Awareness of death in non-human animals (Part I)

Awareness of death in non-human animals (Part I)

There are many documented cases in which different species of animals have shown different types of behaviors toward dead bodies. Although the cases can be considered anecdotal observations and involve small sample sizes, they induce to think that feeling pain for a loss and being aware of death is not unique to humans. In this article we will discuss some cases in which various animal species exhibit surprising behaviors regarding death.

In adult humans the concept of death involves understanding four components: inevitability (all living organisms will die), irreversibility (a dead individual cannot return to life), non-functionality (a dead individual cannot feel, think, perceive or act) and causality (death as a consequence of the malfunction or non-function of one or more vital bodily functions). According to studies, children understand these 4 concepts at the age of 10, although it may vary depending on the child’s experience and maturity.

Awareness of death in non-human primates

From the long-term studies begun by Jane Goodall and Toshisada Nishida, it is known that female chimpanzees often transport the bodies of their dead offspring over a period ranging from a couple of days to several months. In a case documented in 2009, a mother suddenly reappeared in the group carrying a dead young chimp. The hypothesis of the author of the article, T. Kooriyama, is that the chimpanzee would have been stillborn (1-2 days ago), as its head seemed to be pressed at nose level. In addition, there was no sign of cannibalism on the body. When the mother appeared with her, two of the chimpanzees in the group made a display (i.e. demonstrations of strength) towards her. Afterwards, they all sat around the body and one of the males inspected it.  Then a female moved the body to a tree and inspected it as well. Later, the same female took the body, shook it, pushed it violently to the ground and then took it out of sight of the group, appearing half an hour later without the corpse. This observation reveals that a female chimpanzee can carry her dead offspring even when not enough time has passed to establish a mother-daughter relationship. In addition, it is likely that the mother would have continued to transport the corpse if she had not met the group, as she tried to recover her offspring’s body several times.

The following case is also very shocking because it involves the use of tools on a corpse. The young chimpanzee Thomas died from a lung infection. A group of researchers at the University of Saint Andrews (Scotland) observed in this group of chimpanzees in Zambia that when the chimpanzee died, the others showed curiosity about him, visiting him at least once and gathering in a circle around him. When it was time to eat, everyone disappeared except her adoptive mother, Noe, who sat with the body. Shortly after being left alone, the mother removed the leftover food from her son’s mouth with a stalk of grass (video). Then she took a pile of herbs and put them in his mouth. The researchers observed that after removing the herbs, Noe examined them, as if looking for something, and reintroduced them. In addition, she rubbed and inspected the teeth one by one. It is not known if this can be a funerary ritual similar to that of the human being, but as the director of the research group, Edwin van Leeuwen, rightly states, it is one more sample of the existence of compassion in non-human primates.

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An adult female chimpanzee inspects the corpse of her offspring (left) and leaves the body on the ground while feeding (right). Anderson, 2016.

Curiously, the reactions observed are different depending on the type of death. One example is the death of Pansy, a 50-year-old chimpanzee who lived in a Safari along with other fellows, including her 20-year-old daughter. In the days before her death, as if predicting what was to come, her companions were very attentive to her and during the 10 minutes before her death, her group companions groomed and caressed her 11 times, more frequently than in the days before. However, none of them groomed her after she died, although they inspected her mouth and manipulated her limbs. Her daughter, Rosie, remained next to her mother’s body for most of the night, on a part of the inner platform where she had never slept before. The reactions of the other chimpanzees were also interesting, since while they slept in their nests, they changed their posture between 11-42 times, when the usual is that they change between 0-14 times of posture during the night. In addition, the male made 3 displays that night, when in previous studies they saw that he had made the same number of displays (3) but in 29 nights. In addition, after each display it ended up attacking the corpse. During the following days, the group of chimpanzees remained deeply subdued and they ate less than usual. Interestingly, none of them slept on the same platform where Pansy died until a week later. In contrast, a case was documented in which an adult died after falling from a tree. The chimpanzees present carried out aggressive displays accompanied by alarm calls and much mutual contact. Something similar happened when a juvenile died from a leopard attack.

