How Animals Grieve

by Barbara J. King

  Aware of the reptilian danger, the monkeys do post a lakeside guard when low-rankers go into the water. The guard’s job is to send up a cry of alarm when the big lizard is sighted. With a vigilant guard on duty, this method works well enough. On the day in question, however, the guard dozes off as a young monkey is foraging in the lake. By the time other monkeys spy the lizard and cry out, it is too late. The camera captures the monitor trundling off with that peculiar side-to-side lizard shuffle, a dead monkey clamped in its jaws. No one follows. The monkey’s group-mates attempt no rescue. The lizard isn’t mobbed, the monkey isn’t visibly mourned.

  Later, another toque macaque is shown dead beneath a tree, the loser in a male-male fight for group leadership. His limbs are stiff, his mouth stretched in a mild death grimace. His groupmates approach, including some of his offspring; seven or eight monkeys at once crowd the body. Some lean in and take a sniff, others touch the corpse—when one monkey touches the dead one’s locked-upright hand, the hand jerks rigidly back into place. After a while, the curious monkeys move on. The dead leader, beneath the tree, is abandoned.

  The monkeys’ responses to these two deaths may represent commonplace scenarios among wild animals. The young monkey’s death happens swiftly, and the body departs the scene in the predator’s jaws. What, if anything, the surviving monkeys think or feel about the event is opaque to us. In the case of the older leader dispatched by his rival, the group response is notable. The body is explored through sight, smell, and touch. To a human observer, it’s clear that the monkeys who surround the body know something is anomalous: they surely aren’t confusing their dead groupmate with a resting, sleeping, or wounded animal. There are no outward signs of grief.

  In the wild, members of tightly knit primate groups experience a great deal of loss. As reported by primatologist Jeanne Altmann in her now-classic book Baboon Mothers and Infants, the mortality rate for Kenya’s Amboseli baboons approaches 30 percent per annum in the first two years of life. After that, it plunges, but then it rises again, and in adulthood, females suffer a death rate of 12 percent. Though these numbers are specific to certain monkeys during a certain slice of time, demographic profiles suggest they are not unusual for wild animal populations more generally.

  Experiencing the death of a groupmate, then, or even of one’s offspring or other close kin or social partner, is far from rare for group-living wild animals. If we think about mourning and grief in terms of evolutionary theory, a negative hypothesis (the “null hypothesis,” in scientific terms) may come to mind: Wild animals faced with the challenges of survival and reproduction should not expend time or energy on the expression of grief when a group member dies. A weaker version of this same hypothesis would be that wild animals should expend time or energy on grieving only when the resources required for survival are available in sufficient abundance.

  If a death provokes no particular emotional response, might this absence of grief be explained as an energy-saving strategy that is under the control of natural selection? If so, might some of the survivors feel emotion but simply ignore it? Or are no emotions felt? By observation alone, without the invasive measures of stress physiology, we cannot distinguish between these alternatives. (We’ll consider what those invasive measures do teach us in a moment.)

  If any toque macaque is likely to mourn the death of the youngster plucked from the lake by the monitor lizard, it would be his mother. The mother-infant relationship in macaques, as in almost all primates, is exquisitely close. Research shows that in rhesus macaques, a close relative of the toques, mothers and infants share what’s called reciprocal face-to-face communication. This suite of behaviors between moms and babies involves smacking of the lips, mouth-mouth contacts, and, most significant of all, sustained mutual gaze.

  Think of how important mutual gaze is in our own species, as bonds develop between babies and their caretakers. A memory so vivid that I’ve carried it for nineteen years comes from my daughter Sarah’s infancy. It was a Saturday, exactly four weeks since her birth. I was carrying Sarah in my arms across the street in front of our house, on my way to pay a welcome call on new neighbors. When I glanced down at her, bundled up against the chill November air, she locked eyes with me and let loose with a huge smile. It was what developmental psychologists call a social smile, the kind of aware, intentional smile that is set apart from the reflexive mouth movements of a newborn. To me, a tired but otherwise besotted new mother, the mutual gaze and first social smile meant one thing: my baby was loving me back.

