research for zoos

Zoo Atlanta will close early on Sat., April 13 for Members Only Night. Gates close at 4 p.m., grounds close at 5:30 p.m. 

Research in the modern Zoo

Zoos have come a long way from their beginnings as menageries in the 19th century. Rather than showcasing exotic animals purely for profit and entertainment as early zoos did, modern accredited zoos are active participants in scientific research and wildlife conservation. Research and conservation go hand-in-hand: in order to protect wild animals and their habitats, we need to understand these animals and the threats they face. Our mission at Zoo Atlanta – to save wildlife and their habitats through conservation, research, education, and engaging experiences – drives our contributions to these efforts. Read on to find out how to connect your students to current research and inspire conservation action within your classrooms.  

There are two broad types of wildlife research: in-situ research and ex-situ research. In-situ research is conducted out in the wild. This type of research can directly study the threats facing wild animal populations. It allows scientists to monitor and evaluate animal behavior, population dynamics, and ecosystem processes. The benefit of this type of research is that you are studying wild animals in their wild habitats. 

Ex-situ research is that which takes place outside of an animal’s natural habitat, such as here at the Zoo. This type of research can focus on topics like veterinary medicine, animal training, and individual animal personalities and behavior. Ex-situ research allows researchers to study animals up close and evaluate individual animal behaviors, development, and physiology. Ex-situ research can help conservation efforts that help protect wild animals and their habitats by providing information that would be difficult to obtain in the wild. It also helps zoos learn how to take better care of their animals. 

Zoo Atlanta participates in both in-situ and ex-situ research projects. In-situ research efforts are conducted through field work by zoo teammates and by providing support for the research projects of trusted partners. One effort we have participated in is the discovery and  naming of new species of amphibians . Dr. Joe Mendelson, the Director of Research at Zoo Atlanta, is heavily involved in these efforts and argues that taxonomy is “central to our understanding of the planet and central to our efforts to conserve our increasingly threatened biodiversity.” The Zoo partners with the Central Florida Zoo’s Orianne Center for Indigo Conservation and Auburn University to track and monitor re-released  eastern indigo snakes , many of whom were reared at Zoo Atlanta, in the Conecuh National Forest. We also work closely with the  Dian Fossey Gorilla Fund International , an organization devoted to researching and protecting gorillas in Rwanda and the Democratic Republic of Congo. One of our flagship projects focuses on studying a deadly fungus that has caused  Panamanian golden frogs  to become extinct in the wild. We care for a small population of these frogs at the Zoo with the hope that they can one day be re-released into the wild.  

Zoo Atlanta also conducts many ex-situ research projects on Zoo grounds. As one of the only zoos in the United States to house giant pandas, we have been able to  study giant panda  maternal behavior and sensory perception. These studies can help zoos take better care of panda cubs and provide better enrichment for pandas, while also providing insights that may aid wild panda conservation. The Zoo is the headquarters for the  Great Ape Heart Project , which aims to understand heart disease in great apes such as gorillas, orangutans, bonobos, and chimpanzees. The project studies the causes, diagnosis, and treatment for heart disease in great apes. We also collaborate with researchers from Georgia Tech to study how  elephants can use their trunks  to delicately pick up objects and suck in large amounts of water.  Veterinary medicine ,  Komodo  dragon genome  sequencing, and  sidewinder snake  movement and biodesign are just a few of the other ex-situ research projects that Zoo Atlanta participates in. 

Both in-situ and ex-situ research efforts are vital to wildlife conservation. Zoos are particularly well-situated to conduct ex-situ research, which makes them valuable partners to conservation organizations seeking to learn more about how to protect wild animals. They also support in-situ research projects by contributing money, providing staff and expertise to assist with these efforts, and educating the public about the value of research. You and your students can learn more about Zoo Atlanta’s research efforts by visiting the  Research  section on our website or reading  Beyond the Zoo , which outlines more ways that Zoo Atlanta contributes to wildlife research and conservation efforts. Advanced students who are interested in pursuing biological research can peruse our list of  Zoo Atlanta scientific publications . If you want to visit the Zoo, meet some of the animals we care for and study, and talk to knowledgeable Zoo Atlanta staff members, check out our  Teacher Resources  to start planning your trip

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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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Correspondence to Judy P. Che-Castaldo .

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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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April 15, 2009

How Do Zoos Help Endangered Animals?

There are more to zoos than putting animals on display

Dear EarthTalk: Do zoos have serious programs to save endangered species, besides putting a few captives on display for everyone to see? -- Kelly Traw, Seattle, WA

Most zoos are not only great places to get up close to wildlife, but many are also doing their part to bolster dwindling populations of animals still living free in the wild. To wit, dozens of zoos across North America participate in the Association of Zoos and Aquarium’s (AZA’s) Species Survival Plan (SSP) Program, which aims to manage the breeding of specific endangered species in order to help maintain healthy and self-sustaining populations that are both genetically diverse and demographically stable.

The end goal of many SSPs is the reintroduction of captive-raised endangered species into their native wild habitats. According to the AZA, SSPs and related programs have helped bring black-footed ferrets, California condors, red wolves and several other endangered species back from the brink of extinction over the last three decades. Zoos also use SSPs as research tools to better understand wildlife biology and population dynamics, and to raise awareness and funds to support field projects and habitat protection for specific species. AZA now administers some 113 different SSPs covering 181 individual species.

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To be selected as the focus of an SSP, a species must be endangered or threatened in the wild. Also, many SSP species are “flagship species,” meaning that they are well-known to people and engender strong feelings for their preservation and the protection of their habitat. The AZA approves new SSP programs if various internal advisory committees deem the species in question to be needy of the help and if sufficient numbers of researchers at various zoos or aquariums can dedicate time and resources to the cause.

AZA’s Maryland-based Conservation and Science Department administers the worldwide SSP program, generating master plans for specific species and coordinating research, transfer and reintroductions. Part of this process involves designing a “family tree” of particular managed populations in order to achieve maximum genetic diversity and demographic stability. AZA also makes breeding and other management recommendations with consideration given to the logistics and feasibility of transfers between institutions as well as maintenance of natural social groupings. In some cases, master plans may recommend not to breed specific animals, so as to avoid having captive populations outgrow available holding spaces.

While success stories abound, most wildlife biologists consider SSP programs to be works in progress. AZA zoos have been instrumental, for instance, in establishing a stable population of bongos, a threatened forest antelope native to Africa, through captive breeding programs under the SSP program. Many of these captive-bred bongos have subsequently been released into the wild and have helped bolster dwindling population numbers accordingly.

Of course, for every success story there are dozens of other examples where results have been less satisfying . SSP programs for lowland gorillas, Andean condors, giant pandas and snow leopards, among others, have not had such clear success, but remain part of the larger conservation picture for the species in question and the regions they inhabit.

CONTACTS : AZA’s Conservation & Science Program, www.aza.org/Conscience .

EarthTalk is produced by E/The Environmental Magazine. SEND YOUR ENVIRONMENTAL QUESTIONS TO: EarthTalk , P.O. Box 5098, Westport, CT 06881; [email protected] . Read past columns at: www.emagazine.com/earthtalk/archives.php . EarthTalk is now a book! Details and order information at: www.emagazine.com/earthtalkbook .

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January 27, 2023

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The impact of zoos on society is largely underestimated, says study

by University of Exeter

The benefits of zoos to society and local communities are largely underestimated by the wider population, new research shows.

Researchers found zoos have a unique platform to engage visitors with important messages that contribute to human health and well-being and sustainability.

Zoos and aquariums are some of the most popular tourist attractions, with an estimated 700 million visitors globally each year.

The value of zoos to nature conservation and applied animal science is well understood, but the new study says zoos also have an important role to play in how human society thinks of, and cares about, the natural world , which is not widely known.

As part of the study, researchers conducted an in-depth review of the work of zoos, specifically relating to how they fulfill their four key aims—conservation, education, recreation and research—and how each aim has "added value" in representing the benefits of zoos to society.

The online presence of zoos, the publications they generate, and the activities that they support outside of the zoo, were also analyzed by researchers.

Researchers say that integrating zoos as a resource for human health, and educating visitors on biodiversity, conservation, planetary health, human well-being and sustainable living , and enabling a pro-conservation behavior change within the wider society, will enhance the role of zoos further.

"A zoo is more than a place of entertainment and a collection of animals. Zoos allow us to experience nature and are a great resource for understanding more about conservation, biodiversity and sustainability, bringing many positive benefits to human mental health and well-being," said Dr. Paul Rose, Lecturer at the Center for Research in Animal Behavior and Psychology at The University of Exeter.