It has also been seen that chimpanzees (and also gorillas, as we showed in the article about Koko, when she reacted sadly to the death of her beloved kitten All Ball) even react sadly to the communication of a death of another species.  This is the case of Washoe (1965-2007), a female chimpanzee who was “raised” by doctors Beatrix T. and R. Allen Gardner in 1966 after being orphaned (her mother was murdered in Africa) and was then “adopted” by Professor Roger and Deborah Fouts in 1970. Washoe became the first chimpanzee to be taught American Sign Language (ASL). Like Koko, Washoe was able to communicate fear, joy, sadness and empathy. One of her caregivers (much loved by the chimpanzee), Kat, was pregnant and she had to absent for a while. When she returned, Washoe ignored her at first; she was angry with her for her absence… Until Kat could explain herself. What happened is that the caregiver had a miscarriage and unfortunately lost the baby, telling Washoe “my baby died”. The chimpanzee responded with the words “cry” and “please person hug”. Washoe previously gave birth to two babies and both died prematurely. On one of these occasions, after Washoe’s baby was taken away from her because of her death from illness, she asked Fouts “baby?”, to which he replied “baby dead, baby gone, baby finished”. According to Fouts, the chimpanzee dropped her arms on her lap and went to a far corner where she remained with a lost look.

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Washoe y Kat. Friends of Washoe

In the 1960s, there were also reports of mountain gorillas (Gorilla beringei beringei) transporting their dead calves for 2-4 days. Until recently the transport of dead bodies by females who were not related to the offspring had never been documented. However, the research group led by Ymke Warren observed at the Karisoke Research Centre (Dian Fossey Gorilla Fund International) how four females transported the carcasses of two infants from 15 to more than 24 days. Two of the females were first-time mothers (the mothers of the two dead calves) and the other two were nulliparous females, that is, they had never given birth, but they were in the last months of gestation. In spite of the deterioration of the bodies throughout the days, the females treated them as if they were alive: they groomed and defended them if other gorillas approached. The reason why the unrelated females transported the corpses could be explained by the hypothesis of “learning to mother”. It seems probable that the benefits of learning to be a mother can be obtained with corpses, since the motor skills necessary to carry a calf while travelling and looking for food can still be acquired. It should be noted that the offspring of the two females who had not given birth at the time of the observations survived successfully. It is possible that all this was caused by the internal state of the females, since according to several articles, the females of non-human primates are hormonally predisposed to be mothers in the last weeks of gestation.

The Japanese macaque (Macaca fuscata) is another well-studied primate species where the transport of dead calves by their mothers has also been documented. And not only do they transport calves that do not reach 1 month of age, but also older calves, although according to an observational study carried out over 9 years, the percentage of transported calves that died between 1 and 30 days after birth was higher. This could be explained because at that stage the calf is heavily dependent on the mother, which would reinforce the mother in her motherhood. Sometimes even a corpse can be transported until it is mummified. In addition, as in other species, the mothers exhibit behaviors with the bodies as if they were still alive, protecting them, for example, if some curious congener approached the body without life. It has also been seen that these behaviors are not different between first-time mothers and more veteran mothers, so it is possible to think that it is not a learned behavior.

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Macaco transporting the body of an almost mummified calf. Sugiyama et al., 2009

The Japanese macaque (Macaca fuscata) is another well-studied primate species where the transport of dead calves by their mothers has also been documented. And not only do they transport calves that do not reach 1 month of age, but also older calves, although according to an observational study carried out over 9 years, the percentage of transported calves that died between 1 and 30 days after birth was higher. This could be explained because at that stage the calf is heavily dependent on the mother, which would reinforce the mother in her motherhood. Sometimes even a corpse can be transported until it is mummified. In addition, as in other species, the mothers exhibit behaviors with the bodies as if they were still alive, protecting them, for example, if some curious congener approached the body without life. It has also been seen that these behaviors are not different between first-time mothers and more veteran mothers, so it is possible to think that it is not a learned behavior.

Cases have also been documented in which not only the dead calves were transported by their mothers, but also by other females in the group and even females from another group in a primate more genetically distanced from humans. This is the case of gelada (Theropithecus gelada). As in chimpanzees and gorillas, they also observed how mothers and other females groomed corpses.

gelada_muerte_transporte_crías
a) Adult gelada holding its mummified calf 10 days after its death. b) A close-up view of the mummified calf. c) Adult gelada carrying its calf until 48 days after its death. The arrow indicates where the skin of the calf’s head had decomposed. d) Adult gelada grooming its dead calf. e) Juvenile gelada transporting the corpse of a calf of another female in the group. f) Juvenile gelada grooming the corpse of a calf of another female in the group. Fashing et al., 2010

These curious practices would not be a consequence of mothers understanding the concept of death necessarily. However, these behaviors would be biologically illogical, since they do not seem to benefit the mother at all as there is a waste of energy in the transport and care of the corpse. Therefore, there continues to be unknowns in this regard.

