Cláudia Sousa Memorial Fund

For the Advancement of Portuguese Primatology

Final Report 2019

Diana da Silva

Grant By

Professor Tetsuro Matsuzawa, Ph.D.

Primate Research Institute, Kyoto University

Supervisor

Professor Misato Hayashi, Ph.D.

Primate Research Institute, Kyoto University

Japan Monkey Center

Tutor

Raquel Costa,

Primate Research Institute, Kyoto University

ii

Acknowledgements

I would like to express my sincere thanks of gratitude to Professor Matsuzawa for the

creation of the Claudia Sousa Memorial Fund that has contributed so much for the

development of primatology in Portugal, and to the Japan Society for the Promotion of

Science for the financial support. I would also like to extend my gratitude to Professor

Misato Hayashi, for making all the arrangements for my stay in Japan and for making me

feel welcomed, since the first meeting in Portugal. Thanks to Professor Naruki Morimura

for the good company. A very special thank you to Raquel Costa, Morgane Allanic and

Renata Mendonça for all the guidance, patience and friendship. Also, a huge thank you

to all the amazing people that I met, that made me feel at home. At last, a thank you to

Professor Claudia Sousa that till this day continues to inspire us all.

Table of contents 1. Claudia Sousa ............................................................................................................ 1

1.1. Claudia Sousa Memorial Fund .......................................................................... 3

2. The beginning of Primatology in Japan .................................................................... 4

3. Japan Monkey Center (JMC) .................................................................................... 4

4. Primate Research Institute (PRI) ............................................................................... 5

4.1. Cognitive experiments ....................................................................................... 6

4.2. PRI and CICASP seminars ................................................................................ 7

4.3. Journal Club ....................................................................................................... 8

4.4. Interdisciplinary seminar on primatology .......................................................... 9

5. Conferences ............................................................................................................. 10

5.1. 12th International Symposium on Primatology and Wildlife Science (PWS) .. 10

5.2. NerdNite ........................................................................................................... 11

5.3. Symposium for the Support for African/Asian Great Apes (SAGA) .............. 12

6. Traveling ................................................................................................................. 12

6.1. Kumamoto Sanctuary ...................................................................................... 13

6.2. Yakushima Island ............................................................................................ 14

6.3. Kyoto ............................................................................................................... 17

7. Nesting-cup manipulation in chimpanzees and humans ......................................... 18

8. Final remarks ........................................................................................................... 22

9. References ............................................................................................................... 23

1

1. Claudia Sousa

Cláudia Sousa’s (Figure 1) work

inspired me the very first time I read

about her. What truly touched me about

her story was the fact that she was able

to pursue a career in primatology even

though she was from a small country

with limited means for such career

path. Her story gave me hope that, if I

worked hard, took risks, and was

determined on following my passions, I

too could make my own story in

primatology research. Directed by her

steps and from other Portuguese primatologists, I completed my masters in Evolution and

Human Biology at the University of Coimbra and decided to gain some field experience

right after.

Claudia Sousa’s early work began with her master’s project with chimpanzees at the

Lisbon Zoo. Afterwards, she made an important career choice when she took a long bus

trip to Paris in 1998, and met Professor Tetsuro Matsuzawa, a decision that made possible

a collaboration between Portugal and Japan that lasts until this day.

Her work in Japan began at the Primate Research Institute (PRI), one of the most

renowned centers for primatology research. Her first study at PRI started with three

chimpanzee subjects, Ai, Pendensa and Popo, with whom she tested the use of tokens as

rewards in intellectual tasks (Cláudia Sousa & Matsuzawa, 2001). Her results showed that

tokens can be used as an effective reward such as the use of direct food. In addition, they

presented a unique feature of saving behavior, contrary to food reward. During the

experiment the three chimpanzees exhibited different patterns of saving behavior and

transported the tokens for a specific goal, to use them for food exchange. The saving

behavior allowed the conclusion that the subjects were able to plan a future action even

if it was in the proximate future.

Figure 1 Claudia Sousa at Cantanhez National Park, Guine-

Bissau. (Adapted from: Margarida et al., 2016).

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Continuing the same experiment with Ai and her infant Ayumu as subjects, Claudia

Sousa was able to study the developmental behavior of Ayumu in a matching to sample

task. At the age between 1 and 10 months old, Ayumu succeed to exchange the first token

for food (Claudia Sousa et al., 2003). These observations showed that the development

of a new skill in infants, is related to the desire to copy an adult behavior and by the

tolerance showed towards him, a mechanism called BIOL (Bonding and Identification-

based Observational Learning).

