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A Case Study with Mountain Chicken Frogs (Leptodactylus Fallax) and General Recommendations for Pre‐Release Health Screening

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A Case Study with Mountain Chicken Frogs (Leptodactylus Fallax) and General Recommendations for Pre‐Release Health Screening Zoo Biology 9999 : 1–7 (2014) RESEARCH ARTICLE Meeting Ultraviolet B Radiation Requirements of Amphibians in Captivity: A Case Study With Mountain Chicken Frogs (Leptodactylus fallax) and General Recommendations for Pre‐Release Health Screening Benjamin Tapley,1* Matthew Rendle,1 Frances M. Baines,2 Matthias Goetz,3 Kay S. Bradfield,4 David Rood,5 Javier Lopez,6 Gerardo Garcia,6 and Andrew Routh3 1Zoological Society of London, Regent's Park, London, United Kingdom 2Greenfield, School Lane, Govilon, Abergavenny, Monmouthshire, United Kingdom 3Durrell Wildlife Conservation Trust, Les Augrès Manor, La Profonde Rue, Trinity, Jersey, United Kingdom 4Perth Zoo, South Perth, Western Australia 5Veterinary X‐Rays, Regent Park, Princes Risborough, Buckinghamshire, United Kingdom 6Chester Zoo, Upton‐by‐Chester, Chester, United Kingdom Conservation breeding programmes are a tool used to prevent amphibian extinctions. The husbandry requirements of amphibians are complex. Ongoing research is needed to ensure optimal management of those captive‐bred animals destined, in particular, for reintroduction. The UV‐B and vitamin D3 requirements of amphibians are largely unknown. Metabolic bone disease has been reported in a number of species. These include the Critically Endangered mountain chicken frog (Leptodactylus fallax) reared in captivity on diets supplemented with a high‐calcium multivitamin and mineral supplement containing vitamin D3 but without UV‐B provision. Captive‐bred L. fallax being reared for reintroduction to Montserrat were provided with UV‐B radiation from metamorphosis and were fed on insects supplemented with vitamins and minerals. Overlapping heat, light and UV‐B gradients were provided, mimicking what we believe best represents the natural situation and thereby facilitated self‐regulation of UV‐B exposure. A subset of 10 frogs was periodically radiographed to assess skeletal health. Radiographic bone density and anatomical integrity appeared unremarkable when compared with a wild caught L. fallax. In addition to other routine health‐screening, we recommend that radiography be performed to a structured schedule on a subset of all captive‐bred and reared amphibians to assess skeletal health and to gauge the appropriateness of captive husbandry. We demonstrate here that, through the appropriate provision of a combination of both UV‐B radiation and dietary supplementation, L. fallax can be bred and reared in captivity with healthy skeletal development. Zoo Biol. XX:XX–XX, 2014. © 2014 Wiley Periodicals, Inc. Keywords: amphibian; conservation; husbandry; UV‐B; Leptodactylus fallax INTRODUCTION candidates for conservation breeding programmes due to their small size, high fecundity, and low maintenance Amphibians are in decline world‐wide [Alford and requirements, and consequentially the cost effectiveness of Richards, 1999] with extinction rates up to 211 times the such programmes when compared with programmes for other background rate [McCallum, 2007]. Conservation breeding programmes are one of the tools used to prevent amphibian ÃCorrespondence to: Benjamin Tapley, Society of London, Regent’s extinctions [Griffiths and Pavajeau, 2008]. These pro- Park, London, United Kingdom. E‐mail: [email protected] grammes should aim to maintain genetically representative Received 07 March 2014; Revised 12 July 2014; Accepted 06 August 2014 populations of amphibians in captivity for future population supplementation, reintroduction, or translocation pro- DOI: 10.1002/zoo.21170 grammes [Baker, 2007; Shishova et al., 2010; Browne and Published online XX Month Year in Wiley Online Library Figiel, 2011]. Amphibians are often cited as being ideal (wileyonlinelibrary.com). © 2014 Wiley Periodicals, Inc. 2 Tapley et al. vertebrates [Bloxam and Tonge, 1995; Balmford et al., 1996; from sunlight, specifically of UV‐B wavelengths between Jones, 2002]. 290 and 315 nm, causes the photolysis of provitamin D3 It is now apparent that the captive husbandry require- (7‐dehydrocholesterol) to previtamin D3, which is then ments of amphibians are more complex than first thought thermally isomerized into vitamin D3. This is transported in [Browne et al., 2006; Antwis and Browne, 2009; King the bloodstream to the liver and hydroxylated into calcediol et al., 2011; Verschooren et al., 2011; Ogilvy et al., 2012; (25‐hydroxycholecalciferol), the circulating storage form of Dugas et al., 2013; Antwis et al., 2014]. Thus conservation vitamin D3. Calcitriol, the active hormone enabling calcium breeding programmes could potentially produce maladapted absorption from the gut, is synthesized from calcediol by the amphibians