CH 12- Sensory Biology of Elasmobranchs

CH 12- Sensory Biology of
Elasmobranchs
• Exquisite array of sensory systems that
aid in:
– detecting prey and conspecifics
– avoiding predators and obstacles
– orienting in the sea
• Sensory performance can be scaled in 2
general ways:
– Sensitivity
– Acuity
Range of sensory organs
Sound--distances of a couple of
miles
Smell--distances of several football
fields
Lateral line--distances of several
football fields
Vision--distances of dozens of feet
Amp. of Lorenzini--distances of
several feet
Touch & taste--contact
• Photoreception
• Mechanoreception
– Eyes→→Vision
– Inner ear→→ Audition
– Pineal Organ→→
(Hearing),
Ambient Light Levels
Attitude (Yaw, Pitch, Role),
– Endolymphatic Duct→→
Acceleration
Ambient Light Levels
• Electroreception
– Ampullae of Lorenzini→→
Ambient electrical fields,
Temperature
• Chemoreception
– Nasal lamellae→→
Olfaction (Smell)
– Taste buds→→ Gustation
(Taste)
– Pit organs (free
neuromasts)→→
Gustation?
– Lateral line →→Ambient
vibrations
– Spiracular organ→→
Ambient vibrations
– Touch receptors→→
Pressure, Pain, Heat
– Proprioceptors→→ Muscle
tension,
Stomach distension,
Fin position, etc.
– Hair cells→→ Ambient
vibrations
How many senses do sharks have?
Humans- 5 senses, 3 if
grouped by
fundamental
mechanism
• Photoreception
(vision)
• Chemoreception
(smell and taste)
• Mechanoreception
(touch and hearing)
• Sharks- 6-13?, 4 if
grouped by
fundamental
mechanism. Our 5
plus electroreception
Photoreception
• Typical vertebrate eye features: cornea,
iris, lens, retina
shark eye
Photoreception
• Laterally placed eyes allow ~360° visual
field
• Blind areas in front of snout or behind
head when still, size of blind area varies
• Upper and lower eyelids don’t cover entire
eyeball in most elasmo’s; relatively
immobile
• Benthic shark species (orectolobidae)
have more mobile eyelids
Photoreception
• Nictitating membrane (3rd eyelid)- covers
eye for protection (common in
carcharhinids and sphyrinds)
Photoreception
• Some sharks without nictitating membrane
(white shark and whale shark) use
extraoculor muscles to rotate the entire
eye back into the orbit
Photoreception
• In low light conditions, iris muscles
contract to dilate the pupils
– Many deep sea sharks pupils are permanently
dilated
sixgill shark
kitefin/black shark
Photoreception
• In high light conditions, iris muscles relax
and the pupil contracts
• Pupil contraction can also increase a
shark’s visual depth of field
horn shark
nurse shark
angel shark
Pupil shape
• Circular
• vertical slit
– Most deep sea
species
– Carcharhinus spp.
– Negaprion brevirostris
sixgill shark
blacktip shark
Pupil shape
• horizontal slit
• oblique slit
– E.g. Sphyrna tiburo
nurse shark
Scyliorhinus canicula
Pupil shape
• U- crescent shaped
southern stingray
sparsly spotted stingray
spotted stingray
Photoreception
• Some elasmo lenses contain yellowish
pigments that are enzymatically formed
oxidation products of tryptophan
• Filters near-UV light and helps to:
• minimize chromatic aberration
• enhance contrast sensitivity
• reduce light scatter and glare
• Pigments have been found in sandbar
shark, dusky shark, and tiger shark but not
lemon or nurse (Zigman 1991)
Accomodation
• Don’t vary lens shape like humans, but
change position of lens by moving it
toward the retina (distant) or away (near)
Photoreception
• Most sharks thought to be hyperopic (farsighted)
• Hueter of UF has recently shown that restraining
sharks may cause them to contract their lenses
giving a false impression of farsightedness
• By bouncing beams of infrared light off the retina
of free-swimming juvenile lemon sharks Hueter
was able to demonstrate that the sharks were
able to focus on both near and distant objects
• It is possible that many elasmo’s are emmetropic
(neither near nor far sighted)
Choroid
• The only vascularized tissue within the
adult elasmo eye
• Contains specialized reflective layer
known as the tapetum lucidum
– layer of cells covered in a guanine-like
crystalline substance
Tapetum lucidum
• During daylight, special cells called
melanoblasts slide from the base of each
of the plates, covering it completely.
