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Modern Zoos Are Not Worth the Moral Cost

  Credit... Photographs by Peter Fisher for The New York Times

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By Emma Marris

Ms. Marris is an environmental writer and the author of the forthcoming book “Wild Souls: Freedom and Flourishing in the Non-Human World.”

• June 11, 2021

After being captives of the pandemic for more than a year, we have begun experiencing the pleasures of simple outings: dining al fresco, shopping with a friend, taking a stroll through the zoo. As we snap a selfie by the sea lions for the first time in so long, it seems worth asking, after our collective ordeal, whether our pleasure in seeing wild animals up close is worth the price of their captivity.

Throughout history, men have accumulated large and fierce animals to advertise their might and prestige. Power-mad men from Henry III to Saddam Hussein’s son Uday to the drug kingpin Pablo Escobar to Charlemagne all tried to underscore their strength by keeping terrifying beasts captive. William Randolph Hearst created his own private zoo with lions, tigers, leopards and more at Hearst Castle. It is these boastful collections of animals, these autocratic menageries, from which the modern zoo, with its didactic plaques and $15 hot dogs, springs.

The forerunners of the modern zoo, open to the public and grounded in science, took shape in the 19th century. Public zoos sprang up across Europe, many modeled on the London Zoo in Regent’s Park. Ostensibly places for genteel amusement and edification, zoos expanded beyond big and fearsome animals to include reptile houses, aviaries and insectariums. Living collections were often presented in taxonomic order, with various species of the same family grouped together, for comparative study.

The first zoos housed animals behind metal bars in spartan cages. But relatively early in their evolution, a German exotic animal importer named Carl Hagenbeck changed the way wild animals were exhibited. In his Animal Park, which opened in 1907 in Hamburg, he designed cages that didn’t look like cages, using moats and artfully arranged rock walls to invisibly pen animals. By designing these enclosures so that many animals could be seen at once, without any bars or walls in the visitors’ lines of sight, he created an immersive panorama, in which the fact of captivity was supplanted by the illusion of being in nature.

Mr. Hagenbeck’s model was widely influential. Increasingly, animals were presented with the distasteful fact of their imprisonment visually elided. Zoos shifted just slightly from overt demonstrations of mastery over beasts to a narrative of benevolent protection of individual animals. From there, it was an easy leap to protecting animal species.

The “educational day out” model of zoos endured until the late 20th century, when zoos began actively rebranding themselves as serious contributors to conservation. Zoo animals, this new narrative went, function as backup populations for wild animals under threat, as well as “ambassadors” for their species, teaching humans and motivating them to care about wildlife. This conservation focus “ must be a key component ” for institutions that want to be accredited by the Association of Zoos and Aquariums, a nonprofit organization that sets standards and policies for facilities in the United States and 12 other countries.

This is the image of the zoo I grew up with: the unambiguously good civic institution that lovingly cared for animals both on its grounds and, somehow, vaguely, in their wild habitats. A few zoos are famous for their conservation work. Four of the zoos and the aquarium in New York City, for instance, are managed by the Wildlife Conservation Society, which is involved in conservation efforts around the world. But this is not the norm.

While researching my book on the ethics of human interactions with wild species, “Wild Souls,” I examined how, exactly, zoos contribute to the conservation of wild animals.

A.Z.A. facilities report spending approximately $231 million annually on conservation projects. For comparison, in 2018, they spent $4.9 billion on operations and construction. I find one statistic particularly telling about their priorities: A 2018 analysis of the scientific papers produced by association members between 1993 and 2013 showed that just about 7 percent of them annually were classified as being about “biodiversity conservation.”

Zoos accredited by the A.Z.A. or the European Association of Zoos and Aquaria have studbooks and genetic pedigrees and carefully breed their animals as if they might be called upon at any moment to release them, like Noah throwing open the doors to the ark, into a waiting wild habitat. But that day of release never quite seems to come.

There are a few exceptions. The Arabian oryx, an antelope native to the Arabian Peninsula, went extinct in the wild in the 1970s and then was reintroduced into the wild from zoo populations. The California condor breeding program, which almost certainly saved the species from extinction, includes five zoos as active partners. Black-footed ferrets and red wolves in the United States and golden lion tamarins in Brazil — all endangered, as well — have been bred at zoos for reintroduction into the wild. An estimated 20 red wolves are all that remain in the wild.

The A.Z.A. says that its members host “more than 50 reintroduction programs for species listed as threatened or endangered under the Endangered Species Act.” Nevertheless, a vast majority of zoo animals (there are 800,000 animals of 6,000 species in the A.Z.A.’s zoos alone ) will spend their whole lives in captivity, either dying of old age after a lifetime of display or by being culled as “surplus.”

The practice of killing “surplus” animals is kept quiet by zoos, but it happens, especially in Europe. In 2014, the director of the E.A.Z.A. at the time estimated that between 3,000 and 5,000 animals are euthanized in European zoos each year. (The culling of mammals specifically in E.A.Z.A. zoos is “usually not more than 200 animals per year,” the organization said.) Early in the pandemic, the Neumünster Zoo in northern Germany coolly announced an emergency plan to cope with lost revenue by feeding some animals to other animals, compressing the food chain at the zoo like an accordion, until in the worst-case scenario, only Vitus, a polar bear, would be left standing. The A.Z.A.’s policies allow for the euthanasia of animals, but the president of the association, Dan Ashe, told me, “it’s very rarely employed” by his member institutions.

Mr. Ashe, a former director of the U.S. Fish and Wildlife Service, suggested that learning how to breed animals contributes to conservation in the long term, even if very few animals are being released now. A day may come, he said, when we need to breed elephants or tigers or polar bears in captivity to save them from extinction. “If you don’t have people that know how to care for them, know how to breed them successfully, know how to keep them in environments where their social and psychological needs can be met, then you won’t be able to do that,” he said.

The other argument zoos commonly make is that they educate the public about animals and develop in people a conservation ethic. Having seen a majestic leopard in the zoo, the visitor becomes more willing to pay for its conservation or vote for policies that will preserve it in the wild. What Mr. Ashe wants visitors to experience when they look at the animals is a “sense of empathy for the individual animal, as well as the wild populations of that animal.”

I do not doubt that some people had their passion for a particular species, or wildlife in general, sparked by zoo experiences. I’ve heard and read some of their stories. I once overheard two schoolchildren at the Smithsonian’s National Zoo in Washington confess to each other that they had assumed that elephants were mythical animals like unicorns before seeing them in the flesh. I remember well the awe and joy on their faces, 15 years later. I’d like to think these kids, now in their early 20s, are working for a conservation organization somewhere. But there’s no unambiguous evidence that zoos are making visitors care more about conservation or take any action to support it. After all, more than 700 million people visit zoos and aquariums worldwide every year, and biodiversity is still in decline.

In a 2011 study , researchers quizzed visitors at the Cleveland, Bronx, Prospect Park and Central Park zoos about their level of environmental concern and what they thought about the animals. Those who reported “a sense of connection to the animals at the zoo” also correlated positively with general environmental concern. On the other hand, the researchers reported, “there were no significant differences in survey responses before entering an exhibit compared with those obtained as visitors were exiting.”

A 2008 study of 206 zoo visitors by some members of the same team showed that while 42 percent said that the “main purpose” of the zoo was “to teach visitors about animals and conservation,” 66 percent said that their primary reason for going was “to have an outing with friends or family,” and just 12 percent said their intention was “to learn about animals.”

The researchers also spied on hundreds of visitors’ conversations at the Bronx Zoo, the Brookfield Zoo outside Chicago and the Cleveland Metroparks Zoo. They found that only 27 percent of people bothered to read the signs at exhibits. More than 6,000 comments made by the visitors were recorded, nearly half of which were “purely descriptive statements that asserted a fact about the exhibit or the animal.” The researchers wrote , “In all the statements collected, no one volunteered information that would lead us to believe that they had an intention to advocate for protection of the animal or an intention to change their own behavior.”

People don’t go to zoos to learn about the biodiversity crisis or how they can help. They go to get out of the house, to get their children some fresh air, to see interesting animals. They go for the same reason people went to zoos in the 19th century: to be entertained.

A fine day out with the family might itself be justification enough for the existence of zoos if the zoo animals are all happy to be there. Alas, there’s plenty of heartbreaking evidence that many are not.

In many modern zoos, animals are well cared for, healthy and probably, for many species, content. Zookeepers are not mustache-twirling villains. They are kind people, bonded to their charges and immersed in the culture of the zoo, in which they are the good guys.

But many animals clearly show us that they do not enjoy captivity. When confined they rock, pull their hair and engage in other tics. Captive tigers pace back and forth, and in a 2014 study, researchers found that “the time devoted to pacing by a species in captivity is best predicted by the daily distances traveled in nature by the wild specimens.” It is almost as if they feel driven to patrol their territory, to hunt, to move, to walk a certain number of steps, as if they have a Fitbit in their brains.

The researchers divided the odd behaviors of captive animals into two categories: “impulsive/compulsive behaviors,” including coprophagy (eating feces), regurgitation, self-biting and mutilation, exaggerated aggressiveness and infanticide, and “stereotypies,” which are endlessly repeated movements. Elephants bob their heads over and over. Chimps pull out their own hair. Giraffes endlessly flick their tongues. Bears and cats pace. Some studies have shown that as many as 80 percent of zoo carnivores, 64 percent of zoo chimps and 85 percent of zoo elephants have displayed compulsive behaviors or stereotypies.

Elephants are particularly unhappy in zoos, given their great size, social nature and cognitive complexity. Many suffer from arthritis and other joint problems from standing on hard surfaces; elephants kept alone become desperately lonely; and all zoo elephants suffer mentally from being cooped up in tiny yards while their free-ranging cousins walk up to 50 miles a day. Zoo elephants tend to die young. At least 20 zoos in the United States have already ended their elephant exhibits in part because of ethical concerns about keeping the species captive.

Many zoos use Prozac and other psychoactive drugs on at least some of their animals to deal with the mental effects of captivity. The Los Angeles Zoo has used Celexa, an antidepressant, to control aggression in one of its chimps. Gus, a polar bear at the Central Park Zoo, was given Prozac as part of an attempt to stop him from swimming endless figure-eight laps in his tiny pool. The Toledo Zoo has dosed zebras and wildebeest with the antipsychotic haloperidol to keep them calm and has put an orangutan on Prozac. When a female gorilla named Johari kept fighting off the male she was placed with, the zoo dosed her with Prozac until she allowed him to mate with her. A 2000 survey of U.S. and Canadian zoos found that nearly half of respondents were giving their gorillas Haldol, Valium or another psychopharmaceutical drug.

Some zoo animals try to escape. Jason Hribal’s 2010 book, “Fear of the Animal Planet,” chronicles dozens of attempts. Elephants figure prominently in his book, in part because they are so big that when they escape it generally makes the news.

Mr. Hribal documented many stories of elephants making a run for it — in one case repairing to a nearby woods with a pond for a mud bath. He also found many examples of zoo elephants hurting or killing their keepers and evidence that zoos routinely downplayed or even lied about those incidents.

Elephants aren’t the only species that try to flee a zoo life. Tatiana the tiger, kept in the San Francisco Zoo, snapped one day in 2007 after three teenage boys had been taunting her. She somehow got over the 12-foot wall surrounding her 1,000-square-foot enclosure and attacked one of the teenagers, killing him. The others ran, and she pursued them, ignoring all other humans in her path. When she caught up with the boys at the cafe, she mauled them before she was shot to death by the police. Investigators found sticks and pine cones inside the exhibit, most likely thrown by the boys.

Apes are excellent at escaping. Little Joe, a gorilla, escaped from the Franklin Park Zoo in Boston twice in 2003. At the Los Angeles Zoo, a gorilla named Evelyn escaped seven times in 20 years. Apes are known for picking locks and keeping a beady eye on their captors, waiting for the day someone forgets to lock the door. An orangutan at the Omaha Zoo kept wire for lock-picking hidden in his mouth. A gorilla named Togo at the Toledo Zoo used his incredible strength to bend the bars of his cage. When the zoo replaced the bars with thick glass, he started methodically removing the putty holding it in. In the 1980s, a group of orangutans escaped several times at the San Diego Zoo. In one escape, they worked together: One held a mop handle steady while her sister climbed it to freedom. Another time, one of the orangutans, Kumang, learned how to use sticks to ground the current in the electrical wire around her enclosure. She could then climb the wire without being shocked. It is impossible to read these stories without concluding that these animals wanted out .

“I don’t see any problem with holding animals for display,” Mr. Ashe told me. “People assume that because an animal can move great distances that they would choose to do that.” If they have everything they need nearby, he argued, they would be happy with smaller territories. And it is true that the territory size of an animal like a wolf depends greatly on the density of resources and other wolves. But then there’s the pacing, the rocking. I pointed out that we can’t ask animals whether they are happy with their enclosure size. “That’s true,” he said. “There is always that element of choice that gets removed from them in a captive environment. That’s undeniable.” His justification was philosophical. In the end, he said, “we live with our own constraints.” He added, “We are all captive in some regards to social and ethical and religious and other constraints on our life and our activities.”

What if zoos stopped breeding all their animals, with the possible exception of any endangered species with a real chance of being released back into the wild? What if they sent all the animals that need really large areas or lots of freedom and socialization to refuges? With their apes, elephants, big cats, and other large and smart species gone, they could expand enclosures for the rest of the animals, concentrating on keeping them lavishly happy until their natural deaths. Eventually, the only animals on display would be a few ancient holdovers from the old menageries, animals in active conservation breeding programs and perhaps a few rescues.

Such zoos might even be merged with sanctuaries, places that take wild animals that because of injury or a lifetime of captivity cannot live in the wild. Existing refuges often do allow visitors, but their facilities are really arranged for the animals, not for the people. These refuge-zoos could become places where animals live. Display would be incidental.

Such a transformation might free up some space. What could these zoos do with it, besides enlarging enclosures? As an avid fan of botanical gardens, I humbly suggest that as the captive animals retire and die off without being replaced, these biodiversity-worshiping institutions devote more and more space to the wonderful world of plants. Properly curated and interpreted, a well-run garden can be a site for a rewarding “outing with friends or family,” a source of education for the 27 percent of people who read signs and a point of civic pride.

I’ve spent many memorable days in botanical gardens, completely swept away by the beauty of the design as well as the unending wonder of evolution — and there’s no uneasiness or guilt. When there’s a surplus, you can just have a plant sale.

Emma Marris is an environmental writer and the author of the forthcoming book “Wild Souls: Freedom and Flourishing in the Non-Human World.”

Photographs by Peter Fisher. Mr. Fisher is a photographer based in New York.

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February 13, 2014

Ethics at the Zoo: The Case of Marius the Giraffe

Last weekend, a healthy juvenile male reticulated giraffe at the Copenhagen Zoo was killed. His name was Marius. The reason given was that his genes were already sufficiently represented in the giraffe population across the zoos of the European Association of Zoos and Aquariums (EAZA) his brother lives in a zoo in England, for [...]

By Jason G. Goldman

This article was published in Scientific American’s former blog network and reflects the views of the author, not necessarily those of Scientific American

Last weekend, a healthy juvenile male reticulated giraffe at the Copenhagen Zoo was killed. His name was Marius. The reason given was that his genes were already sufficiently represented in the giraffe population across the zoos of the European Association of Zoos and Aquariums (EAZA) – his brother lives in a zoo in England, for example – making him a so-called "surplus animal." Despite the international outcry against it, the giraffe was euthanized, a necropsy was performed by scientists while educators explained the dissection to the gathered crowd, and hunks of meat were fed to the zoo's lions, polar bears, and other carnivores.

The event reveals an ethical dilemma that rests at the core of zoo management: what tradeoffs are acceptable when it comes to animal welfare? (There are those who would rather zoos not exist at all; for the sake of this ethical exercise, we'll leave that conversation for another time.)

The reality is that zoos have an obligation to manage their populations as sustainably as possible, and that includes avoiding overpopulation and preventing inbreeding. Zoos operate at what is called "carrying capacity," which is the upper limit on the number of individual animals for any particular species that a given amount of space can sustain. In the wild, the carrying capacity of a geographic area is defined by the territory needs of individuals, and the amount of food and water available to sustain them. In a zoo, in addition to space, other limiting factors include the time available to care for animals and to maximize their welfare by keepers, curators, and veterinarians, and cost. And welfare is about more than just avoiding illness, injury, or boredom. As Terry Maple and David Bocian wrote in the journal Zoo Biology in 2013, promoting welfare is about "the effort to reach a higher plane of satisfaction, essentially techniques to improve the quality of life from good to great." Preventing overpopulation is, in part, how zoos can maximize the physical and psychological health of each animal; preventing inbreeding is how zoos can maximize the genetic health of each population.

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In the earliest days of the modern zoological park, zoos did not have this problem. The problem, instead, was just keeping animals alive. When animals died, new animals had to be caught from the wild to replace them. In the intervening decades our ethics have evolved (in the vast majority of cases, wild animals are no longer imported to zoos), our scientific understanding of reproductive physiology and veterinary medicine have grown by leaps and bounds, and best practices for husbandry and management have improved. As a result, in many cases, we now face the challenge of limiting population growth.

The Association of Zoos and Aquariums (AZA), which oversees the Species Survival Plans for over 500 species in North American zoos, and other organizations like it (such as the EAZA, of which the Copenhagen Zoo is a member) achieve this through developing population management plans .

These plans consider the available space and resources that each participating zoo has in order to determine how many individuals of each sex and age class can receive adequate care. Combined with information about the genetic lineage of each individual animal, they can develop breeding recommendations . With luck, those pairs who have been matched will take to eachother and produce offspring.

How can zoos prevent individuals who have not been given a breeding recommendation from producing offspring? There are several approaches: they can be housed in a single-sex enclosure if appropriate for the species, they can receive contraception, they can be permanently sterilized, or if there is no space for the animals, they can be transferred to other institutions, or they can be euthanized. Some zoos instead will allow for breeding between non-recommended pairs, but that leaves them with the problem of what to do when the offspring themselves grow to reproductive age.

Each of those approaches comes with positive outcomes as well as tradeoffs with respect to animal welfare.

