Understanding the Ins and Outs of Tool Use in Capuchin Monkeys with Professor Patricia Izar

In this episode of The PrimateCast origins, we’re sharing a lecture from primatologist and cognitive ethologist, Patricia Izar from the University of São Paulo.

Pat is one of the eminent Latin American primatologists, and along with her close friends and colleagues Drs. Dorothy Fragaszy and Elisabetta Visalberghi - see episode #68 for more on this from Elisabetta Visalberghi - she’s been studying the incredible tool use behavior of robust capuchins for the past few decades.

Capuchins are one of the very few non-great ape primates that are known to commonly use tools in nature - they use stones and anvils to crack open tough nuts and aquatic invertebrates (Paywall).

Pat walks us through a series of fascinating experiments with these charismatic monkeys - who by the way you can hear make a series of audio-only cameos in the background while she shows our Zoom audience some videos. Her target? Trying to understand what they know about the tools they use and what benefits they gain from using them.

Check out a short documentary about the EthoCebus project, of which Pat is a key member.

Because of her long history of observing and experimenting with wild capuchins, she challenges the idea from laboratory experiments with captive-reared individuals that capuchins don’t  understand how or why the tools they use work; a commonly held belief that, unlike humans, monkeys don’t really have a strong sense of the ‘folk physics’ underlying their behavior.

Other topics that come up:

• selecting the best tools to use 
• what environmental factors affect when and how capuchins use tools
• how using tools might affect social relationships
• the nutritional benefits of tool use in different seasons
• Have you ever wondered how heavy those stones are?
• playing with perception by providing huge stones that are light as a feather

Pat ends by talking about how this iconic behavior in capuchins can tell us a lot about the evolution of tool use in humans. By studying animals like capuchins, we can learn a lot about the kinds of conditions that are likely to have fostered this cognitively demanding behavior during our evolution.

Although she doesn’t mention it in the lecture, Pat is also a key figure in the profession and development of primatology, both locally in Brazil and internationally. She is currently the President of the Brazilian Society of Primatology, and serves the International Primatological Society as its VP for Education.

The PrimateCast is hosted and produced by Andrew MacIntosh. Artwork by Chris Martin. Music by Andre Goncalves. Credits by Kasia Majewski.

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Transcript

Andrew MacIntosh: 0:00

Welcome to the Primate Cast Origins. Today's origin story comes from Patricia Isar and is all about those amazing tool using capuchins of Brazil. Welcome back to Primate Cast Origins. We are here from experts in the field of primatology and beyond about how they got started and became some of the most influential folks around. I'm your host, andrew McIntosh from Kyoto University's Wildlife Research Center, and this episode is taken from our International Primatology Lecture Series Past, present and Future Perspectives of the field. This is the brainchild of Dr Michael Huffman and, like Our Normal Programming, is brought to you by PsyCASP. The main goal of the lecture series is to share the origin stories of experienced practitioners of primatology and related fields. To do that, mike Huffman has invited a revolving door of renowned scientists to join us on the program and share their own stories with us. The Primate Cast Origins is our way of sharing those stories right here on the podcast. Unlike our normal interview format, these lectures are being done as part of the PsyCASP Seminar in Science Communication, which is aimed at grad students here in the Primatology and Wildlife Science program at Kyoto University. So what you'll hear is a lecture that was recorded in Zoom and generally includes slides, so there may be references to visual aids and videos that are not available in audio only format. But for anyone wishing to see the speakers presenting their talks, we invite you to check those out on the PsyCASP TV YouTube channel.

Andrew MacIntosh: 1:54

Now, in this episode of the Primate Cast Origins, we're sharing a lecture from primatologist and cognitive ethologist Professor Patricia Isar from the University of Sao Paulo. Pat is one of the eminent Latin American primatologists and, along with her close friends and colleagues, doctors Dorothy Fricese and Elizabeth Fisselbergi, who we had previously in this series before, she's been studying the incredible tool use behavior of robust capuchins for the last few decades. Now, capuchins are one of the very few non-grade eight primates that are known to commonly use tools in nature. They use stones and anvils to crack open tough nuts and aquatic invertebrates. In this lecture, pat walks us through a series of fascinating experiments with these charismatic monkeys who, by the way you can hear, make a series of audio only cameos in the background while she shows Zoom our Zoom audience some videos.

