I study a group of free-ranging long-tailed macaques (Macaca fascicularis) in Wat Khao Tamon, a Buddhist temple in the south of Thailand. I primarily focus on their social behavior, and my current project looks at relationships between their social behavior and the likelihood of contracting a tuberculosis infection.

Tuberculosis is a deadly airborne respiratory disease for humans and many other primates, especially macaques in several primate centers [1]. Thus, before entering the primate centers, you need a negative TB result to make sure that you will not spread TB to monkeys. However, many other macaques live in proximity and have frequent interaction with humans, are those macaques also prone to TB?

Research has shown an increase in TB infections among macaques in areas of frequent human contact, but the individual differences in contracting TB remains unknown [2]. Are macaques with frequent interactions with humans more likely to have TB? Alternatively, are macaques with frequent interactions with conspecifics more prone to TB infection?

Very few empirical studies have tried to understand the relationship between social behavior and contracting respiratory infections because 1) we need to get data from each monkey, and identifying wild macaques requires significant time and effort (as a result, this usually happens at a long-term field site) and 2) disease diagnosis requires biological samples that are hard to collect in wild macaques, often time we need to sedate them, and invasive biological collection can inadvertently change their behaviors.

My collaborators (Prof. Suchinda Malaivijitnond and Sutthirote Meesawato) are improving non-invasive techniques to detect TB in wild macaques. With my skill in monkey identification and behavior collection, this collaboration makes a perfect combination to look at behavior and infection. I observe macaques’ social behavior to map connections between individuals who interact to create a network. An individual’s social network connectivity can determine the risk of exposure to infectious agents and influence disease transmission within a group.

My research team collected biological samples from fresh feces, and rope baits (which are sugar-dipped ropes that act as chew-toys) [3] to use for TB detection. Collecting fecal samples doesn’t sound too hard, but collecting fresh identifiable feces is tricky. Sometimes it depends on luck, since some monkeys are poop-shy and for six months of data collection we never saw them defecate in front of us. Thus, my team became very good at telling if a monkey is pooping!

Rope-bait collection requires less of luck. It was very hard at first when monkeys don’t understand that this worm-like object is edible, but once they know, they like it! Since we need individual samples to test if an individual monkey has TB, it is very important to avoid cross-contamination. The tricky part is to find the target monkey when they are alone so that the other monkeys cannot contaminate the rope when the target is done chewing it.

The question I got asked so many times is, how can I recognize each monkey, they look all the same! Well, they are quite different, but humans may not be familiar with them depending on their experience. Imagine you are a teacher at a private school in an unfamiliar area. Everyone has the same hairstyle (school rule), wears the same uniform, and has similar skin tone, hair, and eye color. It would be rough at first to identify individuals! What makes you know them better is when you know their name, and a story of each one, plus when you interact with them!

Back to the monkey world, naming them helps a lot in identification. Observers normally take a lot of pictures to confirm and separate each monkey in a folder and note their defining characteristics. For example, observers often use scars, hair colors or patterns, nipple color (for females), and scrotum color (for males) to help identify individual monkeys.

When I first try to identify a monkey, apart from the identifying characteristic, I always jot down what my first gut feeling is about this monkey. For example, this is Mee-pooh, he is super cute to me! His head is fluffy, his scrotum is bright red, his mouth is always slightly open, and his tail is at his knee (slightly short for a long-tail macaque). What helps me in memorizing the monkey, I said hi to Mee-pooh every time I saw him (even though they probably don’t know their names)!

In this project, I have trained three local Thai students who have very limited experience with monkeys to help me collect data. But first, they need to know each monkey confidently! The first week we just walked around, introducing my assistants to each monkey, what are their identifying characteristics, and asking my assistant what their first guts say about each monkey. I then used what they said to provide hints on individual identity as they tried to guess the name of the monkey. On a rainy day when walking around is not possible, we played a card game, where they need to match the picture of the same monkey in different postures. My assistants took around a month to confidently identify >100 monkeys from one group.

Some tips here about naming monkeys: try not to name them directly after their characteristic. For example, if you name a limping monkey “Limping”, you might get confused if you see another monkey limping. I would name them something like Lupin (similar phonetics with limping) or Moody (after Mad-eye Moody, a character with a limp from the Harry Potter book series). Also, when you don’t know them yet, don’t rely on one character to identify monkeys. Check at least three characteristics. For example, Yolo has yellowish fur, pink foot patches and a portion of the lower left ear is missing.

Once you know them, you will see that each one is very different. And that’s when the fun happens! The best moment of studying monkeys is to ‘monkey gossip’ with other data collectors. Individual variation in behavior is essential to detangle what factor in social interactions contribute to their health.

Nalina Aiempichitkijkarn is a 5th year Ph.D. student in the Animal Behavior Graduate Group at UC Davis in Dr. Brenda McCowan’s Lab. Nalina investigates how sociodemographic traits and social connectedness are correlated with tuberculosis infection in free-ranging long-tailed macaques in Thailand.

References:

[1] Mätz-Rensing, K., Hartmann, T., Wendel, G. M., Frick, J. S., Homolka, S., Richter, E., Munk, M. H., & Kaup, F. J. (2015). Outbreak of Tuberculosis in a Colony of Rhesus Monkeys (Macaca mulatta) after Possible Indirect Contact with a Human TB Patient. Journal of Comparative Pathology, 153(2–3), 81–91. https://doi.org/10.1016/j.jcpa.2015.05.006

[2] Wilbur, A. K., Engel, G. A., Rompis, A., Putra, I. G. A. A., Lee, B. P. Y. H., Aggimarangsee, N., Chalise, M., Shaw, E., Oh, G., Schillaci, M. A., & Jones-Engel, L. (2012). From the Mouths of Monkeys: Detection of Mycobacterium tuberculosis Complex DNA From Buccal Swabs of Synanthropic Macaques. American Journal of Primatology, 74(7), 676–686. https://doi.org/10.1002/ajp.22022

[3] Toyoda, A., Matsudaira, K., Maruhashi, T., Malaivijitnond, S., & Kawamoto, Y. (2020). Highly Versatile, Non-Invasive Method for Collecting Buccal DNA from Free-Ranging Non-Human Primates. BioRxiv, 2020.03.29.015073-2020.03.29.015073. https://doi.org/10.1101/2020.03.29.015073

[Edited by Josie Hubbard and Maggie Creamer]