Psychology assignment 4

The Impact of Environment on the Comprehension of Declarative Communication in Apes

Heidi Lyn1, Jamie L. Russell2, and William D. Hopkins1,2

1Department of Psychology, Agnes Scott College, and 2Department of Psychobiology, Yerkes National Primate Research Center, Atlanta, Georgia

Abstract

A series of recent reports have questioned the ability of great apes to comprehend declarative communication and have sug- gested that this ability is biologically based and may have driven the evolution of human language. We tested three groups of differently reared chimpanzees and bonobos for their ability to understand declarative signals in an object-choice task. The scores of the two groups of apes that were reared in a sociolinguistically complex environment were significantly higher than the scores of the standard-reared group. The results further showed that bonobos did not outperform chimpanzees. Our results demonstrate that environmental factors, particularly access to a sociolinguistically rich environment, directly influ- ence great apes� ability to comprehend declarative signals and suggest that, contrary to recent claims, apes have the biological capacity to utilize purely informative communication.

Keywords

language evolution, apes, social rearing, declarative pointing

Received 3/26/09; Revision accepted 8/19/09

Human children are highly motivated to share information with

other individuals (e.g., Tomasello, 2007). By 12 to 15 months

of age, children begin spontaneously pointing imperatively to

request objects, but also point declaratively—simply to draw

the attention of adults to specific objects (Bates, Camaioni, &

Volterra, 1975). Although recent studies in great apes (i.e.,

hominids: chimpanzees, bonobos, gorillas, and orangutans)

have demonstrated evidence of imperative pointing (Leavens,

Hopkins, & Bard, 2005), it has been suggested that comprehen-

sion and production of declarative gestures is absent in apes or

is highly constrained to socially competitive contexts (Hare,

2007; but see Menzel, 2004). These findings have led some

researchers to suggest that within the primate lineage, under-

standing declarative communication is unique to humans and

is possibly driven by the same biological change that led to

the development of human language (Tomasello, 2007).

The majority of studies on the comprehension of declara-

tive signaling in nonhuman animals have employed the

object-choice test, in which a human experimenter indicates

the location of a hidden food item using a social cue (e.g.,

gaze direction, pointing, or vocalizing). Several studies utiliz-

ing this task have shown evidence of declarative comprehen-

sion in animals other than great apes, including lemurs, dol-

phins, seals, goats, corvids, and canines (e.g., Pack &

Herman, 2007; Ruiz, Gómez, Roeder, & Byrne, 2009; see

Miklósi & Soproni, 2006, for a recent review). However,

results from studies of chimpanzees, gorillas, and orangutans

have been much less clear.

Despite multiple reports that chimpanzees can readily fol-

low the gaze of humans and conspecifics (e.g., Hostetter,

Russell, Freeman, & Hopkins, 2007; Tomasello, Hare, &

Agnetta, 1999), object-choice studies have provided contra-

dictory evidence as to whether chimpanzees, gorillas, and

orangutans can comprehend declarative signals (e.g., Barth,

Reaux, & Povinelli, 2005; Call, Agnetta, & Tomasello, 2000).

In the data published to date, the 32 chimpanzees tested on

the object-choice task had a mean percentage correct of 61%

(Lyn & Hopkins, 2009). Although this mean is significantly

above chance level, of the 32 chimpanzees, only 9 performed

significantly better than 50% correct. Thus, it appears that these

few individual chimpanzees account for the significant results.

Different explanations have been proposed to account for

species differences as well as individual differences in perfor-

mance on the object-choice task. One hypothesis is that bio-

logical or genetic factors play a critical role. For example,

Corresponding Author:

William D. Hopkins, Department of Psychology, Agnes Scott College, 141 E.

