Primates

, Volume 55, Issue 2, pp 185–188

Responses towards a dying adult group member in a wild New World monkey

Authors

    • Universidade Federal de Pernambuco, Cidade Universitária
    • School of Biological SciencesUniversity of Bristol
  • Matthew Philip Keasey
    • Universidade Federal de Pernambuco, Cidade Universitária
  • Nicola Schiel
    • Universidade Federal Rural de Pernambuco
  • Antonio da Silva Souto
    • Universidade Federal de Pernambuco, Cidade Universitária
News and Perspectives

DOI: 10.1007/s10329-014-0412-8

Cite this article as:
Bezerra, B.M., Keasey, M.P., Schiel, N. et al. Primates (2014) 55: 185. doi:10.1007/s10329-014-0412-8

Abstract

Compassionate caretaking behaviour towards dying adult group members has been reported as being unique to humans and chimpanzees. Here we describe in detail the reaction of a wild dominant male common marmoset, a neotropical primate, to the accidental death of the dominant female of its group. The male exhibited behaviours towards the dying female that resembled those of chimpanzees and humans. The long-term relationship between the dominant pair (which lasted at least 3.5 years) and their social status in the group may have contributed to the male’s behavioural response. The male prevented young individuals from approaching the dying female, behaviour previously observed in chimpanzees. The data provide an interesting insight into compassionate caretaking behaviours in New World primates as well as the pair-bond systems of common marmosets. These are rare observations, and thus their detailed descriptions are essential if we are to create a comparative and enhanced understanding of human and nonhuman primate thanatology.

Keywords

ThanatologyCommon marmosetCompassionate caretaking behaviourSocial bond

Introduction

Animal responses to death include burying the dead body (e.g. rats), consumption (e.g. ants) and displays of sexual and aggressive behaviours towards the carcass (e.g. dolphins) (see Nakamichi et al. 1996 for a review). More complex responses to dying conspecifics have also been reported. For instance, elephants perform helping and investigative behaviour towards dying conspecifics, a phenomenon not restricted to group members (Douglas-Hamilton et al. 2006; Merte et al. 2009). A group of dolphins was recently reported as helping a dying individual to swim (Park et al. 2013). There has been a considerable increase in the number of reports of how nonhuman primates behave in response to the death of group members (Kaplan 1973; Boesch 1991; Nakamichi et al. 1996; Fawcett and Muhumuza 2000; Jiu-Quan et al. 2007; Anderson et al. 2010; Biro et al. 2010; Fashing et al. 2010; Cronin et al. 2011; Stewart et al. 2011). One of these reports even suggests mourning (Anderson et al. 2010). Most of these studies focus on chimpanzee groups, and it has been suggested that chimpanzees and humans are unique in performing compassionate-caretaking behaviours towards dying adult members (Fashing et al. 2010). In chimpanzees, these behaviours include sitting by, prolonged grooming and caressing the dying conspecific (Anderson et al. 2010).

There is very little information on the behavioural responses of Neotropical primates to the death of adult group members. Such observations are usually related to predation, fights and infanticide, with no studies addressing group behaviour towards a dying adult conspecific (e.g. Méndez-Carvajal et al. 2005; Cisneros-Heredia et al. 2005; Bezerra et al. 2007, 2008, Ferrari and Beltrão-Mendes 2011; Pavé et al. 2012). In this study, we describe the reaction of a wild dominant male common marmoset, Callithrix jacchus, to the dying dominant female. We also relate our report to human and nonhuman primates. Our detailed observations could help to expand current knowledge of primate thanatology.

Methods

The observations were made during a study conducted in a 32-ha fragment of Atlantic forest in northeast Brazil (71°56′97″S, 35°11′23″W) (see Souto et al. 2007 for details). The common marmosets in the study site had been monitored since September 2001. The study group consisted of 12 individuals: four adult males, three adult females, three juveniles and two infants (see Online Resource 1 for details). Via ad libitum observation (Altmann 1974), we documented the reaction of the group to the death of its dominant female. The observations were recorded on a video camera, a tape recorder Sony DCR-TRV 120 and a note pad. A video footage is available as Online Resource 2.

