인류와 침팬지. 피그미 침팬지 '보노보' 출산과정 인간과 유사. 산파 보노보.

보노보 - 난쟁이 침팬지. 피그미 침팬지. 

 

산파(조산)는 호모 사피엔스 인류만의 독특한 특징들 중에 하나라고 여겨졌다. 산파가 필요한 이유는 그 만큼 인류 출산 과정이 힘들다는 것을 보여준다.

 

그런데 최근 '난쟁이 침팬지'인 보노보의 출산 과정을 담은 비디오 영상에서, 암컷 보노보들이 새끼를 출산하는 암컷을 돕는 과정이 관찰되었다. 이 동영상은  인류의 전통적인 출산과정의 일반적인 특징들이 보노보 출산과정에서도 동일하게 나타남을 보여줬다.

 

인간 출산과 마찬가지로 보노보의 신생 침팬지 출산은 사회적 행사였다. 암컷 보노보들이 새끼가 출산되어 세상 바깥으로 나올 때까지 임신 암컷을 돌보고 보호했다. 

 

또한 옆에서 구경하던 암컷 보노보들은 마지막 출산 진통 기간에 새끼를 손으로 쥐는 동작을 하면서 출산하는 암컷에 힘을 보탰다. 

 

보노보의 출산 과정 관찰을 통해, 인류에게 아이를 출산할 때 사람들이 서로 돕는  '의무적인' 조력의 필요야말로 '사회성'을 발달시킨 주요한 동력이었다는 전통적인 관점에 의문을 제기하게 되었다. 

 

인간과 보노보의 출산 과정이 유사하다는 것은 아마도 여자들과 암컷 난쟁이 침팬지' 보노보 모두 고도의 '사교성'과 집단생활 능력이 있다는 것을 보여준다.  

 

'친족이 아닌' 암컷(여성)들이 강한 사회적 유대(연대)와 협력 체계를 만들어내는 능력을 가지고 있는데, 이러한 능력은 인간 산파(조산)가 출현하는데 필요한 진화적 선결조건이었을 것이다.

 

 

비디오 영상.

 

https://youtu.be/J-9wJAudFKQ

 

bonobos

: a rare anthropoid ape (Pan paniscus) that has a more slender build and longer limbs than the related common chimpanzee (P. troglodytes) and that inhabits a small geographic region in equatorial Africa south of the Congo River

 called also pygmy chimpanzee

 

 

 

 

 

 

 

 

 

 

 

Evolution and Human Behavior

journal homepage: www.elsevier.com/locate/ens  

Evolution and Human Behavior | Journal | ScienceDirect.com by Elsevier

Is birth attendance a uniquely human feature?

 

New evidence suggests that

Bonobo females protect and support the parturient

 

 

Elisa Demuru a,b,⁎, Pier Francesco Ferrari c , Elisabetta Palagi a

a Natural History Museum, University of Pisa, Via Roma 79, Calci 56011, Pisa, Italy

b Department of Biosciences, University of Parma, Parco Area delle Scienze 11a, Parma 43124, Italy

c Institut des Sciences Cognitives Marc Jeannerod, CNRS/Université Claude Bernard Lyon, 67 Bd Pinel, 69675 Bron Cedex, France

 

 

 

A R T I C L E

 

I N F O

 

Keywords:

Pan paniscus

Delivery

Protection

Support

Female gregariousness

Human birth attendance

 

 

A B S T R A C T

 

Birth attendance has been proposed as a distinguishing feature of humans (Homo sapiens) and it has been linked

to the difficulty of the delivery process in our species.

 

 

Here, we provide the first quantitative study based on

video-recordings of the social dynamics around three births in captive bonobos (Pan paniscus), human closest

living relative along with the chimpanzee.

 

We show that the general features defining traditional birth attendance in humans can also be identified in bonobos.

 

As in humans, birth in bonobos was a social event, where

female attendants provided protection and support to the parturient until the infant was born.

 

Moreover, by-

stander females helped the parturient during the expulsive phase by performing manual gestures aimed at

holding the infant.

 

 

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.

 

 

Indeed, birth in bonobos is not

hindered by physical constraints and the mother is self-sufficient in accomplishing the delivery.

 

Although further

studies are needed both in captivity and in the wild, we suggest that the similarities observed between birth

attendance in bonobos and humans might be related to the high level of female gregariousness in these species.

 

 

In our view, the capacity of unrelated females to form strong social bonds and cooperate could have represented

the evolutionary pre-requisite for the emergence of human midwifery. 

 

 

 

 

1. 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 re-

lationship 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 physio-

logical mechanisms in determining the timing of delivery in Homo sa-

piens (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 oc-

ciput 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

https://doi.org/10.1016/j.evolhumbehav.2018.05.003

Received 12 September 2017; Received in revised form 19 March 2018;

 

 

Accepted 3 May 2018

⁎ Corresponding author at: Department of Biosciences, University of Parma, Parco Area delle Scienze 11a, Parma 43124, Italy.

