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The Visual System of Seahorses and Pipefish: a Study of Visual Pigments and Other Characteristics

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The Visual System of Seahorses and Pipefish: a Study of Visual Pigments and Other Characteristics The visual system of seahorses and pipefish: A study of visual pigments and other characteristics. Virginia Jan Mosk Bachelor of Science, University of Melbourne Post Graduate Diploma of Science, The University of Western Australia This thesis is presented for the degree of Master of Science THE UNIVERSITY OF WESTERN AUSTRALIA School of Animal Biology Zoology December 2004 Abstract Syngnathidae (seahorse, pipefish, pipehorses & seadragons) are highly visual feeders with different species feeding on specific types of prey, a behaviour that has been related to snout length. Worldwide, many species have become threatened by habitat destruction, collection for the aquarium trade and exploitation for traditional medicine, as well as recreational and commercial bycatch. Attempts to establish aquaculture programs have been of limited success. Little is known about their visual capabilities in detail. The visual systems of fishes are known to have evolved specific adaptations that can be related to the colour of water in which they live and specific visual tasks such as predator detection and acquisition of food. This study examined the ocular and retinal morphology, photoreceptor structure and spectral sensitivity of adult individuals of a local pipefish (S. argus), local seahorse (Hippocampus subelongatus) which both inhabit green water seagrass beds, and a tropical species of seahorse (Hippocampus barbouri) from blue water coral reefs. Some juveniles were also investigated. Accordingly, we developed an understanding of the features that are common to all syngnathids and those that have evolved for specific environments. Cryosections of the eyes were taken to determine morphological distinctions of this group. Lens characteristics measured using a spectrophotometer determined 50% cut-off wavelengths below 408nm for all 3 species, hence no transmission of UV light to the retina. Histological examination determined a cone dominated fovea in the ventro-temporal retina and very large rods concentrated in the peripheral retina and adjacent to the optic nerve. Microspectrophotometry measured the absorption characteristics of the visual pigments within the photoreceptors showing the presence and maximum sensitivity (λmax) of rods, SWS single cones, and a broad, complex array of LWS double/twin cones. The results are discussed in relation to the light environment inhabited by each species and their feeding requirements. The implications for the design of suitable light environments for aquarium and aquaculture programs for the Syngnathidae are also discussed. Rearing success of this family of fish, for both the aquarium trade and re-stocking programs, would be advised to take lighting regimes and specifics of the animals’ vision into account. i Table of contents Abstract i Acknowledgements vi List of Abbreviations vii Chapter 1: INTRODUCTION 1 The underwater light environment 1 Visual system structural organisation in fish 4 Eye and optics 4 Optics: Cornea and Lens 4 Retinal and photoreceptor structure 6 Colour sensitivity of photoreceptors 8 Development of the fish retina 11 The Syngnathidae 12 Vision in syngnathids 15 Rationale and broad aims of this study 17 Chapter 2: MATERIALS AND METHODS 19 Animals - Stigmatopora argus 19 Hippocampus subelongatus 19 Hippocampus barbouri 20 Pugnaso curtirostris 21 Seahorse and pipefish collection, holding and experiments 22 Morphology 24 Pupil response 24 Measurements of ocular dimensions from cryosections 25 Lens transmission spectra 26 Microspectrophotometry (MSP) 27 Tissue preparation 27 Measurement of visual pigment absorbance spectra 28 Analysis of the visual pigment absorbance spectra 28 Chapter 3: RESULTS 30 External morphology and orientations of the body 30 Adults - Stigmatopora argus 30 Hippocampus subelongatus 31 Hippocampus barbouri 32 ii Snout length as a proportion of head length, and eye diameter as a proportion of snout length 33 Ocular Structure and Dimensions 35 Lens colour and shape 36 Lens transmission spectra 37 Pupil response 38 Retinal structure 38 Histology 40 The photoreceptors and their visual pigments 45 Adults 45 Rods 46 Cones 50 Pairings 60 Juveniles 62 Chapter 4: DISCUSSION 65 Morphology and eye structure 65 Snout length to head length, and eye diameter to snout length 65 Irideal flaps 66 Pupil Dilation 67 Ocular Dimensions and function 68 Lens properties 69 Shape 69 Filtering Effects 69 Photoreceptor structure and photoreceptors 71 Rods 72 Cones 72 Colour sensitivity of the photoreceptors 73 Rods 73 Cones 74 Mechanisms of visual pigment absorbance of double cones 77 Juveniles 77 Future directions 79 REFERENCES 81 iii Acknowledgements