Ryan M. Kempster

Assessing the potential for post-copulatory sexual selection in elasmobranchs

This review highlights the potential role that post-copulatory sexual selection plays in elasmobranch reproductive systems and the utility of this group to further understanding of evolutionary responses to the post-copulatory processes of sperm competition and cryptic female choice. The growing genetic evidence for female multiple mating (polyandry) in elasmobranchs is summarized. While polyandry appears to be common in this group, rates of multiple paternity are highly variable between species suggesting that there is large variance in the strength of post-copulatory sexual selection among elasmobranchs. Possible adaptations of traits important for post-copulatory sexual selection are then considered. Particular emphasis is devoted to explore the potential for sperm competition and cryptic female choice to influence the evolution of testes size, sperm morphology, genital morphology and sperm storage organs. Finally, it is argued that future work should take advantage of the wealth of information on these reproductive traits already available in elasmobranchs to gain a better understanding of how post-copulatory sexual selection operates in this group.

Survival of the stillest : predator avoidance in shark embryos

Sharks use highly sensitive electroreceptors to detect the electric fields emitted by potential prey. However, it is not known whether prey animals are able to modulate their own bioelectrical signals to reduce predation risk. Here, we show that some shark (Chiloscyllium punctatum) embryos can detect predator-mimicking electric fields and respond by ceasing their respiratory gill movements. Despite being confined to the small space within the egg case, where they are vulnerable to predators, embryonic sharks are able to recognise dangerous stimuli and react with an innate avoidance response. Knowledge of such behaviours, may inform the development of effective shark repellents.

Phylogenetic and ecological factors influencing the number and distribution of electroreceptors in elasmobranchs

Electroreception is found throughout the animal kingdom from invertebrates to mammals and has been shown to play an important role in prey detection, facilitating social behaviours, the detection of predators and orientation to the earths magnetic field for navigation. Electroreceptors in elasmobranchs, the ampullae of Lorenzini, detect minute electric fields and independently process these stimuli, thereby providing spatial information to the central nervous system on the location of a source, often potential prey. The ampullae of Lorenzini are individually connected to a single somatic pore on the surface of the skin, with the spatial separation of each pore directly influencing how electrical stimuli are detected and processed. Pore abundance varies across taxonomic groups resulting in unique species-specific differences. The intricate distribution patterns created by the specific positioning of somatic pores on the head are, however, consistent within families, resulting in patterns that are identifiable at higher taxonomic levels. As elasmobranchs evolved, the electrosensory system became more complex and highly specialized, which is evident by a general trend of increasing pore abundance over time. The elasmobranch electrosensory system has evolved to operate efficiently under the environmental conditions of the particular habitat in which a species lives. For example, reduced pore abundance is evident in oceanic pelagic elasmobranchs, for whom visual cues are thought to be of great importance. Pore abundance and spatial distribution may be influenced by multiple factors including head morphology, phylogeny, feeding behaviour and habitat.

Dietary partitioning by five sympatric species of stingray (Dasyatidae) on coral reefs

Dietary characteristics and the degree of dietary partitioning by five species of sympatric stingray were assessed using stomach content and sediment analyses within a coral reef lagoon at Ningaloo Reef, Western Australia (the cowtail Pastinachus atrus, blue-spotted fantail Taeniura lymma, blue-spotted mask Neotrygon kuhlii, porcupine Urogymnus asperrimus rays and the reticulate whipray Himantura uarnak). A total of 2804 items were recovered from the stomachs of 170 rays and 3215 individual taxa from the environment, which were used in selectivity analyses. Twenty-four prey taxa were identified from stomach contents and pooled into 10 taxonomic categories for analysis, of which annelids, prawns, brachyurans and bivalves were the most abundant, together accounting for 96% of the diet. Himantura uarnak had the greatest interspecific dissimilarity in diet, consuming a larger proportion of crustaceans, notably penaeids (41% of total diet) than the other four species of rays, all of which had diets dominated by annelids (71-82% of total diet). Crustacean specialization by H. uarnak may exist to maximize resources and reduce competition among sympatric species. The remaining species may partition resources on the basis of space, rather than diet.

