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CH 12- Sensory Biology of Elasmobranchs. Exquisite array of sensory systems that aid in: –detecting prey and conspecifics –avoiding predators and obstacles.

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Presentation on theme: "CH 12- Sensory Biology of Elasmobranchs. Exquisite array of sensory systems that aid in: –detecting prey and conspecifics –avoiding predators and obstacles."— Presentation transcript:

1 CH 12- Sensory Biology of Elasmobranchs

2 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

3 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

4 Photoreception –Eyes→→Vision –Pineal Organ→→ Ambient Light Levels –Endolymphatic Duct→→ 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? Mechanoreception –Inner ear→→ Audition (Hearing), Attitude (Yaw, Pitch, Role), Acceleration –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

5 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

6 Photoreception Typical vertebrate eye features: cornea, iris, lens, retina shark eye

7 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

8 Photoreception Nictitating membrane (3 rd eyelid)- covers eye for protection (common in carcharhinids and sphyrinds)


10 Photoreception Some sharks without nictitating membrane (white shark and whale shark) use extraoculor muscles to rotate the entire eye back into the orbit

11 Photoreception In low light conditions, iris muscles contract to dilate the pupils –Many deep sea sharks pupils are permanently dilated kitefin/black shark sixgill shark

12 Photoreception In high light conditions, iris muscles relax and the pupil contracts Pupil contraction can also increase a shark’s visual depth of field nurse sharkhorn shark angel shark

13 Pupil shape Circular –Most deep sea species vertical slit –Carcharhinus spp. –Negaprion brevirostris sixgill sharkblacktip shark

14 Pupil shape horizontal slit –E.g. Sphyrna tiburo oblique slit nurse shark Scyliorhinus canicula

15 Pupil shape U- crescent shaped southern stingray spotted stingray sparsly spotted stingray

16 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)

17 Accomodation Don’t vary lens shape like humans, but change position of lens by moving it toward the retina (distant) or away (near)

18 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)

19 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

20 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.


22 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).

23 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)

24 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

25 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

26 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.

27 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

28 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

29 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.)

30 Mechanosenses Hearing Lateral Line System

31 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.

32 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.


34 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

35 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. 1 st proposed as an important auditory (vibration) detector in sharks by Tester et. al. in 1972

36 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

37 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)

38 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°

39 Training sharks s s YouTube - Training Sharks

40 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

41 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

42 Anatomy Functional unit is the mechanosensory neuromast, a group of sensory cells surrounded by support cells and covered by gelatinous cupula


44 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

45 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)

46 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)

47 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.

48 Specialized mechanoreceptors Spiracular organs Associated w/ 1 st (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.

49 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.

50 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 non- pored canals along the midline and around the mouth.

51 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.

52 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.

53 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

54 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

55 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

56 Rheotaxis Removed neuromasts of port jackson sharks showed a reduced ability to orient upstream in a flume when compared to intact individuals (Peach, 2001)

57 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.

58 Electrosensory

59 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

60 Ampullae of Lorenzini


62 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


64 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

65 Processing Hindbrain Midbrain Thalamus Forebrain > > Major players Minor players

66 Regular discharge pattern even at rest Different charges from species also depends on temperature and age Charges will change during development

67 Battery Powered Decreases discharge energy Increases discharge energy Creates a linear function over a range

68 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


70 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

71 Hammerheads Klimley—1993 –Aggregate around seamounts –Follow routes using magnetic anomalies on sea floor –Suggests naturally occurring geomagnetic fields used to navigate

72 Finding a Friend Sense the fields of their buried counterparts –M–Males try to locate females for mating –F–Females try to locate each other for refuge During mating season, better ‘tuned’ to find each other

73 Olfaction and Chemosensory


75 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

76 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

77 Groove into naris Lamella Close-up Olf. Rosette

78 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

79 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

80 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

81 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

82 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. non- food

83 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.

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