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== History ==
== History ==


In 1678, the Italian physician [[Stefano Lorenzini]] discovered from his dissections of sharks that they possessed organs on their heads now called ampullae of Lorenzini. He published his findings in ''Osservazioni intorno alle torpedini''.<ref>{{cite book |last=Lorenzini |first=Stefano |author-link=Stefano Lorenzini |title=Osservazioni intorno alle torpedini |date=1678 |publisher=Per l'Onofri |location=Florence, Italy |doi=10.5962/bhl.title.6883 |oclc=2900213 }}</ref>
In 1678, the Italian physician [[Stefano Lorenzini]] discovered from his dissections of sharks that they possessed organs on their heads now called ampullae of Lorenzini. He published his findings in ''Osservazioni intorno alle torpedini''.<ref>{{cite book |last=Lorenzini |first=Stefano |author-link=Stefano Lorenzini |title=Osservazioni intorno alle torpedini |date=1678 |publisher=Per l'Onofri |location=Florence, Italy |doi=10.5962/bhl.title.6883 |oclc=2900213 }}</ref> The electroreceptive function of these organs was established by R. W. Murray in 1960.<ref name="Murray_1960">{{cite journal |last=Murray |first=R. W. |title=Electrical sensitivity of the ampullae of Lorenzini |journal=Nature |volume=187 |issue=4741 |pages=957 |date=September 1960 |pmid=13727039 |doi=10.1038/187957a0 |bibcode=1960Natur.187..957M |doi-access=free }}</ref><ref name="Murray_1962">{{cite journal|last=Murray |first=R. W. |title=The response of the ampullae of Lorenzini of elasmobranchs to electrical stimulation |journal=The Journal of Experimental Biology |volume=39 |issue=|pages=119–28 |date=March 1962 |pmid=14477490 |doi=10.1242/jeb.39.1.119 }}</ref>


In 1949, the Ukrainian-British zoologist [[Hans Lissmann]] noticed that the [[Gymnarchus|African knife fish (''Gymnarchus'')]] was able to swim backwards at the same speed and with the same dexterity around obstacles as when it swam forwards, avoiding collisions. He demonstrated in 1950 that the fish was producing a variable electric field, and that the fish reacted to any change in the electric field around it.<ref name=LissmannMachinandfish>{{cite journal |last=Alexander |first=R. McNeill |authorlink=R. McNeill Alexander |title=A new sense for muddy water |journal=Journal of Experimental Biology |volume=2006 209: 200-201; doi: 10.1242/jeb.10.1242/jeb.02012 |issue=2 |pages=200–201 |publisher=The Company of Biologists Limited, Histon (Cambridge) |doi=10.1242/jeb.10.1242/jeb.02012 |year=2006 |pmid=16391343 |doi-access=free }}</ref><ref>[[Hans Lissmann|Lissmann, Hans]]. "[https://www.nature.com/articles/167201a0 Continuous Electrical Signals from the Tail of a Fish, ''Gymnarchus Niloticus'' Cuv]", in: ''[[Nature (journal)|Nature]]'', 167, 4240 (1951), pp. 201–202.
In 1949, the Ukrainian-British zoologist [[Hans Lissmann]] noticed that the [[Gymnarchus|African knife fish (''Gymnarchus'')]] was able to swim backwards at the same speed and with the same dexterity around obstacles as when it swam forwards, avoiding collisions. He demonstrated in 1950 that the fish was producing a variable electric field, and that the fish reacted to any change in the electric field around it.<ref name=LissmannMachinandfish>{{cite journal |last=Alexander |first=R. McNeill |authorlink=R. McNeill Alexander |title=A new sense for muddy water |journal=Journal of Experimental Biology |volume=2006 209: 200-201; doi: 10.1242/jeb.10.1242/jeb.02012 |issue=2 |pages=200–201 |publisher=The Company of Biologists Limited, Histon (Cambridge) |doi=10.1242/jeb.10.1242/jeb.02012 |year=2006 |pmid=16391343 |doi-access=free }}</ref><ref>[[Hans Lissmann|Lissmann, Hans]]. "[https://www.nature.com/articles/167201a0 Continuous Electrical Signals from the Tail of a Fish, ''Gymnarchus Niloticus'' Cuv]", in: ''[[Nature (journal)|Nature]]'', 167, 4240 (1951), pp. 201–202.

Revision as of 19:10, 2 April 2022

Electroreceptors (ampullae of Lorenzini) and lateral line canals in the head of a shark.