Starting with the simplest, the issue with permanent sterilization is that, in most cases, it's permanent. While a given animal might not get a breeding recommendation this year, they might next year. Or, perhaps they successfully reproduce but the juvenile doesn't him- or herself survive to breeding age, making it preferable to reintroduce the parent into the gene pool. While sterilization addresses the inbreeding problem, it doesn't address the overpopulation problem.

The problem with transferring the individuals to other institutions – whether that's an animal who hasn't been recommended for breeding, or a "surplus" animal who is the result of a non-recommended mating, is also fairly straightforward. Having cared for an individual animal since birth, one might argue that zoos are collectively responsible for the animal's welfare for the duration of its life. To that end, animals should only be transferred to places that can provide adequately for their health and welfare, which includes appropriate socialization (for social species, like giraffes). In fact, it is a violation of AZA's Code of Professional Ethics to transfer animals to inadequate facilities.

What happens if there is no space to hold and care for an animal, and there are no suitable alternative facilities? Some would argue that it is better to euthanize the animal than to send it to a facility where the quality of its life would suffer. As Ingrid J. Porton points out in Wildlife Contraception , "there are records of transferred zoo-bred mammals from big cats, lemurs, and chimpanzees to a range of ungulate species that have eventually reached roadside animal attractions, circuses, for-profit animal breeding facilities, exotic animal auctions, and the pet trade." And that's to say nothing of any progeny that transferred animal might have in the future. Should length of life be privileged over quality of life? Should length of life be privileged over the uncertain quality of life of potential descendents? Is it better to provide a humane death for an animal when the only alternative would find the animal in a circus or in the backyard of a wealthy private citizen?

Assuming that there is space to keep a non-breeding animal, contraception might be a better approach. Unlike sterilization, contraception is meant to be reversible. But the issue is that in most cases and for most species, contraception is still considered experimental . Long-term research on the safety and toxicity of hormonal contraception is still ongoing. And for some species, it isn't clear yet whether an animal can become pregnant and give birth to viable offspring after months or years of contraceptive administration. "Without conclusive data on the consequences of contraceptive use in all species, the ethical dilemma becomes whether the possibility of health risks associated with contraceptive use is outweighed by the benefit of not separating animals or of not producing surplus animals," Porton writes. Could the contraceptives result in side effects that could shorten the life of an animal, or in illness? Is that an acceptable risk to take when the alternative is producing offspring for which the zoos within a given network can't provide? When some risk is inevitable no matter what approach is taken, is a known risk to the parents preferable to an unspecified gamble on the welfare of future unplanned progeny?

Another downside to contraception, according to some, is that it deprives animals of expressing behaviors related to mating, reproduction, and parenting. They argue that if zoos endeavour to allow the animals in their care to express the widest range of species-typical behaviors as possible, that necessarily includes breeding. That mating and raising young is a "fundamental and enriching part of life," as Porton puts it. She continues, "this view holds that all social aspects of mating and rearing offspring are of overriding importance to the well-being of captive animals and to prevent this experience could be considered unethical." For institutions that have adopted this philosophy, animals are not contracepted and social species are housed in mixed-species enclosures. If there are offspring born from individuals whose genes are already well-represented in the population, then when the offspring is old enough that it would naturally disperse from its mother's social group, as was the case with the Copenhagen Zoo giraffe, then the zoo must decide what to do with that individual.

Here lies the critical tradeoff at the heart of the controversy surrounding the death of Marius at the Copenhagen Zoo.

On the one hand, those against the killing argue that the welfare of the animal in question (Marius) is of paramount importance. They might offer that contraception would have been a better alternative to prevent his birth in the first place, but that once he was born, the zoo has an obligation to continue caring for him, even if he is a so-called "surplus animal." They might argue that he could be contracepted or sterilized to prevent him from breeding and further propogating his genetic materials. Each of those arguments, of course, has its own downside as described above.

On the other hand, advocates for humane euthanasia argue that the welfare of the parents is of greater importance. They point out that the euthanasia would only occur once the juvenile has aged to the point where it would normally seek out a new social group anyway. From the parents' perspective, euthanizing their progeny (outside of their view) is not functionally different from relocating the animal to a different social group in a different institution. And if there's no space to care for the juvenile at a different zoo, or if that space would be better used by an individual with a different genetic endowment, then it may actually be preferable to euthanize the animal, while deriving as much educational and scientific benefit from the process as possible.

In addition, advocates for this position would point out a silver lining, which is that the carcass can then be broken down and used to feed the carnivores. Thus, the giraffe would enjoy maximal welfare while alive, an entirely humane death, and the lions, tigers, and other carnivores, for whom intact carcass meat itself serves as an enrichment item, would enjoy improved psychological welfare and dental health , as research repeatedly demonstrates. It's worth pointing out that, as obligate carnivores, big cats can only survive by eating meat. If the remains of Marius were not fed to them, then they would simply be fed with meat derived from the slaughter of other animals. And you can be sure that the life and death of the Marius the giraffe reflected greater welfare concerns than the factory-farmed animals who wind up in the chow served more routinely at the zoo.

By definition, zoos are an imperfect system insofar as they can not care for an infinitely increasing population and it would be irresponsible to allow it to do so. But that's not to say that nature, red in tooth and claw, is any less imperfect. A giraffe in the wild who is too weak, or too slow, or injured, will be taken down by a hungry lion, with no regard for the welfare interests of its meal, nor for the rest the giraffe's social group who bear witness to that predation. No natural ecosystem can support an infinitely increasing population any more than the artificial ecosystem created by a network of zoos, and without the selective pressure offered by predation, starvation, or drought, zoos must restrict population growth by other means.

For those who are horrified by the idea of Marius's euthanasia, I would ask what alternative they would choose, given the risks and downsides associated with each. And for those who supported the euthanasia, I would ask whether the parents' ability to experience mating and parenting behaviors was worth the uncomfortable outcome for the juvenile.

The answer to these questions is not something that science is equipped address. Science can only describe the various alternatives and what the consequences of those decisions would be. The hard part is weighing the variables and deciding what the most optimal outcome would be, from a set of imperfect choices.

Further reading:

Re-Writing the Death of a Giraffe

Why Did Copenhagen Zoo Kill Marius the Giraffe? Cultural Differences in Conservation

Header image and second image: Masai Giraffe, San Diego Zoo. Third image: Masai Giraffe, Los Angeles Zoo. All photos copyright Jason G. Goldman.

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• Published: 28 June 2018

Evaluating the Contribution of North American Zoos and Aquariums to Endangered Species Recovery

• Judy P. Che-Castaldo   ORCID: orcid.org/0000-0002-9118-9202 1 ,
• Shelly A. Grow 2 &
• Lisa J. Faust 1  

Scientific Reports volume  8 , Article number:  9789 ( 2018 ) Cite this article

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• Biodiversity
• Conservation biology

The challenge of recovering threatened species necessitates collaboration among diverse conservation partners. Zoos and aquariums have long partnered with other conservation organizations and government agencies to help recover species through a range of in situ and ex situ conservation projects. These efforts tend to be conducted by individual facilities and for individual species, and thus the scope and magnitude of these actions at the national level are not well understood. Here we evaluate the means and extent to which North American zoos and aquariums contribute to the recovery of species listed under the U.S. Endangered Species Act (ESA), by synthesizing data from federal recovery plans for listed species and from annual surveys conducted by the Association of Zoos and Aquariums. We found that in addition to managing ex situ assurance populations, zoos frequently conduct conservation research and field-based population monitoring and assessments. Cooperatively managed populations in zoos tend to focus on species that are not listed on the ESA or on foreign listings, and thus it may be beneficial for zoos to manage more native threatened species. Our results highlight the existing contributions, but also identify additional opportunities for the zoo community to help recover threatened species.

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Introduction.

Due to the magnitude and complexity of the global extinction crisis, successful species conservation will require the engagement of all potential partners: state and federal agencies, non-governmental organizations, local communities and resource users, industry stakeholders, and wildlife managers 1 . These diverse partners each bring unique perspectives, expertise, and resources, not all of which will be appropriate or necessary in every case. However, a clear understanding of the potential contributions of each partner will help to identify the most relevant entities to call upon in each case.

Zoos and aquariums (hereafter, “zoos”) are becoming more broadly recognized as important partners for conserving threatened species 2 , 3 . There is a long history of zoos engaging in species recovery, from the American bison and California condor to the black-footed ferret and Panamanian golden frog 4 . However, the role of zoos in species conservation has often focused on ex situ species management, in particular ex situ breeding 5 , 6 . For example, the Conservation Measures Partnership’s Actions Classification 7 identifies 30 distinct types of conservation actions, but specifies a role for zoos in only two of those ( ex situ conservation, outreach and communications). The conservation value of ex situ breeding has also been somewhat controversial, with views ranging from it being a last resort that diverts resources from in situ efforts 8 , to part of a continuum of management actions for threatened species 9 . Even when ex situ breeding is acknowledged as part of the conservation strategy, the ability of zoos to sustain demographically and genetically viable populations for the long-term has been questioned 10 , 11 . Undoubtedly these issues and concerns must continue to be explored, but zoos also contribute to other conservation efforts beyond ex situ breeding 12 , 13 , 14 .

Several publications have explored generally how zoos contribute to species conservation, discussing both in situ and ex situ actions. Ex situ actions can directly target the species ( e . g ., ex situ population management, rehabilitation, gene banking) 7 , or indirectly support conservation through public outreach, biological and veterinary research, and fundraising for other organizations and projects 3 , 14 , 15 . In situ actions can include engaging and educating communities in the species’ native range, protecting and restoring habitat, supplying animals and/or staff for reintroductions, and field-based monitoring 3 , 15 . Although there are many case studies of these individual actions, the extent to which zoos contribute to conservation through these actions is not well understood. One study has evaluated the impacts of a subset of in situ conservation projects branded by the World Association of Zoos and Aquariums 16 , and another summarized the number of breeding and reintroduction projects for threatened species conducted by four Canadian zoos 12 . Thus far, no study has quantified both the in situ and ex situ conservation actions conducted by zoos at a national scale.

In the U.S., all institutions accredited by the Association of Zoos and Aquariums (AZA) include species conservation as a key part of their missions, in accordance with accreditation standards. To fulfill this part of their missions, zoos carry out an array of in situ and ex situ initiatives 4 , and collaborate with other conservation organizations and government agencies. This includes the agencies [U.S. Fish and Wildlife Service (USFWS) and National Oceanic and Atmospheric Administration (NOAA) Fisheries] that implement the U.S. Endangered Species Act (ESA), which was enacted in 1973 to protect threatened species through both extinction prevention and recovery actions 17 . However, the extent and scope of these zoo conservation efforts have not been systematically evaluated beyond annual reports within the zoo community.

The goal of this study was to evaluate the contribution of zoos to the recovery of threatened species in the U.S. by quantifying and summarizing their conservation activities. Our analysis consisted of three parts: (1) Summarize the management actions for which zoos are the responsible parties, based on data from federal recovery plans for listed species; (2) Summarize the recent conservation activities reported by AZA-accredited facilities in responses to the association’s annual field conservation and research surveys; and (3) Quantify the number of listed species that currently have managed populations in AZA facilities in order to identify additional opportunities for species conservation. Using multiple datasets allowed us to compare the contributions as self-reported by AZA facilities against those as recognized by the agencies responsible for implementing the ESA. Due to the scope of our study, we did not aim to quantify the impacts of these conservation activities, although it would be a valuable assessment that could be implemented following the methods of Mace et al . 18 .

In this study we focused on the terrestrial (including invertebrate and amphibian) and avian species listed under the ESA as of February 2017. Therefore, the large number of zoo conservation projects on marine and aquatic species, and the small number on plant species, were outside the scope of this assessment. Zoo conservation projects involving species with other risk statuses ( e . g ., Candidate, Under Review, or Proposed status under the ESA; state-listed; those ranked as Threatened (VU, EN, CR) or Extinct in the Wild (EW) under the IUCN Red List but not listed under the ESA) were also not represented in this assessment. Additionally, we focused on listed species whose native range included the U.S. ( i . e ., U.S. or U.S./foreign listings under the ESA; “U.S. listings” hereafter) in the first two parts of our analysis, but explored the overlap between both U.S. and foreign listings with managed zoo programs in the last section.

Roles of Zoos and Aquariums in Recovery Plans

The ESA requires every listed species to have a recovery plan, which documents the management actions and the criteria that determine when the species can be delisted. We gathered recovery plan data from the USFWS Recovery Plan Ad Hoc Report database ( http://ecos.fws.gov/ecp0/ore-input/ad-hoc-recovery-actions-public-report-input ), by querying all recovery actions that list a zoo, aquarium, or AZA (“zoos”) as the responsible party. As of September 2016, the recovery plans for 73 listed species (15.1% of the 482 listings that have recovery plans) named zoos as responsible for at least one recovery action. Of these, we focused on the 54 terrestrial and avian animals (6 amphibians, 31 birds, 7 invertebrates, and 10 mammals) for this analysis. Forty-two of these species are currently listed as Endangered and eight as Threatened, one is not listed due to extinction but was a species of concern at the time of recovery planning ( Moho bishopi ), and three have been delisted since the plan was written due to recovery ( Urocyon littoralis subspecies littoralis , santacruzae , and santarosae ).

In total, there were 38 recovery plans (some plans included more than one species) that described 468 recovery actions for which zoos were the responsible party. These actions involved 39 individual zoos or aquariums, or else listed AZA as the responsible party (see Table  S1 for complete list of institutions). We determined 11 keywords to represent the major types of conservation activities attributed to zoos (Table  1 ), which were derived through an iterative process. We started with 52 keywords used by AZA to categorize zoo conservation and science projects (see next section), and condensed them into 9 categories ( e . g ., anti-poaching/patrolling, disaster/emergency response, human-wildlife conflict, and wildlife trade were grouped into “threat mitigation”). We assigned these broader keywords to each recovery action based on the action descriptions from the plans, and added two keywords (fundraising, management/planning) to describe recovery actions that did not fit into existing keywords. In some cases multiple keywords were assigned to an action, resulting in a total of 605 keywords assigned.

The majority of recovery actions related to managing and/or maintaining an assurance population (36.1% of keywords), research (27.4%), and population augmentation (23.5%; Fig.  1A ). Research included a broad range of topics relevant to species recovery, from investigating the impacts of contaminants, to modeling disease dynamics, to evaluating methods for habitat restoration. Besides population augmentation, other in situ recovery actions primarily consisted of population monitoring and assessments (12.4%), but there were also a small number of projects related to mitigating threats (1.7%) and to protecting and restoring habitat (0.9%). An unexpected type of zoo recovery action was management and planning (8.3%), which included projects that either involved or supported decision-making by the recovery team, such as coordinating program components, prioritizing tasks, or evaluating existing strategies. These tasks help to improve efficiency and flexibility and therefore can contribute greatly to the success of a conservation program. Other previously recognized contributions from zoos such as education and outreach 7 , 19 and husbandry knowledge and veterinary care 13 were also represented in recovery plans (7.5% and 7.1%, respectively). Finally, zoos contributed to conservation by providing project funds (4.5%), which were raised not only through visitor fees 8 but also by securing state, federal, and private grants. The keyword related to providing rescue, rehabilitation, or sanctuary facilities did not apply to any zoo-based recovery actions described in these plans. However, they may be more likely to be included in plans for ESA-listed marine species ( e . g ., sea turtles).

Conservation activities carried out by North American zoos and aquariums for species listed under the Endangered Species Act, sorted by type using 11 keywords. The number of instances of each keyword is shown at the base of the bars. ( A ) Distribution of the 468 recovery actions for which zoos and aquariums are the responsible party as described in recovery plans; a total of 606 keywords were assigned. ( B ) Distribution of the 644 field conservation and research project submissions by zoos to the 2013–2015 Annual Report on Conservation and Science (ARCS) survey; a total of 786 keywords were assigned.

Recovery actions were distributed unevenly across taxa (Fig.  2A ), with the majority of actions pertaining to birds (357 out of 468 actions). This was because the Revised Hawaiian Forest Birds Recovery Plan 20 included a very similar set of up to 19 recovery actions for each of 19 different bird species (for a total of 289 recovery actions) that involved either the San Diego Zoological Society or the Honolulu Zoo. To compare recovery action types among taxonomic groups, we further clustered the 11 project keywords into three broader categories: ex situ , in situ , and knowledge/capacity. Ex situ included the projects related to animal care and management at zoos (i.e., assurance population, husbandry/veterinary care, rescue/rehabilitation/sanctuary), whereas in situ included projects that took place at the species’ native range (i.e., population augmentation, monitoring/assessments, threat mitigation, and habitat creation/restoration/protection). The remaining project types all focused on increasing biological knowledge or the capacity for conservation (i.e. research, education/outreach, management/planning, fundraising). For birds, all three categories of projects were similarly common, with a slightly lower proportion of in situ projects (Fig.  2A ). In contrast, in situ projects were the most common category for invertebrates. Knowledge and capacity-building projects (primarily research) were the most common type of zoo recovery action for mammals and amphibians, accounting for 56% and 40% of their action keywords, respectively.

Conservation activities carried out by North American zoos and aquariums for species listed under the Endangered Species Act, by taxonomic group. Activities were aggregated into three categories based on the activity type keywords: conservation knowledge or capacity (research, education/outreach, management/planning, fundraising), ex situ (assurance population, husbandry/veterinary care, rescue/rehab/sanctuary), and in situ (population augmentation, monitoring/assessments, threat mitigation, and habitat creation/restoration/protection). The total instances of keywords for each taxonomic group are shown in parentheses. ( A ) Distribution of the 468 recovery actions for which zoos and aquariums are the responsible party from recovery plans; a total of 606 keywords were assigned. ( B ) Distribution of the 644 field conservation and research project submissions by zoos to the 2013–2015 Annual Report on Conservation and Science (ARCS) survey; a total of 786 keywords were assigned.