Andrew MacIntosh: 2:44

Now her target, trying to understand what they know about the tools they use and what benefits they gain from using them. Because of her long history of observing and experimenting with wild capuchins, she challenges the idea which, by the way, came from laboratory experiments with captive reared individuals, that capuchins don't really understand how or why the tools they're using actually work. This is a commonly held belief that, unlike humans, monkeys don't really have a strong sense of the folk physics underlying their behavior. Through her talk, she also explores other questions, like what environmental factors affect when and how capuchins use tools, and how using tools might affect social relationships and, of course, unlock nutritional words that are not available to them otherwise. She ends by talking about how this iconic behavior in capuchins can tell us a lot about the evolution of tool use in humans.

Andrew MacIntosh: 3:34

We might be similar in our tool use capacity to chimpanzees because we share a common ancestor, but capuchins are way over there, in another branch of the primate family tree, and there's a whole bunch of other primates in between them and us that are not tool users at all. So it's fascinating to think about how and why tool use behavior evolves throughout the animal kingdom. Corvids, like crows, are another famous group of tool using species that are way off in a different branch of our family tree. So we can learn a lot about the kinds of conditions that are likely to have fostered this cognitively demanding behavior tool use during our evolution. Although she doesn't mention it in the lecture, pat is also a key figure in the profession and development of primatology, both locally in Brazil and internationally. She's currently the president of the Brazilian Society of Primatology and serves the International Primatological Society at its VP for Education. So, with all that said, I'm sure you're going to love hearing about her impressive work on capuchin tool use. And, as always, here's Dr Mike Huffman with an introduction to Get Us Started.

Michael Huffman: 4:38

I'd like to welcome all of you again to this lecture series. Thanks for coming early in the morning to listen to this. Some of you in other parts of the world may be in the evening, like it is for Pat, but all of you are very welcome and we really appreciate your watching this lecture series. It's a really great pleasure to have Pat join us today. We've been in contact for off and on for quite some time through journal reviews and different processes like that, and I'm very much aware of the work she's done, but I've never probably never heard her actually speak in person. So this is an exciting moment for me and I think you'll all really enjoy what she has to share.

Michael Huffman: 5:23

Coming from my chimpanzee perspective, when I was first starting there was a lot of hype about chimpanzee tool use and how advanced they were and they're the best model for human evolution of tool use. But when I started learning more about the work that the Capuchin researchers have been doing, earlier in the series we had Elisabetta Weisselbergi and she shared some of her work. She's a good friend and a close collaborator with Pat, so I think we'll learn a lot more about Capuchin tool use today. But in my mind, the work that this group in Brazil has been doing is incredible. It really really outdoes, outshines the research on chimpanzee tool use, I think because they've gone into it so much more deeply and have looked at issues that just chimpanzees haven't done yet. So I think we all have a lot to learn from the work that they're doing, and today is the day that we hear from Pat, so I'll hand it over to you. Thank you so much for joining us today.

Patricia Izar: 6:30

Thank you so much, mike, for this presentation. Thank you, sasuomo and Andrew also for all the help here. I'm very excited to be with you virtually. Well, let's go to the lecture. The title of my lecture today is on causes and consequences of tool use lessons learned from wild Capuchin monkeys. And let me show you a little movie. We are seeing here a cascudo. He's the current dominant male of. He's an adult male, but Capuchin monkey Is it working? And or or Makako prego, as we say in Portuguese. Capuchin monkey in Portuguese is Makako prego. He cascudo is crack opening a hard pound nut using a hammer stone as a tool. That's cool. Do is the current. As I said, he's the current dominant male of a wild group of Capuchin monkeys, of course, that lives in this area, the, the Fazenda Boa Vista.