In Bossou, Republic of Guinea, she also carried other important studies, like the

comparison on the use and development of two tools in wild chimpanzees, leaf-tool for

drinking water and nut-cracking (Cláudia Sousa et al., 2009). In her article published in

2009, she defines leaf-tool use as an ambidextrous task, with some individuals showing

the preference for one hand, different from nut-cracking behavior that is highly lateralized

in the same community of chimpanzees. As she explains, differences between the two

tool behaviors are related to the need of adopting different postural positions that leaf-

tool use demands. Her work did not only focus on social learning as she also made

observations of female chimpanzees carrying their dead infants for long periods (Biro et

al., 2010). She also performed some studies on human behavior, in which she found that

human facial attractiveness appears to be linked to the preference for heterozygosity

(Little et al., 2012).

In the final years of her work, she focused on the conservation and ecology of the small

population of chimpanzees in Cantanhez National Park (CNP), Guinea-Bissau. Her work

at CNP is without a doubt the work that has interested me the most, since it was where

she focused on the study of ethnoprimatology. Her vision to improve conservation

strategies, where chimpanzees live alongside people and the importance to understand

not only chimpanzee’s behavior and ecology, but also how people perceive chimpanzees

and behave towards them (Hockings & Sousa, 2013), is something that I deeply believe

to be essential and that I would like to explore in the future. Related to this topic her

research consisted on realizing some surveys on CNP population to understand how locals

perceive the chimpanzees and the park itself (Sousa et al., 2014). Her research at CNP

showed that chimpanzees and locals coexist in a low conflict level because both utilize

different part of the cashew nuts. The chimpanzees consume the fruit and the farmers only

utilize the nut (Hockings & Sousa, 2012).

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Between the time spent out doing fieldwork, she participated as the author in many

book chapters, published national and internationally. Her notable contribution to

primatology work and international career led her to become the Vice-President of the

Primatology Portuguese Association (PPA). Along with these achievements, she also held

lectures at the Nova University of Lisbon and at University of Coimbra, where she taught,

supervised and mentored many aspiring young students.

Sadly, Claudia left too soon, and I was not able to meet her or attend any of her classes,

but her successes and accomplishments are not forgotten. As her ideas and novel scientific

approaches, can still be continued by all the people she has inspired in Portugal, and

everywhere else in the world. Her work, influence, and passion will remain a motivation

through my journey in primatology and I will continue to follow her example.

1.1. Claudia Sousa Memorial Fund

Claudia Sousa Memorial Fund for the Advancement of Portuguese Primatology

(https://langint.pri.kyoto-u.ac.jp/ai/en/claudia/) was created by Professor Tetsuro

Matsuzawa, in honor of Claudia Sousa, the person, and scientist, to inspire Portuguese

students into primatology research. Since 2015, four other previous students, Raquel

Costa, André Gonçalves, Filipa Borges and Daniela Rodrigues, had the chance to visit

Japan and stay at the Primate Research Institute, with all expenses covered and a stipend.

As the 5th awardee, I had the opportunity to travel to Japan from the 19th of September

2019 till the 12th of December 2019.

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2. The beginning of Primatology in Japan

The history of primatology in Japan started

in a particular way, that would leed to a unique

method of field research: individual

recognition; habituation; and long term

observation, that is still practible in nowadays

(Matsuzawa & McGrew, 2008). Back to the

year of 1948, Professor Kinji Imanishi, from

Kyoto University, and two of his students,

Junichiro Itani and Shunzo Kawamura (Figue

2), traveled to the Toi Peninsula, Japan, to study the society of feral horses (Matsuzawa

& Yamagiwa, 2018). However, after a first encounter with a group of wild Japanese

macaques (Macaca fuscata), the team decided that this group was way more complex

than the group of wild horses (Matsuzawa & Yamagiwa, 2018). Therefore, on the 3rd of

December in 1948 the first scientific obervations of non human primates in Japan would

begin in Koshima island (Matsuzawa & Yamagiwa, 2018; Yamagiwa, 2010). Continuous

research allowed very important discoveries about Japanese macaques social ecology,

such as the presence of a matrilineal society, scrict dominance hierarchy, seasonal aspects

of reproduction (Matsuzawa & McGrew, 2008) and evidence of social transmission, with

the famous sweet-potato washing (Hirata et al., 2008).

