animal research at zoos

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

Connect With Your Wild Side #onlyzooatl

Research at the zoo

Oregon Zoo animals have helped answer a wide range of conservation questions. In the process, they're giving scientists the tools they need to protect wildlife in a rapidly changing world.

Everything we learn here is applied out there

How much energy does a polar bear expend while swimming? Can a dog detect the presence of turtles simply by sniffing water? What's the gentlest way to fit a GPS transmitter on a condor?

These are a few of the field conservation questions that Oregon Zoo animals have helped answer. In the process, they're giving scientists the tools they need to protect wildlife in a rapidly changing world.

Zoo animals can reveal insights that are often challenging and sometimes impossible to obtain in the wild. For that reason, zoo animals are more than ambassadors for their wild counterparts; they're aiding in their survival. The Oregon Zoo collaborates with universities, governments and other zoos to fill gaps in scientific knowledge on short- and long-term research projects.

Featured projects

Polar bear energetics.

In collaboration with the U.S. Geological Survey (USGS), keepers trained polar bear Tasul to wear a collar that recorded data about her movements. Scientists videotaped her wearing this "accelerometer" collar and matched the electronic signals with her behavior. Once the signals are calibrated, identical collars can be placed on wild bears, allowing researchers to remotely study their energy usage.

Borneo elephant genetics

Population and Conservation Genetics Group sought blood samples from Chendra, the western hemisphere's only Borneo elephant, for a study on the impact of fragmentation on the patterns of genetic diversity, social structure, and dispersal of Borneo elephants. Borneo elephants—the world's smallest—are critically endangered, and believed to be genetically distinct from other Asian elephants.

Steller sea lion diet

Determining the wild diet of Steller sea lions is important to understanding their impact on endangered salmon runs. Feeding zoo sea lions a diet of fish marked with tiny glass beads allowed researchers to develop a new technique that uses near-infrared spectroscopy to determine the species of fish in sea lion scat.

Condor satellite tracking

The USGS and U.S. Fish and Wildlife Service fitted an Oregon Zoo turkey vulture with a non-invasive leg-loop harness to test the method for use with California condors. The technique may provide condor field biologists with a new tool and facilitate the testing of technologies for tracking large birds (e.g., cell phone/GPS) that require slightly heavier transmitters.

Turtle-sniffing dogs

The Oregon Wildlife Institute (OWI) trained conservation detector dogs to recognize the odor of western pond turtles and their nests for the purpose of canine-assisted nest searches. The Oregon Zoo supplied water samples containing scent of the target species. The dogs are trained to distinguish the target scent from other odors using operant conditioning procedures.

Polar bear diet

Polar bear siblings Tasul and Conrad participated in a USGS study that will help biologists measure the proportion of land and marine-based prey in wild polar bear diet. The study will assist researchers in understanding how wild polar bears adapt to changes in their food supply changes.

The Zoo is free to visit, but entry passes are required for all guests, including infants.

Today's hours: 8 a.m. to 6 p.m. (last entry 5 p.m.)

Elephant Cam

See the Smithsonian's National Zoo's Asian elephants — Spike, Bozie, Kamala, Swarna and Maharani — both inside the Elephant Community Center and outside in their yards.

Now more than ever, we need your support. Make a donation to the Smithsonian's National Zoo and Conservation Biology Institute today!

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Members are our strongest champions of animal conservation and wildlife research. When you become a member, you also receive exclusive benefits, like special opportunities to meet animals, discounts at Zoo stores and more.

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Find and register for free programs and webinars.

About the Smithsonian Conservation Biology Institute

: Meet the Animals of the National Zoo

Founded in 1889, the Smithsonian's National Zoo and Conservation Biology Institute sits on 163 acres in the heart of Washington, D.C.’s Rock Creek Park and is home to more than 2,200 animals representing almost 400 different species.

The Zoo’s commitment to conservation, research, and education also extends to its second campus in Front Royal, Virginia. There, scientists and animal care experts conduct veterinary and reproductive research to save wildlife and habitats for some of the world’s most endangered animals on the sprawling 3,200-acre property.

Meet the Animals

The Zoo's animal webcams are some of the most famous on the internet. Tune in to watch the Zoo's elephants, lions and naked mole-rats — live, 24/7!

Veterinary Care

Daily Animal Demos

Get a front-row seat to keepers working with animals in these daily demonstrations! Throughout the day, you can meet elephants, watch sloth bears slurp ants, see sea lions catch fish and more.

Animal News

#CheetahCubdate: Farewell to Echo and Her Feisty Cubs!

Our Cheetah Cub Cam is winding down for the season. Read the latest update on the future of the cheetah breeding program... and say hello to some old friends!

Pygmy Slow Lorises Are Born at Smithsonian’s National Zoo and Conservation Biology Institute

For the first time, the Small Mammal House is celebrating the birth of two pygmy slow lorises, an endangered species.

Bird House Team Wins Plume Award

Three chirps for our Bird House team! In recognition of their efforts to breed and care for North American songbirds, they received a Plume Award from the Association of Zoos and Aquariums’ Avian Scientific Advisory Group.

The Animals

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Article Contents

Types of collections, benefits of collaboration, challenges to collaboration and integration, actions moving forward, conclusions, acknowledgments.

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Bridging the Research Gap between Live Collections in Zoos and Preserved Collections in Natural History Museums

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Sinlan Poo, Steven M Whitfield, Alexander Shepack, Gregory J Watkins-Colwell, Gil Nelson, Jillian Goodwin, Allison Bogisich, Patricia L R Brennan, Jennifer D'Agostino, Michelle S Koo, Joseph R Mendelson, Rebecca Snyder, Sandra Wilson, Gary P Aronsen, Andrew C Bentley, David C Blackburn, Matthew R Borths, Mariel L Campbell, Dalia A Conde, Joseph A Cook, Juan D Daza, Daniel P Dembiec, Jonathan L Dunnum, Catherine M Early, Adam W Ferguson, Amanda Greene, Robert Guralnick, Courtney Janney, Debbie Johnson, Felicia Knightly, Stephane Poulin, Luiz Rocha, Pamela S Soltis, Barbara Thiers, Prosanta Chakrabarty, Bridging the Research Gap between Live Collections in Zoos and Preserved Collections in Natural History Museums, BioScience , Volume 72, Issue 5, May 2022, Pages 449–460, https://doi.org/10.1093/biosci/biac022

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Zoos and natural history museums are both collections-based institutions with important missions in biodiversity research and education. Animals in zoos are a repository and living record of the world's biodiversity, whereas natural history museums are a permanent historical record of snapshots of biodiversity in time. Surprisingly, despite significant overlap in institutional missions, formal partnerships between these institution types are infrequent. Life history information, pedigrees, and medical records maintained at zoos should be seen as complementary to historical records of morphology, genetics, and distribution kept at museums. Through examining both institution types, we synthesize the benefits and challenges of cross-institutional exchanges and propose actions to increase the dialog between zoos and museums. With a growing recognition of the importance of collections to the advancement of scientific research and discovery, a transformational impact could be made with long-term investments in connecting the institutions that are caretakers of living and preserved animals.

Animal collections are a repository of our shared biodiversity and a valuable resource of scientific research and discovery (Dick 2017 , Miller et al. 2020 ). Natural history museums hold preserved biodiversity collections and associated specimen and ecological data that have long been recognized as an invaluable and irreplaceable resource for biodiversity research and society (Johnson et al. 2011 , McLean et al. 2016 , Funk 2018 , Nelson and Ellis 2019 , Watanabe 2019 , Lendemer et al. 2020 , NASEM 2020 ). Zoos and aquariums (hereafter, we use zoos to refer to both zoos and aquariums) hold living collections of animals and associated data on life history, demographics, pedigree (genealogy), genetics, physiology, morphology, and behavior but are not typically recognized for their value for biodiversity research (see Zehr et al. 2014 for exceptions, but see Conde et al. 2019 , NASEM 2020 ). Despite the potential for synergy that is apparent in the complementary and nonoverlapping specimen and data types held in zoos and natural history museums, formal partnerships between these two institution types are uncommon.

In the present article, we highlight how potential collaborations could enhance the value of both types of collections and advance collective missions of biodiversity conservation, research, and education. We begin by describing the types of collections and associated data held by each institution, with a particular focus on potential complementarity among types of specimens and data. We then describe benefits of collaboration to each institution type, highlight case studies of existing productive collaborations, and identify best practices for collaborations. We address logistical challenges to integrating collection types, including needs in human and cyberinfrastructure and differences in cultures and values between institution types. We conclude with a list of action steps that institutions can take to link and leverage biological collections to advance biodiversity research.

Biological collections can take various forms and encompass different geographic and taxonomic scales.

Living collections and associated data in zoos

Institutions accredited by the Association of Zoos and Aquariums (AZA) hold roughly 800,000 living animals, primarily in the United States (table  1 ; AZA 2021b ). These collections are strongly biased toward vertebrates and, in particular, birds and fish (Conde et al. 2019 , Rose et al. 2019 ). Globally, zoos use a variety of collections software, with at least three million records digitized worldwide within the Species360 management system alone (Species360 2021 ), representing more than 21,000 species. In addition to living animals, zoos hold extensive records for each animal, starting with birth or transfer from the wild. Zoos record information on taxonomy, animal demography, and pedigrees, and they maintain longitudinal information on health, physiology, life history, behavior, and husbandry protocols used during the animal's life such as diet, veterinary treatments, and social groupings. As a part of routine health assessments, conservation breeding programs, or internal and external research projects, zoos periodically collect and preserve biological materials (whole blood, plasma, serum, DNA, gametes, etc.). Usually, zoos store these biological materials on site, either for the short or long term, depending on storage space and the conservation priority of the species. Typically, biobanks are not coordinated among institutions, but the recently launched European Association of Zoos and Aquaria biobank is an example of coordinated sample storage and coordination (Pérez-Espona 2021 ). In the event of an animal's death, the institution performs a thorough necropsy (Griner 1983 , Terio et al. 2018 ), after which the physical specimen is usually destroyed through incineration or other means. The other biological materials associated with the animals are sometimes maintained and stored after the death of the organism; however, the storage and maintenance of these materials are highly variable and dependent on each institution's own policies.

Characteristics of collections and specimen data from natural history museums and zoos.

For animals currently living within the collection, digital records are updated constantly using management software, such as ZIMS, Tracks, PopLink, or similar software (Cohn 2006 , Faust et al. 2019 ). This information is continuously recorded during an animal's life, which is a major difference from records kept at natural history museums, and is maintained in perpetuity after the animal's death. Within AZA-accredited zoos, information typically is shared. This is necessary for the effective management of the entire captive population, which is seen as a single unit despite the fact that individual animals may be spread out across multiple institutions. Each individual animal has a global accession number and one or more local identifiers. Collection management software tracks detailed husbandry data, pedigrees, and medical records. For animals that have died, records are kept digitally within the management software or, in cases of historical records prior to digitization, are kept on paper.

As the mission of modern zoos has evolved into one of conservation and species preservation, the composition of living collections in zoos has changed over time to reduce the percentage of wild-caught individuals and, correspondingly, to increase the number of captive-born animals. Moreover, zoos have increased their focus on rare or endangered species in need of conservation efforts (Conde et al. 2013 , Tapley et al. 2015 ) and have taken on larger numbers of nonreleasable animals from wildlife rehabilitation centers or confiscations from illegal trade (Fa et al. 2011 ). With each of these shifts, there is a corresponding effect on the scientific value of a collection's animals. For wild-caught animals, locality data may be of use, whereas captive-born animals can provide insights into genetics, health, and pedigree. Increased holdings of at-risk species that may be inaccessible elsewhere and rehabilitation of endangered species that are deemed “nonreleasable” provide the opportunity for research into animals that are in need of human intervention.

Preserved natural history collections in museums

Natural history museums hold roughly 500,000,000 to one billion biological specimens in US collections and three billion worldwide (table  1 ; NASEM 2020 ). These can be whole organisms (typically for smaller animals) or parts of those organisms (e.g., skins, skeletons, DNA, tissue, and associated ecto- and endoparasite samples). Natural history specimens typically include locality data, taxonomy, the collection date, and the collector, as well as information on the treatment (i.e., the method of preservation) of the specimen. Generally, the information available on a specimen in a natural history museum begins with a collection event in the field that results in the attainment of specimens. Once the initial specimen information is obtained, it can then be extended through various lenses (e.g., archaeological, paleontological, geological, societal, or taxonomic). Because specimens are normally euthanized for natural history research, the collection of information during the life of the animal is generally limited. Typically, natural history collection records only represent a single instance in the time of the animal's life—specifically, the period just before its death. However, it presents a transition to research that requires preserved specimens.

Specimen data are held in a range of collection management software platforms, such as Specify, Arctos, EMu, and Symbiota. Unlike in zoos, specimen data are typically not shared across institutions through the collection management software itself. Rather, collection management software platforms frequently use a consistent metadata standard (e.g., the Darwin Core), which allows data interchange (Wieczorek et al. 2012 ). In recent decades, museums have dramatically expanded the digitization and accessibility of specimen data, which has profoundly enhanced the value of specimens for biological research (Nelson and Ellis 2019 , Hedrick et al. 2020 , Miller et al. 2020 ). Data aggregators, such as VertNet, GBIF, DiSSCO, and iDigBio, provide access to collection information across institutions and software platforms and have, along with local institutional web portals, made collection information and specimen details increasingly publicly accessible (Constable et al. 2010 ). The digitization of museum records is an ongoing process, but to date, less than 40% of the specimens in US collections are represented online, with a substantial portion of specimen information remaining to be digitized.

Closer collaboration between zoos and natural history museums has clear benefits to both parties (figure  1 ).