  The contours of the emotional relationship between monkey mothers and babies aren’t well studied. It’s reasonable to expect, though, that gaze and facial expressions shared across the generations both enhance infant survival and cause feelings of comfort or pleasure to flow within the pair. Newborn monkey babies cling to their mothers’ bellies; in the beginning, the mother is the infant monkey’s universe, the source of all warmth, nutrition, and safety. For the mother, infant care is all-consuming. She starts out carrying the infant on her body around the clock (except in a few monkey species where dads and siblings help out). Moms may bounce their babies, play with them, smack their lips in affection toward them, and try to catch their babies’ eye to facilitate that mutual gaze.

  That many monkey mothers lose their infants early on is something we know from the mortality profiles. When this happens, some mothers simply put down the body, or leave it where it fell, and carry on with their lives. No visible grief seems to accompany these acts of abandonment. Other mothers, though, continue to carry their infants’ dead bodies. Could this carrying be an expression of maternal grief ?

  Maternal carrying of infant corpses was monitored by primatologist Yukimaru Sugiyama and colleagues for more than two decades in one population of Japanese macaques, close relatives of the toque and rhesus macaques. These monkeys live on the slopes of southern Japan’s Mount Takasakiyama. Infant mortality is high, as we would expect in a wild population; based on an intensive nine-year period of data collection, the death rate within a year of rhesus birth was 21.6 percent. Maternal carrying of the dead was observed over a twenty-four-year span, during which 157 cases were recorded out of 6,781 rhesus births. The researchers compiled statistics on factors like infant’s age at death and duration of corpse-carrying by the mother. Within a week of death, 91 percent of rhesus the infants had been abandoned by their mothers. The longest maternal carry lasted seventeen days, by which time the small carried body was decomposing, fly-ridden, and reeking with a bad odor. Most of the other monkeys avoided that mother, and when juveniles showed an interest in the decaying body, they were rebuffed by her.

  In presenting these data, Sugiyama and his coauthors pose a key question: Does the carrying of dead infants signal maternal emotion or does it instead point to the mothers’ lack of awareness that their infants have died? The null hypothesis for this case must take into account the need for wild animals to budget their energy. The carrying behavior does, after all, represent a substantial energy expenditure by the mother. At Takasakiyama, the monkeys must traverse a steep hill every day, and with a dead infant in tow, mothers lose the free use of one hand. Their movement and their foraging are most certainly compromised. So why do they do it? What does it mean that mothers carried infants significantly more often if the death occurred within thirty days of birth? It was especially common if the infant lived more than one day but died within several days; as Sugiyama’s group notes, this pattern matches up with the time when the infant, not yet able to move around well on her own, begins to cling and breast-feed regularly. Not all dead infants were carried, however. It’s not as if some trigger associated with infant size, weight, or age pushes the mother into an innate response of carrying.

  What’s most curious to me is that infants who lived longer, and who presumably enjoyed a longer period of emotional connection with their mothers, were not carried longer than infants who were barely known by their mothers. Taking all of the data together, I can’t see tha
t the behaviors described for these monkeys fit comfortably with a claim of monkey grief.

  Maternal corpse-carrying behavior has also been described by Peter Fashing and his colleagues, who study the gelada monkeys of Guassa, Ethiopia. Large-bodied and long-haired, the Guassa geladas dwell in the grasslands of the Ethiopian highlands. Over a three-and-a-half-year period, fourteen females at Guassa carried dead infants, some for only an hour, others for much longer. Most carrying episodes lasted between one and four days, with three females carrying their infants for significantly longer periods: thirteen, sixteen, and forty-eight days. In these extended cases, the infants’ bodies gradually became mummified, and as with the Japanese macaques at Takasakiyama, they emitted an unpleasant smell.

  Forty-eight days is a long time to carry a dead body, and suggests to me a decisively willed action on the part of that mother. She resumed reproductive cycling while carrying her dead infant, and was even seen copulating while clutching the infant’s body with one hand. The timing of carrying and then abandoning the body cannot, in this case at least, be explained by hormonal changes that occur when an infant suddenly stops nursing. This mother carried her dead infant right through that period and beyond.

