Study site and subjects

Behavioral observations were conducted on 15 adult chimpanzees—11 females and four males—housed socially at Royal Burgers’ Zoo in Arnhem, the Netherlands (Table 1 for subject demographics). Two females in the sample, Erika and Moni, were added to the colony on 12-02-2016, along with a third adult female who died before the beginning of the current study period (on 14-03-2017). After an introduction process during which the colony was kept in subgroups of varying sizes, the full group was reunited on 18-10-2017 (i.e., 1 month before the current study began).

Table 1 Subject demographics as of the start of data collection (20-11-2017) Full size table

The chimpanzees’ housing consisted of an indoor and outdoor enclosure, measuring ± 386 m2 and ± 7000 m2, respectively. During scheduled feeding and routine transfers from the indoor to the outdoor area, the chimpanzees were temporarily held in a series of smaller enclosures, not visible to the public and hereafter referred to as the ‘backstage’ cages. The design of the outdoor enclosure was semi-natural, and both enclosures were enriched with various climbing structures. The chimpanzees were fed approximately three times daily and had access to water ad libitum.

Data collection

Two observers collected data from 20-11-2017 until 01-06-2018, 4 days a week between 9:00 and 17:00. Daily data collection protocols comprised: a 90-min group observation, 10-min focal observations (one per individual), and ad libitum sampling of agonistic interactions. During group and focal observations, all occurrences of affiliative interactions were recorded (Martin and Bateson 2007), including the initiator, recipient, and type of affiliative behavior (ethogram in Table 2).

Table 2 Ethogram of affiliative contacts used in the current study Full size table

The order of focal subjects was randomized, and both focal and group samples were counterbalanced across days and observers. Two observers were concurrently trained until a Cohen’s kappa value higher than 0.70 was obtained for all observational protocols (0.79 and 0.76 for group and focal observations, respectively) before the data collection period began. Observers always collected data as a pair, with one individual observing, using binoculars if necessary, and the other recording.

The event

On 30-01-2018, 2 months after the study period began, the observers arrived at the zoo shortly before visitor opening hours (at 9:00) and observed Moni holding a dead infant. There was no strong prior indication of Moni’s pregnancy, but physical and behavioral cues on the day of the event (i.e., blood on Moni’s vulva, proximity to and handling of the corpse) indicated that it was most likely hers, which was later confirmed by DNA analysis. The infant was a fully developed male, who appeared to be in good physical condition aside from bite marks on his chest and a large gash on the top of his head. The keepers were alerted, and the chimpanzees were moved to their backstage enclosures, where they remained for the rest of the day. Initially, Moni and the infant’s corpse were kept separate from the rest of the colony as the keepers examined them. Note that the chimpanzees were accustomed to the backstage enclosures and to being separated from the group as part of routine zoo husbandry/management protocol (e.g., to receive additional feeding).

Following the initial examination, other group members were given access to both Moni and the corpse (at approximately 10:00), upon which the observers began collecting data. Data collection on this day deviated from the normal protocol in that all behaviors involving Moni and Fons (the presumed father of the infant, based on the monitored breeding program) were continuously recorded along with proximity data. Additionally, all interactions between other group members and the corpse were recorded. Photographs and videos were taken of notable interactions. Data were collected until 15:45 that day, at which point an unsuccessful attempt was made by the keepers to separate Moni from her infant’s corpse.

The next day (31-01-2018), no observations were scheduled while the chimpanzees remained in the backstage enclosure. On 01-02-2018, following several attempts on the part of the keepers to separate Moni from the corpse, it was appropriated by another female, Tushi. The rest of the group was given access to the indoor enclosure, where normal observations continued while Tushi and the corpse remained in the backstage enclosure. Videos and observations were taken of Tushi while she had the infant. At the end of this day, the group was reunited with Tushi and the corpse. The following day (02-02-2018), the corpse was dropped by Tushi and removed from the group by the keepers. It was examined by the zoo’s veterinarian, who concluded that the infant was stillborn, based on no signs of air ever having been present in the lungs. Thus, despite the extensive wounds on the body (indicating aggression towards the corpse), infanticide was ruled out as the cause of death. Subsequent DNA testing showed that Ghineau, rather than Fons, was the dead infant’s father. A more detailed description of the event can be found in Online Resource 1, and an overview of the timeline is illustrated in Fig. 1.