In addition to working with federal agencies in recovery programs, zoos also collaborate with other partners, including academic institutions, research institutions, or universities (collectively “academic institutions”) and other non-governmental organizations (NGOs). Thus we also examined the involvement of these two types of partners in the recovery actions that specified zoos as a responsible party. All four recovery actions related to habitat creation/restoration/protection listed either academic institutions (2 actions) or other NGOs (2 actions) as additional responsible parties, suggesting such field projects may require larger collaborations to implement. Academic institutions were involved in nearly half of the actions with research as a keyword (54 out of 128 actions), but did not collaborate with zoos as much on other types of recovery actions (<13% for all other types). Other NGOs partnered with zoos most frequently on actions related to assurance populations (26 out of 169 actions) and research (26 out of 128 actions), but proportionally they collaborated primarily on actions related to education and outreach (14 out of 35 actions) and threat mitigation (2 out of 8 actions).

Although recovery plans provide an official documentation of the extent to which zoos participate in recovery programs when the plans were created, they do not provide the full picture. Nearly one-third of all U.S. listed animals do not have a recovery plan (482 out of 710 listed animal species had plans as of September 2016), and finalized plans are rarely updated and therefore tend to exclude more recent or current projects. Additionally, a zoo’s involvement may not have been explicitly described as a recovery action, or only the primary holding facilities may have been identified when multiple institutions are involved.

Conservation Activities Reported by Zoos and Aquariums

We next summarized zoo conservation activities based on the AZA’s field conservation and research surveys from 2013–2015. These surveys are used to produce the association’s Annual Report on Conservation and Science (ARCS; http://www.aza.org/annual-report-on-conservation-and-science ). In the field conservation survey, AZA member institutions report only their conservation efforts that have direct impacts on animals and habitats in the wild. In the research survey, they report on any hypothesis-driven research conducted at these institutions or by their staff and the resulting publications. Response rates differed between surveys and years, with 86–92% of institutions responding for the field conservation survey and 52–64% responding for the research survey between 2013–2015. Although this dataset likely underrepresents the conservation and research projects in zoos for listed species, it still provides the most comprehensive current summary of these activities across AZA. Because of the specific focus of these surveys, the responses would also exclude education programs that do not directly target the local communities in the species’ native range. Therefore our analysis leaves out many of the conservation-oriented education projects carried out by zoos, which can also have significant impacts on achieving biodiversity conservation 21 .

We queried the database of field conservation and research survey responses for references to ESA-listed species in the project titles, descriptions, or the selected focal species. We tallied the number of conservation project submissions, representing unique combinations of institutions, projects, and species. That is, the same project may involve multiple institutions, and we count these as unique projects for each institution. This is because each institution may submit the project under a different name or description, thereby making it difficult to consistently delineate unique projects. Between 2013–2015, 142 AZA institutions reported a total of 644 active conservation projects involving 74 ESA-listed, U.S. terrestrial and avian species (23 mammals, 21 birds, 12 amphibians, 11 reptiles, and 7 invertebrates). Of these, 50 are currently listed as Endangered and 24 as Threatened. Although 54 of the 74 listings have finalized recovery plans, only 18 of those plans mentioned zoos as responsible parties for recovery actions.

Similar to the actions from recovery plans, we assigned each zoo project from the survey data to one or more of the 11 keywords representing different types of conservation activities (Table  1 ). Of the 786 keywords assigned, most were related to research (25.2%), monitoring/assessments (17.6%), population augmentation (16.0%), and managing assurance populations (12.7%; Fig.  1B ). Fundraising directed to recovery programs or conservation organizations (for purposes unspecified in the survey response) accounted for 11.3% of the keywords. Projects related to education and outreach (targeting local communities in the species’ native range) accounted for 5.2% of the keywords, and all other keywords were used fewer than 3% of the time. Compared to the conservation actions described in recovery plans, zoos reported a smaller proportion of activities related to assurance populations, but a larger proportion related to monitoring and assessments, and to habitat creation/restoration/protection. This suggests that zoos are contributing more to in situ conservation projects than is recognized in recovery plans. Zoos also reported more fundraising projects than represented in recovery plans, and additionally reported several projects related to providing rescue, rehabilitation, or sanctuary facilities. Both data sources agreed that research made up a large proportion of the conservation activities in zoos, and that there was great variation in the types of research conducted. Research projects reported by zoos ranged from understanding the genetic structure of Hawaiian petrel ( Pterodroma sandwichensis ) populations, to measuring stress levels of Guam kingfishers ( Todiramphus cinnamominus ) in human care, to developing gene banking methods for black-footed ferrets ( Mustela nigripes ).

Comparing among taxonomic groups, the majority of zoo conservation projects involved listed mammal species (318 of 644 projects), and only 25 projects involved invertebrates. Although the distribution of projects among taxa is similar to a previous assessment of in situ conservation efforts by zoos around the world 16 , none of the mammalian species in our dataset were primates due to our focus on U.S. species. Based on the keyword categories we assigned to each project, we found in situ projects were most common for listed amphibians and invertebrates (Fig.  2B ), and they primarily consisted of population augmentation projects. Knowledge and capacity projects were least common for amphibians and invertebrates, but they made up the largest proportion of projects for mammals, birds, and reptiles (consisting primarily of research projects). Ex situ projects made up less than 20% of all conservation projects reported by zoos for listed mammals, birds, and reptiles. Compared to the actions from recovery plans, a larger proportion of in situ projects were reported by zoos for all taxonomic groups, and a smaller proportion of ex situ projects were reported for all taxa except amphibians (Fig.  2 ).

We estimated the amount that AZA zoos spend on listed species by summing the project expenditures reported in the ARCS surveys. From 2013–2015, total spending on the reported field conservation and research projects specifically targeting the 74 ESA-listed species summed to $28.9 million, or on average $9.6 million per year. For context, the reported average spending per year on the same set of species in 2013–2015 was $146.4 million by all federal agencies, and $7.9 million by all state agencies 22 , 23 , 24 . Among the different types of conservation activities, the majority of funds were spent on assurance populations, followed by population monitoring and assessment and research (Fig.  3A ). Comparing across taxa, expenditures were greatest on conservation projects for bird and mammal species (Fig.  3B ).

Spending by North American zoos and aquariums on conservation projects for species listed under the Endangered Species Act, as reported in the 2013–2015 Annual Report on Conservation and Science (ARCS) survey. The proportional spending (out of the total $28.9 M spent across 3 years) is shown by ( A ) project keyword and ( B ) taxonomic group.

Listed Species with Managed Populations in Zoos and Aquariums

The recovery plans and AZA surveys provide an overview of the extent to which zoos currently contribute to recovering listed species. However, additional opportunities for conservation may exist, as a number of ESA-listed species have ex situ populations in zoos that are cooperatively managed. Since the 1980s, zoos have collaborated in managing the animals in their care through goal setting, cooperative breeding, and exchanging animals across institutions, with the aim of improving the health (e.g., demographic viability, genetic diversity) of those zoo animal populations 25 , 26 . In North America, cooperatively managed populations are those with a Species Survival Plan ® (SSP) program, which is implemented by AZA member institutions. SSPs may also coordinate the conservation, research, and educational initiatives among institutions to support in situ species recovery. These programs therefore represent opportunities for zoos to contribute further to conservation efforts, because they have an established management structure and working partnerships across institutions. Cooperative management also generates a great deal of species-specific knowledge on breeding, veterinary care, behavior, and demography, which can inform or facilitate conservation actions. For example, knowledge on how to breed animals successfully and to care for and rear offspring may be important for helping to improve reproduction of a threatened species. Further, the establishment of an SSP program demonstrates a long-term commitment to the species by multiple AZA institutions, which may be leveraged to promote engagement in and support for wild populations of the same species.

Overall, 143 of the 482 SSP programs (29.7%) were for ESA-listed species, representing 154 listings (which included separate listings for Distinct Population Segments or subspecies of the same species). The majority of these were for species listed as Endangered (83.4%) and as foreign (77.9%). Of the 387 listings for U.S. terrestrial and avian species, 36 (9.3%) currently have zoo populations managed by an SSP program. Interestingly, only 14 of the 54 species whose recovery plans specified roles for zoos had SSP populations, and 24 of the 74 species identified in the AZA surveys had SSP populations. Only 10 species overlapped across the three datasets, meaning they have recovery plans that specified a role for zoos, conservation projects reported by zoos in AZA surveys, and zoo populations managed by an SSP program. This finding suggests that an SSP program is not required for zoos to participate in recovery programs, and many zoos work with listed species outside of the SSP framework. On the other hand, there are additional SSP programs that could participate in that species’ recovery but currently do not.

Most of the SSP programs for listed species involved mammals, with existing programs for 21 of the 74 (28.4%) U.S. mammal listings (Fig.  4A ). All other listed taxa were much less represented, especially invertebrates, for which the American burying beetle was the only listing (out of 148) with an SSP program. The picture was similar when including both U.S. and foreign listings, with 84 additional SSP programs for foreign-listed mammals, and a smaller number of additional SSP programs for foreign-listed birds and reptiles (14 and 13, respectively; Fig.  4B ). In summary, the majority of SSP programs did not manage listed species, but those that did tended to focus on species that were more at risk (listed as Endangered rather than Threatened). There was also a taxonomic bias for SSP programs to focus on mammals and a geographic bias for non-U.S. species, many of which were native to African and Central American countries. Our results parallel findings from a previous study that zoo and aquarium collections favor larger vertebrate species 5 . However, the bias of SSP programs toward non-U.S. species contrasts with an earlier finding that zoos tended to focus on mammal and bird species that are native to economically developed countries 27 .

The proportion of terrestrial and avian animal species listed under the Endangered Species Act that have cooperatively managed populations in AZA-accredited zoos and aquariums, by taxonomic group and listing status (T = Threatened, E = Endangered). ( A ) The proportion of U.S. listings with managed programs for the listed species. ( B ) The proportion of U.S. and foreign listings with managed programs for the listed species. ( C ) The proportion of U.S. listings with managed programs for a congener of the listed species. ( D ) The proportion of U.S. and foreign listings with managed programs for a congener of the listed species.

Zoos have the potential to contribute even further to species recovery, as shown by the number of listed species that have a congener with a managed SSP population in zoos (Fig.  4C,D ). Management of a closely related species in the same genus produces valuable husbandry and biological information that may be useful for informing the conservation of the listed species. Institutions holding the congeners may also develop education programs or design exhibits to promote conservation actions for the closely related listed species. Additionally, since zoos already have the resources and facilities to house a closely related species, it may be possible for those institutions to house the more threatened species instead, if ex situ breeding or rehabilitation is deemed beneficial (of course, species-specific behaviors and requirements will determine the extent to which that would be feasible, while threats and recovery strategies will determine the appropriateness of an ex situ breeding program). Across all taxa, there were SSP programs for the congeners of 70 out of 387 (18.1%) U.S. listings, and 299 out of 969 (30.9%) U.S. and foreign listings of terrestrial and avian species. In particular, there were managed programs for the congeners of 36.5% and 41.4% of U.S. listings for mammals and reptiles, respectively (Fig.  4C ), and 51.5% and 53.2% of total (U.S. and foreign) listings for mammals and reptiles, respectively (Fig.  4D ). This represents a significant body of knowledge and resources that could greatly enhance species recovery efforts, but have yet to be broadly utilized.

Our evaluation showed that zoos contribute to a diverse array of in situ and ex situ conservation efforts, and serve as important partners in the recovery of threatened species in the U.S. Zoo conservation activities (Table  1 ) spanned many of the conservation actions previously described 7 . Beyond maintaining ex situ populations 5 and increasing public understanding of biodiversity 21 , zoos carry out many more in situ projects than typically recognized (though see Olive and Jansen 12 ), including a large number of monitoring projects. We also found that zoos conduct a range of field- and zoo-based conservation research projects, which were nearly as numerous as ex situ breeding efforts (Fig.  1 ). Biodiversity monitoring and research both help to support successful species recovery, but they are not commonly viewed as significant ways in which zoos contribute to conservation. Our findings support earlier studies that showed these critical conservation actions are increasingly being funded or conducted by NGOs 28 , 29 , including zoos.

However, additional opportunities exist. We found that similar to zoo holdings overall 27 , managed SSP populations currently focus on non-threatened species. Among listed species, however, managed programs do tend to prioritize species that are more at risk of extinction. There are many considerations that determine the selection of species for zoo exhibits, and management programs are increasingly including conservation status in their decision-making. However, if a species is especially difficult to house, cannot reproduce successfully, or has low survivorship in zoos, then establishing ex situ populations may not be feasible or worthwhile. Further, there are ways to contribute to conservation even if zoos are managing the less at-risk species that are closely related to a threatened species, as discussed above.

U.S. zoos may also increase their conservation efforts by managing more native threatened species, as our results showed a tendency for SSP programs to focus on foreign-listed species. Ex situ populations would ideally be established in the species’ native range 2 , but currently >90% of the U.S. listed avian and terrestrial species do not have an SSP population in North American zoos. Further research is needed to evaluate whether and the extent to which those listed species would benefit from ex situ population management. Zoos are also carrying out relatively few education and outreach programs that directly impact listed species in the wild (Fig.  1B ). By including more native threatened species, zoos could develop associated education and outreach programs to engage the community most likely to impact the species and promote direct conservation actions. Of course, zoo education programs that do not directly affect wild populations are still valuable 21 , and we reiterate that our review did not summarize the magnitude of those existing efforts.

Finally, our findings suggest a need for greater coordination across zoos and better engagement with other conservation science partners. For example, 40 institutions reported working on various field conservation and research projects for the polar bear in the AZA surveys, but it is unclear the extent to which these efforts were coordinated to maximize their effectiveness. Only 5 recovery plans (for 5 species) named two or more zoos as the responsible party for any recovery action, suggesting such coordination among zoos is infrequent or poorly represented in plans. Only a quarter of the recovery plan actions conducted by zoos involved either academic or NGO partners, although integrating efforts into larger collaborations could lead to better outcomes 29 . However, coordination with other conservation partners may be increasing, as more partnerships between zoos and academic institutions are being formed ( e . g ., Smithsonian-Mason School of Conservation, the Phoenix Zoo - Arizona State University conservation partnership, the Living Earth Collaborative). Other zoo partnerships supporting species recovery include concentrated breeding centers and consortiums such as the Conservation Centers for Species Survival (C2S2), and AZA’s SAFE: Saving Animals From Extinction, a conservation framework launched in 2015 that prioritizes collaboration 14 . There are also efforts to integrate ex situ and in situ species management through the IUCN Conservation Planning Specialist Group’s One Plan Approach 30 , 31 .

In this assessment we focused on terrestrial and avian species listed under the ESA. Thus, the role of zoos in helping to conserve marine animals, plants, and species with other risk statuses remain to be examined. Additionally, further research is needed to evaluate the impacts of the many zoo conservation projects 18 , which could inform and improve future efforts. In summary, our study highlights the wide-ranging conservation actions conducted by North American zoos, and identify opportunities for better integration with the broader conservation community. By evaluating the current role of zoos in species conservation, our study provides a better understanding of the expertise, resources, and opportunities that zoos can offer as one of the many necessary partners in recovering threatened species.

Data availability

The recovery plan data analyzed in the current study are included in the Supplementary Information (Table  S2 ). The AZA survey data, except financial information, are available on AZA’s website ( http://www.aza.org/field-conservation ; http://www.aza.org/research-and-science ). Additional data are available from the corresponding author on reasonable request.

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Acknowledgements

We thank all of the AZA-accredited zoos, aquariums, and certified facilities that submitted information about their field conservation and research to AZA’s annual surveys. We also thank AZA’s Field Conservation and Research and Technology Committees for helping to refine surveys, review data submissions, and work with AZA members on their submissions. We thank A. Ahmad and S.Y. Kim for assistance with data compilation.

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J.P.C., S.G. and L.J.F. co-developed the project. S.G. compiled and analyzed the AZA survey data, and J.P.C. compiled and analyzed the recovery plan and managed program data, and prepared the manuscript and figures. All authors reviewed the manuscript.

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Che-Castaldo, J.P., Grow, S.A. & Faust, L.J. Evaluating the Contribution of North American Zoos and Aquariums to Endangered Species Recovery. Sci Rep 8 , 9789 (2018). https://doi.org/10.1038/s41598-018-27806-2

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Why zoos are good

The days of the Victorian menagerie are over, but modern zoos are much more than a collection of animals and more important than ever

I am a lifelong fan of good zoos (note the adjective) and have visited dozens of zoos, safari parks and aquaria around the world. I also spent a number of years working as a volunteer keeper at two zoos in the U.K. and my own interests now span to the history of zoological collections and their design, architecture and research so it is probably fair to say I’m firmly in the pro-zoo camp.

However, I am perfectly willing to recognise that there are bad zoos and bad individual exhibits. Not all animals are kept perfectly, much as I wish it were otherwise, and even in the best examples, there is still be room for improvement. But just as the fact that some police are corrupt does not mean we should not have people to enforce the law, although bad zoos or exhibits persist does not mean they are not worthwhile institutes. It merely means we need to pay more attention to the bad and improve them or close them. In either case, zoos (at least in the U.K. and most of the western world) are generally a poor target for criticism in terms of animal welfare – they have to keep the public onside or go bust and they have to stand up to rigorous inspections or be closed down. While a bad collection should not be ignored, if you are worried the care and treatment of animals in captivity I can point to a great many farms, breeders, dealers and private owners who are in far greater need or inspection, improvement or both.

If you are against animals in captivity full stop then there is perhaps little scope for discussion, but even so I’d maintain that some of the following arguments (not least the threat of extinction) can outweigh arguments against captivity. Moreover, I don’t think anyone would consider putting down a 10000 km long fence around the Masai Mara to really be captivity, even if it restricts the movement of animals across that barrier. But at what point does that become captivity? A 10000 m fence? 1000 m fence? What if veterinary care is provided or extra food as in many reserves or as part of conservation projects. I’m not pretending that an animal in a zoo is not in captivity, but clearly there is a continuum from zoos and wildlife parks, to game reserves, national parks and protected areas. Degree of care and degree of enclosure make the idea of ‘captivity’ fluid and not absolute.

