Food related innovative behavior of the macaques

FOOD-RELATED INNOVATIVE BEHAVIORS OF
THE MACAQUES

ISLAMUL HADI

SEKOLAH PASCASARJANA
INSTITUT PERTANIAN BOGOR
BOGOR
2013

PERNYATAAN MENGENAI DISERTASI
DAN SUMBER INFORMASI SERTA
PELIMPAHAN HAK CIPTA
Dengan ini saya menyatakan bahwa disertas berjudul Food-Related
Innovative Behaviors of The Macaques adalah benar karya saya dengan
arahan dari komisi pembimbing dan belum diajukan dalam bentuk apa pun
kepada perguruan tinggi mana pun. Sumber informasi yang berasal atau
dikutip dari karya yang diterbitkan maupun tidak diterbitkan dari penulis
lain telah disebutkan dalam teks dan dicantumkan dalam Daftar Pustaka di
bagian akhir disertasi ini.
Dengan ini saya melimpahkan hak cipta dari karya tulis saya kepada

Institut Pertanian Bogor.
Bogor, Mei 2013

Islamul Hadi
G362080011

RINGKASAN
ISLAMUL HADI. Food-Related Innovative Behaviors of The Macaques. Dibimbing oleh BAMBANG SURYOBROTO, KUNIO WATANABE, ACHMAD FARAJALLAH.
Perilaku inovatif dalam perilaku baru yang dilakukan oleh individu hewan
dan terjadi pada frekuensi rendah dan tidak umum ditemukan pada kondisi normal.
Perilaku inovatif memungkinkan hewan dalam menghadapi lingkungan baru dan
mengeksploitasi sumber daya lebih luas. Perilaku inovatif telah diamati dan
didokumentasikan pada berbagai hewan terutama burung dan primata. Hampir
setengah dari perilaku inovatif ini berkaitan dengan perilaku makan termasuk di
antaranya teknik ekstraksi makanan, jenis-jenis makanan baru, dan teknik mengolah makanan.
Pertama, saya mengamati lima kelompok monyet ekor panjang (Macaca
fascicularis) di ketinggian Taman Nasioanl Gunung Rinjani tahun 2008-2009.
Saya mengamati salah satu kelompok monyet tersebut hidup di sekitar Pemandian Air Panas Pengkereman yang memiliki suhu rendah dan miskin sumber
makanan alami. Beberapa individu monyet di dalam kelompok Pengkereman
menunjukkan perilaku mandi air panas. Perilaku tersebut merupakan perilaku inovasi yang baru di dalam kelompok tersebut. Perilaku ini berkembang sebagai

tanggapan terhadap kondisi habitat mereka. Mereka mengambil sisa makanan
dari manusia yang terendam di air panas. Mereka rasakan suhu yang lebih hangat
saat mereka masuk ke air panas. Mereka mampu mengingat dan mengulangi
perilaku ini karena monyet-monyet ini belajar dan mendapatkan keuntungan
nutrisi dan termoregulasi dari lingkugan air panas.
Kedua, saya mengamati perilaku makan ikan yang dilakukan oleh beberapa individu monyet ekor panjang di Taman Wisata Alam Pangandaran tahun
2010-2012. Perilaku ini pertama kali teramati di Kelompok Rengganis pada tahun
2010. Tiga monyet betina dewasa dan satu monyet betina muda makan ikan yang
mereka dapatkan dari jaring yang tertinggal di perahu di Pantai Rengganis. Saat
ini perilaku makan ikan hanya dilakukan oleh sejumlah individu monyet Kelompok Goa Parat dan K12. Perilaku makan ikan ini merupakan perilaku baru yang
dilakukan oleh sejumlah individu monyet ekor panjang di Pangandaran karena
adanya gangguan nutrisi. Kondisi ini mempengaruhi jumlah individu dan kelompok monyet yang ada di Taman Wisata Alam Pangandaran. Selain itu, kondisi
tersebut berpengaruh terhadap perilaku makan monyet ekor panjang di areal ini.
Penurunan jumlah makanan dari pengunjung Taman Wisata sejak krisis ekonomi
Asia tahun 1998 mendorong monyet-monyet di sini untuk berpindah daerah jelajah seperti yang dilakukan oleh Kelompok Rengganis atau mencari sumber
makanan baru yang ada di wilyah jelajahnya seperti yang dilakukan oleh Kelompok Goa Parat. Perilaku makan ikan yang ditunjukkan oleh individu-individu
monyet anggota Kelompok Goa Parat merupakan tanggapan terhadap perubahan
yang terjadi di habitatnya.
Ketiga, saya mengamati perilaku merampas makanan yang dilakukan oleh
individu-individu monyet Jepang (M. fuscata) di Chosikei Monkey Park, Shodoshima Island, Jepang. Perilaku merampas makanan ini didefinisikan sebagai perilaku ketika satu individu memaksa individu lain untuk membuka mulut dan

merampas makanan yang ada di dalam mulut individu lain. Saya melakukan pengamatan pada akhir Juni 2012. Pada pengamatan ini saya mengamatai Kelompok A
yang terdiri dari 214 individu. Saya mencatat umur dan jenis kelamin individuindividu monyet yang melakukan perampasan makanan monyet-monyet yang
menjadi targetnya. Saya juga melakukan pengamatan pengaruh distribusi dan
jumlah makanan yang diberikan oleh penjaga Taman Monyet. Selama pengamatan, saya mencatat 747 kali perampasan makanan yang dilakukan oleh tujuh
monyet (satu jantan dewasa dan 6 betina dewasa). Perilaku ini hanya ditunjukkan
pada saat pemberiaan makan oleh penjaga. Dari 747 peristiwa perampasan, 609 di
antaranya berhasil. Target utama perilaku perampasan ini adalah monyet juvenile
(650 kali perampasan; 578 kali berhasil). Selain itu, betina dewasa (93 kali perampasan; 30 kali berhasil) dan betina muda (empat kali perampasan; sekali berhasil)
juga menjadi target perampasan makanan). Perampasan makanan dengan target
utama monyet juvenil dikarenakan monyet ini secara alami lebih lemah dari
monyet dewasa. Penyebaran dan jumlah makanan tidak berbengaruh terhadap
frekuensi perampasan makanan, tetapi lama waktu makan sangat berpengaruh
terhadap frekuensi perampasan. Lama waktu makan ini menunjukkan jumlah biji
gandum yang tersisa di dalam kantung makanan di mulut monyet-monyet yang
menjadi target perampasan.
Keywords: Perilaku terkait makanan, perilaku inovasi, Perilaku mandi air panas,
Perilaku makan ikan, Perilaku merampas makanan, Macaca fascicularis, M. fuscata.