• During dark or poorly illuminated
conditions, the melanoblasts are drawn
back, exposing the silvery plates (tapetum
lucidum
• Acts as a kind of mirror to reflect light that
would otherwise pass through the retina
(and be lost) back into the eye.
• Improves vision in low light conditions.
Cones
• Cone photoreceptors described in retina of
catsharks (Scyliorhinus spp.; Neumayer,
1897) and dogfish (Mustelus canis;
Schaper, 1899)
• Largely overlooked until Gruber et
al. (1963) described cones in the retina of
the lemon shark (Negaprion brevirostris).
Rods & Cones
• Almost all elasmobranch species studied to date
have duplex retinae w/ rod & cone
photoreceptors
-the density of cones varies between species,
rod dominated (Gruber, 1975)
-Rod to cone ratio ~ 4:13 in lamnid and
carcharhinid sharks (Grueber 1978)
-peak rod to cone ratios range from:
- ~3:1 in the Atlantic stingray Dasyatis sabina
(Logiudice and Laird, 1994)
- 40:1 in the southern fiddler ray Trygonorhina
fasciata (Braekevelt, 1992)
- >100:1 in the smooth dogfish Mustelus canis
(Stell and Witkovsky, 1973)
Cones
• Only elasmo’s that appear to have no
cone photoreceptors are skates [Raja
(Leucoraja) ocellata and L. erinacea] that
are reported to possess only rods (Ripps
and Dowling, 1991)
– Rods appear to have conelike functions under
certain photic conditions
Cones
• At present, it is not known whether
elasmobranchs have color vision
• However, elasmo’s share niches with
teleost fish, turtles and invertebrates that
are known to employ color vision and it
would be surprising if at least some
elasmobranch species did not share this
visual ability
Hart, Lisney, Marshall, & Collin (2004)
• Using microspectrophotometry, study showed
that the retinae of the giant shovelnose ray
(Rhinobatos typus) and the eastern shovelnose
ray (Aptychotrema rostrata) contain three
spectrally distinct cone visual pigments.
• The presence of multiple cone types raises the
possibility that these species have the potential
for trichromatic colour vision, a visual ability
traditionally thought to be lacking from
elasmobranchs.
Visual pigments
• Present in both rods and cones, absorb
photons
• Proteins linked to pigment carrying
substance:
– Rhodopsins - sensitive to blue-green light
– Chrysopsins-sensitive to deep-blue light
– Porphyropsins- sensitive to yellow-red light
Cohen et al. (1990)
• Found visual pigment change in lemon
shark (Negaprion brevirostris)
– Juvenille had porphyropsin (yellow-red light)
– Adult had rhodopsin (blue green
• Visual adaptation matched habitat shift
Photoreception
• Some elasmo’s found to have retinal ares of higher
cone/ganglion cell density
• Horizontal visual streaks with higher cell densities
adaptation of 2-D terrain (bottom or surface)
– horn shark (Peterson and Rowe, 1980)
– lemon shark (Hueter, 1991)
– small-spotted catfish and tiger shark (Bozzano and Collin, 2000)
• Concentric retinal areas more for imaging a limited spot
in visual field (3-D envmt.)
Mechanosenses
• Hearing
• Lateral Line System
Hearing
• Sound moves through water about four
times faster than through air, and lower
frequencies can travel longer distances
than high ones.
