How Animals Grieve

by Barbara J. King

  An obvious place to look for mourning is among mammals who, unlike macaques, geladas, or Okavango baboons, organize themselves into pair-bonded couples. Among birds, pair-bonding is a routine occurrence, but only 5 percent of mammals do it. One exception is a rodent called the prairie vole, and scientific work on the biological and emotional basis of pair-bonding in these small animals may help us think about grief in monkeys.

  In experimental work published in 2008, Oliver J. Bosch and his colleagues decided to look into how even short separations from mated partners would affect prairie vole males. The males to be studied were paired either with females they had never met before or with male siblings they had not encountered since the time of their weaning (a period that ranged from forty-nine to seventy-nine days). After five days together, half of these pairs were separated.

  All of the study males were then subjected to stress tests, including what’s called a forced-swim test, in which the vole remains for five minutes in a beaker of water; a tail-suspension test, in which the vole is hung for five minutes from a stick to which its tail is taped; and an elevated-maze test, which tests the vole’s inherent fear of exposed spaces, again for five minutes. In two of these tests, males who had been separated from female partners showed increased levels of “passive stress coping,” a type of response that correlates to higher depression levels. In the forced-swim test, they tended to float rather than struggle or swim, and in the tail-suspension test, they hung passively. The effect was specific to males separated from females, as opposed to either males paired with male sibs or males kept isolated. It’s the specificity of the effect that’s important here: it shows that it’s the pair bond that matters most, emotionally, to these voles.

  Further, these scientists found that the stress responses were mediated by what’s called the corticotropin-releasing factor (CRF) system. Levels of CRF, thought to mediate anxiety and depression, rose in the males separated from female partners. That ameliorating effect might sound like a good thing for the stressed males, but could the anxiety and depression in fact be adaptive in some way? Bosch’s coauthor Larry Young explained to me that when CRF receptors were experimentally blocked, the voles didn’t show the depressive behaviors. And yes, Young believes that the entire system is adaptive for the voles: “The negative state produced from separation from the partner,” he told me, “serves to drive the male back to their partner, maintaining the pair bond.”

  I experienced an emotional response of my own in reading about these experiments. Five minutes, the length of time a male was forced to swim or hang by his tail, isn’t an eternity, but still I began to wish I’d served on the animal-care committee that approved these tests. Then I read further. In pursuit of answers to the CRF-receptor questions, a number of voles had been decapitated. While these experiments violated no institutional ethics policies, they gave me great pause in weighing the costs to animals of our invasive probing of their emotion (versus behavioral observation or analysis of, say, fecal material). Bosch and his colleagues believe their vole work, both the behavioral and biochemical components, may illuminate the expression of human bereavement. This hope may be realized. But perhaps the voles themselves, when a partner dies, experience grief and bereavement. It doesn’t seem that this question was asked.

  Let’s return to monkeys. None of our closest living relatives, the great apes—chimpanzees, bonobos, gorillas, and orangutans—pair off to raise their young. As noted earlier, this is par for the course among mammals. But the so-called lesser apes, the gibbons and siamangs, do bond in this way, as do some monkeys, including titis, owl monkeys, marmosets and tamarins.

  Even in the context of monkey monogamy, emotion hasn’t been well studied. In South American titi monkeys, males and females form bonds for life. When a male and female pair is forcibly separated by scientists in the laboratory, the animals show their distress through agitated behavior, and their plasma cortisol levels rise. In a comparative study by Sally Mendoza and William Mason, squirrel monkeys subjected in the same way to male-female separation showed no comparable behavioral or physiological changes, presumably because, unlike titis, they are not monogamous. The pair bond in titi monkeys, in other words, isn’t merely a matter of survival and reproductive success—the monkeys matter to each other.

  The same question comes to mind with monkeys as with the voles: How might we move from lab findings that rely heavily on blood chemistry and basic measures of behavioral distress to understanding more about what survivors of a disrupted pair bond experience? A video archive could help answer this question, with the gold standard defined as filmed records shot around the time of death of one monkey, focusing on the surviving partner and other family members. In this way, scientists could make fine-grained behavioral comparisons among monogamous and nonmonogamous, and captive and wild, monkeys.

  Rare events in the lives of monogamous monkeys might be hard to film in the wild. These species are largely arboreal, and as researcher Karen Bales remarked to me, with tree travel it may simply be too difficult for mothers to carry a dead infant or for a monkey to stay in proximity to a dead group member. In captivity, filming such events would be easier. I predict that grief responses will be found to occur among some pair-bond survivors in captivity, but testing of this hypothesis is sorely needed.

  At Miami’s DuMond Conservancy, owl monkeys Betsy and Peanut lived together as pair-bonded partners for eighteen years. Peanut, who was born in the wilds of Peru, was originally shipped to a US research laboratory as a test subject, but after some years and a serious illness he was allowed to retire to the conservancy. At first, he was timid around others of his kind. Then he met Betsy. Primatologist Sian Evans notes that even for owl monkeys, “Peanut and Betsy were unusually closely bonded. They had several offspring, and Peanut was a devoted father, carrying and caring for them all.”