 

 

E-mail address: elisa.demuru@cnrs.fr (E. Demuru).

Evolution and Human Behavior 39 (2018) 502–510

1090-5138/ © 2018 Elsevier Inc. All rights reserved.

T

 

 

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 fa-

vourable 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 emer-

gence from the birth canal in nonhuman primates seems to be the oc-

ciput 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 de-

livery (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-in-

dividual 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 pre-

cluding 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 character-

istics of the species.

 

 

Here, we present the first quantitative analysis on the social dy-

namics 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). In-

dividuals 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 chimpan-

zees, bonobos show a much higher degree of cohesiveness, with dif-

ferent parties ranging in adjacent areas and travelling in the same di-

rection (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-se-

lection (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 en-

vironment 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 bo-

nobos 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” ques-

tioning whether birth attendance could have been already present be-

fore the evolutionary emergence of the “obligation” of assistance.

 

 

1.1. Spatial proximity to the parturient

 

 

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).

 

 

1.2. Female birth attendants and behavioural expression of arousal

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, Predic-

tion 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 fe-

male cohesiveness should be higher in the first phase of the delivery,

before the baby is born and the placenta is expulsed (Prediction 4).

 

 

 

1.3. Protection

 

 

In humans, birth attendants are in charge of protecting the mother

and the newborn from a great variety of both real and symbolic dan-

gers, 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

E. Demuru et al. Evolution and Human Behavior 39 (2018) 502–510

503

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 by-

standers can stay in proximity of the labouring female to protect her

from possible threats (Prediction 5).

 

 

1.4. Practical support by birth attendants

 

 

Traditional birth attendants in humans are generally multiparous

and elderly women (Ford, 1945), thus suggesting that personal ex-

perience 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, physi-

cally 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) practi-

cally helping the mother during the expulsive phase by holding the

infant if necessary. Further, if such practical support is parturient-or-

iented, 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.

 

 

2. Methods

 

 

 

2.1. 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 Sampling = 20 h; All Occurrences

Sampling = 200 h) and June–July 2014 (individual Focal Animal

Sampling = 9.5 h; All Occurrences Sampling = 140 h). During the whole

data collection period, individual Focal Animal Sampling was used to

assess the social bonding characterizing each bystander-mother dyad

(we use the term “mother” to indicate the “parturient female” not in the

day of the delivery). We calculated the hourly frequency of grooming

performed by each bystander towards the “mother” and then we nor-

malized this value on the total hourly frequency of grooming by the

bystander towards all group members.

 

 

 

For the whole periods of data collection, we registered the number

of agonistic conflicts via the All Occurrences Sampling (i.e., we recorded

all the conflicts we observed during the hours of observations).

Hierarchy was assessed by entering decided conflicts into a winner/

loser socio-matrix. Rank was measured by Normalized David's Scores

(see Table S1 for individual NDS values). Normalized David's scores

(NDS) were calculated on the basis of a dyadic dominance index (Dij) in

which the observed proportion of wins (Pij) is corrected for the chance

occurrence of the observed outcome. The chance occurrence of the

observed outcome is calculated on the basis of a binomial distribution,

with each animal having an equal chance of winning or losing every

dominance interaction (De Vries, Stevens, & Vervaecke, 2006). The

correction is necessary when, as in the case of our study groups, the

interaction numbers greatly differ between dyads.

 

 

 

2.2. Data collection on births and video analysis

 

 

2.2.1. Apenheul Primate Park (Apeldoorn, The Netherlands)

Kumbuka, a primiparous and medium ranking female, gave birth on

August 7th, 2009. At that time, the bonobo colony was composed of 10

individuals (2 adult males, 6 adult females, and 2 immature subjects,

Table S1). The subjects were housed in an enclosure with both indoor

and outdoor facility (about 230 m 2 and 5.000 m 2

, respectively).

 

 

2.2.2. La Vallée des Singes (Romagne, France)

 

 

When the multiparous and high ranking female, Ukela, gave birth

(August 4th, 2012), the bonobo colony consisted of 10 individuals (4

adult males, 5 adult females, 1 immature subject, Table S1). The ani-

mals were housed in an enclosure with both indoor and outdoor facility

(about 900 m2 and 10.000 m 2

, respectively). When Lucy, a primiparous

and medium ranking female, gave birth on July 14th, 2014, the colony

consisted of 17 individuals (5 adult males, 7 adult females, 5 immature

subjects, Table S1).

 

 

 

She had access only to the indoor enclosures.

The three mothers remained in their social groups during delivery.

