Ampullae of Lorenzini

Electroreceptors (ampullae of Lorenzini) and lateral line canals in the head of a shark
Inner view of Ampullae of Lorenzini
Pores with ampullae of Lorenzini in snout of Tiger shark
Ampullae of Lorenzini in a Scyliorhinus canicula

IntroductionEdit

The Ampullae of Lorenzini are special sensing organs called electroreceptors, forming a network of mucus-filled pores. They are mostly found in cartilaginous fish (sharks, rays, and chimaeras); however, they are also found in basal actinopterygians such as reedfish[1] and sturgeon.[2] Lungfish have also been reported to have them.[3] Ampullae were first described by Stefano Lorenzini in 1678. Early in the 20th century, the function of the ampullae was not clearly understood, and electrophysiological experiments suggested a sensibility to temperature, mechanical pressure, and possibly salinity. It was not until 1960 that the ampullae were identified as specialized receptor organs for sensing electric fields.[4][5] The ampullae also allow the shark to detect changes in water temperature. Each ampulla is a bundle of sensory cells containing multiple nerve fibres and a jelly-filled canal opening. These open to the surface by a pore in the skin and end in a cluster of small pockets full of a special jelly-like substance. These fibres are enclosed in a gel-filled tubule which has a direct opening to the surface through a pore. The gel is a glycoprotein-based substance with the same resistivity as seawater, and it has electrical properties similar to a semiconductor.[6] It was discovered that each pore in the skin continues into a gel-filled tube that stops at an alveolus-shaped sensory ending. The ampulla was additionally found to contain sense cells that have a single non-motile cilium. Very small voltages of about <0.05 µV/cm are applied to the openings, causing an alteration in impulse firing which in turn triggers responses in medulla and midbrain. The mucus-like substance inside the tubes was previously thought to serve as a passive electrical conductor, carrying the voltage to sense cells in the alveolus ending.[7] This has been suggested as a mechanism by which temperature changes are transduced into an electrical signal that the shark may use to detect temperature gradients, although it is a subject of debate in scientific literature.[8] These sensory organs help fish to sense electric fields in the water. The ampullae are mostly clustered into groups inside the body, each cluster having ampullae connecting with different parts of the skin, but preserving a left-right symmetry. The canal lengths vary from animal to animal, but the distribution of the pores is generally specific to each species. The ampullae pores are visible as dark spots in the skin. They provide fish with an additional sense capable of detecting electric and magnetic fields as well as temperature gradients.

Electric field sensing abilityEdit

Being able to sense these electric fields is related to a variety of behaviors in the shark's daily lives. The ampullae of Lorenzini has been observed to have many functions, including sensory receptors for touch, pressure, salinity, temperature, electric and magnetic fields.[9] By being able to sense these magnetic and electric fields, the sensory ability also aids the shark's ability to navigate, as well as affecting social behaviors such as mating, avoiding predation[10], and giving them advantages for hunting.[11] The ampullae detect electric fields in the water, or more precisely the potential difference between the voltage at the skin pore and the voltage at the base of the electroreceptor cells.[12] A positive pore stimulus would decrease the rate of nerve activity coming from the electroreceptor cells, and a negative pore stimulus would increase the rate of nerve activity coming from the electroreceptor cells. Each ampulla contains a single layer of cells that contains electrically excitable receptor cells separated by supporting cells. The cells are connected by apical tight junctions so that no current leaks between the cells. The apical faces of the receptor cells have a small surface area with a high concentration of voltage-dependent calcium channels and calcium-activated potassium channels.[13] Because the canal wall has a very high resistance, all of the voltage difference between the pore of the canal and the ampulla is dropped across the receptor epithelium which is about 50 microns thick. Because the basal membranes of the receptor cells have a lower resistance, most of the voltage is dropped across the apical faces which are excitable and are poised at the threshold. Inward calcium current across the receptor cells depolarizes the basal faces causing presynaptic calcium release and release of excitatory transmitter onto the afferent nerve fibers. These calcium-activated potassium channels in the apical membrane aid sensory transduction.[14] One of the first descriptions of calcium-activated potassium channels was based on studies of the ampulla of Lorenzini in the skate. Large conductance calcium-activated potassium channels (BK channels) have recently been demonstrated in the ampulla by cloning. Sharks may be more sensitive to electric fields than any other animal, with a threshold of sensitivity as low as 5 nV/cm. That is 5/1,000,000,000 of a volt measured in a centimeter-long ampulla. It has also been noted that the collagen jelly that fills the ampullae canals has one of the highest proton conductivity capabilities of any material created by organisms. Marine cartilaginous fish are shown to have a much higher sensitivity than any freshwater species. Great White Sharks are capable of responding to charges of one-millionth of a volt in water.[15] All living creatures produce an electrical field caused by muscle contractions, and a shark may pick up weak electrical stimuli from the muscle contractions of animals, particularly prey.[16] On the other hand, the electrochemical fields generated by paralyzed prey were sufficient to elicit a feeding attack from sharks and rays in experimental tanks; therefore muscle contractions are not necessary to attract the animals. Sharks and rays can locate prey buried in the sand or DC electric dipoles that simulate the main feature of the electric field of a prey buried in the sand. Any moving conductor, such as seawater, induces an electric field when a magnetic field such as the Earth's is present. The electric fields induced in oceanic currents by the Earth's magnetic field are of the same order of magnitude as the electric fields that sharks and rays are capable of sensing. This could mean that sharks and rays can orient to the electric fields of oceanic currents, and use other sources of electric fields in the ocean for local orientation. Additionally, the electric field they induce in their bodies when swimming in the magnetic field of the Earth may enable them to sense their magnetic heading.

