Pan Africa NewsThe Newsletter of the Committee for the Careand Conservation of Chimpanzees, and the Mahale
Wildlife Conservation Society
ISSN 1884-751X (print), 1884-7528 (online) mahale.main.jp/PAN/

JUNE 2019
P. A. N. EDITORIAL STAFF

Chief Editor:
Kazuhiko Hosaka, Kamakura Womenʼs University, Japan
Deputy Chief Editor:
Michio Nakamura, Kyoto University, Japan
Associate Editors:
Christophe Boesch, Max-Planck Institute, Germany
Jane Goodall, Jane Goodall Institute, USA
Tetsuro Matsuzawa, Kyoto University, Japan
William C. McGrew, University of St. Andrews, UKJohn C. Mitani, University of Michigan, USA
Vernon Reynolds, Budongo Forest Project, UK
Yukimaru Sugiyama, Kyoto University, Japan
Richard W. Wrangham, Harvard University, USA
Takeshi Furuichi, Kyoto University, Japan
Editorial Secretaries:
Noriko Itoh, Kyoto University, Japan
Koichiro Zamma, Nagano College of Nursing, Japan
Eiji Inoue, Toho University, Japan
Takuya Matsumoto, Research Institute for Humanity and Nature,Japan
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VOL. 26, NO. 1

Contents<NEWS>
International symposium to celebrate 40 years of
research on the Taï chimpanzee
Michio Nakamura				2<NOTE>
A five-year-old chimpanzee ranged alone:
Reconsidering independence in ranging
Michio Nakamura & Hitonaru Nishie		

4<NOTE>
Snare-related disability led to the near-fatal accidentof a bonobo at Wamba, Democratic Republic of the
Congo
Nahoko Tokuyama			7<NOTE>A case of maternal response towards dead offspring inwild bonobos: staring, grooming but not carrying
Shintaro Ishizuka				10Pan Africa News, Vol. 26, No.1
Published in June, 2019
Address: c/o Human Evolution Studies,
Dept. of Zoology, Faculty of Science,
Kyoto Univ., Kyoto, 606-8502, JAPANTEL: (+81)75-753-4108
FAX: (+81)75-753-4115
E-mail: pan.editor@gmail.com
URL: http://mahale.main.jp/PAN/
ISSN: 1884-751X (Print), 1884-7528 (Online)1Pan Africa News, 26(1): 2–3 (2019)

NewsInternational symposium to celebrate 40 years of researchon the Taï chimpanzee
Michio Nakamura
Graduate School of Science, Kyoto University, Japan(E-mail: nakamura@jinrui.zool.kyoto-u.ac.jp)

gave a commemorative lecture to reflect on 40 years of
research at the Taï Chimpanzee Project (Figure 2).
On the morning of the second day, the “Field Site
Comparison” session continued. Drs. Simone Pika,
Michio Nakamura, and David Watts spoke about theirfield sites at Loango (Gabon), Mahale (Tanzania), andNgogo (Uganda). At the end of the session, Dr. Hjalmar
Kühl introduced the Pan African Project, which analyzes
dozens of wild chimpanzee study sites for direct behavioral comparisons.
The subsequent session on second day, entitled“Communication,” was chaired by Dr. Klaus Zuberbühler.
In this session, Drs. Catherine Crockford and Katie
Slocombe presented vocalization studies conducted at
Taï and Budongo. Dr. Julia Fischer presented her work
concerning vocalization studies in green monkeys. The“Cognition” session followed, which was chaired by Dr.
Robert Seyfarth. In this session, Drs. Cedric GirardButtoz and Erica van de Waal presented their field experimental studies of cognition in chimpanzees andvervet monkeys, respectively, while Dr. Daniel Haunpresented his studies of human cognition. The last session on the second day, “Cooperation,” was chaired by Dr.
John Mitani. In this session, Drs. Liran Samuni, KevinAn international symposium to celebrate 40 years of
the wild chimpanzee study project at Taï Forest in Côte
d’Ivoire (see Wittig 2018) was held on May 29–31, 2019 at
the Max Planck Institute for Evolutionary Anthropology,
Leipzig, Germany (Figure 1). The symposium also commemorated the retirement of Dr. Christophe Boesch,
who initiated the research project at Taï, and has served
as Director of the Department of Primatology at the
Max Planck Institute (see Boesch 2009: 2012; Boesch& Boesch-Achermann 2000 for some of Dr. Boesch’s
ach ievement s). Approx i mately 40 spea kers f rom
Germany, Switzerland, USA, UK, and Japan, and guests
from Côte d’Ivoire were invited to the symposium. Many
students from the Max Planck Institute and other institutions, who are studying wild chimpanzees, were also in
attendance.
On May 29, the symposium began with the session “Field Site Comparison,” chaired by Dr. Roman
Wittig. Dr. Wittig, together with Drs. Cat Hobaiter, Anne
Pusey, Dave Morgan, Alexander Piel, Takeshi Furuichi,
and Martin Muller, introduced their study sites in Taï,Budongo (Uganda), Gombe (Tanzania), Goalougo (Congo),
Issa (Tanzania), Kalinzu (Uganda), and Kanyawara(Uganda). At the conclusion of the first day, Dr. Boesch