What I would state with absolute confidence is that for many species (but no, not all) it is perfectly possible to keep them in a zoo or wildlife park and for them to have a quality of life as high or higher than in the wild. Their movement might be restricted (but not necessarily by that much) but they will not suffer from the threat or stress of predators (and nor will they be killed in a grisly manner or eaten alive) or the irritation and pain of parasites, injuries and illnesses will be treated, they won’t suffer or die of drought or starvation and indeed will get a varied and high-quality diet with all the supplements required. They can be spared bullying or social ostracism or even infanticide by others of their kind, or a lack of a suitable home or environment in which to live. A lot of very nasty things happen to truly ‘wild’ animals that simply don’t happen in good zoos and to cast a life that is ‘free’ as one that is ‘good’ is, I think, an error.

So a good zoo will provide great care and protection to animals in their care. These are good things for the individuals concerned, but what do zoos actually bring to the table for the visitors and the wider world? This is, naturally, what I want to focus on, but it is I hope worth having dealt with the more obvious objections and misapprehensions.

Conservation – reservoir and return. It’s not an exaggeration to say that colossal numbers of species are going extinct across the world, and many more are increasingly threatened and risk extinction. Moreover, some of these collapses have been sudden, dramatic and unexpected or were simply discovered very late in the day. Zoos protect against a species going extinct. A species protected in captivity provides a reservoir population against a population crash or extinction in the wild. Here they are relatively safe and can be bred up to provide foundation populations. A good number of species only exist in captivity and still more only exist in the wild because they have been reintroduced from zoos, or the wild populations have been boosted by captive bred animals. Quite simply without these efforts there would be fewer species alive today and ecosystems and the world as a whole would be poorer for it. Although reintroduction successes are few and far between, the numbers are increasing and the very fact that species have been saved or reintroduced as a result of captive breeding shows their value. Even apparently non-threatened species and entire groups can be threatened suddenly (as seen with white nose syndrome in bats and the Chytridiomycosis fungus in amphibians) it’s not just pandas and rhinos that are under threat.

Education. Many children and adults, especially those in cities will never see a wild animal beyond a fox or pigeon, let alone a lion or giraffe. Sure television documentaries get ever more detailed and impressive, and lots of natural history specimens are on display in museums, but that really does pale next to seeing a living creature in the flesh, hearing it, smelling it, watching what it does and having the time to absorb details. That alone will bring a greater understanding and perspective to many and hopefully give them a greater appreciation for wildlife, conservation efforts and how they can contribute. All of that comes before the actual direct education that can take place through signs, talks and the like that can directly communicate information about the animals they are seeing and their place in the world. This was an area where zoos were previously poor and are now increasingly sophisticated in their communication and outreach work. Many zoos also work directly to educate conservation workers in foreign countries or send keepers abroad to contribute their knowledge and skills to zoos and preserves helping to improve conditions and reintroductions all over the world.

Research. If we are to save many wild species and restore and repair ecosystems we need to know about how key species live, act and react. Being able to study animals in zoos where there is less risk and less variables means real changes can be effected on wild populations with far fewer problems. Knowing say the oestreus cycle of an animal or their breeding rate helps manage wild populations. Things like capturing and moving at-risk or dangerous individuals is bolstered by knowledge in zoos about doses for anaesthetics, and experience at handling and transporting animals. This can make a real difference to conservation efforts and to reduce human-animal conflicts, and collectively provide a knowledge base for helping with the increasing threats of habitat destruction and other problems.

All in all with the ongoing global threats to the environment it’s hard for me to see zoos as anything other than being essential to the long-term survival of numerous species. Not just in terms of protecting them and breeding them for reintroduction, but to learn about them to aid those still in the wild, as well as to educate and inform the public about these animals and their world: to pique their interest so that they can assist or at least accept the need to be more environmentally conscious. Sure there is always scope for improvement, but these benefits are critical to many species and potentially at least, the world as a whole, and the animals so well kept and content, that I think there can be few serious objections to the concept of good zoos what they can do. Without them, the world would be, and would increasingly become, a much poorer place.

A version of this piece was first published in 2012 here .

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• Conservation

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Research Article

An exploration into the efficacy of public warning signs: A zoo case study

Roles Data curation, Formal analysis, Investigation, Methodology, Writing – original draft

Affiliation Department of Psychology, University of York, York, United Kingdom

Roles Data curation, Formal analysis, Investigation, Writing – review & editing

Roles Data curation, Project administration, Writing – review & editing

Affiliations Craven College, Skipton, United Kingdom, Flamingo Land Ltd., Kirby Misperton, United Kingdom

Roles Conceptualization, Project administration, Resources, Supervision, Writing – review & editing

Affiliations Flamingo Land Ltd., Kirby Misperton, United Kingdom, CIRCLE, Environment Dept., University of York, York, United Kingdom, Tropical Forest and People Research Centre, University of the Sunshine Coast, Sippy Downs, Queensland, Australia

Roles Conceptualization, Formal analysis, Investigation, Methodology, Project administration, Supervision, Writing – review & editing

* E-mail: [email protected]

• Ellie N. Parker, 
• Lauren Bramley, 
• Laura Scott, 
• Andrew R. Marshall, 
• Katie E. Slocombe

• Published: November 9, 2018
• https://doi.org/10.1371/journal.pone.0207246
• Reader Comments

Unauthorised feeding and touching of the animals by visitors to zoos and wildlife parks pose serious threats to the health of both animals and visitors alike. We tested the efficacy of four different “do not feed” signs designed to prevent zoo visitors from feeding a group of meerkats. Signs consisted of one of two different written messages and imagery of either a pair of watching human eyes, or meerkat pawprints as a control. Covert observation of visitor behaviour in the presence and absence of the signs was analysed. Visitors were significantly less likely to feed the meerkats when signs were present, than when they were absent. The effect of the signs was specific to the targeted behaviour in that feeding was reduced, but attempts to touch the meerkats increased with the presence of the signs. We did not find that the presence of watching eyes or the different wording on the signs affected the likelihood of visitors feeding the meerkats. We also examined factors that influenced the likelihood of visitors attending to the signs. We found that children were more likely to attend to signs than adults which has important implications for the design of such signs. Together our findings show that signs are effective in reducing the unwanted behaviours they target but may also result in displacement of these negative behaviours and that children are more likely to attend to these signs than adults.

Citation: Parker EN, Bramley L, Scott L, Marshall AR, Slocombe KE (2018) An exploration into the efficacy of public warning signs: A zoo case study. PLoS ONE 13(11): e0207246. https://doi.org/10.1371/journal.pone.0207246

Editor: Valerio Capraro, Middlesex University, UNITED KINGDOM

Received: June 29, 2018; Accepted: October 26, 2018; Published: November 9, 2018

Copyright: © 2018 Parker et al. This is an open access article distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Data Availability: The data for the current study is available to download from the York Research Database ( https://doi.org/10.15124/cf5a42f1-8e2e-4b10-bc75-deea086a01ee ).

Funding: Flamingo Land provided support in the form of salaries for author A. R. Marshall, but did not have any additional role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. The specific roles of these authors are articulated in the ‘author contributions’ section. No other funding was received for the project.

Competing interests: The commercial affiliation between author A.R. Marshall and Flamingo Land does not alter our adherence to PLOS ONE policies on sharing data and materials. We have no other competing interests to declare.

Introduction

Zoos provide a unique opportunity for visitors to interact with wild and exotic animals. Educational demonstrations, animal rides, public feeding and children’s zoos have long since been commonplace in zoos to attract and engage visitors [ 1 ]. Direct contact is a particular draw for visitors, with research finding 65% of teachers in a survey considered touching the animals important when visiting with students [ 2 ]. However, zoonotic disease transmission poses risks for humans who make contact with animals [ 3 ]. Additionally, visitors may detrimentally affect the animals themselves as proximity to, and interactions with, humans can induce stress [ 4 ].Audience induced stress might, however, be mitigated by chronic exposure in some primate species, and visitors throwing food to primates could have been enriching [ 5 ]. However, unauthorised feeding poses serious nutritional risks for the animals’ health such as increased chance of obesity and diabetes [ 5 ]. It is important to explore how visitor behaviour can be changed so that the risks to both visitors and animals that are associated with unauthorised feeding and physical contact can be effectively reduced.

“Do not feed” signs are one of the oldest forms of signs found in zoos [ 6 ] and play a vital role in promoting zoo inhabitants’ welfare. An investigation into the efficacy of “do not feed” signs found no difference in levels of feeding between no sign and a simple, instructional sign (“Please do not feed the animals”). However, an explanatory sign (“Please do not feed. These animals are on special diets”) significantly reduced feeding in a monkey exhibit [ 7 ]. This highlights the need to understand the aspects of sign design that influence the efficacy of the signs. In terms of wording, research suggests that less may be more as signs with fewer words are read by more people while longer signs attract less attention [ 6 ]. However, once a message has been attended to, even if it is not read carefully, increasing the number of arguments in a message can still increase its persuasiveness [ 8 ].

Simply changing words in economic decision problems can influence peoples’ decisions by suggesting how they should respond [ 9 ]. Compliance with sign messages can also be greatly influenced by the wording and framing of the message. In environmental research, research has found a negatively worded message (“please do not remove petrified wood from the park”) rather than a positively worded message (“please leave petrified wood in the park”) was more successful at deterring people from stealing wood [ 10 ]. A variety of other studies also support a negativity bias, where negative framing increases cooperation with the message. Health psychology research suggests that participants are more likely to perform testicular and breast self-examinations when a message is negatively framed [ 11 , 12 ]. Negatively framed messages seem to be most effective at influencing behaviour when individuals are already interested in the issue: one study found a negatively framed message encouraging animal adoption was significantly more effective than a positively framed message, but only with individuals who were already interested in animal adoption [ 13 ].

The degree to which a sign engages the audience can also be affected by its perceived relevance. Previous research outlines the importance of framing the message personally toward the current reader to maximise its relevance [ 14 ]. Simply using personal pronouns can also make a message more direct and increase its significance to the audience [ 6 ]. Attitudes and behaviours are most likely to change if readers are illustrated as the audience who will be personally affected by their actions [ 15 ].

It is clear that the wording of sign messages affects the likelihood of audiences attending to and complying with them, but imagery has also been shown to affect a sign’s efficacy. Pictures closely related to the accompanying text can significantly increase attention and recall of the related message [ 16 ] and are often more universally understood than text [ 17 ]. Pictograms can therefore be especially useful for zoo visitors with lower literary abilities such as children [ 18 ].

The application of ‘watching’ eyes to messages has been shown to increase prosocial behaviours and adherence to messages prohibiting negative behaviours in a variety of contexts by provoking reputational concerns (e.g. [ 19 , 20 ]). For instance, signs with eyes displaced over 60% of bike theft on a university campus from experimental locations to control locations nearby [ 21 ]. Another line of research into prosocial behaviour found prosociality in an anonymous, one-shot game to be driven by a preference to do the right thing morally and that this preference to ‘do good’ was as strong as the preference to avoid doing wrong [ 22 , 23 ].

The current study aimed to test the efficacy of “do not feed” signs at deterring zoo visitors from engaging in unauthorised feeding or touching of animals and additionally whether different sign wording and the presence of watching eyes affected their efficacy or the attention they drew from zoo visitors. Covert observations of visitor behaviour surrounding a meerkat enclosure were conducted in the absence or presence of signs with varying wording and imagery. We used four signs with a unique combination of wording and imagery. We predicted, in line with previous findings [ 7 ], that there would be a significant reduction in feeding when a sign was present compared to absent. Given the specificity of the sign messages to feeding, it was predicted that there would be no significant difference in the levels of trying to touch the meerkats when the sign was present and absent.

In terms of sign design, it was predicted that there would be a significantly lower proportion of visitors feeding meerkats when signs with a longer explanatory text [ 7 ] and personal wording [ 14 ] were present compared to the signs with shorter, non-personal text. In line with previous findings [ 21 , 24 , 25 ], we predicted there would be a significantly lower proportion of visitors feeding and trying to touch meerkats when signs with watching eyes versus a control image were present. Although the sign doesn’t address touching the meerkats, previous research has found a sign with watching eyes reduced littering even with an unrelated message [ 25 ], thus the watching eyes may also reduce trying to touch the animals which we assumed visitors knew they should not be engaging in.

We examined various factors that might have affected whether visitors overtly paid attention to the sign. As several studies have suggested that sign readers are usually adults rather than children [ 6 , 26 ], we predicted that more adults than children would attend to the signs. In line with previous research [ 6 ] we predicted that more attention would be paid to signs containing the shorter message and that watching eyes may capture attention more than pawprints due to the salient nature of eyes as important social stimuli.

Ethics statement

Both the University of York Department of Psychology and Department of Biology Ethics Committees approved the study, including covert observation and the concept for the study was also approved by the Flamingo Land Ethics Committee. Informed consent could not be obtained without affecting people’s behaviour, however signs were displayed at the park entrances highlighting that observations of visitors were being conducted and all behaviour was observed in a public area where visitors could be expected to be observed by others. The individual in the photos used for the watching eyes in this manuscript has given written informed consent (as outlined in PLOS consent form) to publish this photograph. The data for the current study is available to download from the York Research Database ( https://doi.org/10.15124/cf5a42f1-8e2e-4b10-bc75-deea086a01ee ).

Flamingo Land Theme Park and Zoo (hereafter “Flamingo Land”) was the 4th most visited paid attraction in England in 2016 having experienced 1,610,556 visitors [ 27 ]. This study focussed on a meerkat enclosure where animal keepers anecdotally reported high levels of unauthorised feeding. There was no existing signage on the enclosure studied.

Participants

Participants were observed covertly by experimenters dressed in inconspicuous clothing. Signs at Flamingo Land’s entrance informed visitors that observations may be taking place and all observations occurred in a public place where one might expect to be observed by other visitors and zoo personnel.

Three meerkats aged 8–9 years old lived in the study enclosure (2 males, 1 female). The meerkats were fed a specialised diet twice daily by keepers. During observations they could access an inside area and an outside enclosure where an approximately 1m high wall separated the meerkats from visitors. Observations of all three outdoor enclosure walls available to visitors could be made from one position enabling experimenters to take all occurrence recordings of visitor behaviour.

As observations were covert, data were noted in spreadsheets on the Google Sheets app using the experimenter’s iPhone SE. One sign was placed in the centre of each of the three enclosure walls the visitors had access to, and were produced in the style of all Flamingo Land’s signs ( Fig 1 ). The signs all contained a pictogram with a hand, apple and meerkat silhouette within a prohibited action image ( Fig 1 ), based on previous research suggesting the most effective “do not feed” sign pictograms contain a hand, food item and animal [ 28 ]. Each of the four signs also contained a fully factorial combination of two forms of wording and imagery ( Table 1 ; Fig 1 ). The watching eyes and pawprints images ( Fig 1 ) were 15cm wide and 4cm tall and were laminated and attached with Velcro.

• PPT PowerPoint slide
• PNG larger image
• TIFF original image

The signs had a brown wood-effect background with yellow borders and text. The eyes and pawprints were greyscale.

https://doi.org/10.1371/journal.pone.0207246.g001

https://doi.org/10.1371/journal.pone.0207246.t001

A between-subjects design was used assuming visitors recorded within and between each of the different conditions were independent, thus each visitor only experienced one sign or baseline condition.

All data were collected on weekdays between 11:30am and 2:30pm during the school summer holidays as this was the busiest time of day and year, thus maximising the sample size. Baseline data (no sign) were collected for 10 days and following this, the four sign designs were rotated for 10 days, whereby each day a different sign design was used. Signs were installed prior to the start of each observation session. On eight days the same sign remained for the whole observation period, but on two days the signs were changed part way through to equalise the amount of observation with each type of sign.

Data collection

Data were collected by two experimenters, only when the meerkats were in their outdoor enclosure, and hence only where direct interaction between meerkats and visitors was possible. We sampled 9813 visitors over the course of 60 hours between the dates of 25th July and 23rd August 2016. We collected data in 30 minute sample periods, during which we recorded the number of visitors who visited the meerkat enclosure. We only included visitors taller than the height of the wall (e.g. excluding small children) who stood within 1m of the meerkat enclosure for 10 seconds or more as having ‘visited’ the enclosure. We recorded only visitors who were above 1m tall to ensure that they exceeded the height of the perimeter wall (and hence had full view of the meerkats), and to place focus on individuals who were potentially old enough to understand the signs. Within the 30 minute sample period we also recorded all occurrences of visitors feeding or trying to touch the meerkats. When a feeding event or touching attempt occurred, we recorded the time of the event and the age category (adult/child/both) and perceived gender (male/female/both) of the visitors involved in the event (definitions in Table 2 ).

https://doi.org/10.1371/journal.pone.0207246.t002

On days where the signs were present, we also conducted focal sign observations. The focal sign area was the area within which we deemed that the sign could be easily read. This comprised a 4.66m diameter rectangular area around the sign. Visitors were included in the focal sign sample if they stood within 1m of the wall and within the focal sign area, for 10 seconds or more. We recorded their age category (adult/child) and perceived gender (male/female) ( Table 2 ) and whether they ignored or acknowledged (pointed at, read aloud or commented on the sign) the sign.

Statistical analysis

Generalized Linear Mixed effects Models (GLMMs) with a binomial error structure were used to investigate the influence of categorical explanatory variables (e.g. sign imagery, sign wording) on a binary response variable (e.g. feed meerkats or not). These models were implemented in R (version 3.5.0) [ 29 ] using package lme4 [ 30 ]. As we sampled the behaviour of multiple people within each day and 30-minute sample period, we fitted ‘day’ and ‘sample period’ as random factors [ 31 ] by conducting random intercepts models using the package lme4 [ 30 ]. To assess the significance of a full model we compared it to a null model comprising only the intercept and random effects, using a likelihood ratio test [ 32 ]. For models containing multiple explanatory factors, we assessed the significance of each factor by comparing the full model containing the factor to a reduced model without that factor, using a likelihood ratio test.

To assess the effect of sign presence on visitor behaviour models were run where each individual who visited the meerkat enclosure was entered as a data point (N = 9813). To assess the effect of sign design on visitor behaviour models were run where each individual who visited the meerkat enclosure when a sign was present was entered as a data point (N = 4655). Finally to assess the factors that may influence whether or not a visitor attended to the sign models were run where each individual who entered the focal sign area was entered as a data point (N = 2254).

