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Preschool Children Fail Primate Prosocial Game Because of Attentional Task Demands Judith Maria Burkart*, Katja Rueth
Anthropological Institute and Museum, University of Zurich, Zurich, Switzerland
Abstract
Various nonhuman primate species have been tested with prosocial games (i.e. derivates from dictator games) in order to better understand the evolutionary origin of proactive prosociality in humans. Results of these efforts are mixed, and it is difficult to disentangle true species differences from methodological artifacts. We tested 2- to 5-year-old children with a costly and a cost-free version of a prosocial game that differ with regard to the payoff distribution and are widely used with nonhuman primates. Simultaneously, we assessed the subjects’ level of Theory of Mind understanding. Prosocial behavior was demonstrated with the prosocial game, and did not increase with more advanced Theory of Mind understanding. However, prosocial behavior could only be detected with the costly version of the game, whereas the children failed the cost-free version that is most commonly used with nonhuman primates. A detailed comparison of the children’s behavior in the two versions of the game indicates that the failure was due to higher attentional demands of the cost-free version, rather than to a lack of prosociality per se. Our results thus show (i) that subtle differences in prosociality tasks can substantially bias the outcome and thus prevent meaningful species comparisons, and (ii) that like in nonhuman primates, prosocial behavior in human children does not require advanced Theory of Mind understanding in the present context. However, both developmental and comparative psychology accumulate increasing evidence for the multidimensionality of prosocial behaviors, suggesting that different forms of prosociality are also regulated differentially. For future efforts to understand the evolutionary origin of prosociality it is thus crucial to take this heterogeneity into account.
Citation: Burkart JM, Rueth K (2013) Preschool Children Fail Primate Prosocial Game Because of Attentional Task Demands. PLoS ONE 8(7): e68440. doi:10.1371/ journal.pone.0068440
Editor: Roscoe Stanyon, University of Florence, Italy
Received March 14, 2013; Accepted May 30, 2013; Published July 3, 2013
Copyright: � 2013 Burkart, Rueth. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: The authors have no support or funding to report.
Competing Interests: The authors have declared that no competing interests exist.
* E-mail: [email protected]
Introduction
Humans stand out among primates with regard to their
prosocial behavior, and recent years have seen major efforts to
better understand the evolutionary origin of proactive prosociality
through comparative assessment of that trait across species.
Proactive prosociality (i.e., the economists’ other-regarding pref-
erences [1]) refers to intrinsically motivated prosocial behaviors
that occur spontaneously and are not solicited by the recipients
through direct requests or signaling of need. It has been
documented in several primate species, based on experiments
derived from the economic games typically played with human
subjects. Interestingly, the primate species that are most closely
related to humans are not the ones which score highest in such
games (reviewed in [2,3,4]) which suggests that phylogenetic
proximity to humans is not an important explanatory variable for
variation in primate proactive prosociality. Rather, convergent
selection pressures must be at work, such as the impact of extensive
allomaternal care [5].
However, valid inferences about the evolutionary origin of any
trait, including proactive prosociality, that are based on the
comparative approach critically require accurate measurement of
the trait across species. The use of identical paradigms and
procedures is an important first step in doing so. If such paradigms
reveal similar prosocial responses in different species, including
humans, it then becomes informative to have a close look at the
psychological regulation, for instance with regard to the motiva-
tions underlying the prosocial behavior or the necessity of Theory
of Mind understanding. Unfortunately, it is currently difficult to
disentangle true species differences in prosociality from method-
ological artifacts, because different versions of the predominant
paradigm to assess proactive prosociality, also referred to as
prosocial games [6], have been used for different species. Here, we
investigate how young human children perform in two commonly
used versions of the prosocial game when tested under conditions
identical to nonhuman primates (i.e. non-verbally, without
instructions, same procedures), and compare the psychological
regulation involved in their responses to other primate species that
behave prosocially in such games.
In humans, proactive prosociality is mostly assessed with
dictator games, i.e. anonymous one-shot interactions in which a
player receives an amount of money and has the opportunity to
share any portion of it with a recipient. Players often choose non-
zero contributions for the recipient, and thus show proactive
prosociality (e.g. [7]). Anonymous one-shot interactions are
thought to remove the possibility that players decide to give some
of the money to the recipient based on motives other than
proactive prosociality. Anonymity ensures that players are not
responding to solicitation by the recipient (signs or signals of need,
or even harrassement) and thus show reactive prosociality. The
experiments are one-shot, so players will not expect the recipient
to reciprocate the favor in the future.
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Nonhuman primate adaptations of the dictator game, the
prosocial games, typically give subjects the choice between
different payoff distributions (e.g. one piece of food for ego and
one for the partner [1,1] vs. one piece for ego and none for the
partner [1,0], Table 1). Importantly, the choices of the subject are
then compared to its choices in a control condition when the
partner is absent, to control for a simple preference for choosing a
larger amount of food (i.e. [1,1]) even if in the end, they only get
part of it. A prosocial effect is detected if subjects choose the
prosocial option (in this case, [1,1]) more often when a partner is
present than when it is absent. The distributions are typically
offered physically and the subjects can chose by instrumentally
pulling a tray within reach, but token-exchange versions have been
successfully implemented too [8,9,10].
Since it is not possible to test nonhuman primates in anonymous
one-shot interactions, further analyses have been added to
distinguish between proactive and reactive prosocial responses.
To qualify as proactive, prosocial responses must not be prompted
by recipients and thus also (even though not exclusively) occur in
the absence of any solicitation and signaling of need, such as
begging or reaching attempts [11]. The possibility for reciproca-
tion is removed by testing dyads in only one direction and by
observing the participants’ behavior immediately after the
experiment. In both human and nonhuman studies, it remains
difficult to fully exclude this possibility since in humans, the subject
may have a hardwired disposition to always expect repeated
interactions [12] or in nonhuman primates, reciprocation may go
unnoticed because it occurs after post-experimental observations.
