Genotyping on the ark: A synthesis of genetic resources available for species in zoos

Using molecular genetic information to guide population management can improve the sustainability of species in captivity. However, empirical population genetics has not been commonly applied to species management programs in zoos. One limitation may be the availability of genetic resources (e.g., markers, primers, etc.) for species held in zoos. To assess the extent to which species held in zoos have been studied using population genetics in the wild, we conducted a systematic literature review of close to 8,000 papers. We synthesized information on the availability and scale of population genetics studies across amphibian, bird, mammal, and reptile species held in zoos, and discussed their potential for informing ex situ management. We found that more than half of the species in zoos (52%) already have some genetic markers described in the literature specific for them, or a congeneric species, that could be further developed to aid the management of zoo populations, and the accumulation of these resources has been steady over the past decades. Furthermore, the proportion of species with genetic resources is even higher (62%) for species that are being managed through a formal breeding program in zoos. Our study provides encouraging results for captive program managers interested in integrating population genetics into ex situ management strategies.     

Biology of Animal Stress: Implications for Animal Well-Being

What is environmental enrichment? During the last several decades, zoos and aquariums have come to realize (perhaps belatedly) that animals kept in captivity need environmental enrichment for their well-being (Seidensticher &; Forthman, 1998). Early zoos and aquariums tried to show as many animals as possible; hence, their exhibits were frequently small and bare to permit easy viewing, cleaning, and sterilization. Now, all have come to realize that captive animals need environmental enrichment for their health and for the education and increased expectations of visitors to zoos and aquariums.     

Enrichment for Giant Pacific Octopuses: Happy as a Clam?

What is environmental enrichment? During the last several decades, zoos and aquariums have come to realize (perhaps belatedly) that animals kept in captivity need environmental enrichment for their well-being (Seidensticher & Forthman, 1998). Early zoos and aquariums tried to show as many animals as possible; hence, their exhibits were frequently small and bare to permit easy viewing, cleaning, and sterilization. Now, all have come to realize that captive animals need environmental enrichment for their health and for the education and increased expectations of visitors to zoos and aquariums.     

A review of applications of environmental DNA for reptile conservation and management

Reptile populations are in decline globally, with total reptile abundance halving in the past half century, and approximately a fifth of species currently threatened with extinction. Research on reptile distributions, population trends, and trophic interactions can greatly improve the accuracy of conservation listings and planning for species recovery, but data deficiency is an impediment for many species. Environmental DNA (eDNA) can detect species and measure community diversity at diverse spatio‐temporal scales, and is especially useful for detection of elusive, cryptic, or rare species, making it potentially very valuable in herpetology. We aim to summarize the utility of eDNA as a tool for informing reptile conservation and management and discuss the benefits and limitations of this approach. A literature review was conducted to collect all studies that used eDNA and focus on reptile ecology, conservation, or management. Results of the literature search are summarized into key discussion points, and the review also draws on eDNA studies from other taxa to highlight methodological challenges and to identify future research directions. eDNA has had limited application to reptiles, relative to other vertebrate groups, and little use in regions with high species richness. eDNA techniques have been more successfully applied to aquatic reptiles than to terrestrial reptiles, and most (64%) of studies focused on aquatic habitats. Two of the four reptilian orders dominate the existing eDNA studies (56% Testudines, 49% Squamata, 5% Crocodilia, 0% Rhynchocephalia). Our review provides direction for the application of eDNA as an emerging tool in reptile ecology and conservation, especially when it can be paired with traditional monitoring approaches. Technologies associated with eDNA are rapidly advancing, and as techniques become more sensitive and accessible, we expect eDNA will be increasingly valuable for addressing key knowledge gaps for reptiles.     

