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1. Dissertation

J
Jessica Sherlock

This document summarizes Jessica Sherlock's dissertation on the sensory organs and feeding ecology of elasmobranchs. It begins by acknowledging those who supported her research and writing. The introduction then discusses the four categories of senses in elasmobranchs - photoreception, chemoreception, mechanoreception, and electroreception. It describes the anatomy and function of each sense, and how the senses work together to locate and capture prey. The document aims to analyze how different species' sensory abilities relate to their habitat and diet. It will review literature on each sense and compare sensory capabilities across species. Understanding these links can help develop deterrents to reduce shark bycatch.

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1 OSX-3000 osu270 Sensory Organs and Feeding Ecology in Elasmobranchs Jessica Sherlock School of Ocean Sciences, Bangor University, Menai Bridge, Anglesey, LL59 5AB, UK.
2 OSX-3000 osu270 Acknowledgements I would like to thank my project supervisor Dr Ian McCarthy for his support, guidance and encouragement throughout the process of researching and writing this dissertation. I would also like to thank my tutor Dr Martin Skov for his continuous guidance and belief in me throughout all my time with the School of Ocean Sciences, Bangor University. To my housemates and fellow students, thank you for the late night chats and for answering my multitude of silly questions. Thank you to Phillip Wallace and Beth Saunders for their emotional support and proof reading parts of this paper. My parents and brother, I am forever grateful for your support and love through all my university years. I couldn’t have done it without you.
3 OSX-3000 osu270 Sensory Organs and Feeding Ecology in Elasmobranchs Abstract Elasmobranchs have evolved a battery of senses over millennia used primarily to hunt prey, including a unique sixth sense that enables them to detect electricity. Each of these senses is used in the locating, tracking, capturing or consuming of prey. They can be grouped into four categories; Photoreception, Chemoreception, Mechanoreception & Electroreception. All of these senses have adapted to species ecology, be it habitat or feeding ecology. Species in different habitats, with different dietary preferences, may favor one sensory system over another. Whilst there is limited amounts of quantitative data covering this topic some conclusions have been drawn. Pelagic species which feed on fast moving prey tend to rely more upon their chemosensory and photosensory systems. This allows them to locate and track their prey quicker in the featureless pelagic environment. Species which feed primarily on the benthos are more dependent on electroreception. Their increased pore densities aid the elasmobranch in scanning the seabed for electrical signals given off by hidden or camouflaged prey. A compensatory effect can also be observed between some of the senses. For example, in environments where there is little light or visual stimuli, other sensory systems will become more developed to fill the role of locating prey. It is important to understand the link between sensory ability and species ecology as it can aid with the creation of man-made deterrents. These deterrents can be put onto fish gear to reduce the number of sharks killed as bycatch. Current data sets focus primarily on the visual and electrical capabilities of shark species. Increased research effort into all senses, across the whole elasmobranch family, is urgently needed in order to expand our knowledge of all the interspecies adaptations and to aid the protection of endangered elasmobranch species. Keywords: Elasmobranchs ● feeding ecology ● sensory systems ● photoreception ● chemoreception ● mechanoreception ● electroreception
4 OSX-3000 osu270 Contents Title ........................................................................................................................................1 Abstract ..................................................................................................................................2 Acknowledgements ................................................................................................................3 Contents..................................................................................................................................4 Figures and Tables .................................................................................................................5 1. Introduction ........................................................................................................................6 1.1. Sensory organs in elasmobranchs .......................................................................6 1.1.1. Photoreception......................................................................................9 1.1.2. Chemoreception .................................................................................11 1.1.3. Mechanoreception ..............................................................................13 1.1.4. Electroreception .................................................................................15 1.2. Feeding Ecology................................................................................................16 1.3. Aims of study ....................................................................................................17 2. Methods............................................................................................................................18 2.1. Literature review ...............................................................................................18 2.2. Data collection...................................................................................................19 3. Results & Analysis ..........................................................................................................20 3.1. Photoreception...................................................................................................20 3.2. Chemoreception ................................................................................................21 3.3. Electroreception ................................................................................................23 3.4. Comparative studies ..........................................................................................25 4. Discussion ........................................................................................................................28 4.1. Study Limitations ..............................................................................................28 4.2. Photoreception...................................................................................................28 4.3. Chemoreception ................................................................................................30 4.4. Mechanoreception .............................................................................................32 4.5. Electroreception ................................................................................................34 5. Conclusion........................................................................................................................36 6. References ........................................................................................................................37 6.1. Web Resources..................................................................................................40
5 OSX-3000 osu270 Figures and Tables Figures Figure 1. Sensory ranges of elasmobranchs...........................................................................7 Figure 2. Prey-omitted signal fields .......................................................................................8 Figure 3. Methods used in elasmobranchs to protect the eye...............................................10 Figure 4. Anatomy of the lateral line system in elasmobranchs ..........................................14 Figure 5. Use of elasmobranch electroreception for navigation ..........................................16 Figure 6. Average eye diameter, grouped by species...........................................................20 Figure 7. Average eye diameter, grouped by habitat ...........................................................21 Figure 8. Average lamellae count, grouped by habitat ........................................................22 Figure 9. Average lamellae count, grouped by dietary preference ......................................22 Figure 10. Average pore count, grouped by habitat.............................................................23 Figure 11. Average pore count, grouped by species ............................................................24 Figure 12. Average pore count and eye diameter, grouped by species................................26 Figure 13. Average pore count and eye diameter, grouped by habitat.................................27 Figure 14. Average pore count and eye diameter, grouped by dietary preference ..............27 Tables Table 1. Key terms used in the primary literature search.....................................................18
6 OSX-3000 osu270 1. Introduction There are over 1100 extant species of sharks, rays and skates belonging to the subclass Elasmobranchii within the class Chondrichthyes, or the cartilaginous fishes (Carrier et al., 2012). Fossil records date elasmobranchs back around 400 million years to in the early Devonian period. Since then, elasmobranchs have evolved a battery of specialised senses in order to detect and localise their prey (Huter et al., 2004). Their six senses, along with large brains, are probably the most adapted and diverse of any known predator (Emde et al., 2004). This variety of senses provides elasmobranchs with the ability to detect and consume prey even when one or more of their senses are compromised, such as at night (Klimley & Oerding, 2013). Elasmobranchs, in particular sharks, play a vital role within the marine ecosystem. They help keep fish stocks healthy as they target old and sick fish which benefits not only the biodiversity of the ecosystem but also the fishing industry (Sandin et al., 2008). The main threat elasmobranch populations face is overfishing, particularly as bycatch. In the past 50 years shark catch has increased by 200%, causing a 90% decline in global shark populations (Clarke, 2006; Myers et al, 2007). Loss of this apex predator can cause a shift within the marine food web, creating an inverted trophic pyramid. The removal of any top predator within a food web can cause the number of secondary predators to increase, due to lack of competition (Duffy, 2003). In reef habitats the loss of apex shark species has led to an increase in the number of snappers and jacks. These species feed more frequently and in larger numbers and are therefore reducing the abundance of lower trophic level reef fish (Sandin et al., 2008). Researching the sensory systems and organs sharks use can provide a greater understanding of how they feed. This knowledge can aid the development of deterrents which keep them away from fishing lines and nets therefore reducing bycatch numbers (Hart & Collin, 2015). 1.1. Sensory organs in elasmobranchs Sensory performance can be classed in two ways; sensitivity and acuity. Sensitivity is measured by the minimum stimulus detectable by the system. The acuity of the system is described by the ability to discriminate stimulus characteristics, such as location and type (Hueter et al., 2004). This allows for quantification and comparison of different elasmobranch senses, determining ‘how good’ a sense is (Carrier et al., 2012).
7 OSX-3000 osu270 Elasmobranchs possess a highly acute array of sensory systems; vision, smell, taste, hearing, touch and a unique electrical sense also known as the ampullae of Lorenzini (Emde et al., 2004). Often the senses of elasmobranchs are investigated individually. It is therefore very difficult to accurately understand the exact order in which each sense is prioritised and used (Springer & Gold, 1989). However the anatomy of each of the sensory systems does give some indication as to their range, and therefore order of use. Figure 1 provides a visual representation of each of the shark’s six senses and the order in which they may be used when locating and consuming prey. Low frequency sounds are known to travel great distances underwater (Bright, 2002). The elasmobranch auditory system is highly adapted to these frequencies and is likely to be the first sense to pick up a signal. It is believed that sharks can detect sounds from over a 1 mile away (1.6km), but they are only attracted to these sounds if they are irregular and of a low frequency (Emde et al., 2004; Springer & Gold, 1989; Carrier et al., 2012). The next sense to pick up a signal is thought to be the olfactory system, or sense of smell. Dependant on water currents, elasmobranchs can detect odours at distances up to 500m (Figure 1) (Emde et al., 2004). They will then follow this scent trail, testing the concentration of the scent as they swim. At around 100m pressure sensors in the shark’s lateral line system, on either side of its body, pick up movements in the water. This sense of distant touch guides the shark to a more accurate location of the signal (Carrier et al., 2012). Elasmobranch visual ability can be restricted by water turbidity and light levels. However, in clear well-lit waters elasmobranchs can spot movements at 25 to 50m (Figure 1). Once the prey is within touching distance the fifth and most unique sense starts to pick up minute electrical waves given off by the muscles of the prey (Hodgson & Mathewson, 1978). This sensory system, known as electroreception, uses tiny jelly-filled pores called the ampullae of Lorenzini to detect these signals. The final senses, taste and direct touch, are used when the shark makes direct contact with the prey. They are thought not to aid with detection of prey but with assessing if the prey item is ‘food’ or not (Klimley & Oerding., 2013). Figure 1. Ranges of sensitivity to a stimulus for each of the elasmobranch senses. Adapted from: (Shark Foundation, 2008).
8 OSX-3000 osu270 Figure 2. Visual model of signal field omitted by a prey source. The primary pathway (excluding auditory) elasmobranchs use to detect prey is through olfaction (O). The odour field (shown in blue) can extend over large distances away from the prey source. Elasmobranchs swim up this narrow field until the prey becomes visible (V, shown in red). Once the elasmobranch is within touching distance it can sense pressure changes in its lateral line system. This creates an acoustic nearfield (L, shown by the dotted line). Small electrical signals (E, shown in orange) given off by the muscles of the prey are detected right before contact (T). Water direction is shown by the white arrow. Credit: (Gardiner et al., 2014). To date there has been one multidisciplinary approach to elasmobranch senses by Gardiner et al. (2014). This study was undertaken by blocking out all of the senses of three shark species, with different sensory anatomies and behavioural ecology, and observing their feeding sequences as each individual sense was ‘turned back on’ (Gardiner et al., 2014). It was discovered that even with one or more of their senses restricted the shark were still capable of detecting and consuming their prey. This study also supported previous evidence and theories as to the order in which certain shark species use their senses and how the sensory systems interact. Gardiner then created a physical model of prey signal fields, similar to that of Figure 1. This revised figure not only gives an indication of the range of each of the senses but also the field in which they are detected (Figure 2). It was noted that the auditory system was excluded from this study, however the reason for this exclusion was not explained. It is possible that it was dismissed due to lack of data and difficulty recording this sense. As mentioned previously the elasmobranch auditory system can detect sounds from over a mile away and this is difficult to recreate in a laboratory setting.
9 OSX-3000 osu270 For this paper, the six senses of elasmobranchs (sight, smell, hearing, touch, taste and electroreception) have been grouped in four categories; Photoreception, Chemoreception, Mechanoreception and Electroreception. The rest of this introduction will discuss each sensory category in terms of anatomy and performance. Feeding ecology will also be defined and links between the senses and ecology discussed. 1.1.1. Photoreception Photoreception in elasmobranchs covers the sense of sight. Studies into the visual system of elasmobranchs date back 200 years (Gruber & Cohen, 1978). After a study by Schultze (1866) produced a detailed account of the retinal structure, interest in elasmobranch visual systems spiked (Emde et al., 2004). Before this time the visual capabilities of elasmobranchs were considered to be relatively poor compared with the other sensory systems (Hueter & Gilbert, 1990). By the mid-20th century the visual system in sharks and rays had become very well documented and investigated. Since then, vision has been rarely studied independently and is now often paired with investigations of brain sizes (Gruber & Cohen, 1978). Visual stimuli are detected at a relatively close range (15-25m). This sensory system is primarily used for hunting, however some species are known to successfully feed even when their vision is restricted (Sivak, 1990). Great white sharks (Carcharodon carcharias) have been known to lift their heads out of the water in order to scope out the topside surroundings and track their primary prey species, seals and sea lions, belonging to the family Pinnipedia (Carrier et al., 2012). However, it is not known how well adapted elasmobranch eyes are to above-water vision. Elasmobranch eyes are more complex and well developed than teleost eyes, however they share the same basic anatomy (Carrier et al., 2012). The eyes focus through the use of the rectus muscle which pulls the lens closer to or further away from the retina. This process, similar to that of a focusing camera lens, is different from higher terrestrial vertebrates in which the lens is instead distorted to focus light entering the eye from different distances (Gilbert, 1963). The direction the eyes face is again controlled by the rectus muscle as well as the oblique muscle (Springer & Gold, 1989). Some elasmobranch species have evolved new ways in which to sense light levels. A thin area of skin on the top of their head, which leads directly to the pineal gland in the brain, can detect light. This could be used during diurnal vertical migrations such and those undertaken by megamouth sharks (Megachasma pelagios).
