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Morpho-Functional Adaptations to Digging in Australian Marsupials

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Morpho-Functional Adaptations to Digging in Australian Marsupials Morpho-functional adaptations to digging in Australian marsupials Meg Louise Martin BSc (Hons) A thesis submitted to Murdoch University to fulfil the requirements for the degree of Doctor of Philosophy August, 2020 “An understanding of the natural world and what’s in it is a source of not only a great curiosity but great fulfillment…” Sir David Attenborough i Author’s declaration I declare that this thesis is my own account of my research and contains as its main content work which has not previously been submitted for a degree at any tertiary education institute. ____________________ Meg Louise Martin PhD Candidate August 2020 ii Abstract Digging behaviour has evolved across multiple lineages of Australian marsupials and monotremes, some of which are amongst the most specialised diggers in the world. These animals forage for subterranean food sources, while others dig extensive burrow systems for shelter. The scratch-diggings, in turn, assist in soil turn over, water infiltration, nutrient cycling and dispersal of fungi and seeds, thus playing important roles in ecosystem health. Digging species are capable of generating high out-forces with their forelimbs to excavate soil. As form follows function, forelimb musculoskeletal morphology is expected to be driven by the forces that are imposed by their day-to-day activities, within the constraints imposed by phylogenetic background. In this thesis, I present four studies that quantitatively investigate intra- and inter-specific variation in forelimb adaptations to digging in Australian monotremes and marsupials to examine the link between skeletal morphology and muscle architecture. Representatives of all extant lineages of marsupials (Diprotodontia, Dasyuromorphia, Peramelemorphia, Notoryctemorphia) and monotremes (Monotremata) were used in a correlative study to examine the extent to which functional patterns of limb morphology are influenced by digging behaviour. Study 1 examined ontogenetic development of muscle architecture (muscle mass (mm) and muscle physiological cross-sectional area (PCSA)) in the Quenda (Isoodon fusciventer). This data demonstrated differential development of the muscles acting as main movers of the power-stroke during digging in comparison to recovery-stroke muscles for force production (PCSA) but on the whole suggested mechanical similarity throughout ontogeny in the sample. Study 2 examined the intraspecific relationship between the ontogenetic iii development of muscle architecture and 2D and 3D measures of bone shape to reveal that the shape of the scapula, humerus and third metacarpal show significant covariation with muscle anatomy. However, the relationship was not well-represented by bone indices. In study 3, the covariation between muscle PCSA and bone shape was quantified across a range of species. Bone shape was significantly different between species of different digging abilities; however, differences were not apparent after phylogenetic correction with the exception of the ulnar and third metacarpal shape. A significant link between muscles PCSA and shape was evident, especially for the scapula, humerus and third metacarpal. Study 4 extended the range of species examined for bone measures to reveal that ulnar shape and bone indices show significant differences between behaviour; this relationship was less evident in the scapula, humerus and third metacarpal. Overall, this collective body of work has quantified the extent to which forelimb muscle architecture and bone shape covary. This thesis also highlights the importance of ontogeny in quantitative studies of muscle architecture, and provides novel models of analysis of post-cranial anatomy. This information furthers the understanding of the complex links between vertebrate form and function. The application of these results will assist in making inferences of the behaviour and ecology of extinct species and the roles they may have played within the Australian ecosystem through time and space. iv Statement of candidate contributions The work presented in this thesis was undertaken from June 2015 to August 2020 at Murdoch University (six months pause of candidate May 2019-Dec 2019). Funding for this research was provided by Murdoch University and the Society of Graduate Women WA. This work is original and was carried out by myself, with contributions by my supervisory panel and other collaborators that have been acknowledged for their assistance in the production of the papers. Here, I detail the contributions of all authors towards each of the experimental chapters. Chapter 2 is predominantly my own work. I performed the extensive literature review and drafted the manuscript. All authors