Primates' Socio-Cognitive Abilities: What Kind of Comparisons Makes Sense?

Integr Psych Behav (2015) 49:485–511 DOI 10.1007/s12124-015-9312-8 R E G U L A R A RT I C L E

Primates’ Socio-Cognitive Abilities: What Kind of Comparisons Makes Sense? Jill T. Byrnit 1

Published online: 29 May 2015 # Springer Science+Business Media New York 2015

Abstract Referential gestures are of pivotal importance to the human species. We effortlessly make use of each others’ referential gestures to attend to the same things, and our ability to use these gestures show themselves from very early in life. Almost 20 years ago, James Anderson and colleagues presented an experimental paradigm with which to examine the use of referential gestures in non-human primates: the objectchoice task. Since then, numerous object-choice studies have been made, not only with primates but also with a range of other animal taxa. Surprisingly, several non-primate species appear to perform better in the object-choice task than primates do. Different hypotheses have been offered to explain the results. Some of these have employed generalizations about primates or subsets of primate taxa that do not take into account the unparalleled diversity that exists between species within the primate order on parameters relevant to the requirements of the object-choice task, such as social structure, feeding ecology, and general morphology. To examine whether these broad primate generalizations offer a fruitful organizing framework within which to interpret the results, a review was made of all published primate results on the use of gazing and glancing cues with species ordered along the primate phylogenetic tree. It was concluded that differences between species may be larger than differences between ancestry taxa, and it is suggested that we need to start rethinking why we are testing animals on experimental paradigms that do not take into account what are the challenges of their natural habitat. Keywords Socio-cognitive comparisons . Referential gestures . Object-choice task . Primates . Gaze-following . Socio-ecological demands

* Jill T. Byrnit [email protected] 1

Department of Psychology, University of Southern Denmark, Campusvej 55, DK-5230 Odense M., Denmark

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Integr Psych Behav (2015) 49:485–511

In 1995, Anderson, Sallaberry, & Barbier introduced the object-choice task as an experimental paradigm to examine the capabilities of non-human primates (henceforth primates) to make use of referential cues. In the original or standard version of the object-choice task, one of three opaque containers or cups are baited behind a screen upon which an experimenter-given referential cue, typically a tapping or pointing gesture or a gaze, is directed toward the baited object, and the subject is requested to choose which one of the objects to turn over. Since Anderson and colleagues’ seminal study with capuchin monkeys (Cebus apella), several primate species have been tested on the task (Callithrix jacchus, Cebus apella, Eulemur fulvus, Eulemur macaco, Gorilla gorilla, Homo sapiens, Hylobates lar, Macaca fascicularis, Macaca mulatta, Pan paniscus, Pan troglodytes, Papio anubis, Pongo pygmaeus, Rhinopithecus roxellana, and Saguinus oedipus. See tables below for references). Although results have been very mixed, varying with species, subjects’ rearing histories, the nature of the experimenter-given cues, and the meta-procedures of the object-choice task, primates, overall, do not spontaneously (i.e. from the first trial on) perform successfully on standard versions of the task. They may learn how to use the cues over the course of the experiment, but only after receiving dozens or even hundreds of trials. This is surprising in several ways. Within their first year of life, human infants will follow the gaze of another person (Corkum and Moore 1995) and develop the ability to look toward the direction of a pointing gesture (Morissette et al. 1995). Furthermore, human infants will check back to a person if they find nothing interesting or unusual upon following his or her gaze (Butterworth and Cochran 1980), the so called double look. This has been taken to be an indication that children appreciate that other individuals are attending to something when they are looking somewhere, and developmental psychologists have suggested that these gaze following behaviors are intimately linked with advanced socio-cognitive capacities such as attribution of intentionality (Bretherton and Beeghly 1982). Within recent years, many primate species, besides humans, have been found to follow the visual gaze of a human experimenter (Tomasello et al. 1998; Bräuer et al. 2005; review in Rosati and Hare 2009), and some of these species appear to take the perspective of the experimenter. Thus, subjects will attempt to look around obstacles to see what the experimenter is looking at if his or her line of vision is blocked by a barrier (Povinelli and Eddy 1996a; Bräuer et al. 2005; Amici et al. 2009). Furthermore, they even perform the same kind of double looks as children if they find nothing noteworthy upon following the experimenter’s gaze (Call et al. 1998; Bräuer et al. 2005). However, when human infants as young as 14 months of age are required to follow the gaze of an adult to locate a hidden toy in a hiding game, they effortlessly do so (Behne et al. 2005) whereas non-human primates being directed toward hidden food at best show highly inconsistent patterns of results (see below for a review). Why do the apparent gaze following abilities and perspective taking skills of at least some primate species not transfer into successful use of cues as communicative gestures in the object-choice task? It has been questioned whether gaze-following in itself is indicative of the attribution of intent. Gaze following may serve a variety of purposes, many of which are of central importance to survival and reproduction. Gaze following may alert individuals to food, predators, or mates, and in group living animals, such as many primate species, it may further serve the purpose of keeping score on the relative status of group members, provide information on the whereabouts of allies and enemies and so forth. Given the


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great evolutionary advantages bestowed upon individuals following the gaze of others, it may be that reflexive eye-detector mechanisms have organisms follow the gaze of others without ever thinking about the intent of the looker (see Emery 2000). Within recent years, a number of studies have been conducted on the gaze following behaviors of non-primate animals. Unrelated and quite different species such as domestic goats (Capra hircus) (Kaminski et al. 2005), common ravens (Corvus corax) (Schloegl et al. 2007), and red-footed tortoise (Geochelone carbonaria) (Wilkinson et al. 2010) will follow the gaze of a conspecific or human experimenter, and, considering the diversity of the species tested, it seems plausible that we should expect to find the same gaze following abilities in many other animals. Being capable of following another individual’s gaze, however, is not necessarily the same as possessing the socio-cognitive capacity of appreciating that gazing behaviors signifies an attentional stance, or that gazing may be used deliberately by an individual to direct another’s attention towards something in their mutual vicinity. In a recent gaze following experiment (Liebal and Kaminski 2012), four different gibbon species (Hylobates pileatus, H. moloch, H. lar, Symphalangus syndactylus) looked up more when a human experimenter did so, but they did not perform double looks to check where the experimenter was looking. They did not habituate to the human looking up, either, and the authors conclude that although the gibbons cooriented with the human gaze, they did not appear to take the visual perspective of the experimenter. Other studies, though, have shown primate species to appreciate the attentional state of others. Hostetter and colleagues (2007) found that chimpanzees would display different and relevant kinds of behaviors, visible or vocalizations, in accordance with whether a human experimenter’s eyes were visible or closed/covered (but see Povinelli and Eddy 1996b). Likewise, chimpanzees appear to take into account the knowledge of others when participating in food competition with higher ranking individuals (Hare et al. 2001). Thus, at least some primate species seem to engage in more advanced cognitive processes than merely responding reflexively when following a gaze, and may appreciate something about the relationship between the senses and attentional states. This, however, does not mean that they understand the informational value of a communicative cue. Primates’ unsuccessful performance in the object-choice task, then, could be caused, not by a lack of gaze following skills (which many primate and non-primate species possess), nor by a lack of appreciation of the relationship between the senses and attention (which at least some primate species may also possess), but by a lack of understanding of the communicative purpose of somebody trying actively to direct your attention to something. Here we encounter the next surprise with the primate results of the object-choice task, for it turns out that a number of animal species may be better at employing human referential gestures than primates are. Within the last decade, a large variety of taxa have been tested on the object-choice task (reviews in Miklósi and Soproni 2006; Mulcahy and Hedge 2012). Domestic dogs have proven to be very good at using human cues of many different kinds such as pointing and gazing (Hare and Tomasello 1999; Hare et al. 2002; Bräuer et al. 2006; Kirchhofer et al. 2012), and they do so from the first trial on. Other species bred by humans also make successful use of human cues. Thus, cats (Felis catus) (Miklósi et al. 2005), domestic goats (Kaminski et al. 2005), horses (Equus caballus) (Maros et al. 2008), and domesticated silver foxes (Vulpes vulpes) (Hare et al. 2005) have been found spontaneously to use pointing and/