MorphologyEdit

Throughout the species of sharks, skates, and rays there is a wide diversity of morphologies and adaptations. Some of these adaptations permit species to have greater electric field sensing ability in comparison to other species. Among these adaptations are the cephalofoil of hammerhead sharks as well as varied dispersal of pores found across skate bodies for specialized prey detection. Variation in electroreception is due to the great differences in ampullary networks such as pore density, amount, and distribution along the elasmobranch. In recent studies, higher numbers of pores spread along the body has been correlated to lower threshold sensitivity as more pores contributes to a higher volume of sensory information increasing sensitivity.[10]

CephalofoilEdit

Sphyrnid or hammerhead sharks have flattened expanded heads referred to as the cephalofoil. Patterns of the ampullae of Lorenzini on the cephalofoil of sphyrnid sharks can be utilized to differentiate between different species.[17] The cephalofoil has more pores on the ventral surface than most carcharhinid sharks which have an even distribution across the dorsal and ventral sides of the head.[18]

Skates and RaysEdit

Skates, rays, and other Batoids are often characterized by their flat bodies. Due to their body shape with their mouths on their bottom or ventral sides, skates and rays are benthic feeders. The common shovelnose ray possesses six times more ampullary pores on their ventral sides.[19] The greater density of pores on the ventral side or the bottom of skates results in higher sensitivity to electric fields on that side of the body. The information provided to the skate about changes in the electric field influences their feeding and foraging behavior.[20]

Sawfish RostrumEdit

The sawfish is easily identifiable by its long-toothed rostrum (the “saw”) and its flattened shark-like body. Sawfish possess ampullae pores on their head, ventral and dorsal side of their rostrum leading to their gills in addition to pores on the dorsal side of their body. Considered an electroreception specialist, sawfish possess more ampullary pores than any other sharks, skates, or rays.[21]

BehaviorEdit

Morphology and arrangement of the ampullae of Lorenzini impact the behavior and sensing ability of the shark or ray. The ampullae of Lorenzini allow sharks to sense electric and magnetic fields. This capability has resulted in unique displays of behaviors in both sharks and rays. The ability to detect these fields is dependent on head morphology, which can also shape behavior as a result. Behavioral studies comparing scalloped hammerhead and sandbar sharks established that due to scalloped hammerheads possessing a cephalofoil, shark species exhibited different reactions upon detection of an electric dipole field.[22] The scalloped hammerhead exhibited a spiral tracking orientation and bit the device producing the electric field in comparison to the sandbar sharks. Geomagnetic sensing allows for navigational behavior in scalloped hammerheads in which their ability to sense the boundaries of the earth's geomagnetic field. Scalloped hammerheads have been observed utilizing this as a method of navigation in pelagic, open water environments.[23] Having knowledge of the behaviors that are altered accordingly from signals from the ampullae has allowed researchers to make further progress in developing shark deterrents to improve the safety of humans. One example of this that has been recently studied is the Shark Shield Freedom7™ electric deterrent. The device is described as functioning by producing exponentially decaying electrical pulses with an inter-pulse period. Each pulse has a duration of about 1.2 ms and a peak amplitude of about 105 V and the pulses alternate in polarity. The electrical circuitry and batteries of the device are designed to be worn on the ankle of the user, with the center of the two cylindrical electrodes 160 cm from each other.[24]