A continuous count of visitor arrivals showed 9813 people stopped at the meerkat enclosure studied during our observations. Over the course of 20 observation days, 156 occurrences of feeding and 331 instances of trying to touch were recorded. Table 3 shows that roughly equal percentages of males and females and adults and children were involved in these events, so these events are not being predominantly perpetrated by a single class of visitor. As it was not possible to record the age class and perceived gender of all visitors in the continuous visitor count, we cannot assess if the observed distribution of negative behaviour was different from the expected distribution.

https://doi.org/10.1371/journal.pone.0207246.t003

Presence versus absence of “do not feed” signs

A GLMM with feeding (yes/no) entered as the dependent variable and presence of sign (present/absent) entered as an explanatory factor revealed that the presence of a sign explained a significant amount of variation in feeding behaviour, with feeding being significantly more likely when a sign was absent (proportion of visitors feeding = 0.020) than present (0.009 X 2 (1) = 10.3, p = .001). In contrast, a second GLMM with trying to touch (yes/no) entered as the dependent variable and sign presence (present/absent) as the explanatory variable revealed visitors were significantly more likely to try and touch the meerkats when a ‘do not feed’ sign was present (proportion of visitors TTT = 0.042) than absent (0.026; X 2 (1) = 3.92, p = .047).

Sign design: Wording and imagery

A GLMM with feeding (yes/no) entered as the dependent variable and imagery (watching eyes/pawprints) and wording (personal/non-personal) entered as explanatory factors revealed that the design of the sign did not explain a significant amount of variation in feeding behaviour (X 2 (2) = 0.62, p = .732). Equally, a second GLMM revealed the sign wording and imagery did not explain a significant amount of variation in visitors trying to touch the meerkats (X 2 (2) = 0.49, p = .784).

Factors influencing attention to signs

A GLMM with attention to sign (attended/did not attend) entered as the dependent variable and imagery (watching eyes/pawprints), wording (personal/non-personal), visitor’s perceived gender (male/female) and visitor age (adult/child) entered as explanatory factors revealed that together these explanatory variables explained a significant amount of variation in visitor attention to the signs ( Table 4 ). When the contribution of individual explanatory variables to the model was considered, age was found to explain a significant amount of variation in visitor attention, with significantly more children (proportion of children attending = 0.068) attending to the sign than adults (0.033; Table 4 ; Fig 2 ). In contrast, sign imagery and wording ad and perceived gender of the visitors did not explain a significant amount of variation in visitor attention to the signs ( Table 4 ; Fig 2 ).

https://doi.org/10.1371/journal.pone.0207246.g002

https://doi.org/10.1371/journal.pone.0207246.t004

In line with our predictions, the presence of “do not feed” signs containing a pictogram and text were found to reduce feeding but our results suggest trying to touch the meerkats was significantly increased. This could be due to displacement activity from the reduction in the targeted behaviour of feeding. Although the proportion of visitors engaging in feeding was low (0.02), given the large numbers of visitors that visit the enclosure each day (mean = 506), this level of unauthorised feeding poses a considerable health risk to the meerkats in the form an increased chance of obesity or diabetes. Our results indicate that the application of signage can reduce the proportion of visitor who feed the meerkats by approximately half. Although the presence of signs did not entirely eradicate feeding (potentially due to individuals with pre-formed intentions who may possess less awareness of animal welfare and/or rules and regulations), signs were sufficiently effective to warrant future implementation in other enclosures and zoos with similar visitor behaviour problems. Future research would need to assess whether visitor habituation to such signs, if more widely used throughout an institution and for a longer time period, reduces the efficacy of signs and therefore whether strategies need to be implemented to tackle this (e.g. different designs used on different enclosures and renewal of sign design over time).

The failure to find any effect of sign wording on feeding the meerkats indicates that in combination with the pictogram, that both messages are equally effective. It is also possible, however, that due to the efficacy of signs in reducing the proportion of visitors engaging in this behaviour that there was insufficient variation in the data to find an effect hence a larger scale study may be useful. Future research could also investigate whether implementing signs with wording focused on the negative impacts to the visitors themselves (e.g. being bitten), might be more effective than the wording we used.

The failure of watching eyes to further reduce feeding events may also be due to insufficient variation in the data once signs were present. In contrast to previous research that found watching eyes reduced other negative behaviours that were not specified in the sign text [ 25 ], visitors did not inhibit attempts to touch the meerkats in the presence of watching eyes images. This could be because visitors don’t perceive this is as a negative behaviour, and therefore were not motivated to inhibit it in order to manage their reputation.

In order to change behaviour, signs need to first capture the visual attention of the audience. Whilst the length of text on the sign and the perceived gender of the visitor did not significantly predict attention to the sign, children were more likely to overtly attend to the sign than adults. Children often read signs aloud to their parents [ 33 ] and as our study used reading aloud as a measure of attention, this pattern of results is perhaps not surprising. Our finding is also in line with a previous study that found a higher percentage of children engaged with interpretation signs in a zoo exhibit than adults [ 34 ]. Whilst previous studies have argued that watching eyes increase prosocial behaviour through reputation management processes, rather than simply increased visual attention to the sign [ 25 , 35 ], few studies have measured if more participants pay attention to signs with eyes, which is the first necessary step towards adhering with the sign’s message. Our results indicate that visitors were not more likely to pay attention to signs with eyes compared to pawprints.

The implications of the current study are important for both visitors and meerkats as feeding and trying to touch poses health risks to both the meerkats and visitors [ 3 , 5 ]. Our results suggest “do not feed” signs are effective at reducing feeding but attempts to touch the meerkats were increased due to displacement activity. Although only very small proportions of visitors fed or tried to touch the meerkats, the high visitor numbers experienced by Flamingo Land [ 27 ] means that seemingly small reductions in the proportion of visitors could represent a high number of visitors whose behaviour would be changed. Based on the mean number of people visiting the enclosure each day during our study, the implementation of “do not feed” signs could prevent over 5 instances of feeding each day.

In conclusion, our study found “do not feed” signs selectively dereased the target behaviour, but increased other negative behaviours. Our findings also indicate that the content of signs should be designed to be accessible to a younger population and have important implications for the wellbeing of both zoo-visitors and zoo-animals. Overall, the current study strongly supports the use of “do not feed” signs in zoos to reduce unauthorised feeding.

Acknowledgments

Thank you to Flamingo Land for permission and support to conduct this research.

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What Is the Zoo Experience? How Zoos Impact a Visitor's Behaviors, Perceptions, and Conservation Efforts.

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• Godinez AM 1
• Fernandez EJ 2

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• Fernandez EJ | 0000-0001-5444-6604

Frontiers in Psychology , 30 Jul 2019 , 10: 1746 https://doi.org/10.3389/fpsyg.2019.01746   PMID: 31417469  PMCID: PMC6682629

Abstract 

Free full text , what is the zoo experience how zoos impact a visitor’s behaviors, perceptions, and conservation efforts, andrea m. godinez.

1 Museology Graduate Program, University of Washington, Seattle, WA, United States

Eduardo J. Fernandez

2 School of Behavior Analysis, Florida Institute of Technology, Melbourne, FL, United States

Modern zoos strive to educate visitors about zoo animals and their wild counterparts’ conservation needs while fostering appreciation for wildlife in general. This research review examines how zoos influence those who visit them. Much of the research to-date examines zoo visitors’ behaviors and perceptions in relation to specific exhibits, animals, and/or programs. In general, visitors have more positive perceptions and behaviors about zoos, their animals, and conservation initiatives the more they interact with animals, naturalistic exhibits, and zoo programming/staff. Furthermore, zoo visitors are receptive to conservation messaging and initiatives at zoos and are more likely to participate in on-site conservation opportunities as opposed to after their visits. The research also suggests that repeat visitors are even more inclined to seek out conservation efforts compared to those visiting zoos for the first time. While current research suggests that repeat visitors are more likely to engage in conservation efforts, little is known about causal factors related to such findings, and almost no research exists to-date comparing the conservation efforts of visitors vs. non-visitors. This latter comparison will likely play a greater role in future zoo visitor research, since it poses one of the most important metrics for evaluating the specific effects visiting a zoo can have on people engaging in conservation efforts in general.

• Introduction

Modern zoos have a variety of functions both relative to the species exhibited and the conservation of wildlife in general. According to the Association of Zoos and Aquariums (AZA), some of these goals are: (1) the care and welfare of the animals they exhibit; (2) educating and engaging public, professional, and government audiences; (3) species/habitat conservation; and (4) internal and academic research that increases our knowledge of animals and promotes AZA’s other goals ( Reade and Waran, 1996 ; Fernandez et al., 2009 ; Association of Zoos and Aquariums, 2013 ). In addition, zoos have a legacy of being a form of entertainment and are primarily a destination for visitors to attend in their leisure time ( Carr and Cohen, 2011 ). Approximately 700 million people visit zoos and aquariums worldwide annually ( Moss et al., 2014 ), with a 2011 survey indicating that participating zoos and aquariums spent at least $350 million on wildlife conservation internationally ( Gusset and Dick, 2011 ). In a 2012 report by the AZA, 2,700 conservation programs spent approximately $160 million on field conservation for 650 individual species, in addition to ecosystems ( Association of Zoos and Aquariums, 2012 ). It is these high attendance levels and their associated income that gives accredited zoos the ability to fulfill their mission statements.

While zoos are expanding their missions and welcome a large number of visitors, these institutions also have their critics. Animal rights activists and others argue that many zoos contribute little to conservation efforts and also impair zoo animals’ welfare by placing them in captive environments ( Hancocks, 2001 ; Rose et al., 2009 ; O’Connor, 2010 ). It is crucial to measure the impact of zoos’ education and conservation initiatives to both indicate the extent of how these organizations are fulfilling their missions and continue to demonstrate the importance of the role of zoos in society despite their critics.

Ultimately, whether an opponent or a supporter of zoological institutions, it is critical to ask: How effective are zoological environments for meeting the welfare, conservation, education, and research goals of accredited zoos? More specifically, what can we learn about how particular captive environments help or hinder these goals? And what can visitors tell us about our ability to successfully meet these goals?

The following paper is a literature review of many peer-reviewed studies that examine how the zoo environment impacts visitors, as well as how these visits impact conservation efforts, both within and outside the zoo. We accomplish this by looking across a variety of disciplines and bodies of work that examine zoological institutions and visitor studies including psychology, museology, animal welfare, and environmental education. Keyword searches of “zoo visitor behaviors,” “zoo visitor perceptions,” “zoo visitor conservation,” “zoo visitor learning,” “animal-visitor interactions,” and other terms occurred in the University of Washington Library’s search engine, in Google Scholar, and in search engines of major publications across these fields. We specifically looked for articles where different factors of the zoo environment (the animals themselves exhibit design, programming/interacting with staff) affected visitor behaviors and perceptions. Articles that examined conservation awareness, attitudes, and behaviors with zoo visitors were also prioritized. In addition, reviewing references cited in relevant articles aided in compiling the studies cited in this literature review. Articles that did not look at visitor learning, post-visit outcomes, or observable zoo visitor behaviors were deemed irrelevant. Specifically, we examine (1) what visitors learn from their zoo experience, with an emphasis on how their behaviors and perceptions are changed and (2) how such visits change those visitors, specifically their conservation efforts. Specifically, we examine how visit frequency affects conservation actions and the need for more research on comparisons between visitors and non-visitors in terms of overall conservation support.

What Do Visitors Learn at the Zoo?

Zoos are by design an informal learning environment; unless visiting as part of a formal programmatic experience like a school tour, visitors are coming to zoos during their free time and choose which aspects of the zoo they engage with. Visitors to zoos come in with particular motivations like entertainment, bonding time with their families and friends, and also educational experiences ( Falk, 2005 ; Roe and McConney, 2015 ). For learning to occur, attention is an important pre-cursor for learning ( Altman, 1998 ), as well as connecting with visitors based on their prior knowledge ( Dove and Byrne, 2014 ) and providing entertaining or enjoyable experiences ( Spooner et al., 2019 ).

In order to establish the effectiveness of zoos as a learning environment, it is important to look at a variety of factors that influence visitor learning. Several studies have examined observable behaviors, as well as verbal responses from zoo visitors. These studies have looked at a variety of factors, including the social makeup of visitor groups, educational programming, and the animals in exhibits.

It is also important to understand how visitors cultivate perceptions and attitudes, in addition to studying their behavior, in order to evaluate the effectiveness of a zoo’s education, conservation, and recreation goals ( Anderson et al., 2003 ). Clayton et al. (2009) support the point that educational goals can be improved via perceptions. Specifically, positive perceptions can lead to a visitor who is interested in learning more about animals.

Effects of the Zoo Environment on Visitor Behaviors

One way to examine a visitor’s response to a zoo exhibit is by measuring observable behaviors displayed by visitors. Specifically, (1) time spent in front of or near an exhibit; (2) attention toward an exhibit (e.g., facing and/or talking about an exhibit); and (3) overall crowd size has been used as measures of interest and satisfaction ( Anderson et al., 2003 ; Margulis et al., 2003 ; Fernandez et al., 2009 ; Godinez et al., 2013 ). Attention is an important measure for visitor studies for which attention can suggest what information visitors are potentially processing and is a precursor to learning ( Altman, 1998 ).

Previous studies suggest that visitor behaviors are influenced by both the presence of a zoo animal and the behaviors it displays. These studies have analyzed and tested the “visitor attraction model”; the theory that active animals attract visitors and have used observable measures such as pointing, stopping, and length of time is facing the exhibit. Results suggest visitors attend more to animal behaviors the more visible and active the animal is and also tend to spend more time in exhibits when an animal is visible and active ( Bitgood et al., 1988 ; Altman, 1998 ; Anderson et al., 2003 ; Sellinger and Ha, 2005 ; Davey, 2006a ; Godinez et al., 2013 ).

Debate over visibility of an animal and its influence on visitor behavior has risen from previous research. Bitgood et al. (1988) found that zoo visitors stopped more often and spent more time at exhibits where the animal was more visible. Whereas Philpot’s (1996) study (as cited in Davey, 2006a , pp. 94–95) found that visitors spent more time searching for animals in naturalistic enclosures, which turned the exhibit and observing animal behaviors into an interactive experience.

In addition to the debate, over animal visibility is the size of the animal. Some studies suggest that visitors prefer larger-bodied animals ( Bitgood et al., 1988 ; Ward et al., 1998 ). These findings have the potential to influence zoo decisions on the types of animals they display, even considering larger species typically cost more to care for and exhibit. However, Balmford (2000) re-analyzed the results of the Ward et al.’s (1998) study at the Zurich Zoo, which suggested that zoo visitors preferred viewing larger-sized animals. After re-analyzing the data along with additional data collected from the London Zoo, Balmford argued that in terms of visitor length of time at exhibits, there was no discernible difference between time spent at large-bodied animal exhibits and small-bodied animals. Balmford cautions that measures of visitor attention such as time spent attending to an exhibit and crowd size are not necessarily indicators of popularity or preference; smaller animals are typically housed in smaller exhibits, which may make the exhibit itself less appealing, as well as making it difficult for larger visitor groups to form.

Visitor conversations have also been studied in order to examine the influence of animal presence on visitor attention. Altman (1998) analyzed zoo visitor conversations at three bear exhibits as an indirect measure of attention. Conversations were recorded and later categorized as one of four types: (1) animal-directed; (2) human-focused; (3) animal behavior (directed); and (4) other. The study found that animal activity levels appeared to influence visitor conversations, particularly highly animated behaviors. Animal behavior conversation increased and human-related conversation decreased when animals were “highly animated” and the opposite occurred when the animals were pacing or not visible.

Studies examining the impacts of exhibit designs suggest that the transition to naturalistic exhibits in recent decades improves the animal’s well-being as well as visitor behaviors ( Nakamichi, 2007 ; Fernandez et al., 2009 ). Although the majority of zoo visitors do not interact with signage ( Clayton et al., 2009 ), the context in which an animal is displayed can convey a wealth of information, increase visitor interest, and potentially create a more enjoyable experience. Research also suggests that naturalistic exhibits can increase visitor length of time at an exhibit ( Shettel-Neuber, 1988 ; Davey, 2006a , b ). These stay times are constant, even without the presence of an animal ( Davey, 2006a ; Nakamichi, 2007 ).

Effects of the Zoo Environment on Visitor Perceptions

While interacting with the zoo environment, visitors form perceptions of their surroundings. Previous research argues that zoos can encourage empathy in visitors for the care of zoo animals and, in turn, their wild counterparts and the ecosystems where these animals live. The catalyst for this empathy is positive experiences with animals in zoo environments ( Clayton et al., 2009 ; Kutska, 2009 ).

Previous studies examining visitor perceptions suggest that perceptions can be influenced and changed by their experiences at zoos. Factors that influence visitor perception can include exposure to and interactions with zoo animals, the exhibit’s design, and elements found within the exhibit space (e.g., signage, enrichment items, and feeding stations), public programming around the exhibit, the ability of visitors to interact with volunteers and staff, and preconceived notions of what certain behaviors (e.g., pacing and other potential stereotypic activity) suggest about the overall welfare of that animal. These aspects have the potential to equally foster or hinder respect and appreciation for zoo animals and the institutions that care for them.

Reade and Waran (1996) conducted a study of how zoo visitors and non-zoo visitors perceived zoo animals in general. The results of this study provided baseline data when examining visitor perceptions across many aspects of zoo operations. The study found that there were significant differences between non-visitors and zoo visitors’ perceptions of animals in zoos. Zoo visitors viewed zoo animals more positively in all questions in the study and thought of them as more attractive, happy, and well-kept. Non-visitors tended to have more negative views of zoo animals across all questions and were significantly more likely to perceive zoo animals as “bored.” In addition, non-visitors also viewed enrichment as less important than zoo visitors. The authors therefore concluded that this difference in perception suggests that the general public is not fully aware of the physical and psychological benefits enrichment has for zoo animals.

