key: cord-0332224-h8ra958b
authors: Soldati, Adrian; Fedurek, Pawel; Crockford, Catherine; Adue, Sam; Akankwasa, John Walter; Asiimwe, Caroline; Asua, Jackson; Atayo, Gideon; Chandia, Boscou; Freymann, Elodie; Fryns, Caroline; Muhumuza, Geresomu; Taylor, Derry; Zuberbühler, Klaus; Hobaiter, Catherine
title: Dead infant carrying by chimpanzee mothers in the Budongo Forest
date: 2022-04-30
journal: bioRxiv
DOI: 10.1101/2021.12.22.473786
sha: da691b532fcba765a8d5f412bec26ee8343620cc
doc_id: 332224
cord_uid: h8ra958b

It has been suggested that non-human primates can respond to deceased conspecifics in ways that suggest they experience psychological states not unlike humans, some of which could indicate they exhibit a notion of death. Here, we report long-term demographic data from two East African chimpanzee groups. During a combined 40-year observation period we recorded 191 births of which 68 died in infancy, mostly within the first year. We documented the post-mortem behaviour of the mothers and found that Budongo chimpanzee mothers carried infants after their death on nine occasions, usually until the body started to decompose after a few days. However, we also observed three cases of extended carrying lasting for more than two weeks, one of which was followed by the unusual extended carrying of an object and another which lasted three months. In each case, the corpses mummified. In addition, we report four instances of recurring dead infant carrying by mothers, three of whom carried the corpse for longer during the second instance. We discuss these observations in view of functional hypotheses of dead infant carrying in primates and the potential proximate mechanisms involved in this behaviour.

infants after their death on nine occasions, usually until the body started to decompose after a 27 few days. However, we also observed three cases of extended carrying lasting for more than 28 two weeks, one of which was followed by the unusual extended carrying of an object and 29 another which lasted three months. In each case, the corpses mummified. In addition, we 30 report four instances of recurring dead infant carrying by mothers, three of whom carried the 31 corpse for longer during the second instance. We discuss these observations in view of 32 functional hypotheses of dead infant carrying in primates and the potential proximate 33 mechanisms involved in this behaviour. physiological mechanisms. Specifically, the 'unawareness hypothesis' states that mothers are 89 unable to discriminate between temporarily unresponsive and irreversibly deceased 90 individuals and simply try to avoid the costs of premature abandonment (Hrdy 1999) . The 91 hypothesis predicts that mothers are unable to understand their infants' state and continue 92 providing maternal care (e.g., grooming) and try to elicit responsiveness (e.g., poking, 93 smelling). With increasing time, the ambiguity will dissolve due to the accelerating 94 decomposition of the corpse, which can be mediated by local climate. A second prediction 95 therefore is that dry and particularly hot or cold conditions favouring mummification should 96 also favour prolonged carrying of dead infants (see also 'climate hypothesis': Matsuzawa 97 1997; Fashing et al. 2011 ). The 'post-parturient condition' hypothesis (also referred as 98 'hormonal', see Gonçalves and Carvalho 2019) proposes that the maternal physiological 99 conditions associated with pregnancy and birth favour persistent care of the dead infant as 100 long as the mother is lactating or until resumption of ovulation (Biro et al. 2010; Kaplan 101 1973) . After giving birth, the endocrine system of the mother releases hormones (e.g., 102 oxytocin) that stimulate maternal behaviours (Keverne 1988; Bercovitch 2020) . Here, the 103 prediction is that when a mother loses her infant close to its birth (and the associated 104 hormonal changes), they are more likely to continue to invest in infant care, increasing the 105 likelihood and perhaps duration of any post-mortem carrying behaviour. 106 107 A second kind of hypotheses assumes that primate mothers can have a notion of death, 108 provided they have relevant personal experience. Specifically, the 'learning about death' 109 hypothesis states that chimpanzees do not intuitively understand death but can acquire the 110 notion by learning to attend to the relevant cues (Cronin et al. 2011 ). Here, the predication is 111 that younger or inexperienced mothers are more likely to carry dead-infants than older or 112 experienced mothers to learn about death (Watson and Matsuzawa 2018) . While females 113 could learn by handling the corpses of the offspring of others, another possible source of 114 information comes from experiencing multiple deaths of their own offspring. In addition, 115 experienced mothers might also be more aware of the irreversible change of death due to 116 having interacted with more living infants and/or for longer periods of time. Overall, if 117 mothers' reason for carrying is due to a lack of experience or understanding of what a dead 118 infant is like, they should be less likely to carry or carry for shorter periods dead-infants in 119 subsequent cases. An alternative hypothesis, the 'grief-management hypothesis', also 120 assumes that chimpanzees possess a notion of death, and suggests dead-infant carrying 121 represents a consoling strategy to cope with grief. This hypothesis predicts that mothers who 122 are able to carry their dead infants experience lower levels of 'stress' hormones (i.e., 123 glucocorticoids) than mothers who did not carry them (Nicolson 1991) , which could be a 124 strategy to cope with stress associated with infant loss (e.g., Takeshita et al. 2020) . 125 126 A third group of hypotheses are agnostic about whether chimpanzees possess a notion of 127 death but proposes various adaptive mechanisms that favour post-mortem mothering 128 behaviour. First, the 'learning-to-mother hypothesis' states that dead-infant carrying 129 improves maternal skills (Warren and Williamson 2004) , predicting that the behaviour should 130 mainly be observed in inexperienced primiparous females. Second, the 'maternal-bond 131 strength hypothesis' predicts that mothers with older infants share a stronger bond, due to 132 more extensive association and interactions between them, and are thus more likely to show 133 extensive carrying as compared to mothers with younger infants (Watson and Matsuzawa 134 2018) . 135