AnatomyEdit

The Ampullae of Lorenzini contains two compartments, the ampullengang and the endampulle. The ampullengang is a pore on the skin connected by a tubule that is filled with a dense mucous substance. This substance is rich in acid mucopolysaccharides. The endampulle is connected at the base of the tubule of the ampullengang and is made up of vesicular protrusions of groups of sensitive cells. Both compartments contain branches of nerve endings that attach to alveolar bulbs and are held within a single ampullae.[25] Dendrites of the afferent nerve extend from the ampullae to the ampullary tissue and divide into collateral fibers. These fibers spread out over the alveoli to form synaptic terminals and allow for communication with receptor cells.  A collagen sheath covers the ampullae, canal, and nerve ending of the structure.[26]

Pores are generally concentrated at the surface of the skin around the snout and mouth of sharks and rays. They are also densely distributed on the anterior nasal flap, barbel, circumnarial fold and lower labial furrow.[27] The anatomical arrangements and specifications can differ depending on the ecological niche of the species and what mechanisms better serve them in their environment. Canal size typically corresponds to the body size of the animal but the number of ampullae remains the same. The canals of the ampullae of Lorenzini can be pored or non-pored. Non-pored canals do not interact with external fluid movement but serve a function as a tactile receptor to prevent interferences with foreign particles.[27]

Alternative sensory informationEdit

There is increasing evidence that the ampullae of Lorenzini also contribute to the ability to receive geomagnetic information. As magnetic and electrical fields are very closely related, magnetoreception via the ampullae of Lorenzini has been a relatively newer process being studied. Many elasmobranchs have shown a positive response to artificially generated magnetic fields in association with food rewards demonstrating their magnetoreception sensitivity. The results demonstrate the possibility of magnetoreception as an explanation for sharks and ray’s ability to form strict migratory patterns and identify geographic location.[28] As elasmobranchs swim in the electrically conductive water it creates a detectable voltage difference across the electroreceptors. The local geomagnetic magnitude, vectors, and swimming angle gives the necessary information to have a sense of geographic location and direction as they swim. This would allow for the formation of a bicoordinate geomagnetic map of earth. There is still debate if there are specific magnetoreceptive cells that have yet to be identified that receive this information, but the main hypothesis is indirect sensing by the ampullae of Lorenzini.

The ampullae of Lorenzini are not just organs strictly dedicated to foraging for food. They also play an important role in the reproductive process and promote the ability to find possible mates. Some batoid species of elasmobranchs utilize diurnal visual crypsis which makes it difficult to find mates.[10] The electrical field information that is given off is the same between sexes, however, when mating season approaches males undergo spermatogenesis and increased hormone activity. This changes the resting discharge rate, increasing electroreception sensitivity to lower frequency stimuli. As a result, males increase metabolic costs in order to change their electrosensory system and to ultimately find mates instead of prey. The ampullae of Lorenzini also help adolescent and vulnerable elasmobranchs avoid predation through electroreception. Many of the smaller cartilaginous fish have more pores on the dorsal and posterior part of their body than larger sharks whose ampullary system is denser at the front around the head and mouth. The high pore density around the head and mouth correlate to the foraging needs of large cartilaginous fish. Pore distribution on the dorsal side and posterior end of smaller elasmobranchs relates to predator evasion and spatial awareness.[10]

HistoryEdit

Early in the 20th century, the function of the ampullae was not clearly understood, and electrophysiological experiments suggested a sensibility to temperature, mechanical pressure and possibly salinity. It was not until 1960 that the ampullae were clearly identified as specialized receptor organs for sensing electric fields.[29][30] The ampullae may also allow the shark to detect changes in water temperature. Each ampulla is a bundle of sensory cells containing multiple nerve fibres. These fibres are enclosed in a gel-filled tubule which has a direct opening to the surface through a pore. The gel is a glycoprotein-based substance with the same resistivity as seawater, and it has electrical properties similar to a semiconductor.[31] This has been suggested as a mechanism by which temperature changes are transduced into an electrical signal that the shark may use to detect temperature gradients, although it is a subject of debate in scientific literature.[32][33]