Exhibit design also appears to influence visitor perceptions. Zoos have undergone a substantial transformation over the past few decades in exhibit design, with a greater emphasis on naturalistic exhibits, both in terms of their appearance and functionality for the exhibited animals (e.g., ability to hunt and forage). Much of the support for displaying zoo animals in natural contexts is based on behavioral science and theory. In an article about achieving optimal visitor experiences in zoos, Coe (1985) argued that designs, or contexts, of zoo exhibits can reach visitors on both conscious and unconscious levels. These carefully planned contexts can grab the visitor’s attention, and strong multi-sensory exhibit environments have the potential to create strong behavioral responses, such as greater empathy and desire to conserve the exhibited species. This transition to naturalistic exhibits improves visitor perceptions and encourages appreciation and respect for zoo animals ( Maple, 1983 ; Finlay et al., 1988 ; Reade and Waran, 1996 ; Nakamichi, 2007 ).

Visitor perceptions can also be influenced by animal, keeper, and overall exhibit interactions they have while visiting a zoo. When analyzing how visitor perceptions were influenced by small-clawed otter activities, Anderson et al. (2003) found that public animal training and public animal training with interpretation produced more positive zoo experiences and perceptions of exhibit size than passive exhibit viewing or interpretation-only sessions. The educational approach to animal training programming has also been found to be an important factor in influencing visitor learning. A study by Visscher et al. (2009) found that after being told the same facts about Black Rhinoceros during two different types of animal training programs, the school group who received the interpretive presentation (i.e., audience encouraged to ask questions and could touch training tools) answered more post-program questions correctly than the students who attended a less interactive, fact-based presentation. In addition, a study by Lindemann-Matthies and Kamer (2005) found that visitors who attended a staffed “touch table” at a Bearded Vulture exhibit at the Goldau Nature Park and Zoo were more likely to know more about the biology, ecology, and conservation of vultures both immediately after their visit and 2 months post-visit than those who visited the exhibit but only had access to exhibit signage. In addition, educational zoo theater programming performed by staff with no animals present resulted in both children and adult visitors answering more survey questions correctly after attending the performance than answering the same questions before the theater program began ( Spooner et al., 2019 ).

How visitors perceive their experience, as well as the overall welfare of exhibited animals, can be greatly influenced by what behaviors they see the animals engaged in. Captive animal behavior is often broadly defined as positive, healthy behaviors (e.g., searching, foraging, and non-repetitive activity), and negative, “abnormal” behaviors (e.g., hiding, inactivity, and repetitive behaviors, such as pacing). While an operational classification and functional understanding of these behaviors goes beyond the scope of this paper, how such behaviors affect the visitor experience is critical to an overall understanding of what visitors learn at the zoo.

Bexell et al. (2007) examined visitor perceptions of Giant Pandas while playing or not playing. Those who witnessed Giant Panda play were significantly more likely to rate their experience more positively and have a more satisfying experience than those who did not observe playing. As noted previously, Altman (1998) found visitor conversations changed based on bear behaviors, with animal behavior conversations occurring the most when the bears were active compared to pacing and out of sight.

Another factor that influences visitor perceptions of animal behavior is stereotypic activity, broadly defined as repetitive, invariant behavior patterns with no obvious goal or function ( Ödberg, 1978 ; Mason, 1991 ). In a study by Godinez et al. (2013) , the researchers examined how different jaguar behavioral categories correlated with visitor activity and their ratings of the animals’ predominant behavior displayed, well-being, exhibit quality, and the visitor’s enjoyment. Overall, visitors were able to accurately describe a jaguar’s behavior as inactive, active, or out of sight. However, approximately half of all visitors questioned (~47%) defined pacing and other repetitive behaviors as stereotypic, while the other visitors questioned simply described those behaviors as active and non-repetitive. For visitors who described a pacing pattern or other repetitive behaviors as stereotypic, they were also significantly more likely to rate the jaguar’s well-being, exhibit quality, and visitor enjoyment lower than those who described the behavior as non-repetitive, active behavior. Therefore, it appears that acknowledgement of a behavior as a stereotypy can negatively impact multiple perceptions of a zoo visitor’s visit. Similarly, Miller (2013) found that participants rated the overall care of a tiger as lower when the animal engaged in pacing than inactivity. In addition, the participants who observed a tiger pacing were significantly less likely to support zoos after witnessing this behavior when compared to those who observed an inactive tiger. Furthermore, visitors reported have the most positive emotions regarding zoo animals they observed after experiencing up-close animal encounters with animals displaying active behaviors compared to when the animals were out of sight or engaged in other behaviors ( Luebke et al., 2016 ).

While zoos have made significant strides in reducing stereotypic activity displayed by their animals, these studies suggest that public education about such efforts is also necessary. It may be that part of the bias against such stereotypic activity on the part of the observing visitor is due to a lack of knowing what zoos and similar facilities do to deter such activity. Future studies could examine how educating visitors about behavioral enrichment and other welfare-oriented procedures affects their views of exhibited animals, in terms of both how they view the displays of potentially adverse behaviors and how they view the ability of zoos to care for animals.

Zoo Visitors Conservation Behaviors

Recent studies have focused on quantifying the effect of zoo visitation on the conservation efforts of those visitors. Most studies to-date have examined a visitor’s conservation knowledge related to a specific exhibit or program before and after interacting with those programs ( Hayward and Rothenberg, 2004 ; Lindemann-Matthies and Kamer, 2005 ; Lukas and Ross, 2005 ; Bexell et al., 2007 ; Chalmin-Pui and Perkins, 2017 ), as opposed to greater conservation awareness or analyzing a variety of exhibits and programs ( Reade and Waran, 1996 ; Yalowitz, 2004 ; Falk et al., 2007 ; Adelman et al., 2010 ; Moss et al., 2017a , b ). Research is emerging to suggest that visitors can have a relatively extensive awareness of human impacts on biodiversity conservation, even when they hold misconceptions regarding concepts about biodiversity and ecosystems ( Dove and Byrne, 2014 ).

When analyzing how zoo visitors respond to conservation efforts within zoos, several studies suggest that one of the most significant factors influencing zoo visitors’ conservation knowledge, attitude, and behaviors is repeat visitation. Repeat visitors retain significantly more conservation information, have more positive attitudes about conservation, and conduct more conservation-related behaviors than visitors who are attending the same zoo for the first time ( Yalowitz, 2004 ; Lukas and Ross, 2005 ; Miller et al., 2013 ; Clayton et al., 2017 ; Moss et al., 2017a ). Thus, while we have some knowledge about how repeat visitors differ from first-time visitors, the extent to which this occurs is not known.

In order to evaluate the overall impact zoos may have on increasing visitor interest and activity in conservation efforts, we examine (1) the conservation perceptions, behaviors, and actions taken by the visitor during a given visit; (2) what type of conservation behaviors and perceptions visitors have after their visit; and (3) how do all of these conservation-related efforts differ in zoo visitors compared to those who do not attend zoos.

Visitor Conservation Opportunities at the Zoo

In situ opportunities for conservation activities provide visitors with a tangible way to contribute to conservation efforts, especially since previous work suggests that visitors are uncertain how to become involved beyond donating money ( Ojalammi and Nygren, 2018 ). On-site conservation activities may also reaffirm conservation behaviors and encourage long-term changes in zoo visitors. When comparing visitors’ conservation actions on-site versus off-site, Stoinski et al. (2002) found that visitors were 20 times more likely to do on-site conservation activities than after their visit to the zoo. Furthermore, facilitating conservation actions via staff and programs as opposed to passive visits may increase the potential for visitors to participate in conservation efforts during a visit. In a study conducted during an elephant program at Zoo Atlanta, 350 of 471 visitors studied signed petitions and took solicitation cards. Those who had the highest levels of interaction with the exhibit and elephant program were significantly more likely to return the solicitation cards than those who had lower interaction ( Swanagan, 2000 ).

Another way to encourage in situ conservation behaviors is by offering sustainably made items in zoo gift shops, where proceeds go to support conservation efforts (see Sigsgaard, 2009 , for a case study of one such effort, and the sustainability issues to consider when stocking souvenirs and other goods in zoo gift shops). An additional on-site conservation action is at the point of admission through the “Quarters for Conservation” program. In this program, the zoo adds 50 cents onto the price of admission and gives their visitors a chance to choose which conservation project they would like their quarter to support. This simple program can help frame the visitor’s entire zoo experience and has been implemented in over a dozen US zoos since the program was founded in 2007 ( Hance, 2015 ).

If zoos continue to strive to demonstrate their effectiveness as conservation organizations, then it is crucial that zoos provide on-site opportunities for their visitors to participate in conservation. In situ conservation actions allow zoos to fulfill their missions and demonstrate their impact now. This can also be of great importance when justifying the role of zoos as conservation contributors when critics and others question the effect of zoos on various conservation efforts.

Zoo Visitor Conservation Post-visit

When analyzing conservation knowledge retention, some studies have found that visitors’ conservation knowledge and interest persisted after a zoo visit ( Jensen, 2014 ; Moss et al., 2015 ), but this new understanding rarely results in new conservation actions ( Adelman et al., 2010 ; Miller et al., 2013 ). However, other studies suggest zoos prompt visitors to rethink their roles in conservation issues after their visit ( Falk et al., 2007 ; Clayton et al., 2017 ; Jensen et al., 2017 ). While this is an emerging area of research interest, several studies support that the level and type of engagement with conservation and animals during the zoo experience affect not only visitors’ knowledge retention but also post-visit behavior. Visitors who engaged with films and signage about biodiversity and conservation scored higher on biodiversity knowledge and intent to take part in post-visit conservation actions than those who did not interact with these elements ( Moss et al., 2017b ). Similarly, a study by Hacker and Miller (2016) indicated up-close encounters with elephants and witnessing active behaviors from the animals had positive effects on visitors’ intent to engage with conservation actions post-visit. In a multi-institutional study of dolphin programs in zoos and aquariums by Miller et al. (2013) , participants who witnessed dolphin programs retained much of their conservation knowledge learned from the shows and reported doing more conservation-related behaviors 3 months after witnessing the show than 3 months prior to their visit. Another study examining the effectiveness of touch tables on visitor’s knowledge of bearded vulture biology, ecology, and conservation issues found that visitors who used the touch tables knew more about these items both immediately after their visit and 2-month post-visit than visitors who had not attended the table ( Lindemann-Matthies and Kamer, 2005 ).

In a 2014 study by Jensen analyzing the conservation concerns and conservation self-efficacy of school children both pre- and post-visit, Jensen found an increase in students’ personal concerns about the extinction of species, but marginal differences in if the students felt they could do something about it. Furthermore, a study by Skibins and Powell (2013) suggests that visitors are more inclined to take conservation action for an individual species they connect with, as opposed to conservation of biodiversity on a larger scale. To combat this issue of awareness but lack of action (or widening the impact of said action), others who recommend zoos can take on stronger approaches to motivating visitors to do pro-conservation behaviors that are relevant and easy to implement for a diverse range of zoo visitors ( Smith et al., 2012 ; Grajal et al., 2018 ). However, providing materials for visitors to participate in post-visit conservation actions has occurred in only a few studies. Analysis that has been conducted to-date suggests that materials that coincide with visitors’ daily lives tend to be more effective in encouraging conservation-related behaviors than those that are less frequent and more in-depth actions. For example, at the Monterey Bay Aquarium, 51% of visitors who picked up a Seafood Watch Pocket Guide tried to use the guide when purchasing seafood after their visit to the aquarium. On the other hand, only 10% of visitors tried to use an “Ocean Allies Card” (a list of conservation organizations to join) after their visit, and no participants joined an organization ( Yalowitz, 2004 ).

Zoo Visitors Versus Non-visitor Conservation Actions

To understand fully the degree of impact zoos has on visitors’ conservation efforts, comparisons between zoo visitors and non-zoo visitors are necessary. However, most studies look at zoo visitors alone ( Swanagan, 2000 ; Yalowitz, 2004 ; Falk et al., 2007 ; Miller et al., 2013 ). At least one study to-date indicated that non-zoo visitors viewed zoos as playing an important role in conservation, although non-zoo visitors’ conservation knowledge and attitude were not measured ( Reade and Waran, 1996 ). Because of the importance of comparing differences between zoo visitors and non-zoo visitors to determine the impact zoos have on increasing conservation efforts in general, our final section draws on directions zoos could go in to make such assessments.

• Future Research

Much of the studies done to-date examine changes in visitor behaviors and their perceptions in regard to exhibit design, the presence of animals and their displayed behaviors, and how visitors engage with singular exhibits and/or programs in individual zoos (see “Zoos and Visitors” section of this paper for examples of these studies). This work has laid the foundation for a variety of in-depth questions to be examined moving forward. Specifically, the nuances of how the zoo environment may influence zoo visitors’ appreciation for the animals exhibited, their species’ associated conservation needs, and how the zoo visitors themselves can take conservation actions to support conservation initiatives for the animals’ wild counterparts and their habitats.

As studies continue to examine the conservation impacts zoos have on their visitors, much of the research done to-date can be summarized in an assumed paradigm that zoo visitors go through that are a series of sequential steps with the intended outcome to be conservation-related actions.

Visit → Knowledge → Concern → Intent → Post-visit action

However, this paradigm assumes that knowledge is strongly linked to conservation actions. Recent research indicates that other factors like where you live and demographically related factors are more strongly correlated with conservation behaviors than knowledge ( Moss et al., 2017a ). Based on what studies cited in this literature review indicate, the paradigm could be reframed as follows:

Visit with in situ action → Knowledge → Concern → Intent → Post-visit action

Given the variety of factors influencing visitors in the free-choice learning environment of zoos and the variety of methodologies used to examine the impact zoos have on their visitors, there is a question beckoned to be asked: Is it possible to empirically measure the impact zoos have on their visitors? Many studies mentioned in this review have taken great strides in answering this question—especially when examining how the environment of the zoo (e.g. exhibits and programs) affects behavioral learning and general knowledge of both animal species and the individual animals housed.

Our recommendations are to continue measuring the impact—or to begin measuring the impact—of the following:

having a true control group (non-visitors) to understand the full impact zoos may or may not have on zoo visitor knowledge, perceptions, and behaviors;

increasing opportunities for on-site conservation activities that visitors can do during their visit; this could potentially improve their conservation knowledge and future conservation actions, as well as be a measurable impact of how zoos are contributing to conservation efforts;

providing more opportunities for tangible takeaways for visitors that directly contribute to conservation initiatives post-visit (i.e., Seafood Watch cards, pre-drafted letters to send to legislators, take-home electronic recycling kits) – and then measure the effectiveness of these tools; and

studying the phenomena of repeat visitors being more conservation-oriented than one-time visitors. Also begin to study how repeat zoo visitors compare to those who do not visit zoos at all.

On this last point, knowing that research to-date suggests that repeat visitation is a significant factor in conservation knowledge and appreciation for wildlife, we wonder: are repeat visitors continuing to visit zoos because they are already conservation-oriented and see zoological institutions as places to fulfill this area of interest? Or do they become more concerned with conservation issues over time as a result of the information and experiences they have in zoos? Additional studies that delve deeper into motivations of repeat visitors, and how these attitudes and behaviors develop, could shed light on these questions. Regardless of their motivation, these studies suggest that zoos are fostering conservation with this key group of visitors and that those who come to zoos appear to be receptive to and interested in conservation in the first place ( Falk et al., 2007 ).

Zoo membership is a key tool that is readily available to all zoological institutions to help foster the transition from infrequent to frequent visitors. Looking at the motivation, visitors have when signing up for zoo memberships (cost saving, entertainment, interest in animals, interest in conservation, etc.,), and comparing these motivations to conservation-related knowledge, attitudes, and behaviors of members could provide a critical insight into the field.

Although we have described an array of studies for this review, most of them do not address an important aspect to the effectiveness of zoos—how visitors compare to those who do not attend these types of institutions. With the exception of the few studies mentioned earlier in this paper, we have not been able to find peer-reviewed, published research that compares zoo visitors to non-visitors. A plethora of topics, including conservation attitudes, knowledge of wildlife, and other environmental resources, or how these two groups perceive zoos themselves beckons further examination. We suspect that future visitor research will focus more directly on comparisons between zoo visitor and non-visitor conservation efforts, since this is one of the most important metrics for assessing the impact zoos have on increasing the conservations efforts of their visitors, and a necessary measure for evaluating the effect zoos have on the public supporting conservation efforts in general.

• Author Contributions

AG and EF co-wrote and edited the manuscript, as well as researched literature for this review. AG formatted the manuscript in accordance with Frontiers in Psychology guidelines. EF submitted the manuscript for publication.

Conflict of Interest Statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

• Acknowledgments

We thank Kathryn Owen of Kathryn Owen Consulting for her recommendations on potential sources for this manuscript.

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AIP (Advanced Inquiry Program) graduate student Ezekiel Miller of Cleveland, Ohio, was published in the journal of Social Work in Mental Health . His article is titled "Connecting people to conservation agencies through social media posts: an examination of the power of marketing that zoos maintain."

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As a student in Miami's biology department, Miller is earning a Master of Arts (M.A.) in Biology through Project Dragonfly's AIP while working as a substitute teacher for the Cleveland School District.

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Dilemmas for Natural Living Concepts of Zoo Animal Welfare

Simple summary.

This ethical discourse specifically deals with dilemmas encountered within zoological institutions, namely for the concept of natural living , and a new term— wilding . Wilding refers to extrapolation of the natural living concept to treating an animal as wild, residing in a wild habitat . The problems associated with wilding are detailed. Complexities of natural living versus natural aesthetics as judged by humans, as well as the possibility of innate preference for naturalness within animals are examined. It is argued that unintended and unavoidable genetic and epigenetic drift favouring adaptations for life in a captive environment may still occur, despite zoos best efforts to prevent this from occurring. This article further discusses the blurred lines between natural and unnatural behaviours, and the overlaps with more important highly-motivated behaviours , which may be better predictors of positive affective states in captive animals, and thus, better predictors of positive well-being and welfare. Finally, as we are now in the Anthropocene era, it is suggested that human-animal interactions could actually be considered natural in a way, and notwithstanding, be very important to animals that initiate these interactions, especially for “a life worth living”.

