The interactive effects of ultraviolet-B radiation and other environmental stressors on amphibians

Lesley Ann Alton (2012). The interactive effects of ultraviolet-B radiation and other environmental stressors on amphibians PhD Thesis, School of Biological Sciences, The University of Queensland.

       
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Author Lesley Ann Alton
Thesis Title The interactive effects of ultraviolet-B radiation and other environmental stressors on amphibians
School, Centre or Institute School of Biological Sciences
Institution The University of Queensland
Publication date 2012-05
Thesis type PhD Thesis
Supervisor Craig Franklin
Robbie Wilson
Total pages 173
Total colour pages 5
Total black and white pages 168
Language eng
Subjects 060203 Ecological Physiology
069902 Global Change Biology
Abstract/Summary The phenomenon of global amphibian declines is a testament to the profound effects of human-induced global change on natural environments. With amphibians being the most threatened of all vertebrate taxa, and also important bioindicators of environmental health, understanding the causes of their declines is critical for their conservation, and possibly the conservation of other species. While research over the past two decades has identified a range of potential causative agents, it has become widely accepted that amphibian declines are likely to be a result of complex interactions between multiple environmental stressors that lead to compounding negative effects. The overarching aim of this thesis was to examine the interactive effects of ultraviolet-B radiation (UVBR) and other environmental stressors (predation and temperature) on the early life stages of a model amphibian species, the striped marsh frog Limnodynastes peronii. UVBR is highly damaging to living organisms and has increased globally as a consequence of stratospheric ozone depletion. The coincident timing of the beginning of stratospheric ozone depletion and the beginning of rapid amphibian declines in the late 1970s and early 1980s prompted interest in increased environmental UVBR as a potential contributor to amphibian declines with numerous studies showing that exposure to UVBR is detrimental to amphibians. UVBR has also been shown to interact synergistically with other environmental stressors, including a range of contaminants, aquatic acidification, low temperature, and infectious disease, such that the effect of the stressors combined is greater than that caused by the additive effects of the stressors independently. With the rapid disappearance of amphibian populations from seemingly pristine habitats around the world, understanding how UVBR interacts with natural stressors, such as predation and temperature, is particularly important given that anthropogenic stressors, such as contaminants, may have less of an impact in these habitats. The first specific aim of this thesis was to examine the independent and interactive effects of UVBR and predation stress in the form of predatory chemical cues (PCC) on L. peronii tadpole survival and morphology (Chapter 2). Using a controlled laboratory experiment the following questions were addressed: (1) do UVBR and PCC interact synergistically to enhance the mortality of tadpoles above the additive effects of the stressors independently?; and (2), does exposure to UVBR affect the ability of tadpoles to morphologically respond to PCC? UVBR and PCC were found to interact synergistically to enhance the mortality of L. peronii tadpoles by nearly two-fold above the additive mortality caused by the stressors independently. Exposure to UVBR was also found to suppress the development of predator-induced morphological defences. Specifically, tadpoles simultaneously exposed to UVBR and PCC did not develop the deep tail that was expressed by tadpoles exposed to PCC alone. A deep tail is a prominent feature of tadpoles exposed to predators and is strongly associated with increased tadpole survival in the presence of predators, thus the lack of a deep tail in tadpoles exposed to UVBR and PCC has implications for their fitness in a predator environment. The fitness consequences of UVBR-induced sublethal effects is poorly studied, thus the second specific aim of this thesis was to examine the independent and interactive effects of UVBR and PCC on a suite of traits of L. peronii embryos and tadpoles (embryonic hatching success and hatching time, post-hatch tadpole survival, size, morphology, behaviour, and locomotor performance), and assess tadpole survival time in a predator environment to evaluate the potential fitness consequences (Chapter 3). Exposure to a 3−6% increase in UVBR, which is comparable to changes in terrestrial UVBR associated with ozone depletion, was found to have no effect on any of the traits measured, except survival time in a predator environment, which was reduced by 22−28%. Exposure to PCC caused