Electroreception

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The electroreceptive ampullae of Lorenzini (red dots) evolved from the mechanosensory lateral line organs (gray lines) of early vertebrates. They are seen here in the head of a shark. Electroreceptors in a sharks head.svg
The electroreceptive ampullae of Lorenzini (red dots) evolved from the mechanosensory lateral line organs (gray lines) of early vertebrates. They are seen here in the head of a shark.

Electroreception 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. Electroreception is used in passive electrolocation, detecting objects such as prey by sensing the electric fields they create, and in active electrolocation, generating a weak electric field and sensing the different distortions of that field created by objects that conduct or resist electricity. Active electrolocation is practised by two groups of weakly electric fish, the Gymnotiformes (knifefishes) and the Mormyridae (elephantfishes), and by Gymnarchus niloticus , the African knifefish. An electric fish generates an electric field using an electric organ, modified from muscles in its tail. The field may be in brief pulses, as in the elephantfishes, or a continuous wave, as in the knifefishes. Among the Gymnotiformes is a strongly electric fish, the electric eel, which also locates prey by generating a weak electric field; other strongly electric fish such as the electric ray electrolocate passively.

Contents

The electroreceptive ampullae of Lorenzini evolved early in the history of the vertebrates; they are found in both cartilaginous fishes such as sharks, and in bony fishes such as coelacanths and sturgeons, and must therefore be ancient. Most bony fishes have secondarily lost their ampullae of Lorenzini, but other non-homologous electroreceptors have repeatedly evolved, including in two groups of mammals, the monotremes and the cetaceans.

History

Hans Lissmann discovered electroreception in 1950 through his observations of Gymnarchus niloticus. Gymnarchus niloticus005 (cropped).JPG
Hans Lissmann discovered electroreception in 1950 through his observations of Gymnarchus niloticus .

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. [3] The electroreceptive function of these organs was established by R. W. Murray in 1960. [4] [5]

In 1921, the German anatomist Viktor Franz described the knollenorgans (tuberous organs) in the skin of the elephantfishes, again without knowledge of their function as electroreceptors. [6]

In 1949, the Ukrainian-British zoologist Hans Lissmann noticed that the African knife fish (Gymnarchus niloticus) 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. [2] [7]

Electrolocation

Ampullae of Lorenzini, found in several basal groups of fishes, 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 Ampullae of Lorenzini.png
Ampullae of Lorenzini, found in several basal groups of fishes, 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

Electroreceptive animals use the 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. Electrolocation can be passive, sensing electric fields such as those generated by the muscle movements of buried prey, or active, the electrogenic predator generating a weak electric field to allow it to distinguish between conducting and non-conducting objects in its vicinity. [8]

Passive electrolocation

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. [9] [10] 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.

Active electrolocation

Knollenorgan by Viktor Franz 1921.gif
A knollenorgan electroreceptor. RC=receptor cell; b.m.=basal membrane; n=nerve.
Electroreception system in Elephantfish.svg
The elephantnose fish is a weakly electric mormyrid fish which generates an electric field with its electric organ and then uses its knollenorgans to locate nearby objects. [11]

In active electrolocation, [12] 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. [13] Animals that use active electroreception include the weakly electric fish, which either generate small electrical pulses (termed "pulse-type"), as in the Mormyridae, or produce a quasi-sinusoidal discharge from the electric organ (termed "wave-type"), as in the Gymnotidae. [14] 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 objects. 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 electrolocation 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 have tuberous electroreceptors known as Knollenorgans in their skin. [15]

Elephantfish emit short pulses to locate their prey. Capacitative and resistive objects affect the electric field differently, enabling the fish to locate objects of different types within a distance of about a body length. Resistive objects increase the amplitude of the pulse; capacitative objects introduce distortions. [11]

The Gymnotiformes, including the glass knifefish (Sternopygidae) and the electric eel (Gymnotidae), differ from the Mormyridae in emitting a continuous wave, approximating a sine wave, from their electric organ. As in the Mormyridae, the generated electric field enables them to discriminate accurately between capacitative and resistive objects. [11]

Electroreception of Capacitative and Resistive Objects in Glass Knifefish.svg

Electrolocation of capacitative and resistive objects in glass knifefish.
Gymnotid fish generate a continuous electrical wave, which is
distorted differently by objects according to their conductivity.

Electric eel's electric organs.svg

The electric eel's electric organs occupy much of its body.
They can discharge both weakly for electrolocation
and strongly to stun prey.