Figure 1. The Max Planck Institute for Evolutionary Anthropology, Leipzig

2

Pan Africa News, 26(1): 2–3 (2019)

Figure 2. Dr. Christophe Boesch giving a commemorative lecture on May 29

Overall, the symposium was well-organized, andwas an excellent learning and networking experience
with prominent primate researchers across the globe.
Amazingly, most of these eminent scientists are studying
the common topic of chimpanzees in the wild. Notably,“big data” of behavioral and genomic studies on chimpanzees is now available from several long-term study sites.
Such big data, if re-interrogated with new ideas, will provide new insights into our cousin species in the African
forests.
Finally, I should note that, as proposed by Drs.
Boesch and Wittig, the participants signed an appeal forthe conservation of wild chimpanzees, and a press release
was made during the meeting.

Langergraber and Redouan Bshary discussed collaborative behavior in Taï chimpanzees, Ngogo chimpanzees,
and vervet monkeys, respectively.
On May 31, Dr. Richard Wrangham chaired the session “Competition.” Drs. Roman Wittig and Michael
Wilson discussed within- and inter-group competition
among Taï and Gombe/Kanyawara chimpanzees, respectively. Dr. Julia Lehmann presented her work concerning
the role of friendship when competition becomes severe
among Barbary macaques. Finally, Richard McElreath
presented his work concerning competition among humans in different cultures. Dr. Christophe Boesch chaired“Culture,” the second session on the third day. Drs. Lydia
Luncz, Crickette Sanz, and Caroline Schüppli presented
their studies of material culture in Taï and Goualougo
chimpanzees, and in orangutans, respectively. Dr. Ignaciode la Torre presented work concerning early human stone
technology relative to current stone tool use by nonhuman primates. The final session concerned great ape
physiology, genetics, and health, and was chaired by Dr.
Jacinta Beehner. In this session, Drs. Tobias Deschnerand Melissa Emery Thompson discussed the physiologyof Taï and Kanyawara chimpanzees, respectively. Dr.
Linda Vigilant presented her genetic research in the Taï
chimpanzees, and Dr. Fabian Leendertz presented work
concerning great ape health and disease. After these sessions concluded, Dr. Carel van Schaik summarized thesymposium by introducing the outcomes of the questionnaires participants completed during the symposium.

REFERENCES

Boesch C 2009. The Real Chimpanzee: Sex Strategies in theForest. Cambridge University Press, Cambridge.
Boesch C 2012. Wild Cultures: A Comparison between
Chimpanzee and Human Cultures. Cambridge University
Press, Cambridge.
Boesch C, Boesch-Achermann H 2000. The Chimpanzees of
the Taï Forest: Behavioral Ecology and Evolution. Oxford
University Press, Oxford.
Wittig RM 2018. 40 years of research at the Taï Chimpanzee
Project. Pan Afr News 25:16–18.

3

Pan Africa News, 26(1): 4–6 (2019)Note

A five-year-old chimpanzee ranged alone: Reconsidering
independence in ranging
Michio Nakamura1 & Hitonaru Nishie1,2
1 Graduate School of Science, Kyoto University, Japan
2 JSPS Research Fellow, Japan(E-mail: nakamura@jinrui.zool.kyoto-u.ac.jp)

INTRODUCTION

Chimpanzees (Pan troglodytes) have a long period of
dependency when they are immature. Dependence on themother may have various aspects. Infants are dependent
for almost every aspect: nutrition, transportation, hygiene,
and thermoregulation. Nutritional independence seems tobe achieved at around their third year but infants continue
to suckle the nipple to around fourth to fifth year of age(Matsumoto 2017). After weaning, offspring is considered
to enter juvenility. He/she is no more carried by the mother and eats by himself/herself. Still, juveniles are thought
to be dependent in ranging as they are almost always
together with their mothers (Pusey 1983; Hayaki 1988).
Thus, in many studies about chimpanzee ranging behavior or party size, infants and juveniles are “not counted as
independent animals” (Doran 1997).
Even if not the mother, a juvenile still needs somebody to be near. When a juvenile is away from its mother,he/she follows other adults or stays in a larger party(Pusey 1983). In a rare case when a five-year-old juvenile
male was left behind by his mother who emigrated to aneighboring group for ten months, he was almost always
observed to be together with a particular adult male
(Hiraiwa-Hasegawa & Hasegawa 1988). Thus, even when
juveniles are away from mothers, they are still with somebody else and are “virtually never alone” (Pusey 1990).
Orphans are of special interest in terms of dependency on adults (Nakamura et al. 2014). At Mahale, threeyear-old orphans may survive (Nakamura & Hosaka
2015). Such infant orphans are often “adopted” by somenon-mothers (Boesch et al. 2010; Nakamura & Hosaka
2015). Orphans are also dependent on their “adoptive
mothers” to be carried, groomed, or shared the beds with.
Although juvenile orphans are not “adopted” in such away, they usually need to follow someone. Hayaki (1988)
noted that “young orphans seem to need an attachment toa particular individual.” Although such particular partners
were sometimes less obvious (Nakamura & Hosaka 2015),
juvenile orphans had been always observed in a ranging
party containing at least one adult.
Here we report two cases of a five-year-old orphan
female at Mahale who seemed to have ranged completely
alone. These cases may provide us information to reconsider what independence in chimpanzees’ ranging is.