The existence of multiple -sometime contrasting -hypotheses is likely a reflection of the 137 small and highly variable data available and the diversity of potential drivers of this 138 behaviour across different species. A recent systematic study on 18 primate species (n=48 139 cases) showed that duration of infant carrying is affected by the age of the mother, with older 140 mothers carrying for longer periods (Das et al. 2019 ). However, some species do not fit this 141 pattern, with previous findings by Sugiyama and colleagues (2009) detecting no effect of age 142 in a large study on Japanese macaques. Infants that died of sickness were carried for longer 143 than those who were stillborn or victims of infanticide, while the age of the infant did not 144 follow, or only to follow at an extended distance, individuals who are experiencing high-210 stress events, such as maternal loss. We considered a mother to be carrying a dead infant if 211 they were seen to be doing so on the day following their infant's death. In doing so, we may 212 underestimate occurrences of shorter carries (i.e., under a day), or the total duration of 213 carries. Similarly, as we rarely observed the moment that the mother stopped carrying the 214 dead infant, our estimation of duration may be particularly conservative. However, given the 215 challenges in discriminating the precise moment of infant death from, for example: 216 unconsciousness, we felt that a conservative approach was appropriate. individual because we observed behavioural cues known (or assumed) to be associated with 239 greater than typical arousal (e.g., self-scratching and vigilance) in her interactions with other 240 chimpanzees and we did not want our extended presence to further impact these. 241

Observations of her behaviour were taken on an ad libitum basis whenever she joined the 242 party of chimpanzees that included a focal individual, but we made an effort to locate and 243 observe her for a brief period of time each day to obtain regular updates on her and her 244 infant's state of decomposition. During the births and deaths of UP's infants, regular research 245 practices had been adjusted due to the Covid19 pandemic. In 2020 activities were restricted 246 to shorter hours of observation (7:30 to 13:00) and limited to CH and the permanent field 247 staff, who focused primarily on health monitoring of the chimpanzees during this period; in 248 late 2021, at the time of UP's second extended infant carry, restricted research activities had 249 resumed. Researchers and field staff opportunistically noted any unusual behaviour exhibited. 250 Particular attention was given to how the bodies, and in one event a potential substitute 251 object, were transported, the response of nearby individuals to the mother or the carcass, the 252 interactions of the mother with the corpse, and the state of the corpse. We were not able to 253 collect physiological samples from either corpse to perform laboratory analyses on the cause 254 of death, nor we were able to retrieve either body for autopsy. died together with their mothers and 12 because they were partially dismembered or 264 cannibalised during infanticides. Of the remaining 53 cases, for 46 (87%) we were able to 265 estimate the infant's age at death (±1 month). The majority (n=25; 54%) died within the first 266 month, 17 (37%) at 1-month to 1-year old; 3 (7%) at 1-to 3-years old, and one (2%) at 3-to 267 5-years old. 268