10 OSX-3000 osu270 Figure 3. The nictitating membrane of a blue shark (Prionace glauca) covering half of the eyeball (A). This toughened layer can cover the eye prior to a feeding event where prey may inflict damage when trying to protect itself. Species that do not possess this membrane, such as the Great White Shark (Carcharodon carcharias), can roll their eyes backwards into their sockets to protect them (B). Taken from: (The Liquid Earth, 2014; Sharks Gallery, 2015). A B However this ‘window’ of skin does not possess a lens, unlike the eyes, and so the light cannot be focused in order to determine shape (Springer & Gold, 1989). Unlike teleost species elasmobranchs do have eyelids, however these lids are fixed and cannot cover the eye to protect it (Emde et al., 2004). Elasmobranchs therefore have evolved new ways in which to protect their eyes from the sharp claws or spines of their prey when feeding. Most shark species have developed specialised eyelids, known as the nictitating membrane, to cover the eyeball (Figure 3.A). Other species, such as C. carcharias, which do not possess this layer are known to roll their eyes back into the sockets, exposing the hardened pad on the back of the eye in order to protect the pupils (Figure 3.B) (Klimley & Oerding, 2013). Elasmobranch eyes, like human eyes, do possess contracting pupils. For shallow water species this enables them to control the amount of light entering their eyes by dilating or contracting the pupils (Sivak, 1990). Requiem sharks do this laterally giving them a ‘cat eye’ appearance. Others species, primarily skates and rays, contract their pupils into a ‘U’ shape which creates double vision. They use this to determine distance (Springer & Gold, 1989). Other species have a ragged flap which slides over the pupil reducing the amount of light entering the pupil. Again, this creates double vision and is used to aid depth perception (Sivak, 1990). Light travels slower in water than air and so most elasmobranch species have adapted to low light conditions (Klimley et al., 2013). Their excellent vision in these conditions is primarily
11 OSX-3000 osu270 due to the structure of the eye. The tapetum lucidum, a layer of mirrored crystals, lies behind the retina amplifying the strength of the image. However, the process of amplifying the light reduces the acuity of the image but increases the sensitivity of the system to a stimulus (Carrier et al., 2012; Heath, 1990). Pigments in the photoreceptors of the eye also aid with vision in low light conditions. The red wavelengths within the visible light spectrum are absorbed first within the water column and the green wavelengths absorbed last. This leaves the ocean with a dim, blue-green colour (Klimley et al., 2013). The pigments within elasmobranch eyes are most sensitive to this low-level blue-green light. Current studies on elasmobranch vision are focusing on the ability of colour vision. Around 20 species of shark have been found to have duplex retinas meaning they possess both rod and cone photoreceptors (Springer & Gold, 1989). Theoretically this means that these species should be able to see in colour. Only two species of shark, the sixgill (Hexanchus griseus) and bigeye thresher (Alopias superciliosus), are known to have only rod photoreceptors and should therefore lack colour vision (Springer & Gold, 1989). 1.1.2. Chemoreception Chemoreception in elasmobranchs can be divided into two categories; olfaction and taste. Like teleost fish, elasmobranchs use olfactory system to detect odours within the water flow. It has often been described as the most important sense elasmobranchs use to detect prey as over two thirds of their brain mass is dedicated to smell (Carrier et al., 2012). However, male elasmobranchs also use olfaction to detect female sex pheromones and find a mate (Hodgson & Mathewson, 1978). Interest in this system spiked during World War II in an effort to create preventative shark attack equipment for military personnel (Carrier et al., 2012). The olfactory system is well known and documented for shark species, unlike that of rays and chimeras (Meredith & Kajiura, 2010). Sharks have a pair of nostril-like holes, or nares, under the leading edge of the snout. Each of the nares is divided into two openings by a nasal flap. Water is guided into the incurrent nare opening and is passed over a series of skin folds, the olfactory lamellae, before passing into the olfactory sac. It then exits through the excurrent nare opening on the other side of the nasal flap (Springer & Gold, 1989). The olfactory lamellae increase the probability of a chemical signal being detected as they provide more surface area. Chemical odours passing over the lamellae stimulate neuro-sensory cells which
12 OSX-3000 osu270 send a signal to the brain. This is also known as the chemosensory function (Meredith & Kajiura, 2010). Elasmobranch olfaction is very developed. Contrary to media speculation, sharks cannot detect a single drop of blood in the ocean from miles away. However, some species are able to detect fish extracts in concentrations lower than 1 part in 10 billion (Carrier et al., 2012). Different species are attracted to different chemical signals dependant on their preferred diet (Schluessel et al., 2008). White sharks (C. carcharias) are more sensitive to blood in the water whereas lemon and nurse sharks (Negaprion brevirostris, Ginglymostoma cirratum) are attracted to amino acids and amines from the body fluids of their prey (Schluessel et al., 2008). Once an odour is detected the elasmobranch will swim through the scent trail in an ‘S’ shape pattern, swinging its head from side to side. This enables the snout to pass through the trail, assisting it with determining the direction of the odour. More sedentary species are able to pump water over the nares whilst resting on the sea floor until a scent trail is detected (Klimley & Oerding, 2013). Chemoreception also covers the sense of taste in elasmobranchs. To date there has been very little published research on this sensory system and its relation to feeding and ecology (Emde et al., 2004). However the anatomy and physiology of the system has been described. Elasmobranchs have small pits in the lining of the mouth and throat which contain rod-shaped gustatory sensory cells (Carrier et al., 2012). Once an object is bitten it releases dissolved chemicals. These chemicals attach to the gustatory cells and pass a signal to the brain which tells the shark if the object is consumable or not (Klimley & Oerding, 2013). This can be linked to the bite and release behaviour observed in C. carcharias. In attacks on humans it has repeatedly been noted that after an initial bite, the shark swims away. It is theorised that the taste of that first bite is used to determine if the prey item was the high fat mammal they were expecting. If it is not, they release the item as they do not want to waste time and energy processing and digesting the meal (Hodgson & Mathewson, 1978). It is thought that the taste organs are not as highly adapted as the other sensory systems as they do not play a role in locating prey. Exceptions to this are the many species with nasal barbells like the nurse shark (G. cirratum) and mandarin dogfish (Cirrhigaleus barbifer). These barbells could be used to rake through and taste the sediment in search of food (Springer & Gold, 1989). However, these adaptations could be organs used for the sense of touch.
13 OSX-3000 osu270 1.1.3. Mechanoreception The term mechanoreception is used to cover the senses hearing and touch, including the lateral line system. The auditory system in elasmobranchs is used to detect prey, competitors and potential mates (Corwin, 1978). Sharks and rays are not known to make noise, so theoretically their auditory systems have been shaped by the ambient noises of their habitats (Carrier et al., 2012). Numerous studies have been conducted on elasmobranch hearing (Myrberg, 2001; Popper & Fay, 1977; Wisby et al., 1964). These studies however focus primarily on the anatomy of the system and give little insight into the physiology and relation to the ecology of the animal. Sound travels roughly four times faster in water than air (Wisby et al., 1964). This has allowed hearing to become the first sense elasmobranchs use when hunting. Behavioural evidence suggests that sharks can detect underwater frequencies of up to 1000Hz (Popper & Fay, 1977). However, they are most sensitive to irregular, low frequency vibrations around 40Hz, and are able to detect these over large distances (Springer & Gold, 1989). This type of frequency is similar to that of injured prey or large shoals of fish (Emde et al., 2004). Nevertheless, there is little evidence to suggest they are more sensitive to these frequencies than other fish species, especially those with swim bladder adaptations (Carrier et al., 2012). The ears of elasmobranchs are completely internal, embedded within the frontal skull. These inner ears are made up of a series of channels and sacs known as the membranous labyrinth. In sharks this system is filled with sea water which enters through the endolymphatic ducts. A second layer of fluid filled canals surrounds the membranous labyrinth, protecting and supporting it (Myrberg, 2001). The ears of elasmobranchs, like human ears, are responsible for maintaining balance and equilibrium. The sacculus, a large chamber found within the membranous labyrinth, is lined with otoliths and sensory hair cells. These are responsible for registering any imbalance which then sends a signal to the sharks brain, allowing it to correct itself (Carrier et al., 2012). This is vital for open ocean pelagic species where there are little to no visual cues which can tell the shark which direction is ‘up’. The sense of touch can be split into two subcategories; actual touch and distance touch, also known as the lateral line system (Carrier et al., 2012). Elasmobranchs use actual touch, or direct contact, in the same way they use taste. This sense has no direct effect on detecting prey but rather assessing if the item is edible or not. Many sharks will nose an object before taking
14 OSX-3000 osu270 an exploratory bite in order to determine if the item is worth the energy needed to digest it (Springer & Gold, 1989). Distance touch is experienced through the lateral line system. This system of fluid filled canals runs along the sides of the body in sharks, from the head to the upper lode of the tail (Bleckmann et al., 1989). Two extra canals, the infraorbital and supraorbital, are located exclusively on the head. The placement of the lateral line system in batoids (rays and skates) varies widely, dependant on habitat and feeding ecology (Jordan, 2008). The canals contain small, hair- like receptors which send a signal to the brain whenever a wave of water, entering through an external pore, passes over them (Figure 4). These waves are created by changes in pressure as an animal moves though the water. Erratic vibrations can indicate an injured or sick animal and guide the elasmobranch to the prey item (Bright, 2002). Vibrations are also created by the sharks own movements. The water it displaces as it swims creates ripples which bounce off nearby objects and return to the shark. This allows the shark to create a vibration echo map, similar to sonar mapping, of its surroundings (Klimley & Oerding, 2013). Some shark species also possess rows of pores along the gills and pectoral fins. These pores, also known as pit organs, contain neuromast-like cells that allow the shark to detect changes in temperature which helps migratory species (Maruska, 2001). Before 1980 it was believed that the lateral line system in elasmobranchs was also responsible for hearing (Popper & Fay, 1977). Since then, studies in the early 2000s disproved this but the principle still remains. Considering that sound waves are essentially vibrations, which the lateral line system is known to detect, it is not unreasonable to assume they could use this system to hear (Bleckmann et al., 1989; Maruska, 2001). Figure 4. The elasmobranch lateral line system: interconnected, fluid-filled, canals running from head to tail in shark species. Tiny waves of water enter the system through the external surface pore and pass over the hair-like receptors inside the canal. Taken from: (Bright, 2002).
15 OSX-3000 osu270 1.1.4. Electroreception Elasmobranchs have developed a specialised sixth sense called electroreception. Evolved from the pores in the lateral line system, the jelly-filled pores known as the ampullae of Lorenzini can detect minute electrical signals in the water. These signals are given off by muscle movements, such as heartbeats, of the prey (Kalmijn, 1971). This system was first described by Lorenzini in 1678, but its physiological function remained unknown for three centuries (Carrier et al., 2012). Originally it was thought that the ampullae were a type of mechanoreceptor until studies by Murray (1960) and Dijkgraaf & Kalmijn (1962) investigated the electrosensitivity of the system. The electrosensory system consists of several hundred jelly-filled pores, concentrated primarily around the snout, connected by cylindrical canals. The ‘jelly’ acts as a conductor and picks up any fluctuations in the electrical field of the nearby habitat. This signal is then passed onto the sensory cells which line each pore. A sensory nerve at the base of each pore then transports this information to the brain, telling the shark the intensity and direction of the signal (Springer & Gold, 1989). This system is so sensitive that it can pick up voltage fluctuations as low as 5nV/cm (nano-Volts per centimetre) (Kalmijn, 1982). The ampullae can also pick up changes in pressure and temperature, however they are not as sensitive to these signals as the lateral line system (Brown, 2003). The amount of pores each elasmobranch species has depends on their habitat and feeding ecology. More active species are known to have around 2,000 pores whereas more sedate species can have only a few hundred (Murray, 1962). The use of this sensory system is also dependant on each species. Hammerheads (genus Sphyrna) are thought to use their ampullae like a metal detector, sweeping their heads from side to side over the seafloor in search of prey buried in the sediment (Kajiura, 2001). Other species use electroreception, along with the lateral line system, to guide their mouths to the prey item in the last few moments of feeding. Gardiner (et al., 2014) suggested that in these moments, electroreception takes over from sight and smell as the primary sense. This is particularly useful for species that roll their eyes back into the sockets to protect them, leaving them blind just before contact with their prey (Figure 3). Instead they use their ampullae to guide them by following the electrical waves given off by the muscles of their prey as it tries to escape (Emde et al., 2004).
16 OSX-3000 osu270 It is also theorised that this bioelectrical system may aid geographical navigation (Molteno & Kennedy 2009). Many teleost species use magnetite in their bodies to sense the polarization of the Earth’s magnetic fields (Kirschvink et al., 2001). Elasmobranchs however do not possess magnetite. It is thought they use a combination of the positive ions in saline water and the Earth’s magnetic fields to induce electric fields, which it can detect with its ampullae (Figure 5) (Molteno & Kennedy 2009). This ‘magnetoreception’ can help pelagic species migrate over large distances in the open ocean. These species have been found to have a more even distribution of ampullae than more benthic species in order to detect the induced magnetic field (Carrier et al., 2012). 1.2. Feeding Ecology Feeding ecology is defined as what organisms feed upon (their feeding habits), how the food is acquired (foraging habits) and where the food is found (foraging habitat) (Gerking, 2014). It is often difficult to classify elasmobranch species into individual ecological groups as they move between different niches and depths (Carrier et al., 2012). Sharks, in particular, inhabit a wide variety of ecological niches; from the deep ocean to shallow coastal waters, with some species even frequenting freshwater habitats (Emde et al., 2004). In each of these habitats elasmobranchs have adapted their sensory biology to feed upon their preferred prey item. Some species are plankton eating filter feeders whilst others prefer to feed on invertebrates on the benthos. A few are even at the top of the food chain, preying upon large high-fat mammals (Emde et al., 2004). Each of these prey types has led to elasmobranchs adapting their sensory biology, over millennia, to ensure successful capture of prey. In some cases the size or number of organs changes, whilst in other species a sense may become essentially useless. However each adaptation has allowed elasmobranchs to become one of, if not the most successful species in the animal kingdom (Gerking, 2014). Figure 5. Use of elasmobranch electroreception for navigation. Electric current is induced as the shark swims through the horizontal component of the Earth’s magnetic field. The ampullae of Lorenzini detect this current and supply navigational information to the brain. Credit: (Carrier et al., 2012).
17 OSX-3000 osu270 1.3. Aims of study Often studies of elasmobranch senses and ecology focus on one sense at a time. There are only a handful of studies which address all elasmobranch senses in relation to their feeding ecology and habitat. The aim of this paper is to discuss the battery of senses elasmobranchs possess, focusing primarily on shark species, and look for any relationships between these senses and different feeding ecologies. Habitat may be used during analysis as it can correlate to dietary preference. This review aims to address the hypotheses: 1) There is a relationship between preferred food type and the predominant sensory organ used in elasmobranchs 2) Elasmobranchs in different habitats favour different sensory organs. The null hypothesis of this study addresses that there is no link between the predominant sense organs used and elasmobranch feeding ecology.
18 OSX-3000 osu270 2. Methods 2.1. Literature review Web of Science and Google Scholar were used to conduct a thorough literature search of scientific papers on the subject of elasmobranch sensory organs and feeding ecology. Table 1 presents the key terms searched, and all of their differentiations, either individually or in conjunction with each other. Detailed notes were made on any studies which focused on the size/number of or dominance of any of the sensory organs. Papers were also taken from the reference lists of relevant studies. Web of Science was used as a secondary check during the literature search, due to limitations as literature was only dated as far back as 1970. Also this platform, unlike Google Scholar, does not search grey literature. Bangor University Scientific library was used to gain access to relevant information in textbooks. These peer reviewed texts gave background knowledge on the anatomy and physiology of each of the sensory systems. Search term Differentiations & related terms Elasmobranch(s) Elasmobranchii, shark(s), ray(s). Sensory organs Sensory, organ(s), sense(s), organ size, dominant, distribution, number. Feeding ecology Ecology, niche(s), feeding apparatus, prey. Photoreception Vision, eye(s), pupil, retina, sight, photoreceptors, pigments. Chemoreception Smell, olfaction, olfactory, taste, nasal opening, olfactory lamellae. Mechanoreception Movement, pressure, lateral line, touch, hearing, sound, ear(s), actual touch, distant touch. Electroreception Magnetoreception, ampullae of Lorenzini, ampullae, pores, electric, electricity, bioelectric, navigation. Table 1. Key terms used in primary searches on Web of Science and Google Scholar. Differentiations of each search term are also shown.
19 OSX-3000 osu270 2.2. Data collection The data for this paper was collected from a variety of scientifically reviewed papers. Studies which investigated a quantitative aspect of one or more senses provided the baseline data set. Several sources were compiled in order to create a new data set for each sensory category. Data was extracted from existing figures in literature using the tool PlotDigitizer (2015). The raw data was then used to compile summary statistics, with standard error, and figures. No restrictions were set when collecting data due to the lack of literature and studies available. This data was used in the analysis of the sensory information with comparisons to elasmobranch feeding and the analysis of their known sensory capabilities. Species information, such as habitat and diet, was collected primarily from FishBase.org and then cross checked against two key papers (FishBase, 2016; Kajiura et al., 2010; Hueter & Cohen, 1991). Diet information was classified by the predominant food group each species consumes, e.g. the food group has to make up 50% or more of the overall diet. Species which did not have a clear predominant food group (>50%) were classified as ‘Generalists’, however their diets mainly consisted of a mixture of teleosts, crustaceans, cephalopods and scavenged meals. For photoreception data, the eye diameter of 29 shark species was collected from three independent studies and averaged, with standard error (±1SE). The depth ranges of each species were obtained from FishBase and were used to determine the habitat classification, based on similar classification system used by Kajiura (et al., 2010). Limited quantitative information was available for chemoreception meaning only one study was used for data collection (Schluessel et al., 2008). The number of lamellae was plotted against two habitat groups as well as the predominant food group, again taken from FishBase. Two large data sets, covering 42 species, were used for the electroreception results. The numbers of pores for each species was plotted against its predominant habitat. This data was then compared against eye diameter and then food group. The data collected during the literature search was used to compare each sensory system with either habitat or predominant food group. This can be then used to discuss how feeding ecology can affect the senses of elasmobranchs.