Figure 1. Close-up of Quinoko, a five-year-old orphan
female in 2018zees at the Mahale Mountains National Park, Tanzania
in August and September 2018. The orphaned juvenile inquestion, Quinoko (Figure 1), was born in January 2013,
thus 5 years and 7–8 months old (onset of juvenility) at thetime of the observations. Her mother had died in January
2018 (7–8 months earlier). Her elder sister (born in 2006)
also used to take care of Quinoko in her infancy but had
disappeared (probably emigrated) one month prior to themother’s death. Thus, Quinoko no more had maternal kin
in the M group.

OBSERVATIONS

Case 1
On August 20, 2018, HN and a research assistantwere searching for chimpanzees in the flatter area within
the M group’s home range since morning. They could nothear any vocalizations. At 9:47 h they split into two parties to look for chimpanzees in different locations. Soon,the assistant found Quinoko on a tree. He followed her
for a while as she moved eastward on trees. The assistantgave up following Quinoko when she went off the trail tothe east.
At 10:29 h, H N and the assistant reunited andsearched for other chimpanzees. They could only find two
adult females at 14:39 h at a different place about 1.5 km
from where Quinoko had been witnessed. Judging fromcircumstantial evidence, it seemed that the majority ofchimpanzees were high up in the mountain.

METHODS

Case 2On September 13, 2018, the majority of M-group

The study was conducted on the M group chimpan-

4Pan Africa News, 26(1): 4–6 (2019)

Figure 2. Ranging of Quinoko on September 14, 2018 relative to other chimpanzees’ movement
Quinoko’s travel route is shown in thick black arrow. White circles indicate the locations where she crossed
observation trails. Other chimpanzees’ estimated routes (on 13th and 14th) are shown in dotted grey arrows.
Grey dotted circles indicate estimated locations of vocalizations heard while following Quinoko on 14th. One gridcorresponds to 0.5 km by 0.5 km.

termittently heard, mostly from west. It seems the large
nomadic party was spreading widely and approaching.
Quinoko still moving through trees, headed north to thenorthwest while she replied four times to the vocalizations. At 12:56 h, she was high up in a tree looking at thedirection of the voices. By 13:19 h she was completely
within the range of widespread chimpanzees but still did
not physically meet any.
At 13:26 h, she finally descended to the ground, ran
on the trail, and pant-grunted to an adult male Carter whocame from the west. After this reunion, Quinoko continued to move in this nomadic party until the evening.

chimpanzees went up to the east in the morning. Judging
from the vocalizations, they continued to move southward
in the high mountain on the day (Figure 2, a dotted line to
the right).
On September 14th, MN was heading to where he
can hear vocalizations assuming large party was still on
the mountain. Along the way, at 8:25 h, he found Quinoko
alone on a tree eating Saba comorensis fruits (Figure 2).
As MN followed her, Quinoko moved northward throughtrees, sometimes eating Saba and Pycnanthus angolensis
fruits. At 9:37 h she made a humble bed on a high Cordia
tree and lay down on it (Figure 3). At 9:48 h, chimpanzee
vocalizations were heard from far southeast (still high inthe mountain). Quinoko did not show any response. At
10:00 h she started to move again and ate Saba. She again
rested at 10:39 h. At 11:01 h, chimpanzee calls were heard
again, this time from far south but it seems they climbed
down to flatter area. Soon afterward at 11:03 h, vocalizations came from west-northwest (someone may have preceded the main party). Still, Quinoko did not respond. At
11:13 h, she started to move and ate Saba and Pycnanthus
on the way.
At 12:27 h, many vocalizations came from the west.
This time they were much closer. Quinoko finally vocalized at 12:29 h: a whimper-like “hu hu” then a pant-hootwithout a climax. The other chimpanzees’ calls were in-

DISCUSSION

It is unusual for a five-year-old juvenile to range
alone, even considering that Quinoko was an orphan. In
Case 1, although the observation time was short, it is likely that Quinoko had long been alone because we did notsee other chimpanzees nearby despite a deliberate search.
In Case 2, Quinoko was alone at least for five hours.
Because most chimpanzees had been in the higher area
since the day before, and we found her in the morning, we
believe that she had stayed alone since the day before.
Pusey (1983) noted that one of the reasons why juveniles follow mothers is a need to learn how to find andprocess numerous seasonal and widely dispersed foods.