College Ave., Decatur, GA 30030

E-mail: [email protected]

Psychological Science 21(3) 360–365 � The Author(s) 2010 Reprints and permission: sagepub.com/journalsPermissions.nav DOI: 10.1177/0956797610362218 http://pss.sagepub.com

Research Report

Hare et al. (2005) studied two groups of foxes, one of which

was selectively bred for reduced fearful and aggressive

behaviors toward humans. The selectively bred foxes per-

formed significantly better on the object-choice task than

did the control foxes, a result suggesting that genetic factors

play an important role in canids (Hare, 2007). With respect to

chimpanzees (and potentially other great apes), some studies

have found that performance on the object-choice task is

influenced by whether the test paradigm is a competitive or

a cooperative task (see Moll & Tomasello, 2007, for

a review). For example, Hare and his colleagues (2007)

found that chimpanzees that do not follow cooperative ges-

tures can utilize a competitive gesture (grabbing for food)

to infer the location of a food item; these authors hypothe-

sized that the noncooperative nature of chimpanzee social

behavior and organization is a biological difference from

humans that makes it difficult for chimpanzees to perform

above chance levels on the object-choice task.

According to another hypothesis (the sociolinguistic-

construction hypothesis; adapted from Moll & Tomasello,

2007), after humans� evolutionary split from noncooperative

primate antecedents, humans developed linguistic and social

interactions that fostered the emergence of both imperative

and declarative communication. In this view, humans� ability

to comprehend and produce declarative communication

occurred as the result of an interaction of their biologically

based cooperative nature and their environment, an idea

that is similar to the concept of social scaffolding proposed

by Vygotsky (1978). However, Moll and Tomasello sug-

gested that chimpanzees not only did not develop this envi-

ronmental support for declarative communication, but also

are unable to utilize such support because of their noncoop-

erative nature.

This suggestion is suspect because environmental support

in the form of human contact (enculturation) was implicated

as an important factor in the abilities of primates in several

object-choice studies (Call & Tomasello, 1994; Itakura,

Agnetta, Hare, & Tomasello, 1999; Itakura & Tanaka,

1998). However, these studies were based on relatively few

animals (2 enculturated chimpanzees and 2 enculturated

orangutans), and their findings were contradictory, with

enculturated animals sometimes performing better than stan-

dard-reared animals and sometimes not (e.g., Call et al.,

2000; Call, Hare, & Tomasello, 1998). Indeed, later studies

did not discuss the possibility that human contact affected

results, even when testing the same individual animals (Tom-

asello, Call, & Gluckman, 1997).

The first aim of the study we report here was to examine

the effects of exposure to different human communicative

environments on the comprehension of declarative signals

in two closely related great ape species of the genus Pan:

chimpanzees (Pan troglodytes) and bonobos (Pan paniscus).

According to the biological hypothesis, apes simply lack the

capacity to comprehend declarative signals; if this hypothesis

is correct, all apes should perform poorly on tests of

declarative comprehension. However, according to the socio-

linguistic-construction hypothesis, apes raised in human

communicative environments should perform significantly

better than other apes.

The second aim of this study was to directly compare the

abilities of bonobos and chimpanzees to utilize declarative

social cues in a noncompetitive context. To date, among great

apes, 32 chimpanzees, 8 orangutans, and 7 gorillas have been

tested on the object-choice task; no data are available for

bonobos. Given the differing social structures of the two spe-

cies of Pan, one might predict performance differences on

the object-choice task. Specifically, it has been suggested

that bonobos are a more tolerant and cooperative species

than chimpanzees (de Waal, 1996; Hare, Melis, Woods,

Hastings, & Wrangham, 2007). If this is true, and if tolerance

and cooperation are important components of the evolution

of declarative comprehension (Hare, 2007), then bonobos

should perform better than chimpanzees on cooperative ver-

sions of the object-choice task. We tested this hypothesis by

comparing similarly raised bonobos and chimpanzees on this

task.