Zoos and museums can maintain robust sharing networks across the United States. The Yale Peabody Museum of Natural History has received specimens from zoos across the US (network shown in orange), whereas the Oklahoma City Zoo has shared samples and specimens with universities and museums (network shown in blue). Both zoos and museums can maintain robust local and country-wide networks.

Benefits to zoos

Zoos typically do not have storage facilities or trained staff to curate preserved specimens in perpetuity. Instead, disposal of specimens is a logistical necessity and often a legal necessity, because of permitting or ownership requirements. As an alternative, if zoo specimens of high scientific value are deposited in natural history museums postmortem to become permanent specimens, this may lead to retrospective health information (figure  2 ) and genetic studies that could potentially contribute to assisted reproductive technologies that would benefit zoo collections in the future. Moreover, by extending the scientific lifespan of animals after death, zoos increase the usefulness of their collections and credibility as conservation-oriented and scientific organizations (figures  3 and  4 ; Miller et al. 2004 , Loh et al. 2018 ). This is particularly important for zoos accredited by the AZA, which has placed increasing emphasis on the need to invest in scientific advancement through basic and applied research (Rose et al. 2019 , AZA 2021a ). Collaborating with museums and having museums report back to zoos (or the AZA) about the impact of linking zoo animals with museum specimens would help to raise awareness of the added value of depositing zoo animals in museums and to help zoos articulate to supporters how their animals go on to promote science and conservation after their death. This kind of reciprocal illumination could aid in producing more fruitful collaboration between these institutions.

An Asian elephant from the Oklahoma City Zoo passed away from unknown causes (global accession no. 21,517,980). After the Museum of Osteology (also in Oklahoma) prepared the specimen as a skeleton and found affected and deformed molars, that diagnosis was determined to be the cause of death. The zoo now uses new dental monitoring techniques on its elephants because of this interaction with the museum. Photograph: Jennifer D'Agostino.

One example of a collections management system that can connect living and preserved specimen databases is the Arctos Collection Management system, a web-based multi-institutional collection management platform that currently handles thousands of records of specimens and biosamples from zoo–museum collaborations. Arctos museum records can be reciprocally linked to any external URL, creating the potential to form direct links with zoo databases such as ZIMS. Linking data between museum collection records and zoo databases will allow tracking of samples and their usage over the lifetime of individuals and beyond across multiple facilities and institutions. Data approved for public access can be searched through the main Arctos portal at https://arctos.database.museum and through biodiversity aggregators such as GBIF, enabling sample, project, and trait-based queries to extend the value of these samples and data for future research. Image: Mariel Campbell.

Since 2010, the Sedgwick County Zoo (SCZ) has partnered with the Yale Peabody Museum of Natural History to provide materials for use in a wide range of scientific studies including CT scanning, morphology studies and genome sequencing. SCZ has contributed over 770 specimens and samples to the Museum, including tissues and carcasses representing taxa from Gymnophiona to Proboscidea, and hopes to broaden communication with other potential partners to ensure maximum use of SCZ's resources. To date, specimens and tissue samples that the Zoo donated to the Museum have been used in more than 22 research projects and in university courses. Several SCZ specimens were scanned as part of the openVertebrate (oVert) Thematic Collections Network (NSF grant no. DBI-1,701,714), including YPM HERA 23,166 (Potamotyphlus kaupii), which is one of two specimens of the species (each from SCZ) used to fill in a vital taxonomic gap in the oVert sampling. Scan data and reconstructions are now available via MorphoSource for use by researchers and educators globally ( https://doi.org/10.17602/M2/M389815 , https://doi.org/10.17602/M2/M389823 ). Image reconstruction: Jaimi A. Gray. The image is a rendering of a 3D reconstruction created from CT scan of specimen YPM HERA 23,166. CT scanning done at Nanoscale Research Facility at the University of Florida, with a GE phoenix v|tome|x m 240 micro-CT scanner, and was funded by oVert TCN (NSF grant no. DBI-1,701,714). Segmentation and rendering performed using VG Studio Max (version 3.5.1).

Benefits to natural history museums

Museums receive clear benefits of expanding their collections with a deeper collaboration with zoos (figure  4 ). This includes not only whole or part of the physical specimen but also eggs or embryos, DNA, tissue, and other biological samples and accompanying information. Because many animals in zoos represent species that are rare, endangered, or even extinct in the wild, collecting new specimens from the field could be difficult, impossible, or potentially unethical. Furthermore, zoo specimens are typically accompanied by a lifetime of data on demography, behavior, reproduction, health, husbandry, and more. For smaller collections or collections used primarily for teaching, the broad diversity of species held by zoos may allow for considerable expansion of taxonomic representation in a collection, especially for nonmodel species. In addition, data collected from specimens of captive origin may be valuable to studies in which the taxon would otherwise be lacking (figure  5 ). Natural history museums would certainly benefit from the rich life history records that zoos focus on, because these data are largely unavailable to the museum community.

Patricia Brennan has worked with dozens of collaborators from farms to zoos to acquire specimens that died in captivity and whose bodies are ultimately preserved at museums for posterity, with Brennan facilitating that exchange after she completes her research. These include specimens of snake hemipenes (Nerodia rhombifer; M1) that are inflated with vaseline (M2) and then made into 3D models (M3). Specimens such as these require careful postmortem handling of animals, including rapid preservation. The connections and collaborations necessary to obtain such specimens have not been easy to establish, particularly as it is not always clear whom to contact for this kind of work at these facilities and this collaborative work is not usually part of the research mission of these facilities. Photograph: Bernard Brennan. 3D Images: Genesis Lara Granados and Juliet Greenwood.

Current collaborative efforts

Existing collaborations between zoos and museums may illustrate shared opportunities and mutually beneficial relationships. In figures  1 – 4 , we show several examples of existing collaborations between zoos and museums and demonstrate a range of benefits for these collaborations. Although zoos and museums occasionally exchange specimens, samples, or data, these exchanges are still relatively infrequent and represent a very small percentage of the collection holdings of either zoos or natural history museums. When exchanges do occur, they are typically the result of connections between individual museum staff (collection managers or curators) and zoo staff (curators or veterinarians), instead of a systemic and long-term collaboration that is established between the institutions. Although the AZA accreditation guidelines encourage specimens to be deposited in natural history museums postmortem (AZA 2021a ), large-scale collaborations are typically not initiated by the leadership of zoos or museums or specifically by interinstitutional organizations (e.g., AZA, the Society for the Preservation of Natural History Collections, and other scientific societies). We recommend the staff at zoos and aquariums consider the long-term benefits of having a largely intact specimen (versus the destructive sampling of a full necropsy) for future study at a museum, when it is possible to do so. Even in cases in which the entire voucher specimen may not be available for depositing at museums, the tissue or DNA samples from these animals (along with the associated data) can continue to be a valuable resource (Buckner et al. 2021 , Card et al. 2021 , Thompson et al. 2021 ).

Zoos and natural history museums have distinct cultures, values, organizational structures, research agendas, data management systems, professional societies, and funding strategies. In addition, there are logistical challenges of linking two different types of institutions. These differences can create barriers to effective communication and productive collaborations, but articulating the differences clearly can help identify commonalities and focal points for collaboration. In the present article, we highlight some of the challenges to working across collection types, and identify actions to surmount these challenges.

Distinct institutional cultures and values

The underlying cultural differences between staff in zoos and natural history museums are multifaceted and complex, although they each hold at their core a passion and keen interest in biodiversity and the natural world. In the present article, we focus on several tangible and relevant elements of these differences such as different terminologies and attitudes toward specimens. Different terminologies used between institutions (box 1 ) can inhibit effective collaboration. Because of distinct and largely separate cultures, perceptions of one institution type by another may be outdated or erroneous. Making these misconceptions explicit and correcting them may help bridge cultures and find common institutional values and research objectives (see the “Different research priorities and agendas” section).

AZA. Association of Zoos and Aquariums, the primary organization that accredits zoos and distinguishes among modern zoos and roadside zoos or private animal collections. AZA requires high standards for animal care, recordkeeping, and engagement in scientific research.

Biobank. A repository for biological samples, typically for medical purposes.

Biocuration. Linking metadata about specimens so that information obtained from work with the specimens is retained or connected with the specimen's data in a digital framework.

Biofact. An artifact of organic origin (skull, fur, shell, horn, etc.), frequently used in zoos.

Cosmetic necropsy. Necropsy performed with minimal disruption to the body equal to a surgical incision. Often precludes full diagnostic value.

Conserve. Protect (something, especially an environmentally or culturally important place or thing) from harm or destruction.

Darwin Core. A body of data standards intended to facilitate the sharing of information about biological occurrences. Used by natural history museums, Darwin Core standards allow for data interoperability among software platforms.

Dynamic links . For example, a hyperlink between GenBank and a museum collection's database that would allow a user to find voucher information about the source of genetic data by clicking on a link. As opposed to static (unchanging) links that connect data repositories, which have a static catalog number that doesn't provide taxonomic or collection information and that cannot be automatically updated.

Extended specimen concept. A recent concept that a natural history specimen is more than a singular physical object, and instead that the specimen has extensions to potentially limitless additional physical preparations and digital resources.

iDigBio. Integrated Digitized Biocollections, the US National Resource and Coordinating Center for facilitating digitization and mobilization of information about vouchered natural history specimens. iDigBio aggregates specimen information from natural history collections across institutions.

MorphoSource. A digital repository of three-dimensional models of biological specimens.

Noninvasive research. Research that does not involve physical harm or distress to a living animal or specimen, i.e., photography or sound recording of living animals, CT scanning of preserved specimens.

Preserve. To safeguard and store the body, or parts of the body, of an organism, typically with a “preservative” such as ethanol and formalin or taxidermy, and associated data for future study.

Species360. A nonprofit NGO that produces ZIMS software, a database used by zoos to collect and store information on animals in zoo collections.

Specimen. A live or preserved organism (part of an organism) housed in a collection.

SPNHC. The Society for the Preservation of Natural History Collections.

SSP. Species Survival Plan Programs, AZA's programs to cooperatively manage ex situ populations for long-term sustainability.

TAG. Taxonomic Advisory Group, AZA's organized groups of taxonomic specialists who guide and facilitate cooperative animal management and conservation programs.

Voucher. A permanently preserved specimen deposited in an accessible collection.

ZIMS. Zoological Information Management Software, a software platform created by Species360 used by many zoos for collection and management of live animal collections.

One major critical distinction between the values of zoos and museums is an affective attachment to living animals in zoos (Hosey and Melfi 2012 ), to which there is little to no apparent analog in museums. Through close daily interaction with individual living animals, long-term bonds between zoo staff and the animal they care for can be formed (Meehan et al. 2016 ). Such affection toward a specimen is rarely demonstrated for preserved museum specimens by museum staff. Comparatively, in museums, care for and attachment to specimens takes on several different forms: performing regular preventative conservation and maintenance; ensuring that specimens used for research are not damaged in such a way that could negatively affect their integrity; and ensuring that specimens are properly identified, and cataloged and that they have data that is made accessible to the public and researchers. In many cases, the history of the specimen tells a story that appeals to museum staff and may lead to some genuine attachment to the specimen and its story (such as who collected it, how long ago it was collected, whether it is a type specimen used to describe a new species, etc.). The sense that a specimen represents the past, but can be used into the future often leads to a great sense of responsibility among museum staff, who realize that their work today affects its usefulness in the future including in ways that are yet to be discovered or realized (NASEM 2020 ).

Different research priorities and agendas

The research priorities and agendas of zoos and museums vary, both in terms of their history and involvement in research and in terms of their research focus. Although both institutions may be involved in research, there is a longer history of scientific research and discovery within museums that may have aided in the development of more research-centric views in their institutional mission, whereas more emphasis is given to animal health and welfare within zoos. Museums typically list the contact information of curators and researchers openly on their websites, making research requests and collaboration relatively easy for users (e.g., other scientists interested in collections, members of the public). In comparison, the process of gaining access to information on zoo collections is less clear, and contact information is not readily available for most zoo collections.

In terms of research focus, collection-based research at natural history museums tends to have a wider focus, including basic biology (e.g., anatomy, biogeography, taxonomy, and systematics), evolution (Funk 2018 ), and more applied research (e.g., conservation and global change, Johnson et al. 2011 , emerging infectious disease, Dunnum et al. 2017 , Cook et al. 2020 , Colella et al. 2021 , Thompson et al. 2021 ). In contrast, several recent studies have reviewed research areas targeted by zoos, which illustrate most publications focus on applied research, such as animal sciences, behavior, cognition, husbandry, reproductive biology, welfare, veterinary care, or field conservation (Loh et al. 2018 , Rose et al. 2019 , Hvilsom et al. 2020 ). Museums also largely serve a research community outside of their walls, through specimen loans and, ever more frequently, digital data (e.g., CT scans online). Although zoo research also extends beyond the boundaries of the footprint of the institution, zoo collections are largely inaccessible to the broader research community.

Some museums may consider zoo specimens of low scientific value, because of the lack of locality data (i.e., the coordinates associated with the source population), possible effects of captivity on phenotypes (O'Regan and Kitchener 2005 , Hartstone-Rose et al. 2014 , Zack et al. 2021 ), potential adaptations to captivity (Williams and Hoffman 2009 ), hybridization of recognized or unrecognized taxa in breeding programs (Witzenberger and Hochkirch 2011 ), or necropsy practices. Although these issues may alter some aspects of the scientific value of specimens, there is considerable new research potential in using specimens from zoo collections to understand life history and demographics (Conde et al. 2019 ), to assess and predict the success of ex situ breeding and conservation translocation programs (Poo and Hinkson 2020 , Poo et al. 2021 ), and for diverse downstream genetic and biochemical analyses (Witzenberger and Hochkirch 2011 ). In addition, the use of zoo specimens in systematics or anatomical studies, among others, is still of significant value, given the rarity of some taxa in the wild or the lack of availability of wild-origin specimens in museum collections. In other words, the benefits of using a zoo animal may outweigh the potential effects of captivity or the lack of locality data.