However, at least the latter scenario is rather unlikely in
nonhumans because delayed reciprocation is supposed to be
cognitively demanding [13,14]. Indeed, it has been shown that in
tamarins, prosocial behavior emerges independently of reciprocity
[15], and explicitly offering the possibility to reciprocate does
usually not lead to systematically more prosocial choices in
chimpanzees [16,17,18] and also not in children younger than 4.5
years [6].
The first aim of this study was to assess the validity of different
versions of prosocial games by presenting them to young human
children at an age when a broad range of prosocial behaviors,
including proactive prosociality, is already established (reviewed in
[19,20,21]). Nonhuman primates have been tested with cost-free
and costly versions of the game, most commonly instantiated with
the payoff distributions [1,0/1,1] or [0,0/0,1], or variations of
them that include more vs less preferred foods (Table 1). Crucially,
in [1,0/1,1] or cost-free settings, the donor always receives a
reward but can opt, as a no-cost side effect, to also provide a
reward to the recipient. In contrast, in [0,0/0,1] or costly versions,
the donor never receives anything for itself, but can provide food
at some small cost, e.g. by pulling a tray representing the [0,1]
reward distribution within the recipient’s reach. It has been argued
that motivationally, the costly choice should be more demanding,
as it requires a higher degree of prosociality. Cognitively, however,
the cost-free option should be more demanding because the
subject has to focus attention on more than one piece of food
simultaneously [11], which may potentially lead to false negative
results.
If subjects pass the costly version, but fail the cost-free one, they
are prosocial but are confused by some aspect of the second
version (e.g. the presence of multiple pieces of food). If they pass
the cost-free, but fail the costly test, they are prosocial, but only if it
has no costs. Thus, if payoff distributions don’t matter, as implicitly
assumed by current comparative approaches, the children should
show correlated performance in both tasks, provided they have a
prosocial tendency. If the children show a stronger prosocial effect
in the costly version, this would reflect their young age (possibly
compromising attentional demands) and the strong prosocial
tendencies of children in general.
Whenever the children choose the prosocial option more often
when a partner is present in either version, the psychological
regulation of this behavior can also be addressed. Following the
logic applied in nonhuman primate studies, assessing the role of
solicitation by recipients (signs and signals of need, in human
subjects including verbal requests, verbal negotiation of recipro-
cation) will help disentangle reactive from proactive forms of
prosociality.
The second aim of our study was to assess whether the
performance of human children in the prosocial game is related to
their ability to understand others’ mental states, i.e. level of explicit
Theory of Mind (ToM) understanding. Intuitively, an intricate link
between prosociality and ToM-abilities exists: our decisions
whether and how to help others often include explicit consider-
ation of their needs, desires or beliefs. Indeed, empirical data from
human children suggests that such a link may indeed exist, e.g.
between mirror self-recognition and reactive comforting behavior
[22,23,24], and between the understanding of mind and emotions
and prosociality in preschoolers, with prosociality being assessed
by teacher ratings [24,25] or verbally with regard to future-
oriented prosocial choices [26].
However, prosociality is far from being a unitary phenomenon:
different kinds of prosocial behaviors follow different developmen-
Table 1. Prosocial games played with nonhuman primates.
Species Payoff- distribution Costly?
Prosocial effect?
Chimpanzee 1,0/1,1 no no1
Chimpanzee 1,(1)/1,1 a
no no 2
Chimpanzee 0,(1)/0,1 a
no no 2
Chimpanzee 1,0+0,1b yes no3
Common marmoset 0,0/0,1 yes yes 4
Capuchin monkey 1,1/1,1 c
no yes 5,d
Capuchin monkey 1,1/1,1 c no yes5,d
Capuchin monkey 1,1/1,1 c
no yes/no 6,e
Capuchin monkey 1,1/1,1 c
no yes/no 6,e
Cottontop tamarin 1,0/1,1 no no7
Cottontop tamarin 0,1/0,0 yes no 7
Cottontop tamarin 1,(3)/1,3 a
no no 8
Cottontop tamarin 0,(3)/0,3a yes no8
Long-tailed macaque 1,(1)/1,1 a
no yes/no 9,f
Studies differ with regard to payoff distribution, and whether help is costly. Included are studies only in which subjects have to choose between physically presented payoff distributions by pulling an apparatus within reach. Ref.:
1 Silk et al. 2005,
2 Jensen et al. 2006,
3 Vonk et al. 2008,
4 Burkart et al. 2007,
5 Lakshminarayanan and Santos 2008,
6 Takimoto et al. 2010,
7 Cronin et al. 2009,
8Stevens 2010, 9Massen et al. 2010. a reward written in ’’()‘‘ goes to an empty compartment and is therefore out of reach for both subjects. bdonor is allowed to choose both distributions during one trial. c 1 = favored reward; 1 = less favored reward; 1 = non-favored reward. dtested one-tailed t-test; but not statistically significant if tested two-tailed like other studies did. e yes for subdominant recipient, no for dominant recipient; no for subdominant if invisible, neg. for dominant if invisible. f yes for kin partner; no for non-kin partner; under both conditions prosocial tendency declined with increasing rank number. doi:10.1371/journal.pone.0068440.t001
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tal trajectories without being correlated to each other [27,28], and
are also supported by different neural substrates [29]. Accordingly,
the role of ToM-understanding has to be addressed for each
separately. Our particular focus on proactive prosociality is based
on evidence suggesting that phylogenetically, this trait may have
arisen in humans non-cognitively. The overrepresentation of
cooperatively breeding primates among species that show proac-
tive prosociality both in prosocial games and also under
naturalistic conditions [4] suggests that in humans too, proactive
prosociality may have arisen as a side effect of cooperative
offspring care, rather than resulted from highly advanced,
uniquely human socio-cognitive abilities [30,31]. If so, many of
our unique socio-cognitive capacities can more parsimoniously be
understood as a consequence of proactive prosociality, rather than
vice versa [5,32,33].
