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Sensory Organs and Feeding
Ecology in Elasmobranchs
Jessica Sherlock
School of Ocean Sciences, Bangor University, Menai Bridge,
Anglesey, LL59 5AB, UK.
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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.
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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
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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
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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).
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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).
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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.
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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).
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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
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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
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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.
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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
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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).
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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).
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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).
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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.
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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.
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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.
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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
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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.
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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.
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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.
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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.
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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).
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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
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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
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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.
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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
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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
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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).
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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.
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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).
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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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