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Introduction
In his work with the zoo sector, Christopher Michaels focuses on producing novel science to underpin conservation, husbandry and organisational practice, as well as to build scientific capacity within zoos through training, mentorship and the estabishment of collaborative projects. His primary taxonomic focus is on reptiles and amphibians, but he has worked on a broad range of groups, from mammals, to birds, to invertebrates. Chris also works in health economic, evidence synthesis and HTA.
Publications
Publications (100)
Environmental enrichment is a powerful tool in maintaining positive welfare for captive animals but investigation of this in reptiles has been limited. Monitor lizards are active, intelligent animals that represent high priority targets for enrichment in a captive setting, but more data are required to develop evidence-based recommendations and to...
At the time of our research in 2022, 16.4% of amphibian species on the IUCN Red List were assessed as Data
Deficient (DD). There is minimal funding allocated to the research and reassessment of DD taxa, this prevents them from being
prioritised for conservation. We identified 656 non-DD amphibian species that were previously assessed as DD and us...
As the most threatened vertebrate class on earth, amphibians are at the forefront of the biodiversity crisis, with the recognition of global amphibian declines and extinctions dating back several decades now. The current Amphibian Conservation Action Plan is adopting two strategies to address the goal of the amelioration of the amphibian crisis: th...
In the face of overwhelming and sometimes acute threats to many amphibians, such as disease or habitat destruction, the only hope in the short-term for populations and species at imminent risk of extinction is immediate rescue for the establishment and management of captive survival-assurance colonies (CSCs). Such programmes
are not the final solut...
A 15-year data set of reptile observations at corrugated iron refuges was analysed to describe the spatial and temporal associations between species pairs of viviparous lizards Zootoca vivipara, slow worms Anguis fragilis, northern vipers Vipera berus and grass snakes Natrix helvetica. Of the two snake species, only the viper is known as a routine...
Visual systems adapt to different light environments through several avenues including optical changes to the eye and neurological changes in how light signals are processed and interpreted. Spectral sensitivity can evolve via changes to visual pigments housed in the retinal photoreceptors through gene duplication and loss, differential and coexpre...
Turtles are a globally threatened group of reptiles. Zoo populations may contribute to the conservation of species, including turtles, but collection composition may not align with conservation needs. We combined data from the Zoological Information Management System (ZIMS), EDGE of Existence, the IUCN Red List and the Reptile Database to investiga...
Reptiles are sensitive to electromagnetic radiation at wavelengths between the ultra-violet and infrared bands. Husbandry practitioners designing artificial lighting arrays should aim to provide spectra that approximate those to which a given species has become adapted in nature. This would satisfy biological needs ranging from thermoregulation and...
We followed a standard skeletochronology protocol to assess the age of 17 Oreolalax sterlingae, an Endangered frog from Viet Nam, through the count of lines of arrested growth (LAGs).
The information in this Best Practice Guideline has come from a variety of sources including a literature review, the experience of the authors and others in the captive husbandry of Xenopus longipes as well as direct observations of the species in the field. Amphibian husbandry is a rapidly evolving field and there are many aspects that require fu...
Mountain chicken frogs Leptodactylus fallax are assessed as Critically Endangered on the IUCN Red List due to threats including chytridiomycosis and habitat loss. Ex-situ populations underpin species survival, but captive management is hampered by incomplete species knowledge, including its behavioural biology. In sixteen adult frogs, we investigat...
Ex situ amphibian populations are a key component of global amphibian conservation strategy, and optimal husbandry is vital to ex situ conservation success. Animal behavior can be used to inform captive welfare and improve husbandry practices. However, it has been little used for amphibians compared with mammals and birds. The goal of this study wa...
Captivity can provide a resource-rich environment for snakes which may lead to over-conditioning of individuals. We compared
captive and wild populations of Bitis arietans to see if a difference in scaled mass index (SMI) existed between the samples.
Male B. arietans had significantly higher SMI in captivity than in the wild; there was no differe...
The interest in the welfare of zoo animals, from both the public and the scientific community, has long been biased towards mammals. However, growing evidence of the complex behavioural repertoires of less charismatic animals, such as reptiles, reveals the necessity to better comply with their welfare needs in captivity. Here, we present the effect...
Captive insectivore nutrition is challenging due to the differing nutritional profiles of wild and captive diets and an incomplete understanding of both. Ultraviolet B (UVB)-irradiation has recently been explored as a means of improving prey-insect vitamin D3 and Ca content. Although short-term irradiation has been successful in some species, it ha...