Proactive prosocial behavior in nonhuman primates, assessed
via social games, are highly unlikely to require explicit ToM-
abilities as a prerequisite since to date, there is no evidence that
nonhuman primates fully possess this ability. However, some more
basic ToM-related abilities have been reported for some nonhu-
man primate species. Nevertheless, the distribution of prosociality
measured in prosocial games among non-human primates (see
Table 1), though confusing, does not support the idea that such
more basic abilities linked to ToM are a limiting factor: The most
reliable evidence for prosocial choices in such games come from
capuchin and callitrichid monkeys (marmosets and tamarins),
rather than from chimpanzees, who have more powerful ToM-
abilities compared to the first two species, e.g. with regard to
mirror self-recognition, which is present in chimpanzees [34] but
not in cotton-top tamarins [35], marmosets [36] or capuchin
monkeys [37], or with regard to visual perspective taking, which
shows the same pattern of positive results in chimpanzees [38], and
negative results in capuchin [39] and marmoset monkeys [40].
Thus, across nonhuman primates, there is no link between ToM-
related abilities and the outcome of prosocial games.
Given these species differences, if in human children, explicit
ToM-reasoning turns out to be a precondition for behaving
prosocially in the prosocial games, this would suggest that we
measure a trait that is only superficially similar to nonhuman
primates. Furthermore, this outcome would be consistent with the
idea that prosociality is the result of our derived socio-cognitive
abilities [30,31]. Alternatively, explicit ToM-reasoning may not be
a precondition for and not promote proactive prosocial behavior.
Together with the nonhuman primate data, this would be
consistent with the idea that proactive prosociality rather enabled
the emergence of uniquely human social cognition, both
ontogenetically and phylogenetically [5,32,41].
Methods
Subjects 46 children (23 males, 23 females) were tested in three day-care
centers located in Zurich, Switzerland. The children were between
1.5 and 5 years old (mean = 3.47, sd = 0.73). 31 dyads were
composed and tested in one direction only to exclude reciprocity
effects. The children knew each other and dyads were composed of
same-age (median age difference in dyads: 3.7 months) and same-
sex partners whenever possible. The older subject within each
dyad played the donor role [42]. We included participants as
donors from an age of 2 years, which resulted in a mean age of
donors of 3.8 years (girls, sd = 0.54, n = 13) and 3.4 years (boys,
sd = 0.57, n = 18), respectively. Thus, 70% of the donors were
between 3 and 4 years old, an age range for which we expected
high variation in ToM understanding [43]. Children who
participated both as donor and recipient, did so first as donors,
to avoid carry-over effects.
The relationship quality of the dyads was rated by nursery
teachers as neutral (21 dyads), positive (9 dyads) or negative (1
dyad). The parents filled out questionnaires that allowed us to
calculate the socio-economic status (SES) (assessed according to
[44]) and gave information about the presence of siblings and
sibling position. The experiments were approved by the Ethik-
Kommission of the Kinderspital Zürich, Unterkommission SPUK.
The parents gave written informed consent for the childrens’
participation.
Prosociality Tasks Setup and apparatus. The experimental setup and proce-
dure were directly modeled after that used for marmoset monkeys
[11]. Two identical playpens were used as house-like compart-
ments, one for the donor and one for the recipient (Figure 1). The
compartments were separated by an opaque divider with a
window that allowed visual contact between donors and recipients.
Payoff-distributions were presented on a movable apparatus with
two stacked trays. On each tray two dishes were attached, one at
the donor- and one at the recipient side. The donor, but not the
recipient, could pull the trays within reach of both participants
because handles extended from the trays into the donor
compartment. In each trial, the donor could only pull one tray,
because pulling one tray automatically blocked the other one. A
curtain was placed in front of the playpens at a distance of circa
1.5 m and the entire apparatus could be moved forward to the
playpens and backward behind the curtain. This allowed the
experimenters to bait the apparatus out of view of the subjects
between trials. As reward we used fruits in the training phase and
sweets (Smarties) or salty snacks during the experiment, according
to individual preferences of both dyad partners.
Procedure. A trial started with an experimenter (E) saying
‘‘ta ta ta taaa’’ and opening the curtain. The apparatus was moved
towards to the compartments, which gave the donor the
opportunity to access the handles. After the participant had pulled
one handle or after a delay of 15 sec, a bell signaled the end of the
trail. The apparatus was moved back behind the curtain and the
curtain closed.
The experiment started with a warm-up phase, where
participants had the opportunity to get used to the presence of
the apparatus. They were allowed to freely explore especially the
house –like compartments for 10 min and shown that they could
be separated with the help of a partition. Next, we conducted a
demonstration phase where the experimenter was in the donor
compartment, and run a trial that was presented by a second
experimenter. The demonstration consisted in the experimenter
pulling a reward on its own side within reach and taking this
reward. The demonstration phase was necessary because pilot
trials revealed that unlike the marmoset monkeys, many children
were reluctant to enter the playpens. Following the demonstration,
we tested whether the child liked the reward. A plate with rewards
was offered and the experimenter asked if she liked the reward and
wanted a piece. The test was passed if the child took a reward, and
followed by the training phase after which the children had to be
able to handle the apparatus, and understand the consequences of
pulling the trays. During the training phase, the partition between
the compartments was removed and the subjects thus had access
to both compartments. For the costly payoff distribution (see
below) a reward was placed on one of the four dishes and by
pulling the correct handle the children could make the reward
available for themselves, either in the donor compartment, or in
the recipient compartment. If participants did not pull the correct
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tray in each position at least twice in a row in 20 trials they were
excluded from the study or were assigned to be recipients only.
Once they had passed this criterion, the partition was placed
between the compartments. Now the subject could experience that
she could no longer reach the reward if it was placed on the
recipient side of the trays and that even if pulling the tray with the
reward, they would not be able to obtain it. The procedure was
identical for the cost-free payoff distribution, with the exception
that during the training phase, the participants had to learn to
maximize their reward. Thus, three pieces of food were placed,
two on either board on the donor side and one on one board on
the recipient side and the participants had to pull the [1,1]
distribution rather than the [1,0].
