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 inMahale, Bossou, Tai, and Gombe (Nishida 1973; Hosakaet 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 ofRd 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 thecanopy.
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, Rb10

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 (Tokuyamaet al. 2012). If any member of a bonobo group cannot follow the other members for several reasons, the group maysearch 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 wasconfirmed 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. OneACKNOWLEDGEMENTS

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