"We need places of conservation, such as zoos, to provide us with the education and understanding about the natural world, and for us to be educated, the aims of the zoos need to incorporate increased and meaningful engagement with society and local communities ."

The research found there is still more work to be done and there are many questions for scientists and zoo personnel to explore, as well as evaluating the effect of educational messages, and if the messages are making an impact to human behavior towards planetary health and sustainability.

The paper, written by the University of Exeter, University of Winchester, University of Birmingham, Sparsholt College Hampshire and Dublin Zoo, is published in the Journal of Zoological and Botanical Gardens and is titled "The Societal Value of the Modern Zoo: A Commentary on How Zoos Can Positively Impact on Human Populations Locally and Globally."

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Research power of zoos

Alongside conservation and education, one of the core tenets of a modern zoo is research – but what exactly is the contribution to science from eaza zoos this new piece of fascinating research involving chester zoo’s research officer, dr. lindsay eckley, set out to find out just that..

In this multi-institutional collaboration, comprising of researchers from Chester Zoo, Copenhagen Zoo, and Manchester Metropolitan University, the research team reviewed over 3,300 publications from 291 institutions, which included research topics such as zoology, veterinary sciences, and environmental sciences and ecology. While they found that 65% of institutions had contributed to peer-reviewed science, seven institutions, including Chester Zoo, made up 37% of all publications!

The study also identified a general increasing trend in the number of publications by EAZA members, notably with a more than three-fold increase between 2008 and 2018.

“This paper highlights the tremendous value of zoo research to conservation and the significant contribution that European zoos in particular make to doing practical research that is directly applied to solving welfare and conservation problems on the ground.” – Dr. Simon Dowell, Chester Zoo’s Science Director.

By ensuring that research goes through the peer-review process, zoo researchers ensure their work is of high scientific quality. However, while the study focused on peer-reviewed publications, the authors also highlight the many contributions that zoos have to science outside of peer-reviewed publications through things like contributions to magazines, book chapters, and Best Practice Guidelines, through training opportunities, and by opening their facilities and animal collections to external researchers.

“Scientific evidence is vitally important for making decisions to benefit in-situ and ex-situ conservation. However, to be applied and make a difference on a wider scale, evidence needs to be trustworthy and disseminated. This analysis has shown that zoos and aquaria have the ability to publish valid research in a variety of relevant subjects, but there is room for more. I believe that zoos and aquaria are in a unique position to lead on scientific research and they should be supported to share the results.” –  Dr. Lindsay Eckley, Chester Zoo’s Research Officer.

Figure 1. The number of publications in the top 10 research areas from EAZA zoos between 1998 and 2018.

Read the published research here

OUR TEAM OF EXPERTS WORK IN SIX REGIONS AROUND THE GLOBE – REPRESENTING SOME OF THE PLANET’S MOST BIODIVERSE HABITATS. Discover more about our SCIENCE AND CONSERVATION work.

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Debating the Morality and Value of Zoos

Some readers decry keeping animals in captivity while others tout the educational benefits.

To the Editor:

Re “ The Case Against Zoos ,” by Emma Marris (Sunday Review, June 13):

Ms. Marris argues that leading zoos and aquariums spend an outsized amount on “operations and construction” compared with their expenditures on “conservation projects.”

The reason modern zoos spend so much on operations is simple — effective, science-based zoological institutions focus on the welfare of animals in their care, a moral obligation that does not come cheap. American Humane , the country’s first national humane organization, certifies the humane treatment of animals in more than 60 zoos and aquariums around the globe. These zoological institutions receive our Humane Certified seal as they meet or exceed a science-based set of criteria evaluated by independent auditors who have no stake in the outcome of their decision.

Money spent on proper veterinary care, enrichment activities and nutritious food is not money wasted but rather an investment in the social, and moral, contract we have with animals. To pressure zoos and aquariums to spend less on their animals would lead to inhumane outcomes for the precious creatures in their care.

Robin R. Ganzert Washington The writer is president and chief executive of American Humane.

I am a veterinarian who was a zoo and wildlife park employee for years before obtaining my veterinary degree. Both the wildlife park and zoo claimed to be operating for the benefit of the animals and for conservation purposes. This claim was false. Neither one of them actually participated in any contributions to animal research or conservation. They are profitable institutions whose bottom line is much more important than the condition of the animals.

Animals such as African lions that bred in captivity were “culled” (killed) when their numbers exceeded the financial capability of the zoo to feed them. Baby bears, seals, beavers and other animals were taken in and used by the zoos for financial profit until they were no longer useful, and then either “culled” or released into the wild without the ability to survive. I was taught to recite a spiel on conservation to zoo visitors that was false.

Animals despise being captives in zoos. No matter how you “enhance” enclosures, they do not allow for freedom, a natural diet or adequate exercise. Animals end up stressed and unhealthy or dead.

It’s past time for transparency with these institutions, and it’s past time to eliminate zoos from our culture.

Teri Byrd Vashon Island, Wash.

As a zoology professor and, thanks to my kids, a frequent zoo visitor, I agree with Emma Marris that zoo displays can be sad and cruel. But she underestimates the educational value of zoos.

She cites studies showing that most zoo visitors do not closely read educational signs, arguing that few people experience the zoo other than as a simple family outing. However, those few who gain a serious interest in conservation add up to a lot, given that millions of people visit zoos.

The zoology program at my State University of New York campus attracts students for whom zoo visits were the crucial formative experience that led them to major in biological sciences. These are mostly students who had no opportunity as children to travel to wilderness areas, wildlife refuges or national parks. Although good TV shows can help stir children’s interest in conservation, they cannot replace the excitement of a zoo visit as an intense, immersive and interactive experience. They also get to meet adults who have turned their love for animals into a career, and with whom they can identify.

Surely there must be some middle ground that balances zoos’ treatment of animals with their educational potential.

Karen R. Sime Oswego, N.Y.

Emma Marris briefly mentions sanctuaries. Sanctuaries are a growing and ethical alternative to animals kept in captivity and “on display.” The Global Federation of Animal Sanctuaries is the accrediting body for sanctuaries, with 200 members in the United States and abroad. One hundred percent of the focus of our organization and its member sanctuaries is on the humane care of their animals.

Unlike zoos, sanctuaries receive no government or municipal funding, rely on small staffs supplemented by volunteers, and operate on shoestring budgets. They also take on the additional cost of providing lifetime care for every animal. They do not buy, sell or trade animals and restrict access to the animals, forgoing the lucrative revenue of general admission and attractions. Instead, they rely primarily on public donations for support.

For wild animals that cannot be returned to their natural habitats, true sanctuaries offer the best alternative. It’s what animals deserve and is the moral choice.

Valerie Taylor Phoenix The writer is the executive director of the Global Federation of Animal Sanctuaries.

“The Case Against Zoos” is an insult and a disservice to the thousands of passionate, dedicated people who work tirelessly to improve the lives of animals and protect our planet. Ms. Marris uses outdated research and decades-old examples to undermine the noble mission of organizations committed to connecting children to a world beyond their own.

I’ve specialized in zoo and aquarium marketing as a consultant for 20 years, working directly with animal keepers and their animals to produce commercials that feature everything from sharks to lemurs. I’ve never met more dedicated people in my life. They care for their animals as a parent would care for a child.

Zoos and aquariums are at the forefront of conservation and constantly evolving to improve how they care for animals and protect each species in its natural habitat. Are there tragedies? Of course. But they are the exception, not the norm that Ms. Marris implies. A distressed animal in a zoo will get as good or better treatment than most of us at our local hospital.

The Association of Zoos and Aquariums has been on a continual path of improvement, constantly examining its practices related to animal care and conservation throughout the world.

Most important, Ms. Marris glosses over the true value of zoos and aquariums. When a child looks a gorilla or otter or shark in the eye, something wondrous takes place. A connection is made to a world beyond our own that will live with them forever.

Greg Newberry Cincinnati The writer is president of Animal Instinct Advertising.

I quite agree with Emma Marris. Having lived in Kenya, driving in the Nairobi National Park early in the morning as the animals were beginning to move around, and experiencing the thrill of a black mane lion lying in the middle of the road as if he owned the kingdom, I do not go to zoos. To see the animals no longer able to roam, pacing in small areas, is too cruel to watch.

Frances McClure Oxford, Ohio

As a fellow environmentalist, animal-protection advocate and longtime vegetarian, I could properly be in the same camp as Emma Marris on the issue of zoos. But I believe that well-run zoos, and the heroic animals that suffer their captivity, do serve a higher purpose. Were it not for opportunities to observe these beautiful, wild creatures close to home, many more people would be driven by their fascination to travel to wild areas to seek out, disturb and even hunt them down.