During the experiment, the compartments were separated by
the partition. In the experimental condition, a partner was present
in the recipient compartment, but in the control condition, the
recipient compartment was empty. Each test and control condition
had 9 trials. Half of the dyads were first tested with the test
condition, the other half with the control condition. All training
and experimental phases were videotaped. Importantly, nursery
teachers were absent during testing, to minimize the possibility
that the children behaved prosocially to fulfill the expectations of
these authority figures.
Payoff distributions. Each dyad was tested with two
versions of the game. In the costly version, a reward was placed
in one of the four dishes, alternately on the upper or lower tray.
The reward was on the recipient side during the test trials, and the
subjects could choose to pull the board with the reward within
reach of the recipient, pull the empty board, or not pull at all.
During the first, the fifth, and the ninth trial, the reward was
placed on the donor side (as motivation trials), to keep the donors
engaged in the task as had previously been done for nonhuman
primates. In the cost-free version, the subjects could choose
between a tray baited with a reward for themselves but nothing for
the recipient, or one containing both a reward for themselves and
the recipient. Half of the dyads were first tested with the first
distribution, the other half with the other one.
Data coding. We recorded the response of the donor (pulling
the baited tray, the empty tray, or not pulling) during the
experiments and verified the coding twice afterwards by analyzing
the video tapes. Additionally, we coded the latency until the donor
child had pulled, and whether or not he had looked at the
partner’s plate before pulling. Furthermore, we coded the
recipient’s behavioral (looking at the reward, reaching for the
reward) and verbal (requests for help) signs and signals of interest
in the reward before pulling by the donor. We only recorded those
signs and signals that could be perceived by the donor. These
signals were coded per trial as present or absent. After the
recipient had taken the reward provided by the donor, we also
coded reactions by donors: the donor could not attend to the
recipient taking the reward, neutrally observe the recipient, or
observe her taking the reward with a positive emotional reaction
Figure 1. Experimental setting. Two playpens serve as compartment for the donor (D) and the recipient child (R). The handles (H) of the apparatus can be manipulated from the donor compartment only, and allow to pull the boards (U: upper board; L: lower board) with the dishes within reach. Between trials, the curtains are drawn. doi:10.1371/journal.pone.0068440.g001
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(smiling, verbal comments). Negative emotional reactions did not
occur. 10% of all trials were coded by a second rater. Reliability of
the response of the donor was complete (Cohen’s Kappa = 1).
Latencies where highly correlated between the raters with 93% of
the variation explained (n = 53, p,0.001), and the reliability for
the behavioral coding (signaling by the recipient and reactions by
the donors) was Cohne’s Kappa = 0.8.
Theory of Mind Tasks Materials and procedure. We used a test battery of four
socio-cognitive tasks originally developed by Wellman and Lu [45]
to assess the extent to which the children were aware of the fact
that desires, beliefs or knowledge of others can differ from their
own. A German version of these tests had been developed and
validated by Hofer and Aschersleben [46]. The tests consist of
illustrated short stories and could be ranked by increasing difficulty
on a Guttman scale (diverse desire, diverse belief, knowledge
access, content false belief) by Wellman and Lu [2004] and Hofer
and Aschersleben [2007]. A Guttman scale assumes that if one
passes a particular task, she also passes the lower ranked tasks.
Four tasks were presented in a single session for each child, in a
separate room at the day-care centers. Each of the tasks was coded
as passed or failed.
To validate that the performance in the ToM tasks can indeed
be ranked with increasing difficulty in our sample, we first used
Rasch analyses to validate the order of item difficulty calculated
with the Guttman Scale, as previously done by Wellman and Liu
[45] and Kristen et al. [47]. The dichotomous Rasch Model is a
probabilistic approach which estimates a person’s ability and item
difficulty. If a person’s ability is equal to item difficulty, then the
person passes this task with a probability of 0.5. If a person’s ability
exceeds the item difficulty, she passes this task with a probability
higher than 0.5, relative to the difference in levels and vice versa.
We calculated parameter estimates and fit statistics using the open-
source statistical language R following the protocol described by
Yuelin [48].
Results
Prosocial Behavior in the Costly v s. Cost-free Version In the costly version, the children pulled the prosocial tray more
often in the test condition when a partner was present than in the
control condition when the recipient compartment was empty, by
a margin of 30.1% (SEM = 6.5; one sample t-test on the difference
of prosocial pulling in test minus control conditions,
t(30) = 4.57 p,0.001). In contrast, no prosocial effect, i.e. no
significant difference between test and control condition (mean
difference: 6.77%, SEM = 4.78) was found in the cost-free version
(t(30) = 1.4, p = 0.167; Figure 2). The prosocial effect was bigger in
the costly version (t(30) = 2.75, p = 0.01), and due to more
prosocial choices in the costly version in the partner present
condition t(30) = 3.07 p = 0.004, whereas prosocial choices in the
partner absent condition (control) did not differ between the
versions (t(30) = 20.31 p = 0.76).
Prosocial behavior (difference of pulling the prosocial tray in test
minus control condition) did not increase with the children’s age in
both versions of the game (costly: Spearman’s Rho = 0.088, n = 31,
p = 0.97; cost-free: Spearman’s Rho = 0.198, n = 31, p = 0.282).