All three births occurred during daytime in the indoor enclosures and

were video-recorded by using two cameras. One camera was focussed

on the parturient and on the individuals in her close proximity (physical

contact; ≤1 m), while the other camera was used to record the beha-

viours of group members that were more distant from her (> 1 m). In

all instances the first author was present and controlled the camera

focussed on the mother and on the individuals in her close proximity.

Field assistants and the last author in one occasion were in charge of the

camera focussed on group members staying at a distance of > 1 m from

the mother. When Kumbuka gave birth in 2009 we began filming when

the infant's upper-head was visible, thus resulting in 1-hour footage

(15h56–16h56). Our previous observations on Kumbuka's delivery al-

lowed us to start filming Ukela (2012) and Lucy (2014) as soon as we

noticed they were adopting some unusual body postures that we re-

cognized as being associated with delivery. Therefore, the video-re-

cordings of their deliveries covered a period of many hours (Ukela,

09h23–14h18; Lucy, 09h44–17h47).

 

 

 

 

We analysed our videos by applying the Focal Animal Sampling on

the mothers, and the Scan and All Occurrences Sampling on all group

members (see Altmann, 1974 for sampling methods).

 

 

The Focal Animal

Sampling on the mother permitted precise quantification of the occur-

rence and duration of all the postures/behaviours performed by the

parturient during the delivery and, therefore, identification of the exact

timing of infant and placenta expulsion. On the basis of the timing of

these two events, three phases were defined. T

 

 

o avoid an under-

estimation of the social interactions occurring across the delivery

phases, for Ukela and Lucy we decided to restrict the Scan and All

Occurrences analyses to a shorter period of time. The 1st phase started

from 1 h and a half before the delivery of the infant (infant's birth:

Kumbuka, at 16h02; Ukela, at 12h50; Lucy, at 16h58), the 2nd phase

covered the period from the expulsion of the placenta to its complete

consumption (placentophagia end: Kumbuka, at 16h25; Ukela, at

13h04; Lucy, at 17h14) and the 3rd phase included approximately the

30-min time window from the end of placentophagia.

 

 

The Scan Sampling was used at 30-s intervals to register the iden-

tities of group members (adults and the immature subjects who were

independent from their mothers) who stayed in close proximity (phy-

sical contact; ≤1 m), in loose proximity (1 m < X ≤ 2 m) of the mo-

ther, or beyond (> 2 m). The distinction between close and loose

proximity is meaningful because only the individuals staying in close

proximity of the mother can establish physical contact with her by

extending one arm (≤1 m). Loose proximity was defined as the distance

that can be reached by two individuals extending their arms towards

each other (≤2 m).

 

 

The All Occurrences Sampling was applied to register gestures, facial

expressions, socio-sexual contacts, playful and grooming interactions,

conflicts and charging displays in the whole colony (parturient and

other group members). These behavioural items were then categorized

into positive social interactions (Embracing, Sex, Play, Reach out, Silent

Bared Teeth, Clap hands, Gentle Touch, Head up-down) and negative

social interactions (Push, Bite, Pull, Chase, Jump over, Dismiss,

E. Demuru et al. Evolution and Human Behavior 39 (2018) 502–510

504

Screaming, Charging display).

 

 

 

The concurrent use and the integration of the three techniques al-

lowed quantification of the behaviours of all group members in relation

to the different delivery phases of the mothers.

 

 

Videos were analysed by using the free softwares VLC Media Player

and Kinovea. Before starting systematic data video analysis, the ob-

server (ED) established her intra-observer reliability, reaching a Cohen's

kappa value > 0.85 (Kaufman & Rosenthal, 2009). During the video-

analysis, this procedure was replicated at regular intervals (every 3 h of

videos) in order to check the intra-observer reliability for each beha-

vioural item considered. Cohen's kappa was never < 0.85. This proce-

dure consisted in observing and analysing the same video-sequence

twice (about 15 min of video) and checking for congruency of the two

datasets at regular intervals (about 10 days).

 

 

2.3. Operational definitions and statistics

 

 

 

Using the same techniques that were applied to the delivery day, we

compared the spatial proximity of group members to the mothers

(within two meters, including physical contact) across three days: day

before the delivery, delivery day and day after the delivery.

 

 

To guar-

antee the reliability of the comparison, we selected the same time slot

corresponding to that of each delivery for both the day before and after.

Due to the non-normality of data, non-parametric statistics were used.

For all the analyses involving pseudo-replicated and, therefore, non-

independent data (same individuals included in two samples because

two births took place in La Vallée des Singes), randomization tests were

employed with a number of 10,000 permutations by using Resampling

Procedures (via Resampling Procedures 1.3 package by David C.

Howell)

 

 

 

. The level of significance was set at 5% for all the analyses.

We evaluated which factors explained close (≤1 m; physical con-

tact) and loose proximity (1 m < X ≤ 2 m) of group members around

the parturient via a generalized linear mixed-model (GLMM) analysis.