SUMMARY

ISLAMUL HADI. Food-Related Innovative behavior of The Macaques. Supervised by BAMBANG SURYOBROTO, KUNIO WATANABE, ACHMAD FARAJALLAH.
Innovative behavior is a new behavior performed by individuals, occurred
in low frequencies and restricted to particular area. Innovative behavior may allow
animals in coping new environment and exploit more resources. Innovation as
product and process of learning behavior has been observed and documented in
various numbers of animals, mainly birds and primates. Nearly a half of those
records came from food-related behaviors including food extraction technique,
novel food items, and food preparation. Many of those behaviors were recorded in
anthropogenic disturbance habitat, where animals were challenged by rapidly
changing environments.
First, I observed long-tailed macaques (Macaca fascicularis) in Pengkereman hot-spring in the highland of Mt. Rinjani in Lombok Island in 2008-2009.
They showed innovative behavior in utilizing hot-spring. Two individuals of longtailed macaques were observed in September 5, 2004 incidentally to soak their
limbs into the hot spring water. On August 20-22, 2008, during three consecutive
day surveys, 4, 5, and 6 out of 26 individuals’ macaques immersed their bodies
into the hot-spring stream and pool, respectively. However, this behavior not
performed by individuals of the two groups living in adjacent areas, Pelawangan
Sembalun and Pos 3 Senaru Groups and two others group of Sebau hot spring 20
km eastern of Pengkereman were never observed to soak their bodies in the water.
The behavior was driven by scarcity of natural food source while the artificial
foods from human tourist available in the area of hot-spring. The behavior fixed in

some individuals who learn the thermoregulation advantages of the hot spring
bathing in their habitat in highland with low ambient temperatures.
Second, I observed fish-eating behavior performed by long-tailed macaques
in Pangandaran Recreation Park in 2010-2012. This behavior was firstly observed
in Rengganis Group on November 2010, when three adult and a sub-adult females
ate fishes obtained from unattended net. Recently the fish-eating behavior is
performed only by individuals of Goa Parat and K12 groups of Pangandaran
Recreational Park. The fish-eating behavior that performed by long-tailed macaques in Pangandaran might be newly established as the innovative behavior. After
Asian economical crisis in 1998 long-tailed macaques in the Pangandaran is in
condition of nutritional deterioration. This condition affectted number of individuals and groups of long-tailed macaques in the Recreation Park and also the
feeding behavior of the macaques live in park. Decreasing amount of food from
visitors drove the macaques to move their home range like Rengganis Group or
exploit new source in their home range like Goa Parat Group. The development of
fish-eating behavior by individuals of Goa Parat Group could be the response to
the challenge posed by the changing situation of the habitat.
Third, I investigated the characteristics of a particular food-snatching
behavior in which one individual forced another’s mouth open and grabbed the
food, as performed by free-ranging Japanese macaques (M. fuscata) in Choshikei
Monkey Park on Shodoshima Island, western Japan. I conducted a survey in late

June 2012 and observed one of two monkey troops, comprising 214 monkeys. I
recorded the age classes and sexes of the individuals who performed the snatching
behavior and were snatched from, and examined the effects of provisioned food
distribution and quantity on the frequency of snatching trials and success. During
the survey, I recorded 747 snatching trials, of which 609 were successful, all of
which were performed by seven individuals: one adult male and six adult females.
The snatching behavior occurred only during provisioning. The target animals
were primarily juveniles (650 trials, 578 successful), while cases in which food
was snatched from adult females (93 trials, 30 successful) and sub-adult females
(4 trials, 1 success) were less frequent. Among the juveniles, small juveniles had
food snatched more frequently than large juveniles. The higher frequency of
snatching trials against juveniles was likely due to their subordinate nature.
Neither the distribution nor quantity of the provisioned foods had significant
effects on the number of snatching trials nor did the successes, while the time
elapsed after provisioning have significant negative effects, attributed to a
decrease in the number of wheat grains left within the mouth pouch of the
potential target animals.
Keywords: Food-related behavior, Innovative behavior, Hot-spring bathing, Fisheating, Food-snatching, Macaca fascicularis, M. fuscata

© Hak Cipta Milik IPB, Tahun 2013

Hak Cipta Dilindungi Undang-Undang
Dilarang mengutip sebagian atau seluruh karya tulis ini tanpa mencantumkan
atau menyebutkan sumbernya. Pengutipan hanya untuk kepentingan pendidikan,
penelitian, penulisan karya ilmiah, penyusunan laporan, penulisan kritik, atau
tinjauan suatu masalah; dan pengutipan tersebut tidak merugikan kepentingan
IPB.
Dilarang mengumumkan dan memperbanyak sebagian atau seluruh karya tulis ini
dalam bentuk apa pun tanpa izin IPB

FOOD-RELATED INNOVATIVE BEHAVIORS OF
THE MACAQUES

ISLAMUL HADI

Disertasi
sebagai salah satu syarat untuk memperoleh gelar
Doktor
pada
Mayor Biosains Hewan

SEKOLAH PASCASARJANA
INSTITUT PERTANIAN BOGOR
BOGOR
2013

Penguji pada Ujian Tertutup (17 Desember 2012):
1. Dr Entang Iskandar
(Peneliti pada Pusat Studi Primata LPPM Institut Pertanian Bogor)
2. Dr Yamato Tsuji
(Assistant Professor pada Primate Research Institute, Kyoto University,
Japan)
Penguji pada Ujian Terbuka (23 Januari 2013):
1. Dr Ir Novianto Bambang Wawandono
(Direktur Konservasi Keanekaragaman Hayati, Dirjen PHKA
Kementerian Kehutanan Republik Indonesia)
2. Dr Entang Iskandar
(Peneliti pada Pusat Studi Primata LPPM Institut Pertanian Bogor)

Judul Disertasi : Food-Related Innovative Behaviors of The Macaques
Nama

: Islamul Hadi
NIM
: G362080011

Disetujui oleh
Komisi Pembimbing

Dr Bambang Suryobroto
Ketua

Prof Dr Kunio Watanabe
Anggota

Dr Ir Achmad Farajallah MSi
Anggota

Diketahui oleh
Ketua Mayor Biosains Hewan

Dekan Sekolah Pascasarjana

Dr Bambang Suryobroto

Dr Ir Dahrul Syah MSc Agr

Tanggal Ujian: 23 Januari 2013

Tanggal Lulus:

