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Circular Polarization Vision in Stomatopod Crustaceans Rachel Marie Templin Bmarst (Hons)

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Circular Polarization Vision in Stomatopod Crustaceans Rachel Marie Templin Bmarst (Hons) Circular polarization vision in stomatopod crustaceans Rachel Marie Templin BMarSt (hons) A thesis submitted for the degree of Doctor of Philosophy at The University of Queensland in 2017 Queensland Brain Institute Abstract Perhaps due to relative speed and reliability, the information that light provides is useful to many animals. As a result, visual systems are a major, sensory system in several animal groups. Various aspects of vision become tuned by the environment and behavioural need, including relative sensitivity, speed, colour, and in some species, polarization. The stomatopod crustaceans (mantis shrimps) are remarkable in that they possess, at the retinal level, the most complex colour system known including 12 spectral sensitivities. However, like other crustaceans their lifestyles may also rely on the information they can receive from polarization. This is evident from the range of polarization sensitive areas of their subdivided eye. The hemispheric regions of the stomatopod eye are linear polarization sensitive, in a total of four different e-vector orientations. Additionally, stomatopods are able to rotate their eyes making the actual angle of polarization sensitivity to the outside world arbitrary. Perhaps most interesting in the context of polarization vision is the function of the eighth retinular cells, known as R8, of rows 5 and 6 of the midband region. These birefringent cells act as quarter-wave retarders allowing stomatopods to be sensitive to circularly polarized light (CPL). This ability has yet to be demonstrated in other animals and compared to linear polarization vision (LPV), circular polarization vision (CPV) is not well understood. The aim of this thesis was to further investigate rows 5 and 6 of the midband in a range of stomatopod species, using both behavioural and anatomical techniques. Firstly, through modelling the birefringent properties of the R8 in six species, it is revealed that the ability to discriminate CPL is shared among many stomatopods (Chapter 2). Adaptive pressure to maintain the size of the R8 cell, achieving quarter-wave retardance, suggests that it provides an important role for stomatopods. However, one species included in this study, Haptosquilla trispinosa, is likely sensitive to a different ellipticity of polarized light than circular. Since its discovery in 2008, it was hypothesized that circular polarization vision could provide a covert communication system for stomatopods. Chapter 3 uses behavioural paradigms to examine the discrimination abilities of Gonodactylaceus falcatus, a species of stomatopod with extensive polarization patterns on their bodies, and demonstrates that they use circular polarization as a signal for burrow occupancy. However, as variation in body patterns exist between species, with some species having none at all, other roles for CPL need to be considered. H. trispinosa is one species of stomatopod that lacks circularly polarized reflections, and the birefringent properties of their R8 cells, presented in Chapter 2, favours sensitivity to a form of elliptically polarized light, not circular. Behavioural discrimination tests ii confirm the presence of elliptical polarization vision (EPV) in this burrow dwelling species and further behavioural testing provided possible uses for this new polarization sensitivity. Understanding how an animal uses an ability like CPV, or EPV, when humans are insensitive to this property of light present many challenges. While the retinal anatomy of stomatopods is relatively well understood the neural processing of visual information, a vital part of this understanding, has been relatively neglected in stomatopods. The final research chapter of this thesis (Chapter 5) uses serial blockface scanning electron microscopy to investigate the first optic neuropil, the lamina. A three-dimensional reconstruction of individual lamina cartridges allows identification of cell types and pathways below the retina and provides a new method for use in stomatopod neural architecture investigations. The research presented in this thesis provides evidence contrary to the assumption that row 5 and 6 of the midband provide all species with CPV, despite appearing anatomically identical. We present a number of alternative hypotheses for the function of these rows, highlighting the likelihood that for different species specific roles exist. iii Declaration by author This thesis is composed of my original work, and contains no material previously published or written by another person except where due reference has been made in the text. I have clearly stated the contribution by others to jointly-authored works