20 OSX-3000 osu270 3. Results & Analysis 3.1. Photoreception The average eye diameter of 29 shark species found that deepwater species had larger eyes, as a percentage of their total body length, than pelagic species (Figure 6). No difference was observed between the two pelagic groups. Relevant studies also found that deepwater species had variations in other aspects of their eye anatomy, such as pupil size and shape, lens diameter and densities of photoreceptors (Kajiura et al., 2010). This data was then grouped and averaged for each habitat classification (Figure 7). Standard error analysis supported the outcome that there was no significant difference between eye size for species classified as coastal benthic, coastal pelagic and oceanic pelagic. Deepwater species were classified as living predominantly below 1000m, with the deepest species in this study being the velvet dogfish (Zameus squamulosus) found at 2200m. Figure 6. Average eye diameter (as % of total length) for each species, grouped by environmental classification. Deepwater species (open triangles) have larger eyes than sharks in other habitats, in particular pelagic species (closed circle and squares). Data taken from (Kajiura et al., 2010; Hueter & Cohen, 1991; Gilbert, 1963). Data taken from Kajiura, 2001. 0 0.5 1 1.5 2 2.5 3 3.5 4 4.5 5 Parmaturusxaniurus Heptranchiasperlo Etmopterusbaxteri Etmopteruslucifer Etmopteruspusillus Zameussquamulosus Apristurusbrunneus Squalusacanthias Ginglymostonacirrtum Triakissemifasciata Negaprionbrevirostris Carcharhinusbrevipinna Carcharhinusleucas Carcharhinuslimbatus Carcharhinusmelanopterus Carcharhinusobscurus Carcharhinusperezi Carcharhinusplumbeus Galeocerdocuvier Rhizoprionodonterraenovae Eusphyprablochii Sphynalewini Sphynamokarran Sphynatiburo Alopiaspelagicus Alopiassuperciliosus Lamnaditropis Carcharhinusfalciformis Prionaceglauca AverageEyeDiameter(%TL) Species
21 OSX-3000 osu270 0.00 0.50 1.00 1.50 2.00 2.50 3.00 3.50 4.00 Deepwater Coastal benthic Coastal pelagic Oceanic pelagic AverageEyeDiameter(%TL) Habitat 3.2. Chemoreception Counts of olfactory lamellae per rosette of 21 elasmobranch species ranged widely between two habitats, from 231 in the scalloped hammerhead shark (Sphyrna lewini) to 58 in the eastern shovelnose ray (Aptychotrema rostrata). On average, pelagic species had higher lamellae counts than benthic species, supported by statistical analysis (p = 0.0082) (Figure 8). However, when the species were grouped by their food preference a Tukey test showed there were no significant differences between the groups and numbers of lamellae (0.289 ≤ p ≤ 1.00) (Figure 9). The effect differences between the food groups suggest that mollusc eating elasmobranch could have higher counts of lamellae whilst crustacean consuming have the least. A greater sample size would be needed in order to test this to look for a significant result. Schluessel (et al., 2008) sampled the number of lamellae between males and females of three different species as a control study. It was found there was no significant difference between the sexes (Schluessel et al., 2008). Figure 7. Average eye diameter (as % of total length) for each habitat classification (±1SE). Deepwater species have larger eyes than sharks in all other habitats. Data taken from (Kajiura et al., 2010; Hueter & Cohen, 1991; Gilbert, 1963). Data taken from Kajiura, 2001.
22 OSX-3000 osu270 0 10 20 30 40 50 60 70 80 Benthic Pelagic Numberoflamellae Habitat Figure 9. Average number of lamellae (±1SE) per rosette for 21 elasmobranch species with six different food preferences; T = teleost, P = polychaete, C = crustacean, Ce = cephalopod, E = echinoderms, M = molluscs. No significant differences were observed between food groups (p> 0.05). 95% confidence intervals are shown by error bars. Adapted from Schluessel et al., 2008. Figure 8. Average number of lamellae (±1SE) per rosette for 9 benthic and 12 pelagic elasmobranch species. A significant difference (p=0.008) is observed between the groups with the pelagic group having a higher lamellae count. Adapted from Schluessel et al., 2008.
23 OSX-3000 osu270 0 500 1000 1500 2000 2500 Deepwater Coastal benthic Coastal pelagic Oceanic pelagic AveragePoreNumber Habitat 3.3. Electroreception Pore numbers were taken from 2 independent studies, providing an average for 42 shark species (Figure 11). This data was then grouped and averaged for each of the four habitat classifications. Deepwater species were found to have the lowest numbers of pores (average 838) (Figure 10). However they also possess the widest range of pore numbers, from 2185 on the blackbelly lanternshark (Etmopterus lucifer) to 252 on the frilled shark (Chlamydoselachus anguineus). Coastal pelagic species, found at depths above 200m, were the only group to show a statistically significant difference from the other habitats (p<0.05), and had the highest average pore count (1899) (Figure 10). Species in this habitat were also found to have a more even distribution of pores over the ventral and dorsal surfaces of the head, whereas benthic species had a greater concentration of pores on the ventral surface (Kajiura et al., 2010). Figure 10. Average pore count (±1SE) for each habitat classification. Coastal pelagic species have a higher average pore count than sharks in all other habitats. Data taken from Kajiura et al., 2010; Kalmijn, 1971.
24 OSX-3000 osu270 Figure11.Averageporecountforindividualspecies,groupedbyenvironmentalclassification.Pelagicspecies(closedcircleandsquares)tendto possessagreaternumberofporesthanmorebenthicspecies,withcoastalpelagicspecies(closedcircle)havingthehighestnumbersofpores. DatatakenfromKajiuraetal.,2010;Kalmijn,1971.
25 OSX-3000 osu270 3.4. Comparative studies The data sets of two senses, photoreception and electroreception, were then combined in order to look for any patterns. Questions behind this section of results focused on if there was a relationship between eye size and average number of pores. Do deepwater species have less ampullae of Lorenzini as their eye sizes were expected to be larger? Or is there no relationship? Does one sense compensate for another in different habitats? These data sets were then combined with habitat classification and food grouping. Firstly, the average eye diameter of 26 shark species were compared against their average pore counts (Figure 12). Deepwater and benthic species (the first six species in Figure 12) generally had larger eye diameters and lower pore counts compared to the other species. All the species belonging to the family (Carcharhinus) had similar counts of both eye size and pore count across the family. The data was then grouped into 6 habitat categories (Figure 13). Again, this supported the theory that deepwater species have a significant difference between eye size and pore count, as shown by the effect size and error bars in Figure 13. Coastal pelagic and Oceanic Pelagic groups show a reversed pattern, where they have larger eyes and lower pore counts in comparison to the other habitat groups. Relationships were again observed when the data was regrouped by predominant food type (Figure 14). Species which preferred to feed on teleost and crustacean prey types were observed to favour eye sight over electroreception compared to species consuming cephalopods. There was no statistically significant difference for ‘generalist species’ between eye size and pore count ratios.
26 OSX-3000 osu270 0.00 0.50 1.00 1.50 2.00 2.50 3.00 3.50 4.00 4.50 5.00 0 500 1000 1500 2000 2500 3000 3500 Etmopterusbaxteri Heptranchiasperlo Parmaturusxaniurus Apristurusbrunneus Triakissemifasciata Rhizoprionodonterranovae Ginglymostonacirrtum Negaprionbrevirostris Galocerdocuvier Squalusacanthias Zameussquamulosus Eusphyprablochii Etmopteruslucifer Carcharhinusplumbeus Carcharhinusmelanopterus Carcharhinusbrevipinna Carcharhinusfalciformis Carcharhinusleucas Carcharhinuslimbatus Carcharhinusobscurus Sphynatiburo Prionaceglauca Alopiassuperciliosus Alopiaspelagicus Sphynamokarran Sphynalewini AverageEyeDiameter(%TL) AveragePoreCount Species Pore Count Average Eye Diameter (%TL) Average Figure 12. Average pore count (bar) and eye diameter (line), as a % of total length, for 26 shark species. For deepwater and benthic species (the first six species) eye diameter, as a percentage, is significantly higher than pore count. These species also show the lowest pore count compared to all other species in this study. Data taken from FishBase, 2016; Kajiura et al., 2010; Kalmijn, 1971; Hueter & Cohen, 1991; Gilbert, 1963).
27 OSX-3000 osu270 0.00 0.50 1.00 1.50 2.00 2.50 3.00 3.50 4.00 4.50 5.00 Teleosts Crustaceans Cephalopod Generalist 0 500 1000 1500 2000 2500 AverageEyeDiameter(%TL) Food Group AveragePoreNumber Pore Count Average Eye Diameter (%TL) Average 0.00 0.50 1.00 1.50 2.00 2.50 3.00 3.50 4.00 4.50 0 500 1000 1500 2000 2500 Deepwater Benthic Coastal benthic Bentho pelagic Coastal pelagic Oceanic pelagic AverageEyeDiameter(%TL) AveragePoreCount Habitat Pore Count Average Eye Diameter (%TL) Average Figure 14. Average pore count (bar) and eye diameter (line), as a % of total length, for 26 shark species grouped by dietary preference (±1SE). Species which predominantly feed on crustaceans favour electroreception as they have larger pore counts than eye diameters. Species consuming cephalopods have the largest eye size across all dietary groups, however this data could be skewed due to a low sample size. Data taken from FishBase, 2016; Kajiura et al., 2010; Kalmijn, 1971; Hueter & Cohen, 1991; Gilbert, 1963). Figure 13. Average pore count (bar) and eye diameter (line), as a % of total length, for 26 shark species grouped by habitat (±1SE). Deepwater species have significantly increased eye diameters than other habitat groups but have low pore counts. Oceanic pelagic, coastal pelagic and coastal benthic groups show the reverse. Data taken from FishBase, 2016; Kajiura et al., 2010; Kalmijn, 1971; Hueter & Cohen, 1991; Gilbert, 1963).
28 OSX-3000 osu270 4. Discussion 4.1. Study Limitations The search terms used in this paper returned a limited selection of quantitative data sets investigating the effects of feeding ecology on the biology of elasmobranch sensory systems. The data that was collected was highly skewed. Very few studies investigated the mechanosensory systems of elasmobranchs, and none produced quantitative data in relation to habitat or dietary groups. Studies into the sense of taste resulted in the same lack of data. Primary literature searches were dominated by studies into vision and the electrosensory systems. A further limitation of the data sets included a lack of information on the sex and age of the species in the studies. This reduces the analytical ability of this paper. There was also an apparent skew of research between the elasmobranch subfamilies. Most of the studies focused on shark species, with only a handful including ray species. None of the studies investigated produced results for skate species. Further work could be undertaken on producing multidisciplinary studies, investigating all elasmobranch senses, across several species, each with different habitats and diets. 4.2. Photoreception For most elasmobranch species, sight is one of the most important senses used when hunting prey. Therefore it is not surprising that it is also one of the most adapted senses. The anatomy of the eye differs, primarily due to different habitats. However it is important to look into habitat adaptations as feeding ecology is not just about what organisms eat but also where they find it. One observed adaptation is the size of the eye and pupil. Deepwater elasmobranchs, found between 1000-4000m, tend to have large eyes with relatively large pupils. This increases sensitivity to light and allows for better location of prey, especially species which emit bioluminescence (Lisney & Collin, 2007). Pelagic species (0-200m), such as the oceanic whitetip (Carcharhinus longimanus), are also found to have large eyes, however the size and shape of the pupil differs. They are able to contract and dilate the muscles around the pupil, controlling the amount of light entering the eye. This is important as these species live in environments with high light levels but also extreme fluctuations of these levels (Gruber & Cohen, 1978). The featureless nature of this environment requires acute eyesight as the shark
29 OSX-3000 osu270 needs to be able to spot prey at large distances (Hueter & Cohen, 1991). Prey species also tend to be active and fast swimming, therefore vision is key for tracking their movements. Benthic species have the smallest eye sizes as a percentage of their total length. Vision is less important for these species as they have the ability to use a wider range of sensory systems. The barren nature of some benthic habitats means there are minimal visual stimuli. Most prey species in this environment bury themselves into the sediment or use camouflage (Schultze, 1866). Therefore vision is not as important as other sensory systems, such as electroreception, when hunting prey. The size of the eyes also differs between elasmobranch subfamilies. Sharks generally have larger eyes than batoids. This again relates to habitat as most ray species are benthic and electroreception plays a larger role in hunting for food in this habitat (Sivak, 1990). The dorsoventrally compressed morphology of batoid bodies has also changed the placement of the eyes. For benthic ray species, like the thornback ray family (Platyrhynidae), the eyes are placed more dorsally on the head compared to pelagic species, such as eagle rays (Myliobatidae), where the eyes are more laterally positioned. Lateral placement allows for a greater field of vision, allowing these species to detect prey in the pelagic environment (Carrier et al., 2012). As discussed previously, all elasmobranchs have evolved a new structural layer inside the eye called the tapedum lucidum. This layer of mirrored cells magnifies the amount of light entering the eye and allows elasmobranchs to see in dim conditions (Heath, 1990). To protect their eyes from rapid changes in light levels, pelagic species have evolved another aspect of their ocular anatomy. They can slide a layer of melanin filled cells, known as the melanoblasts, over the tapedum lucidum to reduce the amount of light reflected within the eye (Gruber & Cohen, 1978). Deep sea species, such as the sixgill shark (Hexanchus griseus), lack this layer and therefore any sudden changes in light conditions could blind them. This restricts these species to living and feeding in habitats with constant low light levels. However, H.griseus have been observed in shallower waters in the summer, but this is due to large algal blooms which reduce the amount of light entering the water column. This temporarily opens up a new foraging habitat for this species (Emde et al., 2004). Studies have been done on the size of the optic tectum in elasmobranchs. The optic tectum is a section of the midbrain which is responsible for the behavioural response to visual stimuli. It can therefore be assumed that species with larger tectum rely heavily on vision (Carrier et al., 2012). A study by Lisney (2004) investigated 29 elasmobranch species and found that on average sharks had larger optic tectum (as a percentage of brain mass) than batoids. Of the
30 OSX-3000 osu270 shark species in the study, the active, pelagic species had larger tectum masses than more sedentary benthic species (Lisney, 2004). This is most likely due to the fast moving nature of pelagic prey. Sedentary elasmobranchs are usually ambush predators and do not need to chase their prey. The size of the optic tectum was also observed to decrease as shark species mature (Lisney & Collin, 2007). This is thought to be due to a shift in sensory dependence in relation to changes in habitat and diet. Juvenile sharks are predominately born into shallow coastal ‘nurseries’ or mangrove environments. During their development in these habitats it is important to have sharp vision to not only catch prey but also avoid predators. As the individual grows it moves out into the open ocean where it becomes more reliant on the other sensory systems to locate food over greater distances (Lisney & Collin, 2007). The pigments within elasmobranch eyes also vary dependant on habitat. Juvenile lemon sharks (Negaprion brevirostris) are most sensitive to the green light end of the visible light spectrum. This is thought to be because they live in the mangroves until they mature, where the light filtering through the foliage leaves the water with a green tinge. This allows for sharper vision in this habitat (Hueter & Cohen, 1991). As they mature and move out into the clearer waters of offshore reefs, the pigments change and become more sensitive to blue wavelengths. As discussed earlier, the ocean gets in blue-green colour from the different absorption rates of wavelengths at different depths (Lisney, 2004). Understanding the role vision plays in the feeding strategies of sharks can be used to prevent shark attacks on humans. Previously, methods using electrical pulses and chemical deterrents have produced little success when trialled in Australia. It is now believed that visual deterrents could be more successful at preventing attacks (Hart & Collin, 2015; Thorson, 1987). It could be as simple as imitating the colour and markings of poisonous species, like the banded sea krait (Laticauda colubrina), found in that environment. This same theory can be applied when creating deterrents to keep sharks away from nets and fishing gear, hopefully reducing the amount of elasmobranchs caught as bycatch (Hart & Collin, 2015). 4.3.Chemoreception Whilst vision is a primary sense used when hunting and catching prey, it has a relatively small signal field. It can be drastically affected by weather related turbulence, light levels and turbidity. Olfaction can pick up signals from several hundred meters away, dependant on water currents.
