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Advancing Welfare Science for Reptiles and Amphibians in Zoos and Aquariums

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A special issue of Animals (ISSN 2076-2615). This special issue belongs to the section "Zoo Animals".

Deadline for manuscript submissions: closed (31 March 2022) | Viewed by 43188

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Special Issue Editors

Dr. Grace Fuller

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Guest Editor

Center for Zoo and Aquarium Animal Welfare and Ethics, Detroit Zoological Society, Royal Oak, MI 48067, USA
Interests: animal welfare; zoo research; endocrinology; animal behavior; biomarkers

Jennifer Hamilton

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Guest Editor

Center for Zoo and Aquarium Animal Welfare and Ethics, Detroit Zoological Society, Royal Oak, MI 48067, USA
Interests: animal welfare; zoo; environmental enrichment

Dr. Stephanie Allard

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Guest Editor

National Aquarium, Baltimore, MD 21202, USA
Interests: animal welfare; zoo; aquarium; animal behavior; animal husbandry

Special Issue Information

Dear Colleagues,

Due to their own ethical imperatives, new welfare-focused accreditation standards, and growing public questions regarding the welfare of animals in zoos and aquariums, these institutions are increasingly focused on evaluating and improving the welfare of animals in their care. However, many unanswered questions remain about how to measure and promote the welfare of captive reptiles and amphibians. These taxa pose special challenges to welfare researchers because they often exhibit specialized life history strategies that make them difficult to study (e.g., sit-and-wait predation, fossorial lifestyles); their needs may change radically throughout their lifespans (e.g., metamorphosis, hibernation); or they are often poorly studied (if at all) in the wild or in captivity. This Special Issue of Animals addresses this knowledge gap by broadly considering studies that provide information on evidence-based management, behavior, physiology, or other aspects of captive life for reptiles and amphibians within the context of their overall welfare. We particularly encourage contributors to explore new indicators of welfare specific to these taxa.

Dr. Grace Fuller
Jennifer Hamilton
Dr. Stephanie Allard
Guest Editors

Manuscript Submission Information

Manuscripts should be submitted online at www.mdpi.com by registering and logging in to this website. Once you are registered, click here to go to the submission form. Manuscripts can be submitted until the deadline. All submissions that pass pre-check are peer-reviewed. Accepted papers will be published continuously in the journal (as soon as accepted) and will be listed together on the special issue website. Research articles, review articles as well as short communications are invited. For planned papers, a title and short abstract (about 100 words) can be sent to the Editorial Office for announcement on this website.

Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. Animals is an international peer-reviewed open access semimonthly journal published by MDPI.

Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 2400 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

welfare assessment
herpetology
evidence-based management
welfare indicators
animal behavior
physiology
wellbeing
quality of life
animal care
frogs
toads
salamanders
caecilians
snakes
lizards
turtles
crocodilians
tuatara
amphisbaenians
squamates

Published Papers (9 papers)

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Research

9 pages, 1012 KiB

Open AccessArticle

Impact of Indigestible Materials on the Efficiency of Fecal Corticosterone Immunoassay Testing in Pituophis Species

by Holly Racine, Kinsey Skalican Guthrie, Tyler Hill and Zachary Loughman

Animals 2022, 12(11), 1410; https://doi.org/10.3390/ani12111410 - 30 May 2022

Cited by 3 | Viewed by 1528

Abstract

Measuring fecal glucocorticoid metabolites (FGM) has recently become a sought-after method for assessing stress in animals. While there are many benefits to this methodology, there are also recognized limitations, including the apprehensive interpretation of results. While many factors can influence FGM levels, we aimed to standardize and improve these methods in snakes. Fecal samples were collected from Pituophis species and FGMs were extracted by two different sample collection methods: (1) fecal sample containing undigested materials and (2) fecal samples with undigested materials removed. These extracts were then used to quantify FGM concentrations using a corticosterone EIA kit. The results indicated that the samples with the undigestible materials removed had a 95% increase in overall yield (p < 0.01). Since the collected fecal samples contain 75% undigestible materials by weight, these results support our hypothesis that removing these materials will improve extraction methods for a more reliable measurement of corticosterone. This is the first step towards standardizing the methods for assessing stress by measuring fecal glucocorticoid metabolites in snakes. Full article