The possible evidences that these animals worry or feel their relatives death are not only observational. Some researchers found that wild adult female chacma baboons (Papio ursinus) in Botswana had high levels of glucocorticoids (stress indicators) just after a close relative died from a predator. While other females in the same group, but with no equivalent loss did not exhibit such increased stress.

Awareness of death in dolphins

Epimeletic behaviours (behaviours that provide care and attention) have been documented in several species of cetaceans, both in the wild and in captivity, such as the short-beaked common dolphin (Delphinus delphis), the humpback whale (Megaptera novaeangliae), the pilot whale (Globicephala macrocephalus), the harbour porpoise (Phocoena phocoena), the rough-toothed dolphin (Steno bredamensis) and especially the bottlenose dolphin (Tursiops truncatus). However, the question that concerns us here would be whether any of these species have been seen to have reacted to the death of an individual and if so, what those reactions or behaviours were.

During a routine trip, a research group observed a group of six bottlenose dolphins moving slowly along the coast. As they approached they saw that two of them were trying to hold a dead calf of about 1.5 m at the surface. As the boat approached, the calf was thrown to the bottom, but when the boat retired, the same dolphins lifted it back to the surface. This action was repeated several more times, while the rest of the dolphins remained about 150 m away. The event culminated when the two adults pushed the calf back to the surface, but this time they released it. The researchers were unable to recover the body, so the cause of death is unknown, although no cuts or abrasions were visible. Nor is it known how long they endured the corpse or whether they would have continued to do so if they had not been disturbed. Even so, this case provides strong and direct evidence of epimeletic behavior in free-ranging dolphins, which would have clear implications for the survival of genetically related dolphins.

On another occasion, several fishermen observed an adult dolphin that appeared to be trying to prevent a calf from stranding on the coast. Other dolphins moved clockwise around the presumed mother and calf. When fishermen tried to approach the group, the circulating dolphins began to clap their tails. The dead calf was swollen and with its mouth open. A day later, a son of one of the fishermen came across a similar scene: an adult kept the dead calf afloat while other dolphins swam around them clockwise.

On another occasion it was reported that there was a dead dolphin floating. When the volunteers arrived, they observed an adult pushing the body with its face. As the boat approached, the adult submerged the body and appeared on the surface 50 m beyond. One of the volunteers was able to approach and when he grabbed the calf’s tail, the presumed mother continued to push the body, making it appear that it was still alive. When they knew for sure that the calf was dead, they put the body in the boat and the mother began to swim frantically under and near the boat. Examination of the body revealed bite marks and scratches, the latter present on the right flipper, probably where the adult had held him. Still, the cause of death was inconclusive.

Another group of observers, led by Dave Anderson of the Whale Watching Safari, saw a group of bottlenose dolphins near their boat. The amazing thing was that one of the adult dolphins, specifically a female, carried the body of her dead calf on her dorsal fin (video). According to Anderson, the calf would have been dead for several days, possibly even weeks, as the flesh was rotten. He also pointed out that the animal would probably keep the calf close to the surface so that it could breathe. He assumed this because dolphins do not usually swim with their dorsal fins sticking out of the water continuously, as the female did.

The research group of the Tethys Institute in Italy, led by biologist Joan Gonzalvo, documented a similar behaviour in the waters of the Ionian Sea in this species of dolphin as well. They observed how a female interacted with her dead calf. Depending on the state of the body, it could be deduced that death had occurred a few hours earlier. The mother repeatedly pushed the calf’s body to the surface, resembling an attempt to bring the calf back to life, as Gonzalvo explained.

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Female dolphin interacting with her dead calf. La Vanguardia

A slightly different case occurred off the coast of Mikura Island (Japan). A group of scientists found a dead female dolphin and they tried to recover the body as it was shallow. However, this was impossible because two male dolphins were guarding the body and prevented the observers from approaching.