31 OSX-3000 osu270 The anatomy of the olfactory system varies between species, primarily due to dietary preference. White sharks (Carcharodon carcharias) have the largest olfactory bulbs, relative to body weight, than any other elasmobranch species (Schluessel et al., 2008). The bulbs contain the olfactory lamellae which pick up chemical signals. Larger bulbs suggest a greater dependency on this sensory system. C.carcharias are known to travel large distances in search of whale carcasses using their highly developed olfactory system to guide them. A further reason for large bulb sizes is thought to be because of the high blood volume and strong odours of their primary prey species, pinnipeds. Comparing species with a similar diet to crustacean feeding elasmobranchs, like the lemon shark (N. brevirostris), the size difference between bulbs can be put down to diet (Meredith & Kajiura, 2010). Diet also affects the sensitivity of the system. Different species are attracted to different chemical signals. Some prefer the chemicals within the blood of their prey whilst others are more attracted to the amino acids within the body fluids of their prey (Schluessel et al., 2008). Studies have found that how well adapted the olfactory system is can also depend on habitat. For a pelagic species, such as the oceanic whitetip (C. longimanus), olfaction is the primary sense used. This is mostly likely due to the lack of distinguishable features in the pelagic region and the vast distances this species has to travel in search of food (Meredith & Kajiura, 2010). Tiger sharks (Galeocerdo cuvier) travel between reefs, across the open ocean, to feed on dead or injured migratory turtles using their olfactory system to guide them. This species has the largest proportion of their brains dedicated to smell than any other species (Springer & Gold, 1989). Furthermore, their nares work independently of each other, allowing them to smell in stereo. For more benthic species, like those belonging to the genus Squatina (angel sharks), the olfactory system is not as developed, with reduced number of lamellae and smaller olfactory bulbs. The size of these bulbs changes with age. Just as the optic tectum decreased as a species matures, the olfactory bulbs increase in size and sensitivity with age (Theiss et al., 2009). This suggests that olfaction becomes more important to mature sharks than vision. Again, this is mostly likely to be due to the different habitats juveniles and adults live and feed in. Olfaction however, is not just used when hunting. Sharks and rays produce pheromones to signal their reproductive state and so olfaction is also used to search for potential mates (Carrier et al., 2012). Whilst studies of olfactory lamellae can give an indication as to the sensory ability of the system, their variation in size and shape between species means this method is not fully reliable. Coupling lamellae count data with epithelium surface area provides a better understanding of ability (Schluessel et al., 2008). However, there are limited quantitative
32 OSX-3000 osu270 studies on epithelium surface area, with only a few species having been investigated. Of the species studied it was found that pelagic species, along with having larger olfactory bulbs, also had a greater epithelial surface area than benthic species. This increased surface area increases the ability to detect chemical signals (Schluessel et al., 2008). The structure of the nares also varies dependant on lifestyle. More sedentary benthic species, such as the brownbanded bamboo shark (Chiloscyllium punctatum) and shovelnose ray (Aptychotrema punctatus), have wide rounded nasal openings. This is thought to maximise exposure to the water flow. Fast swimming pelagic species, like the nervous shark (Carcharhinus cautus) and spotted eagle ray (Aetobatus narinari), tend to have either slit like openings or nares that are covered by large flaps in order to reduce the flow rate of water through the nasal opening. This allows them to filter the water at a slower rate so they can pick up any chemical signals and gauge the direction (Meredith & Kajiura, 2010). Whilst the anatomy of the elasmobranch olfactory system is well documented, the relationship between anatomy and ecology is poorly understood. The diversity of this family suggests there could be a wide range of interspecific variation in the importance and function of this sensory system (Theiss et al., 2009). The sense of taste in elasmobranchs is one that has not been quantitatively assessed. This is primarily because this sense does not aid the searching and capturing of prey. Instead, it is used for determining if the prey item, once caught, is worth the energy needed to digest it (Carrier et al., 2012). 4.4. Mechanoreception Elasmobranchs use the pore and canal system in the lateral line to detect waves of pressure generated by predators and prey (Maruska, 2001). This system of canals can be relatively simple or complex and branching, depending on the species and its habitat. In batoids this system is very complex and is mostly likely due to their morphology (Garman, 1888). As they are dorsoventrally compressed they do not have as wide of a field of vision as sharks do. They therefore compensate for this lack of vision with increased sensitivity of the lateral line system. A study by Jordan (2008) investigated these systems in three stingray species, each belonging to a different habitat; bentho-pelagic stingray (Pteroplatytrygon violacea), benthic round stingray (Urolophus halleri) and the pelagic bat ray (Myliobatis californica). It was
33 OSX-3000 osu270 found that in each of these habitats the rays had different anatomical structures of their lateral line systems. U.halleri possessed many non-pored canals which are highly sensitive to skin displacement and direct touch (Maruska & Tricas, 2004). In comparison, the more pelagic species presented a mixture of pored and nonpored canals, with varying levels of branching. M.californica, a highly pelagic species, had the most complex lateral line system with lots of branching pored canals extending to the edge of the pectoral fins (Jordan, 2008). This is beneficial to pelagic species as pored canals allow for an increased sensitivity to the flow of water around them. Benthic species do not need as highly developed canal systems in comparison as they have a wider range of sensory stimuli in the benthic environment. These species also come into direct contact with more objects, such as corals and sediment. Therefore if these species were to have pored canals they would be at an increased risk of the pores becoming clogged with sediment and debris (Maruska & Tricas, 2004). The lateral line system is also known to be able to detect fluctuations in temperature. This may help migratory species, such as the spiny dogfish (Squalus acanthias), follow temperature gradients. In the spring time this species migrates north along the coast of North America to take advantage of spawning salmon and other migratory teleosts. When temperatures start to drop it then migrates back south for the winter (Carrier et al., 2012; Springer & Gold, 1989). With the exception of one study (Maruska, 2001) there is a distinct lack of quantitative, comparative investigations of the lateral line system in elasmobranchs. A common topic of debate amongst sensory shark biologists revolves around ‘is what a shark hears in its inner ears different from the vibrations it picks up in the lateral line system’. Sound is essentially waves of vibrations passed through a medium, and the lateral line system is known to detect vibrations. Therefore, the two systems are often combined and referred to as the acoustico-lateralis system (Corwin, 1978). Field experiments have often demonstrated the sensory capability of the acoustico-lateralis system however none have made links to feeding ecology or habitat preference. It is known that sharks can hear sounds between 10- 800Hz, but show a stronger attraction to low frequency pulsed sounds. This is thought to be because this mimics the sounds distressed prey would emit (Corwin, 1978).
34 OSX-3000 osu270 4.5. Electroreception Like vision, the anatomy of the electrosensory system varies widely between species, habitat and diet affecting the numbers of electrosensory pores and their distributions. Whilst deep water shark species have some of the largest eyes, as a % of their total length, they also have the lowest numbers of ampullae of Lorenzini, however they also present the widest range of pore numbers and distribution. This variation may reflect interspecific differences in feeding strategies. Some species in this habitat feed directly off the benthos and actively search for their food using electroreception, whilst others are ambush predators or scavenge for their food. Others feed on more active prey, e.g. squid, and rely more upon vision and pressure sensors than electrical pores (Murray, 1960). Whilst the numbers of pores for sharks in this habitat are relatively low, the ones they do have are very large epithelial pores. The larger diameter of these pores decreases the electrical impedance along the length of the canal, leading to increased sensitivity to electrical stimuli (Kajiura et al., 2010). Furthermore, the distribution of pores on the body varies with depth. Deepwater species have more pores on their ventral side in comparison to pelagic species. Again, this is due to foraging behaviour as most sharks in this habitat feed off the seabed (Kalmijn, 1988). Dietary preference can also affect the number and distribution of pores. Great hammerheads (Sphyrna mokarran) are known to swing their heads over the benthos in search of the electrical signals given off by stingrays buried in the sediment (Dijkgraaf & Kalmjin, 1962). Qualitative studies have described the complexity of the electrosensory system in skates and believe it to be inversely related to the mobility of their prey. More studies are required to give quantitative evidence for this (Raschi, 1986). Pelagic species are also found have large eye diameters, however their visual ability can be limited by algal blooms and weather related turbulence. Therefore, these species have to rely on other sensory systems to catch their fast moving prey (Kajiura, 2008). They generally have a large number of pores with an even distribution over both the dorsal and ventral side. This makes it easier to detect electrical signals from any direction and aids with magnetoreception / navigation. The ion-rich seawater acts as an electrical conductor. As the water moves over the Earth’s magnetic field lines it generates a weak electrical map of the immediate surroundings which is picked up by the ampullae (Molteno & Kennedy, 2009; Kalmijn, 1982). The sharks can then use this ‘map’ to undergo migratory routes or return to a favourite reef.
35 OSX-3000 osu270 Benthic elasmobranchs were found to have higher pore counts and densities than species in any other habitat. These higher pore densities can be related to a higher electrical sensitivity and therefore a preference for using electroreception (Kajiura, 2001). Batoid species in particular had the highest number of pores out of all of the elasmobranch groups. However, there has been only one published quantitative study to date on this subject (Jordan, 2008). The body morphology of rays and skates and their reduced fields of vision means they rely more heavily on electroreception. They have greater concentrations of pores on the ventral side which they use to scan the benthos in search of food. It was also found that the percentage of fin covered in pores could be linked to swimming style. In active swimming species, like Myliobatis californica, most of their pores are concentrated along the anterior edge of the pectoral fins. This creates a greater search area for this species as their wings move through a large plane (Bedore et al., 2014). It is important to understand the role electroreception has in the feeding strategies of elasmobranchs as this information can be used to create deterrents (Hart & Collin, 2015; Hoenig & Gruber, 1990). Blue shark populations are in decline worldwide caused by high bycatch rates, caught mainly on longline fisheries. It is well documented that this species has a highly developed electrosensory system, used primarily for navigation (Molteno & Kennedy, 2009). Therefore it was believed that attaching magnets to the hooks of longline fisheries could reduce the number of interactions between the sharks and fishing gear. A study by Porsmoguer (et al., 2015) tested two different strengths of magnets in the field during an operational fisheries period. It was discovered that the magnets in fact had an opposite effect than hoped and actually attracted more blue sharks to the lines. However, there have been more successful studies which use an electrical pulse to deter sharks. These have been successfully implemented in coastal swimming areas (Hart & Collin, 2015).
36 OSX-3000 osu270 5. Conclusion As predicted the anatomy of the different sensory systems in elasmobranchs are influenced by feeding ecology. Feeding ecology refers to not only what the individual is feeding upon, but also the habitat in which in hunts. It was found that not only do the different senses adapt to different habitats and dietary preferences but there is also some evidence of compensation. Vision plays more of a role in the location of prey for pelagic elasmobranchs, compared to deep sea species. Because of this, the electrosensory systems do not need to be as developed for these species. Reversely, the electrosensory systems for benthic species have become very complex and sensitive in order to compensate for the reduced number of visual cues. It is still not fully understood how the sensory systems interact with each other and the order in which the systems are used. By investigating the anatomy of these systems and their relationships to ecology we can start to create new methods to protect them. Global shark populations are in decline. Through the creation of man-made deterrents we can start to reduce the amount of elasmobranch caught as bycatch. They can also be used to reduce the risk of attacks on humans, relieving some of the negative media surrounding sharks. There is still a significant lack of quantitative data surrounding all of the elasmobranch sensory systems and their relationships to ecology. Further point of study would be to create more multidisciplinary studies encompassing all of the senses. These studies will need to be carried out on a wider range of elasmobranch species and a range of ages, focusing particularly on batoids where there is a current lack of data. Word Count: 9,919
37 OSX-3000 osu270 6. References Bedore, C. N., Harris, L. L., & Kajiura, S. M. (2014). Behavioural responses of batoid elasmobranchs to prey-simulating electric fields are correlated to peripheral sensory morphology and ecology. Zoology, 117, 95-103. Bleckmann, H., Weiss, O., & Bullock, T. H. (1989). Physiology of lateral line mechanoreceptive regions in the elasmobranch brain. Journal of Comparative Physiology A, 164, 459-474. Bright, M. (2002). Sharks. London: The Natural History Museum. ISBN: 0-565-09159-X. Brown, B. R. (2003). Neurophysiology: sensing temperature without ion channels. Nature, 421, 495-495. Carrier, J. C., Musick, J. A., & Heithaus, M. R. (Eds.). (2012). Biology of sharks and their relatives. CRC press. ISBN: 0-8493-1514-X. Clarke, S. (2006). Global estimates of shark catches using trade records from commercial markets. Ecology Letters, 9, 1115–1126. Corwin, J. T. (1978). The relation of inner ear structure to the feeding behaviour in sharks and rays. Scanning electron microscopy, 2, 1105-1112 Dijkgraaf, S., & Kalmijn, AJ (1962). Behavioral experiments on function of Lorenzini ampules. Science, 49, 400-400. Duffy, J. E. (2003). Biodiversity loss, trophic skew and ecosystem functioning. Ecology Letters, 6, 680-687. Emde, G. von der, Mogdans, J., & Kapoor, B. G. (Eds.). (2004). The senses of fish: Adaptations for the reception of natural stimuli. United States: Springer-Verlag New York. Gardiner, J. M., Atema, J., Hueter, R. E., & Motta, P. J. (2014). Multisensory integration and behavioral plasticity in sharks from different ecological niches. PLoS One, 9, e93036. Garman, S. (1888). On the lateral canal system of the Selachia and Holocephala. Printed for the Museum. Gerking, S. D. (2014). Feeding ecology of fish. Elsevier. Gilbert, P. W. (1963). The visual apparatus of sharks. Sharks and survival, 283-326. Gruber, S. H., & Cohen, J. L. (1978). Visual system of the elasmobranchs: state of the art 1960–1975. Sensory Biology of Sharks, Skates and Rays, Office of Naval Research, Arlington Virginia, 11-116. Hart, N. S., & Collin, S. P. (2015). Sharks senses and shark repellents. Integrative zoology, 10, 38-64.
38 OSX-3000 osu270 Heath, A. R. (1990). The ocular tapetum lucidum: a model system for interdisciplinary studies in elasmobranch biology. Journal of Experimental Zoology, 256, 41-45. Hodgson, E. S., & Mathewson, R. F. (1978). Sensory biology of sharks, skates, and rays. TUFTS UNIV MEDFORD MA DEPT OF BIOLOGY. Hoenig, J. M., & Gruber, S. H. (1990). Life-history patterns in the elasmobranchs: implications for fisheries management. NOAA Technical Report NMFS, 90, 16. Hueter, R. E., & Cohen, J. L. (1991). Vision in elasmobranchs: a comparative and ecological perspective. J. Exp. Zool., Suppl, 5, 1-182. Hueter, R. E., & Gilbert, P. W. (1990). The sensory world of sharks. Discovering Sharks, American Littoral Society, Highlands, 48-55. Hueter, R. E., Mann, D. A., Maruska, K. P., Sisneros, J. A., & Demski, L. S. (2004). Sensory biology of elasmobranchs. Biology of sharks and their relatives, 325-368. Jordan, L. K. (2008). Comparative morphology of stingray lateral line canal and electrosensory systems. Journal of morphology, 269, 1325-1339. Kajiura, S. M. (2001). Head morphology and electrosensory pore distribution of carcharhinid and sphyrnid sharks. Environmental Biology of Fishes, 61, 125-133. Kajiura, S. M. (2008). Sensory Systems in Elasmobranchs. In Shark Deterrent and Incidental Capture Workshop April 10–11, 9. Kajiura, S. M., Cornett, A. D., & Yopak, K. E. (2010). Sensory adaptations to the environment: electroreceptors as a case study. Sharks and their relatives, 2, 393-434. Kalmijn, A. J. (1971). The electric sense of sharks and rays. Journal of Experimental Biology, 55, 371-383. Kalmijn, A. J. (1982). Electric and magnetic field detection in elasmobranch fishes. Science, 218, 916-918. Kalmijn, A. J. (1988). Detection of weak electric fields. In Sensory biology of aquatic animals, Springer New York, 151-186. Kirschvink, J. L., Walker, M. M., & Diebel, C. E. (2001). Magnetite-based magnetoreception. Current opinion in neurobiology, 11, 462-467. Klimley, P. A. & Oerding, S. (2013). The biology of sharks and rays. United States: University of Chicago Press, ISBN-13: 978-0-226-44249-5. Lisney, T. J. (2004). Neuroethology and vision in elasmobranchs. University of Queensland eSpace. Lisney, T. J., & Collin, S. P. (2007). Relative eye size in elasmobranchs. Brain, behaviour and evolution, 69, 266-279.