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or gazing cues. Other non-domesticated species living in daily, close contact with humans may show the same patterns as witnessed by the successful use of human cues by, for instance, South African fur seals (Arctocephalus pusillus) (Scheumann and Call 2004), bottlenosed dolphins (Tursiops truncates) (Pack and Herman 2004), various megachiropteran bats (Pterupus) (Hall et al. 2011), African gray parrots (Psittacus erithacus) (Giret et al. 2008), and hand-reared wolves (Canis lupus) (Udell et al. 2008). Much controversy exists as to the relative contribution of breeding phylogeny and ontogeny in the development of a species’ capability of employing referential cues. This is especially the case when interpreting the results from studies on dogs and wolves (see Wynne et al. 2008; Dorey et al. 2010; Hare et al. 2010; Udell et al. 2010). These results, controversy notwithstanding, are that numerous non-primate species appear to make better use of referential cues in the standard version of the objectchoice task than primates. Leading some authors to draw the conclusion that there exists a discrepancy between the primate and non-primate data, particularly for nondomesticated species (Mulcahy and Call 2009), while others conclude that whereas a variety of non-primate species can pass the object-choice task, all species of great apes, by contrast, have enormous difficulties with the task (Mulcahy and Suddendorf 2011). Over the years, different hypotheses have been put forth to explain why primates, or subsets of taxa within the primate phylogenetic tree such as great apes, do not make better use of the cues in the object-choice task, or why other animal species may do better on the task. Among the more prevalent hypotheses is the suggestion that primates’ competitive life-style inhibits the utilization of referential cues in the standard cooperative configuration of the object-choice task where subjects must understand that another individual deliberately will guide them toward attractive food (Hare et al. 2001; Vick and Anderson 2003; Hare and Tomasello 2004). Alternatively, that domestication of some animal species, especially the dog (and, notably, not any primate species), has sensitized these species to human cues (Hare and Tomasello 1999); that being reared by humans may Benculturate^ great apes to attend to humans’ referential behaviors (Tomasello and Call 2004) as they have come to see humans as problem-solving experts (Bering 2004), or may simply condition animals that spend much time with humans (such as lab-trained primates or show-trained sea mammals) to follow human’s referential cues. In a recent review by Mulcahy and Hedge (2012), it was concluded that the central object-choice version Bthat is only used with apes and other primates typically results in failure^ (p 313). The authors went on to suggest that the reason for the discrepancy between primate and non-primate results on the task is differences in methodology, and that the more peripheral method often used with other animal species will vastly improve primate performance. Given the large differences that exist between critical components across the objectchoice studies, each of the above hypotheses have currently only been put to the test in a few experimental studies and too few data are available to compare the predicative powers of the different claims. The results of future studies will inform us of the merits of the respective hypotheses. However, in the present paper, the argument will be made that not only have almost 20 years of painstaking object-choice work not sufficed to establish all-encompassing principles on primates’ performance on the task, but that neither should we expect in the future to find any one method, procedure, or type of cues that will act as the catalyst to an understanding of what impedes or facilitates the performance of apes, monkeys, or any other such subset of primate taxa. Theories on


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primates’ use of cues in the object-choice task appear to take as their implicit starting point that the object-choice paradigm, if administered the Bright^ way, will allow all primate species, or even all animal species, to display their potential understanding of other’s communicative intent. However, this starting point does not take into account the unparalleled diversity that exists between species within the primate order, including of those parameters that are highly relevant to the requirements of the object-choice task, and to which I shall return later in the discussion. In order to examine whether phylogenetic relationships along the primate tree offer a fruitful organizing framework within which to interpret the results, a review was made of all published results from 1995 to 2014 on primates’ use of gaze cues on the object-choice task. Comparisons were made between frequently used subsets of primate taxa with the hypothesis that no clear, consistent picture would emerge of subset differences in performance. Furthermore, it was hypothesized that no meta-procedures or cues would uniformly facilitate or impede performances with phylogenetic group as the organizing principle.

Methods A literature search on the database GoogleScholar was made on studies examining primates’ use of gaze and glance cues on the object-choice task. The key phrases Bprimates object-choice task^ and Bprimates gaze-following^ were used to find potentially relevant studies from the time period 1995 to February 2014. A plethora of studies have been made over the years on primates’ gaze-following abilities with paradigms that resemble the object-choice task on one or more central features. In order to focus the present review on comparisons frequently made in the literature on non-human primates’ abilities on the object-choice task, only studies which were specifically noted to be employing an object-choice paradigm, or in which it was clear from the introduction and method that this was the purpose of the study, were included in the final review. The latter took the form, for instance, that the authors described in detail the seminal object-choice study by Anderson, Sallaberry, and Barbier (1995) and referred back to this or similar studies when conducting their own study. A number of review articles on the object-choice task have already been published, and their reference lists were used to cross-check for relevant studies to be included in the present review. For the purpose of comparisons, the total numbers of individuals from different primate species were counted and are listed in the tables. This is not an authoritative count as there is considerable overlap in individuals as many of these have participated in several studies and not all authors provide names or other identification markers of their subjects. On face value, it seems that the great apes may be overrepresented in the total counts as the same names of individuals appear in several studies. However, given the fact that the same, relatively few, primate labs have been conducting a large majority of the studies on all species studied, and many studies from the same labs have been conducted within a few years’ time span, it seems reasonable to assume that not only the great apes, but also the other primate species are represented by fewer individuals than indicated in the count. Thus, the count is provided to give a very rough impression of the differences in numbers of animals tested, but is not meant as an authoritative count of different individuals in itself.

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Results Tables 1, 2, 3 and 4 presents an overview of all studies conducted from 1995 to February 2014 on primates’ use of referential gaze and glance cues in the object-choice paradigm. The standard object-choice task refers to the paradigm in which one of two or three opaque objects is baited behind a screen upon which a human (or, occasionally, a conspecific) direct a referential gaze or glance cue toward the baited object, and the subject is requested to choose which one of the objects to turn over. In glance cues the head is fixated toward a central point, while eyes rest at the object. Gaze cues may be emitted Bclose^ or Bfar^ from the object, and, quite confusingly and unfortunately, procedures as to what constitutes far and close gazes are not standardised but take many different forms, not only depending on the differences in size of the primate species tested, but also on more or less unspecified preferences of the authors. Some studies have employed a criterion for successful performance of 80 % correct choices in two consecutive sessions; others examine first trial/ single-trial effects. In the review, the authors’ published results and conclusions are used. When the authors themselves comment on significant results that did not meet the 80 % criterion, it is noted in the tables. Subjects’ rearing histories are included where these have been explicitly stated by the authors, or have been deducible from the articles.1 Species have been ordered after ancestry within the primate phylogenetic tree in the categories of prosimians, New World monkeys, Old World monkeys, and apes. In the tables, same-species studies are ordered chronologically after year of publication, and where more studies from the same year exist, after surnames of first authors. Several of the studies have tested other referential cues than gazing and/or glancing, such as pointing or tapping cues. Subjects’ use of the latter cues in these studies is only mentioned when it may be of direct relevance to their use of gazing or glancing cues. In the headings below and in the tables, Bgaze cues^ refer to both gaze and glance cues. Prosimians’ Use of Gaze Cues in the Object-Choice Task In Table 1 is presented the sole study on prosimian species’ use of referential gaze and glance cues in the object-choice task (Ruiz et al. 2009). Two species were tested, brown and black lemurs (Eulemur fulvus and Eulemur macaco), with the use of an objectchoice task that had been modified to take into account that cues emitted by a conspecific may be more salient and interesting than those given by a human experimenter. Subjects were filmed while presented with a color photo of the adult male in each of their respective groups gazing toward the baited object, and the films were analyzed in terms of whether the lemurs 1) followed the gaze of the photographed male, and 2) chose the object indicated by his gaze. If analyzed solely in terms of successful 1 Rearing categories (after Call and Tomasello (1996). Captive: Many zoo animals and some from laboratories. Have interacted directly with humans only minimally such as, for instance, during feeding and cleaning situations; Nursery-raised: Have been raised from an early age in a nursery setting with peer conspecifics and much contact with human caretakers; Laboratory-trained: Have been raised in captivity and trained in particular tasks, often many kinds, over the years; Home-raised: Also termed enculturated. Have been raised by humans and have participated extensively and intensively in interactions with them and their artifacts in a home-like cultural environment. Many home-raised individuals have also been exposed to some kind of language-training.

Photo of conspecific cue Photo of conspecific cue

No*

No*

Close gaze (head-and-eyes) Far gaze (head-and-eyes) Glance (eyesonly)

Remarks

In the cue cells, Byes^ indicates that at least one subject used the cue consistently, and Bno^ indicates that no subject ever used the cue consistently. An empty cell indicates that the cue was not included in the study. * Significant use of the cue when subjects already co-oriented gaze with the conspecific model. For more details, see review in the main text

Captive

Captive

N= Subject’s rearing history Procedure

4

Ruiz et al. (2009) Eulemur fulvus

Species

Ruiz et al. (2009) Eulemur macaco 2

Study

Table 1 Prosimians’ use of referential gaze cues in the object-choice task

Integr Psych Behav (2015) 49:485–511 491

Cebus apella

Vick and Anderson (2000)

3

1

Captive

Standard

Standard

Standard

Standard

9 containers + 2 choices

1 hand-reared

Captive

Standard

Procedure

9 captive

Subject’s rearing history

Yes

After 120 trials

No

Yes*

Close gaze (head-and-eyes)

Yes

After 90 trials

Yes**

No

Far gaze (head-and-eyes)

After 30–330 trials (w. alternation of eyes between subj. and obj.)

