Current Biology, Volume 19

Supplemental Data

Selection of Effective Stone Tools by Wild Bearded Capuchin Monkeys

Elisabetta Visalberghi, Elsa Addessi, Valentina Truppa, Noemi Spagnoletti, Eduardo Ottoni, Patricia Izar, and Dorothy Fragaszy

Supplemental Procedures

Study Area

Our field site was located at Fazenda Boa Vista in the southern Parnaíba Basin

(9°39’ S, 45°25’ W) in Piauí, Brazil. It is a flat open woodland (altitude 420 m asl)

punctuated by sandstone ridges, pinnacles and mesas rising steeply to 20-100 m above it

[1].

Subjects

Subjects were five adult males, two adult females and one juvenile male. Their

weights, collected four months before the present study, ranged between 3540 g (largest

adult male) and 1780 g (juvenile male). Subjects belonged to a group of 19 monkeys

(Chicao group), composed of five adult males, five adult females, four juveniles, and five

infants (two of which were born during the present study, one of them to Dita, one of our

experimental subjects). Our sample included all the nut-cracking capuchins of the group

except Teninha, a subordinate adult female that never approached the experimental area.

The Chicao group was provisioned in the experimental area with water and some food

(approximately 700 Kcal per day for the entire group). Although capuchins were

provisioned almost daily, they did not visit the experimental area every day. Ten capuchins

routinely use tools to crack open palm nuts, but they have never been presented with

experimental situations requiring tool selection.

Design and Procedure

We presented capuchin monkeys with a choice of stones to transport to an anvil,

where they could crack a nut. Only one of the stones (i.e., the functional one) could be used

effectively to crack the nut. Observation of the spontaneous nut cracking behavior of wild

capuchins over a one-year period prior to this study determined that when adult monkeys

cracked open the species of palm nuts used in the present study (see below), they used

stones heavier than 300 grams, and they did not use weathered sandstones (Spagnoletti

unpublished data). Therefore, in our experiment we manipulated the friability and weight of

the stones.

Capuchins were tested in an area frequently visited in which several sandstone

anvils and one wooden anvil are present (Figure S1). In each trial, the subject had to choose

between two (or among three) stones to crack open a nut. Stones were always positioned in

the same location (hereafter, choice location), at 60 cm from one another. As shown in

Figure S1, the choice location was halfway between a log (wooden anvil, 0.24 m-high) and

a sandstone anvil (low anvil, at ground level), at a distance of 4 m from both of them. Other

sandstone anvils were also present in the area at varying distances: 9 m (ground anvil 1,

0.25 m-high), 3 m (ground anvil 2, at ground level), 12.6 m (high anvil 1, 1.05 m-high), 7

m (high anvil 2, 1.03 m-high), 5.9 (medium anvil, 0.52 m-high).

Figure S1. Schematic Map of the Experimental Area

The gray ovals indicate the stones positioned in the choice location in relation to the anvils

(black ovals), and to the experimenters (E).

Low High 2

Medium Ground 2

High 1

E

Ground 1

Wooden anvil

CHOICE LOCATION

Table S1. Characteristics of the Stones Presented in Each Condition The average weight difference is obtained by calculating the difference in weight for each pair of hammers and by averaging the resulting values. In the Three Stones Size&Weight condition we presented a single big, heavy stone and a single small, light stone; therefore, range and average difference in weight are not provided for these two categories. NATURAL STONES Average weight

± SE (g) Weight range (g) Average weight difference

± SE (g) Average volume ± SE (cm3)

Friability

siltstone sandstone

1009 ± 21 1013 ± 27

923 - 1111 902 - 1155 19 ± 4

417 ± 10 654 ± 62

Size&Weight

big small

994 ± 39 260 ± 12

848 - 1137 205 – 291

734 ± 34

393 ± 24 98 ± 4

ARTIFICIAL STONES Average weight ± SE (g)

Weight range (g) Average weight difference ± SE (g)

Volume (cm3)

Same Size-Different Weight

heavy light

1116 ± 10 99 ± 3

1105 - 1137 91 – 106

1017 ± 5

380 380

Conflicting Size&Weight small heavy big light

804 ± 9 165 ± 3

793 - 823 159 - 173

639 ± 4 380 800

Three Stones Size&Weight big heavy big light small light

1926 165 ± 4 106

NA 159-173 NA

big heavy-big light 1761 ± 4big heavy-small light 1820 small light-big light 59 ± 4