39 OSX-3000 osu270 Maruska, K. P. (2001). Morphology of the mechanosensory lateral line system in elasmobranch fishes: ecological and behavioural considerations. The behaviour and sensory biology of elasmobranch fishes: an anthology in memory of Donald Richard Nelson, Springer Netherlands, 47-75. Maruska, K. P., & Tricas, T. C. (2004). Test of the mechanotactile hypothesis: neuromast morphology and response dynamics of mechanosensory lateral line primary afferents in the stingray. Journal of experimental biology, 207, 3463-3476. Meredith, T. L., & Kajiura, S. M. (2010). Olfactory morphology and physiology of elasmobranchs. The Journal of experimental biology, 213, 3449-3456. Molteno, T. C. A., & Kennedy, W. L. (2009). Navigation by induction-based magnetoreception in elasmobranch fishes. Journal of Biophysics. Murray, R. W. (1960). Electrical sensitivity of the ampullae of Lorenzini.Nature, 187:957. Murray, R. W. (1962). The response of the ampullae of Lorenzini of elasmobranchs to electrical stimulation. Journal of Experimental Biology, 39, 119-128. Myers, R. A., Baum, J. K., Shepherd, T. D., Powers, S. P., & Peterson, C. H. (2007). Cascading effects of the loss of apex predatory sharks from a coastal ocean. Science, 315, 1846-1850. Myrberg Jr, A. A. (2001). The acoustical biology of elasmobranchs. Environmental Biology of Fishes, 60, 31-46. Popper, A. N., & Fay, R. R. (1977). Structure and function of the elasmobranch auditory system. American Zoologist, 17, 443-452 Porsmoguer, S. B., Bănaru, D., Boudouresque, C. F., Dekeyser, I., & Almarcha, C. (2015). Hooks equipped with magnets can increase catches of blue shark (Prionace glauca) by longline fishery. Fisheries Research, 172, 345-351. Raschi, W. (1986). A morphological analysis of the ampullae of Lorenzini in selected skates (Pisces, Rajoidei). Journal of Morphology, 189, 225-247. Sandin, S. A., Smith, J. E., DeMartini, E. E., Dinsdale, E. A., Donner, S. D., Friedlander, A. M. & Sala, E. (2008). Baselines and degradation of coral reefs in the northern Line Islands. PLoS One, 3, e1548. Schluessel, V., Bennett, M. B., Bleckmann, H., Blomberg, S., & Collin, S. P. (2008). Morphometric and ultrastructural comparison of the olfactory system in elasmobranchs: the significance of structure–function relationships based on phylogeny and ecology. Journal of Morphology, 269, 1365-1386. Schultze, M. (1866). The anatomy and physiology of the retina. Archive for microscopic anatomy , 2, 175-286.
40 OSX-3000 osu270 Sivak, J. G. (1990). Elasmobranch visual optics. Journal of Experimental Zoology, 256, 13- 21. Springer, V. G., & Gold, J. P. (1989). Sharks in question. United States: Smithsonian Institution Press. ISBN: 0-87474-877-1. Theiss, S. M., Hart, N. S., & Collin, S. P. (2009). Morphological indicators of olfactory capability in wobbegong sharks (Orectolobidae, Elasmobranchii). Brain, behaviour and evolution, 73, 91-101. Thorson, T. B. (1987). Human impacts on shark populations. Sharks: an inquiry into biology, behaviour, fisheries, and use, Oregon State University, Portland, 31-37. Wisby, W. J., Richard, J. D., Nelson, D. R., & Gruber, S. H. (1964). Sound perception in elasmobranchs. Marine Bio-acoustics, 255-68. 6.1. Web resources FishBase, (2016). Editors; Froese, R., Pauly, D. <www.fishbase.org>. Accessed 02/16. Shark Foundation, (2008). Figure of elasmobranch sensory ranges <http://www.shark.ch>. Accessed: 01/04/16. Sharks Gallery (2015).Image of blue shark nictitating membrane. < http://seashadows.narod.ru/htmlimg/im172.html>. Accessed: 10/04/16. The Liquid Earth (2014). Image of great white shark. Credit: Singleton, K. < http://theliquidearth.org/2014/10/is-the-great-white-shark-really-as-dangerous-as-we-all- think/>. Accessed: 10/04/16.

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1. Dissertation

  • 1. 1 OSX-3000 osu270 Sensory Organs and Feeding Ecology in Elasmobranchs Jessica Sherlock School of Ocean Sciences, Bangor University, Menai Bridge, Anglesey, LL59 5AB, UK.
  • 2. 2 OSX-3000 osu270 Acknowledgements I would like to thank my project supervisor Dr Ian McCarthy for his support, guidance and encouragement throughout the process of researching and writing this dissertation. I would also like to thank my tutor Dr Martin Skov for his continuous guidance and belief in me throughout all my time with the School of Ocean Sciences, Bangor University. To my housemates and fellow students, thank you for the late night chats and for answering my multitude of silly questions. Thank you to Phillip Wallace and Beth Saunders for their emotional support and proof reading parts of this paper. My parents and brother, I am forever grateful for your support and love through all my university years. I couldn’t have done it without you.
  • 3. 3 OSX-3000 osu270 Sensory Organs and Feeding Ecology in Elasmobranchs Abstract Elasmobranchs have evolved a battery of senses over millennia used primarily to hunt prey, including a unique sixth sense that enables them to detect electricity. Each of these senses is used in the locating, tracking, capturing or consuming of prey. They can be grouped into four categories; Photoreception, Chemoreception, Mechanoreception & Electroreception. All of these senses have adapted to species ecology, be it habitat or feeding ecology. Species in different habitats, with different dietary preferences, may favor one sensory system over another. Whilst there is limited amounts of quantitative data covering this topic some conclusions have been drawn. Pelagic species which feed on fast moving prey tend to rely more upon their chemosensory and photosensory systems. This allows them to locate and track their prey quicker in the featureless pelagic environment. Species which feed primarily on the benthos are more dependent on electroreception. Their increased pore densities aid the elasmobranch in scanning the seabed for electrical signals given off by hidden or camouflaged prey. A compensatory effect can also be observed between some of the senses. For example, in environments where there is little light or visual stimuli, other sensory systems will become more developed to fill the role of locating prey. It is important to understand the link between sensory ability and species ecology as it can aid with the creation of man-made deterrents. These deterrents can be put onto fish gear to reduce the number of sharks killed as bycatch. Current data sets focus primarily on the visual and electrical capabilities of shark species. Increased research effort into all senses, across the whole elasmobranch family, is urgently needed in order to expand our knowledge of all the interspecies adaptations and to aid the protection of endangered elasmobranch species. Keywords: Elasmobranchs ● feeding ecology ● sensory systems ● photoreception ● chemoreception ● mechanoreception ● electroreception
  • 4. 4 OSX-3000 osu270 Contents Title ........................................................................................................................................1 Abstract ..................................................................................................................................2 Acknowledgements ................................................................................................................3 Contents..................................................................................................................................4 Figures and Tables .................................................................................................................5 1. Introduction ........................................................................................................................6 1.1. Sensory organs in elasmobranchs .......................................................................6 1.1.1. Photoreception......................................................................................9 1.1.2. Chemoreception .................................................................................11 1.1.3. Mechanoreception ..............................................................................13 1.1.4. Electroreception .................................................................................15 1.2. Feeding Ecology................................................................................................16 1.3. Aims of study ....................................................................................................17 2. Methods............................................................................................................................18 2.1. Literature review ...............................................................................................18 2.2. Data collection...................................................................................................19 3. Results & Analysis ..........................................................................................................20 3.1. Photoreception...................................................................................................20 3.2. Chemoreception ................................................................................................21 3.3. Electroreception ................................................................................................23 3.4. Comparative studies ..........................................................................................25 4. Discussion ........................................................................................................................28 4.1. Study Limitations ..............................................................................................28 4.2. Photoreception...................................................................................................28 4.3. Chemoreception ................................................................................................30 4.4. Mechanoreception .............................................................................................32 4.5. Electroreception ................................................................................................34 5. Conclusion........................................................................................................................36 6. References ........................................................................................................................37 6.1. Web Resources..................................................................................................40
  • 5. 5 OSX-3000 osu270 Figures and Tables Figures Figure 1. Sensory ranges of elasmobranchs...........................................................................7 Figure 2. Prey-omitted signal fields .......................................................................................8 Figure 3. Methods used in elasmobranchs to protect the eye...............................................10 Figure 4. Anatomy of the lateral line system in elasmobranchs ..........................................14 Figure 5. Use of elasmobranch electroreception for navigation ..........................................16 Figure 6. Average eye diameter, grouped by species...........................................................20 Figure 7. Average eye diameter, grouped by habitat ...........................................................21 Figure 8. Average lamellae count, grouped by habitat ........................................................22 Figure 9. Average lamellae count, grouped by dietary preference ......................................22 Figure 10. Average pore count, grouped by habitat.............................................................23 Figure 11. Average pore count, grouped by species ............................................................24 Figure 12. Average pore count and eye diameter, grouped by species................................26 Figure 13. Average pore count and eye diameter, grouped by habitat.................................27 Figure 14. Average pore count and eye diameter, grouped by dietary preference ..............27 Tables Table 1. Key terms used in the primary literature search.....................................................18
  • 6. 6 OSX-3000 osu270 1. Introduction There are over 1100 extant species of sharks, rays and skates belonging to the subclass Elasmobranchii within the class Chondrichthyes, or the cartilaginous fishes (Carrier et al., 2012). Fossil records date elasmobranchs back around 400 million years to in the early Devonian period. Since then, elasmobranchs have evolved a battery of specialised senses in order to detect and localise their prey (Huter et al., 2004). Their six senses, along with large brains, are probably the most adapted and diverse of any known predator (Emde et al., 2004). This variety of senses provides elasmobranchs with the ability to detect and consume prey even when one or more of their senses are compromised, such as at night (Klimley & Oerding, 2013). Elasmobranchs, in particular sharks, play a vital role within the marine ecosystem. They help keep fish stocks healthy as they target old and sick fish which benefits not only the biodiversity of the ecosystem but also the fishing industry (Sandin et al., 2008). The main threat elasmobranch populations face is overfishing, particularly as bycatch. In the past 50 years shark catch has increased by 200%, causing a 90% decline in global shark populations (Clarke, 2006; Myers et al, 2007). Loss of this apex predator can cause a shift within the marine food web, creating an inverted trophic pyramid. The removal of any top predator within a food web can cause the number of secondary predators to increase, due to lack of competition (Duffy, 2003). In reef habitats the loss of apex shark species has led to an increase in the number of snappers and jacks. These species feed more frequently and in larger numbers and are therefore reducing the abundance of lower trophic level reef fish (Sandin et al., 2008). Researching the sensory systems and organs sharks use can provide a greater understanding of how they feed. This knowledge can aid the development of deterrents which keep them away from fishing lines and nets therefore reducing bycatch numbers (Hart & Collin, 2015). 1.1. Sensory organs in elasmobranchs Sensory performance can be classed in two ways; sensitivity and acuity. Sensitivity is measured by the minimum stimulus detectable by the system. The acuity of the system is described by the ability to discriminate stimulus characteristics, such as location and type (Hueter et al., 2004). This allows for quantification and comparison of different elasmobranch senses, determining ‘how good’ a sense is (Carrier et al., 2012).
  • 7. 7 OSX-3000 osu270 Elasmobranchs possess a highly acute array of sensory systems; vision, smell, taste, hearing, touch and a unique electrical sense also known as the ampullae of Lorenzini (Emde et al., 2004). Often the senses of elasmobranchs are investigated individually. It is therefore very difficult to accurately understand the exact order in which each sense is prioritised and used (Springer & Gold, 1989). However the anatomy of each of the sensory systems does give some indication as to their range, and therefore order of use. Figure 1 provides a visual representation of each of the shark’s six senses and the order in which they may be used when locating and consuming prey. Low frequency sounds are known to travel great distances underwater (Bright, 2002). The elasmobranch auditory system is highly adapted to these frequencies and is likely to be the first sense to pick up a signal. It is believed that sharks can detect sounds from over a 1 mile away (1.6km), but they are only attracted to these sounds if they are irregular and of a low frequency (Emde et al., 2004; Springer & Gold, 1989; Carrier et al., 2012). The next sense to pick up a signal is thought to be the olfactory system, or sense of smell. Dependant on water currents, elasmobranchs can detect odours at distances up to 500m (Figure 1) (Emde et al., 2004). They will then follow this scent trail, testing the concentration of the scent as they swim. At around 100m pressure sensors in the shark’s lateral line system, on either side of its body, pick up movements in the water. This sense of distant touch guides the shark to a more accurate location of the signal (Carrier et al., 2012). Elasmobranch visual ability can be restricted by water turbidity and light levels. However, in clear well-lit waters elasmobranchs can spot movements at 25 to 50m (Figure 1). Once the prey is within touching distance the fifth and most unique sense starts to pick up minute electrical waves given off by the muscles of the prey (Hodgson & Mathewson, 1978). This sensory system, known as electroreception, uses tiny jelly-filled pores called the ampullae of Lorenzini to detect these signals. The final senses, taste and direct touch, are used when the shark makes direct contact with the prey. They are thought not to aid with detection of prey but with assessing if the prey item is ‘food’ or not (Klimley & Oerding., 2013). Figure 1. Ranges of sensitivity to a stimulus for each of the elasmobranch senses. Adapted from: (Shark Foundation, 2008).
  • 8. 8 OSX-3000 osu270 Figure 2. Visual model of signal field omitted by a prey source. The primary pathway (excluding auditory) elasmobranchs use to detect prey is through olfaction (O). The odour field (shown in blue) can extend over large distances away from the prey source. Elasmobranchs swim up this narrow field until the prey becomes visible (V, shown in red). Once the elasmobranch is within touching distance it can sense pressure changes in its lateral line system. This creates an acoustic nearfield (L, shown by the dotted line). Small electrical signals (E, shown in orange) given off by the muscles of the prey are detected right before contact (T). Water direction is shown by the white arrow. Credit: (Gardiner et al., 2014). To date there has been one multidisciplinary approach to elasmobranch senses by Gardiner et al. (2014). This study was undertaken by blocking out all of the senses of three shark species, with different sensory anatomies and behavioural ecology, and observing their feeding sequences as each individual sense was ‘turned back on’ (Gardiner et al., 2014). It was discovered that even with one or more of their senses restricted the shark were still capable of detecting and consuming their prey. This study also supported previous evidence and theories as to the order in which certain shark species use their senses and how the sensory systems interact. Gardiner then created a physical model of prey signal fields, similar to that of Figure 1. This revised figure not only gives an indication of the range of each of the senses but also the field in which they are detected (Figure 2). It was noted that the auditory system was excluded from this study, however the reason for this exclusion was not explained. It is possible that it was dismissed due to lack of data and difficulty recording this sense. As mentioned previously the elasmobranch auditory system can detect sounds from over a mile away and this is difficult to recreate in a laboratory setting.
