BIAZA statistics guidelines: toward a common application of statistical tests for zoo research

Zoo research presents many statistical challenges, mostly arising from the need to work with small sample sizes. Efforts to overcome these often lead to the misuse of statistics including pseudoreplication, inappropriate pooling, assumption violation or excessive Type II errors because of using tests with low power to avoid assumption violation. To tackle these issues and make some general statistical recommendations for zoo researchers, the Research Group of the British and Irish Association of Zoos and Aquariums (BIAZA) conducted a workshop. Participants included zoo‐based researchers, university academics with zoo interests and three statistical experts. The result was a BIAZA publication Zoo Research Guidelines: Statistics for Typical Zoo Datasets (Plowman [ 2006 ] Zoo research guidelines: statistics for zoo datasets. London: BIAZA), which provides advice for zoo researchers on study design and analysis to ensure appropriate and rigorous use of statistics. The main recommendations are: (1) that many typical zoo investigations should be conducted as single case/small N randomized designs, analyzed with randomization tests, (2) that when comparing complete time budgets across conditions in behavioral studies, G tests and their derivatives are the most appropriate statistical tests and (3) that in studies involving multiple dependent and independent variables there are usually no satisfactory alternatives to traditional parametric tests and, despite some assumption violations, it is better to use these tests with careful interpretation, than to lose information through not testing at all. The BIAZA guidelines were recommended by American Association of Zoos and Aquariums (AZA) researchers at the AZA Annual Conference in Tampa, FL, September 2006, and are free to download from www.biaza.org.uk . Zoo Biol 27:226–233, 2008. © 2008 Wiley‐Liss, Inc.     

Publication trends in zoo biology: A brief analysis of the first 15 years

Zoo Biology has completed 15 years as a professional journal dedicated to exsitu wildlife research. To assess the journal's representation of zoo and aquarium research, we examined some aspects of its publication record, based on analyses of 395 research articles. The taxonomic representation of Zoo Biology is heavily skewed toward research articles on mammals (73%), with articles on birds, reptiles, and invertebrates contributing only 10%, 7%, and 7%, respectively. Behavior and reproduction (sensu latu) are the predominating disciplinary themes of research, with heavy reliance on non-invasive endocrine methodology using RIA and EIA. The relatively small number of articles dealing with demography and genetics is surprising when one considers the eminent role such analyses have played in Species Survival Plans. Most contributions are multi-authored and arise from U.S. institutions, with collaborative ventures between zoos and universities accounting for 26% of all articles. The academic community, however, contributed nearly one third of Zoo Biology's articles as non-collaborative contributions. University and aquarium affiliations are known to exist, but the products of such cooperation are not appearing in the pages of Zoo Biology. We conclude the taxonomic trends reflect a shortage of research-oriented staff in the zoo and aquarium profession, and a tendency for a significant number of zoo biologists to publish in taxon-oriented journals. Zoo Biol 16:3–8, 1997. © 1997 Wiley-Liss, Inc.     

Meta‐analytic review of the effects of enrichment on stereotypic behavior in zoo mammals

This meta‐analysis reports the effect enrichment has on the occurrence of stereotypic behavior exhibited by captive zoo mammals. The analysis also identifies which types of enrichment are most effective, which groups of animals benefit the most, and which types of stereotypes are most affected by environmental enrichment. The analysis included 54 studies that yielded 63 effect size statistics. Fifty‐seven of sixty‐three effect sizes went in the predicted direction (90%), with the animals participating in less stereotypic behavior during the enrichment condition than in the baseline condition. The mean effect size (correlation coefficient r) was 0.46. The combined P‐value using both fixed and random effects methods was reveled to be <0.0000001. A file drawer N‐value was calculated to identify the number of unretrieved studies (with a combined effect size of zero) that would be needed to nullify the results of this analysis. The file drawer N‐value was 1,726, suggesting that it is highly unlikely that the significant results reported in this analysis are nullified by studies that remain in file drawers. Based on these results it was concluded that enrichment substantially reduces the frequency of stereotypic behavior exhibited by mammals living in zoo environments. Zoo Biol 0:1–21, 2006. © 2006 Wiley‐Liss, Inc.     