assisted in drafting the manuscript and contributed to the design of the review. All authors approved the manuscript for publication. This chapter has been published in the Journal of Morphology. Martin, M. L., Travouillon, K. J., Fleming, P. A. & Warburton, N. M. (2020), Review of the methods used for calculating physiological cross-sectional area (PCSA) for ecological questions. Journal of Morphology, 281, 778-789. doi: http://doi.org/10.1002/jmor.21139 Signatures of Co-Authors: 1. _________________ 2. _________________ 3. _________________ Chapter 3 is predominantly my own work. I collected specimens, carried out muscle dissections, measured FL and pennation angles, undertook the statistical analysis, and drafted the manuscript, 1. NMW collected specimens, assisted in muscle dissections, produced muscle drawing figures and drafted the manuscript, 2. KJT drafted the manuscript, and 3. PAF assisted in statistical analysis and drafted the manuscript. All authors contributed v to the experimental design and gave final approval for publication. This chapter has been published in the Journal of Morphology. Martin, M. L., Warburton, N. M., Travouillon, K. J. & Fleming, P. A. (2019), Mechanical similarity across ontogeny of digging muscles in an Australian marsupial (Isoodon fusciventer). Journal of Morphology, 280, 423:435. doi: http://doi.org/10.1002/jmor.20954 Signatures of Co-Authors: 1. _________________ 2. _________________ 3. _________________ Chapter 4 is predominantly my own work. I collected specimens, carried out all the scanning of specimens, undertook all landmarking, undertook the statistical analysis, and drafted the manuscript, 1. KJT drafted manuscript, 2. ES assisted in statistical analysis and drafted the manuscript, 3. PAF assisted in statistical analysis and drafted the manuscript, and 4. NMW collected specimens and drafted the manuscript. All authors contributed to the experimental design and gave final approval for publication. This chapter has been published in the Journal of Morphology. Martin, M. L., Travouillon, K. J., Sherratt, E., Fleming, P. A. & Warburton, N. M. (2019), Covariation between forelimb muscle anatomy and bone shape in an Australian scratch- digging marsupial: comparison of morphometric methods. Journal of Morphology, 280, 1900-1915. doi: http://doi.org/10.1002/jmor.21074 Signatures of Co-Authors: 1. _________________ 2. _________________ 3. _________________ 4. _________________ vi Chapter 5 is predominantly my own work. I collected and sourced specimens, carried out muscle dissections, measured FL and pennation angles, carried out all the scanning and measuring of specimens, undertook all landmarking, undertook the statistical analysis and drafted the manuscript, NMW assisted in muscle dissections and drafted the manuscript, KJT collected specimens and drafted the manuscript, PAF assisted in statistical analysis and drafted the manuscript. All authors contributed to the experimental design. This chapter has been written for submission to the Zoological Journal of the Linnaean Society. Chapter 6 is predominantly my own work. I collected and sourced all specimens, carried out all the scanning of specimens, measured all the specimens, undertook all landmarking, undertook the statistical analysis, and drafted the manuscript, PAF assisted in statistical analysis and drafted the manuscript, KJT collected specimens and drafted the manuscript, and NMW collected specimens and drafted the manuscript. vii Acknowledgements The completion of this thesis would not have been achieved without the help and support of many people during my PhD. Firstly, I need to thank my amazing supervisors Prof. Trish Fleming, Dr Natalie Warburton and Dr Kenny Travouillon for their support, guidance and patience throughout my PhD. Thank you for sharing your knowledge, expertise and investing endless amounts of time to help me complete this thesis. Trish, thank you for all your assistance and guidance with all my statistical analysis and for providing so much valuable feedback on all my manuscripts. Kenny, thank you for all your help at the museum, sourcing species, and for always correcting my spelling of scientific names! And Nat, I cannot thank you enough for all your encouragement, hugs and for sharing your passion for anatomy with me throughout the last five years. You have offered endless support, guidance and patience throughout this project. I could not have done this without you all, so thank you. I am very thankful for the funders who have helped make this project possible; the Australian Postgraduate Award, and the top-up award from Murdoch University, the Graduate Women WA for the Mary Walters Scholarship that funded me to travel to Sydney to collect data, and the Murdoch University Postgraduate Travel Award that assisted in funding my travel to Washington DC to attend the International
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