(This article belongs to the Special Issue Advancing Welfare Science for Reptiles and Amphibians in Zoos and Aquariums)

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15 pages, 1295 KiB

Open AccessArticle

Using Classical and Operant Conditioning to Train a Shifting Behavior in Juvenile False Water Cobras (Hydrodynastes gigas)

by Michelle L. Williams, Lori A. Torrini, E. Joseph Nolan and Zachary J. Loughman

Animals 2022, 12(10), 1229; https://doi.org/10.3390/ani12101229 - 10 May 2022

Cited by 4 | Viewed by 6360

Abstract

All animals have the capacity to learn through operant conditioning and other types of learning, and as a result, zoos and other animal care facilities have shifted towards the use of positive reinforcement training to shape the behavior of animals under their care. Training offers animals the choice to participate in their own husbandry routines and veterinary procedures, while also providing mental stimulation. By adopting these practices, the welfare of animals in human care has improved, but it has not been applied equally across taxa. Snakes are frequently overlooked in the discussion of choice and control in a captive setting, likely due to the historical misinterpretation of their intelligence and behavioral needs. In this study, a shaping plan was developed for 28 juvenile false water cobras (Hydrodynastes gigas), a rear-fanged venomous species, from four clutches. Snakes were rewarded with food when completing behaviors related to the ultimate goal of following a target into a shift container. The purpose of this study is to incorporate the trained behaviors in routine husbandry practices, while preventing unnecessary stress in the snakes and risk to the keeper. Full article

(This article belongs to the Special Issue Advancing Welfare Science for Reptiles and Amphibians in Zoos and Aquariums)

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17 pages, 2547 KiB

Open AccessArticle

Behavioral Assessment of Six Reptile Species during a Temporary Zoo Closure and Reopening

by Jennifer Hamilton, Kylen N. Gartland, Megan Jones and Grace Fuller

Animals 2022, 12(8), 1034; https://doi.org/10.3390/ani12081034 - 15 Apr 2022

Cited by 7 | Viewed by 3413

Abstract

Although reptiles are commonly housed in zoos and aquariums, their welfare is understudied for the diversity of species housed and the taxon’s current captive population size. The sensory abilities of reptiles have adapted to the varied ecological niches they inhabit, and these evolutionary adaptations impact how reptiles perceive the stimuli around them—including zoo visitors. This study aimed to assess visitor effects on small groups of six reptile species during a temporary zoo closure due to COVID-19 by measuring behavioral diversity, use of space (measured by a spread of participation index), and select behaviors. The species assessed showed diverse responses. The Catalina Island rattlesnakes (Crotalus catalinensis) demonstrated increased investigation and behavioral diversity after the zoo reopened compared to when the zoo was closed, but the European glass lizards (Pseudopus apodus) showed decreases in the amount of time spent exposed to the observers’ view and in their evenness of space use after the zoo was reopened to visitors. The other species, including beaded lizards (Heloderma horridum), Sonoran spiny-tailed iguana (Ctenosaura macrolopha), Arrau turtles (Podocnemis expansa), and dwarf caimans (Paleosuchus palpebrosus), had intermediate changes in their responses to visitor presence. Full article

(This article belongs to the Special Issue Advancing Welfare Science for Reptiles and Amphibians in Zoos and Aquariums)

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14 pages, 2951 KiB

Open AccessArticle

Investigating the Behavior and Personality Structure of the Aldabra Tortoise during Human Interactions and Training Events

by Giovanni Quintavalle Pastorino, Vanessa Smith, Massimo Faustini, Eleonora Bonacina, Davide Guadagnini, Roberto Robbiati, Alice Cavalleri, James Edward Brereton and Richard Preziosi