PRAKATA
Disertasi ini berjudul Food-Related Innovative Behavior of The Macaques.
Pengamatan perilaku innovasi terkait makanan pada monyet ekor panjang telah
dilakukan di Pemandian Air Panas Pengkereman yang berada di Taman Nasional
Gunung Rinjani, Lombok dan Taman Wisata Alam Pangandaran, Ciamis Jawa
Barat. Pengamatan juga telah dilakukan Chosikei Monkey Park, Shodoshima
Island, untuk melihat perilaku inovasi terkait makanan pada Monyet Jepang.
Saya mengucapkan terima kasih kepada para dosen pembimbing Dr Bambang
Suryobroto, Dr Achmad Farajallah and Prof Dr Kunio Watanabe atas bimbingannya. Terima kasih juga saya sampaikan kepada Dr Yamato Tsuji, Prof Yuzuru
Hamada, Prof Hiroo Imai, Prof Akichika Mikami, (Alm) Prof Osamu Takenaka
yang telah mensponsori saya dalam program kerjasama penelitian antara IPB and

Primate Research Institute Kyoto University. Terima kasih yang setinggi-tinginya
saya sampakan kepada seluruh staf pengajar di Biosains Hewan (Dra Taruni Sri
Prawasti M Si, Dr. Dedy Duryadi Solihin, Tri Heru Widarto, M.Sc, Dr. Dyah
Perwitasari, Dr. Rika Raffiudin, Dr. Tri Atmowidi, MSi) dan teman-teman di Zoo
Corner (Dr Kanthi Arum Widayati,Dr Tetri Widiyani, Sarah Nila, SSi, Puji Rianti,
MSi, Eneng Nunuz R, MSi, Elda Irma Kawulur, MSi, Andi Darmawan, M.Si,
Rizqi Amar Absdussalam, SSi, Mbak Tini, Mbak Ani, Pak Adi Surachman) atas
kebersamaannya selama masa pendidikan doktor ini. Terima kasih juga penulis
sampaikan kepda anggota Section Ecology and Conservation, Social System
Evolution, Evolutionary Morphology Section, Primate Research Institute Kyoto
University Japan atas diskusi mingguan selama penulis belajar di PRI. Ucapan
terima kasih kepada Dr Entang Iskandar dari PSSP LPPM IPB dan Dr Novianto
Bambang Wawandono (Direktur KKH PHKA Kementerian Kehutanan RI) atas
segala masukannya pada saat ujian.
Ucapan terima kasih juga tidak lupa saya sampaikan kepada Dedi
Surachman SSi, Adi Nurfebrimansyah SSi, M. Sya’roni SSi, Heru Iswandi SSi,
Faizan SSi, Abdul Basith Nasrianto dan staf Taman Nasional Gunung Rinjani,
Lombok atas bantuannya selama penelitian di Lombok. Bapak Yana Hendrayana
dan staf Taman Wisata Alam Pangandaran dan BBKSDA Jawa Barat atas bantuan
dan ijin selama penelitian di Pangandaran. Terima kasih kepda staf Chosikei
Monkey Park, Shodoshima, Japan (Mr. Ryuji Hida, Akihiro Nishio, Mrs. Chiyoko
Saeki, and Mr. Mitsuyuki Ishii) dan Cooperative Research Program 2012 Primate
Research Institute Kyoto University kepada penulis dan Grant-in-Aid from the
Department of Academy and Technology of Japan (Japanese Society for
Promotion of Science, no. 23780160; 2011–2013 kepada Dr. Yamato Tsuji) atas
segala bantuannya selama penelitian di Jepang. Salah satu bagian dari disertasi ini
yang berjudul “Food snatching of free ranging Japanese macaques observed
on Shodoshima Island : prelimary report” telah dipublikasikan pada Jurnal
Primates pada awal tahun ini.
Terima kasih yang setinggi-tingginya saya sampaikan kepada Dit Jen Dikti
Kementerian Pendidikan dan Kebudayaan RI dan Insitut Pertanian Bogor atas
pemberian dana BPPS dan program SANDWICH LIKE 2009-2010 kepada penulis
untuk belajar di IPB dan Primate Research Institute, Kyoto University, Japan.
Terima kasih juga saya sampaikan kepada ASIAN HOPE project atas bantuan dana

untuk mengikuti the 2010 Pre IPS and IPS congress di Inuyama and Kyoto dan
presentasi poster “Hot-Spring Bathing Of Long-Tailed Macaques Observed in The
High-land of Mt. Rinjani, Lombok, Indonesia” dan makalah berjudul “ Population
status of long-tailed macaque (Macaca fascicularis) and lutung (Trachypithecus
auratus) in Lombok Island, Indonesia.
Akhirnya, terima kasih atas segala dukungan yang diberikan oleh keluarga
besar penulis, Irma Sofiana Afif dan Reyqa Rinjania atas segala dukungan dan
kesabarannya selama penulis mengikuti pendidikan doctor.
Bogor, Mei 2013

Islamul Hadi

DAFTAR ISI

DAFTAR TABEL

xiv

DAFTAR GAMBAR

xiv

I INTRODUCTION
References
II HOT-SPRING BATHING OF LONG-TAILED MACAQUES : AN
INNOVATIVE BEHAVIOR OBSERVED IN THE HIGHLAND OF
RINJANI, LOMBOK, INDONESIA
Abstract
Introduction
Methods
Results
Discussion
Conclussion
References

1
2
MT.
3
3
4
7
10
11
11

III FISH-EATING BEHAVIOR OF LONG-TAILED MACAQUE FROM
PANGANDARAN RECREATION PARK
Abstract
12
Introduction
12
Methods
13
Results
16
Discussion
18
Conclussion
19
References
21
IV FOOD-SNATCHING BEHAVIOR OF FREE-RANGING JAPANESE
MACAQUES OBSERVED ON SHODOSHIMA ISLAND : A PRELIMINARY REPORT
Abstract
Introduction
Methods
Results
Discussion
References