A Case Study of Malayan Tapir (Tapirus indicus) Husbandry Practice Across 10 Zoological Collections

The Malayan, or Asian, tapir (Tapirus indicus) has a diminishing wild population and is becoming more common in captivity as zoos attempt to manage sustainable ex situ populations. Tapirs can be relatively easy to maintain and breed, but captive animals appear to suffer from reduced activity budgets, obesity, and poor public image. A questionnaire‐based survey was designed and sent specifically to 10 collections around the world that exhibit Malayan tapirs, with the aim of assessing husbandry regimes to determine prevalence of standardized practices as well as highlighting any key differences, and to showcase good practice, thus providing information beneficial to those maintaining this species in their zoo. Twenty‐five animals were included in the survey from collections across four continents. The research's major conclusions show differing dietary make‐up, with a lack of forage provision, contrasting with a diverse array of enrichment protocols used. Significant differences were noted between zoos for total amount of food offered (P = 0.000) as well as ratios of forage to concentrate pellet offered (P = 0.004). Comparing food offered to male and female tapirs with published requirements for an “average” of either gender shows not all zoos providing the amount suggested in husbandry guidelines. Intelligently designed and original enrichment was provided to all animals but differences between zoos were noted in the application and “usefulness” of enrichment for individual tapir. Overall, animals are benefiting from enrichment but welfare could be further improved via consistent feeding of ad libitum forage and regular use of browse as a constituent part of daily rations. Zoo Biol. 32:347–356, 2013. © 2012 Wiley Periodicals, Inc.     

Aging in snakes: Results of long-term captivity on rattlesnake (Crotalus viridis oreganus) predatory behavior

Conservation, scientific study, rehabilitation, and public education concerning animals often require or take advantage of captive individuals. The long-term effects of captivity may affect the success and strategies used in such programs. For reptiles in particular, little is known about the effects of long-term captivity. We compared the predatory behavior of the same eight Northern Pacific Rattlesnakes before and after 7 years in captivity. We found few changes in predatory behavior. Most changes were in the rate of tongue flicks before the strike and during recovery of prey; these changes seemed related to accommodation of the snakes to conditions of captivity. However, most aspects of rattlesnake predatory behavior remained unchanged, including the normal ability to target the prey accurately and kill it quickly. Although the snakes had spent over half their lives in captivity and reached a relatively old age, their ability to strike, dispatch, and relocate prey normally was relatively unaffected by captivity or by aging. © 1994 Wiley-Liss, Inc.     

Identifying key conservation sites for the reptiles of the Tandilia mountains in Pampas highlands

Reptile populations are facing a global decline as a consequence of anthropic disturbs. For its conservation, it is necessary to know its geographical distribution and the main factors influencing it. Tandilia Mountains are located in the centre of Buenos Aires province, Argentina. These mountains contain high biodiversity and several endemic species, but the current Natural Protected Areas network covers a low area of ​​0.12 %. In this work, we modelled the geographic distribution of reptiles in the Tandilia Mountains to: a) explore the environmental factors affecting the distribution of reptiles on the highland grasslands of the Tandilia Mountain System and (b) identify the key biodiversity areas. We used ten environmental variables and several sources of records (fieldwork, scientific literature, museum collections, and an online database) to model the distribution of each reptile species. The best sites to propose natural reserves were determined in Zonation software. We determined the representativeness of the current system of Natural Protected Areas in the Tandilia Mountain range by overlapping the sites with the Zonation results. We obtained 20 species distribution models with two general patterns: continuous and patched. In most species, the two most informative variables were growing degree-days below 0 °C and precipitation of the wettest quarter. The current system of Natural Protected Areas of the Tandilia Mountains covers 0.35 % of the conservation priority sites (4341 km²) and therefore is insufficient in protecting reptile biodiversity.     

Late Quaternary reptile extinctions: size matters,insularity dominates

Aim A major Late Quaternary vertebrate extinction event affected mostly large‐bodied ‘megafauna’. This is well documented in both mammals and birds, but evidence of a similar trend in reptiles is scant. We assess the relationship between body size and Late Quaternary extinction in reptiles at the global level. Location Global. Methods We compile a body size database for all 82 reptile species that are known to have gone extinct during the last 50,000 years and compare them with the sizes of 10,090 extant reptile species (97% of known extant diversity). We assess the body size distributions in the major reptile groups: crocodiles, lizards, snakes and turtles, while testing and correcting for a size bias in the fossil record. We examine geographical biases in extinction by contrasting mainland and insular reptile assemblages, and testing for biases within regions and then globally by using geographically weighted models. Results Extinct reptiles were larger than extant ones, but there was considerable variation in extinction size biases among groups. Extinct lizards and turtles were large, extinct crocodiles were small and there was no trend in snakes. Lizard lineages vary in the way their extinction is related to size. Extinctions were particularly prevalent on islands, with 73 of the 82 extinct species being island endemics. Four others occurred in Australia. The fossil record is biased towards large‐bodied reptiles, but extinct lizards were larger than extant ones even after we account for this. Main conclusions Body size played a complex role in the extinction of Late Quaternary reptiles. Larger lizard and turtle species were clearly more affected by extinction mechanisms such as over exploitation and invasive species, resulting in a prevalence of large‐bodied species among extinct taxa. Insularity was by far the strongest correlate of recent reptile extinctions, suggesting that size‐biased extinction mechanisms are amplified in insular environments.     