Another example of distinct research agendas (and agendas in potential conflict) involves destructive necropsies. When a zoo animal dies, there is a critical internal research need and institutional responsibility to conduct a detailed necropsy to determine a cause of death (Griner 1983 , Terio et al. 2018 ). These necropsies are necessary in captive populations, because identifying the cause of death can lead to the prevention of similar issues arising in the remaining zoo population. In contrast, destructive necropsy can make some specimens less valuable to natural history museums, because it interferes with the study of morphology. However, for some taxa, a sample of tissue or blood alone may be invaluable to museums for future research, although it is important to consider that broad sampling of different tissue types may permit organ- or disease-specific sampling or unanticipated research by a broader range of interested parties. In addition to taking potential steps to reduce the destructiveness of necropsies for zoo specimens that are intended for museum transfer, improved communication and collaboration efforts on both sides would work to align research agendas to maximize the value of specimens to both zoos and museums.

Separate and nonoverlapping data management systems

The digitization and integration of biodiversity collection data have opened vast frontiers in scientific discovery (Conde et al. 2019 , Nelson and Ellis 2019 ). Although both zoos and museums hold digitized data in sophisticated data management systems (Cohn 2006 , Nelson and Ellis 2019 ), zoo and museum data are not currently integrated. Moreover, although both types of institutions purchase collections management software, those designed for natural history collection data are generally integrated with community science platforms that are publicly accessible through data aggregators, whereas those used in zoos are not accessible to the public or the larger scientific community through data aggregators or other means.

Legal, political, and ethical barriers to collaboration

There are significant institutional barriers that can prevent effective collaboration. The ownership of individual animals in zoo collections is complex; individual animals may belong to the zoo where they live; may be on loan from another institution; or may be owned by state, federal, or foreign governments. A zoo that is holding an animal may require permission from the owning institution to provide samples to other institutions (even those collected noninvasively), and in some cases, the terms of a loan or holding rights may preclude the collection of samples from an animal or require the destruction of the specimen following its death. Although zoo animals that are of high scientific value may be worth these regulatory obstacles, advance planning may often be required long before the collection of samples from a zoo specimen or transfer of a deceased animal to a museum. Some foresight in negotiating these agreements may go a long way to negating these issues.

Hostility toward zoos by animal rights activists may also prevent sharing sensitive zoo data, including data related to primates, cetaceans, and elephants (Hosey et al. 2020 ) and other charismatic fauna. Some staff or administrators at zoos may feel that the nature—or the very existence—of their institutions and jobs are threatened by animal rights activists (Norton et al. 2012 ). Although the AZA has high standards of animal care that are continually raised and updated, there is concern that bad actors will seek to misrepresent any data and specimens that zoos make available. This alone may make many zoos reluctant to voluntarily share data on husbandry or medical records or even share samples or specimens from these sensitive groups.

Other regulatory barriers may exist in the forms of institutional animal care and use committee protocols, the Nagoya Protocol, and various permitting regulations including the US Department of Agriculture (USDA) Animal and Plant Health Inspection Service, the Endangered Species Act, the Convention on International Trade in Endangered Species, and the Migratory Bird Treaty Act, as well as biosafety and chemical safety regulations. The Nagoya Protocol itself may prevent the transfer of genetic resources (including samples or genetic data) without reference to the original permit or explicit permission from the country of origin. Even the physical process of transferring a sample will have regulatory concerns related to the International Air Transport Association, the USDA, or the US Department of Transportation, and possibly others. In general however, both zoos and museums are required to abide by many of the same laws and regulations, despite the change of some of these issues at the time of the animal's death. Navigating the regulatory labyrinth is key to successful collaboration. Although substantial obstacles may exist, given the degree of overlap in regulatory oversight, such navigation is not insurmountable. In fact, collaborating with museums with more experience with and infrastructure in shipping preserved specimens may benefit zoos; likewise, collaborating with zoos that have high standards of animal care and welfare could benefit museum staff that are collecting, handling, and euthanizing animals in the field.

Increasing the connection between zoos and museums requires concrete steps to be taken to link their digital data, transfer physical specimens across institutions, and create a shared, collaborative, research culture.

Data link and data accessibility

Both zoos and natural history museums have extensive databases critical to the holistic understanding of animal biodiversity (Suarez and Tsutsui 2004 , Cohn 2006 , Conde et al. 2019 , Heberling 2020 ). Although the databases are currently not connected, the opportunity to link their data exists through the Darwin Core metadata standards (Wieczorek et al. 2012 ), which would permit greater integration of data. Although it may not be possible to fully integrate zoo and museum databases using existing infrastructure, integrating data under a common format is certainly an achievable goal in the near future. A shared data language standard will ultimately lead to connecting the information of living and preserved specimens.

Although zoos are understandably reluctant to make sensitive animal data public, the collection management software used by zoos could offer public access to limited data—at a minimum, as a list of species held by an institution or the number of individuals currently held for each species with their accession numbers. Given the public nature of many zoos, some of this information (e.g., the number of species and individuals) is already present for visitors to see and, therefore, sharing such information should not be controversial. Even this basic level of transparency would allow scientists anywhere with research needs to be able to find zoos that hold animal species they might find useful for noninvasive research projects. This level of accessibility would also allow natural history museums to search for individuals at zoos and make requests for tissues or to arrange for transfer of specimens to research collections at the end of an animal's life. We have found that one of the most common frustrations among zoo and museum researchers is not knowing whom to contact at the other institution type in order to begin a collaboration (figure  5 ). Having a website or accessible documentation listing the various roles and contact information for researchers would help facilitate valuable cross-institutional collaborations. We recommend that at least one email address (potentially anonymized for sensitivity) be a dedicated contact for research inquiries. Although it is possible that unwanted inquiries may occur when contact information is made public, the benefits likely outweigh the potential costs. We suggest, as a more localized first step, that zoo and museum staff in relatively close proximity reach out to one another to open lines of communication; we also suggest that interested zoo and museum researchers build coordination and collaboration networks to better address some of the issues raised in the present article.

Specimen and accompanying data transfer

Natural history museums have the capacity to preserve animal specimens, samples, and data in perpetuity. Many zoo animals have high scientific value as living or preserved specimens: rare or endangered animals that cannot be responsibly collected in the wild today, populations destined for reintroduction programs (especially those from which DNA or germlines can be stored for future use; e.g., in long-term longitudinal studies of population genetics), or individuals that have been intensely studied during their lives that can serve as important vouchers for future study. The transfer of specimens from zoos to museums can be divided into two categories: during an animal's lifespan (tissues, blood, DNA , gametes) and postmortem (skeleton, organ, whole specimen). In the former case, collections space within museums can provide a long-term repository permitting the use and study of these samples along with the many other “wild” collections made by these institutions from natural history fieldwork. In the latter case, transfer of animals to natural history museums postmortem would allow research in these individuals to continue for decades or centuries, including research that could help protect and restore biodiversity in the future. To minimize physical damage to zoo animals during postmortem examinations, “cosmetic” necropsies can be performed to preserve the integrity of the scientific specimen. Although less destructive pathology techniques would be valuable, museums are also accustomed to finding great value in some field-collected specimens in less than pristine condition, including highly degraded road kills or specimens freed from the stomach contents of other preserved specimens (Hoving et al. 2013 , Hieb et al. 2014 ). When a zoo specimen is transferred to a natural history museum, both zoo and museum databases should cross-list unique identifiers (e.g., catalog or accession number), so that each institution can track transfer of the specimen. When possible, dynamic links that can allow information from both collection databases to be updated simultaneously should be used, these dynamic data links are for the benefit of both institution types and anyone searching for this information (figure  3 ).

Contributing to the extended specimen concept and greater accessibility

During the first two decades of the twenty-first century, biological specimen collections held in museums and academic institutions have been heavily affected by technological and collections-based innovations. The advent and rapid rise of digitization, for example, has resulted in huge numbers of digital replicas (e.g., CT scans, photographs) of physical specimens being made accessible online. This has led museum curators and collections managers to explore methods for linking their specimen records to related data within and outside of their institutions (e.g., related records from the same collecting event, GenBank records and other sources of genomic data, field notes recorded by collectors, and taxonomic treatments). The publication of The Extended Specimen (Webster 2017 ), follow-up work by the Biodiversity Collections Network (Lendemer et al. 2020 ), a National Academies biological collections report (NASEM 2020 ), and the Alliance for Global Biodiversity Knowledge Discourse consultation facilitated by GBIF (phase 1, www.gbif.org/event/2rUVeHayibJnajGOYgimja/digital-extended-specimen-first-phase-community-consultation , and phase 2, www.gbif.org/event/6FF3aaAHoIkD9JToJjN4Vw/digital-extended-specimen-2nd-phase-community-consultation ) have secured this concept in the literature and launched efforts to more precisely circumscribe the concept of turning a physical specimen into a linked and digitally extended specimen that would have added value for enriching biodiversity research.

The integration of zoo and museum data collected from a single animal is a fitting paradigm for the digital extended specimen concept. The data collected on living animals in zoos (e.g., blood and tissue samples, dietary patterns, behavioral repertoire, disease and illness records) may be far richer and more complete than museum specimens normally provide, especially for animals sampled across a lifetime. Assuming that zoo animals are deposited as specimens in natural history museums on their death, coupling records at these different institutes with bidirectional digital links ensures availability of these data to a broad range of researchers. These shared data can then be added to data aggregators (e.g., iDigBio, GBIF) that make these linked records even more widely accessible and underscore their important role in subsequent scientific efforts (Buckner et al. 2021 ). Specimens, living or dead, that have their metadata in databases will allow for a digital record to exist between the original collectors, caretakers, and curators. Likewise, these databases, when they are public, allow for accessibility that is often a barrier to equity when they are kept completely private. Some sensitive information may be restricted, but the more metadata that are publicly available and accessible, the more equitably the data can be used.

Bridging cultures

Bridging institutional cultures and creating a shared vision of how collections of living and preserved animals can be better integrated are key to advance scientific discovery of biodiversity as a whole. As zoos continue to build up their capacity for research (see AZA 2021a ), there is a clear desire within the research community of both zoos and museums to increase cross-institutional collaboration and exchange of ideas. Scientists from both institutions can make progress through collaborative workshops, shared training sessions, expanding the pipeline for students and younger researchers from diverse backgrounds to work in both settings and for grants to foster the establishment of cross-institutional networks. Ultimately, broad institutional support is needed for lasting change, but a good place to start is through invitations to give seminars, tours of the different facilities, and other exchanges that foster sharing ideas and research by both institution types. It is important to recognize that although there may be cultural differences between institutions, many zoos and museums share the same ultimate goal of conserving species in the wild for the future. Recognizing the idea of an extended specimen concept and acknowledging that the best way to honor an animal may be to preserve it for generations to come can help bridge the differing cultures of zoos and museums. Ultimately, the pathway to bridging cultures requires collaborative initiatives with representatives from both zoos and museums, the development of human connections, and mutual understanding and trust. Although such a pathway may not be easy to traverse, it holds transformative potential for institutions and their staff, for the collections in their care, and for their wild counterparts that both institutions seek to conserve in perpetuity.

Increased coordination between living collections of zoos and the traditional collections of natural history museums is a logical and mutually beneficial relationship. Although nascent collaborations exist that demonstrate the potential of coordination, we argue that the interactions among institutions are severely underdeveloped. We identified areas where the most immediate connections could realize near-term goals, including specimen transfer postmortem, data transfer postmortem, and permanent preservation of zoo specimens and associated data in natural history museums. Furthermore, we point to where a transformational impact could be made with long-term investments in bridging gaps between institutions, such as integrating zoo data with other biodiversity databases and expanding access to and the use of zoo data for biodiversity conservation and global change research. Ultimately, it will have to be the people who work at these institutions who bring cultural change by sharing their scientific ideals and approaches while creating personal connections that lead to collaborations and progress toward shared goals.

The present article was born in digital captivity out of the workshop “Linking and Leveraging Biological Collections: Zoos and Natural History Museums” hosted by iDigBio, Memphis Zoo, Zoo Miami, Yale Peabody Museum of Natural History, and University of Notre Dame and funded by the US National Science Foundation (under grant no. DBI-1547229). The images were provided by Bernard Brennan, Mariel Campbell, Jennifer D'Agostino, Genesis Lara Granados, Jaimi A. Gray, and Juliet Greenwood. Sinlan Poo and Steven M. Whitfield contributed equally to this work.