25
25
26
27
28
29

V GENERAL DISCUSSION
References

31
33

VI GENERAL CONCLUSSION

35

VII REFERENCES

37

VIII RIWAYAT HIDUP

43

DAFTAR TABEL
II.1 Climatic data of Pengkereman area measured during two observation-al
periods
II.2 Number of groups and individuals of long-tailed macaques in high-land
of Mt. Rinjani observed in 2004-2009
III.1 Temporal change of number of group and individuals of long-tailed
macaques inhabited Pangandaran Recreation Park
III.2 Number of individuals involved on fish-eating during the experiment
conducted in November 9, 2010
III.3 Date, location, group and individual numbers performed fish-eating
behavior
IV.1 Daily change on food distribution designed during the study period
IV.2 Indviduals who conduct the snatching behaviour and details of their
target animals, and frequencies and success of the snatching

4
8
16
17
19
27
28

DAFTAR GAMBAR
II.1 Research location on Pengkeraman Area of Mount Rinjani National
Park (1980 m asl)
II.2 Yearly cumulative number of visitor and monthly distribution of
average number visitor to Rinjani National Park from Gate of Senaru
and Sembalun during (2001-2009)
II.3 Some postures of individuals during bathing activities in the hot-spring
area
III.1 Research site of Pangandaran Peninsula which designated as Nature
Reserved and Recreation Park under decree of Ministry of Agriculture
III.2 The Pangandaran Recreation Park and home ranges of Rengganis, Goa
Parat and K12 Groups
III.3 Temporal change of the visitor number to Pangandaran Recreation Park
during period of 1999-2012
IV.1 An adult female (Kanchee) snatching from a juvenile manually and an
adult female (Sarah) snatching from a juvenile orally

6
7
9
14
15
15
28

I
INTRODUCTION
Innovative behavior may allow animals coping with environmental change,
to exploit a wide range of habitat type and to increase their geographical range.
Behavioral innovation may also be a good indicator of general behavioral flexibility, which has long been predicted to be an important determinant among ecological variables (Reader & Macdonald 2005). Behavioral scientists have long
observed that animals in various phylogeny performed behavioral innovation and
differences in innovative tendency (Lefebvre et al. 1997). Classical example of
behavioral innovation concerned with food extraction, preparation, and processing; for example: wheat and potato washing performed by Japanese macaque
(Macaca fuscata) (Kawai 1965; Hirata et al. 2001), novel tool-use by chimpanzees (Pan troglodytes) (Goodall 1964), and milk-bottle-top opening by British
titmice (Parus caeruleus) (Fischer & Hinde 1949). Beside some benefits, innovative behavior also carry ecological and physiological cost such as consuming
hazardous food items, risk from detected by predator, and investment of time and
energy involved in exploiting a new resource.
Kummer and Goodall (1985), in their review on the primate behavioral
innovation, have put the landmark to stimulate the general interest in topic of
animal behavioral innovation. They suggested some behavioral innovations was
derived from ability of the individuals to profit from an accidental happening,
while others resulted from the use of existing behavior pattern for new purposes.
Frequency of occurrence of behavioral innovation correlates with relative brain
size of animals in both birds and primates (Lefebvre et al. 1997; Reader & Laland
2002). For example, over 500 cases of behavioral innovation have been reported
in non- human primates, while over 2200 reports in birds (Reader & Laland 2002,
Lefebvre & Bolhuis 2005). Nearly half of the innovation in non-human primates
relates to foraging context including food extraction and novel food items.
According to Reader and Laland (2005), some potential processes underlying the
behavioral innovation were: 1) neophilia and neophobia, 2) exploration and curiosity, 3) asocial learning and problem solving, 4) insight, 5) creativity 6) behavioral flexibility, 7) social processes.
Genus Macaque, especially fascicularis group (Fooden 1976), disperses
widely in various type of habitat in continental and insular Asia. This group
consisted of rhesus macaques (Macaca mulatta), Japanese macaques (M. fuscata),
Taiwanese macaques (M. cyclopis) and long-tailed macaques (M. fascicularis).
They were found both in natural and man-made habitats (zoo and research center).
Amongst the macaques, members of this group have propensities in behavioral innovation. I assumed behavioral innovation has contributed in their ability to cope
with various conditions during their dispersal. I predict these species get their
advantages from their propensities in behavioral innovation to responses to the
recent anthropogenic modification of their habitat. I emphasize this recent study
on food-related behavioral innovation in the macaques focusing on long-tailed
macaques and Japanese macaques basing on their socio-ecological and behavioral
background with some quantitative approach.

2
I have engaged in the socio-behavioral studies long-tailed macaques living
in Java, Bali and Lombok since 1999. In 2012, further, I got an opportunity to
visit Japan and observe Japanese macaques. During those studies I got several
cases of possibly newly acquired innovative behaviors; that is, hot-spring bathing
and fish-eating of long-tailed macaques (part II and III) and snatching behavior of
Japanese macaques (part VI). In this dissertation, I also describe these three
innovative behaviors and discuss about the possible function of those behavioral
innovations. I also discuss how these behaviors could be realized in what kind of
the circumstances to make clear the key factors of causation of the behaviors and
capabilities of the subject primate species.
References
Fischer J, Hinde RA.1949. The opening milk bottles by bird. British Bird 42: 347357
Fooden J.1976. Provisional classification and key to living species of macaques.
Folia Primatol 25 : 225-236
Fooden J. 1995. Systematic review of Southeast Asian longtail macaques, Macaca
fascicularis (Raffles, [1921]). Fieldiana Zoology 81: 1-206.
Goodall J. 1964. Tool-using aimed throwing in a community of free-living chimpanzee. Nature 201: 1264-1266
Hirata S, Watanabe K, Kawai M. 2001. Sweet potato washing revisited. In:
Matsuzawa T, editor. Primate Origins of Human Cognition and Behavior.
Tokyo (JP): Springer. p. 487-508
Kawai M. 1965. Newly-acquired pre-cultural behavior of the natural Troop of
Japanese monkeys on Koshima Islet. Primates 6: 1-30
Kummer H, Goodall J. 1985. Conditions of innovative behavior in primates. Phil
Trans R Soc Lond B 308: 203-214
Lefebvre L, Bolhuis JJ. 2005. Positive and negative correlates of feeding
innovations in birds: evidence for limited modularity. In: Reader SM,
Laland KN, editors. Animal Innovation. New York (US): Oxford University Pr. p 39-61
Lefebvre L, Whittle P, Lascaris E, Finklestein A. 1997. Feeding innovations and
forebrain size birds. Anim Behav 53: 1077-1097
Reader SM, Laland KN. 2005. Animal innovation: an introduction. In: Animal
Innovation. Reader SM, Laland KN, editors. New York (US): Oxford
University Pr. p 3-35
Reader SM, Laland KN. 2002. Social intelligence, innovation and enhanced brain
size in primates. Proc Nat Acad Sci 99: 4436-4441
Reader SM, Laland KN. 2001. Primate innovation: sex, age, and social; rank
differences. In J Primatol 22: 787-805
Reader SM, Macdonald K. 2005. Environmental variability and primate behavioural flexibility. In: Reader SM, Laland KN, editors. Animal Innovation.
New York (US): Oxford University Pr. p 83-116