3. Japan Monkey Center (JMC)

Japan Monkey Center, https://www.japanmonkeycentre.org/pt/index.html#guide,

was founded in October 17 in 1956, in Inuyama, Achi Prefecture, with the efforts of

Professor Itani Imanishi,. First it started as an institute and later became a museum

(Matsuzawa & Yamagiwa, 2018). Today JMC works as a zoological garden, and it is a

member of the Japanese Association of Zoos and Aquaria (JAZA). The main objective is

promoting education and research in primate studies (Cardinal, 2017). I had the

opportunity to visit JMC in occasion of two conferences and during my free time. JMC

is a zoological museum with a vast number of primate species and, during my visits, I

was able to see some primate species for the first time (Figure 3 and 4).

Figure 2. Imanishi (middle) and his students on

Koshima Island in 1948. (Adapted from:

Matsuzawa & Yamagiwa, 2018).

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JMC is divided in different areas

such as the African Center (with

chimpanzees and gorillas spp.), African

house, Asian House, Madagascar house,

Gibbon house, Wao Land (with ring-

tailed lemurs, Lemur catta) and the

Petting zoo, for children, with domestic

animals (Cardinal, 2017). Species like

siamangs (Symphalangus syndactylus)

and Geoffroy’s spider monkeys (Ateles

geoffroyi) can be found at the Monkey

Scramble and Monkey Skyway. At the

Monkey Valley we can observe

Japanese macaques in a 4.000-meter

square open enclosure. At JMC it’s also

possible to visit the museum, a place that

has around 6.300 specimens’ remains of

skeletal, formalin-preserved brains,

organs and parasites, that belong to the

database Captive Primate Collection

(CAPriCo). The very first publication of

the journal “Primates”, one of the oldest English-language primatology journal in the

world (Matsuzawa, 2015), was published in 1957 by JMC. At the present, JMC still

delegates the editorial board members/advisory, board members/editor-in-chief, host

editorial board meeting, and editorial operation of the journal “Primates”.

4. Primate Research Institute (PRI)

The Primate Research Institute, University of Kyoto (KUPRI), https://www.pri.kyoto-

u.ac.jp/index.html, was founded in 1967 by the Professor Kinji Imanishi and Junichiro

Itani (Matsuzawa & McGrew, 2008). PRI it’s an important international center, that

combines different departments that focus on different fields of primatology, like

morphology, paleontology, physiology, neurophysiology, cognition, genetics, etc. This

makes PRI a unique center on primatology research.

Figure 3. Bolivian Squirrel Monkey (Saimiri

boliviensis) JMC, October 2019.

Figure 4. Olive baboons (Papio anubis), resting at

Baboon Castle, JMC, October 2019.

6

During my stay at PRI I was part of the Language and Intelligence section, that has

been focusing on cognitive research both in the wild and in the laboratory. In 1976

Professor Yukimaru Sugiyama (KUPRI), initiated a long-term field study on a

community of wild chimpanzees in the village of Bossou, southeastern Guinea, West

Africa (Matsuzawa et al., 2002). The research on wild chimpanzees in Bossou englobes

topics like population dynamics, tool-use, social transmission of behavior, feeding

ecology, reproductive behavior, vocalizations and conservation. In 1988 Professor

Tetsuro Matsuzawa and colleagues establish an outdoor laboratory, that consists of an

open area in the forest that allows researchers to observe and record chimpanzee’s

behaviors, with minimum interference. Claudia Sousa started her field work with the

community of wild chimpanzees in Bossou, and here she conducted her research on leaf-

tool for drinking water and nut-cracking. All the recorded observations compose the

“Bossou Arquive”, that has been organized and listed in the past years. This was the result

of a collaboration between PRI and a group of Oxford University, leaded by Susana

Carvalho, Dora Biro and the Ph.D. student Daniel Schofield. This project led Daniel and

colleges to develop a new and pioneer software that allows face detection, tracking, and

recognition of wild chimpanzees in video records (Schofield et al., 2019).

The cognitive research in the laboratory at PRI, started in 1977, with the arrival of Ai

(“love” in Japanese), a 1-year old chimpanzee, born in Guinea (Matsuzawa, 2003). Later,

other chimpanzees joined Ai at PRI, and in April of 1978, the “Ai Project” was established

with the main aim of understanding the cognitive capabilities of non-human primates in

comparison with humans, https://langint.pri.kyoto-u.ac.jp/ai/index.html. A discipline that

is termed comparative cognitive science (CCS) (Matsuzawa & Tomonaga, 2001).

