140 Monkey Faces: Testing how monkeys think about their social world

This entry was originally published on the Yale MacMillan Center’s website. You can view that post here.

A collage of some of the faces I had to memorize to complete data collection. When placed next to each other, individual facial differences (freckles, scars, face shape) begin to emerge. Photo credit: Alyssa M Arre.

Do you think you could recognize 140 of your closest friends? What about 140 strangers? This was the challenge I faced when I began my summer research at the Trentham Monkey Forest, in Stoke-on-Trent, England thanks to a generous Pre-Dissertation Fellowship from the MacMillan Center. Trentham Monkey Forest is a park that’s home to 140 Barbary macaques. Before, I was able to begin my data collection, I had to learn the face of every monkey resident.

During the six-week data collection trip, my goal was to test how monkeys think about their social world. While this type of research, called ‘comparative cognition’ can help inform our understanding about how animals navigate all sorts of situations, it can also improve our understanding of human cognition. Specifically, studying primates can help us make inferences how human cognition evolved. It is impossible to go back and time and see what our last common ancestor could think about, by studying some of our closest living relatives, we can infer what sorts of evolutionary pressures might be required in order for certain cognitive abilities to emerge.

My specific project investigated what Barbary monkeys know about what others can see. As humans, we are able to track other people’s perspectives and even take into consideration what someone might know about someone else’s perspective. We know what others see, know, and feel, and are pretty good at making predictions about how other people will act based on this information. This ability is what psychologists refer to as ‘theory of mind’ and was long believed to be human unique.

A juvenile Barbary macaque watches me from the tree. Photo credit: Alyssa M Arre.

How do you ask a monkey what it knows about what someone else knows? For nonverbal subjects like animals, and also nonhuman infants, we use a measure known as looking-time, or the amount of time the subject looks at the experimental setup. Traditionally, we use this measure to evaluate the subject monkey’s surprise. Like humans, monkeys look much longer when they are surprised at the outcome of a situation. We can compare looking time between different conditions to determine whether monkeys are surprised in the same way as humans. This method has been used in a variety of nonverbal populations, including human infants, as well as a variety of primate and other nonhuman animal species. In my task in particular, I was wondering whether monkeys could make the same predictions as humans about how other people should act based on their visual perspective.

An image of me showing a monkey my cognitive experiment. Photo credit: Dr. Francesca De Petrillo.

In short, for my research I show monkeys magic tricks. At Trentham Monkey Forest, I walked around the park looking for calmly-sitting monkeys that we could test on our experiment. Once located, we approached the monkey and sat about a meter away. The test required two experimenters: one person who presented the experiment, and a second who filmed the monkey’s reaction. Later, someone blind to the experimental hypothesis and the conditions of each video watches the videos back and records when the monkey is attending to the apparatus.

To date, much of the comparative cognitive research has been carried out on only a few select species. Barbary macaques are relatively understudied compared to some of their closest primate relatives, such as the Rhesus macaque. Barbary macaques are genetically very close to Rhesus macaques, but are near opposite in their social behavior. While Barbary macaques are tolerant and friendly, the Rhesus macaque is notorious for being one of the more aggressive and despotic primates. By studying development in both species, we can begin to tease apart how a species’ ecology shapes their cognition. I hope to pursue this type of research for the duration of my graduate career.

A family of Barbary macaques engages in a group grooming session. Photo credit: Alyssa M Arre.

This summer was an incredible learning experience. I am so grateful for the generosity of the MacMillan Center for the Pre-Dissertation Fellowship funding that I received that allowed me to pursue this project, the staff at the Trentham Monkey Forest for allowing me to collect data there, and my two advisers and mentors on this project, Dr. Laurie Santos and Dr. Alexandra Rosati. While we are still working on analyzing the data, perhaps my biggest success was that in time, and much to my own surprise, I learned all 140 monkey faces.

Written by Alyssa Arre, a Class of 2022 graduate student. If you want to keep up with the rest of her research, or are interested in comparative cognition and her field work more generally, you can follow along with her blog, Dispatches from the Field (campuspress-test.yale.edu/alyssaarre), or visit her website at alyssaarre.com.

Day 37: Data collection complete!

