In the deep end: pooling data and other statistical challenges of zoo and aquarium research

Zoo and aquarium research presents many logistic challenges, including extremely small sample sizes and lack of independent data points, which lend themselves to the misuse of statistics. Pseudoreplication and pooling of data are two statistical problems common in research in the biological sciences. Although the prevalence of these and other statistical miscues have been documented in other fields, little attention has been paid to the practice of statistics in the field of zoo biology. A review of articles published in the journal Zoo Biology between 1999–2004 showed that approximately 40% of the 146 articles utilizing inferential statistics during that span contained some evidence of pseudoreplication or pooling of data. Nearly 75% of studies did not provide degrees of freedom for all statistics and approximately 20% did not report test statistic values. Although the level of pseudoreplication in this dataset is not outside the levels found in other branches of biology, it does indicate the challenges of dealing with appropriate data analysis in zoo and aquarium studies. The standardization of statistical techniques to deal with the methodological challenges of zoo and aquarium populations can help advance zoo research by guiding the production and analysis of applied studies. This study recommends techniques for dealing with these issues, including complete disclosure of data manipulation and reporting of statistical values, checking and control for institutional effects in statistical models, and avoidance of pseudoreplicated observations. Additionally, zoo biologists should seek out other models such as hierarchical or factorial models or randomization tests to supplement their repertoire of t‐tests and ANOVA. These suggestions are intended to stimulate conversation and examination of the current use of statistics in zoo biology in an effort to develop more consistent requirements for publication. Zoo Biol 0:1–14, 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.     

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.     

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.     

The impact of in-person and video-recorded animal experiences on zoo visitors' cognition,affect, empathic concern,and conservation intent

Currently there are mixed results regarding the ability for media or more specifically video to increase a person's interest in conservation. However, there is a growing amount of evidence that in-person experiences at a zoo or aquarium can increase a person's interest in conservation. The goal of the current study was to examine the difference between an in-person experience viewing a polar bear training session and watching a video of the same experience on cognition, emotion, empathic concern, and conservation intent. A total of 124 Brookfield Zoo members were randomly assigned to one of three conditions. Condition 1 was an in-person 10 min (Live Animal) experience viewing a training session with a polar bear. Condition 2 participants (Video Animal) watched a video of the same experience from Condition 1 and Condition 3 (Control) listened to the audio from Condition 1 but only viewed an image of one of our animal care specialists. Results suggest that the live condition is associated with higher probability of answering questions correctly, having a positive emotional experience, having greater empathic concern for wild bears, and wanting to get involved in conservation when compared to the control. These impacts were not observed for the video condition suggesting that for this study, watching a video of a training session was not an effective tool for getting people involved in conservation. Future research is needed to better understand this important topic, but we now have further evidence of the importance of in-person zoo experiences.     

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.     

Visitors or Visits? An Examination of Zoo Visitor Numbers Using the Case Study of Australia

Usually cited in reference to the potential reach of zoo education, one of the popular figures for global zoo visitation is that 600 million people visit zoos annually. However, this number needs clarification on two fronts. First, there are many zoo visitors who are not included in the calculation because they visited a zoo that was not included in the count. Second, it does not take into consideration the people visit either the same or different zoos more than once annually. Using data collected from several sources, including zoo visitors themselves, this article focuses on one country—Australia—that contributes 15.6 million to the visitation total, and contends that the correct number of unique annual zoo visitors to Australian zoos is likely to be between 8 and 10 million. However, rather than suggesting an overemphasis on the potential of zoos for educating visitors, having regular repeat visitors represents a distinct advantage for zoos, allowing for progressive education opportunities. Zoo Biol. 32:37‐44, 2013. © 2012 Wiley Periodicals, Inc.     

Technology at the Zoo: The Influence of a Touchscreen Computer on Orangutans and Zoo Visitors

A computer‐controlled touchscreen apparatus (hereafter referred to as “touchscreen”) in the orangutan exhibit at Zoo Atlanta provides enrichment to the animals and allows cognitive research to take place on exhibit. This study investigated the impact of the touchscreen on orangutan behavior and visibility, as well as its impact on zoo visitors. Despite previous research suggesting that providing a single computer system may negatively affect orangutan behavior, there was not a significant increase in aggression, stereotypic, or distress‐related behaviors following the activation of the on‐exhibit touchscreen. We also investigated the possibility that zoo visitors may be negatively affected by technology because it deviates from naturalism. However, we did not find a change in stay time or overall experience rating when the computer was turned on. This research was the first to assess visitor attitudes toward technology at the zoo, and we found that visitors report highly positive attitudes about technology for both animals and visitors. If subjects visited the exhibit when the computer was turned on, they more strongly agreed that orangutans benefit from interacting with computerized enrichment. This study is the first investigation of an on‐exhibit touchscreen in group‐housed apes; our findings of no negative effects on the animals or zoo visitors and positive attitudes toward technology suggest a significant value of this practice. Zoo Biol 31:27;–39, 2012. © 2011 Wiley Periodicals, Inc.     