Death at the zoo: the media,science, and reality

Media characterizations of zoo and aquarium animal deaths were randomly monitored on the internet for a 20‐month period (September 2003–May 2005). Based on 148 samples collected, it was possible to classify articles into one of four categories, which were operationally defined: 1) dispassionate observers; 2) accusers; 3) sympathizers; and 4) balancers. In addition, with the notable exception of seven cases, all of the articles examined focused on large, charismatic mammals, such as gorillas, dolphins, lions, and elephants. Although a majority of the articles examined (70.4%) were either dispassionate and objective or sympathetic, nearly a third (29.6%) were either accusatory or attempted to balance the accusatory statements of animal rights activists with sympathetic statements from zoo professionals. Recommendations are offered for how zoos should deal with the increasing media and public interest in zoo animal deaths, including: 1) a greater commitment to studying the reasons for mortality in a wide variety of species; and 2) an increased investment in record keeping and analysis, which should allow zoos to calculate average life spans in animal populations and to monitor and assess the risk of certain lethal diseases on a real‐time basis. Comparisons are drawn between zoo veterinary practices and human medicine, which are both inexact sciences. Suggestions are made for how the public and key decision‐makers can distinguish between media reports on zoo animal deaths that are legitimate cause for concern vs. those that are sensationalist and meant to generate controversy and sell papers. A greater focus on the science of zoo animal death is necessary for accredited zoos to maintain the public's confidence in their animal care practices. Zoo Biol 0:1–15, 2006. © 2006 Wiley‐Liss, Inc.     

Visitors' perceptions of zoo‐housed lesser anteater (Tamandua tetradactyla) welfare: Observation plays a larger role than a brief informative talk

There is a growing ethical concern in modern society about animals' quality of life. We hypothesize that zoo visitors' perception of zoo animal welfare, particularly in the case of lesser anteaters, changes positively after listening to scientific information. Visitors observing active lesser anteaters in their enclosures at Córdoba Zoo (Argentina) were asked to respond to a questionnaire about animal welfare. The treatment group (T) answered the questionnaire after listening to a brief informative talk based on local scientific studies on lesser anteaters. The control group (C) answered the questionnaire without hearing the informative talk. Visitors (87.2%) considered biological, sanitary, and sociocultural aspects to be necessary conditions for optimum wild zoo‐housed animal welfare. The majority of visitors considered that natural surroundings provide the highest level of welfare for wild animals. Visitors in the T group ranked the zoo as providing a higher level of animal welfare than those in group C. In reference to management measurements, the T group agreed on the positive effect of the application of environmental enrichment (Likert Medians: C = 4 and T = 5; p = .0443). On the basis of their perception, most visitors in both groups stated that the lesser anteaters at Córdoba Zoo appeared to be in a good state of welfare. We interpret this as meaning that, what these Córdoba zoo visitors personally perceived while observing the lesser anteaters carried greater weight than what they learned from the informative talk, though the talk did slightly affect their opinion.     

Research in zoos: a growth area in conservation

Despite early menageries being the source of much useful biological information on anatomy and taxonomy, it is only more recently that the potential for research in zoos has been recongnized. Collections of captive animals are unique and irreplaceable resources for conservation; but without research in zoological parks, progress in conservation science would diminish. There is a flow of information from zoo researchers to field scientists that assists in providing new insights into species biology. Reciprocally, data collected in the field enhance efforts in captive breeding. This paper summarizes the new research initiatives undertaken in zoos, e.g., in the fields of reproductive and genetic technologies, and highlights their significance for conservation and management of threatened species. It is evident that zoo research has a vital role in linking in situ and ex situ conservation. This role needs to be expanded and developed to meet the challenge posed by expanding human and declining wildlife populations and ecosystems.     

Post-occupancy evaluation in the zoo

Post-occupancy evaluations (POE) of the built environment provide systematic information about the success or failure of environmental designs. Research instruments developed for application in human settings can also be adapted for use in zoos. The zoo environment must be evaluated for its impact on animal residents, zoo visitors and staff. Evaluations conducted by our Atlanta research team included studies of the Atlanta Zoo and zoos in nearby cities. The range of available methodologies are reviewed, and the unique constraints of zoo settings are discussed. Our studies indicate that naturalistic environments facilitate the expression of normal and complex animal behavior patterns and tend to enhance the visitor experience. POE represents an exciting new dimension in zoo research and promises to contribute to the success of future generations of zoo design.     

Does zoo herpetology have a future?