5Pan Africa News, 26(1): 4–6 (2019)

Figure 3. Quinoko resting
on a high tree

This means juveniles are still dependent because theylack sufficient knowledge for foraging. However, as we
observed in Case 2, Quinoko ate fruits several times anddid not seem to have difficulty in finding and eating fruits.
At this time, Saba and Pycnanthus, both Mahale chimpanzees’ major foods, were beginning to fruit in many
places. Thus in such a season, the demerit of being alone
on foraging may not be so obvious.
Still, Quinoko’s ranging behavior was not completely
same as usual. Notably, she never descended on the
ground while she was alone. In Case 2, she moved around
2 km only through trees. This is unlikely when we follow
an adult chimpanzee ranging alone. Because at Mahale,
tree canopies are often sparse, there seems to be a certain
cost to move a long distance without descending on the
ground. Quinoko actually seemed to incur extra costs todetour to the place where a branch is close to branch of thenext tree or to jump from a tree to the next. It is possiblethat presence of the human observers may be the reason
that she did not descend on ground. However, Quinoko is
not usually so shy and did not show any nervous attitude
toward us or try to flee. Thus, she might rather have hadsome unspecified anxiety.
Despite such possible anxiety, Quinoko never whimpered or made distress calls when she was far from others. This is contrasting to the situation when a similaraged non-orphan gets lost. He/she would loudly whimperand scream and deliberately search for the mother (Hayaki
1988; Matsusaka 2003). An orphan also whimpers when
he/she temporarily loses sight of the chimpanzee whomhe/she is following. This may mean that juvenile chimpanzees do call only when there is somebody close enoughto hear them. It is understandable that a chimpanzee does
not call when he/she is completely alone not to attract
predators.
Although juvenile chimpanzees almost always range
with others, our observations suggest that they can be
independent in some situations. It is unknown whether
Quinoko chose to be alone (because she was harassed byothers, for example) or was accidentally alone (i.e., got
lost) for some reason. She ranged for a long time and did
not seem to have difficulty in finding food. Still, as she
never descended on the ground and kept moving on trees,
it is suggested that ranging alone may cause some anxiety.
This may be a proximate reason that juveniles are virtu-

ally never alone.

ACKNOWLEDGMENTS

We would like to thank the Tanzania Commission for
Science and Technology, the Tanzania Wildlife ResearchInstitute, and the Tanzania National Parks for the permissions
to conduct field research at Mahale. We thank Dr. T. Matsusaka
for comments on the manuscript. The study was supported by
the MEXT/JSPS kakenhi JP15H04429, #4903 JP17H06381,
JP26284138 (to MN), and 17J40059 (to HN).

REFERENCES

Boesch C, Bolé C, Eckhardt N, Boesch H 2010. Altruism inforest chimpanzees: The case of adoption. PLOS One 5:
e8901.
https://doi.org/10.1371/journal.pone.0008901

Doran D 1997. Influence of seasonality on activity patterns,
feeding behavior, ranging and grouping patterns in Taï
chimpanzees. Int J Primatol 18: 183–206.
https://doi.org/10.1023/A:1026368518431

Hayaki H 1988. Association partners of young chimpanzees in the Mahale Mountains National Park, Tanzania.
Primates 29: 147–161.
https://doi.org/10.1007/BF02381119

Hiraiwa-Hasegawa M, Hasegawa T 1988. A case of offspring
desertion by a female chimpanzee and the behavioral
changes of the abandoned offspring. Primates 29: 319–330.
https://doi.org/10.1007/BF02380955

Nakamura M, Hayaki H, Hosaka K, Itoh N, Zamma K 2014.
Orphaned male chimpanzees die young even after weaning. Am J Phys Anthropol 153: 139–143.
https://doi.org/10.1002/ajpa.22411

Nakamura M, Hosaka K 2015. Orphans and allomothering.
In: Mahale Chimpanzees: 50 Years of Research. Nakamura
M, Hosaka K, Itoh N, Zamma K (eds), Cambridge
University Press, Cambridge, pp. 421–432.
Matsumoto T 2017. Developmental changes in feeding
behaviors of infant chimpanzees at Mahale, Tanzania:
Implications for nutritional independence long before
cessation of nipple contact. Am J Phys Anthropol 163:
356–366.
https://doi.org/10.1002/ajpa.23212

Matsusaka T 2003. [Where’s mom?: An episode of a straychimpanzee.] Mahale Chimpun 2: 5–6.
Pusey AE 1983. Mother-offspring relationships in chimpanzees after weaning. Anim Behav 31: 363–377.
https://doi.org/10.1016/S0003-3472(83)80055-4

Pusey AE 1990. Behavioral changes at adolescence in chimpanzees. Behaviour 115: 203–246.
https://doi.org/10.1163/156853990X00581

Received: 23 October 2018
Accepted: 12 March 20196

Pan Africa News, 26(1): 7–9 (2019)

