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Biomineralisation Processes in the Radula Teeth of the Chiton Acanthopleura Hirtosa (Mollusca: Polyplacophora)

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Biomineralisation Processes in the Radula Teeth of the Chiton Acanthopleura Hirtosa (Mollusca: Polyplacophora) Biomineralisation processes in the radula teeth of the chiton Acanthopleura hirtosa (Mollusca: Polyplacophora) This thesis is presented for the degree of Doctor of Philosophy of Murdoch University, Western Australia 2007 Submitted by Jeremy Albert Shaw, B.Sc. (Hons) Murd. Murdoch University 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 institution. Jeremy Albert Shaw 2007 Abstract A detailed row-by-row investigation of major lateral tooth cusp mineralisation, together with the concomitant development of the superior epithelial tissue surrounding the teeth of the chiton Acanthopleura hirtosa has been undertaken using a combination of light microscopy, and scanning and transmission electron microscopy. A holistic approach has been adopted that encompasses observations over a range of spatial scales, from whole radula mineralisation processes to those occurring within individual tooth cusps at various stages of development. In addition, mineralisation in radulae from freshly collected animals has been compared to that of animals maintained for extensive periods within a newly developed iron-limited system, which restricts radula mineralisation without impeding the formation of the organic matrix. An evaluation of the iron-limitation technique has revealed that maintaining specimens of A. hirtosa within an iron-poor environment results in a significant departure from the normal pattern of mineralisation in these animals. As a consequence of iron-limitation, there is an obvious increase in the number of unmineralised tooth rows in addition to associated alterations in structure and composition at all stages of tooth development. In normal specimens of A. hirtosa, the onset of mineralisation in the tooth cusps occurs following the prior accumulation of iron at the junction zone and the sudden accumulation of iron-containing granules in the cusp epithelium at tooth row 13. The superior epithelium surrounding the tooth cusps undergoes a series of developmental changes leading up to, and following, the onset of mineralisation. In particular, the abundance of mitochondria within the apical cusp epithelium increases, presumably in order to provide the ideal conditions of pH, and thus solubility, needed for the supersaturation of iron and its nucleation at row 13. Once mineralisation has commenced, the microvilli attached to the cusps develop rapidly, and are suggested to i do so in order to facilitate the transport of iron, and thereby ensure that a high concentration gradient of this element into the cusps is maintained. The delivery of iron into the cusps occurs from two fronts, the first from the superior epithelium via the posterior surface, and the second from the junction zone via an internal pathway situated along the lepidocrocite boundary between the magnetite and core regions of the tooth. The existence of a plume of elements between this internal mineralisation pathway and the junction zone, provides the first direct evidence that the junction zone is involved in the storage and release of elements for cusp mineralisation. Data from iron-limited radulae also indicate that iron continues to be deposited at the junction zone in preference to the superior epithelium or cusps, despite the disruption of mineralisation, highlighting the importance of this region in the mineralisation process. Iron-reinstatement experiments have also shown that the internal pathways of iron delivery within the organic matrix remain viable, despite prolonged periods of iron-limitation. In addition, the reinstatement of iron has revealed that the plumes, situated between the junction zone and internal mineralising pathway of the cusp, stem from the centre of the plate-like junction zone, directly above the stylus canal, a tube-like cavity situated within the styli of each major lateral tooth. An in-depth study of the stylus canal has revealed that cells within the canal are remarkably similar to those of the epithelium surrounding the cusps, suggesting that this structure may also be involved in the delivery of ions to the junction zone. The stylus canal is shown to be present in the major lateral tooth cusps of 38 chiton species distributed worldwide, and is therefore likely to be a feature common to all chitons. The presence of the canal, and indeed its absence from the bases of all remaining non iron-mineralised teeth, irrespective of chiton species, also points strongly to a functional relationship between the stylus canal and tooth cusp mineralisation. ii Table of contents Abstract .............................................................................................................................. i Table of contents .............................................................................................................. iii Acknowledgements ............................................................................................................ v Chapter 1: General Introduction ................................................................................... 1 1.1. Mollusca: Polyplacophora ................................................................................. 1 1.1.1. Chiton distribution .................................................................................... 1 1.1.2. Chiton anatomy ......................................................................................... 2 1.1.3. Chiton diets ............................................................................................... 3 1.1.4. The chiton radula ...................................................................................... 3 1.2. Principals and processes of biomineralisation .................................................. 8 1.3. Biomineralisation in chiton radulae ................................................................ 10 1.4. Iron transport and storage................................................................................ 16 1.5. Justifications .................................................................................................... 21 1.6. Aims ................................................................................................................ 22 Chapter 2: General Methods........................................................................................ 24 2.1. Study site and sample collection ..................................................................... 24 2.2. Dissections ...................................................................................................... 24 2.3. Sample preparation for LM and TEM ............................................................. 27 2.4. Sample preparation for SEM ........................................................................... 29 2.5. Microscopy ...................................................................................................... 30 Chapter 3: Iron-limited radula development ............................................................. 32 3.1. Introduction ..................................................................................................... 32 3.2. Materials and methods .................................................................................... 34 3.3. Results ............................................................................................................. 35 3.4. Discussion ....................................................................................................... 39 Chapter 4: Major lateral tooth cusp mineralisation processes ................................. 44 4.1. Introduction ..................................................................................................... 44 4.2. Materials and Methods .................................................................................... 45 4.2.1. Normal radula mineralisation ................................................................ 45 4.2.2. Mineralisation in iron-limited and iron-reinstated radulae ................... 45 4.3. Results ............................................................................................................. 47 4.3.1. Normal radula mineralisation ................................................................ 47 4.3.2. Mineralisation in iron-limited and iron-reinstated radulae ................... 56 4.4. Discussion ....................................................................................................... 67 iii Chapter 5: The Superior Epithelium: Development and Iron Delivery .................. 75 5.1. Introduction ..................................................................................................... 75 5.2. Materials and Methods .................................................................................... 76 5.2.1. Normal epithelial development ............................................................... 76 5.2.2. Iron-limited and iron-reinstated epithelial development ........................ 77 5.2.3. Observations of the organic matrix......................................................... 77 5.3. Results ............................................................................................................. 77 5.3.1 Normal epithelial development ............................................................... 77 5.3.2. Iron-limited and iron-reinstated epithelial development ...................... 105 5.3.3. Observations of the organic matrix......................................................
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