The relationship between humans and nondomestic captive animals has continuously evolved over time. This has coincided with a shift in attitudes from early civilizations, which maintained captive animals for food, work, and entertainment [14]. The origins of animal collections are not well documented, but the first successful attempts to capture and keep native wild animals likely occurred around 10,000_B.C. [2]. Early collections were typically utilitarian and, in fact, began the process of domestication for many species. Yet, some captured animals curiously remained untamed and became early precursors for entertainment-oriented wild animal collections [2]. Between 3000_B.C. and 1456_A.D., civilizations in Egypt, Mesopotamia, China, and India began commonly capturing wild animals for their extraneous collections [15,16]. The difficulty in capturing and showcasing live animals increased their desirability among rulers and other exclusive classes, and wild animal collections began replacing ornamental plant collections in popularity. The practice soon spread throughout regions of Asia, Europe, and the Americas [2]. Moreover, the explosive expansion of intercontinental trade throughout the 15th and 16th centuries resulted in a greater influx of non-native captured animals to these regions. These unfamiliar animals became known as exotique, a French term for objects from distant lands, and were popular trade items [17]. In Europe, large exotic animal collections of monarchs and nobles became known as menageries or seraglios [18]. These exclusive collections were often maintained as proof of the owners’ wealth, power, and access to global trade [17]. Rare animals from these collections made popular gifts among affluent members of Renaissance era societies, which gave rise to a robust trade industry [2,19]. In the Ottoman Empire, smaller groups of well-trained animals were used in traveling menageries, which became the predecessors to circuses [20]. These traveling shows were still exclusive, and opportunities for members of lower classes to witness these animals was typically limited to those in transit, either for trade or as part of a traveling menagerie [18].

The modernization of zoos can be attributed to the combination of better-informed societal attitudes towards animals and advancements in zoo design and management practices [21]. Over time, the purpose of wild animal collections expanded beyond entertainment and status symbols [22]. Collections became platforms to educate the public and advocate for natural resources, ethical human–animal interactions, and healthy wild animal populations [19]. The European Age of Enlightenment throughout the 17th and 18th centuries brought new perspectives regarding interactions with animals in the wild and in collections [2]. Scholars studying the natural world began to better understand the behavioral and anatomical attributes of different classifications of wild animals. Their scientific curiosity led to the realization that zoological gardens were ideal for studying wild animal species, as they could be safely observed, studied, and appreciated for their unique characteristics. The resulting surge of new information sparked a shift in societal attitudes regarding the purpose of animal collections [2]. Slowly, zoological gardens began to combine the entertainment value of menageries with new scientific and educational objectives. Accessibility for commoners increased during the 18th century as admission became more affordable, often costing only the donation of a food item for the animals [23,24]. Traveling menageries brought animals to new locations and new audiences, which further piqued public interest [2]. The slow but revolutionary transition from the recreational spirit of menageries to the science of zoological gardens, or zoos, was reflected in several practices at the earliest institutions [2]. For example, menageries typically displayed animals in long rows of barred cages, which was typically not ideal for animal comfort but best facilitated the logistics of group entertainment [2,25,26,27,28]. Modern zoos instead began to design naturalistic exhibits based on species-specific ecology, which increased animal comfort and allowed study within a more natural setting [2,25,26,27,28]. Staff began receiving training to increase their relevant knowledge, and programs for education, research, and conservation became commonplace [29]. A noteworthy turning point occurred when Empress Maria Theresa marked her succession of Emperor Francis I by transforming Vienna’s once-exclusive Imperial Menagerie into the Tiergarten Schönbrunn (Schönbrunn Zoo). This transformation, which was completed in 1752, opened the doors of the formerly private establishment to the public [17,30]. The Tiergarten Schönbrunn, now recognized as the world’s oldest operating public zoo, became a template for additional public zoos, including Madrid’s Retiro Parque de Buen Retiro (Park of the Pleasant Retreat or Royal Park) and Paris’ Menagerie du Jardin des Plantes (Menagerie of the Garden of Plants) near the end of the 18th century [16,24]. By the early 19th century, science, public education, and animal advocacy had become central objectives for many public zoos. The London Zoo in Regent’s Park was perhaps the first to fully embody this paradigm. It was founded in 1828 by the Zoological Society of London to promote the global conservation of animals and their habitats [17,31]. The London Zoo’s innovative model and design influenced subsequent institutions, including New York’s Central Park Zoo (1860) and the Philadelphia Zoo (1874) in the US [2].