Patricia Izar: 7:47

Fazenda Boa Vista is an area located in the north. Do you see my my arrow here? Can you see it? Fazenda Boa Vista is located in the north eastern region of Brazil, in the city of Gilboas, in the Piawe state. What's important here to show to you is more or less in this region. This is the echo tone between the sejado and the cutting and this, as you can see in this picture and also in this one and this one. These are the open woodland savanna, like Brazilian beoms and I'm showing this picture and this sejado area in the region of Gilboas in Fazenda, boa Vista. It's the transition with the cutting which is, in fact, the semi arid habitat in beyond in Brazil. So it's a very dry sejado and I wanted to show this to you because sometimes, when we think about Brazil monkeys in Brazil people think about the tropical forest, the Amazonia and the Atlantic forest, and this is a very different area. As you can see here, I first visited this area in 2003 with doctors Dorotifra Gazi and Elisabeta Vizalberg that I mentioned before, my colleagues and today my very dear friends, and with them and with the collaboration of the Olivaida family, we established this already long-term project that we call the etosebus, or itosebus, to investigate the ecological, social, cognitive and developmental factors associated to use in this population, and I will talk about it today, all these findings. But I want to emphasize that this talk today, my talk today, is only possible due to this long-term collaboration among three women scientists and all that is involved about being three women one in the United States, another one in Italy and another one in Brazil and also with students from all over the world not only our countries, but we had students from China, from Israel, from India and with the local community. That allowed us to build a long-term database that indeed revolutionized our knowledge on non-human to use.

Patricia Izar: 10:42

First, I think it's important to emphasize that my talk today is on robust Kapuchin monkeys. This is a group of eight biogeographic species that belong to the genus Sapajos. These genus, as you can see here in this map, presents a wide geographic distribution almost all over South America, from Amazonia and Atlantic Forest, sejado, kattinga and Pantanal. So they occupy these different biomes that present distinct ecological features and they present corresponding behavioral variation in relation to these ecological. Different ecological features in many behavioral domains, from body posture and locomotion, more bipedal, more when they walk, more on the ground, also in their navigation systems and in their social systems. But for the purpose of our talk today, I want to highlight their great variation in feeding behavior.

Patricia Izar: 12:02

Kapuchin monkeys are onivorous primates. They include a wide variety of items to complement their preferential forgivry, including meat. But they vary not only in the types of foods, the items they eat, but also in their diet composition. So they are mainly forgivores, but in some populations they are more insectivores and others. They are even more for livros than others, but, most importantly again, for what we are talking today. They can extract foods that are inaccessible for most vertebrates, such as the heart of palm trees, as we can see here Sapajos nigritos, the species that I study in the Atlantic Forest that I'm not talking about today, but they are able to extract the leaves of the palms and eat the heart of the palms and, of course, they can use tools to crack open hard foods, including crabs and oysters, as we can see in these pictures here from the mangrove in Malinian state.

Patricia Izar: 13:22

We first described the customary use of stone tools in Fazenda Boavista in 2004, in this paper of 2004. And you can see in this map here this is the PIE state and Gilboés, fazenda Boavista is here where we first published this report. Right after our publication, antonio Moura and Phyllis Lee published another report here in Serra da Capivara. So Gilboés, fazenda Boavista, in Gilboés, in Serra da Capivara, in São Raimundo Nonato, more or less three kilometers apart. So is this something about PIE state?

Patricia Izar: 14:12

After these first descriptions at that time, we're super surprising. It was really something that everybody was oh my god, a Platini primate using tools. Oh, we never heard about it. It was not known from scientists that they were using tools in nature. And after that these first descriptions, other reports were published and today we know that several populations along the central portion of the distribution of the genus Sapajos used tools. But up to now, these reports that are here with these triangles and stars, all these reports belong or are restricted to three species Sapajos libidinosus, as I mentioned, as in Fazenda Boavista, sapajos flavios and Sapajos chantostenos. So among the eight species, three are reported to use tools, so this could indicate a genetic condition for two use. Fortunately, these three species, in particularly flavios and chantostenos. They occur in the more sherry and open biomes of Sejado and Katzinga, but also in areas of forest. Flavios and chantostenos, indeed, are species of Atlantic forest that reach areas of Sejado and Katzinga, and the forest populations of these species do not use tools. At least, there are no reports of eight. Intensive surveys have been conducted. Eduardo Toni and I revealed these evidence in this paper published in 2008. And now our conclusions still hold true. We suggested that the evidence at that time and it's still true favors the idea that environmental features rather than cognitive differences among species are related to the emergence of two use in certain populations Indeed.

