Causes of mortality in captive cotton‐top tamarins (Saguinus oedipus)

Cotton‐top tamarins have been housed in captivity in the United States for over five decades. These animals initially were managed in biomedical and research facilities, and more recently have been kept in zoos as well. Although the causes of mortality in captive cotton‐top tamarins have been a topic of investigation for biomedical colonies, they have not been addressed for the North American zoo population. In this retrospective study we review the causes of mortality in the AZA Cotton‐top Tamarin Species Survival Plan (SSP)© population during 1997–2001 to assess current husbandry practices and assist in further developing effective husbandry and management programs for this endangered species. Zoo Biol 23:127–137, 2004. © 2004 Wiley‐Liss, Inc.     

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.     

Effects of hand‐rearing on the reproductive success of western lowland gorillas in North America

This study sought to assess the potential effects of hand‐rearing by evaluating the relationships among rearing type and reproductive success in the American Zoo and Aquarium Association's Species Survival Plan^® for western lowland gorillas. Our study included data on 697 gorillas: 257 wild‐born (WB) and 440 born at zoos or related facilities in North America. We found no significant differences in the number of reproductive zoo‐born (ZB) and WB females, but more WB males sired infants than their ZB counterparts. This was influenced by a skew in the number of reproductive years for WB males in the studbook. ZB males showed no difference in infants produced per reproductive year, as compared to WB males, while ZB females produced more infants per reproductive year than did WB females. Mother‐reared (MR), ZB females produced more offspring and used more reproductive opportunity than hand‐reared (HR) females, whereas rearing had no effect on the reproductive success of ZB males. Moreover, MR and partially hand‐reared (PHR) females were more likely to become nurturing mothers themselves. Zoo Biol 21:389–401, 2002. © 2002 Wiley‐Liss, Inc.     

The Sizes of Elephant Groups in Zoos: Implications for Elephant Welfare

This study examined the distribution of 495 Asian elephants (Elephas maximus) and 336 African elephants (Loxodonta africana) in 194 zoos, most of which were located in Europe (49.1%) and North America (32.6%). Cows outnumbered bulls 4 to 1 (Loxodonta) and 3 to 1 (Elephas). Groups contained 7 or fewer: mean, 4.28 (σ = 5.73). One fifth of elephants lived alone or with one conspecific. Forty-six elephants (5.5%) had no conspecific. Many zoos ignore minimum group sizes of regional zoo association guidelines. The American Zoo and Aquarium Association recommends that breeding facilities keep herds of 6 to 12 elephants. The British and Irish Association of Zoos and Aquariums recommends keeping together at least 4 cows over 2 years old. Over 69% Asian and 80% African cow groups—including those under 2 years—consisted of fewer than 4 individuals. Recently, Europe and North America have made progress with some zoos no longer keeping elephants and with others investing in improved facilities and forming larger herds. The welfare of individual elephants should outweigh all other considerations; zoos should urgently seek to integrate small groups into larger herds.     

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.     

A Comparison of Walking Rates Between Wild and Zoo African Elephants

With increased scrutiny surrounding the welfare of elephants in zoological institutions, it is important to have empirical evidence on their current welfare status. If elephants are not receiving adequate exercise, it could lead to obesity, which can lead to many issues including acyclicity and potentially heart disease. The goal of the current study was to compare the walking rates of elephants in the wild versus elephants in zoos to determine if elephants are walking similar distances relative to their wild counterparts. Eleven wild elephants throughout different habitats and locations in Botswana were compared to 8 elephants at the San Diego Zoo Safari Park. Direct comparisons revealed no significant difference in average walking rates of zoo elephants when compared with wild elephants. These results suggest that elephants at the San Diego Zoo Safari Park walk similar rates to those of wild elephants and may be meeting their exercise needs.     

Enzyme‐immunoassay for the measurement of luteinizing hormone in the serum of African elephants (Loxodonta africana)

Circulating patterns of progesterone and luteinizing hormone (LH) in the elephant have been well characterized, and routine monitoring of these hormones is now viewed as a valuable tool for making informed decisions about the reproductive management of elephants in captivity. Currently, LH monitoring in elephants is done with radio‐immunoassays (RIAs); unfortunately, the use of radioactive materials in RIAs limits their application to institutions with laboratory facilities equipped for the storage and disposal of radioactive waste. Enzyme‐immunoassays (EIAs) offer an inexpensive and more zoo‐friendly alternative to RIA. This work reports on an EIA capable of quantifying circulating LH in African elephants. The EIA employs a biotin label and microtiter plates coated with goat anti‐mouse gamma globulin. LH surges in African elephants (n=3) increased fivefold over baseline concentrations (1.00±0.1 ng/ml vs. 0.2±0.1 ng/ml) and occurred 19.3±0.2 days apart. Ovulatory LH surges were associated with an increase in serum progestogens from 4.8±0.4 ng/ml to 11.7±0.4 ng/ml. The ability to quantify reproductive hormones in elephants via EIA is an important step in the process of making endocrine monitoring more accessible to zoos housing these species. Zoo Biol 21:403–408, 2002. © 2002 Wiley‐Liss, Inc.     