3

II
HOT-SPRING BATHING OF LONG-TAILED MACAQUES
OBSERVED IN THE HIGHLAND OF MT. RINJANI,
LOMBOK, INDONESIA
Abstract
Along the survey on the population of long-tailed macaques (Macaca
fascicularis) in highland of Mt. Rinjani, Lombok, I found individuals of Pengkereman Group performed hot spring bathing behavior in hot spring pool and stream
of Pengkereman area (1982 m asl). Two individuals of long-tailed maca-ques
were observed in September 5, 2004 incidentally to soak their limbs into the hot
spring water. On August 20-22, 2008, during three consecutive day surveys, 4, 5,
and 6 out of 26 individuals macaques immersed their bodies into the hot spring
stream and pool, respectively. However, this behavior not performed by individuals of the two groups living in adjacent areas, Pelawangan Sembalun and Pos 3
Senaru Groups and two others group of Sebau hot spring 20 km eastern of Pengkereman were never observed to soak their bodies in the water. The behavior was
driven by scarcity of natural food source while the artificial foods from human
tourist available in the area of hot spring. The behavior fixed in some individuals
who learn the advantages of the hot spring bathing in their habitat in highland
with low ambient temperatures.
Keywords: long-tailed macaque, Macaca fascicularis, Hot-spring bathing,
Innovative behavior, Mt. Rinjani, Lombok
Introduction
The behavioral patterns that are non-universal or present at low occurrence
in few populations are said as innovative behaviors (Van Schaik et al. 2006).
Reader and Laland (2005) regarded innovative behavior as a new or modified
behavioral pattern not previously found in the population.
There are various innovative behaviors of macaques around the world. For
instance, long-tailed macaque (Macaca fascicularis) was reported as using stone
to open oyster shells, using chair for manipulating room key on high place, and
throwing stone (Minakata 1984 firstly appeared in 1920). The stone-tool usage to
open oyster shells had been confirmed to occur in Southern Burma (Carpenter
1887) and Piak Nam Yai Island in Thailand (Malaivijitnond et al. 2007). It was
not found in other places. In Japan hotspring bathing has been known to be performed only by Japanese macaque (M. fuscata) in Jigokudani Monkey Park,
Nagano Prefecture in Japan (Hara 1971; Suzuki 1964; Zhang et al. 2007). Zhang
et al. (2007) reported that hot spring bathing by Japanese macaques in Jigokudani
Monkey Park is influenced by ambient temperature. Many macaques do it more in
winter than summer. It indicates that hot spring bathing by macaques is related to

4
the thermoregulation behavior. However, historically Japanese macaques in
Jigokudani Monkey Park were introduced to the man-made hot spring pool by
providing them with food immersed to water (Zhang et al. 2007).
Along the survey of long-tailed macaques in Lombok Island, I found longtailed macaques performed hot spring bathing in highland of Mt. Rinjani National
Park. The bathing was observed only in a group of macaques live in Pengkereman
area (1982 m above sea level) while other groups were not doing it. I had
opportunity to follow the emergence of the hot spring bathing from 2004 to 2009.
This paper describes this newly established innovative behavior related with
living in highland with low ambient temperature, scarcity of natural food source
and availability of artificial food source in hot spring.

Methods
Mount Rinjani at northern Lombok Island is the highest mount in the island
(3726 m asl) (BTNGR 2009) (Fig. II.1). The mountain is an active volcano. In the
caldera about 2000 m asl there is a lake named Danau Segara Anak (Lake of Sea
Child in the native Sasak language). Hot springs can be seen at several places
around the mountain. The hot spring Aik Kalak (hot water) is located at the
Pengkereman (place for bathing, 08°23′22.7″S, 116°25′11.9″E) at 1982m asl on
the north of Danau Segara Anak (Fig. II.1). The hot-springs flow out to form part
of river Kokok Putih (White River). The Pengkereman area is relatively flat and
provides good bathing places; that is a segment of about 300m of Kokok Putih
River contains several water pools and slow streams and large waterfalls (Fig. 1).
Table II.1 Climatic data of Pengkereman area measured during two observational
periods

Water
Ambient (daytime)
Ambient (midnight)

Temperature measured in (oC)
April 21-22, 2009
August 20-22, 2008
Mean Min Max n
Mean Min Max n
21
18
24
3
36.8
34
39
5
14.3
11
17
4
19.6
10
28
5
13
13
13
2
2.3
1
4
3

The climatic data of Pengkereman area at two observational periods are
presented in Table II.1. April and August correspond to the early and mid of dry
season based on the climatic data measured in the lowland of Lombok during
2001-2008 (Nandini & Narendra 2011). However, in April to early of May rain
could occur in the highland of Mt. Rinjani. In April 21-22, 2009, water from Lake
of Segara Anak overflowed to the hot spring to make the temperature decreased
(see Table II.1).
The custom of hot spring bathing by human was probably started from
1790s when the kingdom of Karang Asem from Bali ruled Lombok Island and the
king designated the area as a holly place of Hinduism. Every summer, Hindu
pilgrims visit the area to offer gold hoping for a good future prosperity (Van der
Kran 2009). This ceremony is called mulang pakelem and, after the ceremony,
peoples take bathe for cleaning their soul.