Electroreception or electroception is the biological ability to perceive electrical stimuli. It occurs almost exclusively in aquatic or amphibious animals since water is a much better conductor of electricity than air. Exceptions include the monotremes (echidnas and platypuses), cockroaches, and bees. Electroreception is used in electrolocation (detecting objects) and for electrocommunication.

Overview

Electroreception, found mainly in aquatic animals, can be active, involving generation of electric fields, or passive, just sensing external fields. Some electroreceptive fish in different taxonomic groups are also electric, able to generate strong enough shocks to stun or kill prey. The stargazers are electric but not electroreceptive. Most electroreceptive animals are fish, using Ampullae of Lorenzini modified from the sensitive Lateral Line; some amphibians also have these organs. Finally, the Monotreme mammals, the echidnas and the platypus, have electroreceptive organs not homologous with Ampullae of Lorenzini. Not all electroreceptive taxa are shown in the diagram.
The electroreceptive organs of sharks and some other fishes, the ampullae of Lorenzini, are jelly-filled canals connecting pores in the skin to sensory bulbs. They detect small differences in electrical potential between their two ends.

an: ampullary nerve;   ca: capsule;   m: body muscles;   sk: skin

In vertebrates, electroreception is an ancestral trait, meaning that it was present in their last common ancestor.[1] This form of ancestral electroreception is called ampullary electroreception, from the name of the receptive organs, ampullae of Lorenzini. Ampullae of Lorenzini exist in cartilaginous fishes (sharks, rays, and chimaeras), lungfishes, bichirs, coelacanths, sturgeons, paddlefish, aquatic salamanders, and caecilians.[1][2]

Other vertebrates that have electroreception such as gymnotiformes, Mormyridiformes, monotremes, and at least one species of cetacean, have secondarily derived electroreceptive organs, not homologous with ampullae of Lorenzini.[3] Ampullary electroreception is passive, and is used predominantly in predation.[4][5]

Two groups of teleost fishes are weakly electric and engage in active electroreception: the Neotropical knifefishes (Gymnotiformes) and the African elephantfishes (Notopteroidei). The monotremes are mammals capable of electrolocation; they are the four species of terrestrial echidnas, and the semi-aquatic duck-billed platypus. Echidnas have about 2,000 electroreceptors on their bill, while the platypus has around 40,000.[6]

Until recently, electroreception was known only in vertebrates. Recent research has shown that bees can detect the presence and pattern of a static charge on flowers.[7]

Electrolocation

Electroreceptive animals use this sense to locate objects around them. This is important in ecological niches where the animal cannot depend on vision: for example in caves, in murky water and at night. Many fish use electric fields to detect buried prey. Some shark embryos and pups "freeze" when they detect the characteristic electric signal of their predators.[8]

Active electrolocation

Further information: Electric fish

In active electrolocation,[9] the animal senses its surrounding environment by generating electric fields and detecting distortions in these fields using electroreceptor organs. This electric field is generated by means of a specialised electric organ consisting of modified muscle or nerves. This field may be modulated so that its frequency and wave form are unique to the species and sometimes, the individual; if two members of a Gymnotiform species such as the glass knifefish come close together, they both shift their discharge frequencies in a jamming avoidance response.[10] Animals that use active electroreception include the weakly electric fish, which either generate small electrical pulses (termed "pulse-type") or produce a quasi-sinusoidal discharge from the electric organ (termed "wave-type").[11] These fish create a potential usually smaller than one volt (1 V). Weakly electric fish can discriminate between objects with different resistance and capacitance values, which may help in identifying the object. Active electroreception typically has a range of about one body length, though objects with an electrical impedance similar to that of the surrounding water are nearly undetectable.

Active electroreception relies upon tuberous electroreceptors which are sensitive to high frequency (20-20,000 Hz) stimuli. These receptors have a loose plug of epithelial cells which capacitively couples the sensory receptor cells to the external environment. Elephantfish (Mormyridae) from Africa use tuberous receptors known as Knollenorgans to sense electric communication signals.[12]

For the elephantfish (here Gnathonemus) the electric field (cyan) emanates from an electric organ in the tail region (blue rectangle). It is sensed by the electroreceptive skin areas, using two electric pits (foveas) to actively search and inspect objects. Shown are the field distortions created by two different types of objects: a plant that conducts better than water (green) and a non-conducting stone (brown).[13]

Passive electrolocation

See also: Passive electrolocation in fish

In passive electrolocation, the animal senses the weak bioelectric fields generated by other animals and uses it to locate them. These electric fields are generated by all animals due to the activity of their nerves and muscles. A second source of electric fields in fish is the ion pump associated with osmoregulation at the gill membrane. This field is modulated by the opening and closing of the mouth and gill slits.[8][14] Passive electroreception usually relies upon ampullary receptors which are sensitive to low frequency stimuli, below 50 Hz. These receptors have a jelly-filled canal leading from the sensory receptors to the skin surface.