Fifty-two North American zoo reptile and amphibian departments were surveyed to determine their contributions to recognized American Zoo and Aquarium Association (AZA)-sponsored programs and formalized research projects over the past 10 years. Surveys also requested information concerning the allocation of resources for conservation and research programs, staff educational background, and entry level salaries. Twenty-two institutions responded to the survey, collectively indicating a total of 164 technical papers, 16 field studies, and 101 non-technical articles completed between 1987 and 1997. Of the 164 technical papers published, 130 (79%) were contributed by three institutions. Of the 16 field studies, seven were outside the United States, whereas nine focused on native species and ecosystems. Six of the reported field studies involved only financial or logistical support. Of the 101 non-technical articles, 42 (42%) were contributed by a single institution. Twenty-one formalized in-house research projects were reported. However, only four appeared to have a clearly defined objective. Survey respondents also reported nine species of reptiles and one amphibian taxon are managed by Species Survival Plans (SSPs). There are currently 12 Taxon Advisory Group (TAG) coordinators, with four of the current coordinators having served on multiple TAG committees. There are 41 AZA-approved studbooks for reptiles and two for amphibians, with 29 having actually been published to date. The average starting salary reported in our survey for entry level keeper positions was $19,500 (range, $13,500–30,000). The average level of education reported was high school graduate. There was no correlation between productivity and higher wages, or level of education. Only one institution received funding specifically for research. We conclude that zoo herpetology departments are not realizing their potential for formalized research and conservation projects and propose recommendations for future involvement. Zoo Biol 17:453–462, 1998. © 1998 Wiley-Liss, Inc.     

First experiences with free‐ranging giant day geckos (Phelsuma madagascariensis grandis,Gray 1870) in the masoala rainforest exhibit in Zurich Zoo,Switzerland

Sixty giant day geckos (Phelsuma madagascariensis grandis) have been introduced into the Masoala rainforest exhibit of Zurich Zoo. Eighteen geckos were monitored during a 3‐month study using the telemetry method. In general, the geckos were able to adapt well under these semi‐natural conditions of the exhibit. The geckos accessed to nearly all locations in the exhibit; some of the animals remained stationary, whereas others covered dozens of meters within a week. They preferred four species of plants as well as the artificial structures supporting the walls and roof of the exhibit, and displayed natural behaviors. Animals were observed feeding on all kind of arthropods and nectar substances, and also on food items dropped from feeding stations for other species. Deliberate feeding targeted at the geckos was finally reduced to a calcium‐rich squash along the visitor's main path. Reproduction was observed frequently within the exhibit. These findings suggest that the geckos will be able to build up a self‐sustaining population and contribute to a nearly‐authentic experience for zoo visitors. Zoo Biol 0:1–7, 2006. © 2006 Wiley‐Liss, Inc.     

What Is the Future for Zoos and Aquariums?

ABSTRACT

Animal welfare concerns have plagued the professional zoo and aquarium field for decades. Societal differences remain concerning the well-being of animals, but it appears a shift is emerging. Scientific studies of animal welfare have dramatically increased, establishing that many previous concerns were not misguided public empathy or anthropomorphism. As a result, both zoo and aquarium animal welfare policy and science are now at the center of attention within the world’s professional zoos and aquariums. It is now possible to view a future that embraces the well-being of individual captive exotic animals, as well as that of their species, and one in which professional zoos and aquariums are dedicated equally to advancing both. Though the ethics of keeping exotic animals and animals from the wild in captivity are still a contentious subject both outside and even within the profession, this study argues. We argue that this path forward will substantially improve most zoo and aquarium animals' welfare and could significantly reduce societal concerns. If animal welfare science and policy are strongly rooted in compassion and embedded in robust accreditation systems, the basic zoo/aquarium paradigm will move toward a more thoughtful approach to the interface between visitors and animals. It starts with a fundamental commitment to the welfare of individual animals.     

Reproductive biology of captive and free-ranging spider monkeys

Records from 42 zoos and from long-term studies of wild populations were analysed to describe the reproductive biology of spider monkeys (Ateles spp.). Both data sets suggested that spider monkey females typically have their first infant between 7 and 8 years of age with an interbirth interval of approximately 32–36 months. Infant sex ratio for zoo populations was approximately 1 male to 1 female; infant sex ratios from wild populations were variable. Zoo records provided adequate sample size to suggest that interbirth interval was not influenced by the sex of the infant produced, and that the sex ratio and the probability of infant survival did not change with the number of infants the mother had produced. The findings of this study have implications with respect to the conservation of New World primate species. Since spider monkeys take a long time to reach sexual maturity and their interbirth interval is longer than that expected based on their body size, their populations may be slow to recover following disturbances. Thus, particular care should be taken for the protection of these species.     