Patricia Izar: 16:43

In a more recent review comparing long-term studies on seven populations of four species of sapagios that use tools and do not use tools, briseida Resendri, renata Ferreira and I addressed existing hypotheses to explain variation in the occurrence of two use among primate populations. More traditionally, feeding tools have been considered a strategy for extracting embedded foods in conditions of fruit scarcity. Tools would be a feeding adaptation to the necessity of finding alternative foods. It's called the necessity hypothesis. Later, the idea that two use would be associated to availability of time and to a higher degree of group cohesion, which are more common features more commonly associated to food abundance, was introduced. This is called the opportunity hypothesis. By comparing our seven populations Briseida, renata and I, we found evidence that two use is associated to higher food availability. So we found populations that do not use tools and have lower food availability than the populations that use tools and also related to the availability of encased foods, favoring the opportunity hypothesis.

Patricia Izar: 18:21

In the same line, in our study population of Fazenda, boa Vista, we analyzed two use in relation to food availability. This was the PhD of Noemi Spagnaletti. We compared the frequency of two use between two groups, one of which was slightly provisioned with palm nuts and corn and the other one was not provisioned, and between the dry and the wet season. In fact we conducted correlations with rainfall. The rainfall is really different between the dry season it's really dry, zero rainfall and the wet season. So we did not find there was no difference between the two groups, provision and non-provision, and between seasons. There was no correlation with rainfall in the frequency of two use. The only correlation we found it was between two use in the non-provision group and the availability of the more abundant nut, the catalan nut, that these group used to crack, again favoring the opportunity hypothesis.

Patricia Izar: 19:45

Now turning to other findings, our research also contributed to the study of two cognition in primates in general. In 2004, when Dorie and Elisa, and also Linda Fedigand, published the complete Kapuchin, a book that summarized everything we knew about the Cebini, the state of the art on two use at that time by Kapuchin monkeys was based on the laboratory studies with captive raised monkeys. The general conclusion was that two use was a chance outcome due to their manipulative and curious and very active behavior. But there was no evidence that the monkeys perceived what was important in materials and actions to achieve this success, and I quote them in the book. They said, from the representational perspective, Kapuchins do not appear to understand why and how certain familiar conditions, such as a hole in the surface, influence the way an object moves across a surface. This affirmation was already challenged by our first studies based on naturalistic observation that strongly suggested Kapuchins were selecting particular stones to use as tools.

Patricia Izar: 21:23

Using survey techniques, we analyzed the features of the stones the monkeys used, as the monkeys used as anvils and as hammers, and compared with random stones available in the area. We analyzed the type of the stone, the frailty, weight, surface dimensions and height above the ground. We discovered the monkeys preferred flat surfaces for anvils, including some woody anvils, as we can see here in this picture. They use much more stone anvils, but some woody anvils as well, and they preferred hard quartesite stones as hammers. We also verified that suitable anvils are relatively common in the area, but suitable Hammers are rare. These river pebbles are rare in the region.

Patricia Izar: 22:31

Indeed, again still with the naturalist observation, we observed that the monkeys transport the hammer stones over at least small distance. Let's see this little movie here. We can see this juvenile one. He grab a stone here. It's a short distance, a meter or less here, but from this data here you can see that in median, juveniles transport stones to angels in median from five meters and about males 30 meters. So we also observed this was more important that they transported heavier stones to crack open palm nuts than other foods such as cashew nuts. So these ladders because this was all based on naturalist observation these ladders to suggest they were capable of at least short term planning regarding the choice of the most adequate two. So a heavy stone for a piasava resistant nut and a small stone for a cashew nut.

Patricia Izar: 23:54

But then we went to test experimentally this idea in the field, this suggestion that we made. We took advantage of this area that you see here in these pictures. This is a natural area where there are several end view stones that the monkeys always use to crack open nuts there and we set up our field laboratory there. We call that our field laboratory now and during the time of our experiments we attract the monkeys with water and palm nuts to the region and for this experiment we removed all natural hammer stones from the area and provided the monkeys with nuts and two or three stones, depending on the experimental condition that we offered.