• Sharks hearing functions optimally in the
low frequency range around 100 Hz
where, for example, oscillations are
generated by injured fish.
Hearing
• A shark’s two hearing organs are located
directly over and behind the eyes,
embedded in the skull cartilage.
• Each is connected externally only by an
endolymphatic duct which ends in a tiny
pore on top of the head.
Inner Ear Anatomy
• 3 semicircular canals used to sense
angular acceleration, not known to be
involved in sound perception
•Saccule,
lagena, and
utricle thought
to be involved
in both
balance and
sound
perception
Macula Neglecta
• Inside the endolymphatic pores are the
endolymphatic ducts which lead to the
macula neglecta and a series of
semicircular canals with which sharks
hear.
• 1st proposed as an important auditory
(vibration) detector in sharks by Tester et.
al. in 1972
Macula Neglecta
• Consists of one patch of sensory hair cells
in rays, two patches in carcharhinids
– hair cells show variety of orientation in rays
• hair cells added during growth (Corwin 1983)
• sex differences found, females have more
• Hair cells oriented in opposite directions in
carcharhinids
Pressure Sensitivity
• Isolated preps of dogfish, S. canicula, have
shown hair cells responding to changes in
pressure (Fraser and Shelmerdine, 2002)
– ↑ pressure led to ↑spiked rates in response to
oscillation at 1 Hz
• Shows that sharks have a sensor that could be
used to sense depth and atm. pressure (more
studies need to be done)
• Blacktip reef sharks, C. limbatus, behaviorally
respond to decreases in atm. pressure
accociated with tropical stroms (Heupel at al.
2003)
Behavior
• Studies by Nelson & Grueber (1963) and
Myrberg et al. (1972) have shown that
sharks can be attracted with low-frequency
sounds in the field.
• Shows that sharks have the ability to
localize a sound source.
– Lemon shark has shown ability to localize a
sound source to ~10°
Training sharks
• http://youtube.com/watch?v=Mbz1Caiq1Y
s
• YouTube - Training Sharks
Lateral Line
• Importance of detecting water movements:
– Small scale flows reveal location of prey,
predators, & conspecifics during social
behaviors
– Large scale flows (tidal currents) provide
information important for orientation and
navigation
Types of mechanosensory end organs:
• Classified by morphology and location:
– superficial neuromasts (pit organs or free
neuromasts)
– pored and nonpored canals
– spiracular organs
– vessicles of Savi
• Spatial distribution determines functional
parameters:
– response, receptive field area, distance range of
system, and which component of water motion
(velocity or acceleration) is encoded
Anatomy
• Functional unit is the mechanosensory
neuromast, a group of sensory cells
surrounded by support cells and covered
by gelatinous cupula
Neromast positions
• Dorsolateral and lateral portions of body
and caudal fin
• Posterior to the mouth (mandibular row)
• Between the pectoral fins (umbilical row)
• Pair anterior to each endolymphatic pore
Neromasts
• Distribution pattern varies among taxa with
one or more neuromast groups absent in
some species
• Neromast number varies from less than 80
per side in spiny dogfish, Squalus
acanthias, to more than 600 per side in the
scalloped hammerhead, Sphyrna lewini.
(Tester and Nelson, 1969)
Neuromast comparison
b. spiny dogfish,
Squalus acanthias,
are few ~ 77 per side
c. nurse shark,
Ginglymostoma
cirratum, are
also few in number
d. bonnethead shark,
Sphyrna tiburo,
are numerous (> 400
per side)
e. scalloped
hammerhead,
Sphyrna lewini, are
more numerous (>
600 per side)
Morphology of lateral line canals
Pored
• In contact w/ water
via pores on skin
surface
• Abundant on dorsal
head of sharks and
dorsal surface of
batoids
Nonpored
• Isolated from the
environment and will
not respond to
pressure differences
• Most common on
ventral surface of
skates and rays. Also
on the head of
sharks.