Zoos are, in that sense, akin to natural history and archaeology museums, serving to satisfy our need for contact with these living creatures while leaving the vast majority undisturbed in their natural environments.

Dean Gallea Tarrytown, N.Y.

Emma Marris selectively describes and misrepresents the findings of our research . Our studies focused on the impact of zoo experiences on how people think about themselves and nature, and the data points extracted from our studies do not, in any way, discount what is learned in a zoo visit.

Zoos are tools for thinking. Our research provides strong support for the value of zoos in connecting people with animals and with nature. Zoos provide a critical voice for conservation and environmental protection. They afford an opportunity for people from all backgrounds to encounter a range of animals, from drone bees to springbok or salmon, to better understand the natural world we live in.

John Fraser Susan Clayton Wesley Schultz Dr. Fraser is the author of “The Social Value of Zoos.” Dr. Clayton and Dr. Schultz are professors of psychology.

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Science at the zoo

Zoos and aquariums are very popular tourist attractions, accepting over 200 millions visitors per year in North America , and around 7 00 millions in the world . While being a prime holiday and weekend destination, zoos also have their critics. Values and ethical concerns are usually put forward by people opposing zoos.

But not all zoos are created (or rather managed) equally. What are called “roadside zoos” often exhibit poor animal welfare and lack any educational, conservation or research efforts. On the contrary, accredited institutions are part of a network of zoos that value animal welfare, the preservation of species and their habitats, and science. They submit themselves to public scrutiny and regular inspections by legal and regulating bodies. As the research coordinator at a zoo (and of course part-time PhD candidate here at Concordia), I wish to highlight how doing research in a zoo can benefit animals, institutions and science in general.

Having diverse animals in the same place allows to conduct multi-species comparative research, a fruitful way to address many fundamental questions about biology, physiology, cognition and evolution. Zoos also offer the opportunity to study rare or endangered species that are difficult to observe in nature. For example, there are less than 100 individuals of the rare and elusive Amur leopard in the wild, but approximately 350 in captivity.

The opportunity to study wild populations of Amur leopards is very limited, therefore, studying captive individuals provides ample opportunity to better understand this species improving conservation efforts. For the Amur leopard, and many other of the 40 000 species threatened with extinction , captive research gives us important information on physiology, reproductive biology, health, behaviour and much more. This data is essential for a better understanding of the species’ biological requirements and to design effective management plans and policies.

Practically, researchers can test new methodologies and material very easily and quickly. Before spending a fortune to buy, transport and use materials in the field, it can be very cost-effective to do pilot-projects at a zoo. Some cutting-edge methods can also benefit from small projects in captivity before becoming widespread and exportable to the field.

Accredited zoos include many professions within their team: keepers, biologists, veterinarians, nutritionists, educators, tradesmen, to name a few. With the addition of outside researchers, including many university professors and students , this allows a multidisciplinary approach to research projects. It unlocks research possibilities and facilitates the development of new methodologies. It is also extremely convenient, for a biologist like me, to be able to simply ask colleagues about their expertise in other fields. Unlike in many other research environments, we are always exposed to different visions and practices, which makes it almost impossible to have a narrow and close-minded view on our research topics.

Research in zoos also allows for the evaluation of practices, systematically and objectively. Being under intense scrutiny, zoos and aquariums need to be transparent and honest about what works or not. Scientific research on our animals’ health and welfare, on the impact of animal care practices and the efficacy of educational efforts are crucial ways to do this. Additionally, when submitted to the peer-review process of scientific publications ( some academic journals are dedicated to zoo research ), our practices are evaluated by anonymous and professional reviewers, and available to the public.

Of course, there are downsides to research projects in captivity. Sample size (i.e. the number of animals that can be included in a study) is limited to animals living in the zoo, although multi zoo collaborations is a way to alleviate this hurdle. The ecological settings (weather, habitat, predators, competitors, human threats, diseases, etc.) are also extremely powerful forces affecting wildlife. Although we have better control on the environment and can focus on very specific questions in a zoo, captive research will never recreate the complexities of the natural habitat.

Overall, zoo research can eventually be funneled into conservation efforts (like the reproduction of endangered species, direct support of field conservation programs or reintroduction in the wild) which is another essential aspect of an accredited institution. As the zoological community strives to increase its investment in conservation in the future, zoos and aquariums will become a hotbed for scientific research , allocating millions of dollars annually on research and hiring more and more research-dedicated staff.

About the author

Louis Lazure is a doctoral candidate in Biology. He received a BSc in problem-based learning Biology (UQÀM, 2005), a master’s in International Ecology (Université de Sherbrooke, 2007) and a MSc in Biology (Western University, 2009).

With his expertise in ecology, zoology and animal behaviour, he worked and conducted wildlife research in many countries and in captive settings. Louis is also the Research Coordinator at Zoo de Granby since 2013. His current research precisely explores raccoon’s cognition within a context of human-wildlife interactions in protected areas

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Assessment of Welfare in Zoo Animals: Towards Optimum Quality of Life

Sarah wolfensohn.

1 School of Veterinary Medicine, University of Surrey, Guildford, Surrey GU2 7AL, UK; ku.ca.yerrus@27100bh (H.B.); ku.ca.yerrus@75200ds (S.D.); ku.ca.yerrus@54400ts (S.T.)

Justine Shotton

2 Marwell Wildlife, Colden Common, Winchester, Hampshire SO21 1JH, UK; ku.gro.llewram@senitsuj (J.S.); ku.gro.llewram@jlliw (W.S.M.J.)

Hannah Bowley

Siân davies, sarah thompson, william s. m. justice, simple summary.

Maintaining a high standard of animal welfare is essential in zoos, and methods of animal welfare assessment should aim to evaluate positive as well as negative states. The indicators that are useful in assessing these are discussed as there is huge variability in the available information about the natural biology for some zoo species. Wild baselines are not always the most accurate indicator of what is right for an animal in captivity, which makes the identification of factors to include within species-specific welfare assessment even more challenging. There is no “one size fits all” welfare strategy as it should account for the range of biological requirements and needs, which it is not possible to define for some zoo species. The different approaches for welfare assessment are reviewed, including the development of the Animal Welfare Assessment Grid which offers an evidence-based tool for continual welfare assessment, using technology where appropriate, to facilitate decision making and lead to improvements in the animals’ quality of life.

Zoos are required to maintain a high standard of animal welfare, and this can be assessed using a combination of resource-based and animal-based indices usually divided into behavioural indicators, physiological indicators and clinical/pathological signs. Modern animal welfare assessments should aim to encompass positive affective states and the indicators that are useful in assessing these are discussed. When developing factors to be scored for each species, there is huge variability in the available information about the natural biology for some zoo species and even less information concerning those animals in captivity. Wild baselines are not always the most accurate indicator of what is right for an animal in captivity, which makes the identification of factors to include within species-specific welfare assessment even more challenging. When planning a welfare strategy for any species, it is important that the full range of their biological requirements and needs are considered, but this can be challenging for some zoo species and it is not possible to define a “one size fits all” welfare strategy. The different approaches for welfare assessment are reviewed, including the development of the Animal Welfare Assessment Grid which offers an evidence-based tool for continual welfare assessment, using technology where appropriate, to facilitate decision making and lead to improvements in the animals’ quality of life.

1. Introduction

Ensuring a high standard of zoo animal welfare is important for both ethical and legislative reasons [ 1 ]. In the UK, there are several pieces of legislation governing the welfare of animals in zoos. These include the Zoo Licensing Act 1981 (ZLA), EC Council Directive 1999/22/EC and the Animal Welfare Act (England and Wales) 2006. The ZLA requires animals to be accommodated under conditions that satisfy the biological and conservation requirements of the species. This includes an environment well adapted to meet the physical, psychological and social needs of the species and a high standard of husbandry with a developed programme of preventative and curative veterinary care [ 2 ]. This legislation has been further augmented by the Secretary of State’s Standards of Modern Zoo Practice which states the expected standard of animal welfare in zoos and is periodically updated to reflect recent advances in understanding [ 3 ]. More detailed methods of assessment are laid out in the Zoos Expert Committee’s handbook (2012) [ 4 ]. The handbook suggests using a combination of resource-based and animal-based indices, and that opportunities are provided for animals to experience positive emotional states rather than just avoiding negative states. Assessment methods are divided into three groups: behavioural indicators, physiological indicators and clinical/pathological signs. It suggests best practice is to carry out welfare audits once or twice yearly [ 4 ].