5
It is just recently that hot spring bathing at the Pengkereman area became
popular and many tourists foreign and native visit the area. Tourists immerse in
these hot spring believing to heal the skin diseases and rheumatism (BTNGR
2009). The west bank of upper area of Pengkereman is designated as camping site
for tourist.
The number of visitor, especially after the Rinjani National Park was
established in 1992, is rapidly increasing from 1920 people in 2001 to 8469 in
2008 (Fig.II.2). The tourist averaged 586.3 individuals per month (min = 13 in
April 2003, max = 1433 in August 2008) during tracking season (April to
December, Fig. II.2).They frequently left food garbages and these provide foods
for macaques. This might be the reason that groups of long-tailed macaques visit
the camping sites, not only the Pengkereman area but also at several others. At
present, we may find macaque groups up to 2700 m asl on the mountain slope
where the uppermost camping site is located (Hadi 2005). In the rainy season
(November to March) the trekking in the area can be very dangerous and peoples
rarely climb up the mountain. Eruption of the volcano, further, may occur at
unexpected time.
The hot spring bathing of long-tailed macaques at Pengkereman was first
observed incidentally on September 2004 along with the population survey being
carried out (Islamul Hadi, unpublished data). I visited again the area three times;
April 30 to May 1, August 20 to 22 2008, and April 21 to 22, 2009. After May 4,
2009 the National Park stopped tracking activities because of the eruption of Mt.
Rinjani and unstable conditions succeeded thereafter.
While in August 2008, I stayed at the camping site from 6:30 of 20th to
11:30 of 22nd and observed the macaques. When they took hot spring bathing the
activity of the party is recorded in terms of time, duration and their detailed
behavior. Macaques did not care much on the presence of observers and it was
possible to record all in video.
Macaque groups other than the Pengkereman were observed when I found
them and information was also collected from rangers of the National Park and
tourists who visited the area. In the northern of Pengkereman, Pos 3 Senaru (2000
m asl), a group of long-tailed macaques was also found. A cool water stream is
also found in their home range. I observed macaque group of Pelawangan
Sembalun at the slope of highland Mt. Rinjani (2700 m asl). It is about 1 km away
northeastern of Pengkereman. The area is the highest camping site for the climber
in the area. There is a small cool water pool which provides fresh water for visitor
who sheltered in the area. Individual identification could be done in some groups.
Some individuals of macaques were recognized as the same member of groups
observed in 2004. Based on information provided by staff of the National Park
(Abdul Basith 2009, personal communication), I observed two groups of longtailed macaques around hot spring of Sebau in March 10-12, 2009. This hot spring
is located 20 km eastern of Pengkereman area with altitude 1380 m asl.

6

380000

400000

420000

440000

460000

N

9080000

80000

60000

9060000

40000

9040000

20000

9020000

400000

Lake

420000

E
S

Lombok Island

380000

W

440000

Mt. Rinjani National Park

460000

Road

Figure II.1 Research location on Pengkeraman Area of Mount Rinjani National
Park (1980 m asl). Point A, B, C are the point where macaques took
bath, A = stream with approximately 30 cm depth, B = stream with
approximately 15 cm depth, C = pool with 3 x 10 m and 90 cm depth

#visitior (individuals)

7

Year

Month

(a)
(b)
onthly distribution
Figure II.2 (a) Yearly cumulative number of visitor and (b) monthly
of average number visitor to Rinjani National Park from Gate of
Senaru and Sembalun
Semb
during (2001-2009) (source:: Rekap Pengunjung
Taman Nasional Gunung
G
Rinjani 2001-2009,
2009, Balai Taman Nasional
Gunung Rinjani, Mataram-Lombok.
Mataram
Results
Most of the part of the highland of Mt. Rinjani beyond 1800 m asl is
covered by volcanic sand with sparsely distributed shrubs and pine trees. There
are 13-18 groups of long-tailed
long
macaques observed in the whole area of Mt.
Rinjani National Park (Hadi et al. 2012). Five of them were found in the highland
of Mt Rinjani (Table II.2).
Observation in 2004
In 2004 three groups were found living on the highland of Mt Rinjani. The
first group is at Pengkereman hot spring area found onn September 44-5, 2004
consisting of 16 individuals.
individuals The second group, Pos 3 Senaru Group, composed
by 22 individuals was found at the northern side of Segara Anak Lake around 3
km from Pengkereman.
Pengkereman The third groups lived at Pelawangan Sembalun (2700 m
asl), consisting of 8 individuals. The two areas are covered by grass with scattered
pine trees. Since the food trees are very scarce in the area they might be unable to
survive without leftover foods of human
huma beings. It is reasonable to expect that the
tourist.
groups were only recently appeared in the area after recurrent visit of tourist
In September 55, 2004 I found two juveniles with their limbs immersed in
the stream (point B in Fig. II.1) of Pengkereman, while other macaques crossed
the stream by stepping
ing on the stone after foraging leftover food
foods. Those two
macaques stayed in the stream for a few minutes without any motion and soon
moved away. Though observation was very limited it seemed that most other
monkeys did not take much attention to the streams. In this initial sight I have no
thermometer to measure the stream’s temperature but perceptionally I found it
was warm.

8
In this year I could also observed Pos 3 Senaru and Pelawangan Senaru
Group at the observational period (Table II.2). However, no macaques were seen
to enter to the fresh water streams or pool.
Table II.2 Number of groups and individuals of long-tailed macaques in
highland of Mt. Rinjani observed in 2004-2009
Number of Individuals
AM AF SM SF JU IN TO
2
7
0
0
6
1
16
Macaques not appeared in the area
1
8
8
4
0
4
2
26
Macaques not appeared in the area
Pos 3 Senaru
1
4
8
0
1
4
5
22
( no hot spring)
1
2
6
0
0
3
1
12
1
7
12
0
2
6
2
29
1
5
9
0
0
7
3
24
Pelawangan Sembalun
1
2
3
0
0
3
0
8
(no hot spring)
1
2
6
0
0
5
0
13
Not observed
Not observed
Sebau
Not observed
(hot spring)
Not observed
Not observed
2
2
5
0
0
3
1
11
1
2
0
0
2
0
5
Note : AF = adult male, AF = adult female, SM = sub-adult male, SF=sub adult female
JU = juvenile , IN = infant, TO = Total
2008 (1) = observed in April-May 2008, 2008 (2) observed in August 2008
Location
Pengkereman
(hot spring)

Year
2004
2008(1)
2008(2)
2009
2004
2008(1)
2008(2)
2009
2004
2008(1)
2008(2)
2009
2004
2008(1)
2008(2)
2009