Author Biographical

Sinlan Poo, Allison Bogisch, Daniel P. Dembiec, Courtney Janney, and Felicia Knightly are affiliated with the Memphis Zoological Society, in Memphis, Tennessee, in the United States. SP is also affiliated with Arkansas State University, in Jonesboro, Arkansas, in the United States. Steven M. Whitfield is affiliated with Zoo Miami and with Florida International University, both in Miami, Florida, in the United States. Alexander Shepack is affiliated with the University of Notre Dame, in Notre Dame, Indiana, in the United States. Gregory J. Watkins-Colwell is affiliated with the Yale Peabody Museum of Natural History, in New Haven, Connecticut, in the United States. Gil Nelson, Jillian Goodwin, David C. Blackburn, Robert Guralnick, and Pamela S. Soltis are affiliated with the Florida Museum of Natural History and with iDigBio, in Gainesville, Florida, in the United States. Patricia L. R. Brennan is affiliated with Mount Holyoke College, in South Hadley, Massachusetts, in the United States. Jennifer D'Agostino and Rebecca Snyder are affiliated with the Oklahoma City Zoo, in Oklahoma City, Oklahoma, in the United States. Michelle S. Koo is affiliated with the Museum of Vertebrate Zoology, at the University of California, Berkeley, in Berkeley, California, in the United States. Joseph R. Mendelson III is affiliated with Zoo Atlanta and with the Georgia Institute of Technology, in Atlanta, Georgia, in the United States. Sandra Wilson is affiliated with the Sedgwick County Zoo, in Wichita, Kansas, in the United States. Gary P. Aronsen is affiliated with Yale University, in New Haven, Connecticut, in the United States. Andrew C. Bentley is affiliated with the University of Kansas, in Lawrence, Kansas, in the United States. Matthew R. Borths and Amanda Greene are affiliated with the Duke Lemur Center, in Durham, North Carolina, in the United States. Mariel L. Campbell, Joseph A. Cook, and Jonathan L. Dunnum are affiliated with the Museum of Southwestern Biology, in Albuquerque, New Mexico, in the United States. Dalia A. Conde is affiliated with Species360 and with the University of Southern Denmark, in Odense, Denmark. Juan D. Daza is affiliated with Sam Houston State University, in Huntsville, Texas, in the United States. Catherine M. Early is affiliated with the Science Museum of Minnesota, in Saint Paul, Minnesota, in the United States. Adam W. Ferguson is affiliated with the Field Museum, in Chicago, Illinois, in the United States. Debbie Johnson is affiliated with Brookfield Zoo, in Brookfield, Illinois, in the United States. Stephane Poulin is affiliated with the Arizona-Sonora Desert Museum, in Tucson, Arizona, in the United States. Luiz Rocha is affiliated with the California Academy of Sciences, in San Francisco, in the United States. Barbara Thiers is affiliated with the New York Botanical Garden, in New York, New York, in the United States. Prosanta Chakrabarty is affiliated with Louisiana State University, in Baton Rouge, Louisiana, in the United States; with the Canadian Museum of Natural History, in Ottawa, Ontario, Canada; with the American Museum of Natural History, in New York, New York, in the United States, and the Smithsonian National Museum of Natural History, in Washington, DC, in the United States.

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Increasing animal cognition research in zoos

Affiliations.

• 1 Department of Psychology, University of Cambridge, Cambridge, UK.
• 2 School of Psychological Science, University of Bristol, Bristol, UK.
• 3 School of Life Sciences, Anglia Ruskin University, Cambridge, UK.
• PMID: 35037289
• DOI: 10.1002/zoo.21674

Animal cognition covers various mental processes including perception, learning, decision-making and memory, and animal behavior is often used as a proxy for measuring cognition. Animal cognition/behavior research has multiple benefits; it provides fundamental knowledge of animal biology and evolution but can also have applied conservation and welfare applications. Zoos provide an excellent yet relatively untapped resource for animal cognition research, because they house a wide variety of species-many of which are under threat-and allow close observation and relatively high experimental control compared to the wild. Multi-zoo collaboration leads to increased sample size and species representation, which in turn leads to more robust science. However, there are salient challenges associated with zoo-based cognitive research, which are animal-based (e.g., small sample sizes at single zoos, untrained/unhabituated subjects, side effects) and human-based (e.g., time restrictions, safety concerns, and perceptions of animals interacting with unnatural technology or apparatus). We aim to increase the understanding and subsequent uptake of animal cognition research in zoos, by transparently outlining the main benefits and challenges. Importantly, we use our own research (1) a study on novelty responses in hornbills, and (2) a multi-site collaboration called the "ManyBirds" Project to demonstrate how challenges may be overcome. These potential options include using "drop and go" apparatuses that require no training, close human contact or animal separation. This study is aimed at zoo animal care and research staff, as well as external researchers interested in zoo-based studies.

Keywords: animal behavior; animal cognition; environmental enrichment; welfare; zoo.

© 2022 The Authors. Zoo Biology published by Wiley Periodicals LLC.

• Animal Husbandry
• Animal Welfare*
• Animals, Zoo* / physiology
• Behavior, Animal / physiology

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• Career Support Fund, University of Cambridge (awarded to RM, supporting RM and EGP)

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• Published: 07 November 2016

Comparative analyses of longevity and senescence reveal variable survival benefits of living in zoos across mammals

• Morgane Tidière 1 ,
• Jean-Michel Gaillard 1 ,
• Vérane Berger 1 ,
• Dennis W. H. Müller 2 ,
• Laurie Bingaman Lackey 3 ,
• Olivier Gimenez 4 ,
• Marcus Clauss 5 &
• Jean-François Lemaître 1  

Scientific Reports volume  6 , Article number:  36361 ( 2016 ) Cite this article

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• Conservation biology
• Evolutionary ecology

While it is commonly believed that animals live longer in zoos than in the wild, this assumption has rarely been tested. We compared four survival metrics (longevity, baseline mortality, onset of senescence and rate of senescence) between both sexes of free-ranging and zoo populations of more than 50 mammal species. We found that mammals from zoo populations generally lived longer than their wild counterparts (84% of species). The effect was most notable in species with a faster pace of life (i.e. a short life span, high reproductive rate and high mortality in the wild) because zoos evidently offer protection against a number of relevant conditions like predation, intraspecific competition and diseases. Species with a slower pace of life (i.e. a long life span, low reproduction rate and low mortality in the wild) benefit less from captivity in terms of longevity; in such species, there is probably less potential for a reduction in mortality. These findings provide a first general explanation about the different magnitude of zoo environment benefits among mammalian species, and thereby highlight the effort that is needed to improve captive conditions for slow-living species that are particularly susceptible to extinction in the wild.

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Introduction

Zoological gardens represent artificial environments in which animals are maintained, bred and displayed. By doing so, zoos achieve a diversity of goals beyond their visitors’ recreation: basic zoological and conservation education reaches 700 million visitors per year all over the world 1 . Continuing research and expertise building by many thousands of zoo staff worldwide continuously improves knowledge of animal, population and ecosystem management. Zoos also aim to maintain viable ex situ insurance populations of endangered species that can be used for re-introduction to the wild 2 , 3 . Zoo staff manages and generates funding for in situ conservation projects 1 , 4 . Finally, zoos facilitate opportunities for researchers to increase expertise in a large variety of areas, from basic zoology to applied husbandry and molecular biology.

When assessing the justification of holding nondomestic species in zoos, the welfare of the individual animals housed in captivity is a critical ethical issue that has to be weighed against these aims 5 . There is no single proxy to measure the welfare of animals. Indicators typically employed include measures of survival (such as longevity, annual survival, or ageing rate), reproduction (such as fertility or litter size), physiology (such as stress hormones or the occurrence of specific diseases) and behavior (such as stereotypies) 5 , 6 . It is typically believed that zoo animals live longer than their free-ranging conspecifics due to the consistent provision of food, water, and shelter from harsh climates, the absence of predation and management to minimize violent intraspecific encounters and accidents, as well as veterinary prophylactic and therapeutic intervention. However, zoo animals may be subject to behavioral deficits 6 . While an increasing number of comparative studies have demonstrated species-specific differences in the response to zoo-conditions 7 , 8 , 9 , and a few species-specific comparisons of survival metrics between free-ranging and captive specimens have been published 10 , 11 , large-scale inter-specific comparisons of captive and free-ranging populations have not yet been performed. Indeed, it is probably difficult to gather accurate demographic estimates in these two contrasted environments for a large range of species. In mammals, comparisons between wild and zoo populations published so far were based on a small number of species (consistently less than 25) and did not control for confounding effects of phylogeny 12 , 13 or were restricted to a narrow taxonomic range (e.g. the mammalian order Artiodactyla 14 ). In addition, these studies have led to conflicting results because they both failed 12 , 13 and succeeded 14 to detect the expected lower actuarial senescence rate (i.e. the rate of decrease in annual survival with increasing age) in zoos. Lastly, none of these studies included survival metrics other than senescence rate, such as longevity or age at the onset of senescence. Therefore, whether the common belief that mammals in zoos outlive their wild counterparts holds true remains unknown.

To address this question, we compared a set of survival metrics derived from life tables available from the literature for males and females of free-ranging populations of 59 mammalian species (including eight different orders, see Supplementary Figure S1 ) to those derived from the data on captive specimens of the same species from the Species360 database 13 , 15 (formerly named International Species Information System database, ISIS). Based on these sex-specific life tables, four metrics describing the survival pattern of each species were calculated: longevity, baseline annual mortality, age at the onset of senescence and rate of senescence ( Fig. 1 ). We compared these metrics between free-ranging and captive populations using linear models and controlled for phylogenetic relatedness among species using a mammal super-tree 16 . An expected higher longevity in zoos can originate from a lower baseline mortality, a later onset of senescence, a lower rate of senescence, or any combination of these measures ( Fig. 1 ).

Graphical displays of the metrics of survival and actuarial senescence analyzed in this study.

Data from female lions ( Panthera leo ) in zoo (in brown) and free-ranging (in green) conditions are used for illustrative purposes. Female lions in the zoo population live longer (age in years) and have a lower baseline annual mortality (in log%), a later onset of senescence (in years) and a lower rate of actuarial senescence (measured as the exponential rate of mortality increase per year).

In 84% of species we analyzed (85% for males and 83% for females, including all carnivores), longevity was higher in zoos than in the wild for both sexes ( Figs 2 and 3A ). The positive relationship between longevity in the zoo and in the wild had a slope less than 1 ( Table 1 ), indicating that short-lived species benefited from living in zoos to a higher extent than long-lived ones ( Fig. 3A ). In about 69% of the species (76% for males and 63% for females), the age at the onset of senescence was identical or delayed in zoos compared to the wild ( Fig. 3B ). The positive relationship between zoo and wild data of onset of senescence also had a slope less than 1 ( Table 1 ), again indicating that species with an early onset of actuarial senescence delayed this onset in captivity to a larger extent than species with a late onset of actuarial senescence. For these latter species, often no difference in response to captivity occurred, and some species even displayed an earlier onset of senescence in zoos ( Supplementary Figure S2 ). The slopes of the relationship between the baseline mortality ( Fig. 3C ) or the rates of actuarial senescence ( Fig. 3D ) at the zoo and in the wild were close to zero ( Table 1 ), indicating that these metrics did not strongly covary between zoo and wild populations. While the baseline mortality was lower in zoos for about 62% of the species (61% for males and 64% for females) and the rate of senescence was lower in zoos for about 73% of the species (76% for males and 71% for females), the nearly horizontal slopes underline the importance of the species’ pace of life for these two metrics: species with a high baseline mortality and high rate of senescence in the wild (i.e. species with a faster pace of life) typically had lower values at the zoo. In contrast, species with a low baseline mortality and a low rate of senescence in the wild (i.e. species with a slower pace of life) typically had higher values at the zoo. Notably, mammals in zoos displayed less variation in both baseline mortality and rate of senescence than in the wild ( Fig. 3 ), indicating more standardized conditions in zoos. All these patterns were remarkably similar for both sexes ( Fig. 3 ).

Longevity in free-ranging and zoo conditions for males (triangles) and females (circles) of each species of Artiodactyla, Carnivora, Primates and other orders (Diprotodontia, Lagomorpha, Perissodactyla, Rodentia and Scandentia).

Species living longer in zoos are indicated with solid lines and species living shorter in zoos are indicated with dotted lines. Full species names are given in Supplementary Table S1 . Animal pictures: nebojsa78©123RF.com.

Comparison of ( A ) longevity, ( B ) age at the onset of senescence, ( C ) baseline annual mortality, and ( D ) rate of senescence (for males and females, respectively) between zoo and wild populations of 59 mammalian species. Points represent raw data, full lines represent the relationship between captive and wild estimates (on a log scale with 95% confidence interval of the model in grey) and the grey dashed line represents the equation y = x. For females, African ( Loxodonta africana ) and Asian ( Elephas maximus ) elephants and hippopotamus ( Hippopotamus amphibius ) were added for illustrative purposes, but were not included in the analysis.

Our findings indicate that, in general, a life in zoos allows mammals to live longer. However, our data suggest that the species-specific pace of life influences the extent to which a given species may benefit from captivity. Species with a faster pace of life typically suffer from high levels of environmentally-driven mortality in the wild including predation 17 , and zoos offer good protection against such causes of mortality. Mammals with a slower pace of life, however, are typically characterized by a later age at first reproduction, a longer gestation period, lower reproductive rates and lower annual mortality 18 . They do not benefit as much from living in zoos in terms of survivorship, or even have a slightly reduced longevity and higher senescence rates, which might be attributable to an earlier onset of breeding in these species in a zoo setting 19 , 20 . Thus, our broad-scale study supports previous work reporting that both Asian and African elephant females live longer in the wild than in zoos 10 ( Fig. 3 ) and provides a first general explanation why different species may benefit with different magnitudes from captivity. Data for the common hippopotamus 21 , included in Fig. 3 for a visual comparison alongside the elephant species, corroborate this interpretation. These findings emphasize that husbandry efforts to optimize the longevity of species with a slower pace of life should be intensified.