Sexual dimorphism is commonly encountered in amphibians. Its presence and its ontogeny in a given species has implications for ecology, conservation and captive husbandry. We monitored changes in length and mass of captive mountain chicken frogs Leptodactylus fallax. Initially, sexes were no different in snout-vent length or mass, but by about 17 m...
Amphibians are challenging to mark for recapture due to their small size and permeable, sensitive, and often frequently shed skins. Photographic identification and pattern matching techniques are increasingly used as a non-invasive method to identify individual amphibians for the purposes of monitoring individuals over time. The Critically Endanger...
Animal behavior and welfare science can form the basis of zoo animal management. However, even basic behavioral data are lacking for the majority of amphibian species, and species-specific research is required to inform management. Our goal was to develop the first ethogram for the critically endangered frog Xenopus longipes through observation of...
The information in this Best Practice Guideline has come from a variety of sources
including a literature review, the experience of the authors and others in the captive
husbandry of Typhlonectes spp. and Potomotyphlus caecilians; a caecilian husbandry
questionnaire that involved both zoological collections, aquariums and keepers from the
private s...
Many birds, including macaws, are highly visual animals able to detect a wide band of light wavelengths ranging into ultraviolet A, but in captivity, full-spectrum lighting is not universally employed. Where purpose-made bird lighting is used, this is typically made with the provision of ultraviolet B radiation and vitamin D3 synthesis in mind. Lim...
Cutaneous bacterial communities can be crucial in modulating amphibian-pathogen interactions, but are highly sensitive to environmental conditions. Many amphibians, in particular salamandrid newts, may inhabit aquatic or terrestrial habitats after metamorphosis. These different conditions can alter the cutaneous bacterial communities of animals and...
Background
The fungal pathogen Batrachochytrium dendrobatidis ( Bd ) threatens amphibian biodiversity and ecosystem stability worldwide. Amphibian skin microbial community structure has been linked to the clinical outcome of Bd infections, yet its overall functional importance is poorly understood.
Methods
Microbiome taxonomic and functional profi...
Multiple clutching, with two or three successful clutches raised in a single breeding season, is reported from two females of Leptodactylus fallax in two European zoos. Previously, only single clutches were known to be raised by this species. Multiple clutching is perhaps unexpected in this species due to its resource-heavy parental care behaviour....
A rhinoceros viper presented with recurrent grey, thickened and crusted tissue protruding from the vent, with unilateral thickening and firmness of the left side of the base of the tail. Under anaesthesia, a plug of caseous material was removed from the inverted left hemipene. Fungal culture of the cloaca showed confluent growth of a single species...
Maintaining Gymnophiona in captivity provides opportunities to study the behaviour
and life-history of this poorly known Order, and to investigate and provide species appropriate welfare guidelines, which are currently lacking. This study focuses on the terrestrial caecilian Herpele squalostoma to investigate its sensitivity to disturbances associa...
Visitors to zoos can have positive, neutral, or negative relationships with zoo animals. This makes human–animal interactions (HAIs) an essential component of welfare and an important consideration in species selection for zoo exhibits and in enclosure designs. We measured the effect of visitors on reptiles by comparing open and closed periods duri...
EAZA Best Practice Guidelines (Striped) fire salamander, Salamandra salamandra (terrestris) is the first version
of the EAZA Best Practice Guidelines for this species. This guideline has evolved out of the growing concern for
extinction of local fire salamander populations due to the introduction of the invasive chytrid fungus
Batrachochytrium sala...
This study compared the resource use of juvenile zoo-living Chinese crocodile lizards, Shinisaurus crocodilurus crocodilurus across three observation windows, spanning nine months, accounting for time of day and lizard age, and under consistent environmental conditions. Lizards showed a significant difference in proportionate resource use, quantifi...
Calcium metabolism in insectivores may be perturbed by insufficient calcium or vitamin D3. Insects may be gut loaded to increase calcium content, and recent research shows that exposure to UVB radiation can increase the vitamin D3 content of some invertebrates. Typical gut loading protocols result in peak calcium content after 24–48 h, while existi...
Tylototriton ziegleri is a newt native to Vietnam with a very limited range and assessed as Vulnerable by the IUCN. It is rarely found in captivity. Larval husbandry, based on field conditions, had mixed success with a high proportion of egg hatch and relatively rapid larval growth rates but also substantial larval mortality, probably due to high s...
