Comparisons of visual capabilities in modern cephalopods from shallow water to deep sea

Chung, Wen-sung (2014). Comparisons of visual capabilities in modern cephalopods from shallow water to deep sea PhD Thesis, Queensland Brain Institute, The University of Queensland.

       
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Author Chung, Wen-sung
Thesis Title Comparisons of visual capabilities in modern cephalopods from shallow water to deep sea
School, Centre or Institute Queensland Brain Institute
Institution The University of Queensland
Publication date 2014
Thesis type PhD Thesis
Supervisor Justin Marshall
Kerstin Fritsches
Total pages 193
Total colour pages 35
Total black and white pages 158
Language eng
Subjects 060805 Animal Neurobiology
060205 Marine and Estuarine Ecology (incl. Marine Ichthyology)
060806 Animal Physiological Ecology
Formatted abstract
Squid have undergone a series of evolutionary changes to form the hydrodynamic body, well-developed senses, and large brain lobes, rendering the most intelligent and fast invertebrate. Remarkably, squid possess large eyes to catch prey and avoid distant threats. Aside from renowned visual performance of squid in well-lit conditions, their large eyes are adaptive to increase light-gathering ability, resulting that squid are active at nighttime as well as in the sunless deep sea.

In an effort to better understand visual function of squid at different light environments, this study aimed using three methods to approach the goals, including interspecific anatomical comparisons of visual systems, behavioural observations, and functional assay of visual system. In Chapter 2, contrast-enhanced magnetic resonance imagery (MRI) was applied to investigate intact coleoids. A digitised neural atlas has been initiated, provided a non-invasive method to identify internal structures. Given MRI anatomical inspections combined with histology, the post-reconstruction of three dimensional brain and eye anatomical models revealed several new morphological adaptations across diverse species, including fovea, retinal ridge, and retinal bump. Also, volume estimation using MRI improved the resolution of standard histological methods. Regional specialisations of the retina, changes of eye shapes, and optical lobe sizes were assessed. In addition to several novel findings, supported by methods in other chapters, these anatomical adaptations correlate well with the living strategy and the light condition of individual species. The retinal deformation and the resulting advantage of eyesight become a unique solution in their daily visual tasks.

Along with gross morphological changes in squid eye dimensions and the deformation of retinal layers, Chapter 3 and 4 focused on the retinal architecture and corresponding functional adaptations. Firstly, light-filtering mechanisms, pupillary activities and dynamic screening pigment movements, were well tuned to optimise light gathering abilities. Furthermore, optical properties of squid eye showed that the enlarged lens and its high resolving power are most likely adapted to enhance light capture and extend its visual range in the twilight realm instead of high resolution visual tasks. Furthermore, a new type of the retinal cell was discovered in the proximal region of the inner segment layer in a group of mid-water squid. The depth distribution range of these squid possessing this dual layered retina was usually broader (50-1000 m) than the depth range (50-400 m) of those contained a regular retina. Positive immuno-histological labelling in this new form of the 2nd order retinal cells showed cross connections between cells in the retina, indicating that squid are likely to develop a neural summation mechanism to enhance light sensitivity analogous to the ganglion cells for deep-sea fish. This type of cross-connectivity in cephalopods has not been noted previously.

The second part of this study aimed to explore the visual function in situ and ex vivo using a common reef squid, Sepioteuthis lessoniana. The assumption that a single class of photoreceptor in cephalopod has a single type of visual pigment has been accepted in the literature with an exception of a Japanese firefly squid, Watasenia scintillans, which three different visual pigments are embedded in three receptors with different morphological features. According to morphological evidence in Chapter 2 and 3, S. lessoniana possesses a unique retina which comprises of two types of photoreceptors with different arrangements of rhabdomere, similar to the photoreceptors of the banked retina of W. scintillans. In Chapter 5, a new protocol of microspectrophotometry (MSP) was developed to solve the difficulty in bleaching visual pigment of cephalopod and accelerate the procedure in investigating the spectral absorption of visual pigment of squid. Furthermore, using this method enables to measure the spectral sensitivity of an individual photoreceptor rather than the regular measurement of the retinal extracts of an entire retina. Given these advantages, the distribution pattern of visual pigment across the retina in S. lessoniana was therefore reconstructed, representing small amounts of variance in spectral sensitivity. Although MSP results demonstrated that this common reef squid only contains a single visual pigment as do all other shallow water cephalopods known, this new method provides a new way in studying cephalopod visual pigment in the future study.

In Chapter 6, a new optical adaptation in squid is described. The eyes of less than terminal adult phases display a retinal bump within the eye, resulting in hyperoptic defocus in a large portion of the dorso-temporal retina. This has been confirmed in S. lessoniana in vivo and vitro. Although this blurring of vision in the critical region of the eye coordinating tentacular strike seems disastrous for these visually-guided predators, the deformation of retina combined with a unique head bobbing behaviour becomes an efficient solution to estimate the distance of objects. When head bobbing, the image of interest objects consecutively pass from focused and defocused retinal regions and the resulting focus differential provides squid a simple cue for distance without stereopsis or parallax, prior to rapid prey-catching tentacular strikes. This unique range finding mechanism is an adaptation to hunting, defense and other important object size identification tasks, against a contrast-poor background.

The third part of this study was using new design baited deep-sea cameras with illumination which is invisible to the animal, allowing the observation of squid visual behaviours in their natural habitat between 500-1100 m. In Chapter 7, the visual ecology of deep-sea squid in areas of diminishing sun light and more frequent bioluminescent flashes was investigating using unobtrusive in situ videography. Custom-designed baited cameras with animal-invisible illumination recorded natural behaviours of squid from four different species at depths between 525-790 m. A light lure emitting artificial bioluminescent flashes triggered apparent squid foraging and attacking behaviours. These included the first observation of feeding behaviour of the giant squid, Architeuthis dux in its natural habitat. Aside from the light lure to attract attention, the use of bait at different ambient light conditions demonstrated that decreasing ambient light intensity significantly disrupted the successful feeding rate in the Humboldt squid, Dosidicus gigas.

Overall, this study provides several new insights into anatomical adaptations of retina and brain in several cephalopod species as well as corresponding functional improvements which are associated with optimising visual capabilities in a large depth and illumination range. In conclusion, cephalopod vision and visual behaviour appear more complex rather than our previous expectation.
Keyword Coleoid
Magnetic resonance imagery
Comparative anatomy of cephalopod brain
Retinal neural circuits
Visual adaptation
microspectrophotometry
Absorbance of visual pigment
Colour-blindness
Retinal bump
range-finding
Matched filter
Giant squid
Visual ecology

 
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Created: Mon, 19 May 2014, 12:26:10 EST by Wen-sung Chung on behalf of Scholarly Communication and Digitisation Service