Last July a female orca named J35 captured worldwide attention for her unprecedented vigil. J35, also known as Tahlequah, is a member of the closely monitored Southern Resident population of orcas in the Salish Sea, off the coast of Washington State and British Columbia. She had just given birth, following a nearly year-and-a-half-long gestation period. It was her second offspring, a daughter, and the first live birth in the declining Southern Resident community in three years. But 30 minutes after birth, the calf died. J35 would not let her baby go. With great effort, she swam with the tiny body on her head and made deep dives to retrieve it when it slipped off. Other members of her pod registered her distress: at one point, a group of females gathered in a tight circle around J35, an act of apparent emotional attunement that lasted at least two hours. Seventeen days and 1,000 miles passed before J35 finally released her daughter’s corpse for good.
J35’s response to her calf’s death was a powerful reminder that humans are not the only species that experiences grief. For decades animal behavior experts were wary of ascribing that emotion to other species. But our thinking has shifted as new evidence has come to light. Six years ago I wrote about the then nascent field of animal grief for Scientific American. Since then, the number of case studies has exploded. Some, such as the example of J35, capture fresh and poignant details from species already known to mourn; others document the phenomenon in new species.
Together these findings are yielding fascinating insights into the origins of grief. Previously it seemed that bereavement was associated with large-brained mammals—namely, primates, elephants and cetaceans. But the latest evidence indicates otherwise. Brainy mammals may grieve in more nuanced ways than some other animals because of their advanced abilities to reason and the complex social dynamics within their groups. It is now clear, however, that the expression of grief does not depend on relative brain size or cognitive power alone. The capacity to form intimate relationships is emerging as a significant, separate factor in determining which species mourn their losses.
The study of animal grief is still sufficiently new that investigators continue to wrestle with how to recognize it. In 2017, within the small mountain city of Prescott, Ariz., an adult female collared peccary—one of a small herd of five of the piglike mammals, also known as javelinas—died. Over the next 10 days the herd mates of this individual visited, ate near, slept right up against her body and protected it from predators. This prolonged response to death was recorded by a motion-sensitive wildlife camera, a birthday present to then third grade student Dante de Kort, who set it up two days after he noticed the peccary corpse near his home. When de Kort shared images of the animals’ behavior at his school’s science fair the next month, he met biologist Mariana Altrichter of Prescott College. That serendipitous encounter between the boy and the researcher led to the publication of an article on the peccaries in the February 2018 issue of the journal Ethology (de Kort was the lead author) and to a renewed conversation among scientists about the definition and scope of grief in the animal kingdom.
De Kort had stationed his camera five meters from the body of the female peccary and set it to take 10-second-long films at intervals of 30 seconds. It captured 93 videos with peccaries in them. For roughly half of the recorded time, herd members walked or stood within five meters of the dead individual. And for more than a third of the time, they contacted the body directly. At various points, they nuzzled, smelled, stared at, bit and tried to lift up the dead body. They also slept in direct contact with it and defended it from coyotes. In nearly half of the recorded time, the same two peccaries (at least, probably the same two, according to best efforts to identify individuals) were present at the body.
In their paper, de Kort and his co-authors noted that the peccaries’ responses expanded the behavioral complexity known for this group and showed that they resembled humans and chimpanzees in their reaction to death. But the scientists stopped short of calling the reaction grief. In fact, they stated that they “cannot determine if there is grieving.”
Peccaries belong to the artiodactyl branch of the mammal family tree. Other members of this group include sheep and antelopes. Little is known about grief in artiodactyls. But the peccaries’ behavior closely matches the criteria for grief I set forth in my 2013 book How Animals Grieve: Survivors alter their behavior in the wake of a death in significant ways that indicate intense distress. Depending on the species, these changes may include atypical patterns of eating or sleeping; withdrawal from social activities; and expression of upset at or near the body through vocalizations, facial expressions or body language.
Can we state with absolute certainty that the peccaries, or some of the peccaries, were grieving, as opposed to exhibiting a generalized distress about a change in the dynamics of their herd? No. My definition of grief relies on interpretation of cues made visible to us by individual animals, and in this practice, there is inevitably room for error because we cannot read animals’ minds or know their intentions. Yet given that we know peccaries form small, cohesive groups characterized mainly by cooperation and friendly interactions such as grooming, I find it just as risky to dismiss the strong likelihood of a grief response. In an e-mail to me, Altrichter explained that she and her colleagues did not want to interpret the emotional aspect of the peccaries’ behavior in their paper, preferring to stick to reporting the observable facts. But she allowed that the creatures’ response “meets a reasonable definition of grief for nonhuman animals.”
