Elasmobranchs (sharks, skates and rays) first appeared over 400 million years ago. They represent a highly diverse group of individuals that have effectively inhabited the majority of marine and some freshwater environments worldwide. The evolutionary success of elasmobranchs has commonly been attributed to their development of highly specialised sensory organs to enhance their capacity to detect potential predators, prey and conspecifics. Despite the large number of sensationalist claims as to the sensory capabilities of elasmobranchs, limited specific and detailed knowledge on their individual senses exists. In recent years, the anatomy of the sensory organs has been investigated for a wide variety of elasmobranchs and has been used to infer the sensory capabilities of species in respect to their biology and ecology. However, behavioural experiments are required to ascertain the sensory capabilities of animals. The aim of this project was to investigate the visual and olfactory capacity of the giant shovelnose ray Glaucostegus typus (Anonymous [Bennett] 1830), behaviourally.
Experiments based on associative learning were utilised to examine the colour vision capacity and brightness discrimination abilities of juvenile G. typus. This approach required conditioning animals to select a specific target in order to obtain food. The rewarded target was later displayed together with a number of different distracter stimuli in order to test their visual discrimination capabilities. Experiments designed to test the olfactory sensitivity of G. typus to potential prey items utilised unconditioned behavioural reactions. In this instance, olfactory stimuli derived from natural prey items of varying concentrations were added to aquaria containing G. typus and the behavioural reactions of the individuals were recorded.
Glaucostegus typus successfully performed a four-choice visual discrimination task, in which individuals reliably discriminated a coloured reward stimulus from six distracter stimuli of the same hue but varying brightness, (binomial probability, p≤0.001). Furthermore, G. typus was able to generalise from their original reward stimulus (with a given brightness and hue) to a larger group of rewarded stimuli that were identical in hue but varied in brightness without additional training. This was demonstrated by their continued ability to discriminate between the rewarded and distracter stimuli (binomial probability, p≤0.004). The ability to successfully discriminate two coloured stimuli, irrespective of brightness cues demonstrates that G. typus possesses colour vision.
The next step was to test the dimensionality of G. typus’ colour vision system. Colours were designed that would only appear different to G. typus if they possessed three spectrally distinct photoreceptor types. Glaucostegus typus completed a two-choice discrimination task in which individuals reliably discriminated between the reward and the distracter stimuli with an accuracy of between 70.0-90.0% correct choices. Results from this study indicate that G. typus possesses a trichromatic colour vision system.
The role that brightness discrimination plays within this species’ visual ecology remains unknown. Our objective was to investigate two aspects of brightness discrimination in G. typus through the use of two-choice discrimination tasks. The first experiment was designed to test whether G. typus was capable of learning the absolute brightness of a trained “grey” stimulus when presented with an array of “grey” distracter stimuli of the same hue but differing brightness, with some brighter, others darker than the reward stimulus. Glaucostegus typus was unable to identify the rewarded stimulus from the eight distracter stimuli. Furthermore, G. typus failed a secondary, more simplistic task in which the number of distracter stimuli rays were required to discriminate between was reduced to three. Their inability to solve this task demonstrates that G. typus is unable to discriminate stimuli on the basis of absolute brightness alone.
The second experiment tested by how much two stimuli were required to differ in brightness in order for G. typus to reliably discriminate between them. Glaucostegus typus was presented with two stimuli of varying brightness and required to select the brighter of the two stimuli to receive a reward. If the animals were able to discriminate between the two stimuli the brightness of the distracter stimulus was increased, resulting in a reduced difference in relative brightness between the stimuli, until G. typus could no longer discriminate the reward from the distracter. Results indicated that G. typus was capable of discriminating between two stimuli that differed by 69.6%, in reflectance, however only one animal was able to discriminate stimuli that differed by 58.9% and further testing of this individual revealed that a difference of 26.4% was no longer sufficient for discrimination. These results imply that G. typus is likely to utilise other visual cues in conjunction with brightness (i.e. colour) to discriminate between objects.
Visual cues are not the only sensory system available to G. typus to aid in the detection of objects including potential predators, prey and conspecifics. Elasmobranchs possess a variety of senses that can be used in combination or individually. Olfaction is one of these senses, which has been investigated in relative detail from anatomical and electrophysiological perspectives. Behavioural experiments have been conducted on sharks. However, to date no information has been published in respect to the behavioural olfactory capabilities of batoids (skates and rays). Due to this lack of knowledge the aim of the olfactory component of this thesis was to investigate the olfactory capabilities of a well-studied species (G. typus) to identify the behavioural responses of G. typus in regard to olfactory cues.
Glaucostegus typus was exposed to a range of chemical stimuli at varying concentrations to determine the types of chemical cues that the rays detected and the behavioural responses elicited to the olfactory cues at the different concentrations. Glaucostegus typus was attracted to teleost fish and penaeid prawn extracts, however they did not respond to olfactory cues pertaining to sandworm and bloodworm extracts and seawater. A number of food searching behaviours were observed that were classified as positive reactions to an olfactory stimulus. Glaucostegus typus detected prawn extract over a range of differing concentrations between 6 x 104 - 1 x 10-6 ppm, suggesting their olfactory sensitivity is relatively high. The behavioural responses of G. typus upon detection of the stimuli included two types of food searching behaviours. A searching pattern including tight circling near the site of the stimulus source was observed throughout all concentrations of prawn extract and was demonstrated to be the most appropriate behaviour to ascertain whether G. typus had detected the stimulus. Whilst a secondary food searching behaviour classified as ‘Behaviour X’ was only observed at the two highest concentrations (6 x 101 and 6 x 104 ppm).
Overall, behavioural experiments support suggestions from previous studies that G. typus possesses well developed visual and olfactory systems. Glaucostegus typus is able to distinguish between objects using colour. This species possesses a trichromatic colour vision system as predicted by the presence of three spectrally distinct photoreceptor types. Experiments on their brightness discrimination abilities suggest that brightness alone is an unreliable cue for object discrimination and that colour vision provides an additional mechanism to aid in the detection and classification of objects such as potential predators, mates and landmarks. Olfaction appears to play a key role in the sensory ecology of G. typus. Rays were attracted to an array of potential food sources via olfactory cues alone and exhibited feeding behaviours similar to those reported for the bonnethead shark Sphyrna lewini and the tiger shark Galeocerdo cuvier. Glaucostegus typus extracts food from below the substrate, where olfaction is predicted to aid in the detection of prey items. The ability to detect low concentrations of olfactory stimuli and orient towards the source without the use of additional senses suggests that G. typus’ olfactory sense is primed to enhance their ability to detect prey items. The behavioural responses of rays to the various tasks undertaken suggest that the visual and olfactory systems of G. typus are well-adapted to aid in the detection of prey items and additionally may be useful for predator avoidance and mate detection.
The experiments undertaken in this thesis are the first of their kind to investigate the visual and olfactory capabilities of a batoid species using behavioural methods. Chapters 2 and 3 report the first published record of not only colour vision but trichromatic colour vision in an elasmobranch. Chapter 4 describes the first study conducted to examine brightness discrimination in an elasmobranch. Chapters 5 and 6 describe olfactory experiments never before conducted on batoids and furthermore describe the first report of concentration dependent behaviour identified in an elasmobranch. The behavioural methods created and described in this thesis provide suitable experimental protocols to further assess the visual and olfactory systems of G. typus along with other elasmobranchs.