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Litoria Wilcoxii) Behavioural Ecology, Reproductive Biology and Colour Change Physiology in the Stony Creek Frog (Litoria wilcoxii) Author Kindermann, Christina Published 2017 Thesis Type Thesis (PhD Doctorate) School Griffith School of Environment DOI https://doi.org/10.25904/1912/1098 Copyright Statement The author owns the copyright in this thesis, unless stated otherwise. Downloaded from http://hdl.handle.net/10072/367513 Griffith Research Online https://research-repository.griffith.edu.au Behavioural ecology, reproductive biology and colour change physiology in the Stony Creek Frog (Litoria wilcoxii) Christina Kindermann B. Sc. (Hons) Griffith University School of Environment Environmental Futures Research Institute Submitted in fulfilment of the requirements of the degree of Doctor of Philosophy July 2016 Abstract Many animals possess the remarkable ability to change their skin colour. Colour change can have several potential functions, including communication, thermoregulation and camouflage. However, while the physiological mechanisms and functional significance of colour change in other vertebrates have been well studied, the role of colour change in amphibians is still relatively unknown and a disconnection between morphology, physiology and function exists in the literature (review presented in chapter 2). In this thesis, I investigate these multidisciplinary components to understand the processes and functions of colour change in stony creek frogs (Litoria wilcoxii), which are known to turn bright yellow during the breeding season. By (1 – Chapter 3) examining the distribution and structure of dermal pigment cells, (2– Chapter 4) determining hormonal triggers of rapid colour change, (3– Chapter 5) investigating seasonal colour, hormone and disease relationships and (4– Chapter 6) determining the evolutionary functions of colour change, I provide a comprehensive explanation of this phenomenon in L. wilcoxii. 1) Dorsal skin colour in L. wilcoxii is determined by the arrangement of two types of chromatophore: melanophores and xanthophores. Rapid colour change is the result of pigment dispersion or aggregation in the melanophores which either exposes or covers the yellow xanthophores. 2) This pigment movement is triggered by the neuro-hormone adrenalin (typical of other species exhibiting rapid brightening). Male frogs turned a vivid yellow within 5 minutes following adrenalin injection and remained so for 3 to 5 hours before rapidly fading back to brown. This timing followed natural observations of amplexing males. Interestingly, adrenalin injections triggered colour change but not sperm release in male frogs, while Human chorionic gonadotropin (hCG) induced sperm release but not colour change. 3) At a seasonal level, reproductive hormone (testosterone) levels and dorsal colour score (yellowness) increased during breeding months whilst stress hormone (corticosterone) levels remained stable. Infection by Bd (Batrachochytrium dendrobatidis, the pathogen that induces chytridiomycosis) was associated with increased corticosterone and decreased testosterone, however did not appear to be influencing colour expression. i 4) Behavioural experiments using model frogs ruled out female preference, and male-male competition was rarely observed, however male vocalisations and movement increased at the sight of a female and model female. Predation trials found no significant difference in attack rates between yellow and brown models exposed to natural field conditions. Overall, this thesis demonstrates both seasonal and rapid dynamic colour changes in male Litoria wilcoxii. Rapid colour change is under neuro-hormonal control and functions in intersexual signal during amplexus. It is likely that seasonal increases in yellow colouration are related to reproductive hormone cycles. The physiological stress response associated with Bd infection could potentially suppress physiological aspects of reproduction, however more research is needed. Colour functions as an intrasexual signal following amplexus that could avert sperm competition and displacement by other males during amplexus, presenting a novel function for rapid dynamic colour change in amphibians. My research expands our understanding of the mechanisms, processes and potential functions of rapid colour change in dichromatic amphibians. ii Declaration This work has not previously been submitted for a degree or diploma in any university. To the best of my knowledge and belief, the thesis contains no material previously published or written by another person except where due reference is made in the thesis itself. All research procedures reported in this thesis were undertaken under the Queensland Department of Environment and Heritage Protection (DEHP) research permit