Material PropertiesEdit

The hydrogel, which contains keratan sulfate in 97% water, has a conductivity of about 1.8 mS/cm, the highest known amongst biological materials.[34] [non-primary source needed]

See alsoEdit

ReferencesEdit

  1. ^ Roth A, Tscharntke H (October 1976). "Ultrastructure of the ampullary electroreceptors in lungfish and Brachiopterygii". Cell Tissue Res. 173 (1): 95–108. doi:10.1007/bf00219268. PMID 991235.
  2. ^ Gibbs MA, Northcutt RG (2004). "Development of the lateral line system in the shovelnose sturgeon". Brain Behav. Evol. 64 (2): 70–84. doi:10.1159/000079117. PMID 15205543.
  3. ^ Roth A, Tscharntke H (October 1976). "Ultrastructure of the ampullary electroreceptors in lungfish and Brachiopterygii". Cell Tissue Res. 173 (1): 95–108. doi:10.1007/bf00219268. PMID 991235.
  4. ^ Murray RW (1960). "The Response of the Ampullae of Lorenzini of Elasmobranchs to Mechanical Stimulation". J Exp Biol. 37: 417–424.
  5. ^ Murray RW (1960)."Electrical sensitivity of the ampullae of Lorenzini". Nature. 187 (4741): 957. doi:10.1038/187957a0.
  6. ^ Fields, RD, Fields, KD, Fields, MC (2007. "Semiconductor gel in shark sense organs?". Neurosci. Lett. 426 (3): 166–170. doi:10.1016/j.neulet.2007.08.064. PMC 2211453. PMID 17904741.
  7. ^ Fields, RD, Fields, KD, Fields, MC (2007). "Semiconductor gel in shark sense organs?". Neurosci. Lett. 426 (3): 166–170. doi:10.1016/j.neulet.2007.08.064. PMC 2211453. PMID 17904741.
  8. ^ Brown BR (2010). "Temperature response in electrosensors and thermal voltages in electrolytes". J Biol Phys. 36 (2): 121–134. doi:10.1007/s10867-009-9174-8. PMC 2825305. PMID 19760113.
  9. ^ Fields, RD, Fields, KD, Fields, MC (2007). "Semiconductor gel in shark sense organs?". Neurosci. Lett. 426 (3): 166–170. doi:10.1016/j.neulet.2007.08.064. PMC 2211453. PMID 17904741.
  10. ^ a b c d Newton, Kyle C.; Gill, Andrew B.; Kajiura, Stephen M. (2019). "Electroreception in marine fishes: chondrichthyans". Journal of Fish Biology. 95 (1): 135–154. doi:10.1111/jfb.14068. ISSN 1095-8649.
  11. ^ Fields, R. Douglas (August 2007). "The Shark's Electric Sense" (PDF). Scientific American. Retrieved 2 December 2013.
  12. ^ Benedict King, John Long. "How sharks and other animals evolved electroreception to find their prey". Phys Org. Retrieved 13 February 2018.
  13. ^ Clusin, WT; Bennett, MV (February 1977). "Calcium-activated conductance in skate electroreceptors: current clamp experiments". The Journal of General Physiology. 69 (2): 121–43. doi:10.1085/jgp.69.2.121. PMC 2215012. PMID 190338.
  14. ^ Bellono, N, Leitch, D, Julius, D (2018). “Molecular tuning of electroreception in sharks and skates”. Nature. 558: 1222-126. doi: 10.1038/s41586-018-0160-9
  15. ^ Benedict King, John Long. "How sharks and other animals evolved electroreception to find their prey". Phys Org. Retrieved 13 February 2018.
  16. ^ Fields, R. Douglas (August 2007). "The Shark's Electric Sense" (PDF). Scientific American. Retrieved 2 December 2013.
  17. ^ Mello, W (2009). “The electrosensorial pore system of the cephalofoil in the four most common species of hammerhead shark (Elasmobranchii: Sphyrnidae) from the Southwestern Atlantic”. Competes reduc biologies. 332 (4): 404-412. doi: 10.1016/j.crvi.2008.11.003
  18. ^ Mello, W (2009). “The electrosensorial pore system of the cephalofoil in the four most common species of hammerhead shark (Elasmobranchii: Sphyrnidae) from the Southwestern Atlantic”. Competes reduc biologies. 332 (4): 404-412. doi: 10.1016/j.crvi.2008.11.003
