Is birth attendance a uniquely human feature? New evidence suggests that Bonobo females protect and support the parturient
Introduction
Birth assistance has been proposed as a distinctive human trait and it has been related to the difficult delivery process in our species (Rosenberg & Trevathan, 2002; Wittman & Wall, 2007). At the basis of the long, painful and unsafe delivery in humans lays the strict relationship between the size of maternal birth canal - determined by the anatomy of pelvic bones - and the size of neonatal head (Trevathan, 2011). In the course of the hominin evolutionary lineage, the pelvis anatomy changed over time in response to different selective pressures connected to bipedal locomotion and childbirth (Trevathan, 2015), with other ecological factors playing an important role (Wells, DeSilva, & Stock, 2012). In particular, the “bipedalism-encephalization conflict” has been thought to be the reason of the extreme altriciality of our neonates and was labelled by Washburn (1960) as the human obstetric dilemma. Although recent studies highlighted the role of other physiological mechanisms in determining the timing of delivery in Homo sapiens (Dunsworth, Warrener, Deacon, Ellison, & Pontzer, 2012), the general idea behind Washburn's obstetric dilemma remains reliable, as sadly confirmed by the rate of maternal and neonatal mortality due to obstructed labour in our species (World Health Organization, 2005). In addition to this size relationship, human parturition is mechanically difficult also because the birth canal has a twisted shape that produces a unique pattern of rotational birth (Trevathan, 2011). Indeed, human infants are typically born facing away from the mother (i.e. occiput anterior) and this position makes it problematic for the mother to use her hands to facilitate the expulsion. The obstetric dilemma and the occiput anterior presentation are thought to represent the biological foundation of birth attendance in humans. According to this view, the outcome of the evolutionary history of human childbirth resulted in a sort of “obligate midwifery”, with attendants being present to support the mother and facilitate the delivery (Rosenberg & Trevathan, 2002; Trevathan, 2015). Although the notion of “obligate midwifery” is widely accepted in the biomedical and anthropological literature (Dundes, 2003; Weiner, Monge, & Mann, 2008), there is still much debate about the species in which this pattern emerged due to the rarity of hominin female fossil pelvis and the variety of factors determining pelvis anatomy (for an extensive review see Gruss & Schmitt, 2015). It is not the goal of this paper to revisit this disputed argument that it is beyond our area of expertise, we just aim to add another point of discussion by drawing the attention towards the process of parturition in one of our closest living relative.
Humans differ from their closest living relatives in their need for assistance during delivery (Brandt & Mitchell, 1971). The more favourable relationship between the dimensions of the maternal birth canal and neonatal head size in nonhuman primates results in less difficult and more rapid deliveries and this is particularly true for great ape species in which infants are small in relation to maternal body size (Rosenberg & Trevathan, 2002). The typical mode of neonatal emergence from the birth canal in nonhuman primates seems to be the occiput posterior (i.e. the infant is born facing the mother's ventrum), which enables nonhuman primate parturients to hold and pull the infant out by themselves, making the mother self-sufficient in achieving the delivery (Trevathan, 2011; but see Hirata, Fuwa, Sugama, Kusunoki, & Takeshita, 2011).
All primates are social animals but the composition of primate social groups and the extent of social interactions differ considerably from species to species (Fleagle, 2013) and this certainly reflects on the moment of parturition. According to the species and the inter-individual relationships, females might give birth in isolation or within their social group and, in the latter case, the type and extent of social interactions with other group members could greatly vary, as confirmed by the available studies describing parturition in nonhuman primates (isolation: Duboscq, Neumann, Perwitasari-Farajallah, & Engelhardt, 2008; Nowak, Porter, Lévy, Orgeur, & Schaal, 2000; Starin, 1988; within group without social interactions: Kinnaird, 1990; Peker, Kowalewski, Pavé, & Zunino, 2009; Turner et al., 2010; Windfelder, 2000; within group with extensive social interactions: Ding, Yang, & Xiao, 2013; Douglas, 2014; Pan et al., 2014). There are several factors determining this paucity of observations. In diurnal species deliveries usually occur at night, thus making their observation very difficult (Jolly, 1972). In the wild, mothers may seek safe/hidden places, thus increasing the difficulty in following the deliveries, whereas in captivity mothers can be separated from their group for veterinary reasons, thereby precluding the possibility of investigating the social dynamics occurring during birth.