We observed 12 carries of dead infants by their mothers (Table 1) , 23% of observed 270 opportunities (n=53). To be included as a case of dead infant carrying we required that the 271 mother be seen with the infant the day after death was estimated to have occurred. In nine 272 cases the minimum carry length observed was 1-3 days, in three cases we observed a longer 273 minimum carry of n=18, n=56, and n= 89 days. These are described in more detail below. 274

The 12 carries occurred in both primiparous (n=1) and multi-parous females (n=11), 275 including a 7 th born infant. However, these observations are likely an under-estimate of the 276 frequency of dead infant carrying behaviour in Budongo mothers. In 36 the mother 277 reappeared alone and could have carried for an unknown period prior to this. In total there 278 were 29 cases where the mother and dead infant were seen together, of these 12 included a 279 death with the mother or infanticide with cannibalism. Of the remaining 17 cases, 12 showed 280 carrying of the dead-infant, a rate of 71%. Of the five cases where the mother was observed 281 with the dead infant but did not carry it, all were infanticides (without cannibalism We found no evidence for a clear effect of seasonality on the onset of carrying behaviour, but 293 our sample size is small (see Fig. 1 ) showed no atypical reactions to KET or to the corpse. Based on the fact that most 324 had shown no other sign of illness, the likely cause of death was inferred to be respiratory 326 infection. During the first day KET was observed scratching herself repeatedly before 327 approaching a water area and when sitting close to a sub-adult male. These scratches 328 appeared to be a sign of arousal (fast and repeated, and not accompanied by grooming or 329 response waiting). On several occasions she moved her hand over the dead body apparently 330 to chase away the flies. Other than this, during the entire 18-day period, she was never 331 observed to provide any direct maternal care (grooming, inspecting, touching, or peering) 332 other than carrying, and regularly left the body at short distances (up to 5m) without visually 333 monitoring it. She did not stop others from approaching herself or the dead infant. When 334 moving or feeding in a tree, the dead body was usually (15 out of 16 observations) placed in 335 her right leg pocket, when on the ground she carried the body in her hand or arm (see Online 336

Resources). On one occasion a nulliparous young adult female (MON) was observed to 337 briefly carry the corpse in one hand while KET followed her. Across the 18-days KYO's 338 corpse decomposed, initially increasing in smell. By the 4 th day, no hair remained on the 339 body. By the 9th day, the body looked "dried". By the 10 th day the pungent smell and number 340 of flies decreased. It is likely that at this stage the body was completely mummified. No other 341 chimpanzees responded noticeably to either the smell or the flies. On the last day of observed 342 carrying, the body was still intact with only eyes missing and one deformed ear. 343 By the 8 th November the corpse appeared fully mummified. UP was last seen with the corpse 358 on the 19 th November, a minimum carry duration of 56-days (although likely several days 359 longer given corpse appeared partially dry on first observation). She was next seen on the 360 23 rd November. When approaching a water hole at the base of a tree, she carried a twig 361 50cm long in her mouth. As she reached the hole she transferred the twig to her hand and 362 left leg pocket, drank, and then returned it to her mouth (see Online Resources). She 363 continued to carry the twig throughout the morning, including while climbing large trees, and 364 when patrolling with the group over several kilometres. She was seen on the 24 th November, 365 and 3 rd and 4 th December, and was again observed to be carrying a similar twig consistently. 366