Animals 2022, 12(4), 419; https://doi.org/10.3390/ani12040419 - 10 Feb 2022

Cited by 2 | Viewed by 2971

Abstract

Human–animal interaction (HAI) can be valuable for captive animals, and many zoo-housed species benefit from interactions with their keepers. There is also an increasing body of evidence that some animal species possess personalities that are temporally consistent. However, the majority of zoo research, particularly on personality and HAI, traditionally has focused on mammals, and there are comparatively fewer studies on reptiles. Research was undertaken at the Faunistic Park Le Cornelle, Italy, to investigate the effects of approach tests and food interaction events on 5 male and 5 female Aldabra tortoise (Aldrabrachelys gigantea) behavior. During human–tortoise interactions, continuous focal sampling of behavior took place. The behavioral differences between individual tortoises, interaction type (approach or training) and person involved in the interaction (keeper, vet, or observer) were analysed using general linear mixed-effects models. The personality components of the tortoises were also quantified using principal component analysis. Overall, the study revealed that individuals acted significantly differently to one another, and that while females initially appeared to display a greater number of shy behaviors, this was not consistent across the group. PCA revealed two personality dimensions in the tortoises: boldness and avoidance. Overall, the study revealed that the tortoises possessed personalities that were independent of sex or scenario. The study also revealed that many tortoises chose to interact with their keepers during training and approach tests: this suggests that human–tortoise interactions may have some enrichment value. Future research could quantify tortoise personality in other scenarios such as in social interactions with other tortoises. Full article

(This article belongs to the Special Issue Advancing Welfare Science for Reptiles and Amphibians in Zoos and Aquariums)

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14 pages, 2087 KiB

Open AccessArticle

Use of Blood Lactate in Assessment of Manual Capture Techniques of Zoo-Housed Crocodilians

by Holly Grace Molinaro, Gen S. Anderson, Lauren Gruny, Emily S. Sperou and Darryl J. Heard

Animals 2022, 12(3), 397; https://doi.org/10.3390/ani12030397 - 08 Feb 2022

Cited by 4 | Viewed by 5182

Abstract

Species-specific welfare indicators are important in promoting positive welfare for zoo animals. Reptiles are a notoriously understudied group in regards to behavior, welfare needs, and husbandry requirements. Using opportunistically obtained samples, we evaluated how blood lactate is affected by variation in manual capture and restraint in crocodilians. Lactate is an indicator of anerobic metabolism in reptiles. It offers a relatively simple and indirect way to assess physiological stress. Determining the best way to reduce struggling during capture and associated stress is of great importance to these species’ overall welfare. Blood samples (N = 53) were collected from 10 different species of crocodilians. It was found that age class was a significant predictor variable of lactate levels after capture, and longer handling time seemed to cause an increase in lactate. Finally, draining enclosure pools for a small number of the captures was associated with higher lactate levels compared to other capture factors that were recorded. This study showed that welfare of captive crocodilians could be improved by shortening the duration of physical restraint events when possible. Developing objective measures of welfare and establishing baseline recommendations for care and handling of crocodilians will ultimately promote and improve their wellbeing, along with that of other understudied reptiles in zoos. Full article

(This article belongs to the Special Issue Advancing Welfare Science for Reptiles and Amphibians in Zoos and Aquariums)

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15 pages, 1422 KiB

Open AccessArticle

Investigating Welfare Metrics for Snakes at the Saint Louis Zoo

by Lauren Augustine, Eli Baskir, Corinne P. Kozlowski, Stephen Hammack, Justin Elden, Mark D. Wanner, Ashley D. Franklin and David M. Powell