This study and thesis only eventuated with the combined assistance of many individuals whom I have the greatest pleasure in thanking: Special thanks to my supervisors Dr Julia Shand and Professor Lyn Beazley. Lyn, for her positive support, enthusiasm and assistance in realising this unusual dream, attending the Seadragon Festival and trips to AQWA. Julia, for providing the quiet, consistent assistance, and warmth and support that I needed throughout the project and her understanding about issues involved in juggling single-parenting of a young child, and other difficulties that life throws at you. We both leant much and I will always have deep respect and admiration. Both wonderful women gave me the space and freedom to peak and trough as I needed. Dr Nicole Thomas and Dr Nathan Hart for their immense assistance during many hours in the dark room with the MSP and analysing the visual pigment data. Warm thanks to Michael Archer for his brilliant expertise in everything computer related, also teaching me and assisting with the histological slides. Michael endured much frustration during my steep learning curve. The lovely Brenda Loney, and the rest of the Neuroscience Lab. for their support, encouragement and kindness. I had many breaks during this study and their faces were always welcoming and positive when I returned. Dr Alan Kendrick for his kindness and generosity in sharing whatever information he had on these wonderful animals’, and for helping me through the seasickness. Dr Glenn Hyndes for his talks on seagrasses and positive interest. Andy Grice and Dr Mic Payne, Dr Craig Lawerence, Glenn Moore and Paul Groves for their passion for seahorses, sharing of information and generosity in providing animals. Also, Project Seahorse, Dragon Search, Victoria & NSW Museums for sharing information. Rudie Kuiter for his informal chats and emails, his zeal and individuality in the study of these beautiful animals. Professor Dale Roberts for critical and very helpful comments on the thesis. Dr Julian Partridge for his optimistic and constructive help with the project generally, assistance with lens transmission data, fishing and newspaper interviews. Dr Ian Williams (and wife Judy) for their kind, gentle, warm and encouraging support throughout the project, guidelines for writing the thesis, completion of the Rottnest swim together, pep talks, training of wilful dogs and breakfasts at ‘Beaches’ and ‘Beverley’. Dr Jasper Trendall for his interest in the project, ‘Leafies’, and valuable comments on a very rough draft of the thesis. Also, the hospitality shown by Jasper and his beautiful lady, Lindy Leggett, on trips to Albany. The inner circle…. Cate Kandiah, Claire D’Angelo, Jackie Hooper, David Worthy, Trish Grindrod, Marion Raad, Lorna Stewart, Karen Dewar, Tim Carew-Reid for their friendship, support and conviction that I really am quite mad…….and Aaron Zee for his sacrifices and patience in allowing me to complete another higher degree whilst mothering him, and zipping him around to his activities. This study spanned from years 5 to 9 of his young life, and the wisdom, interest and support he has shown has always been way beyond his years. iv List of Abbreviations λ ………………………………………………………………………...wavelength λmax ………….…………….wavelength of maximum absorption (lambda max) INL……………………………………………………..….…….inner nuclear layer LWS…………………………………………………….long wavelength-sensitive MSP ……………………………………………………..microspectrophotometry MWS……………………………………………….medium wavelength-sensitive ONL……………………………………………………………..outer nuclear layer OS……………………………………………………………………outer segment PBS ……………………………………………………phosphate-buffered saline RH1…………………………………………………………………...rod rhodopsin RH2………………………………………………………………rod rhodopsin-like SWS……………………………………………………short wavelength-sensitive TCM …………….……….…………………………Traditional Chinese Medicine UV …………….…………………………………………………………..ultraviolet v Chapter I - Introduction Chapter 1. INTRODUCTION The underwater light environment The ocean’s epipelagic zone (from the surface to around 200 meters depth) is considered the photic zone where sunlight penetrates sufficiently to support primary production by photosynthesis and supports the food web (Castro & Huber, 1997). The sun’s electromagnetic radiation is visible to humans when it is of a wavelength in the range 400 to 700 nanometers (nm) (Figure 1). Light of the wavelength of approximately 400nm appears violet to humans. Ultraviolet wavelengths are those shorter than 400nm. Light approaching 700nm appears red. Wavelengths beyond 700nm are termed infrared. Figure 1. The electromagnetic spectrum. (Goldstein, 1996) At the water’s surface, the radiation from the sun extends in a spectral band ranging from approximately 300nm in the ultraviolet to around 1100 nm in the infrared. Light is rapidly attenuated through the depth of the water column by the absorption of both short and long wavelengths. The rate
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