No

No

Yes**

Glance (eyes-only)

In the cue cells, Byes^ indicates that at least one subject used the cue consistently, and Bno^ indicates that no subject ever used the cue consistently. An empty cell indicates that the cue was not included in the study. For more details, see review in the main text. * Non-significant trends. ** Significant results, but did not reach criterion level

Cebus apella

Itakura and Anderson (1996)

3

4

Saguinus oedipus

Cebus apella

Neiworth et al. (2002)

Anderson et al. (1995)

10

Callithrix jacchus

Burkart and Heschl (2006)

N=

Species

Study

Table 2 New World monkeys’ use of referential gaze cues in the object-choice task

492 Integr Psych Behav (2015) 49:485–511

40

Macaca mulatta

Papio anubis

Papio anubis

Papio anubis

Rhinopithecus roxellana

Hauser et al. (2007)

Vick et al. (2001)

Vick and Anderson (2003)

Schmitt et al. (2012)

Tan et al. (2013)

Captive

Captive

Captive

Captive/some lab-training

Captive

Free-living

Captive

Yes

Recr.opp.box

Standard

Standard

Competitive

No

No

Yes*

No

Yes

Standard

No

No

Yes

Recruitment

No

Standard

Standard

Standard

After 330 trials

No

No

Gaze alternated between object and subj.

Used gaze also when eyes closed or looking upward from obj.

Exp. walked away after giving the cue.

Close gaze Far gaze Glance (eyes-only) Remarks (head-and-eyes) (head-and-eyes)

In the cue cells, Byes^ indicates that at least one subject used the cue consistently, and Bno^ indicates that no subject ever used the cue consistently. An empty cell indicates that the cue was not included in the study. For more details, see review in the main text. * Significant result, but did not reach criterion until after 150 trials

5

5

4

4

3

Macaca fascicularis 13

Schmitt et al. (2012)

Anderson et al. (1996) Macaca mulatta

N = Subject’s rearing Procedure history

Species

Study

Table 3 Old World monkeys’ use of referential gaze cues in the object-choice task


Species

Hylobates lar

Pongo pygmaeus

Pongo pygmaeus

Gorilla gorilla

Gorilla gorilla

Pan paniscus

Pan paniscus

Pan troglodytes

Pan troglodytes

Pan troglodytes

Pan troglodytes

Study

Inoue et al. (2004)

Itakura and Tanaka (1998)

Byrnit (2004)

Peignot and Anderson (1999)

Byrnit (2009)

Bräuer et al. (2006)

Lyn et al.(2010)

Povinelli et al. (1997)

Call et al. (1998)


Itakura et al. (1999)

4/12

2

6

7

7

4

3

4

3

1

1

N=

2 home-raised

Lab-trained

2 home-raised 4 lab-trained

Lab-trained

Home-raised

Lab-trained

Nursery

Not reported, but exp.naïve

Captive

Home-raised

Home-raised


Table 4 Apes’ use of referential gaze cues in the object-choice task

Standard

Yes

Yes

Barrier Standard

No Yes

Tube

No

No

Yes

Yes

Yes

Yes

Yes

No

Yes

No

Yes

1 subj.after 28 trials

Yes

Yes

After 30–150 trials

No

No

Yes

Yes

Close gaze Far gaze Glance (eyes-only) (head-and-eyes) (head-and-eyes)

Standard

Standard

Standard w. tubes

Physical/causal

Standard

Standard

Standard

Standard

Standard

Standard

Procedure

Home-raised subj. scored higher with tube and barrier

Subj. were pre-trained to use pointing cues. Use of gaze cues in the second experiment.

Point with alternating gaze between obj. and subj. Gaze with vocalization and alternating between obj. and subj.

Described as enculturated acc. to her dev. story with human caregiver

Remarks


Pan troglodytes

Pen troglodytes

Pan troglodytes

Okamoto-Barth et al. (2008)

Lyn et al. (2010)

Pan troglodytes

Barth et al. (2005)

Pan troglodytes

Pan troglodytes

Call et al. (2000)

Herrmann and Tomasello (2006)

Pan troglodytes


Bräuer et al. (2006)

Species

Study

Table 4 (continued)

10

3

10

12

5–7

12

7

N=

4 home-raised

6 lab-trained

Lab-trained

Nursery + lab-trained

Lab-trained

Nursery + lab-trained

2 home-raised 10 lab-trained

Standard w. tubes

Standard

Competetive (prohibiting)

Cooperative

Standard

Yes

25–33 months: After 64–80 trials

No

No Yes

No

Approach exp. No

Yes

Longitudinal study with repeated testing of subj. from 8 months to 3 years of age.

No

No

Yes


Standard

Standard

Leave procedure

Conspecific

10 lab-trained (not all subj. used in all exp.) Lab-trained

Procedure


Gaze w. alternation between obj. and subj.

Sign. performance w. point w. vocalizations.

Sign. use of competitive cue

Pointing use equally well above obj.

Sign. use of both human and conspecific cue when they approached and squatted beside the baited obj.

Remarks


Homo sapiens

Homo sapiens

Homo sapiens




24 3-year-olds

10 2- year-olds

36 2 & 3year-olds

N=

Home-raised

Home-raised

Home-raised


Standard

Standard

Standard

Procedure

Yes

Yes Yes

Yes

Yes

No

Yes


Children differentiated between cues directed at or above the object.

Gaze: Only 3-year-olds

Remarks

In the cue cells, Byes^ indicates that at least one subject used the cue consistently, and Bno^ indicates that no subject ever used the cue consistently. An empty cell indicates that the cue was not included in the study. For more details, see review in the main text

Species

Study

Table 4 (continued)



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use of the referential cue, the lemurs showed highly inconsistent results ranging from 10 to 100 % correct in a given session. If, however, the subjects’ choice behavior was put in relationship to their gaze-following, it turned out that when the lemurs successfully co-oriented with the photographed male, he or she was significantly more likely to choose the correct location. New World Monkeys’ Use of Gaze Cues in the Object-Choice Task In Table 2 is presented the studies done on New World monkey species’ use of referential gaze and glancing cues in the object-choice task. Three different species have been tested: common marmosets (Callithrix jacchus), cotton top tamarins (Saguinus oedipus), and capuchin monkeys (Cebus apella). In Burkart and Heschl’s (2006) study, 10 common marmosets failed to make consistent use of a far gaze cue with head and body oriented toward the baited object in a standard version of the task. Although given a total of 180 trials, the marmosets did not learn to use the cue either. In an inventive variation of the task, subjects performed markedly more successfully. Instead of two containers, subjects had to choose between nine containers, but also were given the opportunity to check two instead of only one container. In this variation, the marmosets were able to employ both distant gaze and glance cues to choose the correct container. The authors note, however, that even if statistically significant, the performances did not reach standard criterion on 80 %, and no learning effect could be observed. In a study from 2002, Neiworth and colleagues found that a group of four cotton top tamarins did not significantly use gaze or glance cues, and no learning appeared to take place across trials. The results, however, showed non-significant trends that the group used gaze, but not glance to choose between objects, and this despite the fact that the gaze cue was interspersed with trials that delivered no reinforcement for correct choices, trying to minimize the effects of operant conditioning. In the seminal study introducing the object-choice paradigm, Anderson et al. (1995) tested three capuchin monkeys for their use of gazing (and pointing) cues, and, later, capuchins have been tested by Itakura and Anderson (1996), and Vick and Anderson (2000). Anderson et al. (1995) found a gaze cue to be a highly inefficient cue for the capuchins that did not use the cue, not even after receiving a total of more than 1050 gaze trials. Better use of gaze cues were found by Itakura and Anderson (1996) where one capuchin after 120 trials learned to use both distal and proximal gaze cues after, spontaneously, employing tapping and pointing cues. The subject did not learn to use a glance cue although receiving 240 trials. Three capuchins tested by Vick and Anderson (2000) needed 30–120 trials to reach criterion with a tapping cue. Afterward, two of the subjects spontaneously made use of gaze cues. No subjects spontaneously employed a glance cue, but were able to learn to use various combinations of eyes-alone cues (eyes close to object, far from object, or with head fixated centrally) after around 30–300 trials. Old World Monkeys’ Use of Gaze Cues in the Object-Choice Task In Table 3 is presented the studies on Old World monkey species’ use of referential gaze and glance cues. Data on four species are available: long-tailed and rhesus