Predation upon reptiles in Mediterranean habitats of Chile,Spain and California: A comparative analysis

Summary Pradation on reptiles at three Mediterranean-type habitat sites was assessed by computing the incidence of reptiles as a percentage of vertebrates in the diet of each predator species and the incidence of each reptile species as prey for the entire assemblage of predators at each locality. The overall importance of reptiles is lowest in Chile, intermediate in California, and highest in Spain. These differences do not appear to result from interlocality variation in the size distributions of predators or of prey. The incidence of particular reptile species as prey is correlated with their relative abundances in Spain and California, but not in Chile. Behavioral and morphological attributes evidently make some species more vulnerable to predation and others less so than their abundances would predict. Predation on the speciose lizard genus Liolaemus in Chile is sufficient to promote behavioral responses but not major morphological divergence.     

An assessment of gum-based environmental enrichment for captive gummivorous primates

In the wild, many primates consume gums exuded from trees, and many species are gum specialists. In spite of this, few data exist concerning gum feeding in captivity. Using a web-based survey of 46 zoos in 12 countries, we evaluated the extent to which zoos feed gum to primates. We found that although callitrichids and galagos receive gum-based enrichment, cercopithecines generally do not. Environmental enrichment is important for stimulating naturalistic behavior to promote the psychological wellbeing of animals. Thus, gum-based enrichment is important for captive gummivores. Our study highlights the need to improve environmental enrichment for captive gummivores, in particular that of cercopithecines. This is most striking for the patas monkey (Erythrocebus patas), an obligate gummivore. The exchange of ecological data between field research and captive settings is crucial, and is just one way primate caretakers can contribute to the conservation and welfare of some of our closest living relatives.     

Experimental evaluation of environmental enrichment of sea turtles

Although behavioral studies have been conducted at zoos and aquaria for years, documentation concerning the effectiveness of environmental enrichment has dealt primarily with terrestrial animals and marine mammals. Few enrichment studies have been conducted on reptiles. For this study, behavioral observations were made on four captive sea turtles (three loggerhead, Caretta caretta, and one blind green, Chelonia mydas) with enrichment present and absent. Enrichment devices were modified for the special needs of the blind turtle. Behaviors were classified as Resting, Pattern Swimming, Random Swimming, Focused Behavior, Aggression, Hiding, Orientation, and Noncategorized Behavior. It was hypothesized that, when enrichment was present, a decrease in Resting and stereotypic Pattern Swimming would be seen along with an increase in Random Swimming and Focused Behavior. It was found that, when no enrichment devices were present, 77% of the turtles' time was spent in Resting and Pattern Swimming. When enrichment devices were provided, 88% of their time was spent in Random Swimming and Focused Behavior with only 8% spent in Pattern Swimming and Resting. Statistically, there were significant increases in Random Swimming (three of the four turtles) and Focused Behavior (4/4) and significant decreases in Resting (3/4) and Pattern Swimming (3/4) when enrichment devices were present. These results suggest that environmental enrichment is as effective with marine reptiles as has been found with other animals and should be encouraged for all captive sea turtles. Zoo Biol 26:407–416, 2007. © 2007 Wiley‐Liss, Inc.     