No.Group
1

Observation in 2008
I revisited the Pengkereman hot spring site on April 30–May 1, 2008, but
found no monkeys there. At the time no visitor sheltered in the area while the
ambient temperature was cold (see Table II.1) and the pool and stream was covered with cold water overflowed from the Segara Anak Lake (see Table II.1). At
Pos 3 Senaru I found 12 individuals but no monkeys entering the cold water. The
Pelawangan Sembalun Group was found consisting of 13 individuals and they too
did not enter the pool.
In August 19-22, 2008, I visited again the Pengkereman area. I found the
Pengkereman Group and it involved 26 individuals. During the three consecutive
days of observation, I saw the group started their activities from sleeping site
(pine trees, Casuariana junghuhniana Miq.) in southern cliff of Pengkereman area.
They climbed down from the cliff and foraged the leftover foods. They took any
kinds of leftover foods such like cooked-rice, noodle and cassava. After that, some
of them moved to hot-spring pool and/or stream to immerse their bodies in hot
water, while others remained spreading in the area. On the morning of August 20
(10:12-10:25) I found four individuals (two adult males; two adult females)
immersed their bodies completely in the hot-spring pool (Point C in Fig. II.1). In
the second day, August 21, I observed five individuals (an adult male; two adult
females; two juveniles) also immersed their bodies completely in the hot spring
stream (point A) from 08:17-08:25. On August 22, six individuals (two adult

9
males; two sub-adults, two juveniles) again immersed their bodies in the hot
spring pool (point C) from 10:00-10:11. Macaques often jumped down from the
heights of big rocks, swam and/or dived in the hot water. They often played with
or groomed with each other in the hot water. When they took bathe in the hot
water pool (Point C) individuals exhibited various activities including moving,
resting, and aggressive behaviors (drag, bite, chase) as Japanese macaques did in
Jigokudani Monkey Park (Zhang et al. 2007) (Fig. II.3(a)). In the stream (point A),
most individuals immersed their bodies simultaneously and eat remains of human
meal left as garbage inside the hot water ((Fig. II.3(b)). The posture of them as
well as the duration of immersing their bodies into the hot water resemble to
Japanese macaques in the Jigokudani Monkey Park in Japan and human beings
enjoying hot-spring bathing. Thus, in this observation period of 2008 many macaques of Pengkereman Group have already used to enter and immerse themselves
in the hot water stream and pools.
The Pos 3 Senaru group was seen at the same location where they first
found. However, no macaques of the group found to enter fresh water stream. In
this period, I could not found Pelawangan Sembalun group, possibly because of
our time constraint. Another unidentified group, however, was sighted near to the
Pengkereman hot spring area (about one kilometer to the south).
Observation in 2009
I revisited the Pengkereman hot spring on April 21-22, 2009. I found no
monkeys there. I also found no tourist sheltered in the camping site. I could only
found the group of Pos 3 Senaru about 3 kms away from the area. The group consisting of 24 individuals. Here many tourists sheltered.
On March 10-12, 2009, I visited Sebau hot spring. Two groups of longtailed macaques were found in the area. They were five and 11 individuals (Table
II.2), respectively. Those individuals of macaques was not well habituated to
human since they kept distance of more than 15 meters even though I served them
with food. During three days of observation, only human tourists occupied the hot
spring pool (size approximately 3 m x 3 m).

(a)
(b)
Figure II.3 Some postures of individuals during bathing activities in the hot-spring
of Pengkereman area. (a) hot-spring bathing in point C, (b) hot-spring
bathing in point (A)

10
Discussion
Bathing is a commonly observed behavior of long-tailed macaque in the
tropical area. For examples, it was seen in Java (Pangandaran, Cikakak, Solear)
and several places in Bali (Sangeh and Ubud) and Lombok (Suranadi, Gunung
Pengsong and Sekotong) (Islamul Hadi, unpublished data). Fooden (1995) regarded this species as excellent swimmer. All of those activities were recorded in the
lowland. However, hot-spring bathing of long-tailed macaque in lowland and
highland has not been reported yet.
In highland of Mt. Rinjani there are 5 groups of long-tailed macaques (see
Table 2). The area is covered with sparsely distributed shrubs and pine trees that
could not provide enough foods for them. The groups began to forage around the
highland when recurrent tourists visited the area starting from 2003. Macaques
explored the leftover food and this might be the main reason of their presence in
the highland area. Moreover, foods (and/or its leftover) are frequently thrown into
the water of pool and stream
Hot spring bathing of long-tailed macaques seems to appear only recently.
Individuals crossing into hot stream water were first seen in 2004 at Pengkereman.
The hot spring bathing behavior could be driven by their activities in collecting
remains of human meals immersed in shallow hot water pool and stream. Further,
after experiencing the hot water, the behavior could be fixed in some individuals
of the group as the response to the environmental condition, especially to low
ambient temperatures on the highland. The thermoregulation behavior in various
primate populations have been reported, for example, baboons sheltered in cave in
the cold day (Barret et al. 2004). The famous Japanese monkeys in the Jigokudani
Monkey Park also use hot spring bathe more often in winter and less in summer
(Zhang et al. 2007).
The case of Pengkereman macaques may be an innovative behavior since
the behavior is non-universal and occur in low frequency (van Schaik et al. 2006)
and only recently emerge in the population (Reader & Laland 2005). Of those
seven processes underlying innovation (Reader & Laland 2005), exploration and
behavior flexibility may play roles in the emergence of hot spring bathing.
Macaques explored leftover food in hot spring area since the scarcity of natural
food. The immersed food in hot water might attract macaques to enter the hot
spring and experience hot water. Behavioral flexibility in large- and complexbrained taxa, including macaques, might allowed them to modify their behavior
when they exposed to special circumstance (for macaques of Pengkereman Group,
the circumstances are living in highland with low temperatures, scarcity of natural food source and availability of artificial food source in hot spring area). Some
individuals may use the ability to adopt it for their better lives.The adoption
mechanism may include a trigger (that is, food in the hot water) and fixation of
the behavior rewarded by thermoregulation advantages. There are possibilities
that at anywhere the same situation is available the similar innovative behavior
may occur.
In comparison to the Pengkereman Group, I could found two groups live
around hot spring pool of Sebau, 20 km eastern of Pengkereman area at altitude
1380 m asl. They, however, were not showing the hot spring bathing such like the
monkeys of Pengkereman Group. However, the hot spring pool of Sebau is not so