WISP13675913 and the Griffith University Animal Ethics Committee (AEC) permit #ENV/20/12/AEC. _______________________________________________ (Date) _____________________ Christina Kindermann iii Acknowledgements A number of people need to be thanked for helping me with the completion of my PhD. First and foremost, I would like to thank my family for always supporting me and believing that I can do anything I want. To my parents, Sonja and Andy, words cannot describe how much you have supported me, having a bed ready for me whenever I needed to escape city life made many parts of this journey easier. To my partner Basam, even though this doesn’t come close to what you mean to me all I can say is that I love you and I can’t wait for more adventures with you. Thanks to my supervisor Jean-Marc Hero for sharing your fascination with amphibians and your passion for conservation. Most of all thanks for pushing me to publish my work, attend conferences, tutor field courses and assist in various other projects beyond the scope of my research. These experiences have been invaluable and have allowed me to develop as a scientist. Thanks also to Edward Narayan for taking the time to teach me in the lab and for your helpful comments on my papers. And thank you Guy Castley, for coming on board in the last minute and helping me get to the end. There was a large amount of fieldwork involved in this project that would not have been possible without the help of numerous volunteers. I would especially like to thank Daniel Stellmacher, Kristian Owen, Corey Newell, Trish Hall, Sonia Marsonic, Tahlie Page, Billy Ross, Kat Lowe, Mariel Familer Lopez, Basam Tabet and many others who have up their free time to help me out. Thanks also to my wonderful office mate for the laughs, the support and sometimes needed distractions. Much of this study was funded through a postgraduate research scholarship; Jean-Marc Hero provided the remaining funds. The histology component of this study would not have been possible without the facilities and training provided by The University of Queensland Histology Facility, thanks also to Andrew Weeks and Anthony Van Rooyen at Cesar for processing the Chytrid samples. I would also like to thank the journal editors and anonymous reviewers for providing constructive feedback on my submitted papers. Finally, I would like to thank my frogs for giving me an insight into their fascinating world. It has been such a rewarding experience to be able to search for an answer to the questions no one really knew. The sleepless nights I spent along the rocky creek edges were definitely worth it. iv Acknowledgement of co-authored papers included in this Thesis Included in this thesis are four published papers (Chapters 3, 4, 5, and 6), one in review (Chapter 2) which are co-authored with my supervisors and one short communications (Appendix 1) of which I am the sole author. My contribution to each paper, how it relates to the overall thesis aim and bibliographic details are outlined at the front of the relevant chapter. All published papers are presented in their published format and papers in review are formatted according to journal specifications therefore spelling and formatting will vary depending on journal origins and specifications. The bibliographic details and status for these papers are: Kindermann C and Hero J-M (in review) Physiology, function and the ecological drivers of colour change in amphibians. Biological Journal of the Linnean Society. Kindermann C, Hero J-M (2016) Pigment cell distribution in a rapid colour changing amphibian (Litoria wilcoxii). Zoomorphology 135 (2), 197-203, doi:10.1007/s00435- 016-0303-1 Kindermann C, Narayan E J, Hero J-M (2014) The Neuro-Hormonal Control of Rapid Dynamic Skin Colour Change in an Amphibian during Amplexus. PloS one 9 (12), e114120, doi: 10.1371/journal.pone.0114120 Kindermann C, Narayan E J, Hero J-M (2016) Does physiological response to disease incur cost to reproductive ecology in a sexually dichromatic amphibian species? Comparative Biochemistry and Physiology: Part A: Molecular & Integrative Physiology 203,220-226, doi: 10.1016/j.cbpa.2016.09.019 Kindermann C and Hero J-M (2016) Rapid dynamic colour change is an intrasexual signal in a lek breeding frog (Litoria wilcoxii). Behavioral Ecology and Sociobiology 70 (20), 1995-2003, doi: 10.1007/s00265-016-2220-1 Kindermann C. 2015. Litoria wilcoxii (Stony Creek Frog). Interspecific amplexus. Herpetological Review 46 (2): 235 The copyright status of the published papers is held by the relevant journals. Co-authors contributed to these papers by providing (1) Guidance of experimental design; (2) laboratory and technical support; and (3) advice and comments of written material. Appropriate acknowledgements of those who contributed
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