64(6), 1688e1705.
al, J., Byrne, R. W., Mikl
osi, A., & Cs
anyi, V. (2006). Reproducing human actions
and action sequences:“Do as I Do!”in a dog. Animal Cognition, 9(4), 355e367.
Visalberghi, E., & Fragaszy, D. (2002). Do monkeys ape?": Ten years after. In
K. Dautenhahn, & C. L. Nehaniv (Eds.), Complex adaptive systems. Imitation in
animals and artifacts (pp. 471e499). Cambridge, MA: MIT Press.
Voelkl, B., & Huber, L. (2000). True imitation in marmosets. Animal Behaviour, 60(2),
195 e202. https://doi.org/10.1006/anbe.2000.1457.
Whitehead, H., & Rendell, L. (2015). Thecultural lives of whales and dolphins. Chicago,
IL: University of Chicago Press.
Whiten, A., Custance, D. M., Gomez, J.-C., Teixidor, P., & Bard, K. A. (1996). Imitative
learning of artiﬁcial fruit processing in children (Homo sapiens) and chimpan-
zees (Pan troglodytes). Journal of Comparative Psychology, 110(1), 3e14. https://
Whiten, A., Hinde, R. A., Laland, K., & Christopher, S. (2011). Culture evolves. Phil-
osophical Transactions of the Royal Society B: Biological Sciences, 366(1567),
Whiten, A., Horner, V., Litchﬁeld, C. A., & Marshall-Pescini, S. (2004). How do apes
ape? Animal Learning &Behavior, 32(1), 36e52.
Zentall, T. R. (2004). Action imitation in birds. Learning &Behavior, 32(1), 15e23.
Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/15161137.
Zentall, T. R., & Galef, B. G. (1988). Social learning: Psychological and biological per-
spectives. Hillsdale, NJ: L. Erlbaum.
Zuberbühler, K., Gygax, L., Harley, N., & Kummer, H. (1996). Stimulus enhancement
and spread of a spontaneous tool use in a colony of long-tailed macaques.
Primates, 37(1), 1e12. https://doi.org/10.1007/BF02382915.
M.-C. Loretto et al. / Animal Behaviour 163 (2020) 127e134134