800 800 380

Each trial started when one of the experimenters provided a nut to the subject; this

occurred either by positioning the nut on the wooden anvil (at a distance of 4 m from the

choice location), or by throwing the nut near the subject (at a distance of 4 m, or more, from

the choice location). This procedure guaranteed that the subject was equidistant from the

experimental stones, or approximately so. Table S1 reports the characteristics of the stones

used in the five experimental conditions. We weighed the stones to the nearest 1 g using a

digital scale (Polder® scale). We measured the volume of each stone as the difference

between the level of the water in a marked beaker, with a resolution of 25 ml, with the

stone submerged and without the stone. For sandstones (that absorb water), we made the

same kind of measurement filling the beaker with sand instead of water.

In the Friability condition, the non-functional stone (sandstone) cracks more easily

when it strikes the nut than the functional stone (siltstone), whereas in the Size&Weight

condition the functional and the non-functional stones differed in terms of size and,

therefore, weight. The natural stones used in the above conditions were collected outside

the experimental area in locations far from the anvils used by capuchins to crack open nuts

and where the monkeys have never or rarely been observed. Therefore, these stones can be

considered unfamiliar to the subjects.

Artificial stones were made by filling silicon plasters of different size and shapes

with unsaturated liquid polyester resin (Silica synthetic Amorphous Colloidal Silicon

Dioxide, aereosil), and Organic Peroxides for curing (Butanox M 50). Pigments were added

to the resin so that all the stones used in the Same Size-Different Weight condition were

dark green; in the Conflicting Size&Weight condition all the stones were painted gray and

in the Three Stones Size&Weight condition all the stones were painted brown. To obtain

the desired weight, the stone interior was empty, or filled with resin containing either

calcium carbonate or lead beads. In all conditions, whenever a natural or artificial stone

broke, it was replaced by one of the same type and similar weight.

In the Same Size-Different Weight condition, we used 12 pairs of artificial dark

green stones resulting from all the possible combinations between three heavy and four

light stones (Table 1). In the Conflicting Size&Weight condition, we used 12 pairs of gray

artificial stones resulting from all the possible combinations between three heavy and four

light stones. In the Three Stones Size&Weight condition, we used three triplets of brown

stones resulting from the possible combinations among one heavy large stone, three light

large stones and one light small stone. If one or more stones showed signs of use (e.g.

scrapes), all of them were painted again at least 12 hours before the next session. Moreover,

to further rule out the possibility that capuchins could recognize the individual stones on the

basis of signs of use, in most trials with artificial stones the experimenter scattered sand on

the top of all stones.

The experiment was carried out in November 2007 by EV, EA, and NS. Each

subject performed an average of 2.9 ± 1.0 trials per day. All subjects received 10 trials in

each condition, with the exception of Dita in the Same Size-Different Weight and in the

Conflicting Size&Weight conditions (six and seven trials, respectively) and Teimoso in the

Three-Stones Size&Weight condition (four trials). Dita and Teimoso were subordinate

individuals which rarely approached the experimental area if other group members were

present; furthermore, Dita delivered an infant during this study. Conditions were presented

consecutively; since the experimenter did not have full control of which individual would

participate in the trial for which the tool pair was set, the order of presentation was not

pseudo-randomized. The participation of the eight subjects across conditions is shown in

Table 1.

Nuts

Two species of palm nuts were presented: the tucum (Astrocaryum spp.) and the

catulé (Attalea spp.). These nuts are routinely cracked open by capuchins in Boa Vista. We

used two types of nuts since capuchins like food variety [2]. We chose tucum and catulé

since they require the use of tools, but they can be cracked open by most monkeys in the

group; moreover, their peak-force-at-failure is not significantly different (5.15 ± 0.2 kN for

catulè and 5.57 ± 0.25 kN for tucum, [3]). Their exocarp and mesocarp were usually

removed before giving the nut to the subject to increase the probability the monkey would

crack the nut (rather than eat the mesocarp).

Measures Scored

Two experimenters scored the data by paper and pencil from a distance of 5.0 m

from the choice location (see Figure S1), while a third one set the tool pair as required by

the trial and provided the subject with the nut. The experiment was videotaped and scored

for reliability by a naïve observer who was blind to condition. Reliability scored on 25% of

the trials was 100% for first stone touched, transported, used, success and switching; it was

92% for tapping.