4.1. Cognitive experiments

Currently 12 chimpanzees are housed at the

Primate Research Institute and are divided in

two subgroups (Figure 5). Since 2001, both

groups live in a more naturalistic enclosure,

the WISH (Web for the Integrated Studies of

the Human Mind) cages that are connected to

the outdoor, and allow the chimpanzees to

freely choose their movements, in order to Figure 5. Chloe, PRI, November 2019

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mimic the social organization of fission-fusion, of the species in the wild. It is also in PRI

that we can observe a unique climbing structure of 15-m high, to simulate the environment

of natural forest (Figure 6).

The cognitive experiments on chimpanzees at PRI focuses on different areas of

research and are conducted in different laboratories (South Playroom, Lab 2, Lab 4, and

Lab 5). The experiments take place two times per day, from 8:45 am to 11:00 am and

from 1:15 pm to 03:30 pm. Researchers and staff call each chimpanzee by the name and

it is every individual’s choice to participate in the cognitive tasks, or not. I had the

opportunity to observe some of the experiments being done at PRI. It was a very special

moment to me when I first saw Ai and Ayumu entering the experimental booth to perform

number sequence and memory masking tasks. I have read and talked about them before

in classes, and there I was, seeing both so close. Other experimental research at PRI focus

on topics such as the rock-paper-scissors game’s rules (Gao et al., 2018), body inversion

effect (Gao & Tomonaga, 2018), species discrimination, short-term memory, responses

to adult and infant images (Kawaguchi et al., 2019), visual cues to death and sound

response (Hattori & Tomonaga, 2020).

4.2. PRI and CICASP seminars

At PRI every department organizes a weekly seminar, in English, where students or

invited guests have the chance to present their on-going projects. As a member of the

Language and Intelligence section I attended the Psychology seminars at Tuesdays, 5:00

pm, and because ecology is also part of my main interests, I attended the Ecology

Figure 6. Climbing structure, PRI, November 2019

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seminars at Tuesdays 1:00 pm. During the seminars, I was able to observe many different

students and researchers presenting their work (Table 1), that allowed me to have a better

understanding on primatology research.

Table 1 List of weekly seminars at PRI

Seminar Speaker Topic

Psychology

Yuri Kawaguchi “Infants rapidly detect human

faces in complex naturalistic

visual scenes”

André Gonçalves “Visual cues to death,

experiment approach using

eye-tracker”

Raquel Costa “The impact of ecoturism in

the behavior of mountain

gorillas in BINP”

Ecology

Boyun Lee “Does the infant belong to its

mother- changes of allocare

patterns and infant’s choice of

caregiver in Yakushima

Japanese macaques”

Zhihong Xu “Deep learning as a tool in

ecology research”

PRI invited guests

Professor Simone Pika “The Loango Chimpanzee

Project”

Matthew G.Nowak “Conservation of Sumatra’s

Ape species”

Professor Goro Hanya “Coping seasonality by non-

human primates: examples

from Japan and Borneo”

As an awardee of the Claudia Sousa Memorial Fund, I was also part of Center for

International Collaboration and Advanced Studies in Primatology (CICASP). CICASP

organizes weekly seminars and occasionally some workshops, on Wednesdays, 5:00 pm.

This year in CICASP seminars topics such as professional biographies and scientific

debates were explored.

4.3. Journal Club

The Language and Intelligence section organizes bi-weekly journal club meetings, in

which a member presents a scientific publication. Some of the examples are “Emotion

evaluation and response slowing in a non-human primate: New directions for cognitive

Bias Measures of animal Emotion” (Bethell 2016), presented by Srishti Tripathi and

“Do chimpanzees console a bereaved mother?” (Goldsborough et al., 2020), presented by

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André Gonçalves. I also had the opportunity to present a scientific article entitled “Potent

Social Learning and Conformity Shape a Wild Primate’s Foraging Decisions” (van de

Waal et al., 2013). This study investigated how two classes of wild vervet monkeys’

(Chlorocebus pygerythrus), infants and immigrant males, naïve to a local norm, respond

to a local preference.

4.4. Interdisciplinary seminar on primatology

The interdisciplinary seminar is an event where students from Ph.D. and Master

programs, from all departments can interact academically with one another. This year the

event was held on 10th of December, and the program included a variety of activities such

as oral presentations, poster presentations (Table 2), quiz games and a photo exhibition,

where I had the opportunity to exhibit some of my own photos.