The diets provided to many captive insectivores are deficient in calcium and high in phosphorus, which can lead to nutritional disease. Husbandry professionals may address this imbalance through supplementation, but the efficacy of different methods varies between invertebrate taxa. Earthworms are frequently used for aquatic and fossorial insectivo...
The mountain chicken frog (Leptodactylus fallax) is among the 42 % of amphibians threatened with extinction and is dependent upon ex situ populations to recover in the wild. Amphibian captive husbandry is not fully understood and empirical data are required to optimise protocols for each species in captivity. Calcium metabolism and homeostasis are...
The mountain chicken frog (Leptodactylus fallax) is among the 42 % of amphibians threatened with extinction and is dependent upon ex situ populations to recover in the wild. Amphibian captive husbandry is not fully understood and empirical data are required to optimise protocols for each species in captivity. Calcium metabolism and homeostasis are...
Stereotypies (a subset of Abnormal Repetitive Behaviour [ARB]) are characterised by an unchanging pattern of behaviour and in captive animals can be associated with poor welfare. Although well known in certain taxa, little is known about both welfare and ARBs in reptiles, especially snakes. We document an instance of an ARB in a captive snake speci...
Caecilians epitomise the complexities of maintaining poorly known amphibian taxa in captivity. Empirical data on even the most basic husbandry parameters are lacking for most species of caecilian, including the substrate used to maintain them. We used a simple choice chamber to compare two commonly used substrate types. Microcaecila unciolor were h...
Populations of marine turtle are in global decline and 5 of the 6 species are threatened with extinction. • Rehabilitation facilities seek to rescue, rehabilitate and release recovered individuals, but recovery times can vary and some may require permanent captive care and never return to the wild. • Chronic stress associated with captivity and poo...
Ensuring high levels of welfare is imperative for modern zoos, but such organisations must also engage visitors in order to successfully spread awareness and raise conservation funds. It is therefore important to understand the responses of animals to visitor interaction to optimise welfare. Often, the opportunity to interact with humans may be enr...
Dominance is a key component of behaviour in many animal species and is central to social system dynamics, resource acquisition, individual fitness and ultimately reproductive success. We investigated dominance interactions and social behaviours in a group of captive juvenile gidgee skinks (Egernia stokesii). We hypothesised that a dominance hierar...
The fire salamander (Salamandra salamandra and its relatives) is of increasing priority for ex situ conservation due
to the spread of the fungal pathogen Batrachochytrium salamandrivorans in Europe. In captivity, the species may be maintained
on a clinical paper-based or a naturalistic substrate, either of which has its own advantages and disadvant...
Our understanding of captive husbandry for amphibians is rapidly improving as empirical knowledge in this area grows. Early evidence indicates that UVB radiation is an important aspect of captive husbandry for at least some species, and may be critical in combatting nutritional metabolic bone disease and other environmentally linked diseases. Howev...
Between July 2007 and June 2017 there were 86 deaths in the populations of eight caecilian species at the Zoological Society of London (ZSL) London Zoo. The mortality rate (deaths per animal-year at risk) ranged from 0.03 in the Congo caecilian (Herpele squalostoma) to 0.85 in Kaup's caecilian (Potomotyphlus kaupii). Among the 73 individuals examin...
Identifying individual animals is important for studying populations and for the optimal management of individual animals in captivity. In the absence of natural markings that discriminate individuals, such identification may require animals to be marked by researchers. Amphibians are challenging subjects to mark due to their small size and sensiti...
We investigated the effects on behaviour of captive blue tree monitors (V. macraei) when changing between mercury vapour lamps and IR 'Deep heat projector' lamps.
EAZA Best Practice Guidelines are produced by the various TAGs to merge expert husbandry knowledge and make it widely available within and outside the borders of the EAZA community. The guidelines displayed below show best practice standards, which EAZA zoos aim at achieving. They have been compiled using a template and made user-friendly to facili...
The genus Rhacophorus Kuhl & Van Hasselt is currently known to contain 92 species of frogs (Frost 2018), distributed across south and south-east Asia. Rhacophorus feae Boulenger is a large member of this genus and has a seemingly expansive range been recorded from southern Yunnan in China, the Karen hills in Myanmar, northern Thailand, northern Lao...
It is vital to provide appropriate nutrition to maintain healthy populations in conservation breeding programs. Knowledge of the wild diet of a species can be used to inform captive diet formulation. The nutritional content of the wild diet of the critically endangered mountain chicken frog (Leptodactylus fallax) is unknown, like that of most amphi...
[This corrects the article DOI: 10.1371/journal.pone.0185151.].