  • 9. 9 OSX-3000 osu270 For this paper, the six senses of elasmobranchs (sight, smell, hearing, touch, taste and electroreception) have been grouped in four categories; Photoreception, Chemoreception, Mechanoreception and Electroreception. The rest of this introduction will discuss each sensory category in terms of anatomy and performance. Feeding ecology will also be defined and links between the senses and ecology discussed. 1.1.1. Photoreception Photoreception in elasmobranchs covers the sense of sight. Studies into the visual system of elasmobranchs date back 200 years (Gruber & Cohen, 1978). After a study by Schultze (1866) produced a detailed account of the retinal structure, interest in elasmobranch visual systems spiked (Emde et al., 2004). Before this time the visual capabilities of elasmobranchs were considered to be relatively poor compared with the other sensory systems (Hueter & Gilbert, 1990). By the mid-20th century the visual system in sharks and rays had become very well documented and investigated. Since then, vision has been rarely studied independently and is now often paired with investigations of brain sizes (Gruber & Cohen, 1978). Visual stimuli are detected at a relatively close range (15-25m). This sensory system is primarily used for hunting, however some species are known to successfully feed even when their vision is restricted (Sivak, 1990). Great white sharks (Carcharodon carcharias) have been known to lift their heads out of the water in order to scope out the topside surroundings and track their primary prey species, seals and sea lions, belonging to the family Pinnipedia (Carrier et al., 2012). However, it is not known how well adapted elasmobranch eyes are to above-water vision. Elasmobranch eyes are more complex and well developed than teleost eyes, however they share the same basic anatomy (Carrier et al., 2012). The eyes focus through the use of the rectus muscle which pulls the lens closer to or further away from the retina. This process, similar to that of a focusing camera lens, is different from higher terrestrial vertebrates in which the lens is instead distorted to focus light entering the eye from different distances (Gilbert, 1963). The direction the eyes face is again controlled by the rectus muscle as well as the oblique muscle (Springer & Gold, 1989). Some elasmobranch species have evolved new ways in which to sense light levels. A thin area of skin on the top of their head, which leads directly to the pineal gland in the brain, can detect light. This could be used during diurnal vertical migrations such and those undertaken by megamouth sharks (Megachasma pelagios).
  • 10. 10 OSX-3000 osu270 Figure 3. The nictitating membrane of a blue shark (Prionace glauca) covering half of the eyeball (A). This toughened layer can cover the eye prior to a feeding event where prey may inflict damage when trying to protect itself. Species that do not possess this membrane, such as the Great White Shark (Carcharodon carcharias), can roll their eyes backwards into their sockets to protect them (B). Taken from: (The Liquid Earth, 2014; Sharks Gallery, 2015). A B However this ‘window’ of skin does not possess a lens, unlike the eyes, and so the light cannot be focused in order to determine shape (Springer & Gold, 1989). Unlike teleost species elasmobranchs do have eyelids, however these lids are fixed and cannot cover the eye to protect it (Emde et al., 2004). Elasmobranchs therefore have evolved new ways in which to protect their eyes from the sharp claws or spines of their prey when feeding. Most shark species have developed specialised eyelids, known as the nictitating membrane, to cover the eyeball (Figure 3.A). Other species, such as C. carcharias, which do not possess this layer are known to roll their eyes back into the sockets, exposing the hardened pad on the back of the eye in order to protect the pupils (Figure 3.B) (Klimley & Oerding, 2013). Elasmobranch eyes, like human eyes, do possess contracting pupils. For shallow water species this enables them to control the amount of light entering their eyes by dilating or contracting the pupils (Sivak, 1990). Requiem sharks do this laterally giving them a ‘cat eye’ appearance. Others species, primarily skates and rays, contract their pupils into a ‘U’ shape which creates double vision. They use this to determine distance (Springer & Gold, 1989). Other species have a ragged flap which slides over the pupil reducing the amount of light entering the pupil. Again, this creates double vision and is used to aid depth perception (Sivak, 1990). Light travels slower in water than air and so most elasmobranch species have adapted to low light conditions (Klimley et al., 2013). Their excellent vision in these conditions is primarily
  • 11. 11 OSX-3000 osu270 due to the structure of the eye. The tapetum lucidum, a layer of mirrored crystals, lies behind the retina amplifying the strength of the image. However, the process of amplifying the light reduces the acuity of the image but increases the sensitivity of the system to a stimulus (Carrier et al., 2012; Heath, 1990). Pigments in the photoreceptors of the eye also aid with vision in low light conditions. The red wavelengths within the visible light spectrum are absorbed first within the water column and the green wavelengths absorbed last. This leaves the ocean with a dim, blue-green colour (Klimley et al., 2013). The pigments within elasmobranch eyes are most sensitive to this low-level blue-green light. Current studies on elasmobranch vision are focusing on the ability of colour vision. Around 20 species of shark have been found to have duplex retinas meaning they possess both rod and cone photoreceptors (Springer & Gold, 1989). Theoretically this means that these species should be able to see in colour. Only two species of shark, the sixgill (Hexanchus griseus) and bigeye thresher (Alopias superciliosus), are known to have only rod photoreceptors and should therefore lack colour vision (Springer & Gold, 1989). 1.1.2. Chemoreception Chemoreception in elasmobranchs can be divided into two categories; olfaction and taste. Like teleost fish, elasmobranchs use olfactory system to detect odours within the water flow. It has often been described as the most important sense elasmobranchs use to detect prey as over two thirds of their brain mass is dedicated to smell (Carrier et al., 2012). However, male elasmobranchs also use olfaction to detect female sex pheromones and find a mate (Hodgson & Mathewson, 1978). Interest in this system spiked during World War II in an effort to create preventative shark attack equipment for military personnel (Carrier et al., 2012). The olfactory system is well known and documented for shark species, unlike that of rays and chimeras (Meredith & Kajiura, 2010). Sharks have a pair of nostril-like holes, or nares, under the leading edge of the snout. Each of the nares is divided into two openings by a nasal flap. Water is guided into the incurrent nare opening and is passed over a series of skin folds, the olfactory lamellae, before passing into the olfactory sac. It then exits through the excurrent nare opening on the other side of the nasal flap (Springer & Gold, 1989). The olfactory lamellae increase the probability of a chemical signal being detected as they provide more surface area. Chemical odours passing over the lamellae stimulate neuro-sensory cells which
  • 12. 12 OSX-3000 osu270 send a signal to the brain. This is also known as the chemosensory function (Meredith & Kajiura, 2010). Elasmobranch olfaction is very developed. Contrary to media speculation, sharks cannot detect a single drop of blood in the ocean from miles away. However, some species are able to detect fish extracts in concentrations lower than 1 part in 10 billion (Carrier et al., 2012). Different species are attracted to different chemical signals dependant on their preferred diet (Schluessel et al., 2008). White sharks (C. carcharias) are more sensitive to blood in the water whereas lemon and nurse sharks (Negaprion brevirostris, Ginglymostoma cirratum) are attracted to amino acids and amines from the body fluids of their prey (Schluessel et al., 2008). Once an odour is detected the elasmobranch will swim through the scent trail in an ‘S’ shape pattern, swinging its head from side to side. This enables the snout to pass through the trail, assisting it with determining the direction of the odour. More sedentary species are able to pump water over the nares whilst resting on the sea floor until a scent trail is detected (Klimley & Oerding, 2013). Chemoreception also covers the sense of taste in elasmobranchs. To date there has been very little published research on this sensory system and its relation to feeding and ecology (Emde et al., 2004). However the anatomy and physiology of the system has been described. Elasmobranchs have small pits in the lining of the mouth and throat which contain rod-shaped gustatory sensory cells (Carrier et al., 2012). Once an object is bitten it releases dissolved chemicals. These chemicals attach to the gustatory cells and pass a signal to the brain which tells the shark if the object is consumable or not (Klimley & Oerding, 2013). This can be linked to the bite and release behaviour observed in C. carcharias. In attacks on humans it has repeatedly been noted that after an initial bite, the shark swims away. It is theorised that the taste of that first bite is used to determine if the prey item was the high fat mammal they were expecting. If it is not, they release the item as they do not want to waste time and energy processing and digesting the meal (Hodgson & Mathewson, 1978). It is thought that the taste organs are not as highly adapted as the other sensory systems as they do not play a role in locating prey. Exceptions to this are the many species with nasal barbells like the nurse shark (G. cirratum) and mandarin dogfish (Cirrhigaleus barbifer). These barbells could be used to rake through and taste the sediment in search of food (Springer & Gold, 1989). However, these adaptations could be organs used for the sense of touch.
  • 13. 13 OSX-3000 osu270 1.1.3. Mechanoreception The term mechanoreception is used to cover the senses hearing and touch, including the lateral line system. The auditory system in elasmobranchs is used to detect prey, competitors and potential mates (Corwin, 1978). Sharks and rays are not known to make noise, so theoretically their auditory systems have been shaped by the ambient noises of their habitats (Carrier et al., 2012). Numerous studies have been conducted on elasmobranch hearing (Myrberg, 2001; Popper & Fay, 1977; Wisby et al., 1964). These studies however focus primarily on the anatomy of the system and give little insight into the physiology and relation to the ecology of the animal. Sound travels roughly four times faster in water than air (Wisby et al., 1964). This has allowed hearing to become the first sense elasmobranchs use when hunting. Behavioural evidence suggests that sharks can detect underwater frequencies of up to 1000Hz (Popper & Fay, 1977). However, they are most sensitive to irregular, low frequency vibrations around 40Hz, and are able to detect these over large distances (Springer & Gold, 1989). This type of frequency is similar to that of injured prey or large shoals of fish (Emde et al., 2004). Nevertheless, there is little evidence to suggest they are more sensitive to these frequencies than other fish species, especially those with swim bladder adaptations (Carrier et al., 2012). The ears of elasmobranchs are completely internal, embedded within the frontal skull. These inner ears are made up of a series of channels and sacs known as the membranous labyrinth. In sharks this system is filled with sea water which enters through the endolymphatic ducts. A second layer of fluid filled canals surrounds the membranous labyrinth, protecting and supporting it (Myrberg, 2001). The ears of elasmobranchs, like human ears, are responsible for maintaining balance and equilibrium. The sacculus, a large chamber found within the membranous labyrinth, is lined with otoliths and sensory hair cells. These are responsible for registering any imbalance which then sends a signal to the sharks brain, allowing it to correct itself (Carrier et al., 2012). This is vital for open ocean pelagic species where there are little to no visual cues which can tell the shark which direction is ‘up’. The sense of touch can be split into two subcategories; actual touch and distance touch, also known as the lateral line system (Carrier et al., 2012). Elasmobranchs use actual touch, or direct contact, in the same way they use taste. This sense has no direct effect on detecting prey but rather assessing if the item is edible or not. Many sharks will nose an object before taking
  • 14. 14 OSX-3000 osu270 an exploratory bite in order to determine if the item is worth the energy needed to digest it (Springer & Gold, 1989). Distance touch is experienced through the lateral line system. This system of fluid filled canals runs along the sides of the body in sharks, from the head to the upper lode of the tail (Bleckmann et al., 1989). Two extra canals, the infraorbital and supraorbital, are located exclusively on the head. The placement of the lateral line system in batoids (rays and skates) varies widely, dependant on habitat and feeding ecology (Jordan, 2008). The canals contain small, hair- like receptors which send a signal to the brain whenever a wave of water, entering through an external pore, passes over them (Figure 4). These waves are created by changes in pressure as an animal moves though the water. Erratic vibrations can indicate an injured or sick animal and guide the elasmobranch to the prey item (Bright, 2002). Vibrations are also created by the sharks own movements. The water it displaces as it swims creates ripples which bounce off nearby objects and return to the shark. This allows the shark to create a vibration echo map, similar to sonar mapping, of its surroundings (Klimley & Oerding, 2013). Some shark species also possess rows of pores along the gills and pectoral fins. These pores, also known as pit organs, contain neuromast-like cells that allow the shark to detect changes in temperature which helps migratory species (Maruska, 2001). Before 1980 it was believed that the lateral line system in elasmobranchs was also responsible for hearing (Popper & Fay, 1977). Since then, studies in the early 2000s disproved this but the principle still remains. Considering that sound waves are essentially vibrations, which the lateral line system is known to detect, it is not unreasonable to assume they could use this system to hear (Bleckmann et al., 1989; Maruska, 2001). Figure 4. The elasmobranch lateral line system: interconnected, fluid-filled, canals running from head to tail in shark species. Tiny waves of water enter the system through the external surface pore and pass over the hair-like receptors inside the canal. Taken from: (Bright, 2002).
  • 15. 15 OSX-3000 osu270 1.1.4. Electroreception Elasmobranchs have developed a specialised sixth sense called electroreception. Evolved from the pores in the lateral line system, the jelly-filled pores known as the ampullae of Lorenzini can detect minute electrical signals in the water. These signals are given off by muscle movements, such as heartbeats, of the prey (Kalmijn, 1971). This system was first described by Lorenzini in 1678, but its physiological function remained unknown for three centuries (Carrier et al., 2012). Originally it was thought that the ampullae were a type of mechanoreceptor until studies by Murray (1960) and Dijkgraaf & Kalmijn (1962) investigated the electrosensitivity of the system. The electrosensory system consists of several hundred jelly-filled pores, concentrated primarily around the snout, connected by cylindrical canals. The ‘jelly’ acts as a conductor and picks up any fluctuations in the electrical field of the nearby habitat. This signal is then passed onto the sensory cells which line each pore. A sensory nerve at the base of each pore then transports this information to the brain, telling the shark the intensity and direction of the signal (Springer & Gold, 1989). This system is so sensitive that it can pick up voltage fluctuations as low as 5nV/cm (nano-Volts per centimetre) (Kalmijn, 1982). The ampullae can also pick up changes in pressure and temperature, however they are not as sensitive to these signals as the lateral line system (Brown, 2003). The amount of pores each elasmobranch species has depends on their habitat and feeding ecology. More active species are known to have around 2,000 pores whereas more sedate species can have only a few hundred (Murray, 1962). The use of this sensory system is also dependant on each species. Hammerheads (genus Sphyrna) are thought to use their ampullae like a metal detector, sweeping their heads from side to side over the seafloor in search of prey buried in the sediment (Kajiura, 2001). Other species use electroreception, along with the lateral line system, to guide their mouths to the prey item in the last few moments of feeding. Gardiner (et al., 2014) suggested that in these moments, electroreception takes over from sight and smell as the primary sense. This is particularly useful for species that roll their eyes back into the sockets to protect them, leaving them blind just before contact with their prey (Figure 3). Instead they use their ampullae to guide them by following the electrical waves given off by the muscles of their prey as it tries to escape (Emde et al., 2004).
  • 16. 16 OSX-3000 osu270 It is also theorised that this bioelectrical system may aid geographical navigation (Molteno & Kennedy 2009). Many teleost species use magnetite in their bodies to sense the polarization of the Earth’s magnetic fields (Kirschvink et al., 2001). Elasmobranchs however do not possess magnetite. It is thought they use a combination of the positive ions in saline water and the Earth’s magnetic fields to induce electric fields, which it can detect with its ampullae (Figure 5) (Molteno & Kennedy 2009). This ‘magnetoreception’ can help pelagic species migrate over large distances in the open ocean. These species have been found to have a more even distribution of ampullae than more benthic species in order to detect the induced magnetic field (Carrier et al., 2012). 1.2. Feeding Ecology Feeding ecology is defined as what organisms feed upon (their feeding habits), how the food is acquired (foraging habits) and where the food is found (foraging habitat) (Gerking, 2014). It is often difficult to classify elasmobranch species into individual ecological groups as they move between different niches and depths (Carrier et al., 2012). Sharks, in particular, inhabit a wide variety of ecological niches; from the deep ocean to shallow coastal waters, with some species even frequenting freshwater habitats (Emde et al., 2004). In each of these habitats elasmobranchs have adapted their sensory biology to feed upon their preferred prey item. Some species are plankton eating filter feeders whilst others prefer to feed on invertebrates on the benthos. A few are even at the top of the food chain, preying upon large high-fat mammals (Emde et al., 2004). Each of these prey types has led to elasmobranchs adapting their sensory biology, over millennia, to ensure successful capture of prey. In some cases the size or number of organs changes, whilst in other species a sense may become essentially useless. However each adaptation has allowed elasmobranchs to become one of, if not the most successful species in the animal kingdom (Gerking, 2014). Figure 5. Use of elasmobranch electroreception for navigation. Electric current is induced as the shark swims through the horizontal component of the Earth’s magnetic field. The ampullae of Lorenzini detect this current and supply navigational information to the brain. Credit: (Carrier et al., 2012).