Method

Subjects

Three groups of apes were tested. One group consisted of 6

chimpanzees (2 males, 4 females) from the Yerkes National

Primate Research Center of Emory University (YNPRC);

their ages ranged from 11 to 38 years. A second group com-

prised 7 bonobos (4 males, 3 females) residing at the Great

Ape Trust of Iowa (GATI); their ages ranged from 8 to 39

years. The third group consisted of 4 chimpanzees (2 males,

2 females) living at the Language Research Center of

Georgia State University (LRC); they ranged in age from

22 to 38 years.

Both the GATI bonobos and the LRC chimpanzees spent

much of their early years at the LRC as part of a larger

project devoted to fostering two-way communication

between human and nonhuman primates (Lyn, Greenfield,

& Savage-Rumbaugh, in press; Savage-Rumbaugh, 1986;

Savage-Rumbaugh et al., 1993). In 2005, the bonobos moved

to the GATI facility; the 4 chimpanzees remained at the LRC

facility. All 11 of the LRC and GATI apes are socially

housed and are exposed to high levels of complex communi-

cative interactions with human caregivers. The YNPRC sub-

jects, with the exception of one wild-caught individual

(Leslie), were born at the center and were reared following

standard practices for captive apes. These animals are housed

in groups of 2 to 6 chimpanzees and have regular contact

with human caregivers. However, these interactions are typ-

ically limited to basic husbandry contexts, such as shifting

animals from cage to cage and feeding, and to cognitive test-

ing with no specific emphasis on understanding human

communication.

Declarative Comprehension in Apes 361

Procedure

The American Psychological Association�s guidelines for the

ethical treatment of animals were adhered to during all

phases of this study.

In an object-choice task, subjects are required to choose

between two containers in order to find a hidden food item.

In this study, we presented two paper tubes, closed at one

end, one of which was baited with a small piece of food

(an M&M or a small piece of fruit). These tubes were placed

equidistant from the center of a testing surface (a testing table

or piece of cardboard). In most object-choice tasks, subjects

are required to point to the desired container. However, in

our task, the paper tubes allowed the apes to grasp and bring

the tubes inside their enclosure (see Fig. 1). In this way, we

eliminated the need for subjects to produce a gesture and

ensured that individual differences in the production of a ges-

ture were not confounded with ability to comprehend

a declarative cue.

The apes were trained on the task so they would learn to

choose only one tube and to select the one with the food

reward. On the initial trials, the open ends of the tubes faced

the subjects (open trials). Next, the apes were tested with

the closed ends of the tubes facing them (closed trials) so

that they had to watch to see which tube was baited in order

to choose the correct one. Subjects moved from the training

phase to the testing phase only after they chose correctly on

at least 8 out of 10 consecutive trials in each training condition.

On all test trials, the placement of the food in the tube was

hidden from the ape by a blind. Each test session included

a pseudorandomized set of 24 trials, 8 trials in each of three

declarative conditions: point, vocalize, and point and vocal-

ize. All trials started with the experimenter saying the ape�s name to catch his or her attention. Immediately afterward,

the experimenter indicated the correct tube. In the point con-

dition, the experimenter used her whole arm with the index

finger extended to point toward the correct tube (at a distance

of 2–10 cm) while alternating her gaze between the subject

and the correct tube. In the vocalize condition, the experi-

menter leaned toward the correct tube while vocalizing and

alternating her gaze between the tube and the ape. For the

YNPRC chimpanzees, the vocalizations consisted of replicat-

ing a chimpanzee food grunt. For the chimpanzees at the

LRC, this food grunt was alternated with spoken English:

‘‘It�s in this one; the [name of food] is in here.’’ The bonobos

at the GATI heard a simulated bonobo vocalization, a food

peep, alternated with a similar English sentence. In the

point-and-vocalize condition, the experimenter pointed at

the correct tube while alternating her gaze and vocalizing.