that are unsuitable for release [Antwis and kidneys. Low vitamin D3 levels result in insufficient calcitriol Browne, 2009; Ogilvy et al., 2012]. It is imperative that more being produced and, as a consequence, serum calcium levels research is undertaken to ensure that the husbandry of animals fall. The resulting hypocalcaemia stimulates production bred in captivity for the purpose of reintroduction is optimal. of parathyroid hormone, which in turn promotes calcium Nutritional problems have been cited as a major barrier resorption from the bones in order to maintain serum calcium to the implementation of amphibian conservation breeding levels within the very small range compatible with life. programmes [Antwis and Browne, 2009; Browne et al., 2009; Prolonged stimulation of the parathyroid glands results in King et al., 2011; Verschooren et al., 2011; Ogilvy Nutritional Secondary Hyperparathyroidism (NSHP) and et al., 2012; Dugas et al., 2013]. Vitamin D3 deficiency is continuous mobilization of calcium from the bone results in one such nutritional problem; vitamin D3 plays a critical role generalized skeletal decalcification [Holick, 2003]. in regulating calcium metabolism, as well as important roles A healthy skeletal system is of vital importance to in organ development, muscle contraction and the function- amphibians. Compromised skeletal systems may have direct ing of the immune and nervous systems [Wright and impacts on growth, prey acquisition, mobility, reproduction, Whitaker, 2001]. In most vertebrates, vitamin D3 is and animal welfare. Amphibians, in particular anurans, have synthesized via exposure to the ultraviolet B radiation the ability to reserve calcium carbonate in endolymphatic (UV‐B) present in sunlight. Recent “metamorphs,” juveniles sacs in the cranial cavity and spinal canal, which can be drawn and adults of a number of nocturnal frog species have been upon in order to raise the levels of circulating ionized calcium observed basking in sunlight in the wild and diurnal retreat [Stiffler, 1993a]. Amphibians are also able to store calcium sites can also receive reflected UV‐B [K. Bradfield, pers. obs; carbonate as a layer below the skin in both adults and larvae Tattersall et al., 2006; Michaels and Preziosi, 2013]. This may [Bentley, 1984; Cheek et al., 1993]. During metamorphosis indicate that even nocturnal species may rely on exposure to calcium from these stores can be utilized, along with calcium UV‐B radiation to synthesize vitamin D3. Captive Bombina uptake across larval gills, for rapid ossification of bones orientalis that were exposed to UV‐B radiation had [Pilkington and Simkiss, 1966; Bentley, 1984]. Calcium is significantly higher serum vitamin D3 levels than a control also transferred from the female to the yolk during egg group, which did not have access to UV‐B, indicating that this formation [Wysolmerski, 2002]. species is able to photobiosynthesize vitamin D3 [Michaels As a form of MBD, NSHP is diagnosed primarily et al., 2014]. Furthermore, this is supported by studies that through radiography [Klaphake, 2010]. Blood plasma studies have shown that captive‐bred nocturnal frogs housed in may demonstrate imbalances in calcium to phosphorus ratios enclosures without access to UV‐B but that were fed a diet of [Klaphake, 2010]. Frogs can recover from NSHP and bones insects supplemented with vitamins and minerals exhibited can be re‐calcified but skeletal deformities caused by NSHP metabolic bone disease (MBD) [Gagliardo et al., 2010; may be permanent (Figs. 1 and 2). King et al., 2011; Verschooren et al., 2011]. A study on Provision of appropriate UV‐B is clearly important for B. orientalis indicated that routine dietary supplementation the health of some captive amphibians [Antwis and with calcium and vitamin D3 using existing, commercially Browne, 2009; Verschooren et al., 2011] but it is believed available supplements and standard dusting practices did that there may be detrimental effects on growth and not fully compensate for lack of UV‐B exposure and that development if amphibians are exposed to higher levels of currently used gut loading diets may provide insufficient UV‐B radiation than are found in that particular species’ levels of calcium in feeder insects [Michaels et al., 2014]. In microhabitat [Licht, 2003]. To complicate matters, few the laboratory Trachycephalus resinifictrix demonstrated studies have measured the exposure of wild amphibians to improved growth and skeletal development when provided UV radiation in their specific micro‐climates or how this may with UV‐B [Verschooren et al., 2011]. change as amphibians mature [Michaels and Preziosi, 2013]. One of the most common types of MBD is attributed to As UV exposure parameters in the wild are largely unknown vitamin D3 or calcium deficiency [Mader, 2006; Densmore the provision of appropriate, naturalistic, gradients in and Green, 2007]. Vitamin D3 (cholecalciferol)
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