Electrocommunication

The electric eel, Electrophorus electricus, creates electric fields with modified muscles, either weakly for electrolocation or powerfully to stun prey or to repel predators. Some weakly electric knifefishes appear to mimic the electric eel's discharge patterns; this may be Batesian mimicry, to deceive predators that they are too dangerous to attack. Sidderaal (4039238527).jpg
The electric eel, Electrophorus electricus, creates electric fields with modified muscles, either weakly for electrolocation or powerfully to stun prey or to repel predators. Some weakly electric knifefishes appear to mimic the electric eel's discharge patterns; this may be Batesian mimicry, to deceive predators that they are too dangerous to attack.

Weakly electric fish can communicate by modulating the electrical waveform they generate. They may use this to attract mates and in territorial displays. [18] Electric catfish frequently use their electric discharges to ward off other species from their shelter sites, whereas with their own species they have ritualized fights with open-mouth displays and sometimes bites, but rarely use electric organ discharges. [19]

When two glass knifefishes (Sternopygidae) come close together, both individuals shift their discharge frequencies in a jamming avoidance response. [13]

In bluntnose knifefishes, Brachyhypopomus , the electric discharge pattern is similar to the low voltage electrolocative discharge of the electric eel, Electrophorus. This is hypothesized to be Batesian mimicry of the powerfully-protected electric eel. [17]

Fish that prey on electrolocating fish may "eavesdrop" [20] on the discharges of their prey to detect them. The electroreceptive African sharptooth catfish ( Clarias gariepinus ) may hunt the weakly electric mormyrid, Marcusenius macrolepidotus in this way. [21] This has driven the prey, in an evolutionary arms race, to develop more complex or higher frequency signals that are harder to detect. [22]

Some shark embryos and pups "freeze" when they detect the characteristic electric signal of their predators. [9]

Evolution and taxonomic distribution

In vertebrates, passive electroreception is an ancestral trait, meaning that it was present in their last common ancestor. [23] This form of ancestral electroreception is called ampullary electroreception, from the name of the receptive organs involved, ampullae of Lorenzini. These evolved from the mechanical sensors of the lateral line, and exist in cartilaginous fishes (sharks, rays, and chimaeras), lungfishes, bichirs, coelacanths, sturgeons, paddlefish, aquatic salamanders, and caecilians. Ampullae of Lorenzini were lost early in the evolution of bony fishes and tetrapods. Where electroreception does occur in these groups, it has secondarily been acquired in evolution, using organs other than and not homologous with ampullae of Lorenzini.(boldface italic labels). [1] [23]

Fish with electric organs have evolved eight separate times, each one forming a clade: twice during the evolution of cartilaginous fishes, creating the electric skates and rays, and six times during the evolution of the bony fishes. [24] Actively electrolocating fish are marked with a small yellow lightning flash Farm-Fresh lightning.png . Fish able to deliver electric shocks are marked with a red lightning flash Lightning Symbol.svg . Non-electric species are not shown. [23]

Vertebrates
Cartilaginous fishes

sharks, rays Tiburon portada.jpg

Torpediniformes

Electric ray Lightning Symbol.svg Fish4345 - Flickr - NOAA Photo Library (white background).jpg

430  mya
Bony fishes
Lobe-finned fishes

Coelacanths Coelacanth flipped.png

Lungfish Barramunda coloured.jpg

Amphibians

(aquatic salamanders, caecilians; others: lost) Aquatic life (1916-1917) (19559021800) (cropped).jpg

Mammals
Monotremes

(platypus, echidna) Feeding Platypus (6811147158) (white background).jpg Zaglossus bartoni - MUSE.JPG

mucous glands 
in snout
Cetaceans

(Guiana dolphin) Sotalia guianensis (white background).jpg

vibrissal crypts 
(lost)
Ray-finned fishes

bichirs, reedfishes Cuvier-105-Polyptere.jpg

sturgeons, paddlefishes Atlantic sturgeon flipped.jpg

Most bony fishes
Osteoglossiformes
Mormyridae

elephantfishes Farm-Fresh lightning.png Elephantfish spike waveform.svg Gnathonemus petersii.jpg

knollenorgans   
 (pulses)
Gymnarchidae

African knifefish Farm-Fresh lightning.png Knifefish continuous waveform.svg Gymnarchus niloticus005 (white background).JPG

knollenorgans   
 (waves)
Gymnotiformes   
S. Amer. knifefishes

Farm-Fresh lightning.png Elephantfish spike waveform.svg Johann Natterer - Itui-cavalo (Apteronotus albifrons).jpg