Specialized mechanoreceptors
Spiracular organs
• Associated w/ 1st
(spiracular) gill cleft
• Consists of
tube/pouch lined w/
sensory neuromasts
and covered by a
cupula
• Found in sharks &
batiods
Vesicles of Savi
• Consists of
neuromasts enclosed
in sub-epidermal
pouches
• Most abundant on
ventral surface of
rostrum
• Thus far, only found in
some batoids
Biological role and function of spiracular organs and
vesicles of Savi remains unclear.
Distribution of the lateral line canal system and
vesicles of Savi on the dorsal (upper) and ventral
(lower) surface of the lesser
electric ray, Narcine brasiliensis. Canals on the
dorsal surface are bilateral, interconnected and
pored, while the ventral surface lacks a
canal system.
Distribution of the lateral line
canal system on the dorsal
(upper) and ventral (lower)
surface of the butterfly ray,
Gymnura micrura. All canals
(except mandibular) are
interconnected both among
and within sides with
extensive tubule branching
on the dorsal surface. The
ventral system consists of
both pored canals, and nonpored canals along the
midline and around the
mouth.
Stimulus and Processing
• Lateral line can only be stimulated within the
inner regions of the near-field (e.g. 1-2 body
lengths of a dipole source)
• Studies indicate the lateral line system is
sensitive to velocities in the μm s‾¹ range and
accelerations in the mm s‾² range
• Water motion stimuli effectively modulate the
spontaneous primary afferent neuron discharges
sent to the mechanosensory processing centers
in the hindbrain.
– provides animal with info. about the frequency,
intensity, and location of the stimulus source.
Stimulus and Processing
• In addition to 11-12 cranial nerves
described in most vertebrates, lateral line
neuromasts are innervated by a distinct
set of nerves.
• Cephalic region is innervated by anterior
lateral line nerve complex.
• Body and tail innervated by posterior
lateral line nerve complex.
Behavior
• Lateral line system in bony fishes is known
to function in: schooling behavior, social
communication, hydrodynamic imaging,
predator avoidance, rheotaxis, and prey
detection.
• Behavior experiments only for prey
detection and rheotaxis in elasmobranchs
Prey detection
• Lateral line system likely plays an
important role in feeding behavior across
elasmobranch taxa.
• Concentration of mechanoreceptors on
cephalic region of sharks and ventral
surface of batiods supports this view.
– aids in detecting, localizing, and capturing
prey
Rheotaxis
• Recent evidence (Montgomery et al.,
1997) shows how neuromasts provide
sensory info. for rheotaxis similar to that
found in teleost.
• Positive rheotaxis may be important to:
– facilitate water flow over the gills
– to help maintain position on the substratum
– to help orient to tidal currents
– to facilitate in prey detection by allowing them
to remain within an odor plume
Rheotaxis
• Removed neuromasts of port jackson
sharks showed a reduced ability to orient
upstream in a flume when compared to
intact individuals (Peach, 2001)
Maruska, 2001
vesicles of Savi do not apply to shark species;
superficial neuromasts are likely not used for prey
detection by benthic feeding batoids; facilitation of
schooling behavior would only apply to those
species of sharks and batoids that are known to
school.