Note

Snare-related disability led to the near-fatal accident of abonobo at Wamba, Democratic Republic of the Congo
Nahoko Tokuyama
Department of Evolutionary Studies of Biosystems, Sokendai, The Graduate University for Advanced Studies, Japan(E-mail: Tokuyama.nahoko@gmail.com)

INTRODUCTION

metallic wire is prohibited. However, metallic wire iseasily available at the local market and some people use
metallic snares because they trap animals more efficiently
than traditional snares. Bonobos in PE group have beenstudied intensively since September 2010, though they had
been sporadically studied earlier. On November 12, 2017,
when this event was observed, PE group consisted of 27
individuals, including five adult males, nine adult females,
and one adolescent female. The event was observed bytrained local field assistants. Teams of two assistants followed the bonobos by working two shifts (morning andafternoon). I interviewed all four assistants in the eveningthat day.
Gai was first identified as an adult male in PE groupin 2007. His upper limbs were greatly deformed and exhibited typical effects of snare injuries (right: claw-handand hooked-wrist, left: second to fourth digits missing
from the second joint, Figure 1, Waller & Reynolds 2001).
His left upper limb had been deformed before we first
identified him in 2007. His right hand was trapped in a
metallic wire in September 2009 and the wire did not
drop off until November 2010 (T Sakamaki personal com-

In places where their home-ranges overlap with humans, chimpanzees and bonobos are frequently caught
in snares made from metallic wire (Kano 1984; Quiatt etal. 2002). Although the victims are generally able to freethemselves by breaking the sapling to which the wire isconnected, they often fail to remove the wire itself. It is
often weeks to months before the wire drops off on its
own or the limb of the victim rots where the wire tightens. Snare injuries may cause serious infections, which
are sometimes fatal (Hashimoto 1999; Boesch & BoeschAchermann 2000). Moreover, the victims often sufferfrom limb loss or deformation (Waller & Reynolds 2001).
Here, I report a near-fatal (had he not been rescued by human observers) accident encountered by a male bonobo
with snare-related limb disabilities.

METHODS

Bonobos have been studied at Wamba in the Luo
Scientific Reserve of the Democratic Republic of Congo
since 1973 (Kano 1992). Although the use of snares madefrom vines or nylon strings is allowed for subsistence
hunting by local people, the use of snares made from a

Figure 1. Upper limb
deformations of Gai
Area inside the white box
shows his left hand from adifferent angle.

7

Pan Africa News, 26(1): 7–9 (2019)
munication). The thumb and remaining parts of the four
digits of his left hand were capable of a certain amountof movement, though clumsily. His right hand and wrist
were stiff and unmovable. Although slower than other individuals, he could climb trees by holding the trunk using
both of his arms.

him. At 06:47 h, an adult male (Malusu) approached Gai
and threatened him by shaking branches and contest hooting. The other bonobos vocalized and Malusu stopped
threatening Gai. At 07:00 h, an adult male (Turkey), two
adult females (Saku and Marie), and a juvenile male
(Hideo) approached Gai and peered at him.
At 07:20 h, the field assistants judged that Gai could
not get out from the gap by himself and they started cutting down the tree to rescue him. Two adult males (Turkey
and Snare) approached and threatened the assistants byshaking branches and barking, and the field assistants
scared the males off by shouting loudly. The entire partyof bonobos moved several dozen meters away. At 07:24 h,
the tree was cut down to the ground and Gai freed himself
from the gap and ran away.
At 07:34 h, the party of bonobos came back to where
Gai had been caught. After one or two minutes, thebonobos moved about 50 m away and started resting andgrooming on trees. All of the PE group individuals wereobserved there except for Gai. At 09:41 h, two adult males(Turkey and Ikura) and a juvenile male (Kale) moved towhere Gai had been caught. At 09:43 h, an adult female(Marie) and a subadult female (Lucie) joined the males.
At 09:44 h, all of the bonobos climbed down from thetrees and started traveling. The field assistants followed
the bonobos but lost them at 11:10 h because of their quickpace.
At 14:15 h, the afternoon team of field assistants observed Gai walking alone on the ground. He fled from theassistants and was not observed again until December 2,
2017 (19 days).

OBSERVATIONS

November 11, 2017
Two field assistants and I followed a large party ofbonobos from 05:55 h. We observed all PE individuals,
but lost them at 09:47 h due to heavy rain.
November 12, 2017
The morning team of field assistants started searchingfor bonobos at 06:00 h and located them at 06:34 h. The
bonobos had gathered at one place and were vocalizing
loudly. The assistants soon noticed that Gai was stuck ina tree at a height of about 3 m. His left wrist was caught
in a narrow gap where the tree trunk branched into two(Figure 2). The tree trunk and the two branches wereabout 20, 15, and 8 cm in diameter, respectively. Because
his right hand was not capable of gripping, he could not
lift his body high enough to free himself from the gap.
There were multiple teeth marks on the branches (Figure2) and the vines around him were bitten through. Judging
from the fruits of Landolphia sp. scattered on the ground,the bonobos had fed there on the afternoon of November
11. No new night beds were found nearby.
Gai seemed to be exhausted. The other bonobos werein the trees around Gai and making loud calls intermittently. At 06:34 h, when the assistants found the bonobos,
an adult male (Snare) and three adult females (Bokuta,
Maluta, and Nara) were sitting close to Gai and peering at

December 2, 2017
Gai was observed in a party of PE group at 11:23 h.

