A case of spontaneous tool-making by a captive capuchin monkey
- Neotropical Primates 04/2011;
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ABSTRACT: Some populations of capuchins are reported to use tools to solve foraging problems in the wild. In most cases, this involves the act of pounding and digging. The use of probing tools by wild capuchins is considerably less common. Here we report on the results of an experimental field study conducted in southern Brazil designed to examine the ability of wild black-horned capuchins (Sapajus nigritus) to use a wooden dowel as a lever or a probe to obtain an embedded food reward. A group of eight capuchins was presented with two experimental platforms, each housing a clear Plexiglas box containing two bananas on a shelf and four inserted dowels. Depending on the conditions of the experiment, the capuchins were required either to pull (Condition I) or push (Conditions II and III) the dowels, in order to dislodge the food reward from the shelf so that it could be manually retrieved. In Condition I, four individuals spontaneously solved the foraging problem by pulling the dowels in 25% (72/291) of visits. In Conditions II and III, however, no capuchin successfully pushed the dowels forward to obtain the food reward. During these latter two experimental conditions, the capuchins continued to pull the dowels (41/151 or 27% of visits), even though this behavior did not result in foraging success. The results of these field experiments are consistent with an identical study conducted on wild Cebus capucinus in Costa Rica, and suggest that when using an external object as a probe to solve a foraging problem, individual capuchins were able to rapidly learn an association between the tool and the food reward, but failed to understand exactly how the tool functioned in accomplishing the task. The results also suggest that once a capuchin learned to solve this tool-mediated foraging problem, the individual persisted in using the same solution even in the face of repeated failure (slow rate of learning extinction).American Journal of Primatology 05/2011; 74(4):344-58. · 2.46 Impact Factor
Neotropical Primates 14(2), August 2007
Freese, C. H. e Oppenheimer, J. R. 1981. The capuchin
monkeys, genus Cebus, p. 331 – 389.
Em: A. F. Coimbra-Filho e R.A. Mittermeier (Ed.). Ecolo-
gy and behavior of Neotropical primates. Rio de Janeiro,
Academia Brasileira de Ciências, 496pp.
Garber, P. A. 1989. The role of spatial memory in primate
foraging patterns: Saguinus mystax and Saguinus fuscicol-
lis. Am. J. Primatol. 19: 203 – 216.
Hubener, F. e Laska, M. 1998. Assessing olfactory per-
formance in an old world primate: Macaca nemestrina.
Physiol. Behav. 64: 521 – 527.
Hill, O. C. 1960. Primate comparative anatomy and tax-
onomy. Vol. IV - Cebidae, Part A. Edinburgh University
Laska, M. e Hudson, R. 1993. Discriminating parts
from the whole: Determinants of odor mixture percep-
tion in squirrel monkeys, Saimiri. Comp. Physiol. 173:
249 – 256.
Laska, M., Hudson, R. e Alicke, T. 1996. A study of long-
term odor memory in squirrel monkeys (Saimiri sciureus).
J. Comp. Psychol. 110: 125 – 130.
Lorenzi, H. 1992, Árvores Brasileiras. Nova Odessa: Editora
Ribeiro, J. E. L. da S. 1999. Flora da Reserva Ducke: Guia
de Identificação das plantas Vasculares de Terra-firme na
Amazônia Central. Manaus: INPA. 816pp.
Rimoli, J. 2001. Ecologia de macacos-pregos (Cebus
apella nigritus, Goldfuss, 1809) na Estação Biológica
de Caratinga, MG: Implicações para a Conservação de
Fragmentos da Mata Atlântica. Tese de Doutoramento,
Centro de Ciências Biológicas, Universidade Federal
Robinson, J. G. e Janson, C. H. 1987. Capuchins, squirrel
monkeys and Atelines: socioecological convergence with
Old World Primates. Em: Primate Societies, Smuts, B.B.
et al. (eds.). Chicago: Chicago Society Press.
Sigg, H. e Stolba, A. 1981. Home Range and Daily March
in a Hamadryas Baboon Troop. Folia Primatol. 36(1-2):
40 – 75.
