Introduction
Over 26 500 known and evaluated species are at risk of extinction worldwide at various levels and time scales (
IUCN 2018), and biodiversity losses and extinction rates have increased considerably because of the widespread degradation of global ecosystems caused by humans (
Johnson et al. 2017). The conservation of these species often requires that many organizations and institutions work together. Zoos and aquariums are becoming increasingly involved in the conservation of species at risk (
Hutchins and Smith 2003). The World Association of Zoos and Aquariums (WAZA) is a global organization of zoos and aquariums that aims to promote cooperation among its members (
waza.org). WAZA has helped develop the World Zoo Conservation Strategy that encourages zoological institutions to participate in biodiversity conservation efforts as well as providing guidance on how to reach these goals (
IUDZG and CBSG 1993). Canada’s Accredited Zoos and Aquariums (CAZA) is a nonprofit organization founded in 1974 (
caza.ca) that currently has 30 institutional members. CAZA states that zoos and aquariums play a critical role in preserving biodiversity, and this is reflected in their accreditation standards that ensure high-quality animal care, education, and research at their institutions. CAZA maintains these standards through its inspections and policies and protocols.
CAZA members participate in Species Survival Programs and captive breeding and reintroduction programs, while also collaborating with government and nongovernment organizations to preserve species in Canada and abroad (
Galbraith and Rapley 2005). However, quantifying the contribution of zoos and aquariums to conservation-related activities is extremely difficult (
Ferraro and Pattanayak 2006;
Loh et al. 2018). Research productivity in the form of peer-reviewed publications has been used to systematically quantify this contribution for members of the Association of Zoos and Aquariums (AZA), CAZA’s counterpart in the United States (
Loh et al. 2018). Peer-reviewed publications are important contributions to scientific knowledge that can be shared with other practitioners and thus aid in the formulation of informed conservation management decisions (
Loh et al. 2018). However, not all conservation-relevant research will result in peer-reviewed publications, but research productivity of zoos and aquariums can still be related to overall conservation activity, as has been done for universities (
Grant et al. 2007;
Loh et al. 2018). Thus, research productivity provides a foundation with which to assess the conservation contributions of these organizations.
Participating in research is mandated by CAZA for a zoo or aquarium to obtain and maintain accreditation (
CAZA 2008). However, for Canadian zoos and aquariums, few studies have explored their contribution to biodiversity conservation efforts and research productivity in general.
Olive and Jansen (2017) conducted interviews of CAZA’s four largest and oldest zoos, and determined they were all involved in hands-on conservation programs.
Galbraith and Rapley (2005) used surveys to provide insight into the role of research at CAZA institutions, but received only eight responses. The responses received indicated that research was prevalent at the majority of these institutions (
Galbraith and Rapley 2005). Although these studies attempted to quantify the roles conservation and research play at CAZA institutions, the scope of their analysis was limited. To our knowledge, no one has yet quantified the contribution of CAZA organizations to biodiversity conservation efforts in a systematic manner. Understanding patterns of research productivity among CAZA members is important for understanding the contributions zoos and aquariums bring to conservation at large, and this information could be important for CAZA and its members in their strategic planning to identify areas for investment in their programs.
We used research productivity (defined as the number of peer-reviewed publications) to characterize the contribution of Canadian zoos and aquariums to scientific discovery, with a specific focus on publications relevant to biodiversity conservation, in the same manner as
Loh et al. (2018). We use the term “publications” when referring to peer-reviewed publications. Hence, we quantified the number of publications produced by CAZA members, as well as determined the journal outlets and subject areas of these publications. We expected that the number of publications produced by CAZA members would increase over time because of the contemporary transition of zoos and aquariums from sources of entertainment to science centers (
Hutchins and Smith 2003) and that inter-organizational variation between institutions will affect the magnitude of publications produced by each member. These organizational factors include age, organization type, organization size, and the inclusion of the term research in the organization’s mission statement. We expected that older and financially larger institutions would publish more because of their greater resources relative to younger and smaller zoos and aquariums. We also expected nonprofit organizations and those that include research in their mission statement to publish more, as these factors are indicative of an environment that prioritizes research (
Loh et al. 2018). We expected that generally CAZA members would produce fewer publications than their AZA counterparts because the AZA has older and larger institutions than CAZA. Likewise, we expected that CAZA members would produce fewer publications related to biodiversity conservation than AZA members because of the relatively large number of AZA members that have research institutes devoted to conservation (e.g., Smithsonian Conservation Biology Institute, San Diego Zoo Institute for Conservation, Lincoln Park Zoo’s Conservation & Science Department) compared with what is found in Canada.