  • 17. 17 OSX-3000 osu270 1.3. Aims of study Often studies of elasmobranch senses and ecology focus on one sense at a time. There are only a handful of studies which address all elasmobranch senses in relation to their feeding ecology and habitat. The aim of this paper is to discuss the battery of senses elasmobranchs possess, focusing primarily on shark species, and look for any relationships between these senses and different feeding ecologies. Habitat may be used during analysis as it can correlate to dietary preference. This review aims to address the hypotheses: 1) There is a relationship between preferred food type and the predominant sensory organ used in elasmobranchs 2) Elasmobranchs in different habitats favour different sensory organs. The null hypothesis of this study addresses that there is no link between the predominant sense organs used and elasmobranch feeding ecology.
  • 18. 18 OSX-3000 osu270 2. Methods 2.1. Literature review Web of Science and Google Scholar were used to conduct a thorough literature search of scientific papers on the subject of elasmobranch sensory organs and feeding ecology. Table 1 presents the key terms searched, and all of their differentiations, either individually or in conjunction with each other. Detailed notes were made on any studies which focused on the size/number of or dominance of any of the sensory organs. Papers were also taken from the reference lists of relevant studies. Web of Science was used as a secondary check during the literature search, due to limitations as literature was only dated as far back as 1970. Also this platform, unlike Google Scholar, does not search grey literature. Bangor University Scientific library was used to gain access to relevant information in textbooks. These peer reviewed texts gave background knowledge on the anatomy and physiology of each of the sensory systems. Search term Differentiations & related terms Elasmobranch(s) Elasmobranchii, shark(s), ray(s). Sensory organs Sensory, organ(s), sense(s), organ size, dominant, distribution, number. Feeding ecology Ecology, niche(s), feeding apparatus, prey. Photoreception Vision, eye(s), pupil, retina, sight, photoreceptors, pigments. Chemoreception Smell, olfaction, olfactory, taste, nasal opening, olfactory lamellae. Mechanoreception Movement, pressure, lateral line, touch, hearing, sound, ear(s), actual touch, distant touch. Electroreception Magnetoreception, ampullae of Lorenzini, ampullae, pores, electric, electricity, bioelectric, navigation. Table 1. Key terms used in primary searches on Web of Science and Google Scholar. Differentiations of each search term are also shown.
  • 19. 19 OSX-3000 osu270 2.2. Data collection The data for this paper was collected from a variety of scientifically reviewed papers. Studies which investigated a quantitative aspect of one or more senses provided the baseline data set. Several sources were compiled in order to create a new data set for each sensory category. Data was extracted from existing figures in literature using the tool PlotDigitizer (2015). The raw data was then used to compile summary statistics, with standard error, and figures. No restrictions were set when collecting data due to the lack of literature and studies available. This data was used in the analysis of the sensory information with comparisons to elasmobranch feeding and the analysis of their known sensory capabilities. Species information, such as habitat and diet, was collected primarily from FishBase.org and then cross checked against two key papers (FishBase, 2016; Kajiura et al., 2010; Hueter & Cohen, 1991). Diet information was classified by the predominant food group each species consumes, e.g. the food group has to make up 50% or more of the overall diet. Species which did not have a clear predominant food group (>50%) were classified as ‘Generalists’, however their diets mainly consisted of a mixture of teleosts, crustaceans, cephalopods and scavenged meals. For photoreception data, the eye diameter of 29 shark species was collected from three independent studies and averaged, with standard error (±1SE). The depth ranges of each species were obtained from FishBase and were used to determine the habitat classification, based on similar classification system used by Kajiura (et al., 2010). Limited quantitative information was available for chemoreception meaning only one study was used for data collection (Schluessel et al., 2008). The number of lamellae was plotted against two habitat groups as well as the predominant food group, again taken from FishBase. Two large data sets, covering 42 species, were used for the electroreception results. The numbers of pores for each species was plotted against its predominant habitat. This data was then compared against eye diameter and then food group. The data collected during the literature search was used to compare each sensory system with either habitat or predominant food group. This can be then used to discuss how feeding ecology can affect the senses of elasmobranchs.
  • 20. 20 OSX-3000 osu270 3. Results & Analysis 3.1. Photoreception The average eye diameter of 29 shark species found that deepwater species had larger eyes, as a percentage of their total body length, than pelagic species (Figure 6). No difference was observed between the two pelagic groups. Relevant studies also found that deepwater species had variations in other aspects of their eye anatomy, such as pupil size and shape, lens diameter and densities of photoreceptors (Kajiura et al., 2010). This data was then grouped and averaged for each habitat classification (Figure 7). Standard error analysis supported the outcome that there was no significant difference between eye size for species classified as coastal benthic, coastal pelagic and oceanic pelagic. Deepwater species were classified as living predominantly below 1000m, with the deepest species in this study being the velvet dogfish (Zameus squamulosus) found at 2200m. Figure 6. Average eye diameter (as % of total length) for each species, grouped by environmental classification. Deepwater species (open triangles) have larger eyes than sharks in other habitats, in particular pelagic species (closed circle and squares). Data taken from (Kajiura et al., 2010; Hueter & Cohen, 1991; Gilbert, 1963). Data taken from Kajiura, 2001. 0 0.5 1 1.5 2 2.5 3 3.5 4 4.5 5 Parmaturusxaniurus Heptranchiasperlo Etmopterusbaxteri Etmopteruslucifer Etmopteruspusillus Zameussquamulosus Apristurusbrunneus Squalusacanthias Ginglymostonacirrtum Triakissemifasciata Negaprionbrevirostris Carcharhinusbrevipinna Carcharhinusleucas Carcharhinuslimbatus Carcharhinusmelanopterus Carcharhinusobscurus Carcharhinusperezi Carcharhinusplumbeus Galeocerdocuvier Rhizoprionodonterraenovae Eusphyprablochii Sphynalewini Sphynamokarran Sphynatiburo Alopiaspelagicus Alopiassuperciliosus Lamnaditropis Carcharhinusfalciformis Prionaceglauca AverageEyeDiameter(%TL) Species
  • 21. 21 OSX-3000 osu270 0.00 0.50 1.00 1.50 2.00 2.50 3.00 3.50 4.00 Deepwater Coastal benthic Coastal pelagic Oceanic pelagic AverageEyeDiameter(%TL) Habitat 3.2. Chemoreception Counts of olfactory lamellae per rosette of 21 elasmobranch species ranged widely between two habitats, from 231 in the scalloped hammerhead shark (Sphyrna lewini) to 58 in the eastern shovelnose ray (Aptychotrema rostrata). On average, pelagic species had higher lamellae counts than benthic species, supported by statistical analysis (p = 0.0082) (Figure 8). However, when the species were grouped by their food preference a Tukey test showed there were no significant differences between the groups and numbers of lamellae (0.289 ≤ p ≤ 1.00) (Figure 9). The effect differences between the food groups suggest that mollusc eating elasmobranch could have higher counts of lamellae whilst crustacean consuming have the least. A greater sample size would be needed in order to test this to look for a significant result. Schluessel (et al., 2008) sampled the number of lamellae between males and females of three different species as a control study. It was found there was no significant difference between the sexes (Schluessel et al., 2008). Figure 7. Average eye diameter (as % of total length) for each habitat classification (±1SE). Deepwater species have larger eyes than sharks in all other habitats. Data taken from (Kajiura et al., 2010; Hueter & Cohen, 1991; Gilbert, 1963). Data taken from Kajiura, 2001.
  • 22. 22 OSX-3000 osu270 0 10 20 30 40 50 60 70 80 Benthic Pelagic Numberoflamellae Habitat Figure 9. Average number of lamellae (±1SE) per rosette for 21 elasmobranch species with six different food preferences; T = teleost, P = polychaete, C = crustacean, Ce = cephalopod, E = echinoderms, M = molluscs. No significant differences were observed between food groups (p> 0.05). 95% confidence intervals are shown by error bars. Adapted from Schluessel et al., 2008. Figure 8. Average number of lamellae (±1SE) per rosette for 9 benthic and 12 pelagic elasmobranch species. A significant difference (p=0.008) is observed between the groups with the pelagic group having a higher lamellae count. Adapted from Schluessel et al., 2008.
  • 23. 23 OSX-3000 osu270 0 500 1000 1500 2000 2500 Deepwater Coastal benthic Coastal pelagic Oceanic pelagic AveragePoreNumber Habitat 3.3. Electroreception Pore numbers were taken from 2 independent studies, providing an average for 42 shark species (Figure 11). This data was then grouped and averaged for each of the four habitat classifications. Deepwater species were found to have the lowest numbers of pores (average 838) (Figure 10). However they also possess the widest range of pore numbers, from 2185 on the blackbelly lanternshark (Etmopterus lucifer) to 252 on the frilled shark (Chlamydoselachus anguineus). Coastal pelagic species, found at depths above 200m, were the only group to show a statistically significant difference from the other habitats (p<0.05), and had the highest average pore count (1899) (Figure 10). Species in this habitat were also found to have a more even distribution of pores over the ventral and dorsal surfaces of the head, whereas benthic species had a greater concentration of pores on the ventral surface (Kajiura et al., 2010). Figure 10. Average pore count (±1SE) for each habitat classification. Coastal pelagic species have a higher average pore count than sharks in all other habitats. Data taken from Kajiura et al., 2010; Kalmijn, 1971.
  • 25. 25 OSX-3000 osu270 3.4. Comparative studies The data sets of two senses, photoreception and electroreception, were then combined in order to look for any patterns. Questions behind this section of results focused on if there was a relationship between eye size and average number of pores. Do deepwater species have less ampullae of Lorenzini as their eye sizes were expected to be larger? Or is there no relationship? Does one sense compensate for another in different habitats? These data sets were then combined with habitat classification and food grouping. Firstly, the average eye diameter of 26 shark species were compared against their average pore counts (Figure 12). Deepwater and benthic species (the first six species in Figure 12) generally had larger eye diameters and lower pore counts compared to the other species. All the species belonging to the family (Carcharhinus) had similar counts of both eye size and pore count across the family. The data was then grouped into 6 habitat categories (Figure 13). Again, this supported the theory that deepwater species have a significant difference between eye size and pore count, as shown by the effect size and error bars in Figure 13. Coastal pelagic and Oceanic Pelagic groups show a reversed pattern, where they have larger eyes and lower pore counts in comparison to the other habitat groups. Relationships were again observed when the data was regrouped by predominant food type (Figure 14). Species which preferred to feed on teleost and crustacean prey types were observed to favour eye sight over electroreception compared to species consuming cephalopods. There was no statistically significant difference for ‘generalist species’ between eye size and pore count ratios.
  • 26. 26 OSX-3000 osu270 0.00 0.50 1.00 1.50 2.00 2.50 3.00 3.50 4.00 4.50 5.00 0 500 1000 1500 2000 2500 3000 3500 Etmopterusbaxteri Heptranchiasperlo Parmaturusxaniurus Apristurusbrunneus Triakissemifasciata Rhizoprionodonterranovae Ginglymostonacirrtum Negaprionbrevirostris Galocerdocuvier Squalusacanthias Zameussquamulosus Eusphyprablochii Etmopteruslucifer Carcharhinusplumbeus Carcharhinusmelanopterus Carcharhinusbrevipinna Carcharhinusfalciformis Carcharhinusleucas Carcharhinuslimbatus Carcharhinusobscurus Sphynatiburo Prionaceglauca Alopiassuperciliosus Alopiaspelagicus Sphynamokarran Sphynalewini AverageEyeDiameter(%TL) AveragePoreCount Species Pore Count Average Eye Diameter (%TL) Average Figure 12. Average pore count (bar) and eye diameter (line), as a % of total length, for 26 shark species. For deepwater and benthic species (the first six species) eye diameter, as a percentage, is significantly higher than pore count. These species also show the lowest pore count compared to all other species in this study. Data taken from FishBase, 2016; Kajiura et al., 2010; Kalmijn, 1971; Hueter & Cohen, 1991; Gilbert, 1963).
  • 27. 27 OSX-3000 osu270 0.00 0.50 1.00 1.50 2.00 2.50 3.00 3.50 4.00 4.50 5.00 Teleosts Crustaceans Cephalopod Generalist 0 500 1000 1500 2000 2500 AverageEyeDiameter(%TL) Food Group AveragePoreNumber Pore Count Average Eye Diameter (%TL) Average 0.00 0.50 1.00 1.50 2.00 2.50 3.00 3.50 4.00 4.50 0 500 1000 1500 2000 2500 Deepwater Benthic Coastal benthic Bentho pelagic Coastal pelagic Oceanic pelagic AverageEyeDiameter(%TL) AveragePoreCount Habitat Pore Count Average Eye Diameter (%TL) Average Figure 14. Average pore count (bar) and eye diameter (line), as a % of total length, for 26 shark species grouped by dietary preference (±1SE). Species which predominantly feed on crustaceans favour electroreception as they have larger pore counts than eye diameters. Species consuming cephalopods have the largest eye size across all dietary groups, however this data could be skewed due to a low sample size. Data taken from FishBase, 2016; Kajiura et al., 2010; Kalmijn, 1971; Hueter & Cohen, 1991; Gilbert, 1963). Figure 13. Average pore count (bar) and eye diameter (line), as a % of total length, for 26 shark species grouped by habitat (±1SE). Deepwater species have significantly increased eye diameters than other habitat groups but have low pore counts. Oceanic pelagic, coastal pelagic and coastal benthic groups show the reverse. Data taken from FishBase, 2016; Kajiura et al., 2010; Kalmijn, 1971; Hueter & Cohen, 1991; Gilbert, 1963).
