1Robust capuchin tool use cognition in the wild

3Tiago Falótico1,2

51 School of Arts, Sciences and Humanities, University of São Paulo, Brazil

62 Neotropical Primates Research Group, Brazil

7tfalotico@gmail.com

9Abstract

10Most of the studies on primate cognition focus on Catarrhines primates closely related to

11humans. One alternative primate model for understanding primate cognition is the Platyrrhine

12capuchin monkey (genus Cebus and Sapajus), which has several convergent traits to hominins.

13Although capuchins have been targets of cognition studies in laboratories for decades, primates

14in captivity lack the complete social structures and ecological factors associated with free-

15ranging environments. Increasing the focus to wild capuchins represents a welcome change to

16complement captive primate cognition studies in the past decades. Here I do a non-exhaustive

17review of cognition research on wild robust capuchins (Sapajus), focusing on tool use. Those

18studies are on the rise and are a source of valuable information to understand primate

19cognition in natural, evolutionary valid environments, where cognition can be tested and

20studied in situations similar to those in which those traits evolved.

21

22
23--

24Nonhuman primates have been one of the main targets of cognition studies due to their

25evolutionary proximity to humans. Most of those studies focus on species most closely related

26to humans, such as apes and Afro-Eurasian Monkeys [1]. However, the capuchin monkey (genus

27Cebus and Sapajus) is an interesting primate model to understand primate cognition. Those

28American primates are separated by approximately 32-43Ma from the human lineage [2,3] but

29present several characteristics – tool use, high encephalization, hand morphology, dietary

30flexibility [4]– that are like hominoids, making them an excellent alternative model to study key

31cognition traits shared with humans and other apes.

32

33Capuchin monkeys have been targeted for cognition studies in laboratory settings for as long as

34primatology has been a discipline [4]. Easily accessible to researchers and allowing the control

35of certain variables which cannot be as easily controlled in the wild (e.g., diet, opportunities to

36engage in tasks, time of exposure), capuchin monkeys have been studied to examine several

37traits of cognition: physical causality [5–7], tool use [8–13], social reasoning [14–16], learning

38[17,18], among other topics.

39

40Although valuable data can be gathered from captivity, sometimes with the same results as in

41the wild or complementing those [19,20], primates in captive studies usually lack the complete

42social structures associated with wild or free-ranging environments. Moreover, they often do

43not interact with ecological factors wild individuals evolved with, making the ecological validity

44of some of those captive studies more limited compared to wild studies [19,20]. Increasing the
45focus of capuchin cognitive studies to wild individuals was a welcome change in the past 20

46years. The change was not easy, as many early studies on capuchins concentrated in forest

47populations (Amazonian and Atlantic Forest), which made experimental studies difficult as

48capuchins are mainly arboreal in those environments and difficult to observe and interact with.

49However, studies in those environments were successfully done. When, later, field research

50was conducted in more open environments (savanna-like), mainly focusing on tool use, the

51quantity of data increased.

52

53Here I will review some of the work on cognition done on robust capuchins (genus Sapajus) in

54non-captive environments, focusing on tool use. Primatologists and anthropologists have much

55interest in this behavior, as it is a pivotal characteristic of humans. Understanding how

56primates' object physical cognition works (e.g., the physical features they use to select an

57object as a tool; or how they understand the action of a tool), especially in a wild setting, helps

58us to understand better the evolutionary history and origins of tool use behavior. The same

59applies to the social cognition related to tool use. For example, from whom do primates socially

60learn how and where to use objects as tools? How the information flows inside a social group?

61Understanding social learning of tool use is also of great interest because is an essential trait for

62maintaining and spreading cultural behaviors [21]. Cultural variation has been a growing

63interest in primates (and other animals) as it can be a second inheritance system, rapidly

64changing and sometimes coevolving with biological traits [22], and can have an impact on the

65diversity and conservation of animals [23].

66
67Tool use

68Tool use in capuchins has been of much interest, particularly the use of stones as percussors, as

69capuchin monkeys are one of the few non-human primates that habitually use stone tools [24].

70Until about 20 years ago, only captive individuals were observed to execute this behavior

71frequently, and it was hence believed to be a product of captive life. That view began to change

72when capuchins of free-ranging groups living in urban parks were observed to habitually crack

73open palm nuts with stone tools [25,26]. Although not in a completely wild situation, those

74groups of free capuchins spontaneously used stone tools, and the behavior was apparently

75maintained in those groups across generations.