Sexual dimorphism of the electrosensory system: A quantitative analysis of nerve axons in the dorsal anterior lateral line nerve of the blue-spotted fantail stingray (taeniura lymma)

Quantitative studies of sensory axons provide invaluable insights into the functional significance and relative importance of a particular sensory modality. Despite the important role electroreception plays in the behaviour of elasmobranchs, to date, there have been no studies that have assessed the number of electrosensory axons that project from the peripheral ampullae to the central nervous system (CNS). The complex arrangement and morphology of the peripheral electrosensory system has a significant influence on its function. However, it is not sufficient to base conclusions about function on the peripheral system alone. To fully appreciate the function of the electrosensory system, it is essential to also assess the neural network that connects the peripheral system to the CNS. Using stereological techniques, unbiased estimates of the total number of axons were obtained for both the electrosensory bundles exiting individual ampullary organs and those entering the CNS (via the dorsal root of the anterior lateral line nerve, ALLN) in males and females of different sizes. The dorsal root of the ALLN consists solely of myelinated electrosensory axons and shows both ontogenetic and sexual dimorphism. In particular, females exhibit a greater abundance of electrosensory axons, which may result in improved sensitivity of the electrosensory system and may facilitate mate identification for reproduction. Also presented are detailed morphological data on the peripheral electrosensory system to allow a complete interpretation of the functional significance of the sexual dimorphism found in the ALLN.

How Close is too Close? The Effect of a Non-Lethal Electric Shark Deterrent on White Shark Behaviour

Sharks play a vital role in the health of marine ecosystems, but the potential threat that sharks pose to humans is a reminder of our vulnerability when entering the ocean. Personal shark deterrents are being marketed as the solution to mitigate the threat that sharks pose. However, the effectiveness claims of many personal deterrents are based on our knowledge of shark sensory biology rather than robust testing of the devices themselves, as most have not been subjected to independent scientific studies. Therefore, there is a clear need for thorough testing of commercially available shark deterrents to provide the public with recommendations of their effectiveness. Using a modified stereo-camera system, we quantified behavioural interactions between white sharks (Carcharodon carcharias) and a baited target in the presence of a commercially available, personal electric shark deterrent (Shark Shield Freedom7™). The stereo-camera system enabled an accurate assessment of the behavioural responses of C. carcharias when encountering a non-lethal electric field many times stronger than what they would naturally experience. Upon their first observed encounter, all C. carcharias were repelled at a mean (± std. error) proximity of 131 (± 10.3) cm, which corresponded to a mean voltage gradient of 9.7 (± 0.9) V/m. With each subsequent encounter, their proximity decreased by an average of 11.6 cm, which corresponded to an increase in tolerance to the electric field by an average of 2.6 (± 0.5) V/m per encounter. Despite the increase in tolerance, sharks continued to be deterred from interacting for the duration of each trial when in the presence of an active Shark Shield™. Furthermore, the findings provide no support to the theory that electric deterrents attract sharks. The results of this study provide quantitative evidence of the effectiveness of a non-lethal electric shark deterrent, its influence on the behaviour of C. carcharias, and an accurate method for testing other shark deterrent technologies.

The distribution and abundance of electrosensory pores in two benthic sharks: A comparison of the wobbegong shark, Orectolobus maculatus, and the angel shark, Squatina australis

Electroreception is an ancient sense found in many aquatic animals, including sharks, which may be used in the detection of prey, predators and mates. Wobbegong sharks (Orectolobidae) and angel sharks (Squatinidae) represent two distantly related families that have independently evolved a similar dorso-ventrally compressed body form to complement their benthic ambush feeding strategy. Consequently, these groups represent useful models in which to investigate the specific morphological and physiological adaptations that are driven by the adoption of a benthic lifestyle. In this study, we compared the distribution and abundance of electrosensory pores in the spotted wobbegong shark (Orectolobus maculatus) with the Australian angel shark (Squatina australis) to determine whether both species display a similar pattern of clustering of sub-dermal electroreceptors and to further understand the functional importance of electroreception in the feeding behaviour of these benthic sharks. Orectolobus maculatus has a more complex electrosensory system than S. australis, with a higher abundance of pores and an additional cluster of electroreceptors positioned in the snout (the superficial ophthalmic cluster). Interestingly, both species possess a cluster of pores (the hyoid cluster, positioned slightly posterior to the first gill slit) more commonly found in rays, but which may be present in all benthic elasmobranchs to assist in the detection of approaching predators.