Electric eel

Farm-Fresh lightning.png Lightning Symbol.svg Lateral view of Electrophorus electricus.png

ampullary 
receptors
 
Siluriformes
Electric catfish

Farm-Fresh lightning.png Lightning Symbol.svg FMIB 51852 Electric Catfish, Torpedo electricus (Gmelin) Congo River.jpeg

Uranoscopidae   

Stargazers Lightning Symbol.svg Uranoscopus sulphureus (white background).jpg

no electrolocation 
(lost)
425  mya
Ampullae of Lorenzini

Cartilaginous fish

Sharks and rays ( Elasmobranchii ) rely on electrolocation using their ampullae of Lorenzini 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 fields as low as 5 nV/cm. [25] [26] [27] [28]

Bony fish

Two groups of teleost fishes are weakly electric and actively electroreceptive: the Neotropical knifefishes (Gymnotiformes) and the African elephantfishes (Notopteroidei), enabling them to navigate and find food in turbid water. [29] The Gymnotiformes include the electric eel, which besides the group's use of low-voltage electrolocation, is able to generate high voltage electric shocks. [30] [31]

Monotremes

The platypus is a monotreme mammal that has secondarily acquired electroreception. Its receptors are arranged in stripes on its bill, giving it high sensitivity to the sides and below; it makes quick turns of its head as it swims to detect prey. Platypus electrolocation.svg
The platypus is a monotreme mammal that has secondarily acquired electroreception. Its receptors are arranged in stripes on its bill, giving it high sensitivity to the sides and below; it makes quick turns of its head as it swims to detect prey.

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. [32] [33] The platypus has almost 40,000 electroreceptors arranged in a series of front-to-back stripes along the bill, which probably aids the localisation of prey. [29] The platypus electroreceptive system is highly directional, with the axis of greatest sensitivity pointing outwards and downwards. By making saccades, quick head movements 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. [33]

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 only 400, concentrated in the tip of the snout. [29] 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. [34] 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. [33]

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. [35]

Bees

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. [36]

See also

Related Research Articles

Platypus Species of mammal

The platypus, sometimes referred to as the duck-billed platypus, is a semiaquatic, egg-laying mammal endemic to eastern Australia, including Tasmania. The platypus is the sole living representative or monotypic taxon of its family (Ornithorhynchidae) and genus (Ornithorhynchus), though a number of related species appear in the fossil record.

Echidna Family of mammals

Echidnas, sometimes known as spiny anteaters, are quill-covered monotremes belonging to the family Tachyglossidae. The four extant species of echidnas and the platypus are the only living mammals that lay eggs and the only surviving members of the order Monotremata. The diet of some species consists of ants and termites, but they are not closely related to the true anteaters of the Americas, which are xenarthrans. Echidnas live in Australia and New Guinea.

Gymnotiformes Order of fishes

The Gymnotiformes are an order of teleost bony fishes commonly known as the Neotropical or South American knifefish. They have long bodies and swim using undulations of their elongated anal fin. Found almost exclusively in fresh water, these mostly nocturnal fish are capable of producing electric fields for navigation, communication, and, in the case of the electric eel, attack and defense. A few species are familiar to the aquarium trade, such as the black ghost knifefish, the glass knifefish, and the banded knifefish.

Electric fish Fish that can generate electric fields

An electric fish is any fish that can generate electric fields. A fish that can generate electric fields is called electrogenic while a fish that has the ability to detect electric fields is called electroreceptive. Most electrogenic fish are also electroreceptive. The only group of electrogenic fish that are not electroreceptive are the stargazers, in the family Uranoscopidae. Electric fish species can be found both in the ocean and in freshwater rivers of South America (Gymnotiformes) and Africa (Mormyridae). These two groups of weak electric fish diverged and independently evolved similar ways to communicate and localise objects through producing and receiving electric fields. Many fish such as sharks, rays and catfishes can detect electric fields and are thus electroreceptive, but they are not classified as electric fish because they cannot generate electricity. Most common bony fish (teleosts), including most fish kept in aquaria or caught for food, are neither electrogenic nor electroreceptive. There are approximately 350 species of fish that have the ability to create an electric field that can be used for communication, navigation or predation. These electric fishes are found within the bony fishes (Osteichthyes) and the cartilaginous fishes (Chondrichthyes).

Black ghost knifefish Species of fish

The black ghost knifefish is a tropical fish belonging to the ghost knifefish family (Apteronotidae). They originate in freshwater habitats in South America where they range from Venezuela to the