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macaques (Macaca fascicularis and Macaca mulatta), olive baboons (Papio anubis), and golden snub-nosed monkeys (Rhinopithecus roxellana). Schmitt and colleagues (2012) found inconsistent use of gaze cues when they tested 13 long-tailed macaques’ on the object-choice paradigm as part of a larger series of tasks in the so-called Primate Cognition Test Battery introduced by Herrmann et al. (2007). Three of the subjects performed better than random chance. Another macaque species, rhesus macaques, have also shown unsuccessful use of cues in the standard version of the task. Anderson et al.’s (1996) three rhesus macaques subjects did not use gaze or glance cues. Hauser and colleagues (2007) also tested rhesus macaques and found better use of cues in a modified version of the task. The authors tested 40 free-living (but experimenter-habituated) subjects, exploring mostly first-trial effects, with a variety of cues and a procedure where the experimenter walked away after giving the cue. When the standard-type gazing cues were given, the rhesus macaques were not able to employ the cue. However, when the cues were accompanied by a species-specific recruitment gesture (head jutting between potential ally and adversary in a fight), subjects made use of gazing and the recruitment gesture from opposite box to direct them toward the baited box. Three studies have examined the use of referential cues in baboons. Vick et al. (2001) tested four subjects for their use of a gaze or a glance cue. None of the subjects reached criterion with either cue, not even after receiving around 750 trials. In contrast, Vick and Anderson (2003) found baboons to make use of a gaze cue when the basic requirements of the task was altered from cooperative to competitive, making the correct choice of container the one that the experimenter was not oriented toward. One of the subjects performed spontaneously above chance, although taking 150 trials to reach criterion. The baboons were not making successful use of the glance cue where just one subject reached criterion after 330 trials. Not even after receiving more than 750 trials did the remaining subjects use this cue. Schmitt et al. (2012) tested five baboons on the Primate Cognition Test Battery and did not find any significant use of a gaze cue. Recently, the only object-choice study done on a member of the Colobinae subfamily was presented in which Tan et al. (2013) did not find five golden snub-nosed monkeys to make use of gazing cues (with alternation of gaze between subject and object) to either direct them toward or actively avoid the baited object. Neither did the results show any learning effects. Apes’ Use of Gaze Cues in the Object-Choice Task Apes’ use of referential gaze and glance cues in the object-choice task is presented in Table 4. One lesser ape species (whitehanded gibbon, Hylobates lar), all nonhuman great ape species (orangutans, Pongo pygmaeus; gorillas, Gorilla gorilla; bonobos, Pan paniscus; and chimpanzees, Pan troglodytes), and human children (Homo sapiens) have been tested. For the purpose of the present review, studies on human children have only been included if they directly compare the performance of humans and other primate species in the object-choice task. In the single study conducted with a lesser ape species, Inoue and colleagues (2004) found their white handed gibbon subject to make successful use of, both, gaze and glance cues, and she did so from the very first trial on.


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Only two studies have been conducted over the years on orangutans’ use of gaze cues in the object-choice task. Itakura and Tanaka (1998) and Byrnit (2004) found orangutans to make spontaneous use of gazing cues. Itakura and Tanaka (1998), furthermore, found spontaneous use of glancing. Byrnit’s (2004) subjects, however, had to receive 28 trials to use a distal gaze cue, and were not able to use glancing as a cue, not even after receiving around 100 trials. Gorillas’ use of gaze cues has also only been examined two times in the context of the object-choice task. Peignot and Anderson (1999) found their subjects to employ gaze cues but not glance whereas Byrnit’s (2009) subjects did not perform successfully with a gaze cue. Bonobos have been the subjects of two object-choice studies where gaze was used as the referential cue. Bräuer et al. (2006) did not find use of gaze cues, neither in conditions where gaze was continuously on the baited object, nor when the gaze alternated between subjects and the object. Lyn et al. (2010), in contrast, found use of gazing when gaze alternated between subjects and a baited tube, or when an additional vocalization Bfood grunt^ was made in close contact to the baited tube. Of all primates, chimpanzees, by far, are the species most extensively studied on the object-choice task. They have been tested with a variety of different cues and metaprocedures, and have come from many different kinds of rearing and lab-experience conditions. They are also the only species to be participants in a longitudinal study following the development of their use of cues. Results have been quite mixed. Itakura and Tanaka (1998) found that chimpanzees spontaneously were able to use gaze cues successfully. Other findings, however, have showed a much more inconsistent picture. In the standard version of the task, negative results have been reported by Call et al. (1998), Barth et al. (2005), Bräuer et al. (2006), and Herrmann and Tomasello (2006), and positive results by Itakura et al. (1999). Povinelli and colleagues (1997) found use of both distal and proximal gaze cues in the second, but not the first of a series of experiments. However, Povinelli et al. (1999) found chimpanzees spontaneously to use a proximal, but not distal gaze cue in a procedure where subjects were to enter the testing room while the cue was emitted. Employing a similar procedure, also Barth and colleagues (2005) found successful use of a gaze cue. Call and colleagues (1998) modified the task to make use of objects with which the subjects had previous experience, replacing opaque containers with tubes which were open in both ends, but had a piece of cardboard fitted into the middle, blocking a clear view all the way through. The chimpanzees’ performance was highly significant in the tube condition. However, when tubes were substituted by plastic barriers, the chimpanzees did not perform more successfully than with the standard opaque containers. Lyn et al. (2010) also employed tubes instead of containers and found successful use of a gaze cue that alternated between the subject and the baited tube. Call et al. (2000) tested chimpanzees with a variety of cues combining either a gaze or a glance cue with simulated chimpanzee food barks, or other kinds of noise: a snap of the fingers, a slap of the ground, or a tape recorded sound of a bicycle horn. For instance, in one condition, the experimenter would turn his or her head toward the baited cup and give a food bark, upon which the subject, as usual, was to choose one of the cups. In another condition, the experimenter would look at the subject, vocalize, and then turn to look at the object. The rest of the conditions were different variants of this scenario, except for two conditions: a glance-only condition (unaccompanied by any sound) and a

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vocalization-only condition (unaccompanied by other cues). The chimpanzees as a group spontaneously performed better than chance in all conditions in which some kind of sound appeared (be it food barks, snaps, slaps or horns) together with the experimenter’s gaze or glance cue. In contrast, the group as a whole was not able to make use of either a vocalization-only cue or a glance-only cue. Only two other studies have examined chimpanzees’ use of glancing (Itakura and Tanaka 1998; Barth et al. 2005), both with negative results on a standard version of the task. Okamoto-Barth et al. (2008), in the only longitudinal primate study with the object-choice task, found chimpanzees to learn how to use distant gaze at around 25–33 months of age. Subjects, however, did not spontaneously make use of the cues, and required between 16 and 104 trials to reach criterion in the respective conditions, despite being subjected to testing on the task with tapping and pointing cues repeatedly through their infancy. Over the years a handful of studies have directly compared human children’s performance on the object-choice task with that of other primate species, specifically great ape species (see review above of their performance in the same studies). The children have ranged between the age of 18–36 months, and they have been exposed to the standard paradigm and standard cues with one exception where they were tested on a competitive version of the task. Their use of gaze cues has varied consistently in relation to their age. Thus, children the ages of 2, 2 ½, and 3 years old make successful use of close/proximal gaze cues (Itakura and Tanaka 1998; Povinelli et al. 1999). Children within this age span also are able to differentiate between gaze cues directed at or above the baited object (Povinelli et al. 1997). Itakura and Tanaka (1998), furthermore, have found 2-year-olds to make use of far/distal gaze and glance cues. Povinelli and colleagues (1997), however, did not find children this young to master far gaze cues. Neither did Povinelli and colleagues (1999) in a later study find 3-year-olds to make use of a glance.

Discussion In the above, a review was made of all studies on primates’ use of referential gaze and glance cues in the object-choice task. It was the aim of this review to group and analyze results along the lines of the subsets of taxa within the primate phylogenetic taxa that have often been used as natural starting points of comparisons and analysis. When reviewing the data, it becomes clear that a large discrepancy exist between the multitude of object-choice results that exist across primate taxa and the rather categorical and sweeping conclusions that are sometimes made. In this respect, several points stand out, a few of which will be discussed here. The Predicative Powers of Phylogenetic Group? When reviewing the data, it is by no means evident that phylogenetic group is a good predictor of a particular primate species’ performance on the object-choice task although a superficial reading of Tables 1, 2, 3 and 4 might give that impression.


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Comparisons of Unequally Studied Phylogenetic Groups Let’s compare the overall performances of apes (see Table 4) with that of, say, Old World monkeys (Table 3). A quick reading of results could possibly lead to the conclusion that apes make better use of referential gaze cues than Old World monkeys, given that not many positive results on the task stand out for Old World monkeys whereas many do with apes. However, if we look a little more closely at the results, it is equally clear that a much larger number of studies with a larger number of subjects have been conducted with apes than with Old World monkeys. Thus, a summarization reveals that around 74 Old World monkeys have been the subjects of a total of 6 studies whereas around 111 apes (excluding humans) have been the subjects of 15 studies. These are approximate numbers as some subjects have been the participants of several studies, but, nevertheless, it serves to inform us that apes’ performance on the task have been more intensively studied than the performance of Old World monkeys. Comparisons of Phylogenetic Groups on the Basis of Inconsistent Data The above may not be a problem if results turned out to be consistent across studies of different species within the same phylogenetic group. After all, if 10 studies on apes (regardless of individual ape species) showed a consistent picture of good performance on the task then it may not really matter if ape studies outnumber studies on Old World monkeys, or if the number of ape subjects is larger than monkey subjects. However, it is clear that results are nowhere near consistent within phylogenetic group. This is neither the case when comparing relatively broad within group nor relatively narrow. For instance, strictly speaking, lesser apes show better use of cues than great apes, given that the one study on gibbons (N=1 subject) showed successful use of both pointing and gazing cues whereas many of the 15 studies on great apes (N=111 subjects) led to the conclusions that great apes showed rather poor performance with these cues. Similarly, had we stopped doing object-choice studies by the end of 2004, we may have concluded that orangutans performed better on the task than chimpanzees based on the results that Itakura and Tanaka’s (1998) one orangutan subject as well as some of my own three (Byrnit 2004) did quite well on the task whereas a number of studies conducted by, to mention a few, Povinelli and colleagues (1997 1997, 1999), and Call and colleagues (1998 1998, 2000) did not show equally good performances in chimpanzees. Needless to say, none of these hypothetical comparisons between species are valid. The results from one study on a single gibbon described as enculturated does not provide us with a strong foundation by which to perform a comparison with the results of 15 studies on several different species of great apes including individuals coming from a broad variety of histories with humans. Likewise, as we didn’t stop doing object-choice studies in 2004, we soon learned the frustrating fact that chimpanzees’, to mention but just one species, performances on the task are in any way clear or consistent across studies. Nevertheless, comparisons like these are often directly or indirectly made in the literature on the object-choice task, and conclusions are based on data as inconsistent and multifaceted as the ones mentioned.