My final subject! An adult male Barbary macaque. Photo credit: Alyssa M. Arre

Today was a great day. After a few weeks of data collection, I finally finished data collection for my project. For a while, I was worried I would run out of time. Around the end of May, I was having a lot of trouble finding novel subjects who had not seen the experiment already, and was repeatedly testing the same monkey (some as many as four times!).

This happens occasionally, especially with subadults without any significant markings. Presently, we have to exclude a monkey who has already seen the entirety of the test one time, so that our final dataset(s) only include each monkey a single time. This makes sense — we wouldn’t want one monkey’s behavior (especially if it was abnormal) to characterize the results of the entire study. Even though it is commonplace, it is incredibly frustrating because in addition to not being able to count the data, you also feel like an idiot (!) for not recognizing a monkey that you’ve already successfully tested.

In any case, a complete dataset means that the next phase of data analysis begins — coding! While ‘coding’ typically means writing hours of code into some program, coding for a comparative psychologist may mean that, or mean ‘behavioral coding’, during which we go back and watch all of the videos we collected during data collection. Let me explain.

During data collection, we filmed 80 videos, one for every successful subject. Each subject saw three trials to complete a session. The next step in my data collection is to go through these videos and clip each by trial into three separate 10-second clips. I then randomly rename the clips so that they are anonymized. This is an important step to ensure that when we go back and watch videos, we are not injecting any subconscious bias based on how we want the experiment to work out.

Then, two people go back and rewatch all of the anonymized clips and record when they think the subject is attending to the experiment. Formally, this is called the ‘looking time method’ [for a *great* review, see Reference 1], and can be used to measure either the subject’s surprise or the subject’s preference for the stimuli (depending on the experiment and your initial pre-experiment predictions). The two people have to reach an agreement on when the monkey is attending at more than 90% (this varies slightly by subject and by experiment) of the video. We call this the ‘reliability’ between the two videos, and calculate the number by calculating the correlation coefficient between the two individual sets of coding.

Finally, after all of this is completed, we are able to look at whether the trends we predicted are significantly visible in the data. In my experiment, I used the looking time method to measure the subjects’ surprise, so I will be looking at whether my subjects were more surprised in the unexpected condition as compared to the subjects in the expected condition. I’ll check back in when I know the results of the study, but as you can see here, it will probably take some time!

REFERENCES

[1] Winters, S., Dubuc, C., & Higham, J. P. (2015). Perspectives: The looking time experimental paradigm in studies of animal visual perception and cognition. Ethology, 121(7), 625-640.

Day 30: Baby Barbary Macaques

Three baby macaques of three different species. From left to right: A barbary macaque (via Trentham Monkey Forest), a rhesus macaque (Getty Images), and a black crested macaque (ZooBorns).

New babies are an exciting addition to any primate social group, but baby Barbary macaques serve an extra function in primate social groups as a source of currency.

I know what you might be thinking — how could a living individual serve an inanimate function? While traditionally we think of currency as a token or other inanimate object with which we assign value and use in transactions of goods and services, baby Barbary macaques can serve the same function in social “transactions”.

Most notably, baby Barbary macaques are used by male Barbary macaques to de-escalate otherwise aggressive or antagonistic interactions [1]. In moments that are particularly tense, a male Barbary macaque often reaches out and grabs a nearby baby to hold, and sometimes offer, to the aggressive social partner.

A male Barbary macaque exhibits a fear expression at another individual (blurred in the foreground) while carrying a yearling Barbary baby. Photo credit: Alyssa M. Arre

The majority of these social interactions play out like the photograph above. In addition to infant carrying, the submissive Barbary macaque will also make a facial expression called a ‘fear grimace’ that lets the other individual know [s]he (the ‘fear-grimacer’) is not a threat. Barbary macaques have a whole suite of facial expressions to communicate their emotional states to other individuals. In these interactions, the most common among them are the fear-grimace (as illustrated above) and the lip-smack, which is an affiliative gesture meant to reconcile post-conflict interactions.

As compared to other primate species, male Barbary macaques in general spend considerably more time interacting with babies than males in most other Old World primate species. For decades, theorists have argued over two theories explaining why this may be: the agonistic buffering hypothesis, and the male care hypothesis.

The ‘agonistic buffering hypothesis’ is more in line with the social interactions described at the beginning of this post. In other words, males spend a lot of time with baby Barbary macaques to help facilitate social interactions. Imagine: things between you and another monkey getting tense? Grab the nearest baby. Everyone loves babies!