The GATI bonobos and the LRC chimpanzees were pre-

sented with two test sessions in a row. Because of poor perfor-

mance, the YNPRC chimpanzees were given an extra session

of training trials between their test sessions; in these training

trials, they could see the tube being baited, and the correct

tube was also indicated by the experimenter. Additionally,

the 24 test trials in the YNPRC chimpanzees� second testing

session were randomly interspersed with 24 training trials.

Results

Descriptive statistics

Individual performance on the task is summarized in Figure

2. Not unlike laboratory-living chimpanzees described in pre-

vious reports, only 1 of the 6 YNPRC subjects performed

above chance levels, even though they were given extra train-

ing between the two test sessions. In contrast, 5 of the 7

GATI bonobos and all 4 LRC chimpanzees performed signif-

icantly above chance, with no explicit training. The YNPRC

chimpanzees were correct on an average of 55.4% of the tri-

als; however, the GATI bonobos were correct on 74.1% of

the trials, and the LRC chimpanzees on 83.9% of the trials.

Performance analyses

A repeated measures analysis of variance showed significant

main effects for group, F(2, 14) 5 8.73, p 5 .003, h2 5 .56,

and test condition, F(2, 28) 5 3.606, p 5 .04, h2 5 .21, but

no interaction between these two variables, F(4, 28) 5 0.47,

p . .05, h2 5 .06 (see Fig. 3). With respect to the group

effect, Tukey�s honestly significant difference tests showed

that in every condition, the percentage of trials with a correct

response was significantly lower for the YNPRC group

compared with the GATI and LRC groups. Post hoc tests

Fig. 1. Illustration of the setup for the object-choice task. On each trial, two tubes were presented, and one of the tubes contained a piece of food. The subject was allowed to take one of the tubes only. In all trial types, the exper- imenter alternated her gaze between the correct tube and the ape. On a pointing trial (illustrated here), the experimenter pointed to the correct tube. On a vocalizing trial, the experimenter leaned toward the correct tube and vocalized. On a point-and-vocalize trial, the experimenter both pointed to the correct tube and vocalized. In this photograph, Julie (a Yerkes National Primate Research Center chimpanzee) is grasping her choice as the experimenter points to the correct item.

362 Lyn et al.

also showed that performance in the point-and-vocalize con-

dition was significantly better than performance in either the

point or the vocalize condition (see Fig. 3). This result sup-

ports earlier findings that vocalizations and other sounds

enhance performance on a visual object-choice task and

vice versa (a visual cue enhances performance on an auditory

task; Call et al., 2000; Itakura et al., 1999). No other signif-

icant differences were found.

Discussion

The current findings indicate that apes raised in a complex

social-communicative environment outperform other apes

on the object-choice task. Therefore, although it seems that

the ability to use purely informative social cues may be the

result of biological changes in some species (such as canids),

contrary to recent claims (Moll & Tomasello, 2007; Toma-

sello, 2007), at least two great apes share the biological capa-

bility for this behavior with humans, which can be observed

when the apes are given the appropriate environment and

rearing experiences. This finding supports the alternative,

sociolinguistic-construction hypothesis in apes.

Additionally, the ability to comprehend declarative signals

is not more developed in the allegedly more tolerant and

cooperative bonobos than in chimpanzees when the two spe-

cies are reared in similar environments. Therefore, either

cooperation is not the determinant ability in declarative com-

prehension, contrary to recent hypothesizing, or cooperation

is equally developed in bonobos and chimpanzees. The latter

would perhaps not be surprising considering the multiple

reports of chimpanzee cooperation in both wild (e.g., Gilby,

2006) and captive populations (Hirata & Fuwa, 2007;

Savage-Rumbaugh, 1986; but see Silk et al., 2005).

Other studies have pointed to different mechanisms that

may enhance performance on this task. For example, Miklósi

and Soproni (2006) showed that proximal (close) pointing

was easier for apes to follow than distal (distant) pointing.