Furthermore, we analyzed the influence of additional factors on
prosocial behavior with Generalized Linear Models (GLM), with
the presence of a prosocial effect as response variable (i.e. subjects
pulling significantly more often in test compared to control
condition vs. subjects who did not discriminate), separately for
each version of the game. We found no sex differences (costly
version: z = 21.30, p = 0.19; cost-free version: z = 20.07,
p = 0.94), no effect of whether dyads were composed of same- or
different sex partners (costly version: z = 0.13, p = 0.90; cost-free
version: z = 0.82, p = 0.41), relationship quality of the dyad as
rated by the nursery teachers (costly version: z = 0.93, p = 0.35;
cost-free version: z = 20.36, p = 0.72), whether the donor child
had siblings (costly version: z = 0.01, p = 1.00; cost-free version:
z = 0.01, p = 1.00), older siblings (costly version: z = 20.01,
p = 0.99; cost-free version: z = 0.01, p = 1.00) or the sibling
position (costly version: z = 20.01, p = 1.00; cost-free version:
z = 0.01, p = 1.00). We found no effect of socio-economic status
(costly version: z = 0.55, p = 0.59; cost-free version: z = 1.11,
p = 0.27) and no order effects, neither for whether the experiment
started with test or control session (costly version: z = 21.04,
p = 0.30; cost-free version: z = 20.69, p = 0.49) nor for version
order (costly version: z = 0.27, p = 0.79; cost-free version:
z = 21.31, p = 0.19).
Attentional, not Motivational Processes Prevent Prosocial Responding in the Cost-free Version A possible explanation for the contrasting results in the two
versions of the game may be that in the cost-free version, the
donors simply did not pay attention to the recipient child’s payoff
because they were focusing on their own reward. If such
attentional limitations are responsible for the lack of prosocial
responding in this version, we should see that (i) donors pay less
attention to the recipients’ reward dish in the cost-free version
compared to the costly version, and thus (ii) pull more impulsively,
i.e. with shorter latencies. Furthermore, they should (iii) show less
interest in the consequences of their prosocial pulling because this
would often result as an unintended, and thus unnoticed,
byproduct of getting their own reward.
First, as shown in Figure 3, donors looked more often at the
partner’s plate before pulling when there was no reward on their
own side of the apparatus [0,1] than when there was a reward on
both sides [1,1], or during motivation trials when there was only a
reward on the donor’s side [1,0] (chi 2 test, x
2 = 285.62, df = 2,
p,0.001). Indeed, the presence or absence of a reward on the
donor’s side was a good predictor of looking at the recipient’s
reward position (Generalized Linear Mixed Model, random effect:
child, fixed effect: reward, Estimate = 26.127, Std. Error = 0.824,
z value = 27.433, p,0.001).
Figure 2. Prosocial effect. Donors’ (n = 31) pulling of the prosocial distribution ([0,1], or [1,1], respectively) in the presence (test condition, dark bar) or absence (control condition, light bar) of a recipient, for both versions of the dictator game. A prosocial effect was present only in the costly version of the game. ***: p,0.001. doi:10.1371/journal.pone.0068440.g002
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Second, as shown in Figure 4, the donors pulled with longer
latencies when only a reward for the recipient was present (test
trials of costly version) than when a reward was also present for the
subject herself (test trials of cost-free version, permutation test on
an one sample t-test statistic, p,0.001, n = 26) or exclusively for
the subject herself (motivational trials, permutation test on a one
sample t-test statistic, p,0.001, n = 26). Furthermore, the latencies
of the test trials of the cost-free version and the motivational trials
of the costly version did not differ significantly (permutation test on
a one sample t-test statistic, p = 0.184, n = 26). This suggests that
whenever the donors could get a reward for themselves, they
pulled with short latencies, regardless of what this meant for the
potential recipient.
Third, as shown in Figure 5, donors also varied in their
reactions when the recipient took a reward that had been pulled by
the donor for her (146 cases in the costly version, 108 cases in the
cost-free version). In the cost-free compared to the costly version,
the donors were more likely not to attend at all to the recipient
taking the reward (43.5% versus 13% of all cases, respectively),
and less likely to attend neutrally without observable emotional
reaction (43% versus 58%) and also less likely to attend and show a
positive emotional reaction (13% versus 29%; chi 2 test, x
2 = 31.85,
df = 2, p-value ,0.001).
Signs of Interest and Requests for Help Signs of interest (looking at and/or reaching for the reward) and
requests for help were not necessary to release prosocial choices
since in the costly version, 70.5% of all prosocial pulls occurred in
the absence of such signs and signals of need. Indeed, both signs of
interest (looking at the reward, reaching for the reward) and
requests for help did not increase prosocial pulls (Figure 6;
Generalized Linear Model on trial level with prosocial pulling as
response variables, and looking at reward (z = 21.085, p = 0.278),
reaching for the reward (z = 20.888, p = 0.375) and request for
help (z = 0.571, p = 0.568) as fixed factors). When we only examine
the first test trial per dyad, when any previous influence by
recipients can be excluded, 50% of all prosocial pulls occurred in
the absence of any sign or signal of need. In these first trials,
reaching (z = 21.278, p = 0.2) or requests for help 0.791, p = 0.43)
had no effect on prosocial pulling, but looking at the reward
(z = 22.139, p = 0.032) had a negative effect. In the cost-free
version, where we found no overall prosocial effect, the pattern of
results was the same.
Theory of Mind and Prosociality 30 of the 31 donor children attended the four socio-cognitive
tests (the youngest donor child [2.14 years] did not want to attend).
Each child passed at least one test. The maximum score reached
was 4 (cumulative numbers of tests passed). The average child
passed 2.17 tests (n = 24). 8 tests had to be excluded for 6 children,
Figure 3. Attention of donors to the partner’s plate before pulling. Percentage of trials when donors looked at the partner’s plate in test sessions of the costly version (reward on partner’s side), the cost- free version (reward on both sides) and during motivation trials (one reward on donor’s side). The presence of a reward for the partner in addition to a reward to the subject herself does not increase attention to the partner’s plate. doi:10.1371/journal.pone.0068440.g003
Figure 4. Pulling latencies. Latency to pull the prosocial tray during test trials in the costly version, the cost-free version, and to pull the board baited for oneself during motivation trials. The presence of a reward for the partner in addition to a reward to the subject herself does not increase the latency to pull. doi:10.1371/journal.pone.0068440.g004
Figure 5. Reactions of the donor children to recipients taking the provisioned reward. The children could either not attend to the recipient at all, attend with a neutral emotional expression, or attend with a positive emotional expression. doi:10.1371/journal.pone.0068440.g005
Preschool Children Fail Primate Prosocial Game
PLOS ONE | www.plosone.org 6 July 2013 | Volume 8 | Issue 7 | e68440
because of experimenter’s mistakes or inconclusive answers by the
participants.