She was not seen to put it down on the ground. She was seen briefly on the 5 th December, but 367 it was not clear if she had a twig with her, and when she was next observed in the new year 368 (30 th January) she no longer carried anything. 369 370

UP was first seen on the 28 th August 2021 with another dead infant (UP4), estimated to be 1-372

week old. While we did not see her with a live infant, and it is thus at least possible that the 373 infant was not hers, we believe this to be very unlikely. UP was last observed in maximal 374 oestrus approximately 8 months prior to being observed with the dead infant, and all other 375 Sonso females were either confirmed to be pregnant, had unweaned infants at the time, had 376 been observed cycling regularly in the months prior to the observation, or were considered to 377 be post-reproductive. Finally, we know of no other reports of extended carrying of non-kin 378 dead infants. The infant's corpse had started to dry out but had a strong smell and on the 30 th 379

August flies could be seen hovering around it. Given that the corpse still had a strong smell 380 but was already partially dried, it was assumed to have died at least one week prior. The 381 cause of death was unclear; however, UP was observed with wounds on her head and on her 382 left arm. UP was observed using three main carrying styles when traveling on the ground or 383 moving in trees. She either carried the corpse in one hand (typically left one), in the mouth, 384 or in one leg pocket (typically left one) (see Online Resources). When resting, she placed the 385 corpse on her lap, in a leg pocket, held it in one hand, or placed it on the ground close to her. 386 to the corpse, though she was observed moving her hand around the dead body to chase away 388 flies on several occasions. On one instance UP was victim of aggression from other females 389 during which she dropped the corpse, and then followed the group when traveling and left the 390 corpse behind. Soon after, she was observed returning to retrieve the corpse. We observed a 391 juvenile male orphan (KJ) following her and peering close to the corpse on a few occasions. 392

No other individual was observed taking interest in or showing response to the corpse. 393

Throughout the observation period, UP was often seen in large groups and regularly 394 socialising with adult males (e.g., grooming). On this occasion there were no observations of 395 object carrying. UP was seen carrying the corpse on: the 28 th , 30 th and 31 st August; the 2 nd , 396 6 th , 8 th , 9 th , 11 th , 13 th , 14 th , 16 th , 18 th -23 rd ,24 th , 25 th and 29 th September; the 7 th , 12 th , 13 th , 15 th -397 21 st , 26 th , 28 th October; and the 3 rd , 10 th , 14 th and 17 th November. On the 18 th November she 398 was seen without the corpse and had resumed her sexual cycle (with visible sexual swelling) 399 for the first time since the last pregnancy. 400 carrying were relatively short (minimum confirmed carry length of a few days); however, we 441 also reported three prolonged cases of extended infant carrying. Our observations suggest that 442 these mothers, despite the evidence of irreversible loss including absence of any resemblance 443 to living infants, continued to experience a strong attachment to their deceased infants. 444