In the field of animal behavior, or ethology, the reluctance to claim grief outright in the peer-reviewed scientific literature stems from the discipline’s long history of bringing charges of anthropomorphism—the projection of human qualities or capacities onto other species—against scientists who venture into the realm of animal emotion. Those charges are sometimes still leveled within the scientific community today. Yet it turns out that it is the science of animal behavior itself that shows we humans have no monopoly on the expression of sorrow (or, for that matter, its opposite: joy) in the animal kingdom.
A clarification on terminology is key here. In the field of neuroscience, “emotion” is a body state triggered by external stimuli, whereas “feeling” is a mental state that accompanies the changes in body state. In this scheme, feelings are the conscious experiences. By using the term “emotion,” I do not mean to imply that animals are unaware of their own grief, though. In the framework I am using, common in anthropology and developmental psychology, perception and processing of stimuli in brain circuits do prepare an individual to express an emotion, but that emotion emerges in the context of an unfolding event between social partners. It is expressed by animals who are conscious, aware beings. For this reason, I would be surprised if researchers were to observe grief in social insects, such as ants, termites and bees, that retrieve and even sometimes bury corpses of dead companions entirely through a system of chemical signaling, as opposed to conscious decision-making.
Heartbreak all around
The peccaries provide strong evidence that the capacity for grief is not limited to large-brained animals. But they are not the only species to do so.
Film taken at the Donkey Farm Foundation sanctuary in the Netherlands shows distressed donkeys milling around and emitting startlingly loud vocal calls at the body of an old male donkey laid out on the ground. A sorrowful donkey was also the subject of a report sent to me earlier in 2018 from the Farm Animal Rescue and Rehoming Movement (FARRM) animal sanctuary in Alberta, Canada. Founder Melissa Foley and volunteer Stephanie Belland were concerned that a resident donkey named Lena was having great trouble recovering from the death of the horse Jake, with whom she had been very close for three years. When at 32 years of age Jake fell gravely ill, a vet put him down. That first night Jake’s body lay under a tarp until he could be buried, but Lena tore the coverings off. “Throughout the night, Lena circled and refused to leave,” Foley and Belland recalled. “When we buried Jake the next day, she followed his body to the hole we had dug and remained standing over his grave for days, pawing at the dirt and braying throughout the night. She refused to leave even for food and water.”
This description brought tears to my eyes. Over the next weeks Lena began to recover; she gradually resumed normal eating and drinking and sought out the company of other horses. Perhaps the opportunity she had been given to spend time with Jake’s body helped her. Indeed, a growing trend in sanctuaries, zoos and veterinary practices is to allow a surviving companion to do so, an applied outcome of research on animal grief that I welcome.
Ferrets, too, express sorrow at death, according to Salise Shuttlesworth, founder and executive director of the Friends For Life no-kill animal shelter in Houston. In an unexpected and sad turn of events, all four of Shuttlesworth’s female ferrets, between seven and eight years of age, died of unrelated illnesses within a six-week period. The two that lived the longest were Pinky and Effie. When Effie’s adrenal disease reached an advanced stage, Shuttlesworth arranged for in-home euthanasia. Before this point, Pinky had searched the house intensively for her closest ferret friend, who had already died. When Effie’s euthanasia procedure began, Pinky responded strongly again. “She pushed herself between the doctor’s hands and Effie,” Shuttlesworth told me. “When the doctor tried to listen to Effie’s heart, Pinky pushed under the stethoscope. She groomed Effie’s ear. Finally, she just laid against her, still.” For more than two hours after Effie’s death, Pinky didn’t move from that position. She died of heart failure the next day.
Over the years I have also received credible reports of magpies and Canada geese exhibiting great distress at discovering the body of a companion or mate. Learning that cows mourn when their calves die or when, as on many meat or dairy farms, their calves are taken from them days after birth, never to be seen again, contributed to my recent decision to eat mostly plant-based foods.
Yet not every animal response to death qualifies as grief. At my own home, my husband and I photographed events following the death of our rescued cat, Hayley, whom we had put down because she had advanced, untreatable cancer. In the outdoor enclosure where six semiferal cats live, including Hayley’s sister, Kayley, we placed Hayley’s body on the ground on a cloth. Several cats approached, inspected and sniffed the body, but Kayley did not. She sat still and stared at her sister from a distance for many minutes after the others had gone back to their own routines. She did not wail, as cats and dogs sometimes do when faced with the death of a partner. Was Kayley grieving? Based on her close relationship with her sister, I might suspect so, but I cannot responsibly state grief was present when Kayley exhibited no visible signs of it.
Sometimes, too, more credible alternative explanations carry the day. In 2017 a video shot by Jonathan Davis of Randolph, Mass., showed a group of wild turkeys on a street circling the body of a dead cat. When the clip went viral, folk theories erupted: Was this some kind of emotional, cross-species death ritual? Far more likely, wildlife biologists say, the turkeys were instinctively curious about a dead body they noticed, with each one following another in a circle of close inspection.