that I have included in my thesis. I have clearly stated the contribution of others to my thesis as a whole, including statistical assistance, survey design, data analysis, significant technical procedures, professional editorial advice, and any other original research work used or reported in my thesis. The content of my thesis is the result of work I have carried out since the commencement of my research higher degree candidature and does not include a substantial part of work that has been submitted to qualify for the award of any other degree or diploma in any university or other tertiary institution. I have clearly stated which parts of my thesis, if any, have been submitted to qualify for another award. I acknowledge that an electronic copy of my thesis must be lodged with the University Library and, subject to the policy and procedures of The University of Queensland, the thesis be made available for research and study in accordance with the Copyright Act 1968 unless a period of embargo has been approved by the Dean of the Graduate School. I acknowledge that copyright of all material contained in my thesis resides with the copyright holder(s) of that material. Where appropriate I have obtained copyright permission from the copyright holder to reproduce material in this thesis. iv Publications during candidature Peer-reviewed papers Templin, R. T., How, M. J., Chiou, T-H., Roberts, N. W., Marshall, N. J. 2017. Circular polarized light detection in stomatopod crustaceans: a comparison of photoreceptors and possible function in six species. Journal of Experimental Biology, Advanced Online Article. Gagnon, Y. L., Templin, R. M., How, M. J., Marshall, N.J. 2015. Circularly polarized light as a communication signal in mantis shrimps. Current Biology 25, 3074-3078. Conference abstracts Templin, R. T., How, M. J., Chiou, T-H., Roberts, N. W., Marshall, N. J. 2014. Circular polarization vision in stomatopods. Australasian Neuroscience Society, Adelaide, Australia. Gagnon, Y. L., Templin, R. M., How, M. J., Marshall, N.J. 2014. Circular polarization: Covert communication in stomatopods. Australasian Society for the Study of Animal Behaviour, Katoomba, Australia. Templin, R. T., Gagnon, Y. L., How, M. J., Chiou, T-H., Roberts, N. W., Marshall, N. J. 2014. Circular polarization vision in the stomatopod Gonodactylaceus falcatus. International Congress of Neuroethology, Sapporo, Japan. Templin, R. T., Gagnon, Y. L., How, M. J., Chiou, T-H., Roberts, N. W., Marshall, N. J. 2015. A third form of polarization vision: Elliptical polarization vision in Haptosquilla trispinosa. Gordon Research Conference, Neuroethology, Lucca, Italy. Templin, R. T., Gagnon, Y. L., How, M. J., Chiou, T-H., Roberts, N. W., Marshall, N. J. 2015. A third form of polarization vision: Elliptical polarization vision in Haptosquilla trispinosa. Behaviour, Cairns, Australia. Publications included in this thesis Templin, R. T., How, M. J., Chiou, T-H., Roberts, N. W., Marshall, N. J. 2017. Circular polarized light detection in stomatopod crustaceans: a comparison of photoreceptors and v possible function in six species. Journal of Experimental Biology, Advanced online article – incorporated as chapter 2 Contributor Statement of contribution Concept and design (30%) Data collection, analysis and Rachel Templin (Candidate) interpretation (70%) Drafting and editing (75%) Concept and design (20%) Data collection, analysis and Martin How interpretation (15%) Drafting and editing (5%) Tsyr-hui Chiou Concept and design (10%) Concept and design (30%) Data collection, analysis and Nicholas Roberts interpretation (15%) Drafting and editing (10%) Concept and design (10%) Justin Marshall Drafting and editing (10%) Gagnon, Y. L., Templin, R. M., How, M. J., Marshall, N. J. 2015. Circularly polarized light as a communication signal in mantis shrimps. Current Biology 25, 3074-3078 – incorporated as chapter 3 Contributor Statement of contribution Concept and design (60%) Data collection, analysis and Yakir Gagnon interpretation (60%) Drafting and editing (40%) Concept and design (30%) Data collection, analysis and Rachel Templin (Candidate) interpretation (30%) Drafting and editing (25%) vi Concept and design (10%) Data collection, analysis and Martin How interpretation (10%) Drafting and editing (30%) Justin Marshall Drafting and editing (5%) vii Contributions by others to the thesis - Chapter 2: Associate professor Nick Roberts wrote the code for the optical birefringence model. Dr Martin How provided the R8 measurements across the whole retina of a single eye. - Chapter 3: Dr Yakir Gagnon collected the data for the refuge choice experiments and polarimetry. And carried out majority of initial drafting. - Chapter 4: Professor Tsyr-hui Chiou contributed to the ideas of the chapter. - Chapter 5: Dr Hanne Thoen contributed to ideas and interpretation of data, as well as the editing
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