But other primatologists believe this is not the case. A few years later, Taub argued that the males were assisting in infant care, thus, the ‘male care hypothesis’. From his time in the field, he observed that males prioritized spending time with some infants over others, and believed that this was likely due to kinship. In other words, male Barbary macaques are invested in the well-being of their offspring. As handling of the offspring increases their likelihood of survival and social success, male Barbary macaques are just investing in the succession of their own genes.

A male Barbary macaque holds a juvenile. Alyssa M. Arre

This latter hypothesis is intuitive and would be fine, except that this is often not the case. More recent studies conducted on Barbary macaques have demonstrated that males do not often claim paternity of the infants they handle [4, 5]. Instead, by handling babies, Barbary macaques win social favor with female Barbary macaques, securing a higher-likelihood for future mating opportunities [5]. This care-then-mate strategy is counterintuitive to the mate-then-care strategy employed by other species, where both parents contribute to offspring care. Some have characterized the explanation of this behavior as the ‘mating effort hypothesis’ [6], though it has received less support than the aforementioned two hypotheses for infant handling in male Barbary macaques.

It is important to note that the ultimate, albeit subconscious, goal of each male Barbary macaque is to pass on his genes. Each hypothesis described above explains what benefits the male might accrue by forming strong dyadic bonds with infants within the group. While it is *highly* unlikely that each male Barbary macaque is taking into consideration the many fitness benefits this relationship may afford him, it is easy for us to think about the different ways that each hypothesis illustrates fitness benefits the male is granted by spending time on these interactions.

Hopefully you enjoyed this post on baby barbary macaques. Critiques and comments are extremely useful and help me grow as a science writer, so please feel free to send along any thoughts you might have. Thanks for following along!

 

REFERENCES

[1] Deag, J. M., & Crook, J. H. (1971). Social behaviour and ‘agonistic buffering’ in the wild Barbary macaque Macaca sylvana L. Folia Primatologica, 15(3-4): 183-200.

[2] Van Schaik, C. P., & Paul, A. (1996). Male care in primates: does it ever reflect paternity?. Evolutionary Anthropology: Issues, News, and Reviews: 5(5): 152-156.

[3] Taub, D. M. (1980). Testing the ‘agonistic buffering’hypothesis. Behavioral Ecology and Sociobiology, 6(3): 187-197.

[4] Kuester, J., & Paul, A. (1986). Male‐infant relationships in semifree‐ranging Barbary macaques (Macaca sylvanus) of affenberg salem/FRG: Testing the “male care” hypothesis. American Journal of Primatology, 10(4): 315-327.

[5] Ménard, N., von Segesser, F., Scheffrahn, W., Pastorini, J., Vallet, D., Gaci, B., … & Gautier-Hion, A. (2001). Is male–infant caretaking related to paternity and/or mating activities in wild Barbary macaques (Macaca sylvanus)?. Comptes Rendus de l’Académie des Sciences-Series III-Sciences de la Vie, 324(7): 601-610.

[6] Paul, A., Kuester, J., & Arnemann, J. (1996). The sociobiology of male–infant interactions in Barbary macaques, Macaca sylvanus. Animal Behaviour, 51(1): 155-170.

 

 

 

 

Day 28: A new baby!

When we arrived at the monkey forest today, we were greeted with the most exciting news:

A newborn Barbary macaque at Trentham Monkey Forest. Photo credit: Alyssa M. Arre

A baby Barbary macaque!  We spent a bit of time watching the others follow mom and her new baby around before we headed off to start the long day of data collection.

I hope to write more on why babies are so important in Barbary macaques soon (edit: I have now done so here), but for now, I just have time for this quick note. Check back soon for more on Barbary socioecology!

 

Day 18: Half way there!

My fortieth subject, a beautiful adult male Barbary macaque. Photo credit: Alyssa M. Arre

Today, I successfully collected data on my fortieth subject, which means I am halfway done with my data collection for my current project! I am happy to report that everything is going well so far. Additionally, I have been getting better at figuring out who my subjects are without the help of the staff.