The fixed variables included bystander's sex, deltaNDS

(NDS mother − NDS bystander ), delivery phase, mother-bystander social

bonding, and primiparous/multiparous mother (Table S2). Both the

dependent variables (i.e., close and loose proximity) had a Gamma

distribution (EasyFit 5.5 Professional). We tested models for each

combination involving the variables of interest, spanning a single-

variable model to a model including all the fixed factors (full model).

To select the best model, we used Akaike's corrected information cri-

terion (AIC C).

 

 

To measure how much better the best model is compared

to the next-best models, we calculated the difference (Δi or ΔAICCi )

between the AIC C value of the best model and the AIC C value for each of

the other models. Only the models where Δi was ≤2 and the first model

with the Δi > 2 are shown in the Table S3. Moreover, to assess the

relative strength of each candidate model, we employed Δi to calculate

the evidence ratio and the Akaike weight (wi; see Table S3). The evi-

dence ratio provides a measure of how much more likely the best model

is compared to the model i. The wi (ranging from 0 to 1) is the weight of

evidence, or probability, that a given model is the best model, taking

into account the data and set of candidate models (Symonds &

Moussalli, 2011).

 

 

All the analyses were conducted using SPSS Statistics 20.0.

 

 

 

3. Results

3.1. 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

member and the mother across three conditions: day before the de-

livery, delivery day and day after the delivery.

 

 

The time frequency of group members staying in proximity to the

mother significantly differed across the day before, the delivery day,

and the day after in each birth event (Exact Friedman's test - Kumbuka:

χ2 = 9.294, N = 7, df = 2, p = 0.006; Ukela: χ2 = 9.867, N = 8,

df = 2, p = 0.005; Lucy: χ2 = 11.128, N = 13, df = 2, p = 0.003;

Fig. 1). The spatial proximity of group members around the parturient

was much higher in the delivery day compared to the day before and

after (Prediction 1b supported). The results of the Dunnett's tests are

reported in the legend of Fig. 1.

 

 

3.2. Female birth attendants and behavioural expression of arousal

We assessed which variables might explain the close proximity

(≤1 m; physical contact) of group members to the mother (dependent

variable) via a Generalized Linear Mixed Model (GLMM). Delivery

phase, bystander's sex, ΔNDS (NDS mother − NDS bystander ), primiparous/

multiparous mother and mother-bystander social bonding were entered

as fixed factors (Table S2).

 

 

The model with the lowest AICc (133.23) included two factors: sex

and primiparous/multiparous ∗ delivery phase. This model competed

with the second one (AICc = 134.79), which included the same vari-

ables plus bonding (Table S3). For both competing models, only sex

(F = 51.951; df1 = 1; df2 = 41; p = 0.0001; Fig. 2) and primiparous/

Fig. 1. Proximity of group members to the mother (a - Kumbuka, n = 7; b - Ukela, n = 8; c - Lucy, n = 13) the day before the delivery, in the delivery day, and the

day after the delivery. The box plots show the median and 25th and 75th percentiles; the whiskers indicate the values within 1.5 times the interquartile range, IQR.

The open dot is an outlier > 1.5 IQR from the rest of the scores. Only significant differences are reported in the figure.

Dunnett's test: a) Kumbuka - Day before < delivery day: q = 2.265 p < 0.05; delivery day–day after: q = 1.84 NS; day before–day after: q = 0.68 NS. b) Ukela -

Day before < Delivery day: q = 3.90 p < 0.01; delivery day > day after: q = 3.533 p < 0.01; day before–day after: q = 0.26 NS.

c) Lucy - Day before < delivery day: q = 3.47 p < 0.01; delivery day > day after: q = 2.55 p < 0.05; day before–day after: q = 0.14 NS (* ≤ 0.05; ** ≤ 0.01).

E. Demuru et al. Evolution and Human Behavior 39 (2018) 502–510

505

multiparous ∗ delivery phase were statistically significant (F = 6.808;

df1 = 5; df2 = 41; p = 0.0001), with females showing the highest le-

vels of close proximity to the mother (Prediction 2 supported).The first

model had a Wi of 0.633, which means that it explains the 63.3% of the

distribution. The second model had a Wi of 0.288, which means that it

explains the 28.8% of the distribution. The first model was 2.19 and

24.14 times more likely to be the best model than the second and third

models, respectively (Table S3).

 

 

 

By including the same fixed variables, we also ran a GLMM to assess

which variables might explain the loose proximity (1 m < x ≤ 2 m) of

group members to the mother (dependent variable). We found five

competing models which explained the 15.15%, 10.48%, 10.27%,

9.27% and 5.05% of the distribution, respectively (all the data are

shown in Table S3). The presence of so many competing models made it

impossible to identify specific variables which might have an effect on

the loose proximity distribution.