A Visit to the Zoos and Aquariums in Japan II

In the year 2013, the authors, who had already visited some Japanese aquariums and zoos in 2012 (Lange & Tai, 2012), revisited several Japanese aquariums and zoos. They were accompanied by two colleagues from Basle Zoo and the Monterey Bay Aquarium, who joined the tour.Their goals of the tour were focused on new innovative husbandry methods, on new aquarium buildings and new zoo enclosures as well as on rare Japanese endemic animals, which are never or seldom seen outside of Japan.The perfect new aquariums in Kyoto and Kitami City (Hokkaido), but also the very specialized aquariums like the Kamo Aquarium (for jellyfish) in Yamagata, the Chitose Salmon Aquarium (for salmons), the Otaru Aquarium (for sea mammals) and the Umi Kirara Kujukushima Aquarium (for the fauna of the Kujukushima island National Park) have been destinations for this trip. Besides the aquariums also the Asahiyama Zoo (new enclosures for endemic animals of Hokkaido), Kobe Oji Zoo, Kushiro Zoo (many endemic Hokkaido species), Nagasaki Bio Park, Sapporo Maruyama Zoo (new area for South East Asian animals) and the Sasebo Zoological & Botanical Garden were visited.During this tour it was obvious that neither the colleagues in Japan nor the staff in the zoos outside of Japan know sufficient enough about the conception and the husbandry methods in the different institutions in this part of the world. Therefore it is recommendable to organize such tours often for more people, thus both sides can benefit and learn from each other. This again will influence to help to keep the animals better, to attract more visitors in order to inspire them for the conservation of nature and environment.     

When zoo visitors “connect” with a zoo animal,what does that mean?

Connection with a zoo animal may increase conservation‐mindedness in zoo visitors, potentially resulting in conservation‐oriented behavior change. No research has attempted to establish what this “connection” actually means. Visitors (N = 85) to Melbourne Zoo were asked to name the animal with which they most connected, the extent to which they connected with it, and to qualitatively describe what it meant to connect with that animal. Many (but not all) participants connected with charismatic megafauna: primate, great ape, large carnivore, or large herbivore. Qualitative analysis revealed five common themes in the meaning of connection: Appreciation, Attribution, Inspires Emotions, Interaction, and Proximity. Overall connection level was significantly correlated with perceptions of conservation caring for the chosen species. Future research should aim to determine what factors affect a zoo visitor's connection level, which could impact attitudes and behaviors toward conservation.     

Animal behavior and the captive management of wild mammals: A personal view

Behaviorists can undertake noninvasive studies of zoo animals using only the simplest of research tools, unlike those biologists who are concerned with functions below the level of the whole, living organism. With careful interpretation, the results of behavioral studies can be applied to improve the management, husbandry, and exhibition of wild mammals in captivity. This often involves comparisons with research results obtained from studies of animals in the wild, since the behavior of captive specimens may in some measure be altered. Examples are given involving the breeding biology or social organization of three species: (1) barasingha or swamp deer (Cervus duvauceli), (2) mongoose lemur (Lemur mongoz), and (3) drill (Papio leucophaeus). Suggestions are made to improve the allocation of time and resources for research by zoo personnel, including a greater reliance on cooperative efforts to solve problems of common interest.     

Building essential biodiversity variables (EBVs) of species distribution and abundance at a global scale

Much biodiversity data is collected worldwide, but it remains challenging to assemble the scattered knowledge for assessing biodiversity status and trends. The concept of Essential Biodiversity Variables (EBVs) was introduced to structure biodiversity monitoring globally, and to harmonize and standardize biodiversity data from disparate sources to capture a minimum set of critical variables required to study, report and manage biodiversity change. Here, we assess the challenges of a ‘Big Data’ approach to building global EBV data products across taxa and spatiotemporal scales, focusing on species distribution and abundance. The majority of currently available data on species distributions derives from incidentally reported observations or from surveys where presence‐only or presence–absence data are sampled repeatedly with standardized protocols. Most abundance data come from opportunistic population counts or from population time series using standardized protocols (e.g. repeated surveys of the same population from single or multiple sites). Enormous complexity exists in integrating these heterogeneous, multi‐source data sets across space, time, taxa and different sampling methods. Integration of such data into global EBV data products requires correcting biases introduced by imperfect detection and varying sampling effort, dealing with different spatial resolution and extents, harmonizing measurement units from different data sources or sampling methods, applying statistical tools and models for spatial inter‐ or extrapolation, and quantifying sources of uncertainty and errors in data and models. To support the development of EBVs by the Group on Earth Observations Biodiversity Observation Network (GEO BON), we identify 11 key workflow steps that will operationalize the process of building EBV data products within and across research infrastructures worldwide. These workflow steps take multiple sequential activities into account, including identification and aggregation of various raw data sources, data quality control, taxonomic name matching and statistical modelling of integrated data. We illustrate these steps with concrete examples from existing citizen science and professional monitoring projects, including eBird, the Tropical Ecology Assessment and Monitoring network, the Living Planet Index and the Baltic Sea zooplankton monitoring. The identified workflow steps are applicable to both terrestrial and aquatic systems and a broad range of spatial, temporal and taxonomic scales. They depend on clear, findable and accessible metadata, and we provide an overview of current data and metadata standards. Several challenges remain to be solved for building global EBV data products: (i) developing tools and models for combining heterogeneous, multi‐source data sets and filling data gaps in geographic, temporal and taxonomic coverage, (ii) integrating emerging methods and technologies for data collection such as citizen science, sensor networks, DNA‐based techniques and satellite remote sensing, (iii) solving major technical issues related to data product structure, data storage, execution of workflows and the production process/cycle as well as approaching technical interoperability among research infrastructures, (iv) allowing semantic interoperability by developing and adopting standards and tools for capturing consistent data and metadata, and (v) ensuring legal interoperability by endorsing open data or data that are free from restrictions on use, modification and sharing. Addressing these challenges is critical for biodiversity research and for assessing progress towards conservation policy targets and sustainable development goals.     