When planning a welfare strategy of any species, it is important that the full range of their biological requirements and needs are considered. Anything known about an animal’s natural history is an important resource for understanding its requirements and the environmental parameters under which it should be kept in captivity. Therefore, published research articles on the species’ biology may assist in the construction of a welfare strategy in the absence of specific welfare provision guidance. However, the current state of knowledge for many species is not comprehensive and so it is not always possible to use this as a gold standard against which to assess animal welfare [ 5 ], and it is not possible to define a “one size fits all” welfare strategy [ 6 ].

The concept of a life worth living or even a good life [ 7 ] introduces the idea of considering the temporal component of welfare across the duration of the animal’s life and the need to assess quality of life. Frequently welfare assessment simply looks at the presence of pain and the incidence and severity of disease or injury, reflecting current health status and not considering the total components of welfare. For zoo animals, this is particularly relevant since the majority of zoo animals are managed in a way that aims to ensure reasonably good health, but there is sometimes insufficient emphasis on overall welfare including the adequacy of the environment and the opportunity to express a range of normal behaviours. However, these may be contrary to the desire to show off the animal and provide a close up experience with animals to a revenue generating visiting public. Additionally, for zoo animals that are destined to be returned to the wild or are to be used in international breeding programmes, while their health may be optimal, there are plenty of other issues which can impinge negatively on their welfare. While travelling internationally to participate in breeding programmes may sound positive from a human perspective and for conservation reasons, for an animal, this will involve transportation, change in social hierarchy, change in personnel delivering care, a new environment and numerous stressors which could negatively impact on its welfare and quality of life.

The zoo industry has produced a number of guidance documents regarding animal welfare. The World Association of Zoos and Aquaria has recently produced an animal welfare strategy [ 8 ]. This document outlines the conduct expected from WAZA members, including animal welfare measures. Welfare has been defined according to the five freedoms (Freedom from hunger and thirst; Freedom from discomfort; Freedom from pain, injury and disease; Freedom to express normal behaviour; and Freedom from fear and distress) [ 9 ]. WAZA recommends that zoos and aquariums should apply the Five Domains welfare model (Nutrition, Environment, Health, Behaviour and Mental state [ 10 ]) to assess animal welfare by evaluating the four physical/functional domains and then considering the positive and negative affects generated by these factors within the Mental State domain [ 11 ].

2. Assessment of Welfare

The use of objective measurements of welfare to assess it quantitatively, rather than simply qualitatively, will assist with improving an animal’s quality of life. Evaluating the welfare impact of responses to any clinical interventions or changes in management; for example, transportation, or changes in housing need to be included. It is important not only to focus on the absence of suffering and abnormal behaviours, but also to aim to assess indicators of high welfare through assessing quality of life, positive affective states and “pleasure” [ 10 , 12 , 13 , 14 , 15 , 16 , 17 , 18 , 19 , 20 ]. Boissy et al. [ 21 ] reviewed the evidence supporting the existence of these positive affective states in animals and the explicit inclusion of positive welfare outcomes will allow for analyses which can yield more objective policies to improve welfare following retrospective reviews.

It has been suggested that improved welfare states can be achieved through positive anticipation, giving animals control of their environment, and rewarding them with a higher than anticipated reward—“positive contrast” [ 21 , 22 ]. Yeates and Main [ 13 ] reviewed positive welfare assessment and suggested that it should include both assessment of the resources available to the animal and the value it puts on them, together with the positive behavioural, psychological and physiological outcomes of using these resources and environments. However, they cautioned also to assess any long-term negative effects caused by the resources offered, as animals tend to choose what is rewarding in the short-term even where they have potential longer-term detrimental effects [ 13 ]. Modern animal welfare assessments should aim to encompass a measurement of these positive affective states as part of their assessment [ 23 ], and these measures should be incorporated also into zoo animal welfare assessments.

An animal’s response to a reduction in its welfare will be modified by a number of factors and so interpretation of the response will need to include consideration of the individual details of the animal, such as its species, age, and origin—which may all affect its response. The extent of any examination such as observation of feeding behaviour (quantity and pattern of feeding), physiological parameters (such as heart rate, respiration rate, body temperature, muscle tone, and colour of mucous membranes) and possibly biochemical indicators (such as enzyme levels) will depend on the species. The animal may appear dull, depressed, aggressive, or hyper-excitable, but particularly important are how such traits are at variance with its usual behaviour. Particular attention should be given to noticing any changes in gait, posture or facial expression. Vocalisation will also depend on the species and there are a wide variety of different noises produced by each species. The sound emitted may be outside the human auditory range and therefore go unnoticed but may be causing distress to others of the same species. These are very general descriptions on how to assess changes in welfare qualitatively, and the interpretation of such parameters will vary quite widely between observers, depending on their knowledge and experience of the species and the individual animal under observation.

In making an assessment, it is also necessary to consider whether the animal is juvenile or adult, any normal physiological variation (such as pregnancy) and the animal’s individual temperament. The subjective assessment of the welfare of animals may be based on anthropomorphic assumptions. For example, the assumption that situations or states which are distressing for humans will also be distressing for animals is not necessarily the case. This may lead to a tendency to overestimate any poor welfare experienced by animals in some situations, and underestimate it in others. Sometimes quite abnormal states may be classified by some observers as normal, simply because they occur commonly, for example, regurgitation may be seen frequently in non-human primates [ 24 ] but not necessarily recognised as abnormal by animal carers. It is much better to quantify the assessment being made so that it is objective, in order to be able to judge whether welfare has been improved, and to reduce inter-observer variability in making the assessment. When assessing animal welfare there should be assurances that this is not being done from an anthropogenic viewpoint but this can be helpful in the absence of an evidence base and will give the animal the benefit of the doubt. An awareness that certain environmental parameters which we fail to put emphasis on or provide for some species (such as temperature, access to water, etc.), may be valued by the animals much more highly than the factors we feel a duty to provide [ 17 ].

3. Physiological Assessment

There are various components that can be used to contribute to the objective assessment of an animal’s welfare. Traditional measures of welfare include indicators of physiological stress which focus on monitoring autonomic responses, such as changes in heart rate, respiration rate, blood pressure and/or temperature [ 25 , 26 , 27 ]. This requires either restraint or the implantation of telemetry devices which may compound and confound stress measures, however the technology for less invasive devices is developing rapidly. It is important to ensure that the taking of samples simply to measure welfare should not be contributing to the negative welfare state of the animal. Telomere attrition is a cellular biomarker of biological age which provides a molecular measure of cumulative experience that has been proposed to be used to assess the welfare impact of husbandry regimes on animals. The majority of studies on telomere length have been done on blood samples, but in some studies buccal cells have been used, which requires less invasive sampling [ 28 ]. As technologies develop, further markers may be assessed which do not in themselves have a negative impact on the animal simply for the sake of measuring it [ 29 ].

Another traditional measurement of physiological stress has focused on the detection of hypothalamic–pituitary–adrenal axis (HPA) hormones including cortisol in blood, faeces, urine, saliva, tears or hair. One difficulty in the measurement of cortisol can be the interpretation of results. The collection of faeces, urine or saliva samples for cortisol assay is practically complex, particularly from group-housed animals on a forage substrate and the interpretation of results is complicated by considerable individual variation [ 30 ], a natural circadian variation in cortisol levels [ 31 , 32 , 33 ], the fact that a cortisol response is associated with some non-stress stimuli, and the fact that some stress responses may not involve elevated cortisol levels [ 34 ]. These problems have contributed to an increasing dissatisfaction with the use of cortisol to measure stress levels [ 34 , 35 ].

Measurements such as the neutrophil activation assay or measurement of leukocyte cell counts can give an indication of the effect on the immune response. The measurement of acute phase proteins can also be applied to the assessment of welfare [ 36 ]. The leukocyte activation test measures the degree to which blood can produce a further neutrophil response (superoxide production) to an in vitro challenge. Animals under stress will produce a significantly lower leukocyte response than animals that are not stressed and this has been used to assess physiological stress levels in non-human primates [ 37 ]. However, this also requires the taking of blood samples.

Body weight (which must take into account age, sex, development/reproductive condition), and body condition scoring can both be used to assess the physical condition of the animal which will affect its welfare.

4. Behavioural Assessments

Behavioural measurements are critical in assessing the welfare of zoo animals. The first stage in assessing an animal’s wellbeing is to become familiar with the normal appearance and behavioural repertoire for that species. Animals have not evolved to live in man-made enclosures and the behaviour observed due to the constraints of the captive environment may not be the normal behavioural repertoire [ 38 ]. Behavioural observations can be made with different recording methods [ 39 ] but the goal is to ensure that animals have a natural frequency and range of behaviours and to take action to expand the behavioural repertoire by providing adequate environmental enrichment. Quantified behavioural measurement with systematic sampling allows monitoring of change. Some of the behavioural measures that can be used include quality of sleep [ 40 ], behaviours indicating boredom [ 41 ] and willingness to play [ 16 , 20 , 42 ].