tadpoles to hatch earlier, have reduced hatching success, have improved locomotor performance, and survive for longer in a predator environment, but had no effect on tadpole survival, behaviour or morphology. Unlike the findings in Chapter 2, simultaneous exposure to UVBR and PCC resulted in no interactive effects. These findings demonstrate that increased UVBR has the potential to reduce tadpole fitness by compromising their ability to survive encounters with predators, though critically such an effect might not be detectable via some performance measures, such as locomotor performance, which was not altered by exposure to an increase in UVBR. Exposure to PCC, on the other hand, improves tadpole locomotor performance and fitness, which suggests that an increase in locomotor performance does confer some benefit to survival in a predator environment as one would expect, but with regard to the effects of UVBR, there are clearly additional factors that need to be considered when investigating predator-prey interactions. The third specific aim of this thesis was to evaluate the energetic costs associated with being exposed to UVBR, both alone and in combination with PCC (Chapter 4), in order to understand the physiological basis for the observed negative synergistic effect on tadpole survival in Chapter 2. While several studies have examined the lethal and sublethal effects of UVBR, alone and in combination with other environmental stressors, on amphibians, few have considered how UVBR affects amphibian metabolism, or how amphibian metabolism may change in response to exposure to other stressors in addition to UVBR. Using a controlled laboratory experiment, the independent and interactive effects of UVBR and PCC on the tissue and whole-animal metabolic rate (MR) and activity of L. peronii tadpoles were examined. Exposure to UVBR caused tissue MR to increase by 36%, but whole-animal MR to decrease by 14%, which is most likely due to tadpoles reducing their activity levels by 56%. Exposure to PCC had no significant effect on tissue or whole-animal MR, but caused tadpoles to reduce their activity levels by 36%, indicating that the whole-animal MR of tadpoles exposed to PCC is elevated relative to their activity levels. Compared to tadpoles exposed to neither stressor, tadpoles exposed simultaneously to UVBR and PCC showed no change in whole-animal MR despite reducing their activity levels by 62%. These findings show that, for tadpoles, there is an energetic cost associated with being exposed to UVBR and PCC independently, and that this cost is greater when they are exposed to both stressors simultaneously. The synergistic negative effect of UVBR and PCC on tadpole survival found in Chapter 2 is therefore likely to arise as a consequence of the effect of these combined stressors on metabolic rate. The fifth and final aim of this thesis was to examine the thermal-dependence of UVBR effects in the context of an ecologically-relevant fluctuating UVBR and temperature regime to evaluate whether exposure to peak UVBR levels while the temperature is high (35°C) is more detrimental to pre-metamorphic L. peronii than exposure to peak UVBR levels while the temperature is moderate (25°C) (Chapter 5). This was examined by measuring embryonic hatching success and hatching time, post-hatch tadpole survival, size, morphology, locomotor performance, and survival time in a predator environment. Embryos exposed to peak UVBR levels at 35°C hatched 10 h later than those exposed to peak UVBR levels at 25°C, and as tadpoles, were smaller and consequently swam slower, but in a predator environment exhibited no difference in survival time. There was also no effect of experimental treatment on the hatching success of embryos, nor on the post-hatch survival of tadpoles. These findings, therefore, are not sufficiently strong to support the hypothesis that high temperatures enhance the negative effects of UVBR in pre-metamorphic amphibians. The results from these studies reveal that multiple stressors can interact in ways that are not necessarily predictable from single-factor studies, and that examination of the effects of UVBR in the absence of other ecologically-relevant environment stressors potentially underestimates the impact of UVBR on amphibian populations in natural systems. Researchers in amphibian conservation biology should therefore continue to utilise a multi-factorial experimental approach if we are to gain a comprehensive understanding of the stressors and mechanisms responsible for causing global amphibian declines.
Keyword Amphibians
ultraviolet B radiation
Predation
temperature
interactive effects
sublethal effects
morphology
Locomotor Performance
metabolism
fitness
conservation
Additional Notes 1, 32, 35, 43, 161

 
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Created: Tue, 22 May 2012, 13:22:22 EST by Lesley Alton on behalf of Library - Information Access Service