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The Extrapolation of Knowledge About Phylogenetic Group from Data on a Few Genera Even if results were consistent across species within phylogenetic group, we must ask ourselves if we are really comparing something meaningful when we draw conclusions on the whole phylogenetic group from studies on a few species? The review revealed that a highly varied portion of species within phylogenetic group has been tested, and these species may come from only a few genera. Currently, we have results from two prosimian species, three New World monkey species, four Old World monkey species, and five ape species (excluding humans and including one lesser ape and four great ape species). Knowing less than I would like about the particularities of, for instance, the carnivores, I doubt that it would be meaningful to make broad conclusions on the cognition of tigers on the basis of studies on lions. Surely, we would not assume that cognitive faculties are entirely based on the evolutionary history of the common ancestor of tigers and lions, but to some (probably quite large) extent also is based on a complex intermixture of the various social and ecological pressures the individual species has been faced with in more recent evolutionary time, and which, directly and/ or indirectly, have shaped morphological and temperamental features of the species in question. The Socio-Ecological Diversity of Primates and Their Use of Referential Cues Primates are a highly diverse order of animal with huge variance between species, and even between populations within a species, in social systems and ecological challenges (reviews in Smuts et al. 1987; Dunbar 1988; Tomasello and Call 1997; Kappeler and van Schaik 2002). Within the primate order, some species live alone, in pairs, in family groups, or in fission-fussion societies. They live on savannahs, in rainforests, in deserts, and on open country grass-lands. They are diurnal or nocturnal. Their locomotion takes place terrestrially or arboreally. They feed on leaves, roots, insects, seasonal fruit, smaller mammals, and so forth. In other words, primate species may be as different in socio-ecological challenges and life-styles from one another as the individual species would be from a carnivore or a hoofed animal. Hence, to reiterate the question asked by Miklósi and Soproni (2006) whether one single, factorial hypothesis can explain species differences in the use of cues (in their case, a pointing cue), we must ask ourselves if we really would expect one, ultimate hypothesis to fit all primates? Does it, for instance, seem reasonable to assume that a competitive type objectchoice task will be equally meaningful to a chimpanzee and to a cooperative breeder such as a common marmoset? Or do we expect a meaningful cue to be of the same type to ground-living gorillas or baboons as to an arboreal orangutan or gibbon? Expecting the answers to be Bno^ to these questions, it seems unwarranted to draw broad conclusions on, for instance, New World monkeys based on a few studies on two or three New World monkey species, and similarly with the other phylogenetic groups. Of relevance to this, previous phylogenetic comparative analyses have shown no primate genus to perform especially well within particular cognitive paradigms, although genera may differ in overall performance (Deaner et al. 2006. See also MacLean et al. 2011 for discussion on phylogenetic comparisons, and Schmitt et al. 2012 on primate performance on the Primate Cognition Test Battery).


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Likewise, it does not seem based in solid knowledge about differences between primate species when we extrapolate conclusions on, for instance, great apes’ use of referential cues from what we know about, chimpanzees’ performance on the task. Chimpanzees, bonobos, gorillas, and orangutans face very different social and ecological challenges, and evolutionary pressures have shaped quite different temperaments and social behaviors in these species. Chimpanzees, for instance, have been found to prefer a much riskier food option than bonobos (Heilbronner et al. 2008). Chimpanzees and bonobos, also, show differences in tolerance towards conspecifics in food-retrieval tasks (Hare et al. 2007. See also Melis et al. 2006), and display different types of behaviour in food-sharing situations (Byrnit et al. 2015). Although very closely related phylogenetically, chimpanzees and bonobos inhabit different ecologies with different types of food pressures. This places different demands on temperamental factors, food searching strategies, etc., that could reasonably be assumed to influence the performances on a variety of socio-cognitive tasks such as the object-choice task in ways we have not yet delineated. Following the lines of this argument, it is of interest that fox kits, experimentally bred against fear and aggression towards humans, have proven as successful as dog puppies in using human cues in the object-choice task (Hare et al. 2005). The authors conclude that the successful performance of the foxes, which had no previous test experience with the use of human referential cues, is a by-product of selection on temperamental systems rather than a direct selection for improved socio-cognitive abilities. We should expect to see the same kind of temperamental influences on the objectchoice task when primates are the subjects, and temperamental influences could conceivably be along the lines of species differences in e.g. patience, impulsivity, risk preferences, attentiveness, inhibitory control, and general activity levels. We may, for instance, expect differences between species in how attainable it is to even test subjects from this species on the object-choice task. My own experience with non-laboratory, animal park/zoo subjects is that some primate species are either too excitable or impatient (chimpanzees; summary in Byrnit 2005), shy and reclusive (orangutans; Byrnit 2004), or gaze avoidant (gorillas; Byrnit 2009. See also below) that the only subjects from these species that will want to be in contact with the experimenter, sit still for the required amount of time, and pay attention to relevant features of the human experimenter are subjects with histories of previous intensive familiarization with humans. This makes sample errors a major problem when drawing comparisons between species. Some species may not even be tested to begin with as it is not possible outside of a laboratory-situation, or the only subjects whose performance we are able to analyze are individuals brought up under circumstances that are highly unusual and not representative of much in ways of ecological validity for the species in question. Gaze Behaviours in Primates and the Role of Rearing Conditions The inconsistency of results between studies reminds us of the importance of primate infancy and the plasticity of the primate brain. Primate brains, with some variance, are highly undeveloped at birth and a large part of the brain development happens over the years after birth, i.e. in the species typical social environment (for data and discussions

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on primate brain development see e.g. Dunbar 1992; Verhulst 2003). This necessitates exceptionally long periods of immaturity in which they (or, rather, we) learn about their physical and social environment in order to survive and procreate, providing primate species with the plasticity to become highly diverse in their behavioural repertoire even within separate populations of the same species. This has the important consequence for paradigms such as the object-choice task that individual subjects from the same species may differ markedly in relation to differences in their rearing histories, and, especially, their prior histories with humans. One of the few relatively consistent findings from the object-choice studies is that primates being either reared or trained by humans seem to be superior in making use of cues in the task compared to their conspecifics (e.g. Itakura and Tanaka 1998; Itakura et al. 1999; Call et al. 2000; Byrnit 2009). However, this is not a uniform finding (see e.g. Call et al. 1998), and rearing histories are often used as post-hoc explanations that do not specify what kind of human exposure is relevant, sufficient, or necessary in order to make successful use of different kinds of referential cues. Interestingly, the only longitudinal object-choice study conducted to date on a primate species showed that even if not successful on the task initially, infant chimpanzees may begin to use human-given cues with age (Okamoto-Barth et al. 2008). The rearing history of subjects is important to take into account when comparing data across phylogenetic group. A substantial number of great ape subjects that succeed on the task have been reared and/or trained by humans whereas very few primates from other phylogenetic groups have had this kind of exposure to humans. With few exceptions, the latter have either been reared by conspecifics or, if hand-reared, have lived almost all of their lives in groups of conspecifics. Furthermore, prior experience with socio-cognitive laboratory experiments has usually been much less intensive, or entirely non-existent, when subjects are from primate species other than the great apes. Thus, we are not just comparing species from one phylogenetic group with another, but individuals with drastically different types or amount of exposure to, and experience with, humans and our various kinds of referential cues, making it difficult to conclude much about possible phylogenetic differences between groups. Interestingly, the only study on a primate that is not a great ape and that has been designated as enculturated showed one gibbon to make spontaneous and successful use of gaze cues on the task (Inoue et al. 2004). The rearing history of subjects may assert many different kinds of influences on performance on the object-choice task. Maybe the most essential one for the present discussion on the use of gaze cues is what are the species-typical gaze behaviors of the primate species in question and how may this change with being reared or bred by humans? Most, if not all, primate species exhibit very different gaze behaviors than humans. Non-human primates do not stare into each others’ eyes for longer period of times, but rather Bsneak a peak^ (see Emery 2000; Kaplan and Rogers 2002). To many primates, direct staring will be related to threats and displays of aggression. Some domesticated animals, such as dogs and cats, have been bred with the particular purpose of being companionable to humans and as such a whole range of their social behaviors have changed in alignment with this, amongst these their gaze behavior (Miklósi et al. 2005). Non-human primates, regardless of rearing conditions, have not undergone this domestication process and as such will display gaze behaviors very different from humans (Tomasello et al. 2007). These differences in gaze behaviors may be of great importance in whether and how certain animal species, and not