Reptile Ownership in Balkan Countries: Demographics and Reliance on Veterinary Advice

The objective of the research was to determine the profile of reptile owners (n = 238) in terms of their socio-demographic characteristics and evaluations of veterinarians’ expertise. Reptile owners living in four non-EU Balkan countries (Bosnia and Herzegovina, Macedonia, Montenegro, and Serbia) were randomly selected from two social networks. Statistically significant differences were found in snake, lizard, and turtle owners (p < 0.05) in terms of gender, employment status, and monthly earnings. Male owners of reptiles were slightly more numerous (52%) compared with female owners (48%). Sixty-four percent of reptile owners were over 20 years old. The unemployed reptile owners (16%) were about five times fewer in number compared with those who studied at university and those who were employed. Forty-one percent of reptile owners declared high monthly incomes. Forty percent of reptile owners never contacted and had no experience with veterinarians. Fifty-eight percent of reptile owners contacted or visited veterinarians due to the medical condition of their animals, 14% of them contacted veterinarians for advice on reptile keeping, and only 6% did so for a preventive veterinary examination. Forty-seven percent of reptile owners were satisfied with veterinary services. The importance of the results of this survey is that they can provide a basis for adopting legislation on the ownership of reptiles as pet animals, together with being a baseline for monitoring subsequent changes in interest in these animals as pets. The results also identify the need for more dedication from veterinarians in educating reptile owners, and for necessary adjustments in veterinary education.     

Influence of incubation temperature on hatchling phenotype in reptiles

Incubation temperature influences hatchling phenotypes such as sex, size, shape, color, behavior, and locomotor performance in many reptiles, and there is growing concern that global warming might adversely affect reptile populations by altering frequencies of hatchling phenotypes. Here I overview a recent theoretical model used to predict hatchling sex of reptiles with temperature-dependent sex determination. This model predicts that sex ratios will be fairly robust to moderate global warming as long as eggs experience substantial daily cyclic fluctuations in incubation temperatures so that embryos are exposed to temperatures that inhibit embryonic development for part of the day. I also review studies that examine the influence of incubation temperature on posthatch locomotion performance and growth because these are the traits that are likely to have the greatest effect on hatchling fitness. The majority of these studies used artificial constant-temperature incubation, but some have addressed fluctuating incubation temperature regimes. Although the number of studies is small, it appears that fluctuating temperatures may enhance hatchling locomotor performance. This finding should not be surprising, given that the majority of natural reptile nests are relatively shallow and therefore experience daily fluctuations in incubation temperature.     

Unsafe management of a zoological garden as a cause of introduction of an alien species into the wild: First documented case of feral naturalized population of Lama glama in Europe

Zoological gardens host large numbers of wild species and domestic forms, mostly not indigenous to the place where the zoological garden is located. Escapes (or releases) from zoological gardens are recognized as a pathway of introduction of alien species, leading in some cases to a naturalized population. Although previously reported worldwide, scientific accounts of escapes from zoos are rare and often anecdotal. In this note, we document, for the first time in Europe and, to our knowledge, in an area outside its native range, a case of introduction and establishment of a feral population of Llama (Lama glama), originating from a group of animals living in captivity at the Zoological Park of Cavriglia (Tuscany, central Italy). We reconstruct in detail the story of the population since 1974, also reporting preliminary data on abundance, distribution and diet. Finally, we critically evaluate the causes of this introduction, highlighting how unsafe the management of a zoological garden can be, and we discuss the implications for conservation and management perspectives.     

Isolation of Salmonella from environmental samples collected in the reptile department of Antwerp Zoo using different selective methods

