Captive audience

A chimpanzee strips the leaves from a branch, fashioning an expert fishing pole. It squats before a termite mound, dipping the branch into a narrow hole. Then, in an exacting demonstration of tool use, it extracts its prize: picante sauce, or maybe applesauce, depending on the day.

Creating objects like artificial insect mounds to keep chimps cognitively engaged is just one of the many strategies psychologists and their colleagues are using to benefit captive creatures. Scientists are devising clever new ways to improve animals' lives in zoos and laboratories — and in a departure from the past, experts today are rigorously testing their enrichment ideas to determine what works.

"A few decades ago we were relying on impressions about what would be good for animals. People were interested in animal welfare, but there was not a lot of science going on," says Mollie Bloomsmith, PhD, head of behavioral management at Emory University's Yerkes National Primate Research Center. "It's incredible how enrichment has grown into a scientific endeavor."

Group living

When it comes to enhancing the lives of captive animals, psychologists have long led the charge, says Allyson Bennett, PhD, an assistant professor of psychology at the University of Wisconsin–Madison and chair of the APA Committee on Animal Research and Ethics. Psychological research has driven our understanding of "animals' cognitive, social and affective capacities, as well as major effects of environment on brain, behavior and physiology," she says.

Today, cognitive scientists are still in the business of ensuring their nonhuman subjects have fulfilling environments, says Regina Paxton Gazes, PhD, a nonhuman-primate researcher and postdoctoral fellow at Zoo Atlanta. After all, if you're studying things like learning and reasoning, she says, "it's important that your subject is cognitively sound."

For primates and other social mammals, the chance to interact with one another is an important part of a healthy environment. Indeed, one of the most striking changes in recent years has been a move toward social housing for nonhuman primates in laboratories, both Gazes and Bloomsmith say.

In labs of the past, researchers often kept monkeys in individual cages in an effort to minimize aggression and make it easier to control the animals' environments. These days, housing primates in pairs or even larger social groups is the norm. Gazes has shown that monkeys living in large, naturalistic settings can be viable research subjects. In a 2012 study published in Animal Cognition, she and her colleagues gave Rhesus macaques a battery of cognitive tests. They found that monkeys housed in pairs in a laboratory performed similarly to those that lived primarily outdoors in a group of more than 70 individuals.

Primates aren't the only animals to benefit from rich environments, of course. Nor are cognition researchers the only scientists paying closer attention to their research subjects' environs. As the burgeoning field of epigenetics has made clear, an animal's surroundings can affect its behavior and physical health in surprising ways. Scientists have discovered that a creature's environment (its diet, say, or the amount of parental care it received) can alter the expression of its genes by flipping a series of chemical switches on or off. Such epigenetic changes can even be passed down to future generations. "The more we learn about genes interacting with environments, the more important it becomes to pay close attention to those environments — and how changes to them can affect experimental results," says Bennett.

Wild behaviors

Zoos, too, are taking a critical look at their animal habitats. "We talk about the science and art of zoo animal management," says Don Moore, PhD, associate director for animal care sciences at the Smithsonian's National Zoo, in Washington, D.C. When he began his career three decades ago, he says, "[animal] enrichment was based in art. But as more PhD-trained scientists have moved into zoos, we've brought the scientific method with us."

In one example, Moore and his colleagues devised a study to find out why red pandas were pacing abnormally. They tested a series of working hypotheses and discovered that the pandas were agitated by their own reflections in the glass of their enclosure. When the researchers covered the glass with nonreflective plastic, the pandas stopped their march. "We were able to turn pacing off and on like a switch," he says. To reduce stress on the pandas, zookeepers now keep the glass under wraps.

Jason Watters, PhD, head of the behavioral research program at the Chicago Zoological Society and Brookfield Zoo, also takes an evidence-based approach to animal enrichment. "Zoo people are constantly coming up with crazy enrichment ideas. Some are incredibly elegant, and others are totally outrageous. Some work wonderfully and some don't, but it's a great testing ground," he says.

Studying the zoo's fennec foxes, Watters turned a scientific eye toward predictability — something most zoo animals have in spades. He discovered the foxes spent more time searching their enclosure when they were fed on an irregular rather than a predictable schedule. But interestingly, the foxes also dialed down their foraging behavior when their schedule was wholly unpredictable (Zoo Biology, 2011). The trick to optimizing their foraging behavior, he found, was to strike a balance that kept the animals interested but not completely confused.

"We need to provide a safe environment where there is certainty, but at the same time, a reason for the animals to investigate and explore and engage their minds," Watters says.