  • 28. 28 OSX-3000 osu270 4. Discussion 4.1. Study Limitations The search terms used in this paper returned a limited selection of quantitative data sets investigating the effects of feeding ecology on the biology of elasmobranch sensory systems. The data that was collected was highly skewed. Very few studies investigated the mechanosensory systems of elasmobranchs, and none produced quantitative data in relation to habitat or dietary groups. Studies into the sense of taste resulted in the same lack of data. Primary literature searches were dominated by studies into vision and the electrosensory systems. A further limitation of the data sets included a lack of information on the sex and age of the species in the studies. This reduces the analytical ability of this paper. There was also an apparent skew of research between the elasmobranch subfamilies. Most of the studies focused on shark species, with only a handful including ray species. None of the studies investigated produced results for skate species. Further work could be undertaken on producing multidisciplinary studies, investigating all elasmobranch senses, across several species, each with different habitats and diets. 4.2. Photoreception For most elasmobranch species, sight is one of the most important senses used when hunting prey. Therefore it is not surprising that it is also one of the most adapted senses. The anatomy of the eye differs, primarily due to different habitats. However it is important to look into habitat adaptations as feeding ecology is not just about what organisms eat but also where they find it. One observed adaptation is the size of the eye and pupil. Deepwater elasmobranchs, found between 1000-4000m, tend to have large eyes with relatively large pupils. This increases sensitivity to light and allows for better location of prey, especially species which emit bioluminescence (Lisney & Collin, 2007). Pelagic species (0-200m), such as the oceanic whitetip (Carcharhinus longimanus), are also found to have large eyes, however the size and shape of the pupil differs. They are able to contract and dilate the muscles around the pupil, controlling the amount of light entering the eye. This is important as these species live in environments with high light levels but also extreme fluctuations of these levels (Gruber & Cohen, 1978). The featureless nature of this environment requires acute eyesight as the shark
  • 29. 29 OSX-3000 osu270 needs to be able to spot prey at large distances (Hueter & Cohen, 1991). Prey species also tend to be active and fast swimming, therefore vision is key for tracking their movements. Benthic species have the smallest eye sizes as a percentage of their total length. Vision is less important for these species as they have the ability to use a wider range of sensory systems. The barren nature of some benthic habitats means there are minimal visual stimuli. Most prey species in this environment bury themselves into the sediment or use camouflage (Schultze, 1866). Therefore vision is not as important as other sensory systems, such as electroreception, when hunting prey. The size of the eyes also differs between elasmobranch subfamilies. Sharks generally have larger eyes than batoids. This again relates to habitat as most ray species are benthic and electroreception plays a larger role in hunting for food in this habitat (Sivak, 1990). The dorsoventrally compressed morphology of batoid bodies has also changed the placement of the eyes. For benthic ray species, like the thornback ray family (Platyrhynidae), the eyes are placed more dorsally on the head compared to pelagic species, such as eagle rays (Myliobatidae), where the eyes are more laterally positioned. Lateral placement allows for a greater field of vision, allowing these species to detect prey in the pelagic environment (Carrier et al., 2012). As discussed previously, all elasmobranchs have evolved a new structural layer inside the eye called the tapedum lucidum. This layer of mirrored cells magnifies the amount of light entering the eye and allows elasmobranchs to see in dim conditions (Heath, 1990). To protect their eyes from rapid changes in light levels, pelagic species have evolved another aspect of their ocular anatomy. They can slide a layer of melanin filled cells, known as the melanoblasts, over the tapedum lucidum to reduce the amount of light reflected within the eye (Gruber & Cohen, 1978). Deep sea species, such as the sixgill shark (Hexanchus griseus), lack this layer and therefore any sudden changes in light conditions could blind them. This restricts these species to living and feeding in habitats with constant low light levels. However, H.griseus have been observed in shallower waters in the summer, but this is due to large algal blooms which reduce the amount of light entering the water column. This temporarily opens up a new foraging habitat for this species (Emde et al., 2004). Studies have been done on the size of the optic tectum in elasmobranchs. The optic tectum is a section of the midbrain which is responsible for the behavioural response to visual stimuli. It can therefore be assumed that species with larger tectum rely heavily on vision (Carrier et al., 2012). A study by Lisney (2004) investigated 29 elasmobranch species and found that on average sharks had larger optic tectum (as a percentage of brain mass) than batoids. Of the
  • 30. 30 OSX-3000 osu270 shark species in the study, the active, pelagic species had larger tectum masses than more sedentary benthic species (Lisney, 2004). This is most likely due to the fast moving nature of pelagic prey. Sedentary elasmobranchs are usually ambush predators and do not need to chase their prey. The size of the optic tectum was also observed to decrease as shark species mature (Lisney & Collin, 2007). This is thought to be due to a shift in sensory dependence in relation to changes in habitat and diet. Juvenile sharks are predominately born into shallow coastal ‘nurseries’ or mangrove environments. During their development in these habitats it is important to have sharp vision to not only catch prey but also avoid predators. As the individual grows it moves out into the open ocean where it becomes more reliant on the other sensory systems to locate food over greater distances (Lisney & Collin, 2007). The pigments within elasmobranch eyes also vary dependant on habitat. Juvenile lemon sharks (Negaprion brevirostris) are most sensitive to the green light end of the visible light spectrum. This is thought to be because they live in the mangroves until they mature, where the light filtering through the foliage leaves the water with a green tinge. This allows for sharper vision in this habitat (Hueter & Cohen, 1991). As they mature and move out into the clearer waters of offshore reefs, the pigments change and become more sensitive to blue wavelengths. As discussed earlier, the ocean gets in blue-green colour from the different absorption rates of wavelengths at different depths (Lisney, 2004). Understanding the role vision plays in the feeding strategies of sharks can be used to prevent shark attacks on humans. Previously, methods using electrical pulses and chemical deterrents have produced little success when trialled in Australia. It is now believed that visual deterrents could be more successful at preventing attacks (Hart & Collin, 2015; Thorson, 1987). It could be as simple as imitating the colour and markings of poisonous species, like the banded sea krait (Laticauda colubrina), found in that environment. This same theory can be applied when creating deterrents to keep sharks away from nets and fishing gear, hopefully reducing the amount of elasmobranchs caught as bycatch (Hart & Collin, 2015). 4.3.Chemoreception Whilst vision is a primary sense used when hunting and catching prey, it has a relatively small signal field. It can be drastically affected by weather related turbulence, light levels and turbidity. Olfaction can pick up signals from several hundred meters away, dependant on water currents.
  • 31. 31 OSX-3000 osu270 The anatomy of the olfactory system varies between species, primarily due to dietary preference. White sharks (Carcharodon carcharias) have the largest olfactory bulbs, relative to body weight, than any other elasmobranch species (Schluessel et al., 2008). The bulbs contain the olfactory lamellae which pick up chemical signals. Larger bulbs suggest a greater dependency on this sensory system. C.carcharias are known to travel large distances in search of whale carcasses using their highly developed olfactory system to guide them. A further reason for large bulb sizes is thought to be because of the high blood volume and strong odours of their primary prey species, pinnipeds. Comparing species with a similar diet to crustacean feeding elasmobranchs, like the lemon shark (N. brevirostris), the size difference between bulbs can be put down to diet (Meredith & Kajiura, 2010). Diet also affects the sensitivity of the system. Different species are attracted to different chemical signals. Some prefer the chemicals within the blood of their prey whilst others are more attracted to the amino acids within the body fluids of their prey (Schluessel et al., 2008). Studies have found that how well adapted the olfactory system is can also depend on habitat. For a pelagic species, such as the oceanic whitetip (C. longimanus), olfaction is the primary sense used. This is mostly likely due to the lack of distinguishable features in the pelagic region and the vast distances this species has to travel in search of food (Meredith & Kajiura, 2010). Tiger sharks (Galeocerdo cuvier) travel between reefs, across the open ocean, to feed on dead or injured migratory turtles using their olfactory system to guide them. This species has the largest proportion of their brains dedicated to smell than any other species (Springer & Gold, 1989). Furthermore, their nares work independently of each other, allowing them to smell in stereo. For more benthic species, like those belonging to the genus Squatina (angel sharks), the olfactory system is not as developed, with reduced number of lamellae and smaller olfactory bulbs. The size of these bulbs changes with age. Just as the optic tectum decreased as a species matures, the olfactory bulbs increase in size and sensitivity with age (Theiss et al., 2009). This suggests that olfaction becomes more important to mature sharks than vision. Again, this is mostly likely to be due to the different habitats juveniles and adults live and feed in. Olfaction however, is not just used when hunting. Sharks and rays produce pheromones to signal their reproductive state and so olfaction is also used to search for potential mates (Carrier et al., 2012). Whilst studies of olfactory lamellae can give an indication as to the sensory ability of the system, their variation in size and shape between species means this method is not fully reliable. Coupling lamellae count data with epithelium surface area provides a better understanding of ability (Schluessel et al., 2008). However, there are limited quantitative
  • 32. 32 OSX-3000 osu270 studies on epithelium surface area, with only a few species having been investigated. Of the species studied it was found that pelagic species, along with having larger olfactory bulbs, also had a greater epithelial surface area than benthic species. This increased surface area increases the ability to detect chemical signals (Schluessel et al., 2008). The structure of the nares also varies dependant on lifestyle. More sedentary benthic species, such as the brownbanded bamboo shark (Chiloscyllium punctatum) and shovelnose ray (Aptychotrema punctatus), have wide rounded nasal openings. This is thought to maximise exposure to the water flow. Fast swimming pelagic species, like the nervous shark (Carcharhinus cautus) and spotted eagle ray (Aetobatus narinari), tend to have either slit like openings or nares that are covered by large flaps in order to reduce the flow rate of water through the nasal opening. This allows them to filter the water at a slower rate so they can pick up any chemical signals and gauge the direction (Meredith & Kajiura, 2010). Whilst the anatomy of the elasmobranch olfactory system is well documented, the relationship between anatomy and ecology is poorly understood. The diversity of this family suggests there could be a wide range of interspecific variation in the importance and function of this sensory system (Theiss et al., 2009). The sense of taste in elasmobranchs is one that has not been quantitatively assessed. This is primarily because this sense does not aid the searching and capturing of prey. Instead, it is used for determining if the prey item, once caught, is worth the energy needed to digest it (Carrier et al., 2012). 4.4. Mechanoreception Elasmobranchs use the pore and canal system in the lateral line to detect waves of pressure generated by predators and prey (Maruska, 2001). This system of canals can be relatively simple or complex and branching, depending on the species and its habitat. In batoids this system is very complex and is mostly likely due to their morphology (Garman, 1888). As they are dorsoventrally compressed they do not have as wide of a field of vision as sharks do. They therefore compensate for this lack of vision with increased sensitivity of the lateral line system. A study by Jordan (2008) investigated these systems in three stingray species, each belonging to a different habitat; bentho-pelagic stingray (Pteroplatytrygon violacea), benthic round stingray (Urolophus halleri) and the pelagic bat ray (Myliobatis californica). It was
  • 33. 33 OSX-3000 osu270 found that in each of these habitats the rays had different anatomical structures of their lateral line systems. U.halleri possessed many non-pored canals which are highly sensitive to skin displacement and direct touch (Maruska & Tricas, 2004). In comparison, the more pelagic species presented a mixture of pored and nonpored canals, with varying levels of branching. M.californica, a highly pelagic species, had the most complex lateral line system with lots of branching pored canals extending to the edge of the pectoral fins (Jordan, 2008). This is beneficial to pelagic species as pored canals allow for an increased sensitivity to the flow of water around them. Benthic species do not need as highly developed canal systems in comparison as they have a wider range of sensory stimuli in the benthic environment. These species also come into direct contact with more objects, such as corals and sediment. Therefore if these species were to have pored canals they would be at an increased risk of the pores becoming clogged with sediment and debris (Maruska & Tricas, 2004). The lateral line system is also known to be able to detect fluctuations in temperature. This may help migratory species, such as the spiny dogfish (Squalus acanthias), follow temperature gradients. In the spring time this species migrates north along the coast of North America to take advantage of spawning salmon and other migratory teleosts. When temperatures start to drop it then migrates back south for the winter (Carrier et al., 2012; Springer & Gold, 1989). With the exception of one study (Maruska, 2001) there is a distinct lack of quantitative, comparative investigations of the lateral line system in elasmobranchs. A common topic of debate amongst sensory shark biologists revolves around ‘is what a shark hears in its inner ears different from the vibrations it picks up in the lateral line system’. Sound is essentially waves of vibrations passed through a medium, and the lateral line system is known to detect vibrations. Therefore, the two systems are often combined and referred to as the acoustico-lateralis system (Corwin, 1978). Field experiments have often demonstrated the sensory capability of the acoustico-lateralis system however none have made links to feeding ecology or habitat preference. It is known that sharks can hear sounds between 10- 800Hz, but show a stronger attraction to low frequency pulsed sounds. This is thought to be because this mimics the sounds distressed prey would emit (Corwin, 1978).
  • 34. 34 OSX-3000 osu270 4.5. Electroreception Like vision, the anatomy of the electrosensory system varies widely between species, habitat and diet affecting the numbers of electrosensory pores and their distributions. Whilst deep water shark species have some of the largest eyes, as a % of their total length, they also have the lowest numbers of ampullae of Lorenzini, however they also present the widest range of pore numbers and distribution. This variation may reflect interspecific differences in feeding strategies. Some species in this habitat feed directly off the benthos and actively search for their food using electroreception, whilst others are ambush predators or scavenge for their food. Others feed on more active prey, e.g. squid, and rely more upon vision and pressure sensors than electrical pores (Murray, 1960). Whilst the numbers of pores for sharks in this habitat are relatively low, the ones they do have are very large epithelial pores. The larger diameter of these pores decreases the electrical impedance along the length of the canal, leading to increased sensitivity to electrical stimuli (Kajiura et al., 2010). Furthermore, the distribution of pores on the body varies with depth. Deepwater species have more pores on their ventral side in comparison to pelagic species. Again, this is due to foraging behaviour as most sharks in this habitat feed off the seabed (Kalmijn, 1988). Dietary preference can also affect the number and distribution of pores. Great hammerheads (Sphyrna mokarran) are known to swing their heads over the benthos in search of the electrical signals given off by stingrays buried in the sediment (Dijkgraaf & Kalmjin, 1962). Qualitative studies have described the complexity of the electrosensory system in skates and believe it to be inversely related to the mobility of their prey. More studies are required to give quantitative evidence for this (Raschi, 1986). Pelagic species are also found have large eye diameters, however their visual ability can be limited by algal blooms and weather related turbulence. Therefore, these species have to rely on other sensory systems to catch their fast moving prey (Kajiura, 2008). They generally have a large number of pores with an even distribution over both the dorsal and ventral side. This makes it easier to detect electrical signals from any direction and aids with magnetoreception / navigation. The ion-rich seawater acts as an electrical conductor. As the water moves over the Earth’s magnetic field lines it generates a weak electrical map of the immediate surroundings which is picked up by the ampullae (Molteno & Kennedy, 2009; Kalmijn, 1982). The sharks can then use this ‘map’ to undergo migratory routes or return to a favourite reef.
  • 35. 35 OSX-3000 osu270 Benthic elasmobranchs were found to have higher pore counts and densities than species in any other habitat. These higher pore densities can be related to a higher electrical sensitivity and therefore a preference for using electroreception (Kajiura, 2001). Batoid species in particular had the highest number of pores out of all of the elasmobranch groups. However, there has been only one published quantitative study to date on this subject (Jordan, 2008). The body morphology of rays and skates and their reduced fields of vision means they rely more heavily on electroreception. They have greater concentrations of pores on the ventral side which they use to scan the benthos in search of food. It was also found that the percentage of fin covered in pores could be linked to swimming style. In active swimming species, like Myliobatis californica, most of their pores are concentrated along the anterior edge of the pectoral fins. This creates a greater search area for this species as their wings move through a large plane (Bedore et al., 2014). It is important to understand the role electroreception has in the feeding strategies of elasmobranchs as this information can be used to create deterrents (Hart & Collin, 2015; Hoenig & Gruber, 1990). Blue shark populations are in decline worldwide caused by high bycatch rates, caught mainly on longline fisheries. It is well documented that this species has a highly developed electrosensory system, used primarily for navigation (Molteno & Kennedy, 2009). Therefore it was believed that attaching magnets to the hooks of longline fisheries could reduce the number of interactions between the sharks and fishing gear. A study by Porsmoguer (et al., 2015) tested two different strengths of magnets in the field during an operational fisheries period. It was discovered that the magnets in fact had an opposite effect than hoped and actually attracted more blue sharks to the lines. However, there have been more successful studies which use an electrical pulse to deter sharks. These have been successfully implemented in coastal swimming areas (Hart & Collin, 2015).
  • 36. 36 OSX-3000 osu270 5. Conclusion As predicted the anatomy of the different sensory systems in elasmobranchs are influenced by feeding ecology. Feeding ecology refers to not only what the individual is feeding upon, but also the habitat in which in hunts. It was found that not only do the different senses adapt to different habitats and dietary preferences but there is also some evidence of compensation. Vision plays more of a role in the location of prey for pelagic elasmobranchs, compared to deep sea species. Because of this, the electrosensory systems do not need to be as developed for these species. Reversely, the electrosensory systems for benthic species have become very complex and sensitive in order to compensate for the reduced number of visual cues. It is still not fully understood how the sensory systems interact with each other and the order in which the systems are used. By investigating the anatomy of these systems and their relationships to ecology we can start to create new methods to protect them. Global shark populations are in decline. Through the creation of man-made deterrents we can start to reduce the amount of elasmobranch caught as bycatch. They can also be used to reduce the risk of attacks on humans, relieving some of the negative media surrounding sharks. There is still a significant lack of quantitative data surrounding all of the elasmobranch sensory systems and their relationships to ecology. Further point of study would be to create more multidisciplinary studies encompassing all of the senses. These studies will need to be carried out on a wider range of elasmobranch species and a range of ages, focusing particularly on batoids where there is a current lack of data. Word Count: 9,919
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