To what extent improvement of captive conditions has already occurred in zoos cannot be evaluated with our data. For long-lived species, we cannot include animals born in recent years because of the need to include only extinct cohorts to avoid overestimating age-specific mortality rates (i.e. only dead individuals can be included in life tables). If we assume that age-specific mortality decreases over time in zoos thanks to improved husbandry conditions, especially in recent years and independently of a species’ pace of life, then the absence of recent cohorts for long-lived species in our analyses might account at least partly for our finding that the survival benefit of living in zoos was less pronounced in long- than in short-lived species. We might expect improved living conditions in zoos to have delayed positive effects in long-lived species. For example, there has been tremendous effort in building new elephant enclosures in a great number of zoos in the last decade (DWHM and MC, pers. obs.) and large-scale studies have been performed on the potential to increase captive elephant welfare 22 . However, the benefits of such efforts on survival measures will not be detectable before many years from now. In this respect, it should be kept in mind that our findings, especially concerning the longer-lived species, mostly reflect past husbandry practices that are not necessarily representative any longer.

Our study refutes previous conclusions that the rate of actuarial senescence of vertebrates is not influenced by captivity 13 . When accounting for differences in the pace of life among species, we clearly demonstrate that faster-living species senesce at a lower rate in zoos than in the wild. In addition, we show that both males and females respond similarly to captive conditions. Such a discovery provides indirect evidence that the genuine sex differences in survival patterns in mammalian species subjected to high sexual selection 23 involve physiological mechanisms and cannot only be explained by higher susceptibility of males to environmental conditions.

Carnivores show enhanced survival in zoos in our study, but are more susceptible to behavioral abnormalities 7 , highlighting the need for husbandry techniques to reduce these abnormalities while simultaneously maintaining the survival benefits. Although zoos offer simplified environments, social interactions might be as complex and challenging as in the wild, considering the high frequency of non-antagonistic contacts with humans and other species. Do animals, even when born and raised in zoos, perceive their enclosures as a spatial constraint in terms of compressed home ranges, or as an actual restriction of freedom in terms of a limitation of their own choices? Alternatively, do animals perceive zoos as a safe habitat where potential predators, food scarcity, or extreme climatic conditions are absent, allowing them to drastically reduce vigilance 24 ? Our mere comparison of survival metrics between wild and captive populations should not be interpreted as a conclusive ethical judgment. Our findings should rather be considered as evidence that zoos generally enhance the longevity of mammals, except in species where there is little potential for such an enhancement because of their slower pace of life, which is already linked to both a low mortality and a high longevity in the wild. Because species with a slow pace of life are particularly threatened by extinction 25 , maintaining ex situ insurance populations of such threatened species remains a crucial conservation strategy.

Life tables

Zoo and wild population life tables were compiled from the Species360 database and literature, respectively (see Lemaître et al. 14 for more details). Concerning free-ranging populations, publications containing life-tables from semi-captive populations were excluded to allow a strict comparison between captive and free-ranging populations. For 25 species, we collected several life tables from the same or different populations. When available, we gave preference to life tables obtained from longitudinal data. When several life tables of a given quality were available, we averaged them. When life tables were given in months or not with an integer of years, a standardization was made to obtain the survival at each integer age. For 9 species, the total number of individuals followed or considered was not given in the focal study. In such cases, we arbitrarily assumed that 100 individuals were considered per sex (close to the median value of the number of individuals alive at 1 year of age in the life tables we used). For wild life tables with a known total number of individuals (N = 50 species), the lowest was found for females of Mustela vison for which the life table only included 30 individuals, and the highest is observed for males of Oryctolagus cuniculus with a total of 9,020 individuals ( Supplementary Table S1 ). For captive populations, we only used extinct cohorts of animals for which the sex and both birth and death dates were known, implying that animals were born in captivity. Extinct cohorts were defined as all cohorts born before a given year, which is determined as 2013 minus three quarters of the maximum longevity recorded for the species ( Supplementary Table S1 ). As in captivity the sex ratio could be biased due to the culling of some young males during the first year for management issues (mostly in ruminants), we only computed parameters when at least 25 individuals for each sex of each species were alive at 1 year of age to get accurate estimates of age-specific survival. We finally obtained a dataset of 52 species for which data for both females and males were available, with one additional species with male-only data (leading to 53 species in males) and 6 additional species with female-only data (leading to 58 species in females) ( Supplementary Table S1 ). For both captive and wild populations, we made the same calculations to obtain exactly comparable life tables. For visual comparison only, we included data from females of the two elephant species 26 , 27 and sex-combined data from the common hippopotamus 21 in the resulting data plots but did not include them in the analyses, as their data did not correspond to the data selection criteria stated above.

Metrics of survival

To measure species- and sex-specific patterns of survival and actuarial senescence in captive and free-ranging populations, we used four distinct but complementary metrics: the longevity, the baseline annual mortality, the age at the onset of actuarial senescence and the rate of actuarial senescence (see Fig. 1 . for a graphical display of these metrics). The longevity was extracted from species-specific life tables for both males and females and for both captive and wild populations ( Supplementary Table S1 ). We defined longevity as the age at which 90% of individuals from the initial cohort (alive at 1 year of age) had died ( Fig. 1 ). This allows avoiding spurious estimates due to the exceptionally long life of a few individuals 15 . However, this trait (called ‘longevity’ hereafter) is not a direct measure of senescence because it does not include any explicit information about age-dependent decline in survival. For other metrics, we first measured the logit-transformed age-specific mortality from a given life table. We thus constrained survival of 1 to be equal to 0.99, and we fitted a Generalized Additive Model to obtain the age-specific mortality curve. Since both theoretical and empirical evidence reveal that actuarial senescence does not start prior to the age of sexual maturity 28 , 29 , the onset of actuarial senescence was defined as the age at which the annual mortality rate was the lowest between the age at sexual maturity and the age at which 90% of individuals from the initial cohort have died ( Fig. 1 , Supplementary Table S1 ). The age at sexual maturity (in years) was collected for each sex and each species from a specific literature survey ( Supplementary Table S2 ). The baseline mortality for each sex of each species and for both captive and free-ranging conditions was defined as the annual mortality observed at the age corresponding to the onset of senescence ( Fig. 1 , Supplementary Table S1 ). The baseline mortality at the onset of actuarial senescence corresponds to the lowest mortality observed for a given sex, species, and environment (i.e. wild or captive) between the age at sexual maturity and the age at which 90% of individuals from the initial cohort have died. The rate of senescence was measured as the slope of the linear regression of survival (on a log scale) on age computed between the age at the onset of senescence and the age at which 90% of individuals from the initial cohort have died (i.e. our measure of longevity) 30 ( Fig. 1 , Supplementary Table S1 ). For short-lived species and life tables with a small sample size, we used the age at which at least 5 individuals of a given sex were still alive instead of the age at which 90% of the initial cohort was dead, both to achieve unbiased estimates due to the too few years lived by short-lived species, and to avoid estimating survival from less than 5 individuals. All estimates are reported in Supplementary Table S1 and displayed on Fig. 2 and Supplementary Figures S2–S4 .

Comparative analysis

To avoid biased assessment of the variation in survival patterns between captive and free-ranging populations, we controlled all the analyses for the non-independence between species due to shared ancestry using ‘Phylogenetic Generalized Least-Squares’ (PGLS) models 31 . A phylogeny was built for the 59 species ( Supplementary Figure S1 ) using the phylogenetic super-tree of mammals published by Bininda-Emonds et al. 16 , 32 . Survival and senescence metrics were compared between free-ranging and captive males and females using linear models. Longevity and the onset and rate of actuarial senescence metrics were log-transformed, while baseline annual mortality was logit-transformed prior to any analysis. In a first part, the results of which are displayed in the main text, we analyzed the relationship between the metric measured in zoos (dependent variable) and the corresponding metric measured in wild populations (independent variable). A higher (for longevity and onset of senescence) or a lower (for baseline mortality and rate of senescence) value in captivity indicates that the focal species performs better in zoos. In a second part, we tested whether the quality of demographic estimates in the wild (i.e. measured from longitudinal or transversal studies) and species body mass (log-transformed) influenced the relationships between captive and wild metrics. Survival and senescence patterns are strongly associated with body mass 33 . Typically, larger species live longer 18 and show a lower rate of senescence 34 compared to small species, and have a slower pace of life 35 . To assess whether the patterns we report held when accounting for size differences among species, we included log-transformed body mass as a covariate in our models in a secondary analysis. We collected information about sex-specific mean adult body mass from the literature for each species analyzed ( Supplementary Table S2 ). Therefore, for each of the four survival or senescence metrics in zoos and for a given sex, the full model included the corresponding wild metric and mean adult body mass as covariates, and the two-way interaction between the wild metric and data quality (as a fixed factor using longitudinal data as the reference). We then reduced the model by testing nested models by likelihood-ratio tests (LRT) so that the final model only included variables with statistically significant effects. A total of 3 nested models were tested for each of the metrics analyzed ( Supplementary Table S3 ). A G-test was performed in each case. Models including the interaction between data quality and the wild estimates were never selected, whatever the survival or actuarial senescence metric considered ( Supplementary Table S3 ). This suggests that quality of the wild demographic estimates did not influence the relationship between zoo and wild metrics. Moreover, we observed that body mass influenced zoo metrics in the same direction as the pace of life ( Supplementary Table S4 ), leaving the patterns unchanged, whether including body mass in the models or not. All of these results are provided in Supplementary data (Supplementary Tables S3 and S4) . For ruminant species, it has been shown that grazer species (whose natural diet consists mainly of grass) perform better than browser species (whose natural diet consists mainly of leaves or twigs) in captivity, in terms of survival and actuarial senescence 9 , 14 . In a complementary analysis, we therefore took this pattern into account and corrected the four survival and senescence metrics by including the percentage of grass in the natural diet of each ruminant species in the model. For all ruminant species, survival and senescence metrics were then adjusted for 60% (median, N = 27) of grass in the natural diet. However, results remained remarkably similar with or without this correction ( Supplementary Table S5 ). All analyses were performed with R version 2.14.0 36 and parameter estimates are given with the 95% confidence interval.

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Acknowledgements

Data reported in this paper originate from Species360 for captive life tables and from literature for free-ranging life tables, and are available in the Supplementary Materials (Tables S1 and S2) . M.T. is funded by the French Ministry of Education and Research. We thank Jeanne Peter Zocher of the Vetsuisse Faculty (Zurich) for the permission to use her images of hippopotamus, elephants and lion. We also thank Jean-Michel Hatt, Sandra Wenger and Stamos Tahas for comments on the manuscript.

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J.M.G., D.W.H.M., M.C. and J.F.L. designed the study; M.T., J.M.G., V.B., D.W.H.M., L.B.L., M.C. and J.F.L. collated the data; M.T., J.M.G., V.B., O.G., M.C. and J.F.L. analyzed the data; M.T. and M.C. wrote the first draft of the manuscript that then received input from all other authors.

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Tidière, M., Gaillard, JM., Berger, V. et al. Comparative analyses of longevity and senescence reveal variable survival benefits of living in zoos across mammals. Sci Rep 6 , 36361 (2016). https://doi.org/10.1038/srep36361

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Human–Animal Interactions in Zoos: What Can Compassionate Conservation, Conservation Welfare and Duty of Care Tell Us about the Ethics of Interacting, and Avoiding Unintended Consequences?

Simple summary.

This article is an examination of human–animal interactions in zoos from an ethical perspective, their benefits to both human and animal participants, and also their potential risks and ethical dilemmas. Contact with animals can be beneficial for all parties involved, and can indeed lead to pro-conservation and respect for nature behaviours being adopted by humans after so-called “profound experiences” of connecting or interacting with animals. Yet, human–animal interactions may also increase certain individuals’ desires for inappropriate wild-animal ‘pet’ ownership, and can convey a false sense of acceptability of exploiting animals for “cheap titillation”. Three ethical frameworks that may be beneficial for ethically run zoos to incorporate when considering human–animal interactions are: Compassionate Conservation, Conservation Welfare and Duty of Care. Human–animal interactions in zoos may be acceptable in many circumstances, and may be beneficial to both animal and human participants; however, they must be closely monitored through welfare tracking tools. Melding Duty of Care and the two Conservation ethical frameworks would be ideal for assessing the ethical acceptability of such interactions.

Human–animal interactions (HAIs) in zoos can be rewarding for both humans and animals, but can also be fraught with ethical and welfare perils. Contact with animals can be beneficial for all parties involved, and can indeed lead to pro-conservation and respect for nature behaviours being adopted by humans after so-called “profound experiences” of connecting or interacting with animals. Yet, human–animal interactions may also increase certain individuals’ desires for inappropriate wild-animal ‘pet’ ownership, and can convey a false sense of acceptability of exploiting animals for “cheap titillation”. Indeed, this has been reflected in a recent research review conducted on animal–visitor interactions in zoos from a number of different countries and global regions. These are unintended consequences that ”modern, ethical zoos” would try to minimise, or avoid completely where possible, though most zoos still offer close-contact experiences with their animals. Three ethical frameworks that may be beneficial for ethically run zoos to incorporate when considering human–animal interactions are: Compassionate Conservation, Conservation Welfare and Duty of Care. These three ethical frameworks are concerned with the welfare state and outcomes for individual animals, not just the population or species. Human–animal interactions in zoos may be acceptable in many circumstances and may be beneficial to both animal and human participants; however, they must be closely monitored through welfare tracking tools. The World Association of Zoos and Aquariums (WAZA) has published guidelines for human–animal interactions that are mandatory for member institutions to adhere to, although whether these guidelines are taken as mandatory or suggestions at individual institutions is unknown. Some suggestions for relevant extensions to the guidelines are suggested herein. Melding Duty of Care and the two Conservation ethical frameworks would be ideal for assessing the ethical acceptability of such interactions as they currently occur, and for considering how they should be modified to occur (or not) into the future in zoological settings.