This ethical discourse specifically deals with dilemmas encountered within zoological institutions, namely for the concept of natural living , and a new term— wilding . It is agreed by some that zoos are not ethically wrong in principle , but there are currently some contradictions and ethical concerns for zoos in practice . Natural living is a complicated concept, facing multiple criticisms. Not all natural behaviours, nor natural environments, are to the benefit of animals in a captive setting, and practical application of the natural living concept has flaws. Expression of natural behaviours does not necessarily indicate positive well-being of an animal. Herein it is suggested that highly-motivated behaviours may be a better term to properly explain behaviours of more significance to captive animals. Wilding refers to extrapolation of the natural living concept to treating an animal as wild, residing in a wild habitat . This definition is intrinsically problematic, as quite literally by definition, captivity is not a wild nor natural environment. Treating a captive animal exactly the same as a wild counterpart is practically impossible for many species in a few ways. This article discusses complexities of natural living versus natural aesthetics as judged by humans, as well as the possibility of innate preference for naturalness within animals. Zoos nobly strive to keep wild animals as natural and undomesticated as possible. Here it is argued that unintended and unavoidable genetic and epigenetic drift favouring adaptations for life in a captive environment may still occur, despite our best efforts to prevent this from occurring. This article further discusses the blurred lines between natural and unnatural behaviours, and the overlaps with more important highly-motivated behaviours , which may be better predictors of positive affective states in captive animals, and thus, better predictors of positive well-being and welfare. Finally, as we are now in the Anthropocene era, it is suggested that human-animal interactions could actually be considered natural in a way, and notwithstanding, be very important to animals that initiate these interactions, especially for “a life worth living”.

1. Introduction

To preface this article, I would acknowledge and address the implicit assumptions about animal welfare science and philosophy that have brought us to the ethical position herein. I would refer the readers to other published articles which explore the history of animal welfare and ethics in much depth, as these are used as a basis for our understanding and arguments [ 1 , 2 , 3 , 4 , 5 , 6 , 7 , 8 , 9 , 10 ]. This article specifically deals with competing ideals of optimal animal welfare within zoological institutions, namely concepts of natural living , and a new term— wilding . This discourse does not necessarily apply to other captive animal industries such as farms or laboratories.

As other ethicists have written, I agree that zoos are not ethically wrong in principle , but there are currently some contradictions and ethical concerns for zoos in practice [ 5 ]. It should be understood that I am a supporter of zoological institutions and their betterment, although I may disagree with some zoo practices, and between myself and other researchers in ethical views of the specific dilemmas herein. It is also acknowledged that zoos are not going away any time soon (see [ 5 ]), so it is the pragmatic duty of researchers and philosophers to work with zoos constructively. I would also like to acknowledge the positions of other researchers in the field, such as Weary and Robbins [ 9 ], and Yeates [ 10 ]. This article is not intended as a refutation of these other recent articles about natural living and holistic welfare, but rather to present an alternate conception of one part of overall animal welfare that may have been misconstrued in certain zoo environments, leading to in practice incongruence and dilemmas. I acknowledge that my arguments are formulated from my moral and ethical position that humans have an obligation for special protection of captive animals , especially zoo animals, and I subscribe to many (but not all) elements of compassionate conservation ethical theory of contemporary philosophers such as Bekoff [ 11 ] and Gray [ 12 ] over purely utilitarian or consequentialist approaches. At the moment compassionate conservation remains very anti-zoo in its position, however, as Gray [ 12 ] posits, there is much merit in using this ethic to work with zoos constructively, to enhance zoos’ ethics and practices.

I acknowledge the currently accepted academic focus on the three conceptual frameworks (orientations) of animal welfare: biological functioning, affective states, and natural living [ 2 , 13 ]. This is how the science of animal welfare is commonly taught to undergraduate and postgraduate learners in our discipline. It is acknowledged, however, that this not the only way to conceptualise the entire picture of captive animal welfare [ 3 , 9 ], and that these three conceptual frameworks do not encompass all relevant information in all situations. I acknowledge that a predominant model for characterising and assessing good welfare, especially within zoos, is the Five Domains Model of Mellor and Reid [ 14 ] and Mellor and Beausoleil [ 15 ]. Whilst incorporating pluralistic scientific elements of welfare, at its core the Five Domains Model assumes a hedonistic priority of animal welfare, that is, what the animal feels about its life and environment is the most important factor in holistic welfare. In this article a pluralistic basis of welfare is acknowledged, though for the sake of argument a hedonistic basis is prioritised. It is understood, however, that a hedonistic priority also misses some of the whole picture [ 3 ]; hedonism-based welfare conceptions are not dogma. The two scientific concepts of biological functioning and affective states will only be touched on in this article, as my primary focus is to shine a light on how the concept of natural living may have been pushed past its useful bounds in zoo situations.

It should be stated that whilst hedonistic conceptions of welfare are mostly concerned with “how the lives of sentient animals are going, for the sake of, and from the perspective of, the animals themselves” [ 6 ], it is strongly suggested here that (as written by Weary and Robbins [ 9 ]) relationships matter . That is, not only are the self-derived internal states of the individual highly important, but also those emotion-inducing relationships that are important to the individual—such as relationships to conspecifics, other animals, and humans including carers and visitors— and some relationships that others have with that individual may also be important to welfare outcomes (for example, the specific values and attitudes a person holds will affect their relationship with an individual animal, and reinforcers to this relationship create a bi-directional, perpetual feedback loop). These relationships may then be reflected by the internal affective states of both (or all) agents in that interaction [ 16 , 17 ]. This has been characterised by the general Hemsworth-Coleman model of human-animal interactions [ 18 , 19 ]. The general model has been specifically adapted for zoo visitor-animal relationships [ 20 ], pictured below ( Figure 1 ). A very similar model has been proposed for zookeeper-animal interactions as well [ 20 ]. Human values and attitudes towards animals, and the relationships formed between them, can strongly influence subjective (hedonistic) experiences of welfare.

Proposed visitor-animal interaction model (adapted from Hemsworth-Coleman model (2011) by S. Chiew and L. Hemsworth, pers. comms. , 2016) [ 20 ].

2. Natural Living

Natural living is a (sometimes) useful key concept in the assessment of animal welfare, often defined as “providing opportunities for animals to engage in natural, species-specific behaviours” [ 1 , 2 , 10 ]. As a concept, it suggests that animals’ well-being may be considerably improved if they are able to perform species-specific behaviours from their natural repertoire , especially innate behaviours. In practice, this has often been achieved by removing restrictions to these behaviours (whether they are physical or environmental restrictions) and by providing appropriate objects, resources or enclosures with/in which to perform the behaviour(s). Often, definitions of the concept also include phrases about housing animals in natural environments . However, not all natural behaviours, nor natural environments, are to the benefit of animals in a captive setting, and practical application of the concept has many flaws. A main criticism of the use of natural living has been that “the concept of natural is usually too poorly defined to provide a sound basis for animal welfare assessment, and thus when applied uncritically it may lead to poorer welfare instead of an improvement” [ 21 ]. This criticism has been expressed quite commonly in the past few decades [ 1 , 2 , 10 , 19 , 22 ].

Articulation of the concept, and its transposition to practical application in many captive settings have somewhat missed the point entirely. Natural behaviour , natural living and naturalness are poorly-defined key terms that are too often conflated with other concepts and measures of an animal’s overall well-being, such as feelings (affective state) or function (biological functioning) [ 10 ]. Expression of natural behaviours does not necessarily indicate positive well-being of an animal; likewise absence of some natural behaviours does not necessarily indicate suffering [ 23 , 24 ]. Nor should the term natural behaviour be used when actually referring to other conceptual types of behaviours, such as highly-motivated behaviours , which may be natural or unnatural, however there is often significant overlap between these two terms. Herein I will suggest that highly-motivated behaviours may be a better term to properly explain behaviours of more significance to captive animals, and discuss where boundaries between harmless and harmful highly-motivated behaviours may lie (as we still have an ethical obligation to protect animals from harming themselves, whether intentionally or accidentally, in captivity).

3. Wilding: The Natural Living Dilemma

Natural living has been a useful tool for improving welfare, but its practical application, especially within zoos, has been extended beyond its theoretical usefulness, and in many instances has been misinterpreted as what I will herein refer to as wilding . Wilding is a new term created to refer to extrapolation of the natural living concept to treating an animal as wild, residing in a wild habitat . Wild here refers to “living or growing in the natural environment; not domesticated or cultivated” [ 25 ]. From a decade of first-hand experience within the zoo industry, this wilding conception of natural living has been encountered often enough to be considered pervasive amongst many zoo personnel’s implicit beliefs and taught knowledge about how zoos should approach animal welfare, though actual prevalence rates have not been systematically investigated. Indeed, many welfare assessment and monitoring tools deployed by zoos focus somewhat on natural environments and natural behaviours [ 26 ]. This wilding conception is intrinsically problematic for any captive animal industry (especially zoos) as, quite literally by definition, captivity is not a wild nor natural environment [ 27 ]. To place a wild animal in an artificial environment (no matter how accurate a recreation of a natural setting) and still presume to treat it exactly the same as a wild counterpart is practically impossible for many animal species, in a few obvious ways.

Firstly, truly wild animals in nature are not treated by humans in a particular way—they are not under the direct care of humans, however, they may yet be influenced by humans [ 28 ]. These wild animals may be exposed to humans in multiple situations, and even have interactions with humans, but their lives are not solely dictated by humans as captors/guardians. This does not preclude the possibility of interactions (both positive and negative) or conflicts arising between humans and animals, animals venturing into “human spaces”, or encroachment of humans into an animal’s native space [ 28 ]. However, as soon as an animal is placed in captivity, no matter how wild its behaviours or instincts, its care (and indeed its survival) is then determined and controlled by those humans that placed it there. A person cannot place an animal in a captive environment then refrain from providing basic cares or resources (such as food, water and shelter), and yet expect the animal to survive, let alone to thrive. Even in a highly accurate recreation of a natural environment, those basic resources must still be provided by the controlling humans—that is, the environment has been created and curated to provide those resources for the animal, through natural or artificial structures.

Secondly, even if it were the case that humans could provide a perfect replica of an animal’s wild environment with wild conditions, would it be morally or ethically permissible? Would it be (morally) right? Forgetting for a second that this perfect replica would still have been constructed upon another natural or wild environment (thereby destroying a natural habitat and causing displacement of many native species), if truly a replica of natural conditions, then the animals placed in this environment would be subject to both the boons and significant hardships of nature. Nature is often bountiful and has allowed the rise of an amazingly diverse array of living beings, but has also borne witness to countless extinctions and ecological changes. Wild animals often must endure very harsh conditions to survive—conditions that objectively lead to periods of very poor welfare, when measured through scientific welfare concepts (biological functioning and affective states) [ 10 , 28 , 29 , 30 ]. Inclement weather and natural disasters such as droughts, fires or floods, are all common occurrences in nature. Animals must endure a lack of shelter, food or water in many areas; they must avoid predation, injury, and disease; they may experience miscarriages, offspring mortalities or reproductive issues; they often have to compete with other animals (both of their own and other species) for access to resources; and they have to navigate oft-unfair social interactions and hierarchies. Often, living in nature leads to prolonged suffering and ends in premature death for individuals.

Many wild-type or natural behaviours are also maladaptive in a captive environment (such as fratricide or infanticide for extreme examples; to significant inbreeding in closed populations; group ostracism of certain individuals; or unfulfillable migratory behaviours/motivations) [ 12 , 30 , 31 ]. Thus, if it was indeed the objective of captive animal industries, such as zoos, to perfectly replicate natural environments so their animals may live wildly , it follows that all of the hardships of nature would also occur, or would have to be imposed. This is not a tenable ethical position that any zoo organisation is known to advocate. Instead, natural recreations of wild environments in zoos try to focus mainly on positive elements of nature, without imposition of events or states that may significantly diminish the animal’s well-being [ 5 , 26 , 30 , 32 ]. Ethically, one will not find much (or any) opposition to this mode of treatment of the captive animals. This also provides a pro-captivity argument against some anti-captivity, animal freedom -based philosophies—captivity does indeed curtail some freedom of the captive animal, but it also provides solace and shelter from significant welfare-affecting hardships, which may be especially of benefit to those animals whom are most vulnerable to suffering. Indeed, if captivity is providing all of the needs and wants of an animal (including positive affective experiences), but without liberty, then liberty is not necessarily a basic interest of the animal [ 5 ]. Zoos are often the last bastion of hope for many endangered species, as their wild homes have been irreparably damaged or overtaken by ever-expanding human populations [ 12 , 28 , 30 , 33 ]. This is an ever more salient point after the United Nations Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services (IPBES) released a 2019 report which estimates that anthropogenic influences may cause the extinction of 1 million species of animals and plants [ 33 ].

It should be noted that whilst zoos tend to focus mostly on recreating positive elements of nature and reducing negative circumstances, many zoos also understand the impossibility of complete elimination of all negative circumstances, events, or negative feelings within an animal. In fact, many zoos will impose slight negative circumstances if it is believed that they may be of benefit to the animals’ health, fitness, or experience of life [ 34 ]. That is, harmless or minimally harmful negative circumstances are sometimes imposed to increase stress resilience and/or physiological arousal of an animal [ 35 , 36 ]. For example, it has been reported that reliably signalling startling husbandry events can improve stress resilience and welfare of zoo-housed capuchins ( Sapajus apella ), whilst still leading to physiological arousal within the animals [ 37 ]. However, where is the distinction drawn between harmless, minimally harmful and very harmful negatives? And who makes these categorical judgements?

Through collaborative practices shared between many zoos, a few common circumstances for imposing minimally harmful negative events include: rotational predator-prey housing (where predatory species and prey species are rotated into the same enclosure at separate times); predator-prey adjacent housing with visual proximity; olfactory proximity between predator-prey species or dominant-subordinate species (sometimes in the form of “enrichment”, like adding predator bedding material to a prey enclosure); or auditory proximity between predator-prey species (such as housing prey species within earshot of vocalising predators or dominant species, or playing recorded audio of predator/dominant animal vocalisations near prey/subordinate species) [ 26 , 31 ]. These circumstances are thought to confer some resilience to animals through arousal of certain fear and vigilance responses, which can have a wide range of beneficial physiological effects, if not experienced for prolonged periods (acute stressors versus chronic stressors) [ 35 , 36 ]. Therefore, some mild harms are actually of high instrumental value within a captive environment. However, there should be a trepidation of pushing such stress responses too far in prey species, or causing inadvertent frustrations to these animals, for example in adjacent predator-prey housing where predators can visually see prey in very close proximity, but not actually reach them. Repeated frustration of consummatory outcomes may lead to development of negative affective states, as indicated by frustration-type behaviours [ 24 , 34 ]. More evidence is needed of the overall effects of the imposition of these stressors on individual animals, to ensure that the intended arousal and stress resilience is being achieved whilst avoiding unintended frustrations or development of negative affective states in these animals.

4. Natural Living, or Just Natural Looking?

Erstwhile, when considering and implementing positive natural enclosures, zoos may tend to focus only on those that, aesthetically, lead people to believe that the environment is natural . For example, lush plant-life (or well-designed arid/desert habitats), water features, painted backdrops or “mock-rock” walls, absence of artificial structures, and/or limiting contact with visitors (or even staff/keepers) whether the limitations are visual, tactile or proximal. Much of the time, considerations of what is aesthetically pleasing may eclipse considerations of what is functional and appropriate, with respect to evidence-based practices [ 31 ]. More than just looking natural, zoo animals’ enclosures must be able to provide necessary features and structures to allow animals to display a range of important behaviours, provide access to perform positive husbandry practices, and allow ease-of-access for emergency procedures to be adhered to (for both animal emergencies, and other visitor or human emergency situations which may occur). If a natural look is considered forefront, this may lead to functional inadequacies in many enclosures. Sometimes artificial structures in enclosures may be more appropriate to facilitate specific animal behaviours—whereas natural structures may weaken, deteriorate or break (such as tree branches or vines), suitable artificial replacements may provide the necessary environment for the behaviour and be a considerably more durable, sturdy or clean provision, which would require far less maintenance (and therefore monetary cost). As is becoming apparent in novel affective state research, interactions with humans may actually be beneficial and rewarding for some zoo-housed species in some situations [ 38 , 39 , 40 , 41 ]. If a zoo is too focused on wilding their animals, opportunities to truly provide the best positive welfare conditions for the captive animals may be missed or ignored. Therefore, mixed natural/artificial enclosures for animals in zoos, that consider function, aesthetics, appropriate contact with humans, and practicality, may be much more fitting than the natural-only enclosures of the recent past. Two questions we might ask ourselves of mixed natural-artificial environments are as follows:

• Does the animal have the capacity to know that the environment is (partly) artificial?
• Does the animal care if the environment is (partly) artificial?

These are open-ended questions that might be addressed in a separate paper, drawing from current knowledge of animal neurobiology and cognition, and their needs and wants for a “life worth living” [ 4 , 42 ]. There is some evidence that some species do indeed display an innate preference for naturalistic “enriched” enclosures as opposed to basic artificial environments without many features (barren environments) (Box Turtles [ 43 , 44 ]; Coal tits and blue tits [ 45 ]), suggesting that some animals may indeed have a capacity to identify natural environments. Alternatively, perhaps they just innately prefer non-barren , enriched environments—perhaps these animals would be just as likely to select enriched artificial environments over any basic or barren environments. Utilising current animal welfare research and expert consensus a new era of evidence-based enclosure design, natural or not, which consider the animals’ needs foremost, should be the next step forward for zoo institutions [ 46 ]. As will be explored later, unnatural or artificial environments can still be compatible with promoting the expression of natural behaviours.

A dilemma with wilding , then, is that attempts to treat captive animals as wild are partly or wholly incongruent with their actual situation. As has been said in this article before, captive animals are not, nor will they be, wild animals living in a wild environment . Their living environment is completely curated by humans, who must make many decisions for the animals for their best interests. This does not mean that we should attempt to treat all captive animals as we would extensively domesticated animals such as livestock or companion animals (i.e., dogs and cats). Zoos indeed strive to keep their wild animals as “undomesticated” as possible [ 12 ]. This, however, may be an unattainable ideal, due to unintended and unavoidable genetic and epigenetic drifts favouring adaptations for life in a captive environment, despite our best efforts to otherwise prevent this from occurring. Indeed, in a human-animal interaction review chapter, Hemsworth et al. [ 18 ] write about the possibility of unintended domestication in zoos, citing research such as Price [ 47 , 48 ]—“While zoo animals are generally not considered to be domestic animals, domestication can obviously occur with wild animals kept and bred in captivity, such as zoos, but the extent of the domestication process will depend on the rate of artificial selection” [ 18 ]. The chapter also highlights the distinction between domestication of a group of animals, and taming of an individual animal—domestication can be defined as “a process by which a population of animals becomes adapted to man and to the captive environment by genetic changes occurring over generations and environmentally induced developmental events reoccurring during each generation” [ 48 ]; whereas taming is simply “an experiential (learning) phenomenon occurring during the lifetime of an individual animal” [ 47 ]. Domestication is a process most likely to happen to animals that are purposefully kept in captivity, and artificially bred or selected, or genetically altered, by humans. Individual taming may more frequently occur in both captive and wild animals that are in regular contact with humans.