Electrosensory
Ampullary Electroreceptor
• Sensitive to low-frequency stimuli
• Ampullae of Lorenzini
• Temperature gradients detected in voltage
changes
• Used to detect bioelectric fields of prey,
predators, and conspecifics
Ampullae of Lorenzini
Marine vs. Freshwater
• Clusters of 3-6 per
side
• Innervated by 8th
cranial nerve
• Measure drop of field
along length of canal
• Long canals = greater
distance sampled
• Distributed
individually
• Thicker epidermis
• Short canals only
• Smaller ampulla =
micro-/mini-ampulla
Pathways
• DON– dorsal octavolateralis nucleus, in
hindbrain
• AENs—in DON, ascending efferent
neurons, second-orders filter out ‘noise’
• LMN—lateral mesencephalic nucleus,
midbrain
DON -> AEN -> LMN -> Thalamus ->
Forebrain
Processing
•
•
•
•
Hindbrain
Midbrain
Thalamus
Forebrain
>
>
Major players
Minor players
• Regular discharge
pattern even at rest
• Different charges
from species also
depends on
temperature and
age
• Charges will
change during
development
Battery Powered
Decreases
discharge
energy
Creates a linear
function over a
range
Increases
discharge
energy
Prey and Predator Detection
• Used dipoles to
simulate prey
• Did not attack with
dipole covered
• Preferred dipole to
scent
• Egg-encapsulated
skates will stop
ventilating their eggs
in order to stop any
electric discharges
• Only sense frequency
of large predators
Internal Compass
• Thought to be able to estimate drift by
aligning with uniform electrical field (poles
and currents)
• Passive navigation—measures external
voltage gradient
• Active navigation—measures internal
voltage gradient
Hammerheads
• Klimley—1993
– Aggregate around seamounts
– Follow routes using magnetic anomalies on
sea floor
– Suggests naturally occurring geomagnetic
fields used to navigate
Finding a Friend
• Sense the fields of their buried
counterparts
– Males try to locate females for mating
– Females try to locate each other for refuge
• During mating season, better ‘tuned’ to
find each other
Olfaction and Chemosensory
• Circular water movement through nostrils
• Epithelium has bipolar receptor cell with
dendritic knob with microvilli
• Amino acids from prey spark response
• Olfactory bulb—work closely with
epithelium, receives output from axons of
receptors
• Olfactory nerve—fibers, glomeruli, mitral
cells, granular cells
• Lateral hemisphere of brain helps control,
possibly hypothalamus as well
Olfactory Bulb
• Swellings or sub-bulbs that each get input
• Much larger in comparison to other animal
brains
• Size differences between species shows relative
importance of smell
Lamella
Close-up
Olf. Rosette
Groove into naris
Different Studies
• Large Areas of Water
– Would only attack if
only or more nostrils
were open
– Could locate prey
blinded by figure-eight
patterns
– Different methods of
sampling for different
species
• Laboratory
– When studied in circular tanks, more area was
covered in less turns
– Currents create a vector for sharks to follow
– Stagnant water creates a pinpoint of stimuli
Pheromones
• Few pieces of evidence, none direct
• Report of one shark tracking down another
and following second shark with nose
close to vent
• Other accounts spotted unusual swimming
when opposite sex nearby
Predator Avoidance
• Only studied between lemon sharks and American
crocodiles
• Juvenile lemon sharks would become active from tonic
mobility once water sample introduced
• Only samples from habitats where the species have
contact work
Tasty, Tasty
• Majority of taste buds on the roof of the
mouth
– Small papillae with central cluster of receptors
– Nerves associate with bottom of receptors
• Part of final determination of food vs. nonfood
Bibliography
• Carrier, J.C., et. al. 2004. Biology of Sharks and Their
Relatives. CRC Press, Boca Raton, FL. pp. 325-358.
• Hart, N., Lisney. T., Marshall, N., Collin, S. 2004. Multiple
cone visual pigments and the potential for trichromatic color
vision in two species of elasmobranch. The Journal of
Experimental Biology. 207: 4587-4594.
• Hamlett, W. 1999. Sharks, Skates, and Rays: The Biology of
Elasmobranch Fishes. JHU Press. Pg. 311
• Klimley, A.P. 1993. highly directional swimming by scalloped
hammerhead sharks, Sphyrna lewini and subsurface
irradiace, temperature, bathymetry, and geomagnetic field.
Mar. Biol. 117: 1-22.
• Maruska, K. 2001. Morphology of the mechanosensory
lateral line system in elasmobranch fishes: ecological and
behavioral considerations. Environmental Biology of Fishes.
60: 47-75.