  Then, in 2012, Peanut began to weaken. He still foraged for insects at night, right alongside Betsy (owl monkeys are the only monkeys who are nocturnal). But the quality of his movements indicated his frail state, and eventually he became ill. When attempts to treat him failed, the staff returned him to his enclosure, where he could live out his remaining hours with Betsy. As always, Betsy was an attentive partner. She held and nuzzled Peanut until he died.

  Without Peanut, Betsy immediately began to behave differently. For the first time, she sought out and spontaneously interacted in a friendly way with Evans, her caretaker. In the past, Evans told me, Betsy had viewed her as a competitor, as female owl monkeys will do with female humans. But with Peanut gone, there was a behavioral shift. Evans grieved for Peanut and found comfort in Betsy’s companionship. What Betsy felt, Evans says she cannot know, and she doesn’t feel comfortable calling Betsy’s response “grief.” She refers to it instead as “response to loss,” a sort of interspecies shift in bonding that came about as a result of Betsy’s being without her partner.

  So then, do monkeys mourn? Often they do not, at least in a way visible to us. This conclusion holds even in some cases where, from an anthropomorphic perspective, it seems that they should mourn—as with mothers who carry their infants’ corpses for weeks, or the owl monkey Betsy who lost her pair-bonded partner of eighteen years. But some monkeys do grieve, as Anne Engh’s description of Sylvia the baboon tells us. A more robust conclusion awaits the day when statistical or physiological profiles are complemented by vivid descriptions of monkeys’ behavioral responses to death.

  7

  CHIMPANZEES

  CRUEL TO BE KIND

  As the world’s first “astrochimp,” Ham the chimpanzee rocketed into outer space in 1961. Captured from Cameroon, West Africa, brought to the United States, and named for the Holloman Aerospace Medical Center, Ham flew 155 miles above the earth’s surface at five thousand miles per hour on behalf of the American space program. Inside the Mercury capsule, Ham carried out the tasks for which he had been trained; as lights flashed, he pulled levers in response, demonstrating that the effects of sp
ace travel do not harm a thinking primate’s capacities. Ham thus cleared the way to send humans into orbit.

  Few ethical concerns were raised back then, more than a half century ago, about subjecting an ape to this sort of stress. In hindsight this nonchalance seems cavalier, especially given the safety record of previous primate launches. A monkey called Albert I suffocated during his flight in 1948. The following year, Albert II died from impact trauma when his capsule’s parachute failed on returning to earth; Albert III was killed when his rocket exploded at thirty-five thousand feet; and Albert IV was killed on impact in another parachute failure.

  There’s something chilling about this litany of cloned names, a sense that monkey after monkey was sent to his death with no thought to the individual lives risked and lost. Indeed, a name was not bestowed on Ham the chimpanzee until he returned safely to Earth, for fear that his human coworkers in the space program would get too attached to him. In subsequent years, following the quartet of Albert deaths, the record of monkey survival did improve. As late as 1958, though, a monkey died because his capsule could not be located following splashdown in the Atlantic.

  The BBC’s coverage of Ham’s successful flight on January 31, 1961, reflects the lighthearted tone of the day, even as the reporter describes the unexpected outcomes of the Mercury mission:

  Because of his steeper-than-expected climb, the capsule overshot its landing site in the Atlantic off Florida by some way. Ham had an uncomfortable three-hour wait before he was found. Then when rescue helicopters finally arrived, they found the capsule on its side and sinking. It had landed with such force that the heat shield had punched two holes in the capsule. Ham, however, took it all in his stride and when the spacecraft was opened accepted an apple and half an orange in reward.

  Jane Goodall had, by 1961, already begun observing wild chimpanzees in Tanzania. But the world didn’t yet know about chimpanzees’ deep family bonds, their clever making and using of tools, their emotional capacities for love and grief. Looking back, given what is known now, we can only wonder: did Ham really take it all in his stride? Or was he terrified, both because of intense heat and because he was bobbing around untended in the ocean for three hours, not knowing what would happen next? The image is hard for the mind to take, Ham alone in the capsule, with no other being to empathize or to comfort him during what can only have been a truly frightening experience.

  Many years later, at the National Zoological Park in Washington, DC, Ham responded to Melanie Bond, a biologist and ape-keeper, in a way that spoke to her of empathy and comfort. Ham had been retired from the space program into zoo life; for a long seventeen years, he lived in the nation’s capital as the zoo’s sole chimpanzee resident. (His final years, fortunately, were spent in apparent contentment with other chimpanzees at the North Carolina Zoo.) Bond, over the next decades, would spend countless hours caring for great apes both there and at the Center for Great Apes, a sanctuary in Florida, fostering a particularly deep affinity with orangutans. At the time of the incident with Ham, though, in 1977, she was relatively new to the zoo.

  The first deep connection Melanie developed with an ape had been with Archie the orangutan. One day, it was her job to assist in his routine physical, for which he was given an immobilizing drug in his cage. During the examination, Archie stopped breathing. The zoo’s veterinarian, Mitchell Bush, made a heroic effort to bring him back. For forty-five minutes, Dr. Bush compressed Archie’s chest, offering CPR with such vigor that Archie’s sternum cracked. Eventually, all present at Archie’s side were forced to accept that the orangutan had died.