As the field of enrichment science has matured, researchers are starting to focus on more subtle signs of animal well-being. "Historically, animal welfare focused on negative behaviors," says Lance Miller, PhD, a scientist in the behavioral biology division at the San Diego Zoo's Institute for Conservation Research. Was an animal pacing, grooming compulsively or pulling out its hair? "But absence of negative behavior doesn't necessarily equate to good welfare," he says.

In zoos across the country, Miller says, animal-care experts are beginning to take a more proactive approach to animal enrichment. "Many years ago the approach was, ‘Let's try this and see what happens,'" he says. "Now it's really a behavior-based program. We ask, ‘What are the behaviors we want the animals to engage in?'"

He and his colleagues at the San Diego Zoo have studied lions, tigers and cheetahs using preference assessments. In humans such as autistic children who can't communicate well, similar assessments are used to determine likes and dislikes, allowing caregivers to identify the most effective rewards for desired behavior. In the case of the cats, Miller and his colleagues offered the animals a variety of scents and objects, presenting the items in a series of pairs so that the cats could choose their favorite of two. They found an animal's favorite pastimes tend to square with what it would be doing if it were living in the wild. On the savannah, for instance, female lions do most of the hunting. In the zoo, Miller found, females prefer to interact with "boomer balls," large plastic balls they can pounce on and sink their claws into. Males, which in the wild would be out marking their territories, are more interested in fresh branches that they can mark with their scents. Providing opportunities to express these gender-specific behaviors makes for happier cats.

"We let the animals tell us what they want to interact with," he says.

Miller and his colleagues are also working to validate behavioral measures of animal welfare, using cheetahs and okapi as test cases. They're collecting behavioral information about the animals, as well as physiological data such as the amount of stress hormones in the animals' droppings. They hope to determine which behaviors indicate good health and which might be signs of a problem. By codifying those behaviors, zoos could rigorously test new enrichment methods without expensive hormone assays.

"It costs a lot of money to run assays," Miller says. "If we can validate behavioral measures that tell us the same thing, it could be a tool that other institutions could replicate."

Monkey music

As researchers take a critical look at enrichment, they're sometimes surprised by the results. Take music: Some researchers have turned on the radio for their laboratory subjects, assuming the animals would enjoy it, Bennett says. But melodies that are pleasing to our ears may not be so charming to animals. University of Wisconsin–Madison psychologist Charles Snowdon, PhD, and University of Maryland cellist David Teie discovered that cotton-top tamarins were unmoved by most human music. Yet the monkeys showed signs of either anxiety or calm when responding to various songs composed using elements of the tamarins' own calls (Biology Letters, 2009).

Animal-care practices also deserve a second look, says Bennett. For example, she says, animal-care guidelines typically urge cleanliness and sterility. But nature is anything but sterile. While cleanliness is important, it's worth investigating whether we may be taking it too far, she says.

"We might want things like bedding in the cage that can be messy, but are better for the animals' well-being," she says. "Some regulations were rolled out perhaps without a lot of data on whether it's the best thing for animals. Now people are saying we need to look more closely."

For lab researchers, though, adding new toys or activities can present a challenge even if it's the best thing for the animals. Scientists first need to consider how a change in conditions might affect their research results, says Bennett. "You have a balance between respecting the scientific integrity while respecting the animals' welfare," she says. "That doesn't mean we don't want to have better enrichment; it means we need controlled studies to understand what effect it has."

It can also be tricky to implement new enrichment programs in zoos. Zookeepers must balance animal welfare with the need to please visitors and educate the public about conservation, Moore says. Fortunately, those goals aren't necessarily at odds. At the National Zoo, he says, fishing cats (medium-sized Asian wildcats) are periodically given an opportunity to catch their prey from a pool in their enclosure. Exercising that instinct is good for the cats and helps keep zoo-goers engaged in the exhibit. And researchers in Singapore found that orangutans housed in naturalistic enclosures didn't care how many visitors came to see them, as long as the spectators kept their distance. When people came too near, the apes were less likely to engage in play (Applied Animal Behaviour Science, 2011).

What's next on the horizon for animal enrichment? New technology is playing an increasing role. Scientists are monitoring animals with GPS and video to more easily track their movements and activities around the clock. Robotically controlled feeding devices that can be programmed to open and close on schedule allow for unpredictable feeding times, as in Watters's fennec fox experiment. And in some cases, the animals themselves are plugging in. "You see things like iPads used to cognitively challenge great apes," says Miller. "I think technology can be really beneficial."

Whether the tools are experimental or proven, high-tech or low, the field of enrichment science is really coming into its own, says Bloomsmith. "There's a huge role for psychologists in this area. We need behavior analysts applying their training approaches to reduce stress and improve the welfare of animals," she says.

For those who are interested, the possibilities for creativity are vast, adds Miller. "The boundaries are limitless."

Kirsten Weir is a writer in Minneapolis.

Enrichment day at the National Zoo