Over the next few weeks, in addition to data collection for my own project, I also hope to focus more on getting photos of some of the babies and juveniles born since the lab’s last trip. The appearance and facial freckle pattern of the adults does not drastically change from year to year. However, in their first four years of life, the babies change drastically! Here is an example of the same monkey, three years apart:

As we hope to continue returning to the Trentham Monkey Forest, maintaining an accurate ‘Monkey Facebook’ can help our team during future data collection trips. In any case, I am looking forward to the next half of my trip and the remainder of my data collection! Thanks again for following along.

 

Day 14: Happy Birthday Francesca!

Views from the hike on “The Roaches” path in the Peak District, Staffordshire, England.

Today, we took the day off in celebration of Francesca’s birthday (and also because we had worked several 8-12hr workdays in a row and all needed a nice break).

While the day was full of all the typical birthday things (e.g. presents, candles, and ice cream cake), we also decided to check out a nearby national park known as the Peak District National Park.

We completed a trail to a geological formation known as ‘The Roaches’, The ridge looks over Leek, England. We learned the name refers not to the insect, but to the French word for rocks (les roches). Though a short hike (only 505m), the top provided a beautiful lookout over Leek and the surrounding farms.

More views from between “The Roaches” rock formations. Peak District, Staffordshire, England.

We had a great afternoon taking in the countryside, but we are all looking forward to getting back to data collection tomorrow!

Day 9: What exactly are you doing?

Rosie & I testing a male Barbary macaque on my study in May 2018. Photo credit: Dr. Alexandra G. Rosati.

Many times, I’ve been asked by family and friends what exactly it is that I do when I am working with the monkeys. Generally, I respond that I show the monkeys something and then see how they respond. While this is technically true, it is not very specific.

While my research falls into a lot of different categories (developmental psychology, comparative cognition, social cognition, etc.), put simply, I am really interested in what monkeys know about what others know or can see. This ability is called ‘theory of mind’, and it refers to the way that we are able to think about other people’s perceptions, emotional states, beliefs, knowledge (or ignorance), desires, and perspectives [1]. Humans do this every day, all the time. We can think about what other people are thinking when we are talking with them and when we are talking about them, when we are thinking about them, looking at them, etc. If you are chatting with someone and then suddenly they begin to frown, you might infer that something you said made them sad. Similarly, if you are talking with someone and suddenly their gaze shifts to something behind you, you will likely turn around (an aside: this latter ability is called ‘gaze following’ and is so cool that I hope to cover it separately at some point, more on gaze following later..)

Anyways, after decades of work by my adviser and some of her past students, we generally believe that rhesus monkeys, while able to do visual [2] and auditory [3] perspective taking, are not doing ‘theory of mind’ the same way that humans are (the details of this are complicated, but if you are interested, see [4]). Put simply, it does not seem like rhesus macaques can represent events that differ from the current state of the world. A quick example might make this more clear.

Imagine that you are sitting in a room with two of your family members — your mom and sibling. Your mom is cleaning, and your sibling is reading a book, but then gets up to grab something from the other room and leaves the book on the coffee table. While they are gone, you mom accidentally puts the book back on the shelf. When your sibling comes back, where do you think they would look for the book?

For us, this should be easy to figure out: your sibling left the book on the coffee table, so they should look for the book on the table because they didn’t know that your mom moved the book to the shelf since they were out of the room. Even a more simplified version of this task is not so simple for a monkey. In an experiment from 2011, they failed to form expectations about where the person should look for the hidden object [5].

However, as aforementioned, rhesus macaques do seem capable of using another person’s visual perspective. Further, they can use this visual perspective to form an expectation about where the person should search for an object [5]. Because recent studies in different species of macaques show differences in their social cognition [6], I am interested in whether Barbary macaques will form expectations about how a person should act (like rhesus macaques), or will show a different pattern of behavior.

To do this, I sit about a meter away from the Barbary macaques (see the first picture above) and show them a series of actions on a stage. A second person sits directly behind me and films a close-up video of the monkey’s face.

Later, we remove all of the information relevant to the study, and have someone who is blind to the study hypothesis watch all the videos back and code when they think the monkey is looking at the experimental setup. Finally, we compare average looking in the different experimental conditions to see whether or not Barbary macaques generally expect people to act consistently with their visual perspectives.

I will keep you updated with the results with the study as soon as I know, but this can sometimes take months! Let me know in the comments (or contact me directly) if you have any other questions or want to know more about anything I wrote about here. Thanks for following along so far and I hope to update you again soon.