AIMS: To evaluate the environmental spread of Salmonella strains in the reptile department of Antwerp Zoo and to compare different isolation methods for Salmonella. METHODS AND RESULTS: One hundred environmental samples were collected in the service sections and public spaces of the reptile department. After pre-enrichment in buffered peptone water (BPW), selective enrichment was performed in Rappaport Vassiliadis Single Component Enrichment Broth (RVS), Selenite Cystine Broth (SEL) and Mueller Kauffman Tetrathionate Broth (MKTTn). Subculturing on Modified Semisolid Rappaport-Vassiliadis (MSRV) Medium, and the combined use of immunomagnetic separation (IMS) and RVS was evaluated. The isolation media used were Hektoen Enteric Agar (HE), Phenol Red Brilliant Green Agar (BG) and Xylose Lysine Decarboxylase Agar (XLD). Salmonella strains were found in 47 samples (47.0%). Most isolations were made on HE after combined IMS/RVS enrichment. Sixty-six Salmonella strains were serotyped, 29 belonged to Salmonella enterica ssp. enterica (I), 3 to ssp. salamae (II), 29 to ssp. arizonae or diarizonae (IIIa/b), 4 to ssp. houtenae (IV) and 1 strain showed autoagglutination. In addition, a 10-year survey (1995-2004) of Salmonella serovars isolated from reptiles at Antwerp Zoo is presented. CONCLUSIONS: A high prevalence of Salmonella strains was noted in the service sections of the reptile department. Only a few isolations were made in the public spaces. Selective enrichment in RVS was the most efficient. In combination with IMS, this method gave an even higher isolation rate than the International Standard method (ISO 6579:2002). SIGNIFICANCE AND IMPACT OF THE STUDY: This study confirms the importance of reptiles as spreaders of Salmonella in their surroundings. The possible infectious risks for zoo personnel and visitors are evaluated. Improved laboratory protocols for the isolation of Salmonella from the environment are suggested.     

Surveying Attitudes toward Reptiles on Roads: Questionnaire Responses Do Not Directly Translate to Behavioral Action

Roads pose significant threats to reptiles, and understanding the varying perceptual biases of motorists to different taxa may help determine management strategies for urban roads around important refuges such as wetlands. We surveyed Western Australian motorists online, asking them to rank their degree of concern for animal welfare, vehicle damage, and personal safety when hypothetically involved in a vehicle collision with 10 different animal taxa, including reptiles. Respondents also ranked their rescue likelihood for these taxa. We then observed motorist responses to snakes and lizards in the field, where we placed rubber models and controls on the shoulder of an urban road bordering a wetland in Perth, Western Australia. We also estimated the probability of a reptile being struck while crossing the study road at two different road vehicle densities. The online survey respondents claimed high mean concern for the welfare of animals on roads (M = 8.02 ± 2.73 SD out of 10) and low concern for vehicle damage (M = 2.87 ± 2.75) and personal safety (M = 2.91 ± 2.88). Respondents also claimed high mean rescue likelihood (M = 7.06 ± 3.40). In contrast, motorists observed in the field generally ignored objects, including reptiles, on the roadside (79% of n = 1,500). There were no observed intentional strikes on reptiles, one motorist made a rescue attempt (bobtail lizard), and all other responses were to slow down or move away from the treatment. Estimates of strike probability for a reptile crossing the study road at a low traffic volume (2.23 vehicles·min^-1) was > 75% for slow-moving (1 m·min^-1) reptiles, but reduced to ≤ 16% if they were moving quickly (60 m·min^-1). Although motorists did not intentionally strike model reptiles, surveyed attitudes did not directly translate to behavioral action, and crossing a road is risky for an urban reptile.     

World Zoo Conservation Strategy: a blueprint for zoo development

People need a sense of purpose, the setting of clear targets, the encouragement and support of others in striving for and achieving tasks that have been set. This is particularly true for zoo personnel, a profession which is often under critical attack, especially from those who have a philosophical difficulty in accepting the idea of animals in captivity. The zoo world, with its huge number of collections and in excess of 600 million annual visitors, represents a grossly under-utilized force for the conservation of endangered species, for the development of scientific knowledge and the increase of public awareness through environmental education programmes. With targets before them, zoos can better provide, maintain and develop their full potential for the good of conservation. The World Zoo Conservation Strategy (WZCS) is not a new beginning, but a codification of the existing activities of responsible zoos, with the purpose of reminding all zoos and their supporters of the Mission Aims, which they should embrace and develop. It forms a set of standards of activity against which zoos can judge themselves and be judged by others. Zoological collections' ability to achieve the obligations of the WZCS will depend on public support. The Strategy, whilst setting the activity priorities, is also one which will evolve to meet the changing demands of the conservation world.     