Table 2 Personal highlights of the interdisciplinary seminar 2019

Speaker Topic

Drª Marie Sigaude “"Exploiting agricultural lands whilst

avoiding humans: The complicated life of

bison" (Oral)

Sanjana Kadam "Investigation of the Cognitive Model

of Depression and Its Underlying Neural

Mechanisms" (Oral)

Ryotaro Ohara “Perspective taking and self-reflection" (Oral)

Drº Heung-jin Ryu “Changes in urinary sex steroids of

greater horseshoe bats during hibernation

in South Korea" (Oral)

Drª Cécile Sarabian “Disgust as a tool to mitigate human-wildlife

conflicts and enforce appropriate ecotourism

practices?” (Poster)

Drª Cécile Sarabian and Drª Marie Sigaude “Why animal cafes are bad news for wildlife?

Welfare concerns and problematic origins of

wildlife species displayed in Japanese animal

cafés” (Poster)

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5. Conferences

5.1. 12th International Symposium on Primatology and Wildlife

Science (PWS)

Japan Monkey Center

20th-22th September 2019

I attended the PWS Symposium during my first

week in PRI. The event took place for three days, at

JMC, and included talks and presentations concerning

different topics of research. The first session of the first

day, focused on studies of primates both in the

laboratory and in the wild. During the second part of

the afternoon, there was an interactive talk about

communication in science, where some expert guests

exposed some ideas and personal stories about how to

get tools to engage and communicate science with the

general public. The day ended with a poster session

and visual storytelling context. I also had the

opportunity to present a poster communication (abstract below) entitled: “Auditory

enrichment in two primate species kept in the Maia Zoo: common marmoset (Callithrix

jacchus) and green monkey (Chlorocebus sabaeus)” (Figure 7).

In captivity, primates are usually deprived from important stimuli typically found in the wild.

A way to provide a more stimulating and complex environment is through auditory

enrichment. The aim of this study was to explore the effect that music has in two primate

species, Callithrix jacchus (N= 5) and Chlorocebus sabaeus (N=7), living in the Maia Zoo,

Northern Portugal. Each individual under study was exposed to two stimuli (classic music

and rainforest sounds), and to control sessions in which none of the stimulus was played.

Focal sampling and continuous observation were used in 20 minutes sessions, in which

affiliative and agnostic behaviors were registered. The obtained results revealed no evidences

of any significant effect of music in the frequency of agnostic and affiliative behaviors in

either species tested. However, in the common marmoset (Callithrix jacchus) group, a higher

scratching frequency was observed in the context of high numbers of visitors at the zoo. This

might mean that in the future the reduction of visitors and/or staff noise should be an important

concern in species kept in captivity.

Figure 7. Poster communication at

PWS Symposium

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Sessions during the second day of the symposium included topics such as behavior

and ecology, human-wildlife conflicts, evolution and ecology and wildlife research in

Uganda. From these sessions I would like to emphasize the talk of Himani Nautyal

“Interaction between free-ranging dogs and Central Himalayan langur” and

“Understanding the threats to wildlife in Africa”, by Professor Helena Freitas. Finally,

the talk of Dr. Eric Sande “On-site laboratory for international collaborative research on

primate’s ecology and evolution”, that

focused on the collaboration between

Kyoto and Makerere University to

establish an onsite laboratory in

Uganda. After the sessions were

closed, the participants gathered for

the poster and storytelling awards

(Figure 8) and for a get-together party.

During the last day, in order to celebrate the 10th anniversary of CICASP, Professor

Andrew MacIntosh gave to the audience a brief history of the 10 years of CICASP. The

PWS Symposium ended with the closing remarks by Professor Tetsuro Matsuzawa.

5.2. NerdNite

Japan Monkey Center

20th September 2019

NerdNite is an event with the aim to

communicate science in a more fun and informal

way, and it was created by a student, Chris

Balakrishan, in 2003. The first event was held in

Boston city in the US, but quickly spread globally

to more than 100 countries. As part of the PWS

Symposium, NerdNite4000 was organized in

Inuyama, with the edition theme “Time travelling

- A journey through time” (Figure 9). Special

guests gave a brief and interactive talk about the

theme. There were also activities such as a trivia

Figure 8. PWS Symposium poster communication and

storytelling awardees (Adapted from: PSW website).

Figure 9. Nerdnite Inuyama,

September 2019

12

quiz and dance. In general, it was a fun and interesting opportunity to exchange ideas with

other students and researchers.