1. Introduction

Human–animal Interactions (HAIs) are common occurrences in zoological institutions, from husbandry practices to interactions with visitors (both regulated and unregulated) [ 1 , 2 ]. Animal–visitor Interactions (AVIs) are often a large component of zoos’ appeal to visitors, and these experiences are also a large component of zoos’ operations and financial viability [ 1 , 3 , 4 ]. It has been estimated that global zoo attendance is over 700 million visitors annually [ 5 ]. Some of these zoo visitors attend purely for entertainment, and/or for direct interactions with animals (for which they are willing to pay) [ 4 , 6 , 7 ]; however, many visitors to modern zoos report considering zoos and aquaria as centres for education [ 8 , 9 , 10 , 11 ]. AVIs may be classified as “direct contact” (such as holding, feeding, brushing or touching experiences) or “indirect contact” (such as visually viewing, gaze-following and/or mimicking through shared enclosure windows, “scattering” food for the animals from a unique vantage point, auditory communication from traditional enclosure perimeters, or the “solving” of combined human–animal input “puzzle walls” installed in some zoo exhibits for “cognitive enrichment” of the enclosure animals). Globally, zoos vary significantly in their offering of direct and indirect contact animal experiences, but almost all zoos surveyed in a 2019 study promoted one or more types of interaction experiences on their public websites [ 4 ]. Yet, these interactions may be at odds with many of the ethical principles upon which “modern, ethical zoos” have built their new moral foundations, and expound their virtues and “social license” [ 1 , 4 , 12 , 13 , 14 ], such as ensuring positive welfare of their captive animals, promoting "natural behaviours", and being compassionate towards individuals as well as populations in their conservation efforts. This article discusses how three prominent ethical frameworks (which are often explicitly or implicitly utilised by zoos) may be used to examine and justify HAIs in zoos (examining interactions with both visitors and with zookeepers), how new guidelines for AVIs published by the World Association of Zoos and Aquariums (WAZA) [ 15 ] perform under these ethical frameworks, and whether the guidelines work in practice alongside the stated missions of some zoological associations and institutions. The three specific ethical frameworks discussed herein are: Compassionate Conservation, Conservation Welfare, and Duty of Care. These three frameworks are not mutually exclusive, although it is suggested here that a deliberate melding of elements and tenets from all three frameworks could make a robust new framework that would be of relevance to zoological institutions. Furthermore, these three frameworks are concerned with the welfare of individual animals, rather than whole populations or ecosystems as most other Conservation or Environmental ethical frameworks are. Many forms of Environmental ethics and Conservation ethics have been espoused over almost the last 100 years [ 16 ], with the collective aim of saving Earth’s last remaining wild and natural places from being paved over by human expansion/exploitation. These ethical frameworks are mostly characterised by a focus on the overall ecosystem health rather than on individual welfare outcomes [ 16 , 17 ]. These ethics have more recently been criticised for perpetuating the status quo of ecosystem or population health always trumping considerations of individual animals’ welfare [ 16 ] (and a lack of empathy for suffering individuals), for sidestepping problematic issues arising from our increasing knowledge of animal consciousness and sentience (and increasing knowledge of harmful anthropogenic impacts) [ 17 ], and for perpetuating the influential, anthropocentric “land ethic” attitude that species conservation is important, yet often only prioritised after human interests (especially where that land, or the animals on it, are of utility or economic benefit to humans) [ 18 , 19 ].

D’Cruze et al. [ 4 ] list five inter-connected goals that many modern zoos and aquaria share: 1. Conservation; 2. Education; 3. Research; 4. Animal welfare; and 5. Entertainment. While many modern facilities place major emphasis only on the first four goals, and shy away from promoting their facilities as places for human entertainment, as mentioned above, many visitors still report entertainment or leisure as their first reason for attending these places [ 4 , 6 , 7 ]. Many zoos and aquaria exist as private, for-profit enterprises, meaning a certain level of revenue is required to remain operational, and then profit is required to financially contribute to their conservation goals. WAZA report conservation as zoos’ core purpose , but their core activity is animal welfare [ 12 ]. Likewise, the American Association of Zoos and Aquariums (AZA) list their mission as “ helping member institutions and animals in their care thrive, through advancing animal welfare, public engagement, and the conservation of wildlife ” [ 20 ]; and the Australasian Zoo and Aquarium Association (ZAA) list saving (conserving) wildlife by inspiring best practice in conservation and (animal) welfare with support from government and community as their strategic mission for member institutions [ 21 ]. Both of these associations detail supporting member institutions’ financial and operational goals as key goals, as well as supporting and facilitating memorable visitor experiences, but they do not list “entertainment” as a key consideration in their strategic documents [ 20 , 21 ]. In fact, most accredited facilities oppose procuring and displaying animals for entertainment purposes, or training animals for “performances”, as part of their new “ecocentric” ethos [ 1 , 14 ]. It is important to note, too, that member institutions pay monetary fees and dues to continue to be members of these self-regulated associations, but the accreditation processes are independent of institutional membership. Accreditation processes with these associations are a benchmarking tool, for monitoring animal welfare standards and meaningful contributions to conservation within individual institutions [ 22 , 23 ]. Whilst human–animal interactions are not discouraged or banned by these associations, strict guidelines and policies around the acceptability of offering these (especially direct) interactions in accredited facilities are being written into modern documentation [ 13 ]. Here, the ethics and the welfare impacts of two types of HAIs shall be discussed: Animal–visitor Interactions; and lesser scrutinised Keeper–Animal Interactions (KAIs) and Relationships (KARs).

2. Human–Animal Interactions

HAIs have been extensively studied in the agricultural/production animal sector [ 24 , 25 ] and the effects of stockperson attitudes and behaviours on the behaviours and productivity of livestock have been well established, and typified in robust models, such as the Hemsworth–Coleman model [ 25 ] based on the psychological theories of reasoned action and planned behaviour [ 26 , 27 ]. Built upon the Hemsworth–Coleman livestock model, there are also a few models of HAIs in zoos, such as the Hosey model [ 28 , 29 ], and the Chiew–Hemsworth model of animal–visitor interactions (published in [ 30 ]). HAI research in zoos has steadily increased over the last few decades [ 14 ]. The results of many studies report mixed welfare effects of human interactions, from negative effects through to neutral and positive effects [ 4 , 14 , 31 , 32 , 33 , 34 , 35 , 36 , 37 , 38 ], and many of the results have been found to be very individual specific. Most studies of zoo HAIs to date have focused on assessing AVIs, and, so far, very few studies have assessed and quantified KAIs or KARs [ 32 ].

3. Animal–Visitor Interactions

There are now quite a few studies that have uncovered negative effects of visitor presence and interactions on captive zoo animal behaviour and welfare, especially when those interactions are in uncontrolled circumstances [ 4 , 34 , 37 , 38 , 39 , 40 , 41 , 42 , 43 , 44 ]. There are also many assumed detrimental (but currently unknown) effects of controlled interactions, such as in provided and promoted animal–visitor “experiences” within zoos, especially with understudied animals such as reptiles (e.g., handled snakes and lizards) [ 4 , 35 , 36 , 38 ]. Often, the current standards of housing conditions for these animals are also inadequate, however, and this is likely to increase or confound detrimental effects of other interactions or welfare-impacting conditions [ 45 , 46 , 47 ]. Although, there are also a number of studies that show that many zoo species are apparently unaffected by visitors and their behaviours, if only viewed from a distance (i.e., no direct physical interactions), and it has been supposed that these animals simply view visitors as a type of expected “environmental variation” [ 32 , 43 , 44 , 48 , 49 , 50 ].

Studies on the positive effects of AVIs are sparse [ 4 ], and are limited to very few species, such as lemurs [ 51 , 52 ], giant tortoises [ 35 , 53 ], and leopard tortoises [ 36 ]; and possible positive effects of visitors for orangutans [ 54 , 55 ] and meerkats [ 49 ]. Despite the dearth of research on positive AVIs, it is suggested here that, as research increases, more positive effects for some individual animals within captive groups (and possibly in some whole groups or populations) will be uncovered. This may further increase as AVIs are undertaken in a more controlled, ethical, and evidence-based manner, prioritising consideration of what the animal wants from the interaction, rather than the human [ 56 ]. When considering individual animal welfare as the ultimate priority for modern, ethical zoos [ 1 , 12 ] (especially those zoos adhering to Compassionate Conservation, Conservation Welfare and/or Duty of Care ethical frameworks), fostering positive AVIs (and positive HAIs in general) is of the utmost importance. There are countless anecdotal stories, passed between zookeeping and animal care staff, that exemplify positive human–animal interactions with animals under their charge. Properly recording and quantifying these relationships, to provide empirical evidence that these relationships are beneficial (or that they are not, in some circumstances) is suggested to be a next step in better understanding captive animals’ wants for, or against, these interactions.

4. Ethical Frameworks

4.1. compassionate conservation.

Compassionate Conservation is an ethical framework that has flourished in the last decade, originally conceived to deal with many “wicked problems” [ 1 ] for individual animal welfare in wildlife management, that traditional Environmental and Conservation ethics could not effectively grapple with [ 16 , 57 ]. This framework has become an explicit ethical alignment within the code of ethics of some zoos, such as Zoos Victoria [ 1 , 58 ], although the framework as used in a pro-zoo manner [ 1 ] differs from the original Compassionate Conservation approach [ 57 ], which was largely concerned with wildlife management, and was generally aligned to anti-captivity principles. While its beginnings were of an in situ wildlife conservation focus, the principles of Compassionate Conservation as applied to ex situ conservation efforts within a captive zoo environment are largely the same [ 1 ]. Compassionate Conservation, in its different iterations, has been described by various proponents as ascribing mostly to a virtue ethic (the virtue of Compassion), a deontological ethic (Animal Rights theories), or to consequentialist ethics (the greatest good for the most number of animals) [ 59 ]. It is obviously a pluralistic approach, focused on the wellbeing of individual wild animals as well as larger populations and ecosystems. The main four tenets of Compassionate Conservation are: 1. First do no harm; 2. Individuals matter; 3. Inclusivity; and 4. Peaceful co-existence (an explanation of these principles is available in [ 59 ]). However, these tenets have also been criticised for a lack of clarity on how the specifics of this ethical framework can be applied to novel or complex dilemmas, such as individual suffering for the benefit of populations or ecosystems [ 59 ].

4.2. Conservation Welfare

A new ethic, Conservation Welfare (predicated mostly upon principles of Singer’s Utilitarianism [ 60 ]), has been proposed as a more legitimate and pragmatic framework for zoos, aquariums and other captive animal conservation organisations to become adherents of [ 59 ]. Conservation Welfare is the recent application of Animal Welfare ethics (and some principles of Conservation and Environmental ethics) to conservation practices for non-captive wild animals [ 59 ]. Like Compassionate Conservation, it differs from most Environmental ethics as it is largely focused on the wellbeing of individual animals, not just whole populations, species or ecosystems. Conservation Welfare, like Animal Rights and Compassionate Conservation, asserts that animals do indeed possess inherent value, meaning they are morally relevant, though the difference in Conservation Welfare is that this inherent value does not preclude the possibility of the imposition of individual suffering or death, if it is necessary and for the “greatest good” (i.e., it can be “traded-off”). Still, this ethic always endeavours to minimise pain and suffering in individual animals. Thus, as applied to in situ and ex situ conservation practices, a Conservation Welfare ethic is more pragmatic than Compassionate Conservation, in that the direct imposition of some suffering on some individuals is deemed acceptable (and this will not violate any tenets) as long as this suffering is necessary and justified . Although, what is deemed necessary, justified suffering is still somewhat ambiguous [ 59 ].

4.3. Duty of Care

The Duty of Care ethical framework (which was initially a humanistic ethical framework for humans caring for humans, then companion animals, and then other domesticated animals) is often an implicitly nurtured approach within zoos, distributed amongst the new generation of animal care managers and husbandry staff, as this ethical framework also promotes a duty to provide positive welfare conditions to captive animals which aligns with modern zoos’ goals. That is, as guardians of captive animals, we have a moral duty to provide all levels of care to those animals [ 61 , 62 ], including the provision of opportunities for animals to have “ a life worth living ” or to be able to thrive in captivity [ 1 , 63 , 64 ]. The duty of care ethic is a reasonable melding of two ethics—a deontological “duty-based” ethic (a moral obligation towards another), and a “virtue-based” care ethic (both active provision of care to others, and internally “caring about” (i.e., consideration for) others) [ 61 , 62 ]. Duty of care as a concept reaches far beyond simply an ethical framework, with “ currency in legal, philosophical, ethical, and general animal protection discourse ” [ 62 ]. As opposed to Conservation and Environmental ethics at large, these three specific ethical frameworks above are all concerned with the welfare of individual animals rather than populations.