So far we have mentioned cases in which dolphins react to the death of their fellows but… do they react to the death of other species? A fascinating event is what happened to biologist Denise Herzing. During an exploration, a group of dolphins that had already studied before, remained 15 m away from the boat, when the usual for them was to approach to greet and swim in the wake of the boat. Then, Denise and her companions realized that one of the people on the boat had just died in their sleep, so the boat made its way back to port. The group of cetaceans escorted the ship, flanking it about 15 m to the port. When the boat later returned to the sea, the dolphins behaved as usual, approaching to say hello and swimming in their wake. According to the researcher, in her 25 years of dealing with these dolphins, she never saw them behave in such an astonishing way. Did they detect in any way that there was a dying person in the boat? For the time being, it remains a complete mystery.

While the bottlenose dolphin is possibly one of the most studied marine mammals, attention to dead offspring has also been observed in other marine mammals such as the sea otter (Enhydra lutris), the Caribbean manatee (Trichechus manatus), the Californian sea lion (Zalophus californianus) and the common seal (Phoca vitulina).

Awareness of death in elephants

Although the existence of “elephant cemeteries” has been documented, it is not true that these animals go to a particular site when they are going to die. These places with large concentrations of elephant bones seem to indicate that the individuals had died in groups, possibly due to hunting or natural disasters (e.g. periods of drought).

African elephants (Loxodonta africana) not only react dramatically to the corpses of other elephants, they also use their trunks to examine the bones and tusks that they find. In an experiment in which researchers showed a group of elephants several skulls, ivory and wood, it was observed how the animals also touched the ivory with their feet in some cases. In addition, among these three objects in the experiment, elephants showed a greater predilection for ivory. In another experiment in which they provided elephant, rhinoceros and buffalo skulls to the subjects of the experiment, the elephants expressed a clear preference for the skulls of members of their species.

That’s not all. After decades of study, researcher Cynthia Moss discovered that African elephants recognize their dead relatives even if they can only access the bones. On one occasion, this researcher observed how a group of elephants passed near several jaws that had previously been collected for analysis. The entire group stopped to examine them and then continued on their way, but an 8-year-old individual spent several more minutes manipulating one of the jaws. That jaw had apparently belonged to his mother, who had died several years earlier.

In some cases it has also been seen that elephants not only help dying individuals or show special interest in corpses related to them, but also do so with individuals from other unrelated groups. A clear example is the elephant Eleanor, the matriarch of a family unit called First Ladies. One day Eleanor fell to the ground because of a problem with her hind legs. A female elephant from another group, Grace, went to help her, trying to stand her up to walk several times, but Eleanor was very weak and could not even stand. While the rest of the elephants in both herds continued on their way, Grace stayed to watch Eleanor until the sun went down. Unfortunately, the elephant died a few hours later. In the days that followed, up to five groups approached, smelled, touched the body and bowed to it. Of course, so did members of the same family unit. All these cases are clear examples that elephants, like humans, can share emotions such as compassion and have awareness and interest in death.

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Grace trying to get Eleanor on her feet as night fell. Douglas-Hamilton et al., 2006
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Individuals from another family unit (Biblical Towns) and Eleanor’s 6-month-old offspring visiting the corpse of the matriarch of First Ladies. Douglas-Hamilton et al., 2006

According to James R. Anderson, a professor in the Department of Psychology at Kyoto University:

“Other authors have made strong arguments for extending the capacity to grieve to other large-brained, socially complex mammals, notably elephants and cetaceans. But what of the four components of human adults’ understanding of death that were mentioned earlier: inevitability, irreversibility, non-functionality, and causality? Evidence appears strong enough to suggest that for large-brained animals the second and third components apply. However, it remains unknown whether they are capable of understanding that all creatures die (including themselves) and understanding the biological causes of death.”

However, much remains to be studied and future research will provide much to talk about. For the time being, the evidence acquired so far forces us to reflect on the emotional intelligence of animals. How we treat them inhumanely on many occasions. How, in spite of everything, they are not so different from us and how all those psychological and intellectual traits that we have always considered exclusive to our species are more distributed than we believe. Perhaps it is time to change our view of these beings who share this piece of the universe with us. We do not take this matter for granted. Soon we will publish the continuation, in which we will expose new cases with other species and we will discuss in depth if the animals really understand the concept of death. Stay tuned.

 

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