 

 

We examined whether a gender difference regarding the expressions

of gestures, facial expressions and social interactions. Females showed a

significantly higher level of behavioural expression of arousal than

males in both positive (Randomization test for Two Independent sam-

ples, t = −2.596; n males = 12; n females = 16; p = 0.0051) and negative

domains (Randomization test for Two Independent samples,

t = −3.572; n males = 12; n females = 16; p = 0.0016) (Prediction 3 sup-

ported).

Given that the close proximity to the mother and the behavioural

expression of arousal was a prerogative of females, we focussed our

attention on them. We found that the highest level of female cohesion

around the parturient occurred before the delivery of the infant (1st

phase - mother only) and not in presence of the placenta (2nd phase -

mother, infant and placenta) or the infant (3rd phase - mother and

infant) (Anova One-Way Randomization: F = 3.950, n = 13,

p = 0.028; Fig. 3) (Prediction 4).

3.3. Protection

Bystander females directed more negative than positive behaviours

towards males (Paired sample Randomization test; t = 2.048;

n f→m = 21; p = 0.048); whereas in female dyads such a difference was

not found (t = −0.454; n f→f = 15; p = 0.66) (Prediction 5 supported).

Most of the positive social interactions of bystander females were di-

rected to the mother (positive f-mother vs negative f-mother, t = −4.620; n f-

mother = 11; p = 0.0006; positiveff vs positive f-mother , Two Independent

Randomization test; t = −4.876; nff = 15; nf-mother = 11; p = 0.0001)

(Fig. 4). In these analyses only those dyads showing at least one in-

teraction, either negative or positive, were included.

Females also showed aggressive displays with or without objects

towards human observers (zoo staff and researchers). This behaviour

was significantly more frequent in the first phase of delivery before the

infant's birth (Anova One-way Randomization: F = 5.208; n = 11;

p = 0.006; Fig. S1). This behaviour was never observed during

Kumbuka's delivery and never in males.

3.4. Practical support by birth attendants

3.4.1. Tactile/olfactory investigation

The parturients inspected/cleaned their genitals by touching them

and licking the fluids on their hands. This behaviour varied according

to the three different delivery phases: 1st phase = mean 3.05, 2nd

Fig. 2. Mean ± SE of the time spent in close proximity to the parturient

(≤1 m; physical contact) by bystander males and females (*** ≤ 0.001).

Fig. 3. Mean ± SE of the time spent in close proximity to the parturient

(≤1 m; physical contact) by bystander females (n = 13) across the three de-

livery phases: 1st phase = only mother; 2nd phase = mother + in-

fant + placenta; 3rd phase = mother + infant.

Fig. 4. Mean ± SE of hourly frequency of females' positive (Embracing,

Grooming, Grab infant gesture, Reach out, Silent Bared Teeth, Clap hands,

Gentle Touch, Head bob) and negative (Push, Bite, Pull, Chase, Jump over,

Dismiss, Bared teeth/Screaming, Charging display) social interactions towards

the mother (n = 11), towards other females (n = 15) and towards males

(n = 21).

E. Demuru et al. Evolution and Human Behavior 39 (2018) 502–510

506

phase = 0.14, 3rd phase = 1.8. This result suggests that genital fluids

are present during each phase of delivery and it is possible that they

contain important chemical information for the mother.

In all delivery events, bystander females also frequently investigated

the genital region of the parturient by sniffing, licking, or touching,

probably attracted by the fluids. Differently from the parturient, this

behaviour was mainly performed during the first delivery phase before

infant's birth and rapidly decreased thereafter (Randomized Repeated

One-Way Anova: F = 6.69; n = 15; p = 0.0012).

3.4.2. Visual inspection

We defined visual inspection as an individual moving the head to-

wards the genitals of the parturient while standing behind her or

moving around the parturient to gain visual access to her genitals.

During Ukela and Lucy's deliveries all the adult females but one (Lisala,

the less integrated female) visually checked the genitals of the par-

turient (Fig. S2; Video S1). Visual inspection was exclusively observed

before the infant's birth (mean frequency per minute = 0.20 ± 0.07

SE).

3.4.3. Keeping insects away from the mother's genitals

During Ukela's delivery, about 35 min before the infant's birth, the

dominant female (Daniela) of the La Vallée des Singes group repeatedly

waved the hand near the genitals of the parturient to remove a fly

(Video S2).