The Critically Endangered mountain chicken frog (Leptodactylus fallax) has undergone drastic population decline due to habitat loss, hunting, invasive species, and chytridiomycosis. In response, several partner institutions initiated a conservation breeding program. It is important to maintain the captive population in good health. Therefore the pr...
Aquatic predators must forage for prey in a complex three-dimensional environment where the availability of different prey types with different spatial niches may vary. Aquatic predators have evolved a number of ways in which they may respond to this variation, including phenotypic adaptation and behavioural modulation. We investigated whether claw...
In order to better understand the impacts of treatment of infection with Batrachochytrium dendrobatidis (Bd) and Batrachochytrium salamandrivorans (Bsal) it is important to document host species, the effect of infection and response to treatment protocols. Here we report asymptomatic Bd infection detected through duplex qPCR screening of three Mexi...
The IUCN Red List of Threatened Species (Red List) details the extinction risk of the world's species and presents an important biodiversity indicator for conservation policy. Its continued utility relies on it containing up-to-date information on the extinction risk of species. This requires both regular reassessments and the timely assessment of...
Anthropogenic disturbance via resource acquisition, habitat fragmentation and climate change, amongst other factors, has led to catastrophic global biodiversity losses and species extinctions at an accelerating rate. Amphibians are currently one of the worst affected classes with at least a third of species categorised as being threatened with exti...
ZSL, London Zoo herpetofauna species faecal samples.
(PDF)
Test for published[31] nematode universal primer efficacy on nematode tissue DNA and cross-reactivity on Platyhelminth tissue DNA.
A: Nematode universal primers [31] designed for specific amplification of nematode DNA successfully amplified DNA from the nematodes T. muris (Tm) and T. spiralis (Ts). B, C: Nematode universal primers [31] also demonst...
Test for published[19] nematode universal primer efficacy on nematode tissue DNA and cross-reactivity on Platyhelminth tissue DNA.
Nematode universal primers [19] designed for specific amplification of nematode DNA successfully amplified DNA from the nematodes T. spiralis (Ts), A. lumbricoides (Al), N. brasiliensis (Nb), H. polygyrus (Hp) but not T...
Asiatic salamanders, genus Hynobius, deposit paired egg sacks rather than individual or clumped uncovered spawn. This oviposition mode means that clutches are vulnerable to water mould infections of non-viable ova. I trialled five methods of arresting mould infections in the egg sacks of Hynobius dunni, in pairwise comparisons with control sacks. C...
Two strains, D5088T and D5095, representing a novel yeast species belonging to the genus Saccharomyces were isolated from oak tree bark and surrounding soil located at an altitude of 1000 m above sea level in Saint Auban, France. Sequence analyses of the internal transcribed spacer (ITS) region and 26S rRNA D1/D2 domains indicated that the two stra...
The rhino rat snake Gonyosoma boulengeri is a medium-sized arboreal colubrid snake from southern
China and northern Vietnam. Captive specimens maintained at the Zoological Society of London presented little difficulty in husbandry and were found to breed between March and June. A clutch of 9 eggs were laid on the 16 May 2008 and a clutch of 8 eggs...
Tree-runner lizards, Plica plica are neo-tropical ground lizards, native to South America. ZSL London Zoo has bred this species to the second generation (F2); and the 2.1 founder group has produced six clutches with a mean average of three eggs. The eggs were all removed for incubation, producing 11 viable hatchlings. The first F2 breeding took pla...
Water frogs, genus Pelophylax, are culturally and scientifically important taxa and as such are frequently
collected and traded in large numbers. This, among other factors, has led to water frog species becoming both threatened
in parts of the range of the genus and invasive aliens in others, and they are therefore of conservation interest. Captive...
The persistence of many amphibian species may depend on captive breeding programmes, which aim to maintain genetically viable populations in captivity while threat processes in the wild are being addressed, and subsequently provide animals for population supplementation, reintroduction, or translocation programmes. Since the publication of the firs...
Staggering food availability through a delivery device is a common way of providing behavioural enrichment as it is usually thought to increase the amount of natural behaviour due to the unpredictability of the food source. Tree-runner lizards (Plica plica) are a Neotropical, scansorial, insectivorous species. We provided these lizards with an enri...
Captive husbandry and breeding may be pivotal to the successful conservation of many amphibian species, with captive stock providing research subjects, educational tools and animals for release into the wild. Husbandry protocols are missing for many species and sub-optimal for many more, which may limit the success of captive breeding attempts. It...