  Beyond the length of the carrying episodes, what’s striking at Guassa is the interest shown in the corpse by females other than the mother. In two cases, juvenile females were allowed to carry and groom the bodies of infants belonging to adult females in the group. Relatively small gelada groups forage independently during the day, but reunite and cluster together on nighttime sleeping cliffs. In one notable instance, Fashing’s team saw a female carrying a dead infant belonging to a mother from another group; this female groomed the body and allowed a juvenile female to do the same.

  HESTER WITH THE DEAD INFANT HISHAM. PHOTO BY RYAN J. BURKE.

  Even keeping in mind the conservation-of-energy hypothesis for wild animals, I found it surprising that mother monkeys in general don’t show more discernible evidence of grief. During my fourteen months in Kenya, I found the Amboseli baboons to be closely attuned to each other, smart and strategic in their actions, and ready to defend allies and friends. In reading published accounts and talking to other primatologists, though, I was forced to conclude that little evidence for monkey grief has emerged from observation alone.

  In fact, the report by Fashing and his colleagues contains descriptive passages that increase my sense of caution about concluding that monkeys mourn. Two geladas, a mother-infant pair named Tesla and Tussock, died in April 2010. Tesla, the mother, had been severely weakened by sickness that followed from a parasitic infection. During the period of her illness, two younger females helped her out by carrying Tussock, her seven-month-old daughter. But when Tesla became too ill to leave the group’s sleeping cliff, the other geladas departed to forage without her. Slowly, Tesla and Tussock managed to move to a spot about 175 meters from their sleeping position. When the group returned to the cliff that night, Tesla and Tussock’s new position wouldn’t have been visible to them. None of the geladas showed any apparent concern for their missing groupmates, and none searched for Tesla and Tussock. The next morning, the primatologists found Tesla dead. Throughout that day, Tussock, now on her own, stayed by her mother’s body, “crying plaintively and rocking side-to-side.” The next morning, the infant too was found dead.

  It seems likely to me that Tussock felt something upon her mother’s death. How could she not have felt afraid, left alone in the cold, outside the protective web of her group, with her mother lying inert and unresponsive? If she felt grief, she suffered it alone. When I asked Tyler Barry, one of the primatologists at Guassa at the time of these events, for his interpretation of what Tussock might have been feeling, he said, “I would not feel comfortable arguing that Tussock was feeling grief as she cried and rocked. I am pretty sure she hadn’t had milk for almost two days at that point and was probably dehydrated and reaching starvation point. I am sure the cold is what killed her in the end, though, and also may have been a cause of the rocking.”

  Barry confirmed that Tesla and Tussock’s location, away from their sleeping cliff, meant that their suffering would have gone unnoticed by their group. “There was a bachelor group that glanced down at Tesla’s dead body the morning of the second day,” he recalled, “but other than that they were too far away from the normal sleeping spot for the main herd to even hear Tussock.” Gelada males, then, who were not Tesla’s regular associates, showed a brief curiosity response to her body, but the monkeys who might have mourned were too far away.

  If grief does accompany the act of maternal corpse-carrying in monkeys, or an infant monkey’s solitary vigil at the side of her dead mother, we cannot know it from observation. So far, the null hypothesis, which predicts no great expenditure of energy on grief by wild monkeys, remains formidable.

  Primatologists Dorothy L. Cheney and Robert M. Seyfarth, among the world’s leading experts on wild monkey behavior, take note of monkeys’ lack of visible grief in their book Baboon Metaphysics. When monkeys carry infants who are dying, these scientists say, they treat them pretty much the same way as they do their healthy infants. Cheney and Seyfarth embed this observation in a broader context. Monkeys do not share food with sick companions, nor do they come to the aid of elderly or disabled group members. Baboon mothers specifically, they write, “often show a surprising lack of concern for their offspring’s anxiety and distress during water crossings or at other times of separation.”

