The modern zoo’s roles command empirical enquiry to determine the effectiveness of zoos locally and globally. Ten years ago, published work identified the need for empirical research on a diverse range of species beyond charismatic zoo megafauna. We review zoo-based research published in the decade since this original recommendation. We collectively evaluate zoo-themed research papers from those working in zoos and those external to zoos but studying zoo-housed animals. By systematically searching Web of Science© for zoo-based research and performing inductive content analysis to code year, journal, study animal’s taxonomic classification, and research aims and outputs we evaluate trends in zoo-themed research, contrasted with trends in species holding. Significantly more birds and fish are kept compared to mammals, reptiles and amphibians, but mammals are consistently the primary research focus. Whilst output generally rises, only for birds is a steady increase in publications apparent. Husbandry evaluation is a major aim/output, but papers on pure biology, cognition and health also feature. Most publications lead to “specific advancement of knowledge” including validation of methodologies. We show that: (1) trends in species holdings are unrelated to trends in publication; (2) zoo-themed research makes meaningful contributions to science; (3) zoo researchers should diversify their aim/output categories and chosen study species to close the persisting research gaps that we have identified. Finally, we discuss our findings in the context of evident species biases within research outputs across the broader fields of zoology, conservation and ecology.
Zoos and aquariums have the potential to be excellent locations to develop, implement and complete scientific research. Zoo populations enable hypothesis-driven questions to be answered on species/topics that would be challenging in the wild. This is evidenced by, for example, ground-breaking insights into the reproductive biology of the critically endangered Sumatran rhinoceros, Dicerorhinus sumatrensis (Roth et al., 2004) or results on the energetic costs of locomotion in bears, Ursidae (Pagano et al., 2018). Zoological databases that hold information on species’ biology can enhance the scientific literature on natural history and ecology (Conde et al., 2019); information that also informs animal management practices and species conservation strategies both in-situ and ex-situ. As centres for both pure and applied science, the output from zoological collections not only covers a range of disciplines (Loh et al. 2018) but is of increasing value to multiple stakeholders working in all parts of the world with all taxonomic groups.
The four aims of the modern zoo—conservation, education, research and recreation (Mason, 2007, Fernandez et al., 2009) provide a framework for scientific investigation. The importance of research to the modern zoo is reflected in the number of pieces of national zoo legislation that require research activities to be conducted (Hosey et al., 2009). Conversely, entertainment is perceived as the least important role of the zoo (Reade and Waran, 1996), yet visitation must be maintained as zoos can be reliant on entrance fees for income. This income provides a means for zoos to fulfil their roles in conservation and education, hence zoos must remain attractive destinations to visit (Bueddefeld and Van Winkle, 2018). Research into the educational role of the zoo has scrutinised the effectiveness of zoos as learning environments (Marino et al., 2010, Dawson and Jensen, 2011, Moss and Esson, 2013). Despite an increase in zoo visitor studies over the past decade (Jensen, 2010, Moss and Esson, 2010), there is little evidence that zoos promote understanding or pro-conservation behaviour. The importance of robust experimental design and application of “good science” is also evident in literature (Wagoner and Jensen, 2010, Moss et al., 2017) promoting the need for an evidence-based approach.
Such an evidence-based approach extends to animal husbandry, central to which is researching animal behaviour. A majority of zoo scientific studies has previously been shown to be of a behavioural nature (Hosey, 1997). The relevance of behavioural science to conservation outcomes was postulated by Sutherland (1998) who states the importance of conserving behaviour as part of conservation objectives. A potential fifth aim of the zoo, to promote excellence in animal welfare (Fernandez et al., 2009) further supports the need to increase the amount of scientific study and application of such study, into zoo animal management. An increasingly ethically-aware public, who focus on the importance of good welfare and are not just concerned with animal cruelty (Whitham and Wielebnowski, 2013) emphasises the need for zoos to manage their populations to ensure a high quality of life can be attained and maintained for all individuals.
As scientific research that collects data to answer an hypothesis-driven question is key to ensuring husbandry regimes are most appropriate, zoos have invested in collaboration with academics (Fernandez and Timberlake, 2008), in the development of research methodologies (Plowman, 2003, Plowman, 2008) and in the creation of research-focussed committees and working groups (BIAZA, 2018b) to increase and develop their scientific output and its uptake by zoological collections. By expanding on how empirical research is applied within zoological collections (e.g., to husbandry routines, visitor engagement and interpretation objectives, or population management goals) the reach, impact and outcome of each of the zoo’s aims is strengthened.
With a new focus on collection planning for population sustainability (Traylor-Holzer et al., 2019), a paucity of scientific research for many familiar (i.e., commonly-kept, often-seen-in-the-zoo) species has been apparent (Melfi, 2009). This paper (Melfi, 2009) shows that researchers study a limited number of individuals of high-profile, charismatic species—a trend previously noted in the wider field of “wildlife research” (Bautista and Pantoja, 2005). Species less appealing to the public but housed in greater numbers across more zoological collections have been ignored. Likewise, when considering species responses to captivity, mammals are often focal subjects (Clubb and Mason, 2003) and ecological data are used to inform our understanding of their responses to captivity (Mason, 2010, Kroshko et al., 2016). However, for other non-mammalian taxa we consider how they cope with the human-created environment of the zoo less often (Carere et al., 2011). Species with a long history of captivity, well-known and recognisable to the visiting public can still challenge us regarding their optimal captive care (Hatt et al., 2005, Rose, 2018) and empirical, structured research programmes can help redress the balance between what a species needs to thrive and what is provided for survival in the zoo. Therefore, to move forward with species-specific Best Practice (husbandry) Guidelines (EAZA, 2019) less considered taxa, common but “ignored” species or animals perceived as less charismatic, e.g., reptiles, amphibians, fish and invertebrates, (BIAZA, 2018a) need to be the focus of future research attention. Melfi (2009) highlights this lack of research into non-mammals as the cause of anecdote or “rules of thumb” methods of providing captive care.
As such, the aim of our paper was to look retrospectively from 2009 to 2018 to see how much more scientific research has been conducted into the areas identified by Melfi (2009) as lacking a research focus. Specifically, we collected research papers from five different taxonomic groups, to evaluate the range of taxa now included in scientific publications and we investigated if/how uptake and output of evidence, useful for management, has diversified. We used Melfi (2009)’s Table 1 (page 581) and Fig. 2 (page 582) as a guide to what constitutes “forgotten taxa”—focussing on those animals with large populations but limited scientific investigation. We have added invertebrates, amphibians and fish to our analysis that were excluded or not fully included in the original Melfi paper for reasons outlined below. Melfi (2009)’s Fig. 2 shows the relationship between the number of individuals of specific animal species held by British and Irish association (BIAZA) zoos, as well as the number of zoos that hold each represented species, compared to the number of projects conducted on these species, based on records from the BIAZA research database. A bias towards the study of a small number of charismatic mammalian species, for example chimpanzees (Pan troglyodytes), bonobos (P. paniscus), orangutans (Pongo sp.), elephants (Elephas maximus, Loxodonta africana), is clear from this figure. Melfi notes that more projects between 1998 and 2008 were conducted on the two species of Pan compared to all projects on birds, reptiles, amphibians, fish and invertebrates in this sample of BIAZA institutions—90 against 84 studies. We aim to see if such a bias exists in a sample of wider zoo output in the ten years from this dataset being published.