Discussion
The total number of publications produced by CAZA members increased significantly over time, demonstrating that CAZA members are increasingly participating in research, as per the mandate of CAZA. This increase in CAZA research productivity is not simply a correlate of the general increase in peer-reviewed publications at large. The subject areas and journals that CAZA members published in most often demonstrated a strong research focus on the veterinary sciences, with only a small proportion of biodiversity conservation publications produced (6.12%). In addition, the journals that most publications appeared in (
Journal of Zoo and Wildlife Medicine and
Zoo Biology) are specialist journals with readership predominantly limited to the zoo community, indicating that scientific discourse is primarily among zoo and aquarium personnel (
Lawson et al. 2008;
Loh et al. 2018).
Karesh and Cook (1995) argued that veterinary science can be integrated into conservation projects to assess and monitor the health of wild populations, train others how to properly handle wildlife, and to evaluate the success of these projects. Nonetheless, zoos and aquariums may consider publishing in journals with a wider audience base to facilitate knowledge sharing among various organizations, specifically those engaged in biodiversity conservation (
Loh et al. 2018). The number of publications in biodiversity conservation has increased substantially in the last 4 years, from 13 publications in 2013 to 33 in 2017. This suggests that zoos and aquariums are increasing their engagement in biodiversity conservation research, as has been the goal of WAZA (
IUDZG and CBSG 1993). Anecdotal information suggests that CAZA members are hiring increasing numbers of permanent conservation scientists, so this upward trend in publication rates is expected to continue and may explain differences in the proportion of publications in the subject areas of veterinary sciences and biodiversity conservation.
We also examined the organizational factors that contributed to research productivity of CAZA members. Organization type was not a significant predictor of research productivity, which was contrary to our expectations and inconsistent with AZA members (
Loh et al. 2018). We expected nonprofit organizations to publish the most because of institutional attitudes that tend to value biodiversity conservation at these organizations (
Loh et al. 2018). However, there were no significant differences among organization types. This could be due to the relatively low number of publications overall, making it difficult to detect differences. Consistent with
Loh et al. (2018), both mission statement and age significantly affected publications produced. Organizations with research-affiliated terms in their mission statement published more than those without, and age was positively related to the number of publications produced. Mission statements that pledged to contribute to scientific knowledge may be an indicator of organizational attitudes that prioritize and value research (
Loh et al. 2018). Older organizations have had more time to acquire resources, such as money, partnerships, and community engagement, allowing them the flexibility to conduct more research. It can also be postulated that older organizations would be able to acquire more expertise within their staff.
In the analysis of nonprofit organizations, larger organizations produced more publications than smaller organizations, consistent with AZA members (
Loh et al. 2018). Smaller organizations may be constrained by their size and limited in what research they are able to perform, whereas large organizations may have the resources to take on many projects. AZA institutions produced significantly more publications per member than CAZA members, based on a comparison of our results and
Loh et al. (2018), additionally, proportionately more AZA members produced publications relative to CAZA members. This pattern may be the result of the generally older and larger organization size of AZA members. The AZA and CAZA differ in terms of age—the AZA was founded in 1924 whereas CAZA was founded in 1975. The AZA also has considerably more assets than CAZA (AZA—$24 331 211 CAD;
IRS 2017 vs. CAZA—$119 434 CAD;
CRA 2017). It is also worth noting that CAZA’s top publishing institutions (Toronto Zoo, Vancouver Aquarium, Montreal Biodome, and Calgary Zoo) have all been AZA members, and they are also some of Canada’s oldest and largest zoos. This supports the idea that older and larger organizations have higher research outputs because of increased resources. Interestingly, there was no difference between AZA and CAZA in the number of publications per member in biodiversity conservation. This furthers the narrative that there is a strong research focus on the veterinary sciences across North America, as both CAZA and AZA institutions produce high volumes of publications in this area compared with relatively low numbers of biodiversity conservation publications.