Elephant importation from range countries: ethical and practical considerations for accredited zoos

Zoo elephant populations are in serious demographic peril. Advances in elephant management and care are expected to lead to improved reproductive success. The existing cohort of reproductively viable adult females is aging, however, and effective changes may not come fast enough to sustain the population over time. If so, importation of captive, semi‐domesticated, and wild elephants from range countries may be necessary for zoo programs to survive. Yet, due to the high profile elephants now have with animal rights activists, there may be increasing legal and political barriers to elephant importation. This makes it especially important that zoos become more proactive in addressing remaining weaknesses in elephant management and care and building the case for elephants in zoos. This article summarizes the key considerations for AZA‐accredited zoos that are contemplating future importations. These include ethical, legal, practical, public relations, and other considerations. The authors strongly recommend that zoos position themselves for possible future importations immediately instead of waiting until the last minute. It is equally critical that zoos recognize their existing vulnerabilities and attempt to address them proactively; only then, can they take control of their own fate and reduce the potential for later regret. Zoo Biol 25:219–233, 2006. © 2006 Wiley‐Liss, Inc.     

One year later: evaluation of PMC‐recommended births and transfers

To meet their exhibition, conservation, education, and scientific goals, members of the American Zoo and Aquarium Association (AZA) collaborate to manage their living collections as single species populations. These cooperative population management programs, Species Survival Plans^® (SSP) and Population Management Plans (PMP), issue specimen‐by‐specimen recommendations aimed at perpetuating captive populations by maintaining genetic diversity and demographic stability. Species Survival Plans and PMPs differ in that SSP participants agree to complete recommendations, whereas PMP participants need only take recommendations under advisement. We evaluated the effect of program type and the number of participating institutions on the success of actions recommended by the Population Management Center (PMC): transfers of specimens between institutions, breeding, and target number of offspring. We analyzed AZA studbook databases for the occurrence of recommended or unrecommended transfers and births during the 1‐year period after the distribution of standard AZA Breeding‐and‐Transfer Plans. We had three major findings: 1) on average, both SSPs and PMPs fell about 25% short of their target; however, as the number of participating institutions increased so too did the likelihood that programs met or exceeded their target; 2) SSPs exhibited significantly greater transfer success than PMPs, although transfer success for both program types was below 50%; and 3) SSPs exhibited significantly greater breeding success than PMPs, although breeding success for both program types was below 20%. Together, these results indicate that the science and sophistication behind genetic and demographic management of captive populations may be compromised by the challenges of implementation. Zoo Biol 0:1–11, 2006. © 2006 Wiley‐Liss, Inc.     

Calculation of longevity and life expectancy in captive elephants

The concepts of longevity (longest lived) and life expectancy (typical age at death) are common demographic parameters that provide insight into a population. Defined as the longest lived individual, longevity is easily calculated but is not representative, as only one individual will live to this extreme. Longevity records for North American Asian elephants (Elephas maximus) and African elephants (Loxodonta africana) have not yet been set, as the oldest individuals (77 and 53 years, respectively) are still alive. One Asian elephant lived to 86 years in the Taipei Zoo. This is comparable to the maximum (though not typical) longevity estimated in wild populations. Calculation of life expectancy, however, must use statistics that are appropriate for the data available, the distribution of the data, and the species' biology. Using a simple arithmetic mean to describe the non‐normally distributed age at death for elephant populations underestimates life expectancy. Use of life‐table analysis to estimate median survivorship or survival analysis to estimate average survivorship are more appropriate for the species' biology and the data available, and provide more accurate estimates. Using a life‐table, the median life expectancy for female Asian elephants (Lx=0.50) is 35.9 years in North America and 41.9 years in Europe. Survival analysis estimates of average life expectancy for Asian elephants are 47.6 years in Europe and 44.8 years in North America. Survival analysis estimates for African elephants are less robust due to less data. Currently the African elephant average life expectancy estimate in North America is 33.0 years, but this is likely to increase with more data, as it has over the past 10 years. Zoo Biol 23:365–373, 2004. © 2004 Wiley‐Liss, Inc.     