  As Melanie walked away, past a line of caged apes who could see her clearly, she cried for Archie. She remembers it as quiet crying: nothing terribly overt, just tears she couldn’t stop. Melanie saw Ham watching her and said aloud to him, “Yes, Ham, I am very sad.” Moving slowly and gently, Ham reached a thick finger through the cage bars and touched a single tear on Melanie’s cheek. He then smelled and tasted the tear. “I felt empathy,” Melanie remembers. “I felt, ‘someone understands.’”

  What would the skeptics say? That Melanie projected her need for comfort onto a chimpanzee’s actions? Sure, they might admit, Ham was a smart ape, and curious about Melanie’s crying. It was this curiosity that motivated his actions, not any emotional resonance with Melanie’s state of mind, nor any desire to give solace to a friend. To impute such resonance and desire to a chimpanzee is to engage in wishful thinking about humans’ and apes’ emotional similarities.

  In support of the skeptic’s point, films of chimpanzees in the wild rarely include scenes that mirror the gentleness exhibited by Ham. The iconic still photograph of a wild chimpanzee, taken at Gombe, Jane Goodall’s research site in Tanzania, shows an ape who has fashioned a wand tool inserting it into a termite mound to retrieve a protein snack. The videocamera, though, gravitates toward outbreaks of aggression, displays of hotheaded chimpanzee excitement. These recordings lead to descriptions of brutality, as in the case of an attack filmed and narrated by the anthropologist David Watts of Yale University. Watts observed the event among the Ngogo community of chimpanzees of Kibale National Park, Uganda. In the key part of Watts’s footage, a pack of chimpanzee males is seen to surround, then begin to kick and bite, another male called Grapelli. Hurling themselves at the cowering figure, the males inflict injuries so severe that Grapelli died three days later.

  The action of the male chimpanzee mob may seem shocking to us, and may tempt us to label the entire species as violent. After all, similar attacks have been seen in other chimpanzee populations, and they differ appreciably from the hunting behaviors that occur when, for instance, chimpanzees catch and consume colobus monkeys. In Kenya, when I’d return to my house after following baboons all day through the bush, I would often hear the roars of lions through the open-mesh window of my bedroom. I’d be haunted by the thought of zebra, antelope, and wildebeest, out there on the savannah at the big cats’ mercy. Lions ate “my” baboons, too, but with a barking alarm upon sighting a tawny stalking shape, the monkeys would scatter high up into the trees, with at least some hope of escape. Not every monkey always made it, but arboreal refuge did exist for them. Not so for the herbivores, who could run but never hide: for them, no tree, no burrow, no watery hiding place.

  Even so, when a lion brings down a zebra, or a fox snatches a rabbit, the animal hunters aren’t stigmatized as violent. But what of these Ngogo chimpanzees filmed by Watts? They are shown engineering, with shrieking abandon, the horrific end of one of their own; Grapelli belonged not just to the same species but to the same community as the attackers.

  Watts does describe the empathetic response of one of the males who refused to join in the attack mob, and who stayed near Grapelli as much as he could. The vast majority of males, though, showed no such mercy, and certainly nothing like the gentleness shown by Ham to his human friend at the National Zoo. Is it just that in Ham’s case, the chimpanzee drained out of him after he was stolen from his Cameroonian home? So long subjected to the press of human needs—first as a guinea pig in the space program, later as entertainment for zoo visitors—did Ham become only the palest reflection of a wild chimpanzee?

  It’s easy to be swept away by the picture of chimpanzee aggression I’ve painted here, but there’s another side to wild chimpanzees too, a side that brings us much closer to Ham. The expression of chimpanzee grief, in the wild as well as in captivity, has complicated the picture of what is understood to be “natural” for chimpanzees. Arguably the most famous example of grief in the animal world, dated to 1972, is the juvenile chimpanzee Flint’s loss of will to live following the death of his mother Flo.

  At Gombe, Flint had enjoyed his mother’s undivided attention well beyond his infancy. His younger sibling Flame—Flo’s last-born offspring—had died, leaving him the emotional center of his mother’s aging life. As Goodall wrote in In the Shadow of Man, except for nursing (because Flo’s milk had dried up), “Flint again became Flo’s baby. S
he shared her food with him; she permitted him to climb onto her back or even on occasions cling to her belly. She groomed him constantly and, as of old, she welcomed him into her bed at night.” These patterns of behavior persisted until Flint was over six years old, and even after that point, mother and son remained abnormally close. Flo died when Flint was eight years old, and he was unprepared to cope. In a passage from Goodall’s later book Through a Window, we glimpse the depth of Flint’s loss: “The last time I saw him alive, he was hollow-eyed, gaunt and utterly depressed, huddled in the vegetation close to where Flo had died. . . . The last short journey he made, pausing to rest every few feet, was to the very place where Flo’s body had lain.” Only three weeks after his mother’s death, Flint died too, of causes that Goodall unflinchingly attributes to depression and the resultant weakening of his immune system.