Animals 2022, 12(3), 373; https://doi.org/10.3390/ani12030373 - 03 Feb 2022

Cited by 6 | Viewed by 3332

Abstract

Modern herpetoculture has seen a rise in welfare-related habitat modifications, although ethologically-informed enclosure design and evidence-based husbandry are lacking. The diversity that exists within snakes complicates standardizing snake welfare assessment tools and evaluation techniques. Utilizing behavioral indicators in conjunction with physiological measures, such as fecal glucocorticoid metabolite concentrations, could aid in the validation of evidence-based metrics for evaluating snake welfare. We increased habitat cleaning, to identify behavioral or physiological indicators that might indicate heightened arousal in snakes as a response to the disturbance. While glucocorticoid metabolite concentrations increased significantly during a period of increased disturbance, this increase was not associated with a significant increase in tongue-flicking, a behavior previously associated with arousal in snakes. Locomotion behavior and the proportion of time spent exposed were also not affected by more frequent habitat cleaning. These results demonstrate the need to further investigate the behavioral and physiological responses of snakes to different aspects of animal care at a species and individual level. They also highlight the need to collect baseline behavioral and physiological data for animals, in order to make meaningful comparisons when evaluating changes in animal care. Full article

(This article belongs to the Special Issue Advancing Welfare Science for Reptiles and Amphibians in Zoos and Aquariums)

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14 pages, 1920 KiB

Open AccessArticle

Out of Sight, Out of Mind or Just Something in the Way? Visual Barriers Do Not Reduce Intraspecific Agonism in an All-Male Group of Nile Crocodiles (Crocodylus niloticus)

by Austin Leeds, Alex Riley, Megan Terry, Marcus Mazorra, Lindsay Wick, Scott Krug, Kristen Wolfe, Ike Leonard, Andy Daneault, Andrew C. Alba, Angela Miller and Joseph Soltis

Animals 2022, 12(3), 269; https://doi.org/10.3390/ani12030269 - 22 Jan 2022

Cited by 2 | Viewed by 2767

Abstract

Here, we evaluated if visual barriers could reduce intraspecific agonism in an all-male group of Nile crocodiles (Crocodylus niloticus) living in a zoo. Crocodiles were monitored for nearly 100 h, and four “hotspots” of aggression within their exhibit were identified. Within these four locations, visual barriers were placed at the surface of the water with the goal of reducing agonism by targeting sight lines associated with their species-typical minimum exposure posture, where crocodiles submerge their body but maintain facial sensory organs above the water line. Crocodile behavior was then monitored for 226 h, evaluating both short- and long-term effects of the visual barriers. In both observation periods, intraspecific agonism was unaffected by visual barriers. However, crocodiles were more likely to be on land and closer together, after the barriers were installed, showing the barriers affected nonagonistic behaviors. Monitoring of such unintended effects is significant to ensure no welfare concerns are created in any exhibit or husbandry modification attempt. Additionally, time of day and temperature were significant predictors of behavior, highlighting the importance of such factors in the analysis of reptilian behavior. While ineffective at reducing agonism, this is the first published study evaluating exhibit design and behavior of crocodilians in zoos and aquariums. The methodologies and findings here should provide useful information for future behavioral and welfare studies of this understudied taxa. Full article

(This article belongs to the Special Issue Advancing Welfare Science for Reptiles and Amphibians in Zoos and Aquariums)

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20 pages, 4006 KiB

Open AccessArticle

Identification of Animal-Based Welfare Indicators in Captive Reptiles: A Delphi Consultation Survey

by Alexandra L. Whittaker, Brianna Golder-Dewar, Jordyn L. Triggs, Sally L. Sherwen and David J. McLelland