Silva Júnior, J. S. 2002. Taxonomy of capuchin monkeys,
Cebus Erxleben, 1777. Neotrop. Primates 2(1): 29.
Sussman, R. W. 2000. Primate ecology and social structure:
New World monkeys. Needham Heights, Pearson Custom
Terborgh, J. 1983. Five new world primates: a study in
comparative ecology. Princeton University Press, New
Ueno, Y. (1994a). Olfactory discrimination of eight food
flavors in the capuchin monkey (Cebus apella): Com-
parison between fruity and fishy odors. Primates 35:
301 – 310.
Ueno, Y. (1994b). Olfactory discrimination of urine odors
from five species by tufted capuchin (Cebus apella). Pri-
mates 35: 311 – 323.
a case of spontaneous tool-making by a
captive capuchin monkey
Tiago Soares Bortolini
Júlio César Bicca-Marques
Tool use, the use of a free object in the environment as a
functional extension of one’s own body (Beck, 1980), has
been reported in invertebrates, fish, birds, and mammals,
including primates (Alcock, 1989). However, tool use is
not common or widespread in nonhuman primates. It has
been observed in a small number of species including chim-
panzees, bonobos, gorillas, orangutans, some macaques
and baboons, and capuchin monkeys (van Schaik et al.,
1999). Captive capuchin monkeys (Cebus spp.) were long
reported to use tools in a variety of contexts (Visalberghi,
1990; Urbani, 1999). Recently, however, a growing body
of evidence shows that semi-captive and free-ranging capu-
chins in several populations and species use tools, includ-
ing the use of stones as hammers and anvils to crack and
open nuts (Ottoni and Mannu, 2001; Fragaszy et al., 2004;
Moura and Lee, 2004; Waga et al., 2006). Tool-making is
a cognitively complex process that involves an intentional
modification of the tool for improving its efficiency (Beck,
1980). Reports of non-human primate tool-making have
been restricted to the great apes (Boesch and Boesch, 1990;
Fontaine et al., 1995; Tomasello and Call, 1997; Schick
et al., 1999; van Schaik et al., 2003) with the exception
of a few experimentally induced cases in captive capuchins
(Westergaard and Suomi, 1994, 1995; Westergaard et al.,
1995). Here we report a case of spontaneous tool-making
by a captive capuchin monkey.
A group of capuchin monkeys (Cebus sp.) composed of an
adult male, two adult females and three immature males
living in an enriched enclosure 7.0 m long × 8.7 m wide
× 2.9 m high at the Sapucaia do Sul Zoological Park, State
of Rio Grande do Sul, Brazil, was opportunistically (ad
libitum) observed and video-taped in January and Febru-
ary 2007. The enclosure included sand on the floor, trees,
stones, and perches for the monkeys. For enrichment pur-
poses, food was concealed inside ice cubes, PVC pipes, and
On 12 January 2007, an adult female (putative Cebus
nigritus) was observed banging a twig with a piece of stone
against a larger stone, licking/chewing and likely extracting
something from it with her mouth. She was then observed
probing an unseen structure (probably a hole in the enclo-
sure’s drinking fountain) with the modified twig (Fig. 1).
This sequence of events occurred very rapidly. The latency
Neotropical Primates 14(2), August 2007
between the end of banging and the start of probing was
3 to 4 seconds, during which time the female moved from
the banging site to the probing site. After this observation,
the group was monitored for 15 days and no additional
cases of tool-making were observed. The capuchins, how-
ever, often used stones as hammers to crack nuts and other
foods, including ice cubes containing food (Fig. 2).