3.4.4. Grab infant gesture

A peculiar gesture performed towards both Ukela and Lucy by the

two dominant females (Daniela towards Ukela, n = 2; Daniela and

Ukela towards Lucy, n = 3 and n = 1, respectively) was represented by

the grab infant (Video S1). These females put and kept one or both

hands under the genital region of the parturient without touching her

genitals and without licking their hands after (differently from inspec-

tion). It should be noted that this behaviour resembles very much the

motor action pattern performed by the mother in the moments just

before the infant's birth. Similarly to the mother, the other females also

performed this gesture only in the last minutes of the first phase of the

delivery until the birth of the infant. While making the gesture, Daniela

also performed head bobbing (Demuru, Ferrari, & Palagi, 2015; van

Hooff, 1973) and a bared teeth facial expression (see De Waal, 1988;

Pollick & de Waal, 2007) towards the parturient (Video S1).

3.4.5. Hold infant

On three occasions, two different females actually held the infant

during the expulsive phase. During Ukela's delivery, Lucy held first the

head and then the arm of the baby while the mother was moving down

from a rope (Video S3). During Lucy's delivery, Daniela held the head of

the baby and concurrently performed head-shake gestures (Demuru

et al., 2015; van Hooff, 1973).

4. 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 group members, especially females. Indeed, even if

Kumbuka and Ukela had access to the outdoor facilities, offering more

possibilities to hide, they nevertheless preferred to give birth indoor

with others nearby. The higher number of group members around the

three parturients on the day of delivery supports the hypothesis that

birth in bonobos is a social event, with groupmates showing interest

towards the female in labour (Fig. 1). This result is in line with the few

reports in non-human primate species observed in the wild describing

complex social interactions during the delivery (Ding et al., 2013;

Douglas, 2014; Pan et al., 2014).

Our study on bonobos is the first to have quantified the various

phases of parturition with a description of the social dynamics occur-

ring between the parturient and other group members. More specifi-

cally our findings demonstrated that females stayed in close proximity

to the mother, while males remained in the most peripheral areas of the

enclosure (Fig. 2). Bystander females' behaviour towards the parturient

was not limited to mere spatial proximity around the mother, but it

involved a high level of affiliative patterns directed towards her

(Fig. 4). The central role of bystander females during a delivery seems

to be linked to the social relationships of this female-bonded society

(Furuichi, 2011; White, 1996). It is worth remembering that female

affiliative bonds - and therefore social support during birth - cannot be

explained by kinship, differently from the reports on Colobinae mon-

keys (Ding et al., 2013; Pan et al., 2014). Female sociality around birth

in bonobos shares some general elements with human traditional birth

attendance, in which women are almost universally the only individuals

allowed to stay with the parturient and assist her (Cosminsky, 2003;

Eibl-Eibesfeldt, 1989; Ford, 1945). A common trait shared by bonobos

and humans is the formation of strong affiliative social bonds between

unrelated females (Rodseth & Novak, 2006). Unlike human and bonobo

females, chimpanzee females are less gregarious, tend to live more

solitarily with their dependent offspring and their interactions are

generally considered as competitive/antagonistic, due to the competi-

tion over resource (Gruber & Clay, 2016), although a certain variability

in female sociality has been highlighted between East and West African

populations (Langergraber, Mitani, & Vigilant, 2009; Lehmann &

Boesch, 2008). Pregnant and lactating chimpanzee females typically

isolate themselves from the rest of the group (Fujisawa, Hockings,

Soumah, & Matsuzawa, 2016; Furuichi, 2011) and, as far as we know,

only two reports on births in the wild are available (Goodall &

Athumani, 1980; Kiwede, 2000). In their descriptions, the authors do

not describe complex social interactions towards the mother and even if

in these two cases the mothers did not isolate from groupmates, this is

reported as an exception. Moreover, Goodall and Athumani's study

group was food provisioned and this certainly altered the dispersal

pattern of animals. It has been hypothesized that chimpanzee females

isolate themselves to avoid the risk of infanticide by in-group or out-

group males, frequently described in this species (Gruber & Clay, 2016;

Hamai, Nishida, Takasaki, & Turner, 1992; Watts, Sherrow, & Mitani,

2002). Moreover, in this species, intra-group infanticide led by females

has also been reported and may be related to feeding competition

(Pusey, Williams, & Goodall, 1997; Townsend, Slocombe, Thompson, &

Zuberbühler, 2007). It is therefore plausible that the social dynamics

around birth profoundly differ between chimpanzees and bonobos,

where infanticide has never been reported (Gruber & Clay, 2016). The

absence of male coercion over females and the widespread use of sexual

behaviours for social purposes in bonobos, lead to hypothesize that

paternity confusion was the reason behind the absence of infanticide in

this species (Furuichi, 2011). However, recent studies challenge this

view by showing that the reproductive skew of male bonobos is even

higher than that recorded for chimpanzees, and so paternity might be

even more certain in bonobos than in chimpanzees (Surbeck,

Langergraber, Fruth, Vigilant, & Hohmann, 2017).