However, our procedure would be considered to involve

proximal pointing, and the YNPRC chimpanzees still per-

formed poorly. Also, although Povinelli, Reaux, Biersch-

wale, Allain, and Simon (1997) indicated that chimpanzees

trained to look at a specific point indicated by the trainer�s gaze did not, as a group, generalize this response to other

kinds of communicative gestures, Barth et al. (2005) showed

0

10

20

30

40

50

60

70

80

90

100

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T ria

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A za

le a

(F )

YNPRC GATI LRC

D av

id (M

)

Fi on

a (F

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G el

b (M

)

Ja cq

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Le sl

ie (F

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E lik

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K an

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)

M ai

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(M )

M at

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N at

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La na

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M ec

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S he

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Fig. 2. Percentage correct on the object-choice task across the three declarative conditions. Each subject is iden- tified by name, sex (F 5 female, M 5 male), and group. We used binomial tests to evaluate whether each ape per- formed at better-than-chance levels, **p , .01, ***p , .001. YNPRC 5 Yerkes National Primate Research Center of Emory University; GATI 5 Great Ape Trust of Iowa; LRC 5 Language Research Center of Georgia State University.

Declarative Comprehension in Apes 363

that with some methodological changes (bringing the apes

into the testing room after the gaze cue had been established

rather than establishing the gaze cue after the choice was pre-

sented), these apes could follow gaze cues successfully.

Call, Agnetta, and Tomasello�s (2000) findings, similar to

our findings, showed that the addition of vocalizations or

sounds to a communicative cue increased performance, likely

by bringing increased attention to the communicative signal.

More recently, Ruiz et al. (2009) showed that lemurs that

attend the most to a cue, as measured by their visual attention,

are those most likely to follow that cue, a finding suggesting

that perhaps the function of the social-communicative envi-

ronment is to increase attentiveness to communicative cues.

However, Povinelli et al. (1997) demonstrated that his chim-

panzees attended to a communicative gesture (measured by

the chimpanzee looking at the experimenter, then glancing

at the correct box in an object-choice task), but that this did

not predict successful choices. These results suggest that

attention is not the only mechanism driving apes� success

on object-choice tasks. More research is required to begin

to separate out possible mechanisms underlying the differen-

ces between individuals within and between species who are

successful and unsuccessful on the object-choice task.

Vygotsky (1978) noted that the correct social environment

could raise children of a given age to a level of abilities not

normally seen at that age, as long as these abilities were with-

in their ‘‘zone of proximal development.’’ Our results suggest

that the comprehension of declaratives is within the apes� ‘‘zone of proximal capability’’ and can be cultivated under

socially and communicatively rich environments. Because

the ability to acquire declarative comprehension is common

to both apes and humans, researchers must look elsewhere

for a candidate biological change that allowed for the evolu-

tion of human language and cognition.

Acknowledgments

We wish to thank Bill Fields, David Washburn, and Charles Menzel

for their assistance in arranging for the data to be collected at the

Great Ape Trust of Iowa and the Language Research Center of

Georgia State University. We thank the research staff at all three

locations for their assistance.

Declaration of Conflicting Interests

The authors declared that they had no conflicts of interest with

respect to their authorship or the publication of this article.

Funding

Funding for this study was provided by National Institutes of Health

Grants HD-56232 and HD-38105.

YNPRC GATI LRC Group

Point Vocalize Point and Vocalize

0

10

20

30

40

50

60

70

80

90

100

C or

re ct

T ria

ls (%

)

Fig. 3. Mean percentage correct on the object-choice task for each group in each declarative condition. Performance was evaluated relative to chance (m 5 50%) using one-sample t tests, *p , .05, **p , .01, ***p , .001. Error bars represent standard errors. YNPRC 5 Yerkes National Primate Research Cen- ter of Emory University; GATI 5 Great Ape Trust of Iowa; LRC 5 Language Research Center of Georgia State University.

364 Lyn et al.

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Declarative Comprehension in Apes 365

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