The early 20th century brought about infrastructural advancements that helped transform and standardize zoo approaches to better align with modern ideals. In 1907, German wildlife merchant Carl Hagenbeck revolutionized zoo architecture by designing a bar-free facility in Hamburg [24]. Zoos began housing large terrestrial mammals in moat-confined enclosures, a design that better emulated natural habitats and created a more comfortable space between animals and visitors [24]. Traditional cage-style enclosures were used for smaller arboreal species, where appropriate propping could be more easily utilized to simulate natural environments [24]. By 1935, naturalistic enclosures had evolved into wildlife parks, where animals roamed over expansive areas of land and could be observed by visitors in safari-like encounters [32]. Architectural advancements coincided with the establishment of organizations that provided oversight, facilitated information sharing, and offered uniform guidance for captive animal care. In 1924, the role of US zoos and public aquariums in species conservation, publication education, and science was formalized with the founding of the Association of Zoos and Aquariums (AZA) [33]. AZA is a nonprofit organization that collects and disseminates information regarding animal care, population genetics, and species expertise. It also performs inspections and offers an institutional accreditation program in animal care and welfare. Organizations like the European Association of Zoos and Aquaria (EAZA), the Zoo and Aquarium Association (ZAA; Australia), and the South East Asian Zoos Association (SEAZA) fulfill comparable roles in other regions of the globe. The World Association of Zoos and Aquariums (WAZA), which has existed under several names since 1935, is a global alliance of regional and national entities (including the AZA, EAZA, ZAA, and SEAZA) with similar objectives applied on a worldwide scale [34]. In 1948, the International Union for Conservation of Nature (IUCN) was created to gather information regarding the impact of human activity on nature [34]. Although not directly involved in conservation initiatives, the analyses provided by the IUCN help to direct the efforts of relevant organizations.

Despite the growing interest in zoo animal welfare, some aspects have progressed slowly [26]. Although prioritized by modern zoos, animal welfare is not singularly defined. It is generally agreed, however, that welfare considerations include the range of physical, behavioral, and psychological components that constitute an animal’s life experiences and impact how it perceives and interacts with its environment [8,11,36]. When welfare is managed properly, the animal is healthy, well nourished, able to express innate behaviors, and experiences more positive than negative affective states [11]. Productive welfare management can require extensive efforts and investments like new construction or the transfer of animals to new locations. It may also be as simple as providing an animal with the option to move further away from zoo visitors or to choose the terrain on which to rest (Figure 1). Behavioral outcomes related to welfare management were first described by Swiss Zoo Director Heini Hediger in the early 1950s when he began studying how enclosure designs could best accommodate variable factors like flight zones [37]. Among his seminal findings was that perceived safety was the primary concern for most wildlife and far exceeded their interests in pursuing mates or even food. This type of new information allowed enclosures to be designed for more efficient space utilization [26]. Hediger was also among the first to combine elements of psychology, ecology, and pathology in his research in an approach later designated as zoo biology [38]. As zoo animal research has expanded, regulatory oversight has adjusted in kind. The Laboratory Animal Welfare Act (1966) was expanded in 1970 to include warm-blooded animals used for exhibit, which covered essentially all mammals, marsupials, and birds housed in zoos [26]. In 1971, the AZA appointed a standing committee to determine the best practices for the care of zoo species. By 1974, the first institutions were accredited by the AZA through a voluntary process that later became mandatory for AZA membership [33]. Today, AZA accreditation helps to communicate expectations for welfare management and holds member institutions accountable when expectations are not met. Importantly, it also provides an avenue for zoos to formally demonstrate accountability to the community and other stakeholders [26,39].