76With the increase of studies on capuchin species living in Brazilian savanna-like environments

77(Cerrado and Caatinga), mostly Sapajus libidinosus but also S. xanthosternos, we now know that

78robust capuchins living in those biomes habitually use stone tools to access encased food

79(Figure 1) [27–30], making them a good model to understand the cognition related to tool use

80behavior, an issue relevant to human evolution studies [31].

81
82

83Figure 1 – Map of Brazilian biomes with the indication of the presence – sensu [32] – of

84pounding stone tool use behavior in populations of Sapajus spp. Source of data [27–29,33] and

85[T. Falótico, unpublished data]. Map created by Tiago Falótico.

86

87

88Although the percussive use of stones is usual in those populations, there are behavioral

89occurrences that are more restricted, present only in some or only one population, such as the

90use of stones to aid in digging, or stone throwing as tools for communication, that have been

91observed habitually in, so far, one population at Serra da Capivara National Park [33–35]. The
 92same is true for the use of probes, which have been observed occasionally in some wild

93populations, but the habitual use is only known to be done by male capuchins at Serra da

94Capivara [36]. This variation of behavior repertoire (Figure 2) is an exciting topic, as it presents

95an excellent target to study cultural variance (see below).

96

97

98Fig. 2 – Examples of tools used by robust capuchin monkeys in the wild. A) Digging with a stone

99tool. B) hammer stone tool to crack open palm nut. C) Stone on Stone, with fracture of the

100hammerstone. D) probe tool use. Photos by Tiago Falótico.

101

102
103Stone tool choice

104Some of the first studies about the use of stone tools were conducted to determine if and how

105the capuchins chose the stones to be used as tools and which physical properties they took into

106account to do so. This information can show us if these primates can recognize the material

107properties of objects. The results we have are evident on some points. The hardness of the

108target apparently is a significant factor. Several studies have shown a correlation between the

109stone size/weight and the target’s hardness. In places where the main targets are harder palm

110nuts, the stone tools used by capuchins are heavier, sometimes weighing more than an average

111adult male individual. For example, at the Fazenda Boa Vista site, home of the EthoCebus

112project [37], the stone tools used to crack hard palm nuts average 1059g [38]. In populations

113where the monkeys also explore softer or smaller food resources, the stone tool weight

114correlates with the target’s hardness [28,39]. Even in Fazenda Boa Vista, the capuchins can use

115lighter non-lithic percussors to process softer cashew nuts [40].

116The weight, more than size, appears to be a significant factor selected by the capuchin, as

117shown in an experiment in which stones of the same format and size but different mass were

118presented to the monkeys at Fazenda Boa Vista. The capuchins explored and selected the

119heaviest stones to crack a hard-resistant palm nut [41]. However, when exploring different

120resources, softer than palm nuts, capuchins may use other factors to select the tool or not use

121tools at all.

122Cashew nuts (Anacardium spp.) are easier to open than palm nuts. Capuchins can use mouth,

123hands alone, stone tools, or other behaviors (e.g., rubbing green cashew nuts against a trunk to

124produce a hole) to get access to the inner endosperm. Capuchins at Fazenda Boa Vista perform
125a rubbing behavior to open a hole on fresh cashew nuts to access the kernel [42] but can use

126stone tools to crack the harder dry nuts when stones are experimentally provided [40]. At Serra

127da Capivara, where the S. libidinosus population uses stone tools for a greater variety of

128behaviors [27,33–36], the capuchins use stone tools to process all stages of cashew nuts [33].

129However, the selection of the stones to process cashew nuts appears to consider the caustic

130liquid present in the husk of the nuts. Field experiments on tool selection to process cashew

131nuts at Serra da Capivara showed that capuchins select stone tools not only by the weight

132necessary to crack open the target but also considering the area of the tool as protection

133against caustic liquid release by green cashew nuts when break, showing that monkeys can use

134several clues when selecting stone tools [43]. Moreover, in the same set of experiments, it was

135suggested that some individuals could use the asymmetry of cashew nuts, positioning them in

136an optimal way that facilitates the rupture of the shell [44].

137Interestingly, some capuchin populations appear not to explore cashew nuts at all, apparently

138being deterred by the chemical protection of the nuts [28,29,45].

139

140Tool selection can have multiple factors affecting it, depending on the physical properties of the

141targets and raw material availability, suggesting that capuchins perceive multiple physical

142properties. Distance of the tool from the use site can also be a factor in tool selection. In a field

143experiment on this topic, more distant potential tools were less selected by the monkeys.

144However, some individuals continued to prefer heavier stones, even when those were more

145distant [46]. Another experiment also included the transport of the food item as a factor,

146placing apart nuts, two hammers, and an anvil. The capuchins usually obtained the food first,
147even if they had to walk past the hammers. After they secured the nut, they usually selected

148the hammer closer to the anvil, showing a selection sequence that optimized energetic costs

149and resource protection [47].