Molecular systematics for taxonomic placement of a gorilla of uncertain origin

An adult male gorilla was donated from private ownership in 1994 to Zoo Atlanta and became part of the American Zoo and Aquarium Association's Gorilla Species Survival Plan. This animal, Ivan, was captured as an infant in Africa in 1964. Ambiguity regarding origin and concomitant sub‐species designation was resolved by analyzing the cytochrome oxidase II mitochondrial gene known to contain eight diagnostic sites for gorilla sub‐species. Ivan has the diagnostic profile that characterizes the western clade Gorilla gorilla gorilla. Zoo Biol 18:429–432, 1999. © 1999 Wiley‐Liss, Inc.     

ISIS database: An evaluation of records essential for captive management

Species databases are essential for the scientific management of species and specimens in captive wildlife populations. Population managers in North America base their decisions on information in two databases:the International Species Information System (ISIS) and American Zoo and Aquarium Association (AZA) approved regional studbooks. Genetic and demographic management of species relies on studbooks, whereas regional collection planning and management by Taxon Advisory Groups (TAGs) may use a combination of studbooks, direct surveys, and data from ISIS. Use of ISIS data as the primary basis for population management and collection planning is increasing, yet there has been no assessment of how ISIS data differ from studbooks. Thus these databases were compared to determine if they are interchangeable for the purposes of regional collection planning or species management. Population sizes of living individuals in 68 SSP^© taxa were compared to assess the magnitude of differences between the databases. Differences in population size were considerable and highly variable; ISIS on average underestimated the number of living animals in SSP^© taxa populations. Ten studbooks were also analyzed in detail to identify specific types of discrepancies between the two databases. On average, 19.2 ± 2.2% of the information in the ISIS database differed from that in the studbook. Most discrepancies derived from data that were either missing from, or incorrect in, the ISIS database. The most common discrepancies involve parents who were either unidentified or misidentified in the ISIS database (x? = 37.5 ± 5.7% of all records). No single type of discrepancy, however, was prevalent across all 10 species; the overall rate of discrepancies per species was attributable to a combination of discrepancies peculiar to each species. Protocols concerning data entry standards, data collection, and the scope of data collected are likely causes of most discrepancies. In its present form, the ISIS database is not appropriate for single species management; if used cautiously, it can be of assistance in the development of regional collection plans. Development of an ISIS database that is suitable for population management will require an increased commitment to data quality by records keepers, zoological institutions, and ISIS. © 1995 Wiley-Liss, Inc.     

The behavioral effects of exhibit size versus complexity in African elephants: A potential solution for smaller spaces

Population‐level analyses suggest that habitat complexity, but not necessarily space availability, has important welfare outcomes for elephants in human care. At the Dallas Zoo, the opening of a new exhibit complex allowed us to measure the behavior of two female African elephants across three treatments to evaluate the independent effects of complexity and space. Preoccupancy observations were conducted in the elephants’ older exhibit, which consisted of a smaller, more simple yard (630 m²). Subsequent postoccupancy observations measured behavior in two different spaces in the new exhibit: a larger, complex yard (15,000 m²), and a smaller, but complex yard (1,520 m²). The elephants’ overall activity levels were greater in complex habitats, regardless of their size. Similar effects of habitat complexity oversize were observed with greater rates of foraging and lower rates of being stationary. Furthermore, elephants were out of view of visitors significantly more in the small, simple yard compared to either of the more complex habitats. However, exhibit size affected the incidence of stereotypic behavior (with lower rates of stereotypy in the larger exhibit compared to the smaller yards) and investigatory behavior (elephants investigated their environments more with increasing size and complexity). Behavioral diversity also increased with exhibit size and complexity. These results indicate that space availability alone is not sufficient to enhance the behavioral welfare of zoo elephants. Therefore, facilities with limited space can still encourage species‐appropriate behaviors and improved welfare for the elephants in their care by converting a small, simple area into a more complex habitat.     

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.     