Although we do not know what happened immediately
prior to this behavioral sequence and could not see whether
the female acquired anything as a result of probing, the
speed at which this sequence of events occurred is highly
suggestive of a causal understanding during object ma-
nipulation and seems to qualify as a case of spontaneous
tool-making. Future research will focus on confirming the
capuchin monkeys’ capability to make tools, an ability
that would suggest less cognitive difference than is pres-
ently thought to exist between capuchins and the great apes
(Visalberghi, 1990, 1997; Urbani and Garber, 2002). In
addition to suggesting that capuchin monkeys understand
cause and effect relationships during object manipulation,
these findings strengthen the argument that the mainte-
nance of captive animals in enriched environments is an
important strategy to allow the expression of the species’
fullest behavioral repertoire. A previous study of the same
group (200 hours during 2002 – 2003) in this enclosure,
but with minimum enrichment (paved ground, a single
swing and no feeding enrichment), failed to record any case
of tool use (D.B. Montano, personal observation). Envi-
ronmental enrichment serves an important function in im-
proving capuchin monkeys’ welfare by reducing boredom
and eliciting tool use.
We thank the staff of the Núcleo de Zoologia of the Sapu-
caia do Sul Zoological Park, especially Renato Petry Leal
and Marcelo Linck, for the permission to conduct this
study. We also thank Paul A. Garber and Bernardo Urbani
for reviewing an earlier version of this manuscript.
tiago soares bortolini, Instituto de Biociências, Uni-
versidade Federal do Rio Grande do Sul, Avenida Bento
Gonçalves 9500, Campus do Vale, Prédio 43323 Sala 115,
Porto Alegre, RS 91501-970, Brazil, e-mail: <tbortolini@
gmail.com>, and Júlio césar bicca-marques, Laboratório
de Primatologia, Faculdade de Biociências, Pontifícia Uni-
versidade Católica do Rio Grande do Sul, Avenida Ipiranga
6681 Prédio 12A, Porto Alegre, RS 90619-900, Brazil,
Alcock, J. 1989. Animal Behavior. 4th ed. Sinauer,
Beck, B. B. 1980. Animal Tool Behavior. Garland, New
Boesch, C. and Boesch, H. 1990. Tool use and tool making
in wild chimpanzees. Folia Primatol. 54: 86 – 99.
Fontaine, B., Moisson, P. Y. and Wickings, E. J. 1995. Ob-
servations of spontaneous tool making and tool use in a
captive group of western lowland gorillas (Gorilla gorilla
gorilla). Folia Primatol. 65: 219 – 223.
Fragaszy, D., Izar, P., Visalberghi, E., Ottoni, E. B. and
Oliveira, M. G. 2004. Wild capuchin monkeys (Cebus
Figure 1. Adult female capuchin monkey (putative Cebus nigritus) using a hammer stone and an anvil stone to pound on a twig that was
then inserted into a crevice (photos from video frames).
Figure 2. Adult female using a stone to crack open an ice cube
with food inside.
Neotropical Primates 14(2), August 2007
libidinosus) use anvils and stone pounding tools. Am. J.
Primatol. 64: 359 – 366.
Moura, A. C. A. and Lee, P. 2004. Capuchin stone tool use
in Caatinga dry forest. Science 306: 1909.
Ottoni, E. B. and Mannu, M. 2001. Semifree-ranging
tufted capuchins (Cebus apella) spontaneously use tools
to crack open nuts. Int. J. Primatol. 22: 347 – 358.
Schick, K. D., Toth, N., Garufi, G., Savage-Rumbaugh,
E. S., Rumbaugh, D. and Sevcik, R. 1999. Continuing
investigations into the stone tool-making and tool-using
capabilities of a bonobo (Pan paniscus). J. Archaeol. Sci.
26: 821 – 832.
Tomasello, M. and Call, J. 1997. Primate Cognition. Oxford
University Press, New York.
Urbani, B. 1999. Spontaneous use of tools by wedge-
capped capuchin monkeys (Cebus olivaceus). Folia Prima-
tol. 70: 172 – 174.
Urbani, B. and Garber, P. A. 2002. A stone in their hands…
Are monkeys tool users? Anthropologie 40: 183 – 191.
van Schaik, C. P., Deanes, R. O. and Merrill, M. Y. 1999.