Many fish that prey on electrogenic fish use the discharges of their prey to detect them. This behaviour, "eavesdropping",[15] has been observed in the electroreceptive African sharptooth catfish (Clarias gariepinus) whilst hunting weakly electric Marcusenius macrolepidotus.[16] This has driven the prey to evolve more complex or higher frequency signals that are harder to detect.[17]

Electrocommunication

Main article: Electrocommunication

Weakly electric fish can communicate by modulating the electrical waveform they generate, an ability known as electrocommunication.[18] They may use this for mate attraction and territorial displays. Some species of catfish use their electric discharges only in agonistic displays.

In one genus of bluntnose knifefishes Brachyhypopomus, the electric discharge pattern is similar to the low voltage electrolocative discharge of the electric eel. This is hypothesized to be Batesian mimicry of the powerfully-protected electric eel.[19]

Evolution

Fish with electric organs have evolved eight separate times: twice during the evolution of cartilaginous fishes, creating the electric skates and rays, and six times during the evolution of the bony fishes.[20] One of the cartilaginous fish organs, the Ampulla of Lorenzini, is ancestral to the vertebrate clade, meaning that it is present in all vertebrates unless it has secondarily been lost. Among extant vertebrates, it is found in fishes of all kinds and in some amphibians, but not in reptiles, birds, or mammals.[1]

Taxonomic distribution

Sharks and rays

Sharks and rays (members of the subclass Elasmobranchii), such as the lemon shark, rely heavily on electrolocation in the final stages of their attacks, as can be demonstrated by the robust feeding response elicited by electric fields similar to those of their prey. Sharks are the most electrically sensitive animals known, responding to direct current (DC) fields as low as 5 nV/cm.[21]

Bony fish

The electric eel (actually a knifefish, not an eel), besides its ability to generate high voltage electric shocks,[22] uses lower voltage pulses for navigation and prey detection in its turbid habitat.[23] This ability is shared with other gymnotiformes, which are typically present in murky habitats.

Monotremes

The platypus is a monotreme mammal that uses electroreception.

The monotremes, including the semi-aquatic platypus and the terrestrial echidnas, are the only group of mammals that have evolved electroreception. While the electroreceptors in fish and amphibians evolved from mechanosensory lateral line organs, those of monotremes are based on cutaneous glands innervated by trigeminal nerves. The electroreceptors of monotremes consist of free nerve endings located in the mucous glands of the snout. Among the monotremes, the platypus (Ornithorhynchus anatinus) has the most acute electric sense.[24][25] The platypus has almost 40,000 electroreceptors arranged in a series of stripes along the bill, which probably aids the localisation of prey.[26] The platypus electroreceptive system is highly directional, with the axis of greatest sensitivity pointing outwards and downwards. By making quick head movements called "saccades" when swimming, platypuses constantly expose the most sensitive part of their bill to the stimulus to localise prey as accurately as possible. The platypus appears to use electroreception along with pressure sensors to determine the distance to prey from the delay between the arrival of electrical signals and pressure changes in water.[25]

The electroreceptive capabilities of the four species of echidna are much simpler. Long-beaked echidnas (genus Zaglossus) possess only 2,000 receptors and short-beaked echidnas (Tachyglossus aculeatus) have merely 400 concentrated in the tip of the snout.[26] This difference can be attributed to their habitat and feeding methods. Western long-beaked echidnas live in wet tropical forests where they feed on earthworms in damp leaf litter, so their habitat is probably favourable to the reception of electrical signals. Contrary to this is the varied but generally more arid habitat of their short-beaked relative which feeds primarily on termites and ants in nests; the humidity in these nests presumably allows electroreception to be used in hunting for buried prey, particularly after rains.[27] Experiments have shown that echidnas can be trained to respond to weak electric fields in water and moist soil. The electric sense of the echidna is hypothesised to be an evolutionary remnant from a platypus-like ancestor.[25]

Dolphins

Dolphins have evolved electroreception in structures different from those of fish, amphibians and monotremes. The hairless vibrissal crypts on the rostrum of the Guiana dolphin (Sotalia guianensis), originally associated with mammalian whiskers, are capable of electroreception as low as 4.8 μV/cm, sufficient to detect small fish. This is comparable to the sensitivity of electroreceptors in the platypus.[28] To date (June 2013), these cells have been described from only a single dolphin specimen.