11
wide and there is only one pool available. The pool is occupied intensively by
human. It is very difficult for macaques to share it with human. If, however,
macaques could find food immersed in the hot spring pool and in doing so they
conditionally learn the thermoregulation advantage of the hot water, it can be
expected that individuals of Sebau Group might eventually bath in the hot spring.
Conclussion
I conclude that the hot-spring bathing by long-tailed macaques only found
in Pengkereman Hot-Spring in highland of Mt Rinjani National Park. The behavior is an innovative behavior performed by members of Pengkereman Group. The
behavior emerge because of the macaques is attracted to enter hotspring to obtain
the food. They get nutritional and thermoregulation advantages from hot-spring.
References
Barrett L, Gaynor D, Rendall D, Mitchell D, Henzi SP. 2004. Habitual cave use
and thermoregulation in chacma baboons (Papio hamadryas ursinus).
J Hum Evol 46: 215–222
[BTNGR] Balai Taman Nasional Gunung Rinjani. 2008. Buku Informasi Taman
Nasional Gunung Rinjani (in Indonesian). Mataram (ID): Balai Taman
Nasional Gunung Rinjani. p 1-25
Carpenter A. 1887. Monkeys opening oysters. Nature 36:53.
Fooden J.1976. Provisional classification and key to living species of macaques.
Folia Primatol 25 : 225-236
Hadi I. 2005. Distribution and present status of long-tailed macaques (Macaca
fascicularis) in Lombok Island, Indonesia. Nat Hist J Chula Univ Supl 1:
90
Hadi I, Suryobroto B, Perwitasari D. 2007. Food preference of semi-provisioned
macaques based on feeding duration and foraging party size. Hayati J
Biosci 14 : 13-17
Malaivijitnond S, Lekprayoon C, Tandavanitj N, Panha S, Cheewatham C,
Hamada Y. 2007. Stone-tool usage by Thai long-tailed macaques (Macaca
fascicularis). Am J Primatol 69:227–233.
Minakata K. 1984. Ethnography and Folklore on Monkeys (in Japanese).Tokyo
(JP) : Heibonsha. p 1-364
Nandini R, Narendra BH, 2011. Kajian perubahan curah hujan, suhu dan tipe
iklim pada zone ekosistem di Pulau Lombok (abstract in English). J
Analisis Kebijakan Kehutanan 8: 228-244
Reader SM, Laland KN. 2005. Animal innovation: an introduction. In: Animal
Innovation. Reader SM, Laland KN, editors. New York (US): Oxford
University Pr. p 3-35
Suzuki A. 1964. An ecological study of wild Japanese monkeys in snowy area
focused on their food habits. Primates 6: 31-72.

12
Van der Kraan A. 2009. Lombok: Penaklukan, Penjajahan dan Keterbelakangan.
Supanra MD, translator. Mataram (ID): Lengge. Translation from: Lombok: Conquest, Colonization, and Underdevelopment, 1870-1940. p1-502
Van Schaik CP, van Noordwijk M, Wich, SA. 2006. Innovation in wild Bornean
orangutans (Pongo pygmaeus wurmbii). Behaviour 143: 839 – 876
Zhang P, Tokida E, Watanabe K. 2007. Habitual hotspring bathing by a group of
Japanese macaques, Macaca fuscata, in their natural habitat. Am J Primatol 69: 1425-1430.

13

III
FISH-EATING BEHAVIOR OF LONG-TAILED MACAQUES
OBSERVED FROM PANGANDARAN RECREATION PARK
Abstract
I observed fish-eating behavior performed by long-tailed macaques in
Pangandaran Recreation Park. This behavior firstly observed in group of Rengganis on November, 2010, while three adult females and a sub-adult female ate
fishes obtained from unattended net left in docked boat. Recently the fish-eating
behavior is performed only by individuals of Goa Parat and K12 groups of
Pangandaran Recreational Park. The fish-eating behavior that performed by longtailed macaques in Pangandaran might be newly established as the innovative
behavior. After Asian economical crisis 1998 long-tailed macaques in the
Pangandaran is in condition of nutritional deterioration. This condition affected
number of individuals and groups of long-tailed macaques in the Recreation Park
and also the feeding behavior of the macaques live in park. Decreasing amount of
food from visitors drove the macaques to move their home range like Rengganis
Group or exploit new source in their home range like Goa Parat Group. The
development of fish-eating behavior by individuals of Goa Parat Group could be
the response to the challenge posed by the changing situation of the habitat.
Key words: Pangandaran, long-tailed macaque, Macaca fascicularis, fish-eating,
innovative behavior
Introduction
The long-tailed macaques (Macaca fascicularis) are flexible in their food
choices. They are regarded as frugivorous because in non-provisioned habitats
their diet is dominated by fruit (Hasanbahri et al. 1996; Yeager 1996). In humanaltered places (for example, recreation parks and temples), they tend to be omnivorous by shifting their diet to include food items introduced by human (Wheatly
1989; Son 2003; Hadi et al. 2007).
Macaques have to fulfill their animal protein requirements by catching
small animals like insects, crustacean, bivalves and snails (Fooden 1995). Fish is
not known to be in the list of natural food of macaques until recently the longtailed macaques in Sumatera and Kalimantan were reported to catch and eat live
fish (Stewart et al. 2007). Rhesus macaque (M. mulatta) is also recorded to eat
live fish in Sundarban, India (Majumder et al. 2012). Workers (Stewart et al. 2007
and Majumder et al. 2012) regarded these incidental findings as innovative
behavior. They did not explained the persistence of the behavior in the population.
On the other hand, there was a detailed report on fish-eating behavior by Japanese
macaques (M. fuscata) in Koshima Island (Watanabe 1989). This innovative
behavior was started by peripheral adult males before spreading in the groups. The
behavior is reconfirmed to be persisted in the population by Leca et al. (2007). In

14
addition to macaques, some researchers reported fish eating in chacma baboons
(Papio ursinus; Hamilton & Tilson 1985) and olive baboons (P. anubis; Ransom
1981).
Along the routine work in 2009-2012 on the population monitoring of
long-tailed macaques in Pangandaran Recreation Park we found individuals
consuming various species of fish originally discarded by fishermen. They also
stole fishes from docked boats and from unattended fishing nets. We call this as
“fish-eating behavior”. This behavior seemed to be established recently. Here we
describe the fish-eating as an innovative behavior of the long-tailed macaques in
response to changes in their environment. This innovative behavior may allow
them to add new item into their diet and get nutritional advantage for their
survival.

Methods
Study Site
Pangandaran Nature Reserve i