Figure 2. Tree in which Gai was trapped.
Field assistant, Iyokango Bahanande, demonstrates how Gai was trapped in the gap between the branches. Although
the assistant is putting his right arm in the gap, Gai was trapped by his left arm. Teeth marks on the branches can be
seen.

8

Pan Africa News, 26(1): 7–9 (2019)
for bonobos re-visiting these injured individuals. First,
bonobos might care about the injured or immobilized
individuals. Although the bonobos leave the injured individuals to feed or to find appropriate bed sites, they mightcome back at a later time to check on the condition of the
injured individuals. The other possibility is that bonobos
just tend to be drawn to irregular events. Bonobos sometimes gather around trapped animals, dugout canoes that
local people make in the forest, and so on. In such cases,
bonobos often approach, peer, touch, and shake branches
toward the objects (Hayashi et al. 2012; N Tokuyama
personal observation). Bonobos also sometimes re-visit
the place of an unusual event after a few hours or days (NTokuyama personal observations). Although it is difficult
to understand the motivation for bonobos re-visiting andgathering around Gai, this case may contribute to our insight into the behavioral characteristics and emotions ofwild bonobos.

Figure 3. Injuries on the inside and outside of Gai’s left
wrist
Photos were taken on December 12, 30 days after theaccident.

All individuals except Gai had been observed daily between November 12 and December 2, suggesting thatGai was ranging alone during this period. He had severe
abraded wounds on the inside and outside of his left wrist(Figure 3) but showed no apparent signs of debility.

ACKNOWLEDGMENTS

I sincerely thank the field assistants for sharing their detailed account and precious information, as well as for rescuing
Gai. I thank the Research Center for Ecology and Forestry and
Ministry of Scientific Research, DRC for supporting my fieldresearch. I am also grateful to Dr. Tetsuya Sakamaki and Dr.
Takeshi Furuichi for their information and discussions. I also
thank Dr. Gaku Ohashi for his helphul comments and suggestions, and Dr. Kirsty Graham for proofreading my English writing. This study was financially supported by the Japan Society
for the Promotion of Science Grant-in-Aid for JSPS Research
Fellow (JP17J06911).

DISCUSSION

Based on indirect evidence, Gai might have been
trapped in the gap of the branches when he was climbing down after eating Landolphia sp. on the afternoon ofNovember 11. The branches could have been more slippery than usual because of heavy rain in the morning ofthat day. The teeth marks on the branches and chewed
vines around him indicated that he had been struggling
to free himself. He seemed to be already exhausted when
the field assistants found him early in the morning on
November 12. Without their rescue, Gai might have eventually died. After surviving the initial infection, snare
injuries had been considered to give minimal effect on an
individuals’ survival (Kano 1984; Stokes 1999). However,the current case shows that snare injuries can cause serious accidents even years after the original injury. It is
important for researchers and governments to perceive theongoing risk of snare injuries and make further effort toraise awareness in local communities.
During the incident, the other group members gathered around Gai and were vocalizing loudly. Although
they did not show any apparent behavior that would help
Gai to free himself from the gap in the branches, somebonobos approached and peered at him. A male behaved
aggressively toward Gai, but he stopped when other bonobos vocalized toward them. There were no night beds
around Gai, which indicates that Gai spent the night ofNovember 11 by himself. After Gai had become trapped,
other bonobos might have left Gai in the afternoon ofNovember 11 and then come back early in the morning ofNovember 12. I have observed a very similar case in thesame group in 2011 (Tokuyama et al. 2012). An adult male
was caught in a snare. The other members of the party left
him in the evening, but the next morning, they travelledback to where he had been trapped.
Two possibilities are considered to be the motivation

REFERENCES

Boesch C, Boesch-Achermann H 2000. The Chimpanzeesof the Taï Forest: Behavioural Ecology and Evolution.
Oxford University Press, New York.
Hashimoto C 1999. Snare injuries of chimpanzees in the
Kalinzu Forest, Uganda. Pan Afr News 6: 20–22.
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Hayashi M, Ohashi G, Ryu H 2012. Responses toward a
trapped animal by wild bonobos at Wamba. Anim Cogn 15:
731–735.
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Kano T 1984. Observations of physical abnormalities among
the wild bonobos (Pan paniscus) of Wamba, Zaire. Am J
Phys Anthropol 63: 1–11.
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Kano T 1992. The Last Ape: Pygmy Chimpanzee Behavior
and Ecology. Stanford University Press, Stanford.
Quiatt D, Reynolds V, Stokes EJ 2002. Snare injuries tochimpanzees (Pan troglodytes) at 10 study sites in east andwest Africa. Afr J Ecol 40: 303–305.
https://doi.org/10.1046/j.1365-2028.2002.00356.x