Ties that bind
Beyond greatly expanding the diversity of species found to mourn, these and other recently documented examples of animal grief are illuminating the social conditions that foster this emotion. Writing in a 2018 special issue of Philosophical Transactions of the Royal Society B devoted to animal and human responses to death, Claire F. I. Watson and Tetsuro Matsuzawa, both at Kyoto University’s Primate Research Institute in Japan, observed that most reports about responses to death in mammals to date concern mothers and their dead offspring. This is true. But there are some interesting exceptions to this rule.
We now know that in primates, close social relationships beyond the maternal-infant one may yield intense responses to death. When Thomas, a nine-year-old male chimp, died from a rampant lung infection at the Chimfunshi Wildlife Orphanage in Zambia in 2011, other apes in his group of 43 spent time at his body, often with a physical stillness that is quite atypical for this excitable species of ape. Describing the behavior in a paper published in 2017 in Scientific Reports, Edwin J. C. van Leeuwen of the University of St. Andrews in Scotland noted that two close social partners of Thomas displayed marked reactions. Pan, the adult male with whom Thomas had forged a friendship, visited and inspected the body more often than the other two males did and displayed energetically around the body. Noel, an adult female who had adopted Thomas in the wake of his mother’s death, did something never before observed in chimpanzees: she cleaned Thomas’s teeth using a grass tool. Noel persisted in this activity even when other chimps had been enticed away from the body by sanctuary workers offering fruit, a preferred food. We cannot know how long the animals’ unusual behaviors—at a minimum, consistent with grief—would have continued had Thomas’s body not been removed by sanctuary staff 20 minutes after its discovery.
Other examples of grief outside the bounds of the mother-infant bond come from our more distant primate cousins. Six years ago I noted a near absence of convincing evidence for emotional responses to death in monkeys. That situation has changed—we now have reports of these behaviors in common marmosets and Barbary macaques. And in 2016 Bin Yang of the Shaanxi Institute of Zoology in China and his colleagues announced that they had observed responses to death in Sichuan snub-nosed monkeys in central China. A female had fallen from a tree and struck her head on a stone. As she lay, gravely injured, her group mates surrounded her for close to an hour and “closely tended” her, “peering at and occasionally sniffing her face, grooming and embracing her, and gently pulling her hand,” Yang and his co-authors reported. The single adult male of the group gave warning calls when an infant and a juvenile from another one-male group attempted to approach. When the female died, this male touched her repeatedly and pulled on her hand. He left after about five minutes, then returned the next day with his group to the spot where she had died (the body had been buried by a research assistant). The male had had a strong bond with the female over a three-year period after her immigration into the male’s group.
As far as animal grief research has come, so much more remains to be discovered. For one thing, our hypotheses about the factors that determine whether or not a species experiences grief need testing. A 2018 paper in Zoology by Giovanni Bearzi, president of the Italian nonprofit organization Dolphin Biology and Conservation, suggests a way forward. Bearzi and his colleagues combed through all records published between 1970 and 2016 that describe so-called postmortem attentive behavior (PAB) by individual cetaceans. Both wild and captive cetaceans were included, but events that occurred in captivity under conditions that would not occur in the wild were excluded. Behaviors observed included a whale or dolphin attending a body, keeping a body afloat and carrying a body. Whereas in some cases of PAB, the survivor animal may be attempting to revive a social partner, in other cases, it clearly meets the criteria for grief: altered behavior lasting for days that indicates distress. The study found that nearly a quarter of the 88 species of dolphins and whales showed some kind of PAB. An overwhelming majority (92.3 percent) of these cases occurred in Delphinidae, a family of relatively small-bodied cetaceans that include dolphins, orcas and pilot whales. In contrast, the large-bodied mysticetes, or baleen whales, were, with a single exception, not observed to show any PAB. Intriguingly, Delphinidae are larger-brained and more social than baleen whales. Here lies the future of animal grief research: comparative analyses of responses to death across closely related species.
More than any other topic in animal behavior I have written about over the course of 30 years, animal grief strikes a chord. Why? A cross-species perspective on grief tells us that intense emotion expressed around death is not exclusive to humans but is found in other animals whose social relationships go beyond adaptive “bonding” for survival and reproduction. Recognizing this fact gives us an important pathway to connect with the natural world. But beyond suffering emotionally as the result of separation from a friend or loved one, do individuals of any species other than our own grasp the permanence of death? Do they anticipate their own death? I wonder whether any scientific evidence could satisfactorily answer questions of this nature. As ethological observations proceed, however, they are likely to reveal an ever sharper picture of who grieves and under what circumstances.