5.3. Symposium for the Support for African/Asian Great Apes

(SAGA)

Japan Monkey Center

16th-17th November 2019

SAGA, https://www.saga-jp.org/indexe.html, is

an organization within Japan, that was created in

1998 with the main aim of promoting conservation,

welfare, and non-invasive scientific research of

great apes (Matsuzawa, 2016). As a result of a

collaboration with SAGA, another important

association was established in Japan, The Great Ape

Information Network (GAIN), a database that

contains records of all great apes in zoos and other

facilities in Japan. SAGA holds a symposium every

year with free attendance and mostly in Japanese, to

promote and debate awareness on primate’s good

welfare. This year, SAGA Symposium was organized at JMC (Figure 10), and I attended

the English talk by Drº Matthew Nowak on “Conservation on Sumatra’s great apes”.

During this talk it was covered the main threats that orangutans (Pongo spp.) and gibbons

(Hylobates spp.) face in Sumatra, and, some exciting information about the recently

discovered species of orangutan, Tapanuli orangutan (Pongo tapanuliensis)

(https://www.iucnredlist.org/species/120588639/120588662).

6. Traveling

The Claudia Memorial Fund grant makes possible for the awardees to visit places in

Japan that are part of the history of primatology in Japan. I visited places such as

Kumamoto Sanctuary, Yakushima island, and Kyoto city. During my free time, I also

took the opportunity to visit Inuyama Castle and Gifu Castle on Gifu prefecture.

Figure 10. SAGA Symposium 2019

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6.1. Kumamoto Sanctuary

18th November 2019

Kumamoto Sanctuary, https://www.wrc.kyoto-u.ac.jp/kumasan/indexE.html, is

located at the Peninsula of Uto, Kumamoto and it was established in 2007 as the first

Chimpanzee Sanctuary in Japan. Right after SAGA Symposium, I traveled to Kumamoto

with Professor Naruki Morimura. During my visit to Kumamoto Sanctuary, I met the staff

and I had the opportunity to visit the facilities and learn about the routine of the sanctuary.

Kumamoto Sanctuary is home to 6 bonobos (Figure 11), relocated from San Diego Zoo

in the US and 53 chimpanzees (Figure 12), that were rescued from biomedical research.

Some of the facilities and cages at the

sanctuary are still the ones that were

used by the pharmaceutical company,

however, today their purpose is

different (Figure 13). Since the

foundation of the Kumamoto Sanctuary,

some big improvements were done,

such as some work on the social life of

the chimpanzees and reallocation

programs to decrease the number of

individuals (Morimura et al., 2011).

Also, the construction of enriched

outdoor enclosures and a tunnel system to allow the movement of individuals between

Figure 11. Bonobo, VJ, at Kumamoto Sanctuary Figure 12. Chimpanzees at Kumamoto Sanctuary

Figure 13. Playroom at Kumamoto Sanctuary. The room

that before was used to keep chimpanzees isolated, was

transformed in a playroom. The main purpose is

introducing individuals to each other in a gradual way, to

allow group formation.

14

the three main buildings. Every day the team at the sanctuary follows a strict routine of

feeding, cleaning booths, and outside enclosures and preparing contraceptive pills for

females. Some of the research being done at Kumamoto Sanctuary includes eye-tracking

and study of emotions. At the end of the day, I had the opportunity to visit Mizumi Port

and I was able to observe some Indo-Pacific finless porpoise (Neophocaena

phocaenoides) swimming in the bay.

6.2. Yakushima Island

19th-22th November 2019

Yakushima island is situated 60 km off the southernmost tip of Kyushu Island, in

Kagoshima prefecture. It is a unique place with a very rich flora and fauna, where it is

possible to find around 1.900 species and subspecies of plants, such as the ancient sugi

trees (Cryptomeria japonica). Also, 16 mammal species, such as the Yakushima Japanese

macaque (Macaca fuscata yakui) and the sika deer (Cervus nippon). Because of its

uniqueness, Yakushima Island was considered a World Heritage site in 1993, by

UNESCO. I traveled to Yakushima Island in the company of Professor Tetsuro

Matsuzawa and Professor Naruki Morimura. Once we arrived, we joined the students and

professors of the Yakushima field course, at the field site base camp. The Japanese

macaque research in Yakushima started in

the mid-1970s after Junichiro Itani and

Shunzo Kawamura visited the island to

survey Macaca fuscata yakui (Yamagiwa,

2010). Before reaching the field base camp,

is still possible to see the first house that was

built to conduct primatology research on the

island (Figure 14).