Fig. 1 Timeline of events described in the current study, on 30-01-2018 observations occurred outside of the regular schedule and no observations took place on 31-01-2018. Observations resumed on 01-02-2018, excluding Tushi who was held in the backstage enclosures with the infant’s corpse. On 02-02-2018, the infant’s corpse was removed and Tushi reunited with the rest of the group Full size image

Data analyses

Our analyses aimed to assess whether other chimpanzees increased their affiliation toward the bereaved mother, Moni. First, we analyzed data across all individuals to determine whether there were any subject-level differences in receipt of affiliation over time. In the case of significant between-individual variation, we would subsequently inspect these differences to compare the bereaved mother’s received affiliation trajectory to that of the other chimpanzees. This approach allowed us to determine whether changes in affiliation around the event were specific to the bereaved mother or more general. This multiple regression framework allowed us to account for several alternative factors that could potentially underlie any observed changes in affiliative patterns.

Because pregnant chimpanzees receive less affiliation (Nishida 1979) while swollen females tend to receive more (Wallis and Lemmon 1986), we added female estrus state to our overall analytical approach. Further, because the colony was outdoors more frequently than indoors in the post-period compared to the pre-period (due to warmer seasonal weather), which could impact affiliation rates, we included location of observation. Additionally, due to the introduction program that preceded the study period, it is possible that any increase in affiliation could reflect the natural integration process (Schel et al. 2013); therefore we specifically compared behavior received by Moni to that received by Erika, the other newly introduced female.

Model specifications

First, we investigated affiliation patterns within the group (i.e., group analysis) across the study period by means of a generalized linear mixed model (GLMM; Baayen 2008) with a Poisson error distribution and a log link function in the R statistical environment v3.5.2 (R Core Team 2018). Data were structured dyadically (representing all possible actor–recipient dyads) per day, extracting corresponding given–received affiliation information from both partners’ focals and the daily group observation. The predictors of individuals’ “received affiliation” (i.e., counts per day) comprised the estrus state (i.e., in estrus vs. not in estrus vs. pregnant), age, sex, and rank of both the actor and recipient, and the location of observations (indoors or outdoors) as fixed effects. Daily observations were typically restricted to indoors or outdoors, but in some cases (< 10%) they were conducted in both enclosures; in these instances, the location in which most observations occurred was used. Further, we fitted the actor, recipient, dyad, and date as random intercepts, and “dyadic observation time” as an offset term (to account for different observation durations). To assess whether chimpanzees exhibited a differential trajectory of received affiliation over time, we incorporated random slopes of date nested in recipient. Given our interest in a (temporary) oscillation of received affiliation toward the bereaved mother, here, we allowed for a non-linear (i.e., sigmoidal) effect of time on received affiliation per individual by implementing the squared term of date nested in recipient (i.e., “1+date+I(date^2)||recipient”). Finding that this term significantly explained variance in individuals’ received affiliation would allow for a more in-depth exploration of the shapes of individuals’ trajectories, and specifically an investigation of the bereaved mother’s hypothesized increase in received affiliation immediately following the event. The overdispersion parameter of the model (i.e., 1.14) was acceptable such that the model output could be validly interpreted (threshold ~ 1.20; Payne et al. 2018). Model stability was good, as indicated by the range of estimates obtained when excluding individuals one at a time (Online Resource 2: Fig. 5).

Second, we explored the specific determinants of received affiliation for the bereaved mother in relation to other group members by running separate Poisson models with a log link function for every individual as the recipient of the affiliation (i.e., individual analyses). In order to avoid overfitting, we included only the fixed effects that pertained directly to the key potential alternatives under study (“estrus state” and “location of observation”). The same random effects structure as in the group analysis was fitted, except for the random intercept term for the recipient (i.e., here constrained to one individual). For each individual receiver, the model predictions were plotted to the actual received affiliation per month (note that since only 1 day was observed in June, this was included in May for plotting purposes). Additionally, we considered differences in received affiliation from the month pre-event (January) to the month post-event (February), to determine whether the bereaved mother’s observed increase was relatively larger than that of other group members. In order to identify how many and which group members drove the bereaved mother’s pattern of received affiliation, we also examined the results of her model per actor.

Inferences of statistical significance were based on P values (< 0.05) as extracted from model comparisons (with and without predictor of interest; Barr et al. 2013) using the likelihood-ratio test (Dobson 2002). Given that our hypothesis in the group analysis concerned the test of one particular term (namely the random slopes term of date squared nested in the recipient of affiliation, i.e., “1+date+I(date^2)||recipient”), we refrained from testing a full-null model comparison, where the null model would represent the absence of all fixed terms except the intercept. For the individual analysis focused on the bereaved mother, we did precede inspection of the individual effects by a full-null model comparison (Forstmeier and Schielzeth 2011), where the null model only included the intercept (set to 1).

Qualitative data

Lastly, more descriptively, we considered the quality of the affiliative behaviors received and given by the bereaved mother on and around the day of the event, focusing on several affiliative behaviors that are typical of reassurance contexts in chimpanzees, namely body kiss, embrace, mouth–mouth kiss, and finger/hand in mouth (Fig. 3, Fraser and Aureli 2008; Goodall 1989).