We validated the ToM measure in two ways. First, we used the
Rasch model to validate whether the results from our sample fit a
Guttman scale. While the first task, the diverse desire task, was
passed by most of the participants (26/30), the number of children
who passed the following tasks decreased continuously, with only 2
children (out of 30) passing the final one. The fit statistics (Table 2)
indicate that our data correspond to the pattern described in the
much larger samples from Wellman and Liu [45] and Kristen
et al. [47]. Thus, as in the previous studies, performance in the
ToM tasks could be meaningfully ranked according to their
difficulty.
Second, ToM scores showed a weak sex difference with girls
outperforming boys (Mann-Whitney U = 37.5, p = 0.047), as
expected. However, due to the narrow range of ages tested,
ToM scores were not positively linked with age to a significant
degree (all subjects: Rho = 0.335, p = 0.109, n = 24; girls:
Rho = 0.311, p = 0.352, n = 11; boys: Rho = 0.251, p = 0.408,
n = 13).
Having validated our ToM scores, we asked whether they were
correlated with prosocial behavior, i.e. the difference of pulls in
test vs control sessions. This was not the case, either in the costly
(Rho = 20.028, p = 0.895, n = 24) or the cost-free version
(Rho = 20.101, p = 0.64, p = 24). Since mentalizing ability has
been hypothesized to impact reactive, rather than proactive
prosociality, we also analyzed proactive and reactive prosocial
behavior separately. For each donor, we calculated an index of
proactive prosociality, i.e. the proportion of all trials without
signaling in which donors pulled the prosocial option (where
signaled trials were those in which reaching for reward, looking at
reward, and requesting help by recipients occurred; signaling was
only included if it occurred prior to pulling and was perceived by
the donors). Likewise, we calculated the proportion of all trials
with signaling in which donors pulled the prosocial distribution.
Since part of these pulls may have been motivated by proactive
prosociality despite the presence of signaling, we calculated the
difference between the two proportions as index for reactive
prosociality (i.e. proportion of prosocial pulling in signaled trials
minus the proportion of pulling in non-signaled trials). Again,
ToM scores were not related to either proactive or reactive
prosociality, in the costly (proactive: Rho = -.242, p = 0.254,
n = 24; reactive: Rho = 0.021, p = 0.936, n = 18) as well as in the
cost-free version (proactive: Rho = 0.305, p = 0.148, n = 24;
reactive: Rho = 20.146, p = 0.650, n = 12; the higher sample sizes
for proactive pulling are due to the fact that the majority of all food
deliveries (70.5%) occurred in the absence of signaling).
Discussion
We assessed the validity of different versions of prosocial games
commonly used with nonhuman primates by presenting them to 2-
Figure 6. Effect of signs and signals of need on prosocial pulling. Percentage of trials in which prosocial pulling occurred following different kinds of signaling (dark bars) or without signaling (light bars). Figures inside the bars represent numbers of trials. For instance, prosocial pulling occurred in 85% of 121 trials in which no signaling of any kind occurred (total). Looking = recipient looks at reward; reaching = recipient tries to access reward with arm, request = recipient verbally asks for reward. doi:10.1371/journal.pone.0068440.g006
Table 2. Rasch analyses.
Items Children who passed (%) Item difficulty Standardized infit Standardized outfit
Content false belief 0.04 3.95 1.26 3.43
Knowledge access 0.42 0.02 1.02 1.18
Diverse belief 0.63 21.27 0.71 0.56
Diverse desire 0.83 22.71 1.00 0.78
The higher the ‘‘item difficulty’’ - score, the higher the difficulty level of the item. Fit statistics (standardized infit and outfit values) have an expected value of 0. Values .2.0 indicate a misfit [77]. doi:10.1371/journal.pone.0068440.t002
Preschool Children Fail Primate Prosocial Game
PLOS ONE | www.plosone.org 7 July 2013 | Volume 8 | Issue 7 | e68440
to 5-year old human children, i.e. at an age when prosocial
behavior can be expected. We used an identical experimental
setup and procedure as previously used to assess proactive
prosociality in marmoset monkeys [11] and implemented two
versions of the game, a costly and a cost-free one. Like the
monkeys, the children were tested with group members as
partners, had to pass pretest criteria to make sure that they had
understood the consequences of their choices, and were not
verbally instructed to behave prosocially. At the same time, we
assessed their level of ToM development with a set of standardized
tests [45,47].
Some Payoff Distributions Prevent Prosocial Responses Due to Attentional Demands As expected based on their age (reviewed in [19,20,21]), the
children behaved prosocially in the costly version of the game,
where the donor children could either provide a reward to the
partner or not, without ever obtaining anything for themselves.
However, prosocial behavior could not be demonstrated statisti-
cally with the cost-free payoff-distribution, despite a bigger sample
size than in typical nonhuman primate studies that mostly include
less than 20 subjects, often less than 10 (for references, see Table 1).
The absence of prosocial behavior in the cost-free version is
likely to be a false negative result, because the children did show
prosocial behavior in the motivationally even more demanding
costly version, where they incur a small cost (pulling the tray),
whereas in the cost-free version, they can provide food as a side
effect of pulling the tray for themselves. Detailed behavioral
analyses suggest that the false negatives occurred because the
donor children were oblivious to the donor dish as soon as their
own dish was baited: In the cognitively demanding but cost-free
version of the game, they were distracted by the opportunity to get
their own payoff, and did not pay attention to the recipients’
payoff. Indeed, their overall behavior in the cost-free version of the
game was the same as when they could pull food only for
themselves (i.e. in motivation trials) with regard to their attentional
focus and response latencies. When they nevertheless did provide a
reward in the cognitively demanding version, they likely more
often did so inadvertently, since they paid less attention to the
recipient actually taking the reward, and less often showed a
positive emotional reaction to the partner taking the reward
compared to the costly version.