 

 

 

Another interesting

explanation for the absence of infanticide in bonobos is the recent

Offspring Dominance Hypothesis (Walker & Hare, 2017). This hypothesis

suggests that young bonobos evolved to play a central role in triggering

female coalitionary aggression against males in this species. As a matter

of fact, female bonobos are very protective towards their offspring and

their coalitions most frequently occur against males that attacked a

young individual (Surbeck & Hohmann, 2013; Tokuyama & Furuichi,

2016). Females' alliances served to control male attacks, especially

against infants, and led to a decrease in male aggressiveness and the

absence of infanticide in this species. This seems to be in line with our

E. Demuru et al. Evolution and Human Behavior 39 (2018) 502–510

507

 

 

 

results showing that most of bystander females' agonistic displays were

directed towards males, who were actively kept away from the par-

turient (Fig. 4). Tokuyama and Furuichi (2016) reported that in male-

female dyadic conflicts, males prevailed in 31.1% of cases, whereas

they never defeated a coalition of females.

 

 

If this is true in daily social

dynamics, it should be even more so during labour when the female is

experiencing a state of vulnerability that can be deduced by her unusual

behaviours, such as straining fixed postures and slow movements.

Therefore, social isolation could be dangerous for a parturient, because

she would be more vulnerable to the attacks of males or predators.

Remaining within the social group could have been favoured by natural

selection because of the advantage for the parturient to receive pro-

tection from other females. This interpretation is supported by our

findings showing that bystander females became very aggressive to-

wards familiar zoo staff and researchers who were observing the births

in the adjacent rooms (Fig. S1).

 

 

The few mixed-sex affiliative interactions occurring in proximity to

the parturient involved the dominant female (Daniela) and her adult

sons or her favourite male (Videos S1, S4). These males did not direct

any particular attention to the parturient, but interacted only with

Daniela. Interestingly, this female is the only one that has her adult sons

living with her. The importance of mother-son relationships has been

highlighted in several contexts and strongly influences the social in-

tegration of males, as well as their reproductive success (Furuichi,

1997; Hohmann & Fruth, 2003; Surbeck et al., 2011, 2017).

The spatial distribution pattern we found during the delivery par-

allels what has been already described in the wild during the feeding

activity of the parties (i.e., subgroups; Furuichi, 2011). In the presence

of a monopolizable food resource, the alliance of socially bonded fe-

males gathers around it and occupies the core area, whereas less in-

tegrated females and males stay in the peripheral area (Furuichi, 2011;

Gruber & Clay, 2016; Parish, 1994).

 

 

Previous observations on birth in

bonobos reported that placentophagia is present in this species (Bolser

& Savage-Rumbaugh, 1989; Douglas, 2014; Kirchshofer, 1963; van

Elsacker et al., 1993; see Young & Benyshek, 2010 for a review on

placentophagia in humans), and we therefore hypothesized that the

desirable and monopolizable resource could be represented by the

placenta. Unexpectedly, we found that the phase characterized by the

highest proximity levels to the mother did not coincide with the pre-

sence of the placenta (Fig. 3), but it was concentrated in the first phase

of the delivery, when only the mother was present. Therefore, it is not

the placenta - neither the infant - the reason why females gather around

the parturient. Although females are certainly attracted by the placenta,

they showed a sort of inhibition in approaching the mother while she

was consuming it. We registered two attempts of placenta stealing (one

during Kumbuka's delivery and the other during Lucy's).

 

 

 

These attempts

were performed by dominant females, were not repeated and all three

mothers consumed their own placentas without other interferences.

From an evolutionary perspective, one may hypothesize that the strong

interest displayed by females towards the parturients could have been

originally motivated by the potential food resource represented by the

placenta.

 

 

However, in the natural history of bonobos, the high level of

tolerance and the female complex social network might have driven the

shift of attention from the placenta to the parturient and her peculiar

emotional/physical condition.

 

 

This transition is likely to have made the

delivery a critical period for demonstrating the motivation to protect a

group mate in a vulnerable condition and, therefore, to test and

strengthen those social bonds which are the pillars of the bonobo fe-

male-bonded society.

 

 

This motivation is also demonstrated by the high

levels of affiliative behaviours performed by bystander females towards

the mother (Fig. 4).

 

 

These females continuously monitored the course

of the delivery by exploring parturient's genital area by touching,

licking and sniffing and by visually checking it. These behaviours

dropped immediately after infant's birth. The inspections involving

body contact (i.e., touching, licking and sniffing) may be driven by the

attraction for birth fluids. However, this behaviour was not explained

by the presence of genital fluids per se, as they were present in all the

phases of the delivery, especially in the second one. The fact that visual

checking followed a time pattern similar to inspection, but it cannot be

explained by a physical attraction for fluids, led us hypothesize that

touching, licking and sniffing might also serve a “monitoring” function.