Stress is a physiological and behavioural adjustment which aims to maintain homeostasis. It is possible to reduce and minimise stress levels but it has both benefits and harms to the individual, there is a point at which it will develop into distress. The question is always: how far? Where is the cut-off point? It will develop into distress when there is compromise on other biological processes such as growth, reproduction etc. Uncertainty may induce a state of distress, and such a situation may induce abnormal behaviours. The best known pathological forms of behaviour are behavioural stereotypies which are frequently observed in various species kept in captivity. Stereotypic behaviour is a form of behaviour thought to be induced by chronic frustration [ 43 ], often in response to a barren environment. It may manifest itself as extremes of behaviour (such as pacing, or repeated circling, head turning or self-harming) or as early signs of behavioural disturbance with a significant shift in the range and frequency of behaviours and the development of unusual, non-functional behaviour. The incidence of abnormal behaviours and inappropriate time budgeting, such as overgrooming, and the presence of neophobia are all parameters that can be measured. Trichotillomania is an example of an obsessive compulsive disorder associated with psychological stress, and in humans is relieved by anti-depressants. Many captive animals show forms of coat loss that are apparently absent in wild or free-living conspecifics, resulting from grooming or plucking behaviours directed at themselves or at other individuals. In primates, it is a pathological intensification of natural grooming behaviour, frequently with hair ingestion and is a symptom of psychogenic maladjustment to a poor environment, which can be reduced by the use of various types of environmental enrichment. Quantifying alopecia to assist with welfare assessment in primates (as in many species) can be done using a scoring system as shown in Honess et al. [ 44 ]. Mason and Latham [ 45 ] estimated that stereotypy prevalence for wild carnivores in zoos was 82% of individuals. However, their review concludes that stereotypic behaviour is not always associated with poor welfare and there may be beneficial consequences from performing the repetition to ameliorate welfare in a poor environment—a sort of “do it yourself enrichment”. Studies using voles kept in small cages showed that these stereotypies can be reduced through the use of the opioid antagonist naloxone [ 46 ]. This suggests that the occurrence of stereotypy is associated with the release of endorphins, which may elucidate the functional significance of stereotypies. However, even if stereotypies may be biologically significant to the animal, their incidence indicates that the animals have been (or still are) in a state of chronic stress. Hence, housing conditions within which stereotypies develop should be avoided.

There are various indicators which are useful in facilitating the goal of producing and assessing positive affective states in zoo animals including: controllability and predictability, individual temperament, social behaviours, goal directed behaviours, play behaviours, preference testing, consumer demand tests and cognitive bias tests, and anticipatory behaviour.

Thus, when considering stress, it is also necessary to review the animal’s controllability and predictability of relevant environmental changes. Chronic stress may occur when relevant environmental aspects have a low predictability and/or are not very well controllable over a long period of time. For example, animals may be able to predict the delivery of food, but the event may be beyond their control. The absence of control over an aspect of life as important as food can be a critical stress-eliciting factor in some husbandry systems. However, this does not mean that an ideal environment should be totally predictable and controllable and there is evidence that a certain degree of unpredictability is required to avoid the negative aspects of boredom.

Assessing what animals themselves choose and put value on in their environment can be a useful tool to assess welfare [ 47 ]. Kirkden and Pajor [ 48 ] proposed four important questions that need to be answered when investigating animal preference: whether the animal wants to avoid or obtain the resource; which resource it prefers among available resources; how strong this preference or absolute motivation is; and whether these preferences, or the strength of these preferences, are affected by environmental changes. Importantly, giving animals choices for short-term positive affective states must be balanced with assessment of long-term harm (e.g., ad libitum food access resulting in obesity) [ 13 , 49 ]. Giving animals access to what they value highest, either through preference testing or consumer demand studies [ 50 , 51 ] or, ideally, by providing a variety of resources that the animal can choose between depending on its affective state at the time, may improve zoo animal welfare.

With the modern age of readily accessible and affordable technologies, there is scope to provide much more control to zoo animals. This could include switches they operate to change temperatures, light levels and humidity; or even the scope to give animals tools which could let them better convey their needs to their human carers [ 49 ]. It is the duty of modern zoos to investigate these novel technologies and measure their effect on animal behaviour through robust behavioural monitoring strategies.

A challenge for zoo researchers is to collect enough data on the range of environmental parameters that are important for the huge variety of species kept in zoos, ideally from behavioural research performed in their wild environments, to inform management best practice. This would enable a large database of behavioural repertoires and natural history knowledge to be summated across varied taxonomic groups, to better inform our assessment of positive affective states. Determining indicators of good welfare for species in captivity is a challenge, as historically welfare has been assessed using wild conspecific behaviour as the baseline. However, it is important to recognise that captive wild animals in zoos generally lead very different lives to their wild counterparts, and their welfare needs in the captive situation will therefore need to be assessed to some extent independently of this wild data. Reviews have supported the idea that captive wild animals that are fully able to engage in their environments and to have positive social interactions through living in conditions that reflect their natural habitats may achieve high welfare and positive affective states, provided their basic physiological and psychological needs are appropriately met [ 19 , 20 , 47 ]. However, environments that fully mimic “the wild” are not necessarily better for welfare [ 51 ] and providing for optimal captive zoo animal welfare should provide some aspects of the wild environment (such as opportunity for foraging, exploration and choice) and withhold some of the stressors (such as presence of predators).

When developing factors to be scored for each species, there is huge variability in the available information about the natural biology for some species and even less information concerning those animals in captivity. Scimitar-horned oryx ( Oryx dammah ) have been regarded as an endangered species from the late 1980s before becoming extinct in the wild in the year 2000. Their natural habitat prior to extinction includes locations such as the Sahara and areas of vast desert and sub-desert (IUCN SSC Antelope Specialist Group, 2016) [ 52 ]. Thus, there is less available literature and documentation of the species’ natural behaviours and group structures in the wild, when compared to other captive zoological species. This makes the identification of factors to include within species-specific welfare assessment more challenging.

If captive animals exhibit different behaviours to the wild, should that always be an indicator of poor welfare [ 53 ]? Recognised wild behaviours and group sizes are sometimes used as baseline indicators of the very best welfare, but wild baselines are not always the most accurate indicator of what is right for an animal in captivity. For example, male Amur tigers in the wild would be solitary animals that only interact with conspecifics for mating and territory/resource disputes, whereas, in captivity, they seem to have improved welfare when they are part of a group [ 54 ]. “As wild” should not always be the starting point for the best welfare but further research needs to be undertaken before a clear baseline can be determined. Even if this were achieved, there would always be individuals for which “normal” is different and therefore defining factors for welfare scoring will always have its challenges.

When considering zoo animal welfare, each animal’s individual temperament or “personality” may play a role in its ability to cope with the captive environment. Not only does the reaction to a stressor vary, but also the type of reaction will differ among individuals. Many animal species, including humans, show different coping styles in response to a particular stressor. The distinction between types of individuals (such as proactive or reactive copers) plays a role in the development of a social hierarchy and the stability of social groups. This has been more widely researched in farm animals: one study in dairy ewes identified three emotional states: “fear susceptible”, “intermediate” and “calm, non-emotive ewes”, based on their responses to learning tasks and fear tests [ 55 ]. These ewes’ temperaments also determined their reproductive and production success and different reactions to maternal care of offspring, with the non-emotive ewes showing consistent care of their lambs while the emotive ewes showing increased anxiety states after giving birth [ 55 ]. Further studies have also supported that calm ewes give better maternal care [ 56 ]. Robinson et al. [ 57 ] found that captive chimpanzees showing indicators of positive welfare (as judged from survey results) tended to show more extraversion and lower neuroticism behaviours.

Bond-affirmation behaviours such as allo-grooming and other social behaviours such as sexual activity and maternal or group offspring care are also suggested to be associated with positive affective states [ 20 , 21 , 50 ]. Facial expressions and vocalisations such as purring or chirping may also suggest positive affective states and could be useful welfare indicators [ 13 , 21 , 40 , 58 ]. Zoos face the additional challenge of observing and understanding these behaviours in the captive environment, particularly as some of them may be too subtle for our human perception to detect, or outside our audible range.

Interactions with humans can contribute to negative or positive welfare [ 19 , 40 , 59 , 60 ]. Zoo animal training, conducted primarily through positive reinforcement training, can help to produce positive affects in zoo animals and potentially to improve staff attitudes to animals under their care [ 59 , 61 ]. Using positive reinforcement training and strengthening the animals’ trust in care staff can help to reduce the necessity of fear-driven management of zoo species (such as herding animals away from staff to lock them inside a house). Records of what training is undertaken and the responses and engagement of the animal should be included in welfare scoring assessments.