The absence of prosocial behavior in the costly version of the
game is consistent with a recent result by House et al. [49], who
tested 3- to 8-year-old human children in a costly version of a
prosocial game previously used with chimpanzees [31]. The
children did not choose the prosocial option more often when a
partner was present (although a prosocial effect became apparent
after statistically controlling for trials that were accompanied by
laughter).
Our finding that payoff distributions critically matter whether a
prosocial effect can be found is highly relevant, because being able
to reliably assess prosociality across species is the crucial
precondition for properly identifying the socio-ecological factors
that favor the evolution of this trait. The costly payoff-distribution
or variations of it based on more or less desirable food, is popular
with researchers because it demands only minimal levels of
prosociality. Our results, however, suggest that it is exactly this
version of the game that this prone to false-negative results, and
this may arguably be the case in other species too. Indeed, for
some species, negative evidence for prosociality in instrumental
pulling taks contrasts with positive evidence from token exchange
paradigms [8,9], and one explanation may be that the latter
removes the attentional demands that may prevent prosocial
responding in instrumental pulling tasks.
The fact that seemingly trivial differences in experimental
design can have far-reaching consequences for our conclusions is
not unique to prosociality tasks but has been noticed repeatedly in
comparative cognition research in a broad range of domains, as
reflected in controversies surrounding visual-perspective taking
[50,51,52], object-choice tasks (reviewed in [53]) or causality
understanding [54,55,56,57]. In each of these cases, similar to the
present study, small methodological differences demonstrably lead
to fundamentally different conclusions about the presence or
absence of an ability; thus, whenever such methodological
modifications are confounded with species identity, it becomes
impossible to draw conclusions about species differences regarding
a specific ability.
Contemporary comparative cognition research thus faces a
serious challenge, and the recent recommendation by Silk &
House [3] that we urgently need standardized tasks that allow for
species comparisons, including humans, not only applies to
prosociality tasks. However, the situation may be particularly
precarious in tasks that not only involve an experimenter, the
subject, and the stimulus material, but in addition also a social
conspecific partner, as is the case in prosociality tasks. In such
situations, on top of having to manipulate a cognitively demanding
apparatus, subjects are involved in two social relationships
simultaneously, the one with the experimenter (who tries to be
as neutral as possible, but nevertheless will be perceived as a
intentional agent, even by small-brained monkeys [58,59]) and the
one with the conspecific social partner. That the simultaneous
integration of all these requirements is cognitively demanding is
evident from capuchin monkeys, who failed to show targeted
helping even though they separately understood the instrumental
task and showed a motivation to help in cognitively more simple
situations [60].
Ideally, such a standardized approach to assess proactive
prosociality relies on very simple, intuitive setup and not only
shows whether it is present in a species (for instance, in very
specific dyads under highly artificial dyadic experimental situa-
tions), but should also provide information about its distribution
across age and sex-classes and, most importantly, how prevalent it
is under naturalistic situations in the whole-group context (cf. [4]).
The recently developed group-service paradigm aims at providing
exactly this kind of information, by applying a single experimental
setup and procedure to assess proactive prosociality to a wide
range of species, testing them in their natural groups and over
extended periods of time [61].
Proactive and Reactive Prosociality Prosocial responses did not require explicit requests or even the
perception of signs or signals of interest in the food by recipients.
At least a part of the prosocial responses thus reflect proactive,
rather than reactive prosociality [4], as was the case in common
marmosets in the same test paradigm.
Signaling of need by recipients decreased, rather than increased,
prosocial choices. This is surprising in the context of the child
literature, where reactive sharing has been described to be more
robust and emerge earlier (e.g. [62]). It is less surprising, however,
in the context of the nonhuman primate literature. Signals of
interest such as begging and reaching attempts either had no, or
even a negative, effect in prosocial games in chimpanzees [8,63],
tamarins [64], and marmosets [11], and arguably only a positive
one in capuchin monkeys ([65] decline of prosociality when no
visual contact was possible]). This mostly negative influence of
signaling need may indicate species differences, but also, and more
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likely so, that behavioral categories used in these studies lump
together functionally highly heterogeneous signals. For instance,
unsuccessful reaching attempts may be understood as sign of need
and thus elicit prosocial behavior, but may also be perceived as
independent solution of the task. Thus, subjects observing the
recipient reaching for the food may automatically process this
event as ‘‘the recipient is accessing the food independently,
removing the need for my assistance.’’ This may also explain the
contradictory finding that in another recent study, signaling
promoted prosocial responses in human children [62], whereas in
the present study, it decreased them. Alternatively, this discrep-
ancy may reflect a more strategic decision to respond to an adult
authority figure rather than to a peer (see also below).
Disentangling different signs and signals, and whether and how
they are perceived by partners, is an important next step for future
research and possibly also key to understanding the distribution of
prosocial behaviors across nonhuman primates.
Under natural conditions, proactive prosociality of simple acts
such as food offering is more prevalent in monkeys, in particular in
cooperatively breeding ones with shared infant care, whereas
reactive prosociality is more prevalent in great apes, in particular
in the form of targeted, instrumental helping (reviewed in [3,4]).