Stokes EJ 1999. Feeding Skills and the Effect of Injury on
Wild Chimpanzees. PhD thesis, Universty of St. Andrews,
St. Andrews.
Tokuyama N, Emikey B, Bafike B, Isolumbo B, Iyokango
B, Mulavwa MN, Furuichi T 2012. Bonobos apparently
search for a lost member injured by a snare. Primates 53:
215–219.
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Waller JC, Reynolds V 2001. Limb injuries resulting fromsnares and traps in chimpanzees (Pan troglodytes schweinfurthii) of the Budongo Forest, Uganda. Primates 42:
135–139.
https://doi.org/10.1007/BF02558140

Received: 31 January 2019
Accepted: 12 March 20199

Pan Africa News, 26(1): 10–12 (2019)

Note

A case of maternal response towards dead offspring in wildbonobos: Staring, grooming but not carrying
Shintaro Ishizuka1,2
1 Primate Research Institute, Kyoto University
2 Japan Society for Promotion of Science(E-mail: ishizuka.shintaro.37x@kyoto-u.jp)

INTRODUCTION

Comparative thanatology is a research branch thatscientifically studies death from various perspectives,
such as ethologically, physiologically, or psychologically.
Research on animal behaviors has been particularly focused on how animals respond to dead conspecifics (reviewed in Goncalves & Biro 2018). In two species of thegenus Pan, one of the most well-known responses towards
dead conspecifics is the carrying of dead offspring by
their mothers. It has been reported that mother chimpanzees (Pan troglodytes) have carried their dead infants in
Mahale, Bossou, Tai, and Gombe (Nishida 1973; Hosaka
et al. 2000; Kooriyama 2009; Matsuzawa 1997; Biro etal. 2010; Boesch & Boesch-Achermann 2000; Goodall1968). However, in bonobos (Pan paniscus), there are only
a few available reports that mothers also carry their deadoffspring (Kano 1992; Sakamaki personal communication). Another type of response by mother bonobos is theeating of the corpses of their dead infants after they carried the corpses (Fowler & Hohmann 2010; Tokuyama etal. 2017). These reports suggest that there is variation in
the responses of mothers towards their dead offspring inbonobos, whereas our understanding of such responses
is still scarce due to the limited number of observational
cases. That is why more observational reports are required for a better understanding of the responses towards
dead conspecifics in the genus Pan. Here we report a newcase of maternal response towards dead offspring in wildbonobos.

METHODS

The study subjects were a group of wild bonobos(called the PW group) at Wamba, the Democratic Republicof the Congo (Kano 1992). In 2010, two groups of wildbonobos were recognized around the area previously usedby the P group. One of the two groups was named the “PWgroup”. All individuals of this group have been identiﬁed
since 2012. In 2014, this group consisted of 14 individuals,
including ﬁve adult/adolescent males and four females,
which were estimated as immigrant and parous during
the observation period. Field research concerning the PW
group has been carried out sporadically since 2011 (almost once per month). Two local assistants and I followed
a mother bonobo, Rebekka (Rb), and her daughter, Rida
(Rd), on January 13 and 14, 2016. At the time of observation, Rb was estimated to be 13 years old. Rd was born in2015 and estimated to be first offspring of Rb.

OBSERVATIONSJanuary 13, 2016
We found Rb and Rd in bed within the canopy at
6:56 h. Rb coughed frequently and Rd appeared limp,
although Rd still clung to the body of Rb, suggestingthat both of them were unwell. When we found them, noother members of the PW group were nearby. Although
Rb sometimes fed on fruits of Musanga cecropioides, shespent most of her time resting in the canopy.
At 10:26 h, Rb climbed down to the ground. Suddenly,
Rb put the body of Rd on the ground. Rd screamed several times, while Rb kept about a 2 m distance from Rd andstayed motionless on the ground. At 10:36 h, Rb began tocarry Rd again. They both returned to the canopy.
At 10:55 h, Rb climbed down to the ground again, andstarted to move around. At 11:08 h, Rb put the body of
Rd on the ground again, then watched Rd from a branchapproximately 2 m above the ground. At 11:18 h, Rb began to carry the body of Rd again and climbed up to the
canopy.
At 13:28 h, we realized that Rd did not cling to thebody of Rb, although Rb still held the body of Rd. At thistime, Rd might have already been dead. At 13:45 h, Rb
dropped the body of Rd, then climbed down to a position about 2 m from the corpse. Rb stared at the corpse
while drinking water. Rb stayed near the corpse of Rd
but returned to the canopy at 14:00 h, without carrying
the corpse. At 15:00 h, we finished the observations, but
before leaving we changed the posture of Rd to take aphotograph.
January 14, 2016
We found Rb and the corpse of Rd at 6:56 h, at thesame place where observations from the previous day hadfinished. Rb coughed often and seemed to still be unwell.
As on the previous day, Rb sometimes fed on fruits ofMusanga cecropioides but spent most of her time resting.
At 9:03 h, Rb climbed down to the ground and visitedthe corpse of Rd. Rb touched the corpse gently, grooming
it for a few seconds. Rb stayed with the corpse until 9:11 h,
before finally returning to the canopy.
At 12:25 h, Rb visited the corpse of Rd again. Rb
started to groom the corpse (Figure 1). After Rb continued grooming for about one minute, she stopped and returned to the canopy (at 12:26 h).
At 13:30 h, members of the PW group appeared
around Rb and the corpse of Rd. Rb joined the membersof the group and started to range with them. Finally, Rb