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others, are able to employ gaze cues in the object-choice task. Gaze avoidant species may, for instance, fail experimental criteria of first establishing eye contact with the human experimenter before proceeding to using the gaze cue, and/or not be able to use the cue because indirect looking at the experimenter does not allow correct reading of the direction of the cue (see e.g. Byrnit 2004 on orangutan use of gaze cues). Do Primates Perform Less Successfully than Other Animals? With the advent of object-choice studies on animals other than primates, a joyless tide of conclusions have descended upon us, making it appear as if non-primates (as a big uniform group) make better use of referential cues in the task than primates (as an equally uniform group). Fortunately, as the present review reveals, the primate data are not as lackluster as comparative analysis sometimes make it out to be. As discussed previously, the primate species are not at all a uniform group, and not so when it comes to performances on the object-choice task either. Thus, depending on the viewpoint and the studies chosen to be representative of the primate field, it may be concluded that primates perform remarkably well, as witnessed by, for instance, the flawless orangutan performance in Itakura and Tanaka’s (1998) study, or the almost perfect gibbon use of cues in Inoue et al.’s (2004). Had we chosen another viewpoint, however, primates appear remarkably bad as witnessed by the poor performances of gorillas in my own study (Byrnit 2009), or the even more dismal performances of capuchin monkeys in Anderson and colleagues’ (1995): 1050 trials without mastering a gaze cue! By operating with these broad phylogenetic groups of primate taxa in comparative analyses, we seriously run the risk of obscuring the fact that many non-primates do not perform more successfully than primates. Domesticated dogs being the noticeable exception (see discussion in Udell et al. 2010), we are not at the point where data warrant us making the sweeping conclusion that non-primates perform better than primates. If the subjects tested belong to a species which have been bred by humans (see references in the introduction), they tend consistently to do better than nonhuman primates. With other non-primate species, however, it is rather the case that although some particular non-primate individuals do better than some particular primate-individuals, other primate individuals with different rearing histories, tested with other cues, objects, or methodologies may do better than the non-primate individuals. What makes the conclusions even harder still is the fact that very different criteria of success have been, and are presently, used both between primate studies and especially between primate and non-primate studies. Hence, whereas many non-primate studies operate with statistically significant use of cues in a designated number of trials, a large number of the primate studies have required subjects to reach criteria of e.g. 80 % correct trials in two consecutive sessions. If subjects have failed to reach this criteria testing has either been terminated or subjects’ use of the cue have been classified as unsuccessful performance, regardless of the fact that the same subjects may spontaneously have reached significant results in the first trials but never made it to two consecutively successful sessions at 80 % correct. These successful, initial results are often disregarded, although had the same stringent criteria been used with other species or in other primate studies, the conclusions might possibly be quite different. This is the current state of knowledge base on the existing data from both primate and non-primate object-choice studies. The future may enlighten us to reach other

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conclusions, but as of now, results are muddled and complex, and show that particular primate species sometimes perform more successfully than particular non-primate species, and vice versa, depending on an alarming number of factors such as species compared, criteria of success used, meta-procedures, cues, rearing histories of both primate and non-primate subjects, breeding history, and previous experience with cues or socio-cognitive testing. Does One Size Fit All: Ecological Validity of the Object-Choice Task? As the review reveals, there has been no lack of creativity on the part of object-choice researchers in trying to come up with variations on the task to improve performance. Thus, primates have been tested with two, three, or nine objects; human experimenters, conspecifics, or photos of conspecifics. Subjects have been encouraged to use taps, points, gaze, glance, sounds, or markers as referential cues. The cues have been delivered stationary or dynamically; from a distance or in proximity, and so forth. Some authors have done praiseworthy efforts to try to make the task more ecologically valid by, for instance, mimicking cues or situations that subjects might encounter in a natural context. Thus, gaze or glance cues, for instance, have been supplemented with vocalizations resembling natural food grunts, or gaze cues have alternated between the subject and the baited object. Objects with which subjects have possessed previous experience, such as tubes instead of opaque containers, have been used. The paradigm, also, have been turned from a cooperative situation into a competitive one where subjects are to compete over food with the experimenter. As object-choice studies vary between them on many different parameters, only few studies have been carried out with each of the modifications to the task. Competitive type object-choice studies have been successful with chimpanzees (Herrmann and Tomasello 2006), and baboons (Vick and Anderson 2003). Studies where containers have been replaced by tubes have shown successful performance in bonobos (Lyn et al. 2010) and chimpanzees (Call et al. 1998). Alternation of gaze between subject and object have been a successful cue for chimpanzees and bonobos (Lyn et al. 2010), but not for golden snub-nosed monkeys (Tan et al. 2013). Mulcahy and Hedge (2012) reviewed the data on the task and reached the conclusion that if the methodology is changed into a more peripheral design, it will greatly improve the performance of primates. Some of the paradigmatic changes described above show primates to be able to make use of experimenter-given cues. This, however, does not mean that they necessarily show better results than the standard version of the task. Competitive type objectchoice studies, for instance, have shown significant use of cues in some species, but as the rest of the studies by default are cooperative type tasks, and some of these also show successful use of cues, it would not be correct to conclude that competitive processes allow for better performance in primates in general, or even in one particular species specifically. Likewise, distal pointing worked as a successful cue for one orangutan in a study by Mulcahy and Suddendorf (2011), but given that the default, standard version is a more proximal, centrally presented cue, and some studies (Itakura and Tanaka 1998; Byrnit 2004) have shown good use of this cue by orangutans, it is not necessarily the case that primates, or just orangutans, perform better with distal, peripheral cues than with proximal, centrally presented ones. It may be so, but as of yet a conclusion such as this is not substantiated by the existing data.


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Maybe it’s time that we start rethinking the scope of our hypotheses and stop looking for overriding principles, cues or meta-procedures that will work in general for all primates, great apes, Old World monkeys, or any other such broad group of phylogenetically related, but quite diverse species. It seems fair to say that the standard version of the object-choice task, with all its interesting qualities, presents a scenario that no primate would ever remotely come across in its natural environment. Intriguingly, the present review shows that, contrary to what one might think, human beings do not always perform successfully with all the cues in the object-choice task, at least not until they are older than 3 years of age. The literature has documented how humans, the referential cue readers par excellence, as young as 14 months of age make use of referential cues outside the object-choice task (see the introduction), and from this we may conclude that successful or unsuccessful performance on the object-choice task is not entirely explained in terms of whether or not a species is capable of attributing intent to other individuals. The object-choice task seems to require capacities other than attributional skills, these being related to a broad range of factors such as, to mention a few likely candidates, temperament, motivation, gaze aversion, experience with cultural artifacts such as objects and experimental settings, etc. Nothing in the evolutionary past of non-human primates could possibly prime them for the multifaceted and humanspecific requirements, and even the occasional cue contradictions, of the object-choice task. Instead, in order to perform successfully on the task, primates must rely on whatever is at hand from within their species-specific capacities, evolved to solve species-specific challenges within the spheres of social life, foraging strategies, ecological challenges, and so forth. To this end, different species will rely on both their general socio-cognitive skills and other factors such as the species’ primary sense modality (see e.g. Plotnik et al. 2014 on elephants’, Elephas maximus, use of cues), locomotive abilities, sensitivity to human actions (see e.g. Udell et al. 2010 on dogs), ability to inhibit its impulses (e.g. Vlamings et al. 2009), among many other factors. We should address the question of why we keep on testing non-human animals on tasks that seem to make absolutely no sense to them? What kind of knowledge do we hope to gain about other animals’ capacities, socio-cognitive or other, by imposing on them paradigms that may be as arbitrary to them as having humans competing with sharks on registering blood in water? One obvious answer to this question is that the object-choice task is easy to design and use as a test. Furthermore, it produces data that are seemingly easy to analyze. However, as it should be clear by now, it is highly debatable what these data, actually, tells us about non-human animal capacities? It is like distributing standardized questionnaires to humans: a seemingly simple research design with answers that are easily comparable, until we start to think about the multitude of reasons people may have to answer Byes^ or Bno^ to the same question. Furthermore, the researcher does not gain any knowledge about these reasons from the answers on the questionnaire. Instead of continuing our possibly fruitless search for one overall explanation to fit all primates or groups of primates within ancestry on a testing paradigm that allow for only a few, human-defined responses which may or may not be of any importance or relevance to the animal species in question, it is suggested that we, instead, take into account ecological and social factors to guide our search for which type of cues a specific species may use to gain information about their natural habitat and within the framework of what are the challenges of their daily lives. These studies should take into

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account that our abstract intellectual and theoretical debates on the use of referential cues may entirely overlook how socio-ecological challenges may create similarities and differences within ancestral lines that operates across phylogenetic relatedness. This also means that no singular test procedure will work for all primate species or even for all individuals within one species. We should not expect one size to fit all. Acknowledgments I would like to thank the anonymous reviewers for helpful comments on this paper. Furthermore, as usual, many thanks to Henriette Westh, Timothy Wooller, and Jennifer Nevile for dedicated proofreading, and inspiring and insightful suggestions on my work.