Patricia Izar: 24:50

We offered natural stones and some artificial stones that we built with the collaboration of a colleague from the geology department in the University of Sao Paulo. So we built these artificial stones that could be large but empty, and so they would be light and small, very dense ones that would be heavy, so different from the natural stones, in which size and weight are correlated the larger the hammer stone, the heavier it is in natural stones. So we gave them natural stones, so ascent stones that cracks easily where they beat the stones and the seed stones that usually they use as hammers. And we provided with small and large natural stones. And then we started with the conflicting conditions showing them, giving them the small heavy stones and the large light stones. We can see here from this graph that in all conditions, with the natural stones and the artificial stones, the monkeys chose significantly, chose the functional stone significantly above expected, by chance, as their first choice. It was extremely interesting that when we first set up the experiment and they went straight to the large with the artificial stones, then they went to the large stone first and they grabbed to leave the stone, expect that stone to be heavy and then it was light. So they lost their balance at the first and they were like something strong and then they went and tapped that stone and they went to the small one and tapped. So after the first trial, that was, they were deceived by our artificial condition. They went to the first choice in all other experiments. So we concluded this is evidence that the monkeys perceive the affordance of the stone that make it inefficient too. In addition, we have shown through kinematic analysis, using videos of nut cracking, that the monkeys also adjust their body movement according to the task demand. This was the PhD of Madhu Mangalam.

Patricia Izar: 27:52

We show that they crack the less resistant to cune nut. I was talking about the Orbignia, the Piazava nut, the Catulé. These are very resistant nuts To cune. It's the genus astrocarium. It's a small, rounded, much less resistant kind of soft palm nut and not exactly soft but because they have to crack, but much less resistant. And so they cracked this less resistant nut by striking a light stone repeatedly with moderate force, that is, by not exceeding a threshold. We can see here the black bars the amplitude of the strike for the to cune nut and the gray bars are for the Piazava nut. So the amplitude is much higher for the Piazava. So they not exceed the threshold for the to cune and they modulate the kinematic parameters of each strike on the basis of the condition of the nut, that is, the development of the fracture following the preceding strike. So when they first hear they perceive that the nut was first fractured. They use less amplitude when cracking at a cone. In contrast, they crack at the more resistant Piazava nut by striking a headstone with the maximum force that they could generate, without modulating the kinematic parameters of their strikes, until the nut cracked. So it's like they perceive the differences of the nuts and that they adjust their body movements to in accordance. So, in summary of what I said up to now, our studies have shown that Kaputin monkeys perceive the affordances of their materials used as tools, of the nuts they will crack open and of their body actions, and that they make at least short term planning to achieve success with minimum cost. This body of evidence shows that these wild monkeys are cognitively different from the captive raised monkeys that I mentioned before, that were the object of that affirmation in 2004 in the complete Kaputin. We suggest that these differences are the result of their development, of the development of these wild monkeys within the tradition of two use.

Patricia Izar: 30:48

So I'll show you that using stone hammers in Boa Vista is a challenging task. Hammer stones weigh on average almost 1.2 kilos, which is the weight see here. I'm not talking about this work, but we, we waited these monkeys for 13 years, from a very end. So we have their weight during their development, since they they are very time. Here we show in red the females, in blue the males, and we can see that a stone of 1.2 kilos see here is a three years old females. She's already an almost an adult female. So a stone like that is the weight of an adult females. Some stones weigh twice a female that a male can can hold a fork, even a female. We saw one female lifting a four kilos stones once.

Patricia Izar: 31:54

So it's a very demanding task, it's hard and it takes images. Here we show that more or less this is proficiency in, in that cracking, and here is the age in months. So it's more or less with five, six years that they are reaching proficiency, finally reaching proficiency in this test. So the images we see here homeo is not cracking, trying to not back trying. So the images like homeo, they must master how to hold the hammer stone, how to position the net. But ultimately what we show is that proficiency is best explained by the decrease of these random behaviors that you see the here he's doing the right behavior, but then he starts to tap the, to be the, the, the nerds on the stone, and he turns. And we age and they decrease more and more these silly behaviors and and and this is related to to the increase in proficiency it's like they become more focused in what is really important for success. So this is achieved by individual practice with the material, the stunts and the nuts over the years. So is this individual learning? So how the development of tooling skills in immature capuchins is directly and indirectly affected by the actions of others, in other words, is socially mediated.