150

151Another topic studied in the field is how efficiently the monkeys use the stone tools, perceiving

152the object’s properties and plastically adjusting their responses. They can perceive and adjust

153the behavior to the weight of the stone and the resistance of the target - heavier stones to

154crack more resistant targets [28,39]. Even other dimensions can be used to these adjustments,

155such as area, as in the case of capuchins using larger stones to protect themselves from cashew

156nut caustic liquid [43]. The monkeys also learn to use the stones more efficiently over time.

157After a few uses, a proficient tool user will quickly learn how to grip an unknown stone more

158efficiently, adjusting their grip dynamically during the strike (e.g., avoid striking with a slanted

159trajectory, missing the nut, or losing control), after a few uses [48].

160

161Social learning

162Another interesting theme is how capuchins learn and diffuse knowledge among the group's

163individuals, maintaining a behavioral tradition through social learning.

164Although this question has been widely addressed in the laboratory [49–52], field experiments

165provide a more ecologically valid way of testing this. A significant body of evidence shows that

166capuchins use stimulus enhancement as a major form of social learning, especially when

167learning to use stone tools, using cues from the presence or previous manipulation leftovers

168from conspecifics, even without direct observation [53–55]. The target (or models) young
169capuchins choose to observe or be closer to are not random, though, in the case of nut-

170cracking, they appear to observe older, more proficient, and dominant individuals. This pattern

171may lead to access to more leftover food in the tool use area, reinforcing the exploration of the

172tool use site and its objects [55].

173In capuchin groups living in Serra da Capivara, social learning was studied using an experimental

174apparatus with two possible solutions. This allowed researchers to track the chain transmission

175of each solution throughout each group using Network-Based Diffusion Analysis [56,57],

176showing that young monkeys presented the same pattern of observation as in the case of

177nutcracking, observing more proficient individuals [58]. In another population, Fazenda Boa

178Vista, observations showed that young monkeys were more likely to reuse stone tools used by

179another individual, focusing on their behavior on actions relevant to cracking nuts [59], and that

180object manipulation is more efficient in adults [60].

181

182This modification of the environment because of the stone tool use was also thought to be

183compatible with Niche Construction theory. This theory says that the animals can modify their

184environment, sometimes cumulatively over time, changing sources of natural selection in their

185environment, and creating new ecological niches [61]. In the case of stone tool use, this niche

186could be the nut-cracking site, as social diffusion may depend on the conspicuousness and

187permanence of tools and leftovers to create a learning environment [62]. For stone tools that

188usually are left at the tool site, where they can be reused, the niche construction is a good

189explanation, and probably one of the reasons that stone tool use is more frequent than, for

190example, throwing stones, which do form tool use site. Stick tools used for probing also do not
191create many reusable sites. Even though some capuchins can quickly learn, at least in a

192scaffolded situation, to pull probes to obtain a reward [63], others, such as the population of S.

193libidinosus from Fazenda Boa Vista, did not solve a similar task with probes [64], showing that

194there may be variance in that capacity.

195Differences in the behavioral repertoire between populations of robust capuchins have been

196the target of several studies in the past years to identify cultural traits and the factors leading to

197them [27]. The culture of non-human animals, particularly primates, has been of great interest

198[65], including initiatives to identify capuchin monkeys’ cultural variance [66]. Behavior

199variations are essential not only to understand cultural evolution in primates but also to argue

200for the conservation of rare cultural behaviors in the wild, such as some of the variants of

201capuchin stone tool use behavior or probe tool [23,67]

202

203Conclusion

204The study of tool use cognition in wild capuchin monkey populations can be a source of

205information to understand primate cognition - such as physical properties of objects and food,

206selective observation and learning bias from proficient models, and plasticity in the use of

207objects as tools. Research with a focus on individuals living in a natural, evolutionary valid

208environment that may better reflect the ecological pressures (physical and social) where those

209cognitive traits evolved, providing more robust results. There is still a need to improve methods

210to control confounding variables in wild settings experiments, but using both captive and wild

211experiments can help us to understand primate cognition better.

212
213

214Conflict of interest statement

215Nothing to declare.

216

217

218Acknowledgments

219I thank the organizers of the special issue for the invitation and the reviewers for helpful

220suggestions to improve the manuscript. During the writing of this manuscript, the author was

221supported by the São Paulo Research Foundation (FAPESP #2018/01292-9; 2019/00716-2) and

222the National Geographic Society (Explorer grant NGS-64133R-19).

223

224

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