Promoting positive human-animal interactions in all aspects of zoo care has the potential to increase zoo animals’ welfare, and positive relationships may themselves offer enrichment to zoo animals [ 59 ]. Again, zoo staff need to recognise that what promotes positive welfare in domestic species can be very different in zoo species, particularly those that are wild-caught. Studies have shown that care staff interactions with zoo animals through barriers create a more favourable animal–staff relationship than interactions where care staff enter enclosures [ 59 ]. Further research into the visitor effects on zoo animal welfare are also needed [ 62 ]; while generally visitor presence or behaviours can act as stressors, the way in which visitors interact with zoo species can help to reduce this effect (such as crouching rather than standing in front of enclosures for primate species [ 63 ]). It would be prudent for zoos to investigate novel ways to promote positive welfare through public interactions, some examples of which have been documented [ 61 , 62 ].

Rich environments providing a variety of stimuli and opportunities for exploration, foraging, food acquisition and other goal-directed behaviours are likely to contribute to positive affective states in animals [ 20 ]. Inquisitive exploration and information gathering, which an animal performs to seek stimulation, is thought to be self-rewarding, and animals choose to perform these behaviours when their basic needs have been met [ 21 ]. Studies on contra-freeloading have shown that many animals in certain circumstances prefer to work for a resource such as food, rather than having “easy” access to it and that provision of problem-solving tasks can result in less negative affective states and abnormal behaviours [ 49 ].

Another measure identified as a potential indicator of positive welfare is play [ 16 , 20 , 21 , 42 ]. Bateson [ 64 ] suggested play is intrinsically motivated, occurring when the animal is healthy and not stressed, and that play behaviours in themselves are rewarding. He further categorised “playful play” (as opposed to the wider biological definition of play) as play occurring when the animal is in a positive affective state [ 64 ], and highlighted that it is often not possible for human observers to differentiate this type of play in animals. Play has been shown to be a reward for maze-learning in rats [ 65 ], while play behaviour in lambs was almost eliminated after castration [ 66 ]. Other studies [ 67 ] suggest it is currently not possible to determine whether play does indeed suggest improved welfare compared to neutral welfare states, and it is important to remember that not all species engage in behaviours that we interpret as play [ 42 ]. While generally negative affective states may reduce play activity, this is not always the case; there is evidence that play can also increase during some stressful situations and different types of play activity may occur under different affective states [ 42 , 67 ]. Therefore, currently, the link between play behaviours and positive affective state remains unclear [ 13 ], but data on its usefulness as a positive welfare indicator are increasing, including a number of studies looking at the effects of play in farmed pigs [ 50 ].

Assessing what is important to animals and recording their resulting behaviours, can be a useful tool in measuring affective states. These “tests” include preference testing, consumer demand tests and cognitive bias tests (or “judgement” tests) [ 50 ]. The capacity for zoos to use these tests as tools varies across species and is limited by aspects such as finances and available time for animal training. Offering animals’ choices and assessing their responses can help inform which resources zoo animals prefer in captive environments; this area has been studied in more depth in farmed animals such as mink [ 68 ]. A study of captive orang-utans found that they preferred to position themselves facing the window to view the visitor area [ 60 ]. Cognitive bias assessment may be a useful indicator of positive affective states in animals [ 69 , 70 , 71 , 72 , 73 ]. This is the idea, originally from human psychology research, that an animal with an “optimistic” bias (i.e., having a positive affective state) will react in tests more positively to neutral stimuli and vice versa [ 74 ]. Mendl et al. [ 70 ] reviewed this topic in domestic and non-domestic species, but while explored in domesticated animals [ 75 , 76 ], there have been limited studies in captive wildlife species.

While enriching environments can help animals to cope with future change and stressors, it is also possible that those animals which then move to more barren environments may suffer more than those that had never experienced enriched environments. Douglas et al. showed that pigs housed in enriched environments showed a more “optimistic” response to judgement bias tests; when they were then moved to a sparse environment they reacted more “pessimistically” in the tests compared to those pigs only housed in barren environments [ 77 ]. This is a particular concern for zoos, where animals are frequently moved between collections as part of breeding programmes or for management reasons, and the quality of enclosures at each location is not consistent. Captive rhesus macaques have shown differing responses to ambiguous stimuli compared to known stimuli during cognitive bias testing, depending on whether a positive (environmental enrichment) or negative (veterinary intervention) event preceded the test [ 78 ]—with macaques performing the test after a veterinary intervention reacting in a more pessimistic way to neutral stimuli while those that took the test after enrichment showed a more optimistic response. Similar studies in captive European starlings ( Sturnus vulgaris ) have supported this [ 79 , 80 ], and there are further examples in farm animals including lambs [ 81 ]. One study in squirrel monkeys found that lower levels of environmental enrichment resulted in more negative responses to a novel stimulus, but stated that the degree of variation of response between individuals was high, and enrichment should be tailored to the individual to be effective [ 82 ]. Other studies have focused on the expression of social behaviours and their correlation with optimistic performance in judgement bias tests, for example in dolphins, a highly social species [ 83 ]. Burman et al. [ 84 ] showed that in rats, even short-term decreases in anxiety states through environmental manipulation (in this case, decreased light intensity), can affect judgement bias, making rats behave more optimistically in tasks after only brief spells in lower-light environments, suggesting short-term effects are also important.

Cognitive bias testing in animals is a relatively new tool that researchers are using to investigate animal behaviour and welfare, and care is needed in the interpretation of these studies due to confounders and limited validation [ 74 ]. These tests require substantial training before the animals can perform them, and this in itself may modulate the animal’s affective state [ 74 ]. Cognitive bias assessment may prove challenging to perform in zoo species on a day-to-day basis, but it suggests that encouraging positive affective states through means such as social and environmental enrichment, as appropriate to the individual and the species, should result in animals that have a more positive reaction to novel stimuli and situations.

Anticipatory behaviour, a goal directed behaviour that occurs prior to the acquisition of a reward, may reflect how regularly zoo animals have positive experiences [ 85 ]. It may also help to produce a temporary positive affective state, which may be of importance to animals in fairly consistent environments [ 21 , 86 , 87 ]. A group studying grizzly bears found the bears that showed increased pacing prior to cognitive judgement testing showed more optimistic choices in these tests [ 88 ]. However, another study in dolphins found increased anticipatory behaviour for food-reward-based training sessions in individuals that showed more pessimistic responses in cognitive bias tests [ 89 ], and another showed that rats in more enriched environments showed less anticipatory behaviour to rewards than those living in standard environments [ 90 ]. These findings should be interpreted with caution due to differences between the tests. There is a definite need for zoos to examine all types of anticipatory behaviour in more detail, so that we can better understand the welfare implications of these behaviours.

5. Current Frameworks for Welfare Assessment in Zoos

Several examples of frameworks for zoo animal welfare assessment have recently been published in peer reviewed journals. These include frameworks focussed on organisational structure and staff roles [ 91 ], assessments for auditing individual species [ 92 , 93 , 94 , 95 ] and for monitoring class level taxonomic groups [ 96 ].

Kagan et al. [ 91 ] proposed a universal framework developed by the Detroit Zoological Society. This focuses on ensuring that techniques are developed within zoos to assess all potential indicators of welfare, including affective states. The importance of this has been highlighted by several others [ 11 , 97 , 98 , 99 ]. The advantage of this approach is that it starts with institutional philosophy and policy thereby ensuring that welfare programmes and developments are fully supported and appropriately resourced. The framework also highlights several important features of programme management, including taking an “animal-centred” approach where high quality of life experience for the individual is the over-riding factor in collection planning.

The emphasis on consideration of the entire 24 h life experience of zoo animals is shared by other proposed frameworks, in particular the “24/7” approach to zoo animal welfare proposed by Brando et al. [ 92 ]. This model for welfare assessment is an adaptation of the twelve welfare assessment criteria outlined in the Welfare Quality framework for food production animals [ 100 , 101 , 102 ]. They propose two new criteria relating to feeding and perceived control resulting in a tool with fourteen criteria for the assessment of each species. Natural history, biology, ecology, diet, habitat, social structure and activity patterns are some of the topics proposed to be taken into account when developing a species specific animal welfare programme. This evidence base may then be used to highlight potential mismatches between the wild and captivity. Consideration must be given to the 24 h experience of animals but practically monitoring this can be challenging to achieve.