 

REFERENCES

[1] Frith, C., & Frith, U. (2005). Theory of mind. Current Biology15(17), R644-R645.

[2] Flombaum, J. I., & Santos, L. R. (2005). Rhesus monkeys attribute perceptions to others. Current Biology, 15(5), 447-452.

[3] Santos, L. R., Nissen, A. G., & Ferrugia, J. A. (2006). Rhesus monkeys, Macaca mulatta, know what others can and cannot hear. Animal Behaviour, 71(5), 1175-1181.

[4] Martin, A., & Santos, L. R. (2016). What cognitive representations support primate theory of mind?. Trends in Cognitive Sciences20(5), 375-382.

[5] Marticorena, D. C., Ruiz, A. M., Mukerji, C., Goddu, A., & Santos, L. R. (2011). Monkeys represent others’ knowledge but not their beliefs. Developmental Science, 14(6), 1406-1416.

[6] Rosati, A. G., & Santos, L. R. (2017). Tolerant Barbary macaques maintain juvenile levels of social attention in old age, but despotic rhesus macaques do not. Animal Behaviour, 130, 199-207.

Day 7: One hundred and forty monkey faces

A family of Barbary macaques grooming.
A family of Barbary macaques grooming one another. Photo credit: Alyssa M. Arre.

Today, I finished my first week collecting data at the Trentham Monkey Forest. I am hoping to make another post later about the town we are living in (Kingsley, Stoke-on-Trent, England), on the monkey park (Trentham Monkey Forest) that we are working in, and the species that we are working with (Barbary macaque), but for now, a quick recap on the last week!

We arrived at the park first thing on Monday (7 May 2018) morning to meet with the director of the park. He was super friendly and helpful. We went over the rules of the park, met with some of the staff, and then finally headed through the front gate to meet the monkeys first hand!

As I mentioned in an earlier post, Trentham Monkey Forest is home to 140 Barbary macaques. Unlike some of the other field sites that I have worked at in the past, these monkeys do not have easily visible tattoo IDs. This means that we have to learn all of the monkeys by sight — no easy task!

How do we tell all the monkeys apart? There are a few tricks that help us distinguish one monkey from another.

First, Barbary macaques live in large social groups, and they typically stay in these groups for their entire lives. Because the monkeys at Trentham Monkey Forest are allowed to live freely like they would in the wild, they too live in two large social groups. For us, the first step is generally to figure out what social group we are working in, so that we can narrow down the list of possible monkeys.

Next, we identify the sex of the monkey. Though the monkeys only exhibit very subtle sex differences after they go through sexual maturity (around 5/6 years old for females and 7/8 years old for males). I was really terrible at this when I first arrived, but got better over the week. Males are generally larger than females, have a larger build, and more pronounced canine teeth [1].

(A quick aside: It is pretty rare that we get a glimpse of the teeth as the monkeys only show them when they yawn. Monkeys will yawn when they are trying to warn another individual to stay away [2], so we have luckily not had any of those directed at us.)

Last but not least, adult female Barbary macaques have sex skin swellings which show individual differences: the swellings manifest as large, cushion-looking pads of skin on their butt [3]. They can be pink or deep blue/purple (or some combination of the two colors), and have different patterns and scars. While these help us distinguishing female versus male adults, they are not as pronounced in young Barbary macaques.

Once we know the group and the sex of the individual, we start to flip through our monkey ‘Facebook’. Every day we carry around tablets that have a folder of close-up monkey faces (like the images I shared above), and compare the monkeys sitting in front of us to the monkey face images that we have where we verified the individual identity with a staff member or the professor that we are working with. The monkeys have different patterns of freckles, moles, and scars on their faces, different nose and general face shapes, and different face and surround hair coloration patterns. To my surprise, with some practice, we have become pretty good at distinguishing one monkey from another. Each day is a little easier than the last!

Alright, well it is time for me to get back to working on the monkey Facebook. Check in again next week for more on the Barbary macaque and where I am living for the summer. Thanks for following along so far.

 

REFERENCES

[1] Paul, A., Kuester, J., Timme, A., & Arnemann, J. (1993). The association between rank, mating effort, and reproductive success in male Barbary macaques (Macaca sylvanus). Primates, 34(4), 491-502.