There are a number of reasons why zoos and aquariums should seek to enhance the production of peer-reviewed publications, particularly in biodiversity conservation. First, it facilitates knowledge sharing among the community of conservation practitioners, whether zoos, academic, government, or nongovernment organizations. Second, the process of peer-review ensures some standard in the science being produced. Finally, the credibility of zoos as conservation organizations can only be enhanced by the production of peer-reviewed science in this field. One way that has been proposed to increase zoos’ and aquariums’ research productivity is by increasing collaborations with academic institutions (
Fernandez and Timberlake 2008). Zoos and aquariums and academic institutions often have common goals regarding animal biology and conservation, such as understanding behaviour, the conservation and propagation of species, and education (
Fernandez and Timberlake 2008). Therefore, it is puzzling that collaborations between these groups are rare (
Maple 2008). Often zoos and aquariums have different research interests than academic institutions, with the former being more focused on programs to promote the well-being of their animals and the latter focused on the biology and behaviour of frequently used species (
Mellen and MacPhee 2001;
Fernandez and Timberlake 2008). However, zoos and aquariums and academic institutions can combine these interests for mutual benefit (
Fernandez and Timberlake 2008). Academics can use the unique environment zoos and aquariums provide for studying species, whereas academic research based on field observations may increase the success of reintroduction efforts led by zoos and aquariums (
Fernandez and Timberlake 2008).
Research productivity is not a perfect measure of zoos’ and aquariums’ contribution to biodiversity conservation because of the research-implementation gap often observed in the field of conservation biology (
Knight et al. 2008;
Arlettaz et al. 2010). Often conservation research is not implemented in the field, so research is not always indicative of conservation action (
Knight et al. 2008;
Arlettaz et al. 2010). Zoos and aquariums also engage in biodiversity conservation in ways that may not be captured by the metric of research productivity. Zoos and aquariums are centers for education about wildlife and their conservation (
Miller et al. 2004). Annually, more than 700 million people visit zoos and aquariums around the world, providing a unique opportunity to educate the public about conservation (
Gusset and Dick 2011). Zoos and aquariums also contribute to conservation initiatives by providing funding to biodiversity conservation organizations; worldwide, zoos and aquariums are among the main providers of conservation funding in relation to major international conservation organizations (
Gusset and Dick 2011). They also participate extensively in captive breeding programs to preserve endangered species for possible reintroduction (
Conde et al. 2011;
Harding et al. 2016). It is recognized that captive populations are necessary to avoid the loss of many species (
Mallinson 2003). For instance, the population of Vancouver Island marmots (
Marmota vancouverensis), an endemic mammal, dropped to approximately 30 individuals in 2003, prompting a zoo-based recovery strategy to be put in place (
Roach 2017). Owing to the joint captive breeding and reintroduction program led by the Toronto Zoo and Calgary Zoo, as of 2017 a conservative estimate of 140–190 marmots exist in the mountains of British Columbia (
Roach 2017).
Zoos and aquariums present unique opportunities to study animals in ways that are not possible in the wild and are therefore invaluable for the conservation of species (
Hutchins and Conway 1995). As conservation is a mandate of CAZA (
CAZA 2008), the production of peer-reviewed publications may be one way to assess the growth of conservation research at zoological institutions. By identifying size and age of organizations as significant predictors of research productivity, as well as the inclusion of research-focused wording in the strategic plans of zoos and aquariums, CAZA and their members can make strategic decisions to either prioritize research at the larger and older institutions or support the conservation research activities of smaller and younger organizations. Further work should examine patterns of research productivity of zoos and aquariums across other jurisdictions (e.g., European Association of Zoos and Aquaria, the Australasian Zoo and Aquarium Association). Other factors that can impact the research productivity of zoos should also be analyzed including the taxonomic composition of the collection of zoos (e.g.,
Rose et al. 2019), the background changes in the publication landscape including the overall increase in research output by the scientific enterprise at large, and any differences in the publication cultures of veterinary sciences and biodiversity conservation. Importantly, it is also worth examining the other significant aspect of the modern zoo—conservation education. Examining patterns of organizational characteristics related to the productivity and efficacy of education programs of zoos using tools such as that described by
Barriault and Rennie (2019) would give further insight into the continued evolution of zoos and aquariums.