Bees

Bees collect a positive static charge while flying through the air. When a bee visits a flower, the charge deposited on the flower leaks over time into the ground. Bees can detect both the presence and the pattern of electric fields on flowers, and use this information to know if a flower has been recently visited by another bee and is likely to have a reduced concentration of nectar.[7] Bees detect electric fields through insulating air by mechano-reception, not electroreception. Bees sense the electric field changes via the Johnston's organs in their antennae and possibly other mechano-receptors. They distinguish different temporal patterns and learn them. During the waggle dance, honeybees appear to use the electric field emanating from the dancing bee for distance communication.[29][30]

History

In 1678, the Italian physician Stefano Lorenzini discovered from his dissections of sharks that they possessed organs on their heads now called ampullae of Lorenzini. He published his findings in Osservazioni intorno alle torpedini.[31] The electroreceptive function of these organs was established by R. W. Murray in 1960.[32][33]

In 1949, the Ukrainian-British zoologist Hans Lissmann noticed that the African knife fish (Gymnarchus) was able to swim backwards at the same speed and with the same dexterity around obstacles as when it swam forwards, avoiding collisions. He demonstrated in 1950 that the fish was producing a variable electric field, and that the fish reacted to any change in the electric field around it.[34][35]

See also

References

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  14. ^ Bodznick, D.; Montgomery, J. C.; Bradley, D. J. (1992). "Suppression of Common Mode Signals Within the Electrosensory System of the Little Skate Raja erinacea" (PDF). Journal of Experimental Biology. 171 (Pt 1): 107–125. doi:10.1242/jeb.171.1.107.
  15. ^ Falk, Jay J.; ter Hofstede, Hannah M.; Jones, Patricia L.; Dixon, Marjorie M.; Faure, Paul A.; Kalko, Elisabeth K. V.; Page, Rachel A. (2015-06-07). "Sensory-based niche partitioning in a multiple predator–multiple prey community". Proceedings of the Royal Society B: Biological Sciences. 282 (1808). doi:10.1098/rspb.2015.0520. ISSN 0962-8452. PMC 4455811. PMID 25994677.
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  20. ^ Kirschbaum, Frank (2019). Structure and Function of Electric Organs. Boca Raton, Florida: CRC Press. pp. 75–87. doi:10.1201/9780429113581-5. {{cite book}}: |work= ignored (help)CS1 maint: date and year (link)
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  28. ^ Czech-Damal, N. U.; Liebschner, A.; Miersch, L.; et al. (2012). "Electroreception in the Guiana dolphin (Sotalia guianensis)". Proceedings of the Royal Society B. 279 (1729): 663–668. doi:10.1098/rspb.2011.1127. PMC 3248726. PMID 21795271.
  29. ^ Greggers, U.; Koch, G.; Schmidt, V.; et al. (2013). "Reception and learning of electric fields". Proceedings of the Royal Society B. 280 (1759): 1471–2954. doi:10.1098/rspb.2013.0528. PMC 3619523. PMID 23536603. 20130528.
  30. ^ Greggers, U. "ESF in bees". Free University Berlin.
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  32. ^ Murray, R. W. (September 1960). "Electrical sensitivity of the ampullae of Lorenzini". Nature. 187 (4741): 957. Bibcode:1960Natur.187..957M. doi:10.1038/187957a0. PMID 13727039.
  33. ^ Murray, R. W. (March 1962). "The response of the ampullae of Lorenzini of elasmobranchs to electrical stimulation". The Journal of Experimental Biology. 39: 119–28. doi:10.1242/jeb.39.1.119. PMID 14477490.
  34. ^ Alexander, R. McNeill (2006). "A new sense for muddy water". Journal of Experimental Biology. 2006 209: 200-201, doi: 10.1242/jeb.10.1242/jeb.02012 (2). The Company of Biologists Limited, Histon (Cambridge): 200–201. doi:10.1242/jeb.10.1242/jeb.02012. PMID 16391343.
  35. ^ Lissmann, Hans. "Continuous Electrical Signals from the Tail of a Fish, Gymnarchus Niloticus Cuv", in: Nature, 167, 4240 (1951), pp. 201–202.

Further reading

External links

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