Animals 2021, 11(7), 2010; https://doi.org/10.3390/ani11072010 - 05 Jul 2021

Cited by 17 | Viewed by 7090

Abstract

There is an increasing focus on evidence-based welfare assessment by animal care staff in zoos, along with a strong interest in animal welfare by the zoo-visiting public, to the extent that this can influence their choice of institutions to visit. Regulatory oversight of animal welfare standards continues to strengthen across many jurisdictions. Zoos are increasingly formalizing their practices with the development and refinement of evidence-based welfare assessment tools. There has been a drive for welfare assessment tools to comprise both resource-based and animal-based measures. However, animal-based indicators are not always well characterized, in terms of their nature and whether they infer a positive or negative affective state. This is especially so for reptiles, which are often considered behaviorally inexpressive and are under-researched. In this study, a Delphi consultation approach was used to gather expert opinion on the suitability of potential animal-based indicators of welfare for inclusion in a welfare assessment tool across four families of reptiles: Agamidae, Chelidae, Pythonidae, and Testudinidae. Two rounds of online surveys were conducted eliciting responses from a global group of professionals who work with reptiles. In the first survey, respondents were provided with an author-derived list of potential animal-based indicators for consideration of their validity and practicality as welfare indicators. The indicators were refined for the second survey including only those indicators that were considered valid or practical on the first survey (≥4 on a 5-point Likert scale), and that achieved ≥70% consensus amongst experts. In the second survey, respondents were asked to re-evaluate the reliability and practicality of the indicators and to rank them on these facets. Eight to ten assessment indicators for each family of reptiles were identified from Survey 2. These indicators were often health related, for example, presence of oculo-nasal discharge or wounds. However, some true behavioral indicators were identified, such as showing species-specific interest and alertness. These indicators should now be incorporated into taxon-tailored welfare assessment tools for trial and validation in captive reptile populations. This study provides a next step towards developing reptile-specific animal welfare assessment tools for these often-overlooked animals. Full article

(This article belongs to the Special Issue Advancing Welfare Science for Reptiles and Amphibians in Zoos and Aquariums)

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16 pages, 1108 KiB

Open AccessArticle

Bold Frogs or Shy Toads? How Did the COVID-19 Closure of Zoological Organisations Affect Amphibian Activity?

by Jack Boultwood, Michelle O’Brien and Paul Rose

Animals 2021, 11(7), 1982; https://doi.org/10.3390/ani11071982 - 02 Jul 2021

Cited by 19 | Viewed by 7203

Abstract

Amphibians are an understudied group in the zoo-focussed literature. Whilst commonly housed in specialist exhibits and of real conservation value due to the global extinction crisis, amphibian welfare is not often investigated empirically in zoo settings. The limited research that is available suggests that enclosure design (structure, planting and naturalistic theming) has a positive impact on the time that amphibians will be on show to visitors. However, the categorisation of any “visitor effect” (i.e., influences of visitor presence on amphibian activity and time on display) is hard to find. The COVID-19 pandemic forced the closure of zoological organisations in the UK for several months from March 2020, with gradual re-openings from the summer into autumn and winter. This event provided a unique opportunity to study the effect of the lack of visitors, the presence of essential zoo staff only, the wider return of organisational staff, and then the return of visitors over a prolonged period. This project at WWT Slimbridge Wetlands Centre assessed the number of individuals of six species of amphibian—common toad (Bufo bufo), common frog (Rana temporaria), smooth newt (Lissotriton vulgaris), pool frog (Pelophylax lessonae), golden mantella (Mantella aurantiaca) and golden poison dart frog (Phyllobates terribilis)—visible to observers under different conditions. All amphibians were housed in a purpose-built indoor exhibit of individual enclosures and were recorded when visible (as a proportion of the total population of the enclosure) during closure, the return of extra centre staff and visitor periods. The results showed species-specific differences in visibility, with some species of amphibian being more likely to be on view when the presence of people at their enclosure was less likely or in smaller numbers. Such differences are likely related to the specific camouflage or anti-predation tactics in these focal species. Further study to quantify amphibian sensitivity to, and perception of, environmental change caused by public presence (e.g., light levels and sound) would be useful welfare-themed research extensions. Our results can help inform husbandry, collection planning and amphibian enclosure design to reduce any noticeable visitor effects, and provide a useful benchmark for further, more complex, welfare assessment measures. Full article

(This article belongs to the Special Issue Advancing Welfare Science for Reptiles and Amphibians in Zoos and Aquariums)

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