Supplemental Results

Switching Behavior

After touching the first stone, subjects could (a) immediately transport it to the

anvil, or (b) explore the other stone(s) before deciding which stone to transport to the anvil.

Switching between stones could occur zero, one, or more times. In the Friability condition

only one subject switched once. In the Size&Weight condition switches between stones

occurred in 7.5% of the trials (four subjects switched). In Same Size-Different Weight and

Conflicting Size&Weight conditions, switches occurred in 30.3% (Same Size-Different

Weight condition, seven subjects) and in 23.4% (Conflicting Size&Weight condition, seven

subjects) of the trials. Finally, in the Three Stones Size&Weight condition switches

occurred in 70.3% of the trials (all subjects switched). Trials with switches occurred

significantly more with artificial stones than with natural ones (T= 0, N = 7; p = 0.018).

Overall, in the trials in which switches occurred, subjects switched on average 1.0 ± 0.0

(Size&Weight condition), 1.22 ± 0.12 (Same Size-Different Weight condition), 1.05 ± 0.05

(Conflicting Size&Weight condition), and 1.59 ± 0.12 (Three Stones Size&Weight

condition) times per trial. Figure S2 illustrates a trial in which several switches occurred in

the Three Stones Size&Weight condition.

S

S

a

fed

b c

Figure S2. Switching Behavior in the Three Stones Size and Weight Condition

The stones are positioned as follows: left, small light stone; center, large light stone; right,

large heavy stone (from the reader’s point of view). Chicao, an adult male, contacts the left

stone (A), turns his head towards the other stones (B), and switches (white arrow) to the

middle stone (C). Then, he switches (white arrow) to the correct stone (E), transports it to

the wooden anvil (not shown), and lifts the hammer stone to crack open a tucum nut (F)

(Photos by Noemi Spagnoletti).

Latency to Choose

The time elapsed between the first contact with either stone at the choice location and the

onset of the transport to the anvil reflects the individual’s decision-making processes. The

decision-making process was straightforward in terms of latency to transport, which did not

differ significantly among conditions (Friability condition: 8.10 s ± 2.65 s, Size&Weight

condition: 5.35 s ± 1.39 s, Same size-Different weight condition: 6.82 s ± 1.32 s,

Conflicting Size&Weight condition: 6.81 s ± 1.63 s, Three-stones Size&Weight condition:

8.44 s ± 1.12 s; Friedman ANOVA: χ24 = 5.14, N = 7; p = 0.27, NS).

Anvil Use

Overall, the preferred anvil was the log (used in 76.6% of the trials) followed by the

low anvil (used in 9.4% of the trials). The distance covered by subjects with the selected

stone was similar across conditions. On average, capuchins bipedally transported the

selected stone for 4.25 m ± 0.05 m, at a height of 0.31 m ± 0.03 m. In 1.1% of the trials,

capuchins cracked open nuts also on a 1.6 m-high tree fork (2.4 m from the choice

location), and in one instance a female with a new-born infant (Dita) cracked open the nut

on a 6.9 high-tree (2.4 m from the choice location).

The weight of the functional stones ranged between 793 g and 1926 g; thus, the

stones transported ranged from 22% to 54% of the weight of the largest subject (Chicao),

and from 44% to 108% of the lightest subject (Tucum). Stones were transported on average

for 4.62 ± 0.6 m.

Supplemental References

1. Visalberghi, E., Fragaszy, D., Ottoni, E., Izar, P., de Oliveira, M. G, and Andrade, F. R.

D. (2007). Characteristics of hammer stones and anvils used by wild bearded

capuchin monkeys (Cebus libidinosus) to crack open palm nuts. Am. J. Phys.

Anthropol. 132, 426-444.

2. Addessi, E. (2008). Food variety-seeking in capuchin monkeys. Physiol. Behav. 93, 304-

309.

3. Visalberghi, E., Sabbatini, G., Spagnoletti,N., Andrade, F. R. D., Ottoni, E., Izar, P. and

Fragaszy, D. (2008). Physical properties of palm fruits processed with tools by wild

bearded capuchins (Cebus libidinosus). Am. J. Primatol. 70, 1-8.