  19. ^ Wueringer, BE, Tibbets, IR, (2008). “Comparison of the lateral line and ampullary systems of two species of shovelnose ray”. Reviews in Fish Biology and Fisheries. 18 (1): 47-64 doi: 10.1007/s11160-007-9063-9
  20. ^ Tricas, TC, (2001). “The neuroecology of the elasmobranch electrosensory world: why peripheral morphology shapes behavior”. The behavior and sensory biology of elasmobranch fishes: an anthology in memory of Donald Richard Nelson. 77-92 doi: 0.1007/978-94-017-3245-1_6
  21. ^ Wueringer, BE, Peverell, SC, Seymour, JE, Squire, LJ, Kajiura, SM, (2011). “Sensory systems in sawfishes: Part 1 the ampullae of Lorenzini”. Brain Behavior Ecology. 78: 139-149 doi: 10.1159/000329515 The electrosensitive rostrum of sawfish is believed to be utilized to search for food and stun prey.
  22. ^ Mello, W (2009). “The electrosensorial pore system of the cephalofoil in the four most common species of hammerhead shark (Elasmobranchii: Sphyrnidae) from the Southwestern Atlantic”. Competes reduc biologies. 332 (4): 404-412. doi: 10.1016/j.crvi.2008.11.003
  23. ^ Klimey, AP, (1993). “Highly directional swimming by scalloped hammerhead sharks, Sphyrna lewini, and subsurface irradiance, temperature, bathymetry, and geomagnetic field”. Marine Biology. 117 (1): 1-22 doi: 10.1007/BF00346421
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  25. ^ Fishelson, Lev; Baranes, Avi (1998). "Distribution, morphology, and cytology of ampullae of Lorenzini in the Oman shark, Iago omanensis (Triakidae), from the Gulf of Aqaba, Red Sea". The Anatomical Record. 251 (4): 417–430. doi:10.1002/(SICI)1097-0185(199808)251:43.0.CO;2-P. ISSN 1097-0185.
  26. ^ Wueringer, Barbara E.; Tibbetts, Ian R.; Whitehead, Darryl L. (2009-02-01). "Ultrastructure of the ampullae of Lorenzini of Aptychotrema rostrata (Rhinobatidae)". Zoomorphology. 128 (1): 45–52. doi:10.1007/s00435-008-0073-5. ISSN 1432-234X.
  27. ^ a b Winther-Janson, Marit; Wueringer, Barbara E.; Seymour, Jamie E. (2012-11-30). "Electroreceptive and Mechanoreceptive Anatomical Specialisations in the Epaulette Shark (Hemiscyllium ocellatum)". PLOS ONE. 7 (11): e49857. doi:10.1371/journal.pone.0049857. ISSN 1932-6203. PMC 3511481. PMID 23226226.CS1 maint: PMC format (link)
  28. ^ Newton, Kyle C.; Kajiura, Stephen M. (2020-09-29). "The yellow stingray (Urobatis jamaicensis) can discriminate the geomagnetic cues necessary for a bicoordinate magnetic map". Marine Biology. 167 (10): 151. doi:10.1007/s00227-020-03763-1. ISSN 1432-1793.
  29. ^ Murray RW (1960). "The Response of the Ampullae of Lorenzini of Elasmobranchs to Mechanical Stimulation". J Exp Biol. 37: 417–424.
  30. ^ Murray RW (1960). "Electrical sensitivity of the ampullae of Lorenzini". Nature. 187 (4741): 957. doi:10.1038/187957a0.
  31. ^ Brown BR (2003). "Sensing temperature without ion channels". Nature. 421 (6922): 495. doi:10.1038/421495a. PMID 12556879.
  32. ^ Fields, RD, Fields, KD, Fields, MC (2007). "Semiconductor gel in shark sense organs?". Neurosci. Lett. 426 (3): 166–170. doi:10.1016/j.neulet.2007.08.064. PMC 2211453. PMID 17904741.
  33. ^ Brown BR (2010). "Temperature response in electrosensors and thermal voltages in electrolytes". J Biol Phys. 36 (2): 121–134. doi:10.1007/s10867-009-9174-8. PMC 2825305. PMID 19760113.
  34. ^ Bellono, N, Leitch, D, Julius, D (2018). “Molecular tuning of electroreception in sharks and skates”. Nature. 558: 1222-126. doi: 10.1038/s41586-018-0160-9

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