The conditions for tool use in primates: Implications
for the evolution of material culture. J. Hum. Evol. 36:
719 – 741.
van Schaik, C. P., Ancrenaz, M., Borgen, G., Galdikas, B.,
Knott, C. D., Singleton, I., Suzuki, A., Utami, S. S. and
Merrill, M. 2003. Orangutan cultures and the evolution
of material culture. Science 299: 102 – 105.
Visalberghi, E. 1990. Tool use in Cebus. Folia Primatol. 54:
146 – 154.
Visalberghi, E. 1997. Success and understanding in cogni-
tive tasks: A comparison between Cebus apella and Pan
troglodytes. Int. J. Primatol. 18: 811 – 830.
Waga, I. C., Dacier, A. K., Pinha, P. S. and Tavares, M. C.
H. 2006. Spontaneous tool use by wild capuchin mon-
keys (Cebus libidinosus) in the Cerrado. Folia Primatol.
77: 337 – 344.
Westergaard, G. C. and Suomi, S. J. 1994. The use and
modification of bone tools by capuchin monkeys. Curr.
Anthropol. 35: 75 – 77.
Westergaard, G. C. and Suomi, S. J. 1995. The manufac-
ture and use of bamboo tools by monkeys: Possible im-
plications for the development of material culture among
east Asian hominids. J. Archaeol. Sci. 22: 677 – 681.
Westergaard, G. C., Greene, J. A., Babitz, M. A. and
Suomi, S. J. 1995. Pestle use and modification by tufted
capuchins (Cebus apella). Int. J. Primatol. 16: 643 – 651.
conservation in Porto alegre, rio Grande
do sul, brazil
lines and howler monkey
Luisa Xavier Lokschin
Rodrigo Cambará Printes
Juliane Nunes Hallal Cabral
Urban growth affects ecosystems in several ways, leaving
them more vulnerable (Alberti and Marzluff, 2004). In
Porto Alegre, the combined effects of human presence in-
cluding deforestation, hunting and other indirect effects are
reducing howler’s area distribution with consequences still
unknown (Lokschin et al., 2005). Human density within
a primates’ geographical area should be considered by the
World Conservation Union (IUCN) in the evaluation of
species status (Harcourt and Parks, 2003). The southern
brown howler monkey (Alouatta guariba clamitans, Ca-
brera 1940) is considered an endangered species in Rio
Grande do Sul (Marques, 2003); in Brazil and globally it is
considered near threatened (Machado et al., 2005; Rylands
et al., 2006).
There are many species of Neotropical primates living
close to urban areas, including: Alouatta clamitans (Buss,
1996), Alouatta caraya (Codenotti et al., 2002), Callicebus
nigrifrons (Oliveira et al., 2003), Saguinus leucopus (Poveda
and Sánchez-Palomino, 2004) and Saguinus bicolor (Vas-
concelos et al., 2005). Problems and threats linked to ur-
banization, such as danger from vehicles when crossing
roads, predation by dogs and electric hazard, are already
documented for A. clamitans (Printes, 1999; Alonso et al.,
2005), C. jacchus (Menezes, 2005) and S. bicolor (Vascon-
celos et al., 2005). Ecosystems close to urban areas are im-
portant for wildlife (Dickman, 1987) and measures must
be taken to guarantee their existence. Howler monkeys (A.
g. clamitans) utilize areas of forests close to urban develop-
ments and are suffering from contact with several electric
hazards. Here we describe a way to mitigate the occurrence
of such accidents around Porto Alegre.
Porto Alegre is the capital city of the state of Rio Grande
do Sul, Brazil (Fig. 1), with a population of 1.4 million
(IBGE, 2006). Approximately 10% of the municipal area
is natural semi-deciduous seasonal forest, influenced by At-
lantic rainforest (Brack et al., 1998; Velez et al., 1998). The
southernmost area of the municipality (Fig. 2) is a rural
landscape containing a number of small villages. The most
important natural areas are also in this zone, which is also
the most important area for howler monkeys (Alouatta
guariba clamitans) (Romanowski et al., 1998; Lokschin
et al., 2005). Lami Biological Reserve, the only biological