References Amici, F., Aureli, F., Visalberghi, E., & Call, J. (2009). Spider monkeys (Ateles geoffroyi) and capuchin monkeys (Cebus apella) follow gaze around barriers: evidence for perspective taking? Journal of Comparative Psychology, 123, 368–374. Anderson, J. R., Sallaberry, P., & Barbier, H. (1995). Use of experimenter-given cues during object-choice tasks by capuchin monkeys. Animal Behaviour, 49, 201–208. Anderson, J. R., Montant, M., & Schmitt, D. (1996). Rhesus monkeys fail to use gaze direction as an experimenter-given cue in an object-choice task. Behavioural Processes, 37, 47–55. Barth, J., Reaux, J. E., & Povinelli, D. J. (2005). Chimpanzees’ (Pan troglodytes) use of Gaze cues in objectchoice tasks: different methods yield different results. Animal Cognition, 8, 84–92. Behne, T., Carpenter, M., & Tomasello, M. (2005). One-year-olds comprehend the communicative intentions behind gestures in a hiding game. Developmental Science, 8, 492–499. Bering, J. M. (2004). A critical review of the Benculturation hypothesis^: the effects of human rearing on great ape social cognition. Animal Cognition, 7, 201–212. Bräuer, J., Call, J., & Tomasello, M. (2005). All great ape species follow gaze to distant locations and around barriers. Journal of Comparative Psychology, 119, 145–154. Bräuer, J., Kaminski, J., Riedel, J., Call, J., & Tomasello, M. (2006). Making inferences about the location of hidden food: social dog, causal ape. Journal of Comparative Psychology, 120, 38–47. Bretherton, I., & Beeghly, M. (1982). Talking about internal states. Developmental Psychology, 18, 906–921. Burkart, J., & Heschl, A. (2006). Geometrical gaze following in common marmosets (Callithrix jacchus). Journal of Comparative Psychology, 120, 120–130. Butterworth, G., & Cochran, E. (1980). Towards a mechanism of joint visual attention in human infancy. International Journal of Behavioral Development, 3, 253–272. Byrnit, J. T. (2004). Nonenculturated orangutans’ (Pongo pygmaeus) use of experimenter-given manual and facial cues in an object-choice task. Journal of Comparative Psychology, 118, 309–315. Byrnit, J.T. (2005). Primate theory of mind: a comparative psychological analysis. Published Ph.D. monograph. Department of Psychology, Aarhus University, 2005, 3. Byrnit, J. T. (2009). Gorillas’ (Gorilla gorilla) use of experimenter-given manual and facial cues in an objectchoice task. Animal Cognition, 12, 401–404. Byrnit, J.T., Høgh-Olesen, H., Makransky, G. (2015). Chimpanzee (Pan troglodytes) and bonobo (Pan paniscus) willingness to share highly attractive, monopolizable food sources. J of Comp Psych. doi:10. 1037/a0039351 Call, J., & Tomasello, M. (1996). The effect of humans on the cognitive development of apes. In A. E. Russon, K. A. Bard, & S. T. Parker (Eds.), Reaching into thought: The minds of the great apes. Cambridge: Cambridge University Press. Call, J., Hare, B. A., & Tomasello, M. (1998). Chimpanzee gaze following in an object-choice task. Animal Cognition, 1, 89–99. Call, J., Agnetta, B., & Tomasello, M. (2000). Cues that chimpanzees do and do not use to find hidden objects. Animal Cognition, 3, 23–34. Corkum, V., & Moore, C. (1995). Development of joint visual attention in infants. In C. Moore & P. Dunham (Eds.), Joint attention: Its origin and role in development. New Jersey: Erlbaum. Deaner, R. O., van Schaik, C. P., & Johnson, V. (2006). Do some taxa have better domain-general cognition than others? A meta-analysis of nonhuman primate studies. Evolutionary Psychology, 4, 149–196.


509

Dorey, N. R., Udell, M. A. R., & Wynne, C. D. L. (2010). When do domestic dogs, Canis familiaris, start to understand human pointing? The role of ontogeny in the development of interspecies communication. Animal Behaviour, 79, 37–41. Dunbar, R. I. M. (1988). Primate social systems. Ithaca: Cornell University Press. Dunbar, R. I. M. (1992). Neocortex size as a constraint on group size in primates. Journal of Human Evolution, 20, 469–493. Emery, N. J. (2000). The eyes have it: the neuroethology, function and evolution of social gaze. Neuroscience & Biobehavioral Reviews, 24, 581–604. Giret, N., Miklósi, Á., Kreutzer, M., & Bovet, D. (2008). Use of experimenter-given cues by African gray parrots (Psittacus erithacus). Animal Cognition. doi:10.1007/s 10071-008-0163-2. Hall, N. J., Udell, M. A. R., Dorey, N. R., Walsh, A. L., & Wynne, C. D. L. (2011). Megachiropteran bats (Pteropus) utilize human referential stimuli to locate hidden food. Journal of Comparative Psychology, 125, 341–346. Hare, B., & Tomasello, M. (1999). Domestic dogs (Canis familiaris) use human and conspecific social cues to locate hidden food. Journal of Comparative Psychology, 113, 173–177. Hare, B., & Tomasello, M. (2004). Chimpanzees are more skilful in competitive than in cooperative cognitive tasks. Animal Behaviour, 68, 571–581. Hare, B., Call, J., & Tomasello, M. (2001). Do chimpanzees know what conspecifics know? Animal Behaviour, 61, 139–151. Hare, B., Brown, M., Williamson, C., & Tomasello, M. (2002). The domestication of social cognition in dogs. Science, 298, 1634–1636. Hare, B., Plyusnina, I., Ignacio, N., Schepina, O., Stepika, A., Wrangham, R., & Trut, L. (2005). Social cognitive evolution in captive foxes is a correlated by-product of experimental domestication. Current Biology, 15, 226–230. Hare, B., Melis, A. P., Woods, V., Hastings, S., & Wrangham, R. (2007). Tolerance allows bonobos to outperform chimpanzees on a cooperative task. Current Biology, 17, 619–623. Hare, B., Rosati, A., Kaminski, J., Bräuer, J., Call, J., & Tomasello, M. (2010). The domestication hypothesis for dogs’ skills with human communication: a response to Udell et al. (2008) and Wynne et al. (2008). Animal Behaviour, 79, e1–e6. Hauser, M. D., Glynn, D., & Wood, J. (2007). Rhesus monkeys correctly read the goal-relevant gestures of a human agent. Proceedings of the Royal Society of London B: Biological Sciences, 274, 1913–1918. Heilbronner, S. R., Rosati, A. G., Stevens, J. R., Hare, B., & Hauser, M. D. (2008). A fruit in the hand or two in the bush? Divergent risk preferences in chimpanzees and bonobos. Biology Letters, 4, 246–249. Herrmann, E., & Tomasello, M. (2006). Apes’ and children’s understanding of cooperative and competitive motives in a communicative situation. Developmental Science, 9, 518–529. Herrmann, E., Call, J., Hernández-Lloreda, M. V., Hare, B., & Tomasello, M. (2007). Humans have evolved specialized skills of social cognition: the cultural intelligence hypothesis. Science, 317, 1360–1366. Hostetter, A. B., Russell, J. L., Freeman, H., & Hopkins, W. D. (2007). Now you see me, now you don’t: evidence that chimpanzees understand the role of the eyes in attention. Animal Cognition, 10, 55–62. Inoue, Y., Inoue, E., & Itakura, S. (2004). Use of experimenter-given directional cues by a young whitehanded gibbon (Hylobates lar). Japanese Psychological Research, 46, 262–267. Itakura, S., & Anderson, J. R. (1996). Learning to use experimenter-given cues during an object-choice task by a capuchin monkey. Cahiers de Psychologie Cognitive, 15, 103–112. Itakura, S., & Tanaka, M. (1998). Use of experimenter-given cues during object-choice tasks by chimpanzees (Pan troglodytes), an orangutan (Pongo pygmaeus), and human infants (Homo sapiens). Journal of Comparative Psychology, 112, 119–126. Itakura, S., Agnetta, B., Hare, B., & Tomasello, M. (1999). Chimpanzee use of human and conspecific social cues to locate hidden food. Developmental Science, 2, 448–456. Kaminski, J., Riedel, J., Call, J., & Tomasello, M. (2005). Domestic goats, Capra hircus, follow gaze direction and use social cues in an object choice task. Animal Behaviour, 69, 11–18. Kaplan, G., & Rogers, L. J. (2002). Patterns of gazing in orangutans (Pongo pygmaeus). International Journal of Primatology, 23, 501–526. Kappeler, P. M., & van Schaik, C. P. (2002). Evolution of primate social systems. International Journal of Primatology, 23, 707–740. Kirchhofer, K. C., Zimmermann, F., Kaminski, J., & Tomasello, M. (2012). Dogs (Canis familiaris), but not chimpanzees (Pan troglodytes), understand imperative pointing. PLoS ONE, 7, 2. Liebal, K., & Kaminski, J. (2012). Gibbons (Hylobates pileatus, H. moloch, H. lar, Symphalangus syndactylus) follow human gaze, but do not take the visual perspective of others. Animal Cognition. doi:10.1007/s10071-012-0543-5.