How Elasmobranchs Sense Their Environment

1. Introduction 2. The Visual System 2.1. The Eye and Image Formation 2.2. Photoreception and Spectral Sensitivity 2.3. The Retina and the Choroidal Tapetum 2.4. Visual Sampling 2.5. Visual Abilities 3. The Non-visual System 4. The Auditory and Vestibular Systems 4.1. The Inner Ear 4.2. Vestibular Control 4.3. Auditory Abilities 5. The Electrosensory System 5.1. Structure and Spatial Sampling of the Ampullary Organs 5.2. Role in Passive Electroreception 5.3. Role in Magnetoreception 6. The Lateral Line System 6.1. Canal and Superficial Neuromasts 6.2. Sensitivity to Hydrodynamic Stimuli 7. Cutaneous Mechanoreception 8. The Chemosensory Systems 8.1. The Olfactory Apparatus and the Sampling of Water-Borne Substances 8.2. Olfactory Sensitivity 8.3. The Gustatory Apparatus 8.4. Gustatory Sampling and Sensitivity 8.5. The Common Chemical Sense 9. Sensory Input to the Central Nervous System in Elasmobranchs 9.1. Neuroanatomy 9.2. Assessing the Relative Importance of Each Sensory Modality 9.3. Encephalization 9.4. Neuroecology 10. Perspectives on Future Directions Elasmobranchs occupy a diversity of ecological niches with each species adapted to a complex set of environmental conditions. These conditions can be defined as a web of environmental signals, which are detected by a battery of senses, that have enabled these apex predators to survive relatively unchanged for over 400 million years. Signals such as light, odors, electric and magnetic fields, sound, and hydrodynamic disturbances all form a sensoryscape that each species can detect and process. However, the biophysical signals and their propagation within each ecological niche differ and place selection pressures on the ability of a specific sensory modality to detect and respond to prey, predator, and mate. This review investigates how elasmobranchs sense their environment by examining a diversity of species from different habitats, the ways in which they sample their sensoryscape, the sensitivity of each of their senses, and the effect this has on their behavior. The relative importance of each sensory modality is also investigated and how sensory input to the central nervous system can be assessed and used as a predictor of behavior. Although there is still a great deal we do not understand about elasmobranch sensory systems, the anatomical, physiological, molecular, and bioimaging approaches currently being used are enabling us to ask complex behavioral questions of these impressive predators.

Electrosensory-driven feeding behaviours of the Port Jackson shark (Heterodontus portusjacksoni) and western shovelnose ray (Aptychotrema vincentiana)

Elasmobranch fishes (sharks, skates and rays) possess a highly sensitive electrosensory system that enables them to detect weak electric fields, such as those produced by potential prey organisms. Despite several comparative anatomical studies, the functional significance of interspecific variation in electrosensory system morphology remains poorly understood. In the present study, we directly tested the electrosensitivity of two benthic elasmobranchs that share a similar habitat and feed on similarly sized prey items (Port Jackson sharks, Heterodontus portusjacksoni, and western shovelnose rays, Aptychotrema vincentiana), but differ significantly in their electrosensory system morphology. Aptychotrema vincentiana possesses almost five times the number of electrosensory pores of H. portusjacksoni (~1190 and ~239 respectively), yet both species are able to initiate feeding responses to electric-field gradients below 1 nV cm–1, similar to other elasmobranch species tested. However, A. vincentiana showed a greater ability to resolve the specific location of electrosensory stimuli, because H. portusjacksoni would more often overshoot the target and have to turn around to locate it. These results suggested that differences in abundance and distribution of electrosensory pores have little to no effect on the absolute electrical sensitivity in elasmobranchs, and instead, may reflect species-specific differences in the spatial resolution and directionality of electroreception.

Visual specializations in five sympatric species of stingrays from the family dasyatidae

The eyes of five ray species (Taeniura lymma, Neotrygon kuhlii, Pastinachus atrus, Himantura uarnak and Urogymnus asperrimus) from the same taxonomic family (Dasyatidae) and the same geographic region (Ningaloo Reef, Western Australia) were studied to identify differences in retinal specializations that may reflect niche specialization. The topographic distributions of photoreceptors (rods and all cones) and ganglion cells were assessed and used to identify localized peaks in cell densities that indicate specializations for acute vision. These data were also used to calculate summation ratios of photoreceptors to ganglion cells in each species and estimate the anatomical spatial resolving power of the eye. Subtle differences in the distribution of retinal neurons appear to be related to the ecology of these closely related species of stingrays. The main specialization in the retinal cell density distribution is the dorsal streak that allows these animals to scan the substrate for potential prey. The blue-spotted fantail ray, T. lymma, showed the highest peak density of rods (86,700 rods mm-2) suggesting a specialization for scotopic vision. The highest peak density of cones (9,970 cones mm-2) was found in H. uarnak, and the highest peak density of ganglion cells (4,500 cells mm-2) was found in P. atrus. The proportion of rods to cones in the dorsal streak was higher in the two smaller species (12.5-14:1 in T. lymma and N. kuhlii) than the larger stingrays (6-8:1 in P. atrus, H. uarnak and U. asperrimus). Visual specializations in different sympatric species are subtle but may reflect specializations to specific ecological niches.