During my second day, I joined the students of the parasitology group of the field course,

led by Professor Andrew MacIntosh. We started the day following groups of wild

Japanese macaques into the forest and collecting fecal samples, for later analyses. It was

an amazing opportunity to observe Japanese macaques’ natural behaviors and learn more

about their ecology (Figure 15 and 16). The Japanese macaques of Yakushima Island

exist in smaller groups than the other subspecies and during mating season, females may

Figure 14. First house of Yakushima field site for the

study of Japanese macaques.

15

create a bond with males from other groups. As result, males move between groups to

solicit mating with estrous females (Yamagiwa, 2010). Occasionally, we were lucky to

be in the presence of sika deer’s that would feed close to the monkeys (Figure 17). During

the rest of the day, we had lunch at Ohko-no-taki waterfall, visited the Lighthouse of

Yakushima and finished our day trip at Yoggo Valley (Figure 18 and 19). The day ended

in the parasitology laboratory at the base camp, where I assisted the Ph.D. student Vanessa

Gris on the fecal samples processing.

Figure 15. Ph.D. student Vanessa Gris collecting

fecal samples Figure 16. Japanese macaques social grooming

Figure 17. Japanese macaque and Sika deer Figure 18. Ohko-no-taki waterfall

Figure 19. Yoggo Valley

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The next day at Yakushima island started before sunrise when Professor Tetsuro

Matsuzawa, Professor Naruki Morimura and I went for a day trip to hike Miyanoura-dake

mountain (Figure 20, 21, 22). Mt. Miyanoura, or also known as “Alpes of the sea” is the

highest mountain in the island and the highest peak in Kyushu, with an elevation of 1.935

m. The hike started following the 12.8 km Yodogawa-tozanguchoi route through amazing

views of valleys, forest, wetlands with innumerous different plant species. After 5 hours

of hikking we reached Mt. Miyanoura summit. At the top, we were able to contemplate

an amazing view and appreciate the beauty of Yakushima Island. During my last day at

Yakushima, I joined the students on a trail to Shiratani Unsuikyo (Figure 23).

Figure 20. Beginning of Mt. Miyanoura trail Figure 21. Mountain view during the hike

Figure 22. Half-way to the summit of Mt.Miyanoura

hikking

Figure 23. Students at Shiratani Unsuikyo trail

17

6.3. Kyoto

25th-28th November 2019

In Kyoto I was hosted by Drª Renata

Mendonça and I visited Arashiyama, a

district in the city with a variety of

attractions. There I could visit the

Iwatayama Monkey Park, where it is

possible to observe free-ranging

Japanese macaques (Figure 24 and 25),

since March 1957. The first scientific

observations of Japanese macaques in

Arashiyama began in 1955 with

Naonosuke Hazama, from Kyoto

University, after some attempts of food

provisioning (Huffman, 1991).

Today around 130 monkeys roam the

surroundings of the park, and frequently

gather in the square for their three-daily

feeding. The park is located 160 m of sea

level and gives a unique view over Kyoto

city (Figure 26 and 27).

Figure 24. Japanese macaque infant, at Iwatayama

Monkey Park

Figure 26. View over Kyoto city, Iwatayama

Monkey Park Figure 27. Maple tres, at Iwatayama Monkey Park

Figure 25. Japanese macaque infant nursing and

social grooming, at Iwatayama Monkey Park

18

On my second day at the city, I visited

the University of Kyoto and the Kyoto

University Institute for Advanced Study

(KUIAS), https://kuias.kyoto-u.ac.jp/e/.

Kyoto University (Figure 28) is the

second oldest Japanese university and a

leading research institute affiliated with

19 Nobel Prize laureates. KUIAS is a

research center led by a team of

distinguished professors with outstanding

achievements in their respective fields, such as Professor Tetsuro Matsuzawa. Being an

old capital of Japan, Kyoto has a lot of history and a variety of sacred places, such as

Buddhist temples and Shrines. I visited Ginkakuji Temple, or “Temple of the Silver

Pavilion”, a World Cultural

Heritage Site, built-in 1490

(Figure 29). Besides the

beautiful Buddhist architecture,

it’s possible to walk around the

gardens, that at the time were

filled with vibrant Autumn

colors. My time in Kyoto ended

with the visit to Sanjusangen-do

temple, famous for its 120 m

long hall and 1001 Buddhist

statues from the 12th and 13th century.