10Pan Africa News, 26(1): 10–12 (2019)
possible reason for this may be that the dead offspring
was her first offspring. Because her experience in maternal care was relatively short, carrying offspring might not
be natural for Rb compared to other mothers who carried
their dead offspring in the genus Pan. Another possible
reason may be that her illness was too serious to permit
her to carry the corpse. After she went to the corpse forthe first time, she still coughed often and appeared to be
unwell. Moreover, because Rd had been already dead at
the time, the energetic costs for carrying must have been
larger than when the infant had been alive. It might havebeen too hard for Rb to carry the corpse at the time.
Although female bonobos are highly gregarious(Furuichi 2011), Rb stayed alone after we started observations at 6:56 h on January 13, until members of her group
visited her at 13:30 h on January 14. When members ofbonobo groups become seriously unwell, they may stay bythemselves. However, members of the group came to theplace where Rb was staying, suggesting that they might
have been searching for Rb and Rd. A similar case has
been reported where members of a bonobo group returned
to an individual captured by an artificial snare (Tokuyama
et al. 2012). If any member of a bonobo group cannot follow the other members for several reasons, the group may
search for the individual rather than abandoning it.
In chimpanzees, it has been recognized that mothers
often carry their dead infants. However, this report suggests that mother bonobos may not be strongly engaged incarrying their dead infants. This implies potential interspecies differences in maternal response towards deadoffspring in the genus Pan. For a better understanding ofsuch differences, more observational reports are needed inboth species.

Figure 1. Rb groomed her dead infant

left the corpse of Rd. Following the appearance of theother members of the PW group, neither they nor Rb responded at all towards the corpse, and eventually left. We
followed the party, including Rb, and finished the observations at 15:00 h.

DISCUSSION

Previous repor ts on non-human primates haveshown that mothers have continued to carry the bodies of their offspring (reviewed in Watson & Matsuzawa
2018; Goncalves & Carvalho 2019), whereas it is unclear
whether Rb carried her dead infant until she released
the corpse of Rd from the canopy. In this report, it was
confirmed that Rd was alive at 11:18 h and her corpse
was dropped at 13:45 h during the same day. This meansthat her corpse might be carried for a maximum of approximately 2 hours. This possible duration of carrying issimilar to those reported in bonobos (Fowler & Hohmann2010; Tokuyama et al. 2017). However, it is shorter thanthose reported in chimpanzees. For example, in Bossou, amother chimpanzee carried her dead offspring for 27 days
and groomed it regularly (Biro et al. 2010). In Mahale, amother chimpanzee carried her dead infant for at least 111
days (Hosaka et al. 2000). Although the number of available data is still scarce, duration of maternal carriage of
their dead offspring may be longer in chimpanzees than inbonobos. This may be because female bonobos are moresocial than female chimpanzees (Kano 1992; Furuichi
2009; Surbeck et al. 2017). Mother bonobos may choose
to leave their dead offspring in order to perform intensesocial interactions with other alive conspecifics.
After the corpse of Rd was dropped down, Rb returned to the corpse at least twice. Although it is unclear
whether she recognized the death of her offspring, at least
she had remembered about her until the time of the second visit to the corpse. Moreover, Rb groomed her deadinfant during these visits. This behavior may be maternalcare which is sometimes continued after the death of her
infant, as it is observed in various species of primates(reviewed in Watson & Matsuzawa 2018). On the otherhands, the number of her grooming opportunities was
only twice and she did not carry the corpse again. One

ACKNOWLEDGEMENTS

I thank the Research Centre for Ecology and Forestry andthe Ministry of Scientific Research, Democratic Republic of theCongo for permitting our research. I also thank Dr. T. Furuichi,
Dr. T. Sakamaki, and local assistants at Wamba for helps in myfieldworks, and Mr. A. Goncalves for valuable comments on
my manuscript, and Mr. J. A. Pastrana for helps in my English
writing, and Dr. K. Hosaka for reviewing and providing helpfulcomments on my manuscript. This study was financially supported by Japan Society for the Promotion of Science Grantin-aid for JSPS fellows (17J09827 to Shintaro Ishizuka), andthe Leading Graduate Program in Primatology and Wildlife
Science of Kyoto University.

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Received: 13 April 2019
Accepted: 15 May 201912