510


Lyn, H., Russell, J. L., & Hopkins, W. D. (2010). The impact of environment on the comprehension of declarative communication in apes. Psychological Science, 21, 360–365. MacLean, E. L., Matthews, L. J., Hare, B. A., et al. (2011). How does cognition evolve? Phylogenetic comparative psychology. Animal Cognition, 15, 223–238. Maros, K., Gácsi, M., & Miklósi, A. (2008). Comprehension of human pointing gestures in horses (Equus caballus). Animal Cognition, 11, 457–466. Melis, A. P., Hare, B., & Tomasello, M. (2006). Engineering cooperation in chimpanzees: tolerance constraints on cooperation. Animal Behaviour, 72, 275–286. Miklósi, Á., & Soproni, K. (2006). A comparative analysis of animals’ understanding of the human pointing gesture. Animal Cognition, 9, 81–93. Miklósi, A., Pongrácz, P., Lakatos, G., Topál, J., & Csányi, V. (2005). A comparative study of the use of visual communicative signals in interactions between dogs (Canis familiaris) and humans and cats (Felis catus) and humans. Journal of Comparative Psychology, 119, 179–186. Morissette, P., Ricard, M., & Décarie, T. G. (1995). Joint visual attention and pointing in infancy: a longitudinal study of comprehension. British Journal of Developmental Psychology, 13, 163–175. Mulcahy, N., & Call, J. (2009). The performance of bonobos (Pan paniscus), chimpanzees (Pan troglodytes), and orangutans (Pongo pygmaeus) in two versions of an object-choice task. Journal of Comparative Psychology, 123, 304–309. Mulcahy, N. J., & Hedge, N. J. (2012). Are great apes tested with an abject object-choice task? Animal Behaviour, 83, 313–321. Mulcahy, N., & Suddendorf, T. (2011). An obedient orangutan (Pongo abelii) performs perfectly in peripheral object-choice tasks but fails the standard centrally presented versions. Journal of Comparative Psychology, 125, 112–115. Neiworth, J. J., Burman, M. A., Basile, B. M., & Lickteig, M. T. (2002). Use of experimenter-given cues in visual co-orienting and in an object-choice task by a New World monkey species, cotton top tamarins (Saguinus oedipus). Journal of Comparative Psychology, 116, 3–11. Okamoto-Barth, S., Tomonaga, M., Tanaka, M., & Matsuzawa, T. (2008). Development of using experimenter-given cues in infant chimpanzees: longitudinal changes in behavior and cognitive development. Developmental Science, 11, 98–108. Pack, A. A., & Herman, L. M. (2004). Bottlenosed dolphins (Tursiops truncatus) comprehend the referent of both static and dynamic human gazing and pointing in an object-choice task. Journal of Comparative Psychology, 118, 160–171. Peignot, P., & Anderson, J. R. (1999). Use of experimenter-given manual and facial cues by gorillas (Gorilla gorilla) in an object-choice task. Journal of Comparative Psychology, 113, 253–260. Plotnik, J. M., Shaw, R. C., Brubaker, D. L., Tiller, L. N., & Clayton, N. S. (2014). Thinking with their trunks: elephants use smell but not sound to locate food and exclude nonrewarding alternatives. Animal Behaviour, 88, 91–98. Povinelli, D. J., & Eddy, T. J. (1996a). Chimpanzees: joint visual attention. Psychological Science, 7, 129– 135. Povinelli, D. J., & Eddy, T. J. (1996b). What young chimpanzees know about seeing. Monographs of the Society for Research in Child Development, 61, 3. Povinelli, D. J., Reaux, J. E., Bierschwale, D. T., Allain, A. D., & Simon, B. B. (1997). Exploitation of pointing as a referential gesture in young children, but not adolescent chimpanzees. Cognitive Development, 12, 423–461. Povinelli, D. J., Bierschwale, D. T., & Cech, C. G. (1999). Comprehension of seeing as a referential act in young children, but not juvenile chimpanzees. British Journal of Developmental Psychology, 17, 37–60. Rosati, A. G., & Hare, B. (2009). Looking past the model species: diversity in gaze- following skills across primates. Current Opinion in Neurobiology, 19, 45–51. Ruiz, A., Gómez, J. C., Roeder, J. J., & Byrne, R. W. (2009). Gaze following and gaze priming in lemurs. Animal Cognition, 12, 427–434. Scheumann, M., & Call, J. (2004). The use of experimenter-given cues by South African fur seals (Arctocephalus pusillus). Animal Cognition, 7, 224–230. Schloegl, C., Kotrschal, K., & Bugnyar, T. (2007). Gaze following in common ravens, Corvus corax: ontogeny and habituation. Animal Behaviour, 74, 769–778. Schmitt, V., Pankau, B., & Fischer, J. D2012]. Old World Monkeys compare to apes in the primate cognition test battery. PLoS ONE, 7, e32024. doi: 10.13/1/journal.pone.0032024. Smuts, B. B., Cheney, D. L., Seyfarth, R. M., Wrangham, R. W., & Struhsaker, T. T. (Eds.). (1987). Primate societies. Chicago: University of Chicago Press.


511

Tan, J., Ruoting, T., & Yanjie, S. (2013). Testing the cognition of the forgotten colobines: a first look at golden snub-nosed monkeys (Rhinopithecus roxellana). International Journal of Primatology. doi:10.1007/ s10764-013-9741-5. Tomasello, M., & Call, J. (1997). Primate cognition. New York: Oxford University Press. Tomasello, M., & Call, J. (2004). The role of humans in the cognitive development of apes revisited. Animal Cognition, 7, 213–215. Tomasello, M., Call, J., & Hare, B. (1998). Five primate species follow the visual gaze of conspecifics. Animal Behaviour, 55, 1063–1069. Tomasello, M., Hare, B., Lehmann, H., & Call, J. (2007). Reliance on head versus eyes in the gaze following of great apes and human infants: the cooperative eye hypothesis. Journal of Human Evolution, 52, 314–320. Udell, M. A. R., Dorey, N. R., & Wynne, C. D. (2008). Wolves outperform dogs in following human social cues. Animal Behaviour, 76, 1767–1773. Udell, M. A. R., Dorey, N. R., & Wynne, C. D. L. (2010). What did domestication do to dogs? A new account of dogs’ sensitivity to human actions. Biological Reviews, 85, 327–345. Verhulst, J. (2003). Developmental dynamics in human and other primates. New York: Adonis Press. Vick, S.-J., & Anderson, J. R. (2000). Learning and limits of use of eye gaze by capuchin monkeys (Cebus apella) in an object-choice task. Journal of Comparative Psychology, 114, 200–207. Vick, S.-J., & Anderson, J. R. (2003). Use of human visual attention cues by olive baboons (Papio anubis) in a competitive task. Journal of Comparative Psychology, 117, 209–216. Vick, S.-J., Bovet, D., & Anderson, J. R. (2001). Gaze discrimination learning in olive baboons (Papio anubis). Animal Cognition, 4, 1–10. Vlamings, P. H. J. M., Hare, B., & Call, J. (2009). Reaching around barriers: the performance of the great apes and 3-5-year-old children. Animal Cognition. doi:10.1007/s10071-009-0265-5. Wilkinson, A., Mandl, I., Bugnyar, T., & Huber, L. (2010). Gaze-following in the red-footed tortoise (Geochelone carbonaria). Animal Cognition, 13, 765–769. Wynne, C. D. L., Udell, M. A. R., & Lord, K. A. (2008). Ontogeny’s impacts on human-dog communication. Animal Behaviour. doi:10.1016/j.anbehav.2008.03.010. Jill T. Byrnit received her PhD on primate socio-cognition from Aarhus University, Denmark. Since 1999, she’s been working within the field of evolutionary and comparative psychology and has been conducting research studies on the socio-cognitive capacities and social lives of non-human primates, primarily the great apes. She’s a former postdoctoral fellow from Department of Psychiatry and Biobehavioral Sciences, Semel Institute, University of California, Los Angeles (UCLA) and Wake Forest University, North Carolina where she was part of a larger project on personality, temperament, and impulse control in vervet monkeys. Earlier, she did her Master’s thesis at the Brain, Mind, and Behavior Unit, University of California, Davis (UC Davis) on personality dimensions and social stressors in rhesus macaques. She’s the author and co-author of international publications on great apes’ sharing behavior and use of referential cues, and has authored and co-authored several books on the comparative psychology of humans and other primates. Recently, she coauthored a comprehensive textbook (edited by H. Høgh-Olesen and T. Dalsgaard) on personality which is used at several Danish universities and has been sold to Norway. She is presently working as an assistant professor at University of Southern Denmark.

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