7. Nesting-cup manipulation in chimpanzees and humans

A very unique characteristic of humans is how intense and complex their tool use is,

however since the discovery of Jane Goodall on chimpanzee tool behavior, many other

forms of tool manipulation had been observed in a great number of non-human primates,

and even in one bird, the New Caledonian crow (Corvus moneduloides) (Hunt, 1996). An

important aspect of tool use behavior is object manipulation, a precursor of tool use

behavior, that can exhibit different forms of complexity (Hayashi, 2015). Matsuzawa

Figure 28. At Kyoto University

Figure 29. Ginkakuji Temple, Kyoto

19

(1996) defined different

levels of chimpanzee tool

use, “Tree structure

analysis” (Figure 30).

Level 1 is the most basic

form of object

manipulation, with the use

of one single action, such as termite fishing. Level 3 is the most complex also defined as

a meta-tool, a skill of manipulation rare in the wild that has been observed in nut cracking.

To examine the cognitive process that underlie the complexity of object manipulation in

non-human primates, the “nesting cup task” has been adopted (Hayashi, 2007; Johnson-

Pynn et al.,1999; Westergaard & Suomi, 1994). This method was first used to access

cognitive development in human children (Greenfield et al., 1972).

The human speech follows a hierarchical organization, in which phonemes (units of

language), morphemes and sentences combine in a sequential way to form the human

speech (Matsuzawa, 2001). Object manipulation seems to follow the same hierarchical

organization, and Greenfield et al. (1972) defined three strategies to combine cups in

human children: pairing, pot, and subassembly. The pairing method consists of one single

action, in which one cup being placed in or on a second cup. The pot strategy comprises

two or more cups combined successively. Method three, subassembly consists of two or

more cups being moved as a unit to another cup, or structure (Hayashi, 2007). Results

showed (Greenfield et al., 1972) that the manipulative strategies follow the same

development order of grammatic structure, and that the same way grammar complexity

increases with age, the subassembly method increases after 3 years of age.

To have a better insight into the complete sequence of

nesting cup manipulation, Hayashi (2007) created a

new a notation system consisting of sequential codes.

This system was first applied in experiments with three

infant chimpanzees, their respective mothers, and two

human children. The coding system of Hayashi (2007) follows a combination of two

numbers and one letter (Figure 31). The first number refers to the object manipulated by

the subject. The objects consisted of two cup sets (1 to 5 and 1-10), numbered according

to the color and size. The second letter of the code refers to the action, or how the cup

Figure 30. “Tree structure analysis” (Adapted from: Matsuzawa, 1996)

Figure 31. Scheme of notation system

(Adapted from: Hayashi, 2007)

20

was manipulated. Every possible action was already defined (Table 3). At last, the second

number refers to a location. An example of a coded sequence would bet the following

one:

“1N5/3U5/1D15/3N5/1N35”

cup1 is inserted in cup5/cup3 contacts cup5/cup1 disassemble cups15/cup3 is inserted in

cup5/cup1 is inserted in cups35//

Table 3 List of codes used in the notation system (Adapted from: Hayashi, 2007)

Action code Description

U (Put) Contact cup(s) to other cup(s) and retrieve it without releasing

N (Insert) Insert cup(s) onto another cup(s)

P (Pile) Pile cup(s) onto another cup(s)

H (Hit) Hold cup(s) and hit another cup(s)

D

(Disassemble)

Take out cup(s) from a set of combined cups

F (Floor) Put cup(s) on the floor

T (Touch) Touch cup(s) without changing their position

R (Replace) Take cup(s) and change their position on the floor without contacting

another cup(s)

V (Reverse) Reverse direction of a cup

M

(Miscellaneous)

Any other kind of behavior such as bite or throw; Simultaneous

manipulation of another cup(s)

L (Fall) Fall from a set or taken out by other individual

// All cups combined into one structure

//E Trial ended by subject or tester

* Inverted cups

21

During my stay at PRI, I followed the same coding scheme to code video clips of infant

chimpanzees (Pal, Ayumu and Cleo) and human children performing nesting-cup tasks,

that were realized some years ago.

Table 4 Nesting cup video clips information.

Subjects Age* Total videos coded

Infant chimpanzee ± 6 till 8 years old 57

Human children ± 1 till 4 years old 119

*Age relates to the age of subjects since the beginning of the experiments till the end.

The resulting coding will be further analyzed at University of Tokyo.

22

8. Final remarks

My experience at the Primate Research Institute gave me exceptional opportunities,

both personal and academic. First, I was able to be in a very enriching academic

environment, where I could expand my scientific knowledge and skills, debate ideas and

very important to learn from other students and professors. Lastly, I had a unique

opportunity to experience Japanese culture and visit beautiful places around Japan.

23

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