Guidelines for creating a food safety HACCP program in zoos or aquaria

The Hazard Analysis and Critical Control Point (HACCP) monitoring system has been used traditionally to increase quality control in human food production operations and there is pressure to implement it at the producer and purchaser levels of the food chain. Recently, the concept of HACCP monitoring has extended to food fed to domestic animals. Captive wildlife facilities, such as zoos and aquaria, would benefit from a well‐organized, food safety and nutritional monitoring system. Zoos and aquaria spend significant resources in time and money on maintaining the health of their animals; much of this energy is focused on disease prevention and adequate nutrition. The result of these combined efforts is the implementation of a HACCP program in zoo food management. Although zoo food handling standards have been implemented through the American Zoo and Aquarium Association (AZA) accreditation process, food borne disease outbreaks and malnutrition still exist. By implementing an organized approach to monitoring the quality of food delivered to the animals, the safety and nutritional value of the foods will increase, while decreasing the financial loss due to food waste and time spent caring for ill animals. This report provides a framework for implementing a HACCP program into the food preparation and handling system of zoos and aquaria. Zoo Biol 0:1–11, 2005. © 2005 Wiley‐Liss, Inc.     

Variation in nature: its implications for zoo elephant management

Despite many advances in animal care and welfare over the past few decades, zoos have been criticized recently for the quality of their elephant management programs. More specifically, critics have argued that elephants live miserable lives in captivity and thus should not be kept in zoos. Poor health and reproductive success, they say, are the result of the combined impact of: a lack of exercise; exposure to cold temperatures and disease; and stress due to the use of “brutal” training techniques, chaining and inappropriate social environments. Everyone, including zoo professionals, seems to agree that improvements in zoo elephant management are necessary and appropriate. However, there is considerable disagreement on how to proceed and little information on which to base such decisions. One tactic that the critics have adopted in their efforts to promote change is their frequent reference to “nature” as a yardstick for gauging the adequacy of zoo animal management and care. An argument is made that direct zoo–wild comparisons are of questionable utility and may be invalid from a scientific perspective. Some critics talk about “nature” as if it represented a fixed set of rules by which captive managers must either abide by or risk diminishing the health and welfare of their charges. However, many aspects of elephant natural history vary greatly depending on prevailing environmental conditions and elephants may be much more flexible than many critics are giving them credit for. Thus, although zoo animal managers should look to nature for clues about how to best care for captive elephants, they should not feel constrained by them. This revelation is not intended as an excuse for poor elephant management or to support the status quo. On the contrary, a better approach is to develop realistic and biologically meaningful metrics that reflect the quality of elephant care and welfare and to use them to measure the success of evolving zoo elephant programs. Zoo Biol 25:161–171, 2006. © 2006 Wiley‐Liss, Inc.     

Captive breeding and infant mortality in Asian elephants: A comparison between twenty western zoos and three eastern elephant centers

Poor reproductive success compromises the long-term viability of captive Asian elephant populations. A questionnaire was designed to assess the importance of reproductive behavior and husbandry factors on breeding success. This was circulated to a number of institutions, zoos, and circuses in Asia, Europe, and North America, all of which kept Asian elephants. The aims were to compare Asian elephant breeding success in different institutions, establish possible causes for any differences, and make recommendations for improving the welfare and breeding success of the animals. The results showed that breeding success in most of the zoos was notably lower and the percentages of stillbirths and infant mortality were relatively higher when compared with those of the institutions in Asia. Female elephants in zoos appeared to reach sexual maturity and reproduce earlier than those in the Asian establishments. However, zoo elephants produced fewer young per female. The different facilities and husbandry methods used are described. Recommendations are made for both short- and long-term changes that could be used to modify existing practices to improve the welfare and breeding success of captive Asian elephants. Zoo Biol 17:311–332, 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.     

Soft and persistent—The influence of sand-flooring and calves on the resting behavior of a zoo-kept African elephant (Loxodonta africana) group

Caring for all aspects of zoo elephants’ well-being is considered a major challenge. Providing an appropriate flooring substrate to facilitate lying rest presents a meaningful part of a holistic management concept. Investigating the impact of a new sand flooring on the nocturnal resting behavior of a breeding group of seven African elephants living at one zoo revealed more total lying rest, longer bouts of lying rest and a reduced side preference in the adult females. With an average total daily lying rest of about 1.5–2.0 hrs, the investigated zoo elephants expressed longer lying rest compared to recently reported data from free-ranging individuals in Botswana. In addition, the presence of nursing calves in the observed elephant group seemed to impact the resting pattern of all group members, with around 60% of all lying bouts being discontinued after interruption by the youngsters. With respect to observed nursing during leaning rest, we encourage the installation of appropriate horizontal structures in breeding facilities to support leaning rest behavior of their female elephants. In doing so, zoos may improve rest quality of nursing females, and, in general, the welfare aspect of sleep for their elephants.     

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.