Estimated number of snake species that can be managed by Species Survival Plans in North America

A survey designed to estimate the number of snake enclosures available for Species Survival Plan (SSP) programs was distributed to all North American zoos containing 100 or more reptile and amphibian specimens. Of the 52 zoos surveyed, 44 (84.6%) responded, indicating that 790 (26.3%) of the 3,012 snake enclosures were available for SSP programs. Available enclosures were classified by size and existing themes to help define limitations of the potential SSP space. This spatial information was then used in conjunction with existing population genetics models to estimate that up to 16 snake species can be accommodated by SSP programs in these zoos collectively. Values used in the models were estimates of those for an average snake species with a generation time of 15 years, lambda of 1.15, with 26 effective founders, and an n_e/n ratio of 0.3. It was further assumed that 90% of the genetic variation would be maintained in each species for a period of 100 years. Tactics to increase the number of species that SSP programs can accommodate include: increase reserve space, devote more space for SSP snakes, lengthen generation time, promote gene exchange with wild populations, goal SSP programs for less than 200 years, invest in short-term programs, involve the private sector, build new enclosures, increase the number of snakes per enclosure, and encourage participation of non-North American institutions. To maximize biological diversity in relation to captive carrying capacity, it is recommended that SSP programs represent both infraorders of living snakes and as many families within those infraorders as possible. Although not all 16 families of snakes are likely to be represented due to exhibit value, obtainability, and husbandry success, it may be possible to represent as many as nine families in 16 SSP programs. © 1993 Wiley-Liss, Inc.     

The biogeographical assignment of a west Kenyan rain forest remnant: further evidence from analysis of its reptile fauna

Aim The Kakamega Forest, western Kenya, has been biogeographically assigned to both lowland and montane forest biomes, or has even been considered to be unique. Most frequently it has been linked with the Guineo‐Congolian rain forest block. The present paper aims to test six alternative hypotheses of the zoogeographical relationships between this forest remnant and other African forests using reptiles as a model group. Reptiles are relatively slow dispersers, compared with flying organisms (Aves and Odonata) on which former hypotheses have been based, and may thus result in a more conservative biogeographical analysis. Location Kakamega Forest, Kenya, Sub‐Saharan Africa. Methods The reptile diversity of Kakamega Forest was evaluated by field surveys and data from literature resources. Faunal comparisons of Kakamega Forest with 16 other African forests were conducted by the use of the ‘coefficient of biogeographic resemblance’ using the reptile communities as zoogeographic indicators. Parsimony Analysis of Endemism and Neighbour Joining Analysis of Endemism were used to generate relationship trees based on an occurrence matrix with paup *. Results The analysis clearly supports the hypothesis that the Kakamega Forest is the easternmost fragment of the Guineo‐Congolian rain forest belt, and thus more closely related to the forests of that Central–West African complex than to any forest further east, such as the Kenyan coastal forests. Many Kenyan reptile species occur exclusively in the Kakamega Forest and its associated forest fragments. Main conclusions The Kakamega Forest is the only remnant of the Guineo‐Congolian rain forest in the general area. We assume that the low degree of resemblance identified for the Guineo‐Congolian forest and the East African coastal forest reflect the long history of isolation of the two forest types from each other. Kenyan coastal forests may have been historically connected through forest ‘bridges’ of the southern highlands with the Congo forest belt, allowing reptile species to migrate between them. The probability of a second ‘bridge’ located in the region of southern Tanzanian inselbergs is discussed. Although not particularly rich in reptile species, the area should be considered of high national priority for conservation measures.     

Protective and territorial behavior in captive siamangs (Hylobates syndactylus)

Protective and territorial behavior was observed in 14 heterosexual pairs of adult siamangs in 11 zoos for a total of 1,155 h. The study shows that the quality of protective and territorial behavioral patterns was similar in the wild and in captivity. Under zoo conditions, the behavioral response (except calling) to conspecific and human rivals was similar. Males could be found more often at the front of the enclosure and were more active in protective and territorial behavior than were females. Males were more attentive to happenings outside their enclosures than were their mates, whereas females concentrated their protective and territorial activities on specific people or females of a conspecific group. Although the duration of each song and the average number of duet sequences as well as the temporal distribution of calling throughout the day were similar in the wild and in the zoo, the total duetting rate differed remarkably: it was much higher in captivity. Siamangs in acoustical and visual contact with neighboring conspecifics spent more time singing than did siamangs without such contacts. In captivity, pairs without young seemed to be more engaged in protective and territorial behavior patterns than were parents. Zoo Biol 16:309–325, 1997. © 1997 Wiley-Liss, Inc.