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THE INFLUENCE OF CAROTENOIDS ON FITNESS RELATED TRAITS IN ANURANS: IMPLICATIONS FOR EX SITU CONSERVATION
[Thesis]. Manchester, UK: The University of Manchester; 2011.
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Abstract
Amphibians are facing an extinction crisis, and in many cases it has become necessary to conserve species in captivity. Unfortunately, our understanding of the nutritional requirements of amphibians in captivity is currently limited. There have been anecdotal reports that captive bred amphibians have duller skin colouration than wild members of the same species. Many amphibians use carotenoid pigments in skin colouration. Carotenoids are yellow-red pigments synthesised by photosynthetic tissues, however vertebrates cannot synthesise them de novo and rely entirely on dietary sources. Reduced colour in captive bred amphibians could therefore result from limited carotenoid availability in the diet. Limited access to carotenoids could have further negative consequences on health and reproductive success since carotenoids are known to function in the immune, antioxidant and reproductive systems of other vertebrate taxa. The role of carotenoids in amphibian fitness is currently unknown, and the aim of this PhD was to assess the importance of carotenoids to anuran amphibians. Skin colour may be influenced by carotenoid availability, and it was therefore important to establish a suitable method for quantifying skin colour in amphibians. In Chapter 1 I assessed two methods for colour quantification, including digital photography and spectrometry. Neither method was significantly more accurate than the other, however I chose to use photography for my studies for reasons of practicality. In Chapters 2 and 3 I assessed the role of carotenoids in the reproductive systems of wild frogs. I found that carotenoid-based skin colouration was involved in the breeding behaviour of wild Agalychnis moreletii frogs. I found positive assortative mating by colour in that frogs were found mating with individuals with similar carotenoid-based colouration. This assortative mating by colour may be driven by mutual mate choice, or may have evolved to prevent mismatched pairing with a sympatric and phenotypically similar species (A. callidryas). I then analysed the carotenoid composition of eggs produced by wild A. moreletii and Phyllomedusa trinitatis, which are tree frogs with similar reproductive ecology but different egg deposition strategies: Agalychnis moreletii deposits green eggs on the surface of leaves while P. trinitatis wraps pale cream eggs in leaves. The concentration and diversity of carotenoids was significantly higher in A. moreletii than P. trinitatis and potential ecological explanations for this are discussed.In Chapter 4 I investigated carotenoid availability in the diet of captive amphibians by analysing the carotenoid composition of commonly used feeder-invertebrates. I assessed interspecific variation in carotenoid accumulation in three feeder-cricket species (Gryllus bimaculatus, Gryllodes sigillatus and Acheta domesticus), which were all fed one of three diets (wheat-bran, fish-food based diet, fresh fruit and vegetables). All three cricket species were a poor source of carotenoids unless they were gut-loaded on a carotenoid-rich diet. Nutrient retention over a two-day period was poor across species. Finally, there were significant interspecific differences in gut-loading capacity, with G. bimaculatus having the greatest capacity. This study shows that carotenoid availability to captive amphibians will be limited unless they are fed specific feeder invertebrate species, recently gut-loaded on carotenoid-rich foods. In Chapters 5, 6 and 7 I assessed the influence of carotenoids on fitness related traits in captive anurans. I firstly assessed colour degradation in captive-reared A. moreletii frogs and looked at whether skin colour could be improved through increased carotenoid availability in the diet. I found that carotenoid-based skin colour degraded quickly in captivity but could be improved through dietary supplementation with carotenoids, however there was a critical period during post-metamorphic growth for deposition of carotenoids in the skin. Next, I investigated the effect of carotenoids on larval growth and development, and post-metamorphic growth, development, skin colour and reproductive success in captive A. callidryas frogs. I found no direct effect of carotenoids during larval stages, however there were carry-over effects on post-metamorphic growth and skin colour. Increased post-metamorphic carotenoid availability positively influenced growth, skin colour and reproductive success. Similarly to A. moreletii, there was a critical period during post-metamorphic growth for deposition of carotenoids in the skin. Finally, I examined the protective potential of carotenoids in Silurana (Xenopus) tropicalis tadpoles that were exposed to ultraviolet (UV) light. Exposure to UV light significantly reduced tadpole survival and there was no evidence that carotenoids afforded any protection. Nevertheless, in tadpoles that were not exposed to enhanced UV light, carotenoids increased survival. Furthermore, carotenoids had a significantly positive effect on the developmental rate of tadpoles in both UV limited and UV enhanced environments. The studies in this PhD show that carotenoid availability has important consequences on fitness related traits in anuran amphibians, which include effects on growth, skin colour, reproductive success and survival. Carotenoid availability to captive amphibians will, however, be low unless they are provided with feeder invertebrates that have been recently gut-loaded on carotenoid-rich foods. These findings should be considered when recommendations are made on the nutritional requirements of amphibians in captivity as they could significantly improve the fitness of captive-bred individuals, and thus increase the success of ex situ conservation programmes.