Similarly, Koene [ 94 ] focused on using behavioural adaptations to assess zoo animal welfare. This approach involved developing databases of species characteristics and comparing behaviours in natural and captive environments to highlight welfare problems. The authors also suggest an adaptation of the Welfare Quality framework for use in giraffe and propose that a gold standard using nature as a reference may be possible, although others have suggested limitations using this approach [ 5 ].

The Welfare Quality framework was also adapted by Clegg et al. [ 93 ] to develop the “C-Well” assessment for use in captive bottle-nose dolphins ( Tursiops truncatus ). In this case, the assessment included eleven criteria and 36 species-specific measures. The authors highlight the importance of the inclusion of animal-based measures. Others have suggested the importance of animal-based measures, though cautioned that some physiological measures are not always practical to use in zoo animals [ 53 ]. This framework suggests that measures should be considered in light of the species under assessment, rather than trying to find a set of criteria which works for all.

Additionally, von Fersen et al. [ 95 ] proposed a decision tree for inspectors to use when assessing zoo animal welfare. This four-step approach begins with a survey including life history and current management. These data are then analysed and scored producing a preliminary report. The third stage involves an in-situ inspection where the survey data is verified and behavioural observations are undertaken alongside hormone analysis. The findings from this stage are then scored and conclusions drawn in the final stage. The framework was proposed as a result of discussions focussing on marine mammal welfare and was implemented for the assessment of captive bottle-nose dolphins and Antillean manatee ( Trichechus manatus manatus ).

The animal’s quality of life should be used for decision-making and to do this an objective assessment of quality of life is needed [ 103 ]. Combining a range of assessment parameters into one usable entity has been identified as an important goal in providing a practical, objective and robust assessment of welfare. The Animal Welfare Assessment Grid (AWAG) was developed for monitoring the welfare and cumulative lifetime experience of primates in research institutions [ 104 , 105 ]. The AWAG records physical health, psychological wellbeing, environmental comfort, and veterinary and management procedural events, encompassing the five domains of animal welfare, and drawing attention to the temporal component of welfare that is often overlooked which allows an assessment of quality of life affected by all the events that occur. The AWAG enables a numeric, as well as visual, representation of the animal’s welfare and represents a valuable tool for those tasked with oversight of, or monitoring of, animals in captivity. The structure of the AWAG makes it highly adaptable for any species. It was validated in experimental primates [ 105 ] and Justice et al. [ 96 ] successfully adapted the AWAG for use in zoos as a monitoring tool which highlights perceived positive and negative welfare impacts. These can then be investigated further using other auditing methods [ 96 ]. In a zoo setting, scores are generated using zoo animal care staff daily reports. This tool is computer based and possesses advantages over the farm animal Welfare Quality protocol [ 95 ] since it generates visual representations of welfare [ 92 ] which are potentially very useful to zoo managers for demonstrating current levels of welfare and informing management decisions [ 96 ].

In addition to these published studies, the AWAG has been trialled further within a zoological collection on giraffe ( Giraffa camelopardalis ), scimitar horned oryx ( Oryx dammah ) and large felids (namely Amur tiger ( Panthera tigris altaica ), Amur leopard ( Panthera pardus orientalis ), snow leopard ( Panthera uncial ) and cheetah ( Acinonyx jubatus )), The first stage of these additional studies was identifying a set of species-specific factors to score within each of the four parameters defined by the AWAG tool. These factors were developed through discussions with experienced animal care staff, zoo veterinarians, and a zoologist at the collection, as well as extensive research into the species being studied to identify the most appropriate indicators of these species’ welfare in captivity. Research into known abnormal behaviours for each species was also carried out to ensure that the factors scored would pick up known species-specific issues. It is important to develop factors that will realistically and objectively assess the animal’s quality of life but which are also feasible and practical to measure within the constraints of the zoo environment. With the AWAG system, these factors can be easily adapted and improved for a species or individual animal over time as the tool is further validated.

The AWAG system can be used to look at either a group of animals or individuals and has been validated against both in these studies. Whether to assess the individual or the group will depend on how the information is captured by the animal care teams, how easy it is to identify an individual, and whether there are any specific concerns about an individual animal. The focus of the animal care staff should always be to look after the welfare and needs of the animals in their care and they only have a limited working day in which to do this. The continued planned development of the AWAG into a simple app based system would make it much easier for the care staff to enter a welfare score directly. The continued development of automated recording technologies to assess behavioural indicators which can link into the AWAG system will also assist with 24/7 monitoring.

The AWAG offers an evidence-based tool for continual welfare assessment, but it should be constantly adapted to include measures of good welfare, using technology where appropriate. For example, computer image recognition software is becoming highly detailed and has been used to assess facial grimace (as a proxy for pain/poor welfare) in mice [ 106 ]. This technology could therefore also be used to monitor positive facial expressions, once these have been determined, as an assessment of positive affective states [ 40 ]. Other technologies, such as auditory monitoring devices, closed circuit television (CCTV) recording and remote or invasive devices to measure heart rate, temperature and heart rate variability could also be used to detect both positive and negative states, and may soon be commercially available to zoo communities. Immune markers and monitoring the sleep patterns of animals could also provide information on the affective state [ 13 , 40 ]. While not practical in the zoo animal setting, research-based imaging techniques such as electroencephalography and functional magnetic resonance imaging studies, which have been used to investigate positive affective state and pleasure-centre responses in humans, could also be used in animals [ 13 ], but not if the effect of the monitoring decreases their welfare.

6. Conclusions

The majority of published studies on zoo animal welfare have focused on mammalian species [ 17 , 107 ]; however, it is necessary to perform evidence-based assessments of zoo welfare across taxonomic groups to inform the management strategy. The perception of zoo animal welfare should be from the animals’ perspective rather than our anthropogenic view, when aiming to ensure positive affective states. Much zoo husbandry and housing provision is based on what has worked previously (or is working currently) and this “status quo” is then adopted into best-practice guidelines, instead of from an evidence-based approach [ 17 ]. The challenge is to validate the measures of positive affect in zoo species, confounded further by the challenges of small sample sizes and challenging working environments for the collection of robust, repeatable experimental data [ 107 ]. Due to the paucity of wild data, it can be difficult, or even misleading, to use this to assess the welfare of zoo animals. However, the AWAG can be used to create a benchmark against which zoo managers can assess welfare improvements over time, which will assist with solving the issues around trying to create a “gold standard”. The AWAG is a highly adaptable tool which aims to assess each animal, as an individual, over the course of its life. Building the themes of positive affective state measurement into this welfare assessment ensures we are able to identify more than just compromised welfare, and thus improve our provision of conditions for positive welfare and life experience in zoo animals.

Attending to the welfare needs of animals is not a passive process; it requires a continuous planning, implementation, assessment, and revision cycle. The assessment of welfare facilitates not only the retrospective illustration of quality of life and the impact of enrichment, husbandry and procedures, but also helps enable the projection of future harms to the animal related to anticipated change, or lack of change. However the assessment of welfare alone is not sufficient and does nothing for the animal whose perception of its own welfare is not affected by the reason it is maintained (whether it is for exhibition or breeding use, for example) [ 108 ]. The outcome of monitoring and assessment must be action to improve welfare and the welfare assessment is simply the tool to demonstrate the action is effective. The continuing development of IT systems of activity monitoring which automatically link to animal unit databases will provide data in the future that can be used to quantify welfare and can be reviewed and reassessed at regular time points.

Zoos have competing priorities: to entertain; to engage and inspire the public to love the natural world and support conservation; to ensure revenue is created to pay for running costs, reinvestment and conservation project support; and to provide the animals in their care with a life worth living and ideally a good life [ 103 ]. Public perception of what contributes to good welfare in zoos is often conflicting and comes from the anthropocentric assessment of perceived welfare and enclosure aesthetics [ 109 ]. It is our duty to increase knowledge and understanding of animal behaviour, welfare, enclosure design and enrichment to improve the animals’ quality of life.

Author Contributions

Conceptualization, S.W.; Methodology, S.W., J.S. and W.S.M.J.; Software, S.W.; Validation, S.W., J.S. and W.S.M.J.; Formal Analysis, H.B., S.D., and S.T.; Investigation, H.B., S.D., and S.T.; Resources, S.W., J.S. and W.S.M.J.; Data Curation, H.B., S.D., and S.T.; Writing—Original Draft Preparation, S.W.; Writing—Review and Editing, S.W., J.S. and W.S.M.J.; Supervision, S.W. and W.S.M.J.; and Project Administration, S.W.

This research received no external funding.

Conflicts of Interest

The authors declare no conflict of interest.