Results

The observations were conducted on the 7 February 2005. From the moment the dominant female (F1B) fell from the tree until the time of her death was 153 min. Falling from the tree, the female was injured when her head/body hit a ceramic vase. The most remarkable behaviour during this time came from the dominant male (M1B) (Fig. 1). While F1B was agonizing on the ground, M1B showed five main postural behaviours towards her: embracing, sniffing-like, sitting by, mounting/copulatory movements and watching (see Online Resource 3 for a complete timetable of events). The watching behaviour lasted for periods of up to 20 min. The male also displayed protective (scanning and alarm calling) and aggressive (mobbing) posture against possible predators and unrelated individuals. In such situations, he also uttered alarm 1 and tsik calls (Bezerra and Souto 2008), respectively. The subordinate members of the group only observed the dying female from a distance, having no physical contact with her. M1B, however, left the two infants that he was carrying in a tree canopy before going to the ground to interact with F1B. He also gently mobbed the juveniles that tried to approach F1B on the ground. Her death led to a number of changes in the study group, including the disappearance of one of the infants after 2.5 weeks. Most importantly, M1B disappeared 3–6 months after her death. The events that followed are detailed in Online Resource 4.
https://static-content.springer.com/image/art%3A10.1007%2Fs10329-014-0412-8/MediaObjects/10329_2014_412_Fig1_HTML.jpg
Fig. 1

Observed behaviours to the death of a mate. a Dominant male is vigilant and embracing the injured dominant female; b male embracing and sniffing the female; c male sitting by the female; d female having body spams. (See Online Resources 2 and 3 for video sequence of events and full table with chronology of behaviours. Images obtained directly from video footage)

Discussion

The subordinate group members had no physical contact with the injured dominant female and left the area before her death. On the other hand, M1B stayed in the area for the entire period (>2 h). He also performed several close-contact and caretaking behaviours towards the female, which could indicate some level of compassion. Previous reports of wild dominant female common marmoset deaths have not included intimate and close-contact behaviours by any group member towards a dead or dying individual (Lazaro-Perea et al. 2000). M1B and F1B had been the dominant pair of group since August 2001 (when we first started monitoring the group). This long-term partnership may have been a key factor for the observed events; i.e. the pair bond (and group dominance by the pair) existed for at least a third of the average life expectancy of a wild common marmoset (Ross 1991). Furthermore, considering postpartum estrous in common marmosets (e.g. Dixson 1998), the female could possibly have been pregnant, thus carrying M1B’s new infants. The disappearance of M1B (within ~3 months) and possibly his death followed the loss of F1B (M1B was not observed in any of the surrounding marmoset groups). M1B had no apparent physical injuries prior to or immediately after F1B’s death.

The dominant male prevented the juveniles and infants from approaching the dying female on the ground. In the Thai forest, young chimpanzees were also prevented from approaching an adolescent female that died after a leopard attack (Boesch 1991; Boesch and Boesch-Achermann 2000). Conversely, in wild toque macaques (Macaca sinica), several group members (including juveniles) seem to care for the injured by grooming and cleaning wounds (Dittus and Ratnayeke 1989). Why youngsters are prevented from approaching a dying/dead conspecific in some nonhuman primates is unclear. However, as juvenile common marmosets are independent and mobile (Souto et al. 2007), their protection is unlikely to be the reason M1B blocked their approach to the dying F1B. It thus remains very difficult to evaluate how nonhuman primates perceive death due to the rarity and complexity of such observations.

M1B uttered the alarm 1 call several times during the observation. Common marmosets seem to utter this call in response to aerial predators and usually move to denser vegetation after hearing it (Bezerra and Souto 2008, Bezerra et al. 2011). Intriguingly, the call was uttered when there was no evident aerial predator close to the area. Interpreting the out of context use of this alarm call is difficult. The stressful situation (injured dominant female in the open) could have contributed to M1B uttering calls not necessarily related to their usual context.

Pair-bond formation and maintainance reflects a close social–sexual relationship between male and female common marmosets (e.g. Silva and Sousa 1997; Snowdon and Ziegler 2007). The dominant pair led a relatively stable social group, with a total of eight infants born between August 2001 and February 2005 (unpublished data). The performance of close contact compassionate-caretaking behaviours towards a dying adult fellow group member in nonhuman primates was suggested to be restricted to chimpanzees (Fashing et al. 2010). Nevertheless, our observations suggest that this may not be the case, with the social bonding between the individuals, long-term relations and individual ranking in the group playing major roles on the reaction to a dying conspecific.

Acknowledgments

We thank the reviewers Wolfgang Dittus and Eckhard W. Heymann for valuable comments that improved this manuscript. BMB was funded by a CNPq grant (# 130770/2005) over the course of the marmoset study.

Supplementary material

10329_2014_412_MOESM1_ESM.pdf (63 kb)
Supplementary material 1 (PDF 63 kb)
View video

Supplementary material 2 (MPG 120032 kb)

10329_2014_412_MOESM3_ESM.pdf (62 kb)
Supplementary material 3 (PDF 62 kb)
10329_2014_412_MOESM4_ESM.pdf (44 kb)
Supplementary material 4 (PDF 43 kb)

Copyright information

© Japan Monkey Centre and Springer Japan 2014