The global reach of zoos and aquariums in visitor numbers and conservation expenditures

A survey conducted by the World Association of Zoos and Aquariums, in collaboration with national and regional zoo and aquarium associations, showed that annually more than 700 million people visit zoos and aquariums worldwide and are thus potentially exposed to environmental education. Furthermore, the world zoo and aquarium community reportedly spends about US$ 350 million on wildlife conservation each year. Therefore, the world zoo and aquarium community has the potential to play an important role in both environmental education and wildlife conservation. Systematic reviews are encouraged to provide further evidence for the effectiveness of zoos and aquariums as centers of education and conservation.     

The historical development of zoo elephant survivorship

In the discussion about zoo elephant husbandry, the report of Clubb et al. (2008, Science 322: 1649) that zoo elephants had a “compromised survivorship” compared to certain non-zoo populations is a grave argument, and was possibly one of the triggers of a large variety of investigations into zoo elephant welfare, and changes in zoo elephant management. A side observation of that report was that whereas survivorship in African elephants (Loxodonta africana) improved since 1960, this was not the case in Asian elephants (Elephas maximus). We used historical data (based on the Species360 database) to revisit this aspect, including recent developments since 2008. Assessing the North American and European populations from 1910 until today, there were significant improvements of adult (≥10 years) survivorship in both species. For the period from 1960 until today, survivorship improvement was significant for African elephants and close to a significant improvement in Asian elephants; Asian elephants generally had a higher survivorship than Africans. Juvenile (<10 years) survivorship did not change significantly since 1960 and was higher in African elephants, most likely due to the effect of elephant herpes virus on Asian elephants. Current zoo elephant survivorship is higher than some, and lower than some other non-zoo populations. We discuss that in our view, the shape of the survivorship curve, and its change over time, are more relevant than comparisons with specific populations. Zoo elephant survivorship should be monitored continuously, and the expectation of a continuous trend towards improvement should be met.     

The effectiveness of indigestible markers for identifying individual animal feces and their prevalence of use in North American zoos

Techniques for analyzing hormone metabolites in animal excreta have created many opportunities for noninvasive monitoring of health, reproduction, and welfare in zoo animals, but can be difficult to implement when individual samples are not readily identifiable in animal groups. A common approach to this problem is to feed animals an indigestible marker that subsequently appears in feces, but there has been little systematic research on the use of such “fecal markers.” First, we used an online survey to assess the prevalence of fecal marker use in North American zoological institutions. Second, we conducted a series of experimental tests utilizing commonly employed fecal markers in a variety of typical zoo taxa to determine the: (1) effectiveness of several markers to accurately distinguish samples in a variety of species, (2) minimum quantity of marker needed for detection, and (3) length of time between ingestion and detection in the feces. The majority of the 45 institutions that completed the survey reported using fecal markers with their collections. The survey also revealed that the most frequently used markers are seeds/grains and food colorants, with the former generally used in Carnivora and the latter in Primates. Our experimental data confirmed the success of these taxa/marker combinations and also revealed that food colorants function as markers in a variety of avian, reptilian, and mammalian species. Our data describe successful fecal markers for a wide variety of zoo taxa and should, therefore, be useful for zoological managers and researchers needing to employ fecal markers in future investigations. Zoo Biol 30:379–398, 2011. © 2010 Wiley‐Liss, Inc.