It is currently impossible to draw conclusions on the extent of birth sociality in nonhuman primates due to the absence of multiple reports on the same species that does not permit to comprehend whether some forms of social support are present/recurrent in species other than humans. Such an approach is essential to control for the high individual behavioural variability and to link the results to the social characteristics of the species.
Here, we present the first quantitative analysis on the social dynamics during three daytime births in captive bonobos. The bonobo (Pan paniscus), together with the chimpanzee (Pan troglodytes), is the closest living human relative (Prüfer et al., 2012). Both Pan species live in a fission-fusion social system, meaning that they live in large social groups, so-called communities, that can count up to 150 individuals (for an extensive review see Boesch, Hohmann, & Marchant, 2002). Individuals of the same community typically split to form sub-groups, so-called parties, whose composition changes over time (Boesch et al., 2002). Although the social system is the same, compared to chimpanzees, bonobos show a much higher degree of cohesiveness, with different parties ranging in adjacent areas and travelling in the same direction (Furuichi, 2009). Bonobos and chimpanzees are both characterized by male philopatry and female dispersal (Kano, 1992) and this leads to a higher degree of relatedness between males than between females (White, 1996). According to the principle of kin-selection (Hamilton, 1964), a higher level of cooperation among males should characterize both Pan species. However, this is not the case. Whereas chimpanzees follow this general biological rule (Morin et al., 1994), bonobos represent a well-known exception with females showing a higher degree of cohesiveness, alliances and support than males (Surbeck, Mundry, & Hohmann, 2011; Tokuyama & Furuichi, 2016). These strong relationships provide unrelated females with the ability and the potential to be dominant over males (Furuichi, 2011; Gruber & Clay, 2016). Moreover, it seems that female gregariousness, together with a relaxed feeding competition, allowed bonobos to evolve as a less aggressive and more tolerant species compared to chimpanzees (de Waal & Lanting, 1997; Furuichi, 2011; Hare, Wobber, & Wrangham, 2012; Kano, 1992; Palagi, Paoli, & Borgognini Tarli, 2006).
With regard to bonobo births, only four births have been reported in captivity (Bolser & Savage-Rumbaugh, 1989; Kirchshofer, 1963; van Elsacker, Vervaecke, Walraven, & Verheyen, 1993) and one in the wild (Douglas, 2014), but in such studies the description of the social environment is either missing because the mother was isolated from other group members by the zoo staff (Bolser & Savage-Rumbaugh, 1989; Kirchshofer, 1963) or it is qualitatively described (Douglas, 2014; van Elsacker et al., 1993).
In this study, first we will test some hypotheses to understand if birth in bonobos shares some of the general elements characterizing traditional birthing practices in humans. The results obtained on bonobos will be then discussed through a comparative approach focussed on the two Pan species and on humans. Our study aims at contributing to the current debate on the evolutionary origin of “midwifery” questioning whether birth attendance could have been already present before the evolutionary emergence of the “obligation” of assistance.
Review of the cross-cultural literature reveals that giving birth in presence of others is almost a human universal (Newton & Newton, 2003; Schiefenhövel, 1983). There are few exceptions to this universal pattern, as in the case of the !Kung population of South Africa where the concept of isolated birth represents a cultural ideal linked to the high symbolic value attributed to personal courage (Shostak, 2014). Also by the !Kung, however, isolated birth is a rarely achieved ideal, especially for women giving birth for the first time (Konner & Shostak, 1987).
If bonobo parturients prefer to give birth in presence of others, we predict that they should not tend to isolate themselves from the rest of the group (Prediction 1a). Moreover, if a social interest towards the parturient is shown also by bonobos, we predict that group members should gather around the mother during the hours of delivery compared to other days (Prediction 1b).
In humans, birth attendance is typically undertaken by women who provide emotional and psychological support to the mother and who are generally her friends or kin (Cosminsky, 2003; Ford, 1945; Newton & Newton, 2003). Bonobo females establish strong and long-lasting affiliative bonds, even though they are not closely related (Furuichi, 2011; Tokuyama & Furuichi, 2016). If bonding also plays a role during the delivery in bonobos, we predict that females should stay in closer proximity to the parturient (≤1 m, including physical contact, Prediction 2) and display higher levels of behavioural expression of arousal than males (Prediction 3).
During delivery, bonobo bystander females could be attracted by three different elements: the mother, the placenta and the newborn. If close proximity is a parturient-oriented behaviour, we predict that female cohesiveness should be higher in the first phase of the delivery, before the baby is born and the placenta is expulsed (Prediction 4).
In humans, birth attendants are in charge of protecting the mother and the newborn from a great variety of both real and symbolic dangers, such as attacks of wild animals (Konner & Shostak, 1987), physical injuries or negative supernatural forces (Dundes, 2003). Also the common exclusion of men from birthing practices may reflect a form of protection, given that men are often very anxious and apprehensive and this could perturb the mother (Glazer, 1989).
Bonobo females form coalitions and alliances to support and defend each other (Furuichi, 2011; Parish, 1994; Tokuyama & Furuichi, 2016). During the delivery, the parturient is highly vulnerable and could be easily attacked if left alone. Therefore, we predict that female bystanders can stay in proximity of the labouring female to protect her from possible threats (Prediction 5).
Traditional birth attendants in humans are generally multiparous and elderly women (Ford, 1945), thus suggesting that personal experience is essential for the formal recognition of this role by the community. The practical support of birth attendants can include checking of genitals and contractions, providing hygienic care, physically sustaining the mother and helping her by holding the baby during the expulsive phase (World Health Organization, 1996).
Accordingly, in bonobos, we predict that female attendants should engage in i) monitoring by visual and tactile inspection of the mother's genitals, ii) keeping the parturient's genital area clean and iii) practically helping the mother during the expulsive phase by holding the infant if necessary. Further, if such practical support is parturient-oriented, all these activities should be concentrated during the first phase of the delivery when the placenta is not present and the infant has not been born yet.
Section snippets
Study groups and data collection
Observations of births were made during a long-term research project spanning several months on the behaviour of captive bonobos (Pan paniscus) in two European primate parks. In the Apenheul Primate Park (Apeldoorn, The Netherlands) data collection covered the period August–October 2009 (individual Focal Animal Sampling = 25 h; All Occurrences Sampling = 502 h). At La Vallée des Singes (Romagne, France) data collections were performed in the periods June–August 2012 (individual Focal Animal
Spatial proximity to the parturient
The three bonobo parturients did not show any attempt to isolate themselves from the rest of the group and the two females that had access to both indoor and outdoor facilities chose to give birth indoor (Prediction 1a supported).
To examine whether the delivery caused a change in the social dynamics of the group around the mothers, we selected the same time slot corresponding to that of each delivery for both the day before and after. We compared the spatial proximity (≤2 m) between each group
Discussion
Our results show that birth in bonobos shares some elements with traditional birth attendance in humans (i.e., spatial proximity to the parturient, female birth attendants, control and protection, emotional engagement and practical support - World Health Organization, 1996).
Our observations seem to confirm that, similarly to the only birth reported in the wild (Douglas, 2014), parturients in bonobos do not have the tendency of isolating themselves and they well accept the presence of other
Conclusions
Our results on bonobos question the traditional view that the “obligatory” need for assistance was the main driving force leading to sociality around birth in our species (Trevathan, 2011). Indeed, bonobo females stay in proximity to the parturient, support and protect her, even if birth in this species is not hindered by physical constraints and the mother is self-sufficient in accomplishing the delivery. We suggest that the similarities observed between birth attendance in bonobos and humans
Ethic statement
This study was purely observational (with no manipulation whatsoever) and bonobos were observed and filmed with the permission of the directors of the parks. Thus, the ethics committee of the University of Parma (Animal Care and Use board) waived the need for a permit.
Acknowledgements
We wish to thank the directors and the keepers of the bonobo colonies at the Apenheul Primate Park (Apeldoorn, the Netherlands) and La Vallée des Singes (Romagne, France) for allowing and facilitating data collection; Francesca Coppola and Francesca Bertolottifor their assistance in data collection; GladezShorland for sharing information; Lynne Murray for her critical revision of an early version of the manuscript.
References (81)
- et al.
Measuring and testing the steepness of dominance hierarchies
Animal Behaviour
(2006) - et al.
Daytime birth and parturition assistant behavior in wild black-and-white snub-nosed monkeys (Rhinopithecusbieti) Yunnan, China
Behavioural Processes
(2013) - et al.
Daytime birth of a baby crested black macaque (Macaca nigra) in the wild
Behavioural Processes
(2008) The genetical evolution of social behaviour. II
Journal of Theoretical Biology
(1964)- et al.
The self-domestication hypothesis: Evolution of bonobo psychology is due to selection against aggression
Animal Behaviour
(2012) - et al.
Can you believe my eyes? The importance of interobserver reliability statistics in observations of animal behaviour
Animal Behaviour
(2009) Sex and food control in the “uncommon chimpanzee”: How bonobo females overcome a phylogenetic legacy of male dominance
Ethology and Sociobiology
(1994)- et al.
Birth, obstetrics and human evolution
BJOG
(2002) - et al.
Male reproductive skew is higher in bonobos than chimpanzees
Current Biology
(2017) - et al.
Do friends help each other? Patterns of female coalition formation in wild bonobos at Wamba
Animal Behaviour
(2016)
Female-led infanticide in wild chimpanzees
Current Biology
Bipedalism and parturition: An evolutionary imperative for cesarean delivery?
Clinics in Perinatology
Observational study of behavior sampling methods
Behaviour
Post-conflict behaviour of wild chimpanzees (Pan troglodytes schweinfurthii) in the Budongo Forest, Uganda
Behaviour
Periparturitionalbehavior of a bonobo (Pan paniscus)
American Journal of Primatology
Parturition in primates: Behavior related to birth
Cross-cultural perspectives on midwifery
The communicative repertoire of captive bonobos (Pan paniscus), compared to that of chimpanzees
Behaviour
Bonobo the forgotten ape
Reconciliation and consolation among chimpanzees
Behavioral Ecology and Sociobiology
Emotionality and intentionality in bonobo playful communication
Animal Cognition
Female sociality during the daytime birth of a wild bonobo at LuiKotale, Democratic Republic of the Congo
Primates
Metabolic hypothesis for human altriciality
Proceedings of the National Academy of Sciences
Human ethology
Primate adaptation and evolution
The complete capuchin: The biology of the genus Cebus
Placentophagy in wild chimpanzees (Pan troglodytes verus) at Bossou, Guinea
Primates
Agonistic interactions and matrifocal dominance rank of wild bonobos (Pan paniscus) at Wamba
International Journal of Primatology
Factors underlying party size differences between chimpanzees and bonobos: A review and hypotheses for future study
Primates
Female contributions to the peaceful nature of bonobo society
Evolutionary Anthropology
Anxiety and stressors of expectant fathers
Western Journal of Nursing Research
An observed birth in a free-living chimpanzee (Pan troglodytes schweinfurthii) in Gombe National Park, Tanzania
Primates
A comparison between bonobos and chimpanzees: A review and update
Evolutionary Anthropology
The evolution of the human pelvis: Changing adaptations to bipedalism, obstetrics and thermoregulation
Philosophical Transactions of the Royal Society B
New records of within-group infanticide and cannibalism in wild chimpanzees
Primates
Mechanism of birth in chimpanzees: Humans are not unique among primates
Biology Letters
Intra-and inter-sexual aggression by bonobos in the context of mating
Behaviour
Cited by (7)
Male and female birth attendance and assistance in a species of non-human primate (Rhinopithecus bieti)
2020, Behavioural ProcessesCitation Excerpt :An alternative hypothesis is infant attraction. Within this framework, it is assumed that conspecifics are attracted to the sounds, smells, and presence of neonates, and as a byproduct of attempting to engage or hold the infant, they assist the mother with the delivery, regardless of whether they are kin or nonkin (Demuru et al., 2018). In the case of assisting females, this could represent a form of ‘aunting’ behavior, which is commonly reported in several primate species (Kirkpatrick, 2011).
Living to fight another day: The ecological and evolutionary significance of Neanderthal healthcare
2019, Quaternary Science ReviewsCitation Excerpt :Whilst care for the ill and injured is often portrayed as uniquely human, such care is also recorded in both non-human primates and in social mammals in general. Examples of short term care for ill or injured peers are seen in non-human primates, particularly apes, and range from tending wounds (Fabrega, 1997; Hart, 2011; Fashing and Nguyen, 2011) to more complex practices such as birth assistance (Demuru et al., 2018). These behaviours fit within primate and ape tendencies to respond to distress through consolation as well as capacities to help in a targeted way (Romero et al., 2010; Clay and de Waal, 2013; Pérez-Manrique and Gomila, 2017).
School Bullying and Marginalisation: Harmonising Paradigms
2022, School Bullying and Marginalisation: Harmonising ParadigmsIs History the Same as Evolution? No. Is it Independent of Evolution? Certainly Not
2022, Evolutionary Psychology