Training zoo biology in tropical countries: A report on a method and progress

In 1987 the National Zoological Park inaugurated a Zoo Biology training program for developing country zoos, particularly those in the tropics where the threats to biological diversity are greatest. The program last 2 to 4 weeks, is targeted to mid-level zoo managers, and aspires to improve the care and management of wildlife in zoos through in situ training. A host zoo in the foreign country is responsible for selecting and inviting trainees from other zoos in the country or region. Training activities include daily lectures, demonstrations, quizzes, problem solving exercises, and class projects. In addition, the class participates in creating an animal inventory for the host zoo, and endemic species are identified for studbook compilation and captive propagation projects. Most mid-level zoo managers in tropical developing countries are college-educated men in their thirties, and have on average less than 10 years of zoo experience. We evaluate our program, and discuss the problems confronting tropical zoos in the developing world. Finally, we suggest ways that zoos in developed countries can influence tropical conservation through training and education.     

Attitude of zoo visitors to the idea of feeding live prey to zoo animals

Two hundred UK zoo visitors were asked about their attitudes regarding the feeding of live prey to zoo animals. All visitors agreed with live insects being fed to lizards, providing it was done off-exhibit, and only 4% objected if done on-exhibit. Seventy-two percent of visitors agreed with live fish being fed to penguins on-exhibit and 84.5% agreed to feeding live fish off-exhibit. However, only 32% agreed to a live rabbit being fed to a cheetah on exhibit, whereas 62.5% agreed to this if done off-exhibit. In general we found female interviewees more likely to object to the feeding of live vertebrate prey. Comments volunteered by interviewees suggested that they agreed with feeding live vertebrate prey because ‘it is natural’. If they objected, it was because ‘it would upset them or their children’. Zoo Biol 16:343–347, 1997. © 1997 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.     

Interactions among environmental enrichment,viewing crowds,and zoo chimpanzees (Pantroglodytes)

The primary purpose of this study was to investigate whether or not a group of zoo chimpanzees responded to environmental enrichment differently given higher weekend crowds in contrast to lower weekday crowds. Findings showed that foraging, feeding, and object-using were more likely with new enrichment; conversely, grooming, playing, watch-idle, and aberrant behaviors were more likely with 1 day-old enrichment. Across both new and 1 day-old enrichment, however, high crowds corresponded with diminished frequencies of foraging, object-using, grooming, and play. The study's second purpose was to examine how zoo visitors responded to chimpanzees under varying conditions of environmental enrichment. Analysis of zoo visitors' verbatim responses suggested that the public's behavior was influenced by desires to interact with the chimpanzees, the state of the chimpanzees' habitat, the relative complexity of the chimpanzees' activities, and human sociocultural norms. Thus a variety of contextual factors were found to influence the behavior of chimpanzees and humans alike. Future research is encouraged that investigates the ways in which multiple elements within the full captive socioecology of chimpanzees fluidly interact to influence the effectiveness of environmental enrichment as well as zoo visitors' responses to, and lasting impressions of, zoo chimpanzees. Zoo Biol 17:211–230, 1998. © 1998 Wiley-Liss, Inc.     

Species Management Benchmarking: Outcomes Over Outputs in a Changing Operating Environment

Species management has been utilized by the zoo and aquarium industry, since the mid‐1990s, to ensure the ongoing genetic and demographic viability of populations, which can be difficult to maintain in the ever‐changing operating environments of zoos. In 2009, the Zoo and Aquarium Association Australasia reviewed their species management services, focusing on addressing issues that had arisen as a result of the managed programs maturing and operating environments evolving. In summary, the project examined resourcing, policies, processes, and species to be managed. As a result, a benchmarking tool was developed (Health Check Report, HCR), which evaluated the programs against a set of broad criteria. A comparison of managed programs (n = 98), between 2008 and 2011, was undertaken to ascertain the tool's effectiveness. There was a marked decrease in programs that were designated as weak (37 down to 13); and an increase in excellent programs (24 up to 49) between the 2 years. Further, there were significant improvements in the administration benchmarking area (submission of reports, captive management plan development) across a number of taxon advisory groups. This HCR comparison showed that a benchmarking tool enables a program's performance to be quickly assessed and any remedial measures applied. The increases observed in program health were mainly due to increased management goals being attained. The HCR will be an ongoing program, as the management of the programs increases and goals are achieved, criteria will be refined to better highlight ongoing issues and ways in which these can be resolved. Zoo Biol. 32:230–237, 2013. © 2012 Wiley Periodicals, Inc.     