How did Columbus zoo animals react to eclipse? Researchers observed chirps, trumpets, naps

The Columbus Zoo and Aquarium hosted more than 7,000 guests Monday for its "Solar-Bration."

But while guests, and humans across Ohio, were looking up at the sky Monday, some researchers at the Columbus Zoo were looking at the animals and watching how they reacted to the solar eclipse — if they reacted at all.

As the eclipse neared totality and the sky grew dark, many of the animals in the study thought it was nighttime and simply went to sleep, observers told The Dispatch. Some elephants chirped, and the red-crowned cranes went unusually quiet.

It was a unique opportunity to study the zoo’s animals during an eclipse, which only happens every hundred years, Tom Schmid, president and CEO of Columbus Zoo and Aquarium said.

“This is actually pretty big for us because, to our knowledge, there’s not a lot of research and not a lot known out there," said Shannon Borders, curator of the Heart of Africa at the Columbus Zoo. “The knowledge we gain here can only help animals at other zoos and other institutions.”

The Ohio State University School of Environment and Natural Resources teamed up with the Columbus Zoo’s observation interns to document the behavior of animals selected for the study every afternoon for two weeks and will do so for two more weeks. This way, they can compare their behaviors.

How did the animals react during the eclipse?

A hush did not fall over the crowd at the Columbus Zoo Monday as the solar eclipse reached totality. Children jumped, danced, clapped and cheered as the world went as dark as night and the hot day turned cool. Researchers said it could be difficult to parse in some cases if animals were reacting to the eclipse or to people making noise.

How did the animals behave around and during the solar eclipse?

The sloth bear, red pandas, tufted deer, reindeer and ostriches all took naps.

"It was very cute because the girls (the ostriches) literally stopped what they were doing and headed to the back as if they were going to bed," Borders said. "About seven minutes afterward, it started to lighten back up a little bit, and they all stood up, and they started grooming as though they were preparing for the day."

Ashlyn Halseth, who was observing the cougar, said the large cat slept through most of the eclipse, but during totality, when it got very dark, the cougar became alert and looked toward the sun.

The most exciting reaction perhaps came from some of the zoo's elephants who let out chirping sounds and a trumpet. One started thumping her trunk during the darkness.

"Sonny and Rudy are sisters, and when they get excited, they like to be close to each other, and they like to touch each other," said Adam Felts, director of animal wellbeing at the Columbus Zoo. "One of the cutest things was they were surrounding Sabu (the herd's male elephant), and their tails were still in contact with each other, just making sure they were both OK. It was pretty cute to watch."

While the elephants were making more noise than usual, the red-crowned cranes went completely silent and began running around.

"Which is unusual for them because they were vocalizing all day long. I'd been there since about 12 (noon), and they had been nonstop chirping," Emma Blanton said.

The official research won't be released for weeks or months; it will take a while to collect more data on the animals and then to make comparisons.

Other animals that were part of the study include polar bears, brown bears, manatees and kangaroos.

How the research was conducted

“I think one of the coolest things about it is trying to get in the head of the animals,” said Courtney Anderson, a doctoral student in the School of Environment and Natural Resources at Ohio State University. “When we were making our species list and trying to decide which animals we were going to focus on, we kind of had to think about it from their perspective and how a bear might perceive an eclipse and why that might be important versus an ostrich.”

Anderson said they picked a mix of animals to study from different regions around the world. 

During observation periods, particularly during the eclipse, observers write down every 15 seconds what the animal is doing, like eating, walking, sniffing, sleeping, etc.

Anderson told The Dispatch early Monday she and the other researchers would not totally miss out on the eclipse as long as they peeked during 14-second windows. 

“We’re going to make 14-second intervals. As long as we take a data point every 15 seconds, we have time in between that we can (look up),” Anderson said.

Check out: The Dispatch's live coverage of the solar eclipse in Ohio

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How did Fort Worth Zoo animals react to total solar eclipse? Scientists explain

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The first time Martha Silva experienced a total solar eclipse, she was 8 years old watching birds “fly like crazy” around a park in Colombia. Decades later, Silva knew where she wanted to be when the eclipse crossed Texas on April 8: the Fort Worth Zoo.

“Beyond the astronomy implications and the fact that the sun gets shaded, it’s what impact it has on animals, that they don’t understand what’s going on,” Silva, who lives in Fort Worth with her family, said. “I wanted the kids to experience that. It’s the second time they’ve seen it in a zoo.” 

Cloudy conditions couldn’t dim the excitement inside the zoo as visitors and researchers gathered to observe animal reactions to the eclipse. As families gazed into the sky, tortoises rushed toward their barn to recreate their nighttime routine. Giraffes huddled near the entrance to their enclosure. 

Silverback gorilla Elmo yawned more frequently — typically a display of aggression and dominance among primates, said Adam Hartstone-Rose, the North Carolina State University professor leading a study of animal behavior during the eclipse. 

“But Elmo is like the most chill silverback I’ve ever seen,” Hartstone-Rose joked. “So for him, yawning is just like a slightly higher level of social communication. … When a silverback does a full-on dominance thing, you know about it. This was level one on the meter.”

After months of planning, Hartstone-Rose brought dozens of high school students and researchers to Fort Worth to recreate his 2017 study of animal eclipse reactions at a South Carolina zoo. This time around, his team also collected data sheets from zoo visitors and people across the U.S. who entered their observations through the Solar Eclipse Safari website . 

Susie and Jeremy Kimbrell of Lubbock extended their stay in Fort Worth for an extra day to bring their daughter, Carsyn, to see the eclipse. While they considered going to Six Flags, Carsyn — an aspiring veterinarian — enjoyed watching flamingos squawk during the eclipse. The family filled out an observation sheet together after sunlight returned.

“I was honestly wanting to see what the lions were doing, but we were at the wrong place at the wrong time,” Susie Kimbrell said. “We saw the flamingos, and they looked back and forth really weirdly for a couple minutes and then, when it was complete, they all huddled up.” 

In Hartstone-Rose’s previous study, the zoo was extremely crowded and the eclipse elicited loud yelling and screaming from the crowd. That behavior appeared to have an impact on some animals in 2017. Giraffes in South Carolina began running as if they had been startled in the wild, a sign of anxiety. 

Crowds in Fort Worth were much more manageable and “more polite,” Hartstone-Rose said. Though primates and lions appeared to notice that something unusual was happening, their heightened awareness didn’t turn into stress or anxiety responses like in 2017. 

“I’m excited about the research finding, which is that I think we can fairly accurately attribute the anxiety to people being silly,” he said. “When people are only moderately excited, then the animals in general — although they seem confused and more vigilant — it didn’t reach the level of peak anxiety, which I think is a great place to land.” 

Shortly after the eclipse reached 100% totality at 1:41 p.m., North Carolina State doctoral student Ashley Deutsch was feeling much less stressed. Between the time the eclipse started around noon and its peak, Deutsch was zooming across the zoo to deliver video and audio equipment to research groups and conduct her final check-in with students to make sure they had what they needed. 

Thirty students traveled from British Columbia in Canada to be part of the historic research project. Edward Csuka, a physics teacher at Terry Fox Secondary School in Port Coquitlam, British Columbia, said the trip was the culmination of 14 months of fundraising, training and coordinating with Hartstone-Rose. 

“Most of the time, students in school, they don’t really do science,” Csuka said. “They might learn science, but we’re doing science. We’re going to be part of a big publication — the largest in the world, ever — of animal behavior during a total solar eclipse.” 

Once Deutsch and her team land back in North Carolina, they will start transcribing all the paper data sheets filled out by zoo visitors and researchers. She expects over 1,000 data sheets from all over the U.S. 

“Our first step will be collecting everything that we observed in this zoo, and seeing what kind of trends we can see here,” Deutsch said. “Then the next step would probably be synthesizing that with the rest of the country.” 

With their work just beginning, Hartstone-Rose said his team made the right decision by bringing their study to Fort Worth. The project attracted international media attention to the zoo, drawing a documentary film crew and reporters from as far as Japan. 

“All of the keepers, all of the curators, all of the media people have been partners 100% in this,” he said. “The zoo is magnificent. This is arguably the best zoo I’ve ever been to.” 

Haley Samsel is the environmental reporter for the Fort Worth Report. You can reach them at [email protected].

At the Fort Worth Report, news decisions are made independently of our board members and financial supporters. Read more about our editorial independence policy here .

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by Haley Samsel, Fort Worth Report April 8, 2024

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Haley Samsel Environmental Reporter

Haley Samsel is the environmental reporter for the Fort Worth Report. You can reach them at [email protected]. Her coverage is made possible by a grant from the Marilyn Brachman Hoffman... More by Haley Samsel

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