Patricia Izar: 33:53

These are the results of two and a half years study following 15 individuals younger than six years old by a team of four researchers in two pairs one observer registered registering the behavior of the focal immature and the other registering the neighbors, the activity of neighbors within 10 meters radius. This is the PhD of your not as hard. This method allowed us to analyze the focal monkeys behavior with nuts and stones and its presence near and use in relation to the start, continuation and end of cracking by other members of the group. We have shown that. I will show the little movies as just to illustrate on what I'm showing in the graphs.

Patricia Izar: 34:49

We have shown that the images manipulate nuts and debris, the debris, the debris, more often when they can see and hear others, other members of the group, nuts cracking. See here these gray bars show when there's nuts cracking activity in the group. So they manipulated more of these nuts and debris when there is activity in the group. And it's the opposite with other objects they manipulate less when there is activity of nuts cracking in the group. Then we also show that they manipulate. This is Homeo. Again, they manipulate nuts and debris more often when they are near an anvil here, more when they are near an anvil than when they are away. Again, it's the opposite with other objects, even in the absence of others. So the artifacts also affect their practice. And finally, we have also shown that the images stay near an anvil more often when there is activity on. Others are nuts cracking than when there is no nuts cracking activity. We can see here even near. In fact I will show later that they are nuts. The adults are not super tolerant of the others when they are nut cracking, but see how close Aserola is of her mother, amore is of her mother here, and so they stay near, more near the anvil when there is practice.

Patricia Izar: 36:46

So, in conclusion, both the actual observation of the activity of others and the artifacts of this activity the nut leftovers and stones facilitate the practice of percussing nuts and stones from a very early age. In Fazena, boavista, artifacts left behind when cracking nuts facilitated the practice by images, and adults cracking at those sites draw their attention to these artifacts. Recently we have shown that the older the monkeys get, what I'm showing here is the reuse of stones previously used by a conspecific, and they have shown that these reuse also increases with age. The older the monkeys get, the more they reuse the stones previously used by a conspecific. So we suggest that for the putings, the stones acquire their two value with the practice. This was the PhD of Andres Ballestados Adia and I want to show you this move of a very young one, olivia. She just throw the function of a stone. She's very young, so an adult use that stone. And then she goes there and she throw that one and she starts to play with the nuts and in a while she will play with the sandstone. See, grab the sandstones and start to play, and soon others will come here and do the same. So when they are older then they will start to reuse the functional stone.

Patricia Izar: 38:40

Finally, we show that the tradition of nut cracking with stones in Fazenda, boavista affects learning processes by influencing memory and attention of younger monkeys. When others we see here in this red bar the first red bar when others start to crack nuts, the youngsters immediately start to manipulate and percuss nuts. But, what is important, they sustain this behavior for longer after the nut cracking ends. Here we can see one minute after two minutes, three minutes, even eight minutes after the end of this activity, there is still one or other immature manipulating nuts and stones, and this is significantly different from other foods that they manipulate. So social influence on learning affects not only what's learned but the learning process itself. Just a little movie Over here is Giatobá, a former dominant male who just cracked eight already.

Patricia Izar: 39:56

Now he's leaving and present, present at that time a young juvenile. He's now a grown up already. He tries to manipulate some other young crime and he tries to percuss the nut Again. There's no activity anymore. See, no sound of nut cracking, just others crying. And he stays there. Now, now, really.