Zoos through the Lens of the IUCN Red List: A Global Metapopulation Approach to Support Conservation Breeding Programs

Given current extinction trends, the number of species requiring conservation breeding programs (CBPs) is likely to increase dramatically. To inform CBP policies for threatened terrestrial vertebrates, we evaluated the number and representation of threatened vertebrate species on the IUCN Red List held in the ISIS zoo network and estimated the complexity of their management as metapopulations. Our results show that 695 of the 3,955 (23%) terrestrial vertebrate species in ISIS zoos are threatened. Only two of the 59 taxonomic orders show a higher proportion of threatened species in ISIS zoos than would be expected if species were selected at random. In addition, for most taxa, the management of a zoo metapopulation of more than 250 individuals will require the coordination of a cluster of 11 to 24 ISIS zoos within a radius of 2,000 km. Thus, in the zoo network, the representation of species that may require CBPs is currently low and the spatial distribution of these zoo populations makes management difficult. Although the zoo community may have the will and the logistical potential to contribute to conservation actions, including CBPs, to do so will require greater collaboration between zoos and other institutions, alongside the development of international agreements that facilitate cross-border movement of zoo animals. To maximize the effectiveness of integrated conservation actions that include CBPs, it is fundamental that the non-zoo conservation community acknowledges and integrates the expertise and facilities of zoos where it can be helpful.     

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.     

Survey and interzoo studies used to address husbandry problems in some zoo vertebrates

In addition to genetic and demographic considerations, SSP coordinators have been asked to systematically address husbandry issues. Three approaches to the study of captive management issues are typically used: (1) large numbers of individuals are housed at a single institution maintained in a situation that facilitates systematic evaluation of the captive environment, (2) an investigator travels to many institutions to gather data on a single taxon, or (3) an investigator surveys existing information by assembling data from a large number of individuals at a variety of institutions. Each approach has both advantages and disadvantages in terms of feasibility and the type of results obtained. The use of surveys to obtain information about husbandry parameters from a large number of animals maintained at a variety of zoos is quite possibly the most common approach used among zoo managers. Zoo husbandry surveys are typically developed to address issues problematic to a particular species, including reproductive failure and health issues. Unfortunately, surveys appear to be an often misused research tool among zoo professionals. Surveys can be improved by working with psychologists or sociologists at local universities, by narrowing the focus of the survey's purpose, and by carefully constructing each question. © 1994 Wiley-Liss, Inc.     

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.     

An Hourly Variation in Zoo Visitor Interest: Measurement and Significance for Animal Welfare Research

A methodological difficulty facing welfare research on nonhuman animals in the zoo is the large number of uncontrolled variables due to variation within and between study sites. Zoo visitors act as uncontrolled variables, with number, density, size, and behavior constantly changing. This is worrisome because previous research linked visitor variables to animal behavioral changes indicative of stress. There are implications for research design: Studies not accounting for visitors' effect on animal welfare risk confounding (visitor) variables distorting their findings. Zoos need methods to measure and minimize effects of visitor behavior and to ensure that there are no hidden variables in research models. This article identifies a previously unreported variable—hourly variation (decrease) in visitor interest—that may impinge on animal welfare and validates a methodology for measuring it. That visitor interest wanes across the course of the day has important implications for animal welfare management; visitor effects on animal welfare are likely to occur, or intensify, during the morning or in earlier visits when visitor interest is greatest. This article discusses this issue and possible solutions to reduce visitor effects on animal well-being.     

Taxonomic re-evaluation of the jaguar

The purpose of this report is to re-examine jaguar (Panthera onca) subspecies using morphometric skull characters and multivariate statistical methods to analyze differences. Eleven skull characters used historically to define jaguar subspecies were measured on 170 specimens in U.S. natural history museums. Relationships among the eight recognized subspecies of jaguar were examined. using Multigroup Discriminant Analysis (MDA) and univarite statistics. Discriminant analyses of these skull characteristics does not indicate distinct groups, supporting the null hypothesis. This analysis was conducted to add to systematic studies such as DNA analysis to assist the Felid Taxon Advisory Group (Felid TAG) and the American Zoo and Aquarium Association (AZA) establish valid taxonomic differences in the jaguar. Zoo Biol 16:107–120, 1997. © 1997 Wiley-Liss, Inc.