5. WAZA Guidelines for AVIs

WAZA have specifically published a set of “ Animal-Visitor Interaction Guidelines ” [ 15 ], based on their 2003 Code of Ethics [ 65 ] and their 2015 Animal Welfare Strategy [ 12 ]. There are six key recommendations for AVI’s listed in the document, with further subsections devoted to recommended procedures to meet these guidelines. The six recommendations are:

Prima facie, these guidelines are sensible and easily interpretable ways for reducing the negative impacts of AVIs on animals. However, individual institutional adherence to these “guidelines” in varying regions may be incomplete, inadequate, or altogether ignored (in favour of financial viability or human experience, for example). Likewise, the auditing of guideline adherence seems to be self-prompted by each individual institution, rather than by a broader regulatory body. Institutional adherence to WAZA and regional association guidelines is largely unknown, or at least reviews are held confidentially. Properly assessing these guidelines would also take an individualistic approach, whereas many zoo facilities often keep “encounter groups” consisting of multiple animals of the same species, and often assess their welfare collectively. Individual welfare assessments are becoming more common globally, especially with the development of specific welfare-monitoring tools (following the Five Domains model), such as WelfareTrak ® (Chicago Zoological Society, Chicago, IL, USA) [ 14 , 66 ]. Other issues include interpretation of specific guidelines. For example, guideline 3 states, “ make no unnecessary demands on animals ”, though, what exactly necessary or unnecessary demands during human interaction encounters are is ambiguous. One of the most important guidelines is number 4—“ provide animals with choice of whether to participate or not ”. Choice and control over their immediate situation are now known to be important for an animal’s overall wellbeing and agency, which can lead to positive welfare states, and these concepts are currently being taught to new generations of zookeepers and animal husbandry professionals as crucial provisions for captive animals wherever possible and pragmatic [ 14 , 67 , 68 ]. It is also suggested that it would be pertinent to add an additional guideline here around safe interaction practices, as follows: “7. Only interactions with non-dangerous animals should be allowed and conducted, and if there is a reasonable chance of harm (even if minimal) to either the human or the animal participants, these interactive experiences should be terminated immediately. ” That is, direct physical contact “experiences” with large predatory animals, such as Tigers, Lions, Bears or Orcas, which could potentially cause serious injury or death to the human participants, should not be offered nor conducted by modern, ethical zoological and aquarium facilities. Currently, many of these offered experiences rely on harmful or abusive training practices, physical restraint, bodily mutilations (such as declawing or teeth removal), and punishments to maintain physical and psychological “control” over these large dangerous animals [ 69 ]. This does not preclude the possibility of beneficial positive HAIs between keepers and these animals, nor in fact between unfamiliar visitors and these animals, but direct contact in these situations is always of the highest risk. It should also be mentioned that most accredited zoological facilities have prohibited abusive and/or bodily mutilation practices in their codes of ethics [ 13 , 15 , 65 ], yet these practices still persist at many eco-tourism or unregulated destinations in many regions [ 69 ].

6. Keeper–Animal Interactions

Currently, AVIs are the focus of much research effort [ 4 , 66 , 70 , 71 ]. However, close examinations of keeper–animal interactions and relationships (KAIs; KARs) are sparse, with a few varying results [ 32 , 55 , 72 , 73 , 74 , 75 ]. Due to the persistence of many “ folklore husbandry ” practices [ 45 ], there is a strong possibility that we are currently ignoring many established negative relationships between zookeepers and animals under their charge [ 32 ]. Although, most modern zoological facilities and (nearly all) animal care professionals endeavour to minimise harmful interventions and to ameliorate possible negative HAIs before they become established negative HARs that would be detrimental to the animal’s overall welfare [ 1 , 75 ]. Furthermore, even though they are often communicated through folklore husbandry, many anecdotal stories and personal experiences (some documented in photographs or short videos) shared broadly over social media can sometimes be beneficial for improving KAIs and KARs in circumstances where objective, empirical evidence is not currently available. Folklore husbandry is a double-edged sword, however, and the established folklore is often very resistant to change even when presented with solid scientific evidence to the contrary [ 45 , 46 ].

To date, specific studies on positive KARs have found the following animal-focused results: increased reproductive success in small cats [ 76 ]; lower faecal glucocorticoid metabolites in clouded leopards [ 77 ], white rhinoceros [ 78 ], and Asiatic and African elephants [ 74 ]; reduced abnormal and stress-related behaviours after positive reinforcement training (PRT) in chimpanzees [ 79 ] and polar bears [ 80 ]; and increased responsiveness to husbandry cues after PRT in black rhinoceros, zebras and Sulawesi macaques [ 81 ]. Similarly, human-focused results found that zookeepers reported stronger, more positive KARs with tortoises that they conducted public-visible training sessions with [ 82 ]; another recent study found that zookeepers’ self-reported job dissatisfaction rose when “Keeper-Elephant Bonds” were weaker [ 74 ]. Apart from Alba et al. [ 82 ], all of these KAI studies have focused on mammalian species. Very little is known about KAIs with other classes of animal. It is strongly suggested that an increase in the empirical investigation of KAIs and KARs is necessary and warranted.

7. Are the Benefits Worth Allowing These Interactions?

As just described above, there are some reported benefits (for both humans and animals) of positive KARs in zoos. There is also marginal evidence to suggest that positive AVIs can be beneficial for the animals involved and documented evidence that these interactions do indeed improve visitor experiences, conservation caring and learning [ 4 , 70 ]. So, is there a good case for allowing and promoting AVIs in zoos? The answer is complicated, but yes. As with all complex dilemmas, the devil is in the details, as it were. Firstly, the guidelines as set out by WAZA, plus the suggested 7th recommendation above, should be closely adhered to, to prevent negative effects of close interactions. However, a new model for clearly identifying when these interactions are being “ asked for ” by captive animals needs to be developed (i.e., being more attentive to what animals actually “ want ”, and aware of how we interpret it [ 56 ]). Interactions that are “asked for” by animals means circumstances where animals have been observed “soliciting” interactions from people, either through glass or other barriers, or by direct contact at shared fence lines (as in the case of the Aldabran Giant Tortoises studied in [ 35 ]). Currently, many zoos have moved towards a highly “hands-off” model of animal keeping, such that most direct contact interactions between humans (both visitors and zookeepers) have been minimised, or totally abolished, and are discouraged as much as possible. Yet, this may be a counter to enhancing the overall welfare of animals in some circumstances, especially in situations where the animals are highly motivated to interact but are denied this rewarding outcome. Sufficient time should be dedicated by animal care managers to allow zookeepers or other staff qualified in animal behaviour to observe daily interaction solicitation or engagement by individual animals under their charge, to identify more opportunities for “ positive affective engagement ” interactions that may currently be overlooked or unnoticed. Furthermore, identifying specific individuals that may benefit from positive KAIs or AVIs should be prioritised by zoos as well. These animals may not always solicit interactions, but other personality factors may be apparent that could predict higher enjoyment of these interactions were they to be offered—factors such as high levels of boldness and curiosity are suggested to be a good starting point for investigation. For human participants, provision of these so-called “ profound experiences ” [ 1 ] in safe, controlled zoo environments can indeed be very beneficial for inciting pro-environmental and pro-conservation behaviour and attitudinal change in visitors, ultimately contributing to the zoos’ conservation goals in meaningful ways [ 3 , 43 , 66 , 83 , 84 ]. “Connecting” with wildlife has been rated as a top priority by zoo visitors, although the type of “connections” that they are seeking can vary significantly [ 71 ].

8. Unintended Consequences

Although AVIs may potentially be rewarding for all parties involved in some circumstances, there are also a number of risks associated with close contact experiences offered within zoos. Obviously, there are a number of health and safety issues for both animal and human participants that are involved in these interactions (especially direct physical contact interactions), some of which have been detailed elsewhere [ 4 , 14 , 69 ]. There is also a growing worry among zoo researchers, managers, educators and behaviour change specialists that providing opportunities to directly interact with animals in zoos may “normalise” the behaviours and promote a false sense of acceptability of engaging in these same behaviours in inappropriate circumstances, such as with wild animals or at unregulated “roadside zoos” and eco-tourism destinations with very poor animal welfare standards [ 4 , 69 , 85 , 86 ]. Interactive experiences that present these animals as “tame” or “cute” may also increase the desire to own these types of animals as exotic pets [ 87 ], and celebrities posing with animals at “roadside zoos” and poorly regulated eco-tourism destinations in social media posts can further normalise this problematic behaviour in unaware members of the public. There is a very real potential that “behavioural spill-over” [ 88 ] could occur after these experiences; thus, approach and interaction behaviours would be attempted by visitors in inappropriate circumstances (such as encounters with animals in the wild), especially because the interaction experienced in the zoo environment is likely to be highly rewarding emotionally and physiologically, leading to an increased motivation to engage in these types of behaviours more often [ 88 ].

Compounding these concerns, the ethical values and beliefs that certain individuals hold about interacting with wildlife may very likely increase the risks of inappropriate or ill-advised behaviours occurring. Historically, zoos were created as displays of imperial majesty—purely for elevating social/cultural status, human awe and entertainment [ 1 , 89 , 90 , 91 ]. Modern zoos are attempting to transform into ethical biodiversity conservation organisations that promote education and positive animal welfare [ 3 , 10 , 11 , 92 , 93 , 94 , 95 ], yet entertainment and leisure are still two commonly reported reasons for attending these destinations by patrons [ 1 , 89 , 90 , 91 ]. Indeed, a zoo visitor survey conducted by the author [ 96 ] found that one of the five extracted ethical alignments of visitors was labelled “ human interaction and entertainment priority ”. Visitors that aligned with this component had high agreement responses on questionnaire items such as “ humans should be allowed to interact with ALL animals in the zoo ”, “ zoo animals are like pets ”, “ zoo animals should be treated like pets ”, and “ I believe that it is acceptable to keep ALL types of animals in zoos ”. Patrons that hold these types of ethical views about interactions with wildlife are likely to be minimally concerned with the animal welfare risks associated with these interactions. They may also be less concerned with evaluating or acknowledging unsatisfactory animal handling and keeping conditions at unregulated, poor-welfare eco-tourism destinations, as their main priority in those moments is their own enjoyment (and they will engage in behaviours that are contrary to their usual moral attitudes) [ 97 ]. To counter this problem, engaging (yet stringent) educational elements must be built into interactive animal experiences offered by zoos, to attempt to change perceptions of these interactions as being harmless enjoyable interactions for all parties involved towards a realistic understanding of how the animals may actually feel about such interactions (and why this matters).

9. What Do the Ethical Frameworks Say?

From a Compassionate Conservation perspective, these types of human–animal interactions would usually be discouraged quite strongly. This is because there are many potential risks of harm to the animals involved (even though minor or non-existent in ideal settings), which would violate the first tenet. The repercussions and undesirable consequences listed above would also likely violate the tenet of peaceful co-existence, as most wild animals would be quite fearful or defensive towards humans approaching them for interactions. Whilst the controlled interactions in zoo environments could be beneficial to fostering pro-environmental attitudes if participants were educated correctly, the inherent risks of direct contact interactions are probably too great to allow. The Conservation Welfare framework would only allow these interactions to occur in very controlled circumstances, but would not completely discourage nor prohibit all of these types of direct interactions. The main principle that would have to be followed, however, is that only those interactions that are “asked” for by the captive animals (not the humans), and could be delivered in an absolutely safe and controlled manner, would be deemed acceptable. Although, uncontrolled HAIs at shared fence lines or through glass viewing windows would likely also be acceptable in circumstances where the animals were initiating or soliciting such interactions. Ergo, if the animal is “asking” for the interaction, and the interaction is deemed safe and minimal or zero risk, then this interaction could be used to increase both the individual animal’s wellbeing and welfare, and conservation caring in humans. Though Conservation Welfare would also be opposed to and concerned about negative “behavioural spill-over” into inappropriate circumstances with wildlife or poor welfare destinations, as this is counted-productive to conservation efforts and to fostering respect for nature. Duty of Care ethics would be mostly concerned with the impacts upon the individual animals within that particular captive environment, so many more HAIs in these circumstances would be deemed acceptable. The main principle followed would be to provide that which is best for the overall welfare for individual animals, and hence allowing and facilitating HAIs and AVIs that are positive and rewarding would be best practice. These interactions would have to be assessed for risks and for safety; however, the framework would only be concerned with the participants as they are in the immediate environment, not what the humans could potentially do in other circumstances or other times outside of the interaction. Therefore, effective communication and education for pro-environmental or conservation caring behavioural change in the human participants would not be considered a priority during these allowed interactions.

10. Conclusions: Promoting Positive Interactions

There are many potential risks inherent in HAIs in all circumstances. However, in specific settings there are also many potential benefits, with the potential to greatly enhance animal welfare conditions and human attitudes towards animal (and natural habitat) conservation and environmental caring. They could potentially be a very powerful tool to increase public awareness, engagement, and support for conservation practices and for achieving the goals of many zoological institutions. However, risks to animal and human participants, as well as the risks of inciting future inappropriate behaviours need to be thoroughly assessed and appropriately mitigated, and all direct HAIs should only be conducted in strictly “very low-risk” scenarios. There is great potential to vastly improve positive affective engagement in animals that are highly motivated to engage in these interactions, providing them with more choice and control over their captive environments [ 64 , 67 , 98 ]. Welfare monitoring tools (such as WelfareTrak ® ) should be utilised during all encounters, and direct behavioural observations from each and every session should be rigorously recorded, to ensure that only animals that are benefitting from interacting are continually used in “encounter programs”. Those animals that display fear, avoidance and/or defensive behaviours before, during, or after encounters should cease being used for these types of close-contact experiences. Behavioural observers must also become much more acutely aware of reptile species’ particular behaviours, as these animals’ full behavioural repertoires are still somewhat unknown [ 38 ]. Likewise, more accurate recognition of unreactive, torpid animals (that may be overwhelmed mentally and physiologically by both acute and chronic stressors) as animals that are not coping with their environments and/or handling must be treated as a priority for relevant behaviourists and animal care staff. Melding Duty of Care and the two Conservation ethical frameworks would be ideal for assessing the ethical acceptability of such interactions as they currently occur, and for considering how they should be modified to occur (or not) into the future in zoological settings.

Acknowledgments

The author wishes to acknowledge the help of Paul Hemsworth in testing and tempering the conceptual, ethical and scientific arguments presented within. The author also wishes to thank Peter Sandøe for honing his argument formulation and philosophical and ethical thinking over the course of his PhD as well as the Animal Welfare Science Students of the University of Melbourne (AWSSUM) graduate student group members for their critiques, comments and support throughout the construction of this paper. This paper represents an ethical chapter of a broader ethical and experimental animal welfare PhD thesis conducted through the Animal Welfare Science Centre, Faculty of Veterinary and Agricultural Sciences, University of Melbourne, Australia. https://www.animalwelfare-science.net/ .