  When mothers carry not a dying but a dead infant, other baboons show interest, as we’ve seen with other monkeys—but an interest of a limited nature. “In the minds of other group members,” Cheney and Seyfarth write, “the infant’s status seems to change soon after it dies: they cease to treat it as an infant.” The baboons inspect the corpse but never direct grunting vocalizations to it, as they would were the infant alive. They do not try to pry the corpse from the mother. Most interestingly, if the mother puts down the corpse and moves away, a close relative or male friend may guard the baby until she returns. If scientists approach the corpse with the aim of obtaining a DNA sample, group members may threaten them. Cheney and Seyfarth conclude that the baboons’ response is not an expression of grief or empathy but instead is organized around ownership—the idea that the infant once belonged, and indeed still belongs, to a particular female and to the social group as a whole.

  What happens when we add physiological measures to straightforward observation? Cheney and Seyfarth carried out their long-term baboon research at the Moremi Game Reserve of Botswana’s Okavango Delta; one study done under their supervision adds some biochemical insight to the question of monkey grief. Like the baboons at Amboseli, the Okavango baboons live in multimale, multifemale troops, and female relatives organize themselves into close-knit groups called matrilines. Grandmothers, mothers, daughters, aunts, nieces, and young sons and nephews all spend time close together in social grooming and social alliances. At puberty, the males transfer into another group. This pattern means that in any given group, the adult males tend to be strangers to each other, unlike the related adult females.

  In the Okavanga group, as at Amboseli, predation is quite high. During a sixteen-month period in 2003 and 2004, twenty-six baboon deaths were recorded. All but three were healthy animals. Ten were known to have been taken by predators, based on researchers’ direct observation of the attack or by the presence of the body; the remaining thirteen were suspected to have met the same fate, based on predator sightings or alarm calls vocalized by the monkeys.

  Living amid this sort of danger, the Okavango baboons become stressed, and that stress shows up in their bodies. Researcher Anne L. Engh and her coworkers collected fecal material from the female baboons in order to measure levels of the glucocorticoid (GC) hormone, a type of stress hormone that circulates in the body, then is excreted through bodily waste. The researchers found that in the four weeks following a predation event in the group, females’ GC levels increased measurably.
This finding makes intuitive sense; imagine witnessing a lion or a leopard stalking your circle of family and friends, then singling one out and and making a kill. Stress hormones in our bodies would flare up too under conditions like these.

  Probing further, the research team discovered the chemical signature of grief in the baboons. The GC levels of twenty-two “affected females,” each of whom had lost a close relative to predation, were compared to those of a control group made up of females who had experienced no such loss. The affected females showed significantly higher GC levels. Engh and her colleagues emphasize that while predator attacks were witnessed by many adult females in the group, only the “bereaved” females showed significantly higher levels of GC.

  The bereaved monkeys’ elevated stress levels lasted only four weeks, perhaps because the females soon began to increase the number of their grooming partners and the rate at which they participated in grooming. In monkeys, to groom and be groomed by a partner is a soothing social activity as much as it is a hygienic one. As Engh’s team put it, “Bereaved females attempted to cope with their loss by extending their social network.” While it’s rash to make facile comparisons between monkeys and humans, I can’t help but think of the person who, after mourning a loved one, gradually reaches out to potential new friends in the community, church, or workplace.

  I was also struck by Engh and her coauthors’ willingness to use the word “bereaved” in their scientific publication. Here was the first clear indicator that I had come across of monkey grief, and it was approached in terms of physiology rather than of social behaviors that might indicate mourning. But when I asked Engh whether any of the Okavango female baboons had shown signs of grief, I learned something that had not been mentioned in the peer-reviewed article. Engh shared her recollection of Sylvia and her adult daughter Sierra, two baboons who were unusually close. “They groomed each other almost exclusively,” Engh told me, “and spent much of their time together.” Then Sierra was killed by a lion. To Engh, Sylvia appeared depressed. She sat apart from the other baboons and did not initiate social interactions. This went on for a week or two. “Sylvia was high-ranking and intimidating,” Engh says, “so it didn’t seem unusual that other females didn’t approach her, but I was surprised that she had no apparent interest in interacting with anyone.” In fact, it was Sylvia’s behavior that led Engh to initiate the GC study. Sylvia had been close with her daughter, and when that closeness was stolen by death, it brought her to grief. As fits the monkeys’ pattern, Sylvia’s altered behavior lasted only a few weeks. She then widened her social circle by befriending other females.