To unpack this, we should consider other historical animal domestications. The domestication process has taken thousands of years for those animals that we now consider domesticated. In that time, these animals have been subject to multiple selective pressures including artificially imposed selective breeding, turning them from a “wild-variant” into domesticated animals, specifically chosen for their desirable adaptations. A strong argument against the concept of natural living for these domesticated animals, therefore, is that these animals don’t actually represent or reflect any animal which may be found in the wild or in nature [ 10 ]. They have transformed into animals that don’t fill any natural ecological niche, whose existence is solely reliant upon human intervention and care, and their persistence is reliant upon humans’ continual propagation of that lineage. Of course, if all human interference or interaction were to cease, these “unnatural” animals are still a part of the biotic community of Earth, and they would be able to freely breed and propagate themselves. Yet still they would not be a part of the current natural ecosystem , they still would not have a natural ecological niche, and many cases of free-living livestock or pets (feral animals) in many inappropriate locations have led to irreparable habitat degradation or even ecosystem collapse [ 28 , 30 ].

Many researchers posit the co-evolution of wolves and humans, rather than the one-way domestication of the animal [ 49 ]. Both species adapted to working with each other (for the benefit of both) over tens or hundreds of thousands of years. Wolf-human co-evolution is now suggested to have happened at multiple historical intervals in different geographical regions, leading to the rise of an entire species (or sub-species), dogs ( Canis familiaris , or Canis lupus familiaris ), and a multitude of breeds [ 49 ]. This co-evolution theory may plausibly explain the domestication process of most modern livestock and pets. Novel research also suggests that the co-evolution of humans and many of our domestic species may have been modulated and propagated by the shared experience of bonding, through the ubiquitous neurotransmitter oxytocin [ 50 , 51 ]. While general consensus would not consider zoo-housed animals as domesticated, we must consider that humans have unintentionally started these animals down a similar domestication pathway, as we now approach the third century of keeping animals in zoos, with many captive animal lineages able to be traced back over 100 years in captivity [ 12 ]. This generational captive breeding (including artificial selection of mates) will certainly have profound effects on the prevalent adaptations of these captive animals—adaptations to life in a captive environment and in close proximity with humans. Speculatively, it is possible that close contact with humans may be activating oxytocin pathways in many captive zoo species, leading to positive affiliative (or bonding) human-animal interactions. Indeed, some researchers are starting to focus on reported keeper-animal bonds in zoos [ 52 , 53 ]. However, 300 years is still a shorter timespan than the domestication process for most other animals we keep today (with exception for some farmed species, such as rapidly “domesticated” mink and foxes), and most animals displayed in zoos still resemble and behave like their wild counterparts far more than any newly bred type of domesticated animal.

One of the core tenets of zoos is to display wild animals that have, and will retain, a certain wildness to visitors, not to breed new types of domesticated animals [ 12 ]. Therefore, many practices and safeguards are employed by zoos to try to maintain this wildness . However, the efficacy of our attempts to retain wildness may eventually be mooted by uncontrollable selective pressures of generational life in captivity. If zoos exist 1000 years from now, zoo animals may have significantly drifted from true representations of their wild counterparts (many of which will be extinct in the wild). But, zoos will still strive to maintain wildness. And for many animals, zoos’ careful management will at least succeed in slowing the rate of domestication, but inevitably some genetic or epigenetic drift (mitochondrial drift), or even morphological drift, might still occur regardless of our procedures and safeguards. Thus, these captive animals that still resemble wild species must have specific requirements for care and housing that may differ from common practices for domesticated animals. This is the care that zoos should, and do, provide. But zoos must also make many ethical judgements and decisions which will benefit the animal for a full and rich life in captivity, whether wild or domesticated or somewhere in-between.

There is significant pressure on zoos to exist to advance both animal welfare and wildlife conservation priorities. Indeed, the World Association of Zoos and Aquariums (WAZA) cite conservation as zoos’ core purpose , but fostering positive animal welfare is their core activity [ 32 ]. However, this animal welfare strategy document also quite plainly acknowledges that often conservation priorities may compromise optimal welfare, but zoos should always endeavour to minimise welfare-reducing conditions [ 32 ]. A strong priority of zoos is to avoid genetic drift towards domestication of their captive held wild animals, but, as explained above, there is still a risk that time will change these animals in unknowable ways. This is not written intentionally as an inflammatory argument against genetic selection and diversity processes utilised by zoos, but merely as an acknowledgement of the inherent entropy of many natural systems, and an acknowledgement that humans do not have absolute control of natural processes. But, we do our best with the science and technology that we have available. This ethical wildness dilemma has been explored in context of other arguments, such as human-controlled facilitated adaptation to climate change impacts [ 29 ]. It should also be considered that there may be negative impacts of zoos maintaining wildness in their non-releasable captive animals, especially in species known to have low behavioural plasticity [ 30 ]. For example, some wild animals may be very prone to negative welfare states due to captivity, manifesting in fear or anxiety responses and behavioural patterns [ 24 , 30 ], whereas domesticated or semi-domesticated species (or wild species with high behavioural plasticity) may potentially cope better in captive environments [ 30 ].

5. (Un)Natural Behaviours

Part of the natural living concept is a focus on allowing animals to express natural behaviours . As has been pointed out by many, however, the definition of natural behaviour is problematic, especially when referring to domesticated species with no natural or wild equivalent animal, and therefore, no known natural behaviours (for review, see [ 10 ]). Again, wilding runs into problematic territory here, by over-emphasising or reinforcing only those natural behaviours that are generally displayed by the species in the wild . Academics have suggested multiple alternative terms for natural behaviour that may better define what is intended, such as normal behaviours or species-typical behaviours [ 1 , 10 , 18 , 34 ]. However, these terms still struggle to articulate which behaviours are definitely included as natural, and behaviours classified in this way may be adaptive or maladaptive for a captive environment. For example, migratory behaviour would be considered normal or typical for a migratory bird species, but is maladaptive in captivity as the animal can not fulfill that motivation [ 30 ]. Many behaviours that are displayed by a species in nature have no function or purpose in a captive setting. Simply because a natural behaviour is not displayed in captivity does not infer that the animal is in a state of distress or suffering. If a natural behaviour serves no purpose for the animal in its captive environment, the motivation to perform the behaviour may be very low or non-existent [ 19 , 23 , 24 , 34 ].

Therefore, more important measures of welfare-positive behaviours for captive animals are highly-motivated behaviours , and highly-rewarding behaviours . These behaviours may be part of a natural repertoire, or wholly unnatural —only displayed in captivity. So-called unnatural behaviours may be the most adaptive for the animal’s captive environment, and may be important for positive affective experiences for that animal. Unnatural behaviours do not fit with the ethos of the concept of natural living or wilding , and attempts may be made to extinguish these behaviours. However, this may actually be of more harm to the animal than benefit—if the behaviour is highly motivated, frustration of that motivation may lead to a negative affective state, and possibly a negative welfare state [ 24 ]. Restricting an animal’s behaviours to only those which are considered natural may also significantly reduce that animal’s ability to make choices (reducing self-determined agency), which in turn leads to a perceived lack of control over their situation, which is known to negatively affect coping efforts and welfare of captive animals [ 31 , 54 , 55 , 56 ].

Another curiosity of nature is what I will term unexpected natural behaviours . These are behaviours that will be performed by wild animals in specific unnatural situations, such as interacting with artificial running wheels or mirrors placed in wild environments. Quite a few “popular science” documentaries and online videos show the effects of placing these sorts of objects in nature. Often animals in these videos will run in the artificial wheel, or stare at their reflection for long periods [ 57 ]. These are wholly wild animals that are interacting naturally with artificial ( unnatural ) objects. Following from this, many behaviours in captive animals may be incorrectly classified as unnatural , as they are behaviours that are also displayed by wild animals with access to the same or similar unnatural objects.

To increase well-being and assist positive welfare outcomes for captive animals, focus needs to shift from a fixation on what are considered natural behaviours to those behaviours which the animal appears highly-motivated to perform. Thus, rather than focus on treating animals as though they were wild , it would be more pertinent to focus on allowing animals to express highly-motivated behaviours , particularly if deprivation or frustration of these behaviours results in significant stress, reduced fitness and/or a negative affective state [ 24 ]. Expressing highly-motivated behaviours may also afford the animals more agency and choice within their environments [ 54 ], which should be allowed within reasonable limits—the allowed behaviours must not compromise the safety or health of the individual performing the behaviours, or of the other animal(s) or human(s) involved (i.e., allowing a predator to hunt for live prey does not consider the ethical obligations for the safety of the intended prey animal). This may be categorised into harmless and harmful wants of an animal. Harmless wants may include highly-motivated behaviours such as foraging, climbing, playing or resting. Harmful wants may include highly-motivated behaviours such as feeding, hunting or fighting without restriction . The important factor here is that harmful wants without restriction can lead to harmful consequences (negative, self-injurious or self-destructive outcomes) for the individual performing the behaviour, or for individuals that are the target of the behaviours. A classic example is allowing Labradors access to food ad libitum will often result in excessive overeating causing multiple long-term health problems, such as obesity and other related conditions. These limits need to be examined carefully and thoroughly, as they will be very species- and individual-specific behavioural limitations. Many zoos are already doing this, however consensus for an ethical and practical realignment towards promoting highly-motivated behaviours instead of natural behaviours needs to be agreed to and endorsed by zoological institutions, associations, workers and allies.

6. Are Human-Animal Interactions Natural?

Whether zoos focus on natural behaviours or highly-motivated behaviours, both of these may still include direct interactions with humans. It is often supposed or assumed that human-animal interactions in zoos are an unnatural phenomenon, however, there is one clear way to counter this presumption. In nature, wild animals encounter many other species around them, to which they must adapt, and often interact with, in positive, negative and neutral ways (from symbiotic relationships to parasitic or predatory relationships). Most wild animals now have to adapt not only to their historically natural ecosystem conspecifics, but also to a multitude of invasive species that were previously unknown to them or their ancestors [ 28 , 30 ]. Also, as we now live in the Anthropocene era, wild animals increasingly have to adapt to the ever-growing and ever-encroaching human population, in an increasingly human-affected world [ 28 , 30 , 33 ]. In captivity, then, are not humans one of those species to adapt to, and to interact with? Humanity often assumes some removal of our species from the rest of nature, that we are somehow a step apart from other animals. It is doubtful that this is how other animals view humans, however. Often one of the great curiosities of the natural world is how competing animal species may form symbiotic balances that benefit all, and actively help each other in interactions. These would be deemed natural behaviours . Therefore, if many species actively interact with other species as a mode of adaptation to their environment, would it not follow that human-animal interactions in zoos could actually be considered quite natural adaptations? And if those interactions are highly-motivated in the animal, should we encourage them?

Whether these interactions are deemed natural or unnatural , allowing for positive human-animal interactions may be one avenue of increasing positive affective experiences for animals, especially if those animals are highly motivated to interact with humans (whether it be zookeepers or zoo visitors) [ 39 ]. These interactions must be subject to rigorous safety evaluations for all participants, of course. However, the current status quo of wilding frameworks often view these interactions as undesirable in any and all situations, regardless of the animal’s motivations behind the intended behaviours. Again, frustration of these motivations may actually be detracting from an animal’s well-being. If an animal is highly motivated to interact with humans in or around its environment, and if those interactions are considered safe for all participants, then those interactions should be allowed to occur, or even promoted (through supervised offerings of such interactions). Obviously some interactions are exempt from these stipulations, when considering an animal’s overall health or best interests (such as veterinary procedures or restraint for medical treatment), though positive reinforcement training schedules can often remove some of the harshest penalties to the animals these situation might present (such as training for quick, mildly-aversive hand-injections, blood sampling, or “crate training” for restraint and transport) [ 37 , 58 ].

An animal’s motivation to engage in positive human-interactions may vary from day-to-day, based on other internal and external factors, but the animal should never be confined to, or negatively coerced into, an interaction scenario. The choice to interact should always be on an animal’s own terms. This may not be the case for all human-animal interactions currently deployed by zoos across the world. Often, many “encounter” or “interaction” animals are not afforded a choice of whether to participate or not, or are housed in inadequate areas that may increase their desire to escape that area, even if it means having to interact when they are unwilling [ 59 , 60 ]. Most industry-accredited zoos have their own welfare charter, and have processes and policies implemented to safeguard encounter animal well-being, and to try to offer as much choice as possible to the animals before being handled for interactions. Indeed, the guidelines published by WAZA [ 32 ] state that: “ Interactive experiences should be non-invasive, safe and non-stressful for animals. Monitoring of all animals involved in interactions must be ongoing and have professional oversight. Risks to animal welfare should be minimised by carefully considering whether interactive experiences are appropriate, and if they are, by accommodating the animals’ particular needs ” (p. 74).

7. Conclusions

Natural living may be a useful concept for developing robust measures of holistic zoo animal welfare, but care must be taken to avoid the pitfalls and dilemmas explored in this article. Specifically, wilding is a concept that may not truly be providing zoo personnel with an appropriate ethical or conceptual basis for optimizing evidence-based animal welfare. Zoos will continue existing well into the future, and so more appropriate measures of what is important to an animal for a “life worth living” in captivity should tend towards highly-motivated behaviours rather than just natural behaviours . Human-animal interactions in zoos are a source of debate and controversy, however, if implemented appropriately, they may significantly enhance animal well-being and holistic animal welfare (which may still be distinctly different concepts, even though the words are now often used interchangeably [ 10 ]), as they are often relationships of great importance to captive animals. Further exploration of what might constitute positive human-animal interactions, both scientifically and ethically, as well as ways of implementing such interactions without leading to unintended or “undesirable” human behavioural patterns emerging (such as an increased desire to “own” exotic wildlife) shall be forthcoming as a follow-up to this article.

Acknowledgments

The author wishes to acknowledge the immense help of Peter Sandøe in testing and tempering the ethical arguments presented within. Thank you, Peter. The author also wishes to thank Paul Hemsworth, Sally Sherwen and Jenny Gray for their critique, comments and guidance. This paper represents an ethical chapter of a broader ethical and experimental PhD thesis conducted through the University of Melbourne, Australia.

This research was supported by an Australian Government Research Training Program (RTP) Scholarship.

Conflicts of Interest

The author declares no conflict of interest.

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Case Study: Elephants at the LA Zoo 2018

Presented 7/7/18

August 10, 2018

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Case Study: Elephants at the LA Zoo

This webinar was pre-recorded. Watch it now!

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OAKLAND ZOO

Oakland Zoo (OZ) was established in 1922 and is managed by the Conservation Society of California (formerly East Bay Zoological Society), a 501(c)3 nonprofit organization dedicated to the conservation of wildlife both locally and globally. With over 700 native and exotic animals, the Zoo is recognized for its outstanding animal care–particularly the elephant care program–and for their LEED-certified veterinary hospital—the largest wild animal veterinary facility in Northern California.

For more than 19 years, Schultz & Williams (S&W) has partnered with the Oakland Zoo on a range of projects to support the Zoo, including business planning, membership and fundraising consulting and implementation of their multi-channel direct response program for membership and annual fund. In recent years, S&W was asked to assist with a gift membership campaign to help expand the Zoo’s base of membership support and assist in its mission to inspire respect and stewardship of the natural world, while providing a quality visitor experience at the Zoo.

Introducing New Multi-channel Strategies

S&W prides itself on taking innovative risks based on past campaign successes and in-depth analysis. Since last year’s gift membership campaign, S&W recommended new strategies to expand reach and influence prospects to buy a gift membership and support the Oakland Zoo.

Establishing a Successful Campaign

After several years of working together, S&W and the Oakland Zoo have formed a successful partnership—one that is built on trust and collaboration. Providing strategic guidance, implementation and analysis, S&W worked with the Oakland Zoo to develop and manage a strong and successful gift membership campaign during the competitive holiday season.

The Challenge

The holidays are an opportune time to maximize membership sales as a gift offer, especially during Cyber Weekend. For this campaign, we set out to craft a compelling membership gift offer and optimize campaign response by reaching both OZ’s current constituencies and new audiences

The Solution

S&W prides itself on taking innovative risks based on past campaign testing and in-depth analysis. Based on results from the previous year’s gift membership campaign, S&W was able to recommend new strategies to expand reach and influence prospects to buy a gift membership and to support the Oakland Zoo’s mission. These strategies included:

• Positioning Oakland Zoo membership as both a unique gift-giving opportunity as well as a way to support the Zoo’s conservation mission.
• Expanding campaign reach through multi-channel digital marketing strategies, including responsive emails, online advertising, social media posts, and promotion on the Zoo’s homepage (carousel slider and two lightboxes).
• Expanding outreach to new audiences through social media targeting and prospect segmentation.
• Developing a responsive email template to facilitate a more user-friendly experience for prospects and maximize overall campaign response.
• Increased promotions around Cyber Weekend, including customized emails, social media ads, and digital promotions on the Zoo’s website to create a sense of urgency around the “best deal” on gift memberships.
• Integrating with the Zoo’s branding and marketing to present strong, cohesive messaging across all promotional channels.

In 2017, the campaign yielded nearly twice the number of responses as the previous year, with a 120% increase in net income. The email series yielded 140 more responses compared to the previous year, resulting in nearly 64% more net revenue.

Increased and targeted promotions contributed to increased response across all digital channels as compared to the previous year. The addition of promotions around Cyber Weekend, along with the new responsive email template (which likely contributed to a 55% increase in email response over the previous year) helped optimize overall campaign response.

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