The author was supported by an Australian Government Research Training Program (RTP) merit-based PhD Scholarship.

Conflicts of Interest

The authors declare no conflict of interest.

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Scientists push new paradigm of animal consciousness, saying even insects may be sentient

Bees play by rolling wooden balls — apparently for fun . The cleaner wrasse fish appears to recognize its own visage in an underwater mirror . Octopuses seem to react to anesthetic drugs and will avoid settings where they likely experienced past pain. 

All three of these discoveries came in the last five years — indications that the more scientists test animals, the more they find that many species may have inner lives and be sentient. A surprising range of creatures have shown evidence of conscious thought or experience, including insects, fish and some crustaceans. 

That has prompted a group of top researchers on animal cognition to publish a new pronouncement that they hope will transform how scientists and society view — and care — for animals. 

Nearly 40 researchers signed “ The New York Declaration on Animal Consciousness ,” which was first presented at a conference at New York University on Friday morning. It marks a pivotal moment, as a flood of research on animal cognition collides with debates over how various species ought to be treated. 

The declaration says there is “strong scientific support” that birds and mammals have conscious experience, and a “realistic possibility” of consciousness for all vertebrates — including reptiles, amphibians and fish. That possibility extends to many creatures without backbones, it adds, such as insects, decapod crustaceans (including crabs and lobsters) and cephalopod mollusks, like squid, octopus and cuttlefish.

“When there is a realistic possibility of conscious experience in an animal, it is irresponsible to ignore that possibility in decisions affecting that animal,” the declaration says. “We should consider welfare risks and use the evidence to inform our responses to these risks.” 

Jonathan Birch, a professor of philosophy at the London School of Economics and a principal investigator on the Foundations of Animal Sentience project, is among the declaration’s signatories. Whereas many scientists in the past assumed that questions about animal consciousness were unanswerable, he said, the declaration shows his field is moving in a new direction. 

“This has been a very exciting 10 years for the study of animal minds,” Birch said. “People are daring to go there in a way they didn’t before and to entertain the possibility that animals like bees and octopuses and cuttlefish might have some form of conscious experience.”

From 'automata' to sentient

There is not a standard definition for animal sentience or consciousness, but generally the terms denote an ability to have subjective experiences: to sense and map the outside world, to have capacity for feelings like joy or pain. In some cases, it can mean that animals possess a level of self-awareness. 

In that sense, the new declaration bucks years of historical science orthodoxy. In the 17th century, the French philosopher René Descartes argued that animals were merely “material automata” — lacking souls or consciousness.

Descartes believed that animals “can’t feel or can’t suffer,” said Rajesh Reddy, an assistant professor and director of the animal law program at Lewis & Clark College. “To feel compassion for them, or empathy for them, was somewhat silly or anthropomorphizing.” 

In the early 20th century, prominent behavioral psychologists promoted the idea that science should only study observable behavior in animals, rather than emotions or subjective experiences . But beginning in the 1960s, scientists started to reconsider. Research began to focus on animal cognition, primarily among other primates. 

Birch said the new declaration attempts to “crystallize a new emerging consensus that rejects the view of 100 years ago that we have no way of studying these questions scientifically.” 

Indeed, a surge of recent findings underpin the new declaration. Scientists are developing new cognition tests and trying pre-existing tests on a wider range of species, with some surprises. 

Take, for example, the mirror-mark test, which scientists sometimes use to see if an animal recognizes itself. 

In a series of studies, the cleaner wrasse fish seemed to pass the test . 

The fish were placed in a tank with a covered mirror, to which they exhibited no unusual reaction. But after the cover was lifted, seven of 10 fish launched attacks toward the mirror, signaling they likely interpreted the image as a rival fish. 

After several days, the fish settled down and tried odd behaviors in front of the mirror, like swimming upside down, which had not been observed in the species before. Later, some appeared to spend an unusual amount of time in front of the mirror, examining their bodies. Researchers then marked the fish with a brown splotch under the skin, intended to resemble a parasite. Some fish tried to rub the mark off. 

“The sequence of steps that you would only ever have imagined seeing with an incredibly intelligent animal like a chimpanzee or a dolphin, they see in the cleaner wrasse,” Birch said. “No one in a million years would have expected tiny fish to pass this test.”

In other studies, researchers found that zebrafish showed signs of curiosity when new objects were introduced into their tanks and that cuttlefish could remember things they saw or smelled . One experiment created stress for crayfish by electrically shocking them , then gave them anti-anxiety drugs used in humans. The drugs appeared to restore their usual behavior.

Birch said these experiments are part of an expansion of animal consciousness research over the past 10 to 15 years. “We can have this much broader canvas where we’re studying it in a very wide range of animals and not just mammals and birds, but also invertebrates like octopuses, cuttlefish,” he said. “And even increasingly, people are talking about this idea in relation to insects.”

As more and more species show these types of signs, Reddy said, researchers might soon need to reframe their line of inquiry altogether: “Scientists are being forced to reckon with this larger question — not which animals are sentient, but which animals aren’t?” 

New legal horizons

Scientists’ changing understanding of animal sentience could have implications for U.S. law, which does not classify animals as sentient on a federal level, according to Reddy. Instead, laws pertaining to animals focus primarily on conservation, agriculture or their treatment by zoos, research laboratories and pet retailers.

“The law is a very slow moving vehicle and it really follows societal views on a lot of these issues,” Reddy said. “This declaration, and other means of getting the public to appreciate that animals are not just biological automatons, can create a groundswell of support for raising protections.” 

State laws vary widely. A decade ago, Oregon passed a law recognizing animals as sentient and capable of feeling pain, stress and fear, which Reddy said has formed the bedrock of progressive judicial opinions in the state.  

Meanwhile, Washington and California are among several states where lawmakers this year have considered bans on octopus farming, a species for which scientists have found strong evidence of sentience. 

British law was recently amended to consider octopuses sentient beings — along with crabs and lobsters .

“Once you recognize animals as sentient, the concept of humane slaughter starts to matter, and you need to make sure that the sort of methods you’re using on them are humane,” Birch said. “In the case of crabs and lobsters, there are pretty inhumane methods, like dropping them into pans of boiling water, that are very commonly used.”

Evan Bush is a science reporter for NBC News. He can be reached at [email protected].

Zoo animals got quiet, exhibited nighttime behavior during total solar eclipse

S cientists and zookeepers watched Monday as giraffes, gorillas, lions, macaws and flamingoes exhibited unusual behavior during the total solar eclipse . 

Because total eclipses happen so infrequently , researchers don't know much about how they impact animals. They studied animals on Monday at several zoos situated along the eclipse path of totality , such as the Fort Worth Zoo in Texas. Animals were largely calm at the Fort Worth Zoo, though some, including the gorillas, lions and lemurs, showed increased signs of vigilance and curiosity. 

"Most importantly, we did not observe any signs of increased anxiety or nervous behaviors," a Fort Worth Zoo spokesperson said. "And by the time totality had passed, things went back to normal, almost immediately!"

Several animals at the Fort Worth Zoo made their way toward their barn doors, which is where they go at night, as the skies darkened during the eclipse, the zoo spokesperson said. The Aldabra tortoises, giraffes, elephants, kudu, bonobos, coatis and gorillas all headed toward their barns. 

Zoos were also able to observe some unique daytime behavior from nocturnal animals. At the Fort Worth Zoo, a ringtail cat and two owl species showed increased activity during the day.

Also in Texas, zookeepers at the Dallas Zoo saw giraffes and zebras run around during the eclipse. Chimpanzees patrolled the outer edge of their habitat at the zoo while all but one of a bachelor group of gorillas went to the door they use to go in at night. 

An ostrich at the Dallas Zoo laid an egg during the eclipse. Other birds got louder before totality, then went silent. Flamingos and penguins huddled together. 

Birds also showed unique behavior at the Indianapolis Zoo, a zoo spokesperson said. Macaws, budgies and other birds got quiet and roosted up high, which is nighttime behavior.

"You can hear they're totally silent now - not a peep, and no movement," Indianapolis Zoo President and CEO Dr. Robert Shumake said in a video recorded during totality. 

Flamingos at the zoo huddled together and also got quiet. Cheetahs and a warthog displayed behavior normally seen during the evening. The cheetahs paced at the highest point of their grassy yard during the eclipse while a warthog waited at its back gate. 

At the Philadelphia Zoo, which was not on the path of totality, visitors observed the animals during the partial eclipse, CBS Philadelphia reported. Visitors were able to sign up with zoo staff, pick an animal to observe and use their phones to track behavior before, during and after the eclipse. Most of the zoo's animals seemed pretty unfazed by the partial eclipse.

Researchers also studied zoo animals during the 2017 solar eclipse . In a study published in 2020, researchers noted they'd reviewed the behavior of 17 species — mammals, birds and reptiles — at the Riverbanks Zoo in Columbia, South Carolina, during the eclipse. They said around 75% of species showed a change of some sort in response to the eclipse. They largely exhibited behaviors usually seen in the evening or at night, with some animals showing signs of anxiety.

Zookeepers and researchers in the U.S. won't get a chance to do this kind of research during a total eclipse again until 2044 , when the next total eclipse in the contiguous U.S. will happen. Just three states are on the path of totality for the Aug. 23, 2044 eclipse, according to  The Planetary Society .

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It’s a Bronx tail.

For 125 years, the Bronx Zoo has dazzled and inspired visitors with exotic and beautiful creatures like gorillas and tigers and lemurs — oh, my!

“Guests love to see the care, the dedication and the passion that our staff have for making sure that these animals were well cared for,” Jim Breheny, director of the Bronx Zoo and a Throggs Neck native, 64, told The Post.

“There’s the connection and the bond they have between each other.”

In honor of the quasquicentennial jubilee, the Bronx Zoo is rolling out a new quarter-mile walking trail of beastly art on Saturday called Animal Chronicles, which features 13 unique environmental scenes, 68 sculptures of critters and more artistic nods to the zoo’s illustrious history in animal rescue.

“It’s just amazing, you know?” Breheny said. “People say you can learn something from talking to anybody. It’s the same thing here. You can learn something from interacting with any animal.”

He’s enjoyed this unique connection firsthand for quite some time: Breheny has been at the zoo for 51 years, starting with a role at the children’s zoo when he was 14 in the early 1970s. As a young animal lover, Breheny admitted he simply filled out a form, made a call and was hired.

“No, I never thought I would be in this position,” he joked of his current job title.

Mane attraction

During his five decades on the job, Breheny has interacted with all of the zoo’s creatures, including working the camel rides in his early years. However, some of the wildest stories with the animals happened outside the confines of the zoo — but still on the job.

In 2003, Breheny, who has a graduate degree in biology from Fordham, was attending a speech on responsible pet ownership when, ironically, he was summoned to yank a tiger illegally kept inside a Harlem apartment.

“I honestly didn’t believe it. I thought it would be like an ocelot or a bobcat,” he recalled. “People exaggerate all the time.”

It turned out to be Ming, the infamous “fully grown” tiger who “took up the entire apartment,” and Breheny and his team were responsible for getting the tiger out of the apartment. It took two doses of sedatives to knock the big guy out.

While the Ming rescue has been the most adrenaline-pumping incident of Breheny’s tenure, there were other eventful incidents involving “venomous snakes” over the years, too.

Around 2005, Breheny had been in talks with the Pakistani government to obtain Leo, a rare snow leopard who brought new genetics into the species population.

“His genetic contribution through breeding was really important to the snow leopard population in North America,” said Breheny, who noted cubs of a few generations past are currently on display.

Numerous animal inhabitants also evolved into celebrity attractions at the Fordham Road institution, going all the way back to the 1903 snow leopard attraction, North America’s first showcasing of the species.

In 1990, Rapunzel the Sumatran rhinoceros — a currently endangered species — was a fan favorite until her death in 2005.

Breheny most remembers her “easy-going” demeanor and as a “great animal.”

There was also Pattycake, the first gorilla born in NYC. In 1972, she was born in the Central Park Zoo, but broke her arm young and was transferred to the Bronx Zoo. She became an incredibly important permanent resident in the early 1980s before she died at 40 in 2013.

“That was the first gorilla that we raised. She was certainly a charismatic animal,” Breheny said.

“We learned how much infant gorillas are like infant humans.”

As the majestic gorilla grew, integrated and bred, she also was one of the first to start painting. Breheny has one of her final works inside his office.

Born to be wild

Since 1899, the zoo — a haven for alligators, lemurs, penguins, poison dart frogs and more from around the world — has blazed a trail in the field of animal care.

“One of the biggest advancements I’ve seen is how the animals and staff interact through advances in behavioral enrichment and training,” said Breheny.

He added that while years ago, animals would have to be put under anesthetic for blood work tests, now trained workers are able to safely collect samples while the patients are fully conscious.

Even with big cats, picking up their tail to draw blood can be safely executed. \

Initiatives like this began in 1901. While still in its infancy, the zoo launched the first American veterinary program in a zoological park, which evolved into a full-on animal hospital in 1916.

More so, the beastly oasis, first called the New York Zoological Park, was intentionally created to play a pivotal role in preservation — a stark contrast to what the nation had seen at the 19th century’s turn. The tourism magnet was a happy coincidence.

“When they were planning the zoo around 1895, everyone in America still had the idea, ‘This is just another circus-type of thing,’ ” Angel Hernandez, the official historian of the Bronx Borough President’s Office, told The Post.

“There was no place to study the animals, their habitats and the countries they originated from,” Hernandez said. “So the idea was that the New York Zoological Park was to be innovative and to address these issues — and to give more animals space.”

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