An important factor contributing to this dissociation is likely to be
a cognitive one: targeted, instrumental helping arguably both
requires an understanding of the partner’s goals and a situational,
causal understanding of which behavioral means are most likely to
achieve these goals (see also [66,67]) as well as the ability to
integrate such representations in a helping motivation [60]. On
the other hand, proactive prosociality, typically measured in food
offering contexts may well rely on much simpler cognitive
regulation. Under naturalistic conditions, all individuals always
need food, and a representation of conspecifics as food-motivated
entities may thus be developmentally canalized. Thus, the current
pattern suggests that nonhuman primates vary with regard to an
intrinsic, proactive helping motivation expressed in cognitively
simple contexts, and also that some species such as chimpanzees
may be able to behave prosocially in more complex situations due
to more powerful cognitive capacities. Notably, these are not
necessarily the same species that show particularly high proactive
prosociality in the first place, but rather behave prosocially when
prompted to do so, by begging or even harassment. At the same
time, more general cognitive constraints may prevent other species
from showing instrumental helping despite high proactive helping
motivation.
Prosociality and Theory of Mind Higher levels of explicit ToM understanding did not increase
prosocial behavior in the prosocial game, in both versions of the
task. Likewise, ToM did not bias children towards more proactive
(i.e. the probability to pull prosocially in the absence of signs and
signals of need by recipients) or reactive prosocial tendencies (i.e.
the probability to pull prosocially as a response to signaling minus
proactive prosociality).
One might argue that our sample was too small to conclude that
no relationship exists between the level of ToM development and
performance in prosocial games. However, the ToM measure
employed was valid. In the present study, we were able to replicate
the findings by Kristen et al. [47] and Wellman and Liu [45]
regarding the increasing difficulty of the tasks. Further consistent
with other studies (e.g. [68,69]), girls slightly outperformed boys.
However, we found no significant age effect, presumably due to
the narrow age range of the participants which was chosen to
minimize the confounding effect of age when investigating the
relationship between ToM and prosociality. Because the measure
was valid, the absence of any correlation indicates that this
relationship, if present, could not have been strong.
Therefore, our results instead indicate that ToM reasoning is
not the key factor in eliciting proactive prosociality in young
children. This finding is consistent with the result by Sally and Hill
[70] who show that prosocial choices in the ultimatum game but
not in the dictator game are influenced by false belief
understanding. Dictator games are used by economists to assess
other-regarding preferences or proactive prosociality, whereas the
veto option in ultimatum games adds a strategic dimension [7].
Together, these results are in favor of scenarios that imply a very
early, rather indiscriminate onset of (proactive) prosociality during
human ontogeny, which is later constrained by strategic decisions
based on ToM reasoning (see also [6,71]). Thus, importantly,
ToM reasoning may not only drive decisions towards more
prosocial behavior, but also result in decisions when to inhibit a
prosocial impulse.
One possible caveat is that this conclusion is based on the use of
an explicit ToM measure. ToM development can be traced back
to much younger ages [72], and it can therefore be argued that it is
such earlier levels that are relevant for the emergence of
prosociality. Indeed, mirror self-recognition, for instance, as an
early manifestation of self-other differentiation has been linked to
the emergence of comforting behavior [22,23,73], i.e. one form of
reactive prosocial behavior. However, since comforting, helping,
and sharing are dissociated developmentally [27,28] and neuro-
biologically [29], these must be rather separate phenomena and
thus likely be regulated differently. Our experiment arguably
assesses sharing behavior (but note that subjects don’t give up any
of their own food), and the lack of a relationship is thus not
inconsistent with the above mentioned studies.
Whether earlier and more implicit forms of ToM play a role in
prosocial game performance cannot be answered based on the
present study. However, comparative data suggests it does not,
since those early ToM-related abilities evidenced by some species
do not predict prosocial game performance across nonhuman
primates. Some of these abilities are likely to be present in most
nonhuman primates (reviewed in [58,59,74]) whereas others, such
as mirror self-recognition, can only be found in great apes, but not
monkeys [34], including callitrichids [36]. Nevertheless, callitri-
chids, but not chimpanzees show proactive prosociality in
prosocial games. The socio-cognitive abilities that enable mirror
self-recognition may thus be relevant for the observed distribution
of reactive, instrumental helping across primates, as argued above,
but not involved in the regulation of proactive prosociality.
Conclusion This study leads to two important conclusions. First, seemingly
trivial differences in experimental design of prosociality studies can
have far-reaching consequences on our conclusions, including
differences regarding payoff distributions as in the present study,
but also the nature of the task (instrumental pulling vs. token
exchanges), the amount of time provided to respond, or competing
demands of attention and affect [75]. Any further advancement in
understanding the origin of prosocial behavior critically requires
unified approaches that yield comparable data, both at the
construct level and at the level of experimental design and
procedure.
Second, an emerging pattern of findings in both developmental
and comparative psychology is that prosociality is a multidimen-
sional phenomenon. In developmental psychology, different forms
prosocial behaviors have been shown to follow separate, non-
correlated developmental trajectories [27,28], to be supported by
different neural substrates [29], and to be regulated differently,
Preschool Children Fail Primate Prosocial Game
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with ToM, for instance, playing a role in some forms but not in
others ([22,23,24,26,70,76]; this study). Comparative data now
likewise points to the necessity to distinguish different kinds of
prosocial behavior, a key distinction being that between proactive
and reactive forms of prosociality, as reflected in the role of
understanding signs and signals of need for eliciting prosocial
behaviors, and the dissociation between performance in prosocial
games and targeted helping across species [3,4]. Merging the
findings from the two fields seems an obvious next step, and it is a
valid working hypothesis to assume that the distinct forms of
human prosocial behaviors may have different phylogenetic
histories. Once the evolutionary roots have been identified, we
can more easily examine the adaptive function of each kind of
prosocial motivation.
Acknowledgments
We would like to thank all the children for participating in this study, the
parents for their consent and filling out the questionnaires, and the staff of
the daycare centers for their support and the possibility to carry out the
experiments in their facilities. We are grateful for the highly valuable
comments and inputs by Trix Cacchione, Sonja Koski, Carel van Schaik,
Ellen Meulman and Joe Henrich on earlier versions of the manuscript.
Author Contributions
Conceived and designed the experiments: JB. Performed the experiments:
JB KR. Analyzed the data: JB KR. Wrote the paper: JB KR.
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