Patricia Izar: 40:50

So nut cracking has other consequences on the life of these kapuchin monkeys. It enhances competition for food sources, what is evident by the decreased tolerance of dominant female starboard subordinates in two sites. Here I'm showing this association index between pairs of individuals, of females of different hanking or high high hanking, high, middle hanking, the different diets and in fruit trees, in palm trees and in the two sites. And we can see here for both studied group, the unprovision and the provision, the association index between females is significantly lower in two sites compared to the other food sites, even a zappable food sites that the individuals can monopolize, and this is related also to an increased contest competition. We see more direct, not actual aggression but formal, but we see direct competition in two sites, much more than it would be expected by the time they spend there. And this is probably related to the rigid, linear female dominance hierarchy, very stable over the years, that we observed in Fazenda Boavista and what is very different from what we observed in the other my other study populations in Atlantic Forest where dominance relations between females are almost absent, they are almost egalitarian. So they are loose dominance relations in these populations that do not use too. So we suggest that to use increased linearity of the dominance hierarchy so affects the social structure of the group and in fact we found a similar effect of decreased spatial association when comparing the spatial association of the entire group, not only females, including the males of all ages. We use the same database of two and a half years we compiled for the study of Yonet on the development of two youths that we had the data on the identity of imaturs and we were in the neighbors and we were able to build the association networks. Considering the activity nut cracking are others and location on the end view or outside the end views we build the association networks and we saw that the association networks during nut cracking on the end views were less dense and more modular than during other activities in other locations. So if this is such a difficult food source to obtain, that increases the possibility of getting a grass it's hard to acquire why the monkeys are so attracted to it.

Patricia Izar: 44:10

We have just shown that the kernel of palm nuts obtained with the aid of tools significantly increases the diet quality of caputin monkeys in Fazenda, boa Fista. This was published last year using a nutritional ecology study based on daily focal follows of individual monkeys. That was the PhD of my student, lucas Peternelli dos Santos. We compared days when the monkeys used tools to crack open palm nuts versus days when they did not use tools. On days when they crack open palm nuts with tools, they acquired higher levels of fat, carbohydrate and energy, lower levels of, I would say, non-digestible fibers. When they use tools, then when they do not use tools and these fibers decrease the absorption of nutrients. And they also acquired a more balanced diet in terms of the ratio between the non-protein energy intake and protein ingested on days when they used tools versus the days when they did not use tools. So two use did not increase the amount of food, not increased diet quantity, but increased their diet quality.

Patricia Izar: 45:57

So, in summary, what we learned from these wild caputin monkeys from Fazenda Boa Fista is that two use is a tradition that emerges in populations that rely on stractive foraging, coupled with ecological contexts that favor manipulation and practice with two materials. This is a skill acquired through a long process of practice that is stimulated by the activity of skilled conspecific and by the artifacts of this activity. Two use has important consequences for the life of these caputins. It contributes substantially to improve their diet and, as such a rich source, it increases within group competition for food, affecting patterns of society. Finally, I think our findings may illuminate causes and consequences of two use in ancestral hominins.

Patricia Izar: 47:09

For a long time, two use and two making were considered a feature of the genus Homo and it has been linked to brain growth and its social and life history correlates and the increase in meat eating. We now have sufficient evidence of two use in hominins much prior to the genus Homo and perhaps even two making, as we can see in this just published paper. In science they are showing these two sites in Kenya of the genus Paranthropus and these sites are dated almost three million years ago. So this is really really a node to use, and perhaps even two making that they were using to extract bone marrow. So to understand the evolution of these two use as a feeding adaptation that predates the appearance of the genus Homo.

Patricia Izar: 48:22

Of course it's important to study the living apes, as Mike did with the chimpanzees in Tanzania as a case of common ancestry, but it's also important to study the more distant robust kaputin monkeys that offer a possibility to study a convergence. The appearance of two using distant clades allow us to search for factors associated to this feature. For example, our results on the nutritional significance of tools for kaputins suggests using natural stone tools in feeding may have improved the diet quality of hominins much prior to the appearance of Homo and maybe also of this may be associated to this cascade of related social consequences that are now attributed to the genus Homo. So I think this is an important, an additional importance contribution of our study. And with that I end my talk. I would like to thank you again a lot, a lot, for this invitation to be here. I thank all the funding agencies that made this long-term study possible, the permits and all the students, as I said, the laboratory, and if you have other questions after today, you can contact me here. Thank you very much.