Neither female had any other living offspring and one, after eventually abandoning her dead 445 infant after 56 days, carried an object: a twig, for at least another two weeks. In the three 446 cases of prolonged carrying that we report, dead-infant carrying was not accompanied by 447 other forms of maternal care, such as grooming or other forms of maternal attention or 448 interactions, which sometimes occurs very early after an infant's death (Matsuzawa 1997; 449 Biro 2011), suggesting that the two mothers had become aware of the biological facts. Both 450 mothers were forced to use atypical modes of infant carrying, including mouth carrying, more 451 typically used for objects (Lonsdorf et al. 2020) , as live infants cling to the back or belly of 452 chimpanzees do not often cannibalise their own dead infants (but see Fedurek et al. 2020 for 454 two exceptions). Overall, these data suggest that the 'unawareness hypothesis' is unable to 455 fully explain chimpanzee behaviour towards dead conspecifics. 456 providing support and UP's cases providing counterevidence, it may be worth noting that 514 these were UP's third and fourth infants in a five-year period, the first two having been killed 515 at under a month old in within-community infanticides (one suspected, one confirmed). As a 516 result, it may be difficult to assess the nature of her bond with these infants. Her possible use 517 of a 'substitute object' in her carrying of a twig together with the even more prolonged 518 second carry suggest she had a particularly strong motivation to carry. These observations, 519 combined with the fact that all recorded instances of carrying in our dataset concern infants 520 who died before weaning age, seem to indicate that maternal behaviours, which are not 521 limited to maternal care, and the bond between the mother and the offspring likely play an 522 important role in dead infant carrying (Fernández-Fueyo et al. 2021). 523 Wrangham 2010). This behaviour typically peaks in juveniles and is more frequent in 550 females and while it is observed in some adult females it ceased once they became mothers 551 (Kahlenberg and Wrangham 2010) . The description of log doll use in Bossou is of particular 552 interest here, as it was carried by a juvenile female during the period that her mother was 553 carrying her sick infant sister, who subsequently died and whose body was also then carried 554 (Matsuzawa 1997 ). UP's behaviour was observed multiple times over several weeks. Unlike 555 the descriptions of other 'dolls' she was not seen to play with or interact with the object, 556 treating it instead in the same way as she had her infant's corpse. Thus, in addition to object-557 carrying being associated with the absence of infants in nulliparous mothers, it may also be 558 associated with the loss of an infant in bereaved chimpanzee mothers. In humans, the use of 559 transitional objects has been suggested to function as a coping mechanism for grief following 560 a bereavement (Graham et al. 1987; Lister et al. 2008) . A similar suggestion has been made 561 for beluga whales where both wild (Smith and Sleno 1986 ) and captive (Kilborn 1994) , 562 individuals have been seen to carry inanimate objects, apparently as 'surrogates'. The captive 563 whale carried a buoy followed the the removal of her dead calf immediately after birth 564 (Kilborn 1994) , and in the wild observations included carrying of planks and netting (Smith 565 and Sleno 1986). Further observations are necessary to validate the use of object carrying 566 following the death of an infant as a coping mechanism in primates, 567 568 To sum up, our observations are consistent with previous observations that chimpanzee 569 mothers respond to the death of their infants with carrying behaviour across communities. 570 aware of the loss but are continuing to display a strong attachment to the bodies of their 572 infants and may be affected by psychological processes akin to human grieving. 573

Nevertheless, more detailed hormonal data are needed for a test of this potential mechanism. 574 A combination of ecological conditions favouring mummification, and social factors, such as 575 the strong bond shared between mothers and their infants, may explain the three particularly 576 extended carries by Budongo chimpanzees. While we did not observe other indications of 577 maternal care in these cases, we are cautious about interpreting this as a wider absence in 578 Budongo mothers. Mothers' pattern of behavioural responses to death may be individually 579 specific and nuanced, resulting from a combination of physical, ecological, and psychological 580 factors, and more observations are needed to generalise at the population or species level. 581 Our interpretations are limited by the small number of observations and the multitude of 582 possible influential factors to consider. We encourage researchers and long-term field sites to 583 continue to report the rare behaviours observed in different populations, for example by 584 contributing to open-access databases such as 'ThanatoBase' 585 (http://thanatobase.mystrikingly.com), to allow a richer exploration and more robust 586 hypothesis testing of non-human primates' reaction to death through data sharing and 587 collaborations across sites. 588

We are grateful to all field assistants of the Sonso and Waibira communities who provided 591 essential assistance throughout the observation period. We are thankful to the management, 592 staff, and researchers of the Budongo Conservation Field Station for their support and thank 593 the project's founder Vernon Reynolds. We thank the Royal Zoological Society of Scotland 594 for their long-term financial support to the field station. We thank the Uganda Wildlife 595 work in Uganda. We also thank André Gonçalves 

A primatological perspective on death

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A comparative perspective on the evolution of mammalian reactions to 615 dead conspecifics

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prolonged carrying, non-624 mother carrying, and partial maternal cannibalism

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Mortality of wild and captive chimpanzees

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Death and bereavement across cultures

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Anecdotes in primatology: temporal trends, 758 anthropocentrism, and hierarchies of knowledge

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The chimpanzees of the Budongo forest: Ecology, behaviour and 767 conservation

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