[2] Deputte, B. L. (1994). Ethological study of yawning in primates. I. Quantitative analysis and study of causation in two species of Old World monkeys (Cercocebus albigena and Macaca fascicularis). Ethology, 98(3‐4), 221-245.

[3] Nunn, C. L. (1999). The evolution of exaggerated sexual swellings in primates and the graded-signal hypothesis. Animal Behaviour, 58(2), 229-246.

Day 0: The summer of monkeys

Today marks the beginning of what will be a 13-week summer of monkeys. My itinerary over the coming months includes a long trip to the United Kingdom, followed by some time in my favorite place in the entire world, and wraps up with a week in San Antonio, Texas. Let me explain.

MAY & JUNE

Later this evening, I will debark on a flight to Heathrow International Airport, followed by a short train ride to Trentham, U.K. There, I will be conducting social cognitive research at the Trentham Monkey Forest, home to 140 Barbary macaques (Macaca sylvanus). Native to the Algerian Mountains, Barbary macaques are unique for a few reasons. First, they are the only macaque species known to reside outside of Asia. Similar to the other macaques, they are highly skilled at adapting to just about anywhere and can survive in a range of ecosystems including forests, grasslands, and of course, the mountainous regions of Algeria & Morocco. In addition, Barbary macaques engage in alloparenting, or cooperative care of the offspring by nondirect relatives [1].  Father macaques also help in caring for their own offspring. This is highly unusual among primates, and especially among macaques. Finally, the Barbary macaques are believed to be more tolerant than the species I typically study [2], the rhesus macaque (more on them below!).  As such, the Barbary macaques provide a really neat study species for us to look at in comparison to other more despotic species to see how sociality influences cognition.

JULY

sunset on a beach in puerto rico
Sunset at la Playa Punta Santiago, Puerto Rico. Photo credit: Alyssa M. Arre.

Following my extended stay in the United Kingdom, I will head to Punta Santiago, Puerto Rico. Punta Santiago, Puerto Rico is a small fishing village on the east coast of Puerto Rico. Of the last four years, I’ve lived in Punta Santiago collectively for about a year and a half and have come to deeply love the community there. Needless to say, I am really looking forward to going back.

Right off the coast is a small island called Cayo Santiago, and home to the Cayo Santiago Biological Field Station. There are over 1,200 rhesus macaques (Macaca mulatta) on the island, diverse in age, sex, and social status, giving us the unique opportunity to study social cognition in a free-living primate under naturalistic conditions. As aforementioned, rhesus macaques are despotic — they exhibit a strict linear dominance hierarchy where there is an alpha male and then a number of males that each rank a little bit lower than the last. Compared to many of the other macaques, and especially the Barbary macaques, they are aggressive and exhibit relatively low rates of reconciliatory behaviors [3]. Rhesus macaques are well studied — to date, we know a lot about their social cognition thanks to the work of the Comparative Cognition Lab at Yale and a number of other labs around the world that travel to Puerto Rico to study these monkeys [4]. More on the field site, Punta Santiago, my research, and Puerto Rico more generally later, but you will have to follow along for those updates!

AUGUST

My final destination for the summer is San Antonio, Texas, where I will be attending the 41st Meeting of the American Society for Primatologists. I’ve never been to Texas before, so I’m pretty excited to visit and I’m hoping I’ll have at least a little time to explore. If you have any recommendations for a day trip or dinner, please let me know!

Alright, well, I have a bit of writing to get to, but I hope that this provides some insight into my crazy life, and some relief to my friends and family who keep asking me to explain where I will be all summer. I’ll try to update this blog regularly with some details about my travel and information about my research. Stay tuned for more photos!

REFERENCES

[1] Small, M. F. (1990). Alloparental behaviour in Barbary macaques, Macaca sylvanus. Animal Behaviour39(2), 297-306.

[2] Thierry, B. (2007). Unity in diversity: lessons from macaque societies. Evolutionary Anthropology: Issues, News, and Reviews16(6), 224-238.

[3] Waal, F., & Ren, R. (1988). Comparison of the reconciliation behavior of stumptail and rhesus macaques. Ethology78(2), 129-142.

[4] Drayton, L. A., & Santos, L. R. (2016). A decade of theory of mind research on Cayo Santiago: insights into rhesus macaque social cognition. American journal of primatology78(1), 106-116.