An indication of the prosocial nature of parturient-oriented beha-

viour during the first phase of delivery is the episode of Daniela, who

repeatedly removed a fly from Ukela's genitals. Removing flies is fre-

quently performed by bonobos, but as a self-directed behaviour, and

never addressed towards conspecifics (Video S2).

 

 

 

The supporting and active role played by females is confirmed by a

number of observations. Some females displayed a grab-like gesture

when the head of the infant became visible, with one or both hands

extended under the genital region of the parturient without touching

either the infant's head or the mother's genitals. This gesture mirrors the

same gesture performed by the mother herself as birth approaches and

serves to hold the head of the infant once it emerges. Such a beha-

vioural pattern appears to be an action aimed at grabbing the newborn.

It must be noted, however, that the three mothers were self-sufficient in

achieving the delivery by promptly catching the infant and by carrying

in a ventral position. Nonetheless, in three cases we observed two fe-

males helping the mothers to hold the infant. During Ukela's delivery,

Lucy intervened twice by holding the infant's head and arm while the

parturient was moving down from a rope and therefore could not grasp

the infant firmly and safely (Video S3). The mother showed no signs of

fear or aggressiveness and seemed to tolerate and accept the bystander

intervention of temporarily holding the infant. Ukela in particular, was

extremely tolerant and allowed any other group member to approach

and groom the newborn in the days following the delivery, thus con-

firming that the mother does not perceive group mates as a threat to the

infant.

 

 

Another similar behaviour was performed by Daniela during Lucy's

delivery. Daniela also held the infant's head together with the par-

turient (i.e. Daniela put her hand on Lucy's hand) and concurrently

shook her head towards the mother after engaging in a face-to-face

contact with her. This complex communicative pattern was also ob-

served during Ukela's delivery and it indicates a positive engagement of

bystander females.

 

As a whole, our results show bonobo female attendants provide

support and protection to the parturient, thus demonstrating that these

elements are not exclusive to humans.

 

 

 

 

We are conscious that our study has some limitations concerning the

generalizability of our findings at species level due both to the small

sample size and to the captive environment. It is certain that small

sample sizes are more susceptible to support alternative explanations.

Generalized curiosity towards a rare event happening within the colony

could be accounted as a possible explanation of proximity.

 

 

However, in

our opinion, curiosity-driven proximity should be equally widespread

among all group members and, more importantly, we would expect a

higher proximity of group members when the real “novelty” appears -

i.e. the newborn - but it has not been the case.

 

 

The scientific validity of

research on animals living in high-standard captive conditions has been

demonstrated by a wide array of behaviours that were first observed in

captivity and then confirmed in the wild (e.g., reconciliation in chim-

panzees - captivity: de Waal & van Roosmalen, 1979; wild: Arnold &

Whiten, 2001; tool use in capuchin monkeys - Fragaszy, Visalberghi, &

Fedigan, 2004). Moreover, the only report on bonobo birth sociality in

the wild (Douglas, 2014), despite the difficult conditions for describing

the behavioural events, nevertheless confirms that the complex soci-

ality we observed cannot be considered as the artefact of the captive

environment.

 

 

5. Conclusions

 

 

 

Our results on bonobos question the traditional view that the “ob-

ligatory” need for assistance was the main driving force leading to

E. Demuru et al. Evolution and Human Behavior 39 (2018) 502–510

508

 

 

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 might be linked to the high level of female gregariousness

characterizing these species, differently from chimpanzee.

 

 

The simila-

rities between bonobo's female gregariousness and human's female

gregariousness - a prerequisite for birth attendance in our view - can be

either the result of convergent evolution or common descent. Similar

socio-ecological factors could have led to a phenomenon of convergent

evolution between bonobos and humans. In these species female gre-

gariousness was selected for because it increased the survival prob-

ability of females.

 

 

This phenomenon of convergence could have arisen

at different moments and in different species along the hominin lineage

whenever the benefits of female gregariousness outranked its costs. On

the other hand, common descent would imply that the last shared an-

cestor between Homo sapiens and the two Pan species showed female

gregariousness and that this behavioural trait could have then been

maintained in the course of the hominin evolutionary lineage. There-

fore, the absence of female gregariousness in chimpanzees would be a

derived feature, maybe linked to a more competitive nature of female-

female relationships. According to this view, the bonobo would be more

similar to last common ancestor with humans (Zihlman, Cronin,

Cramer, & Sarich, 1978), but this topic is debated (Johnson et al.,

1981).

 

 

Certainly, both scenarios raise interesting questions and both the

Pan species must be taken into account when trying to reconstruct the

evolution of complex human behaviours, such as midwifery.

Supplementary data to this article can be found online at https://

doi.org/10.1016/j.evolhumbehav.2018.05.003.

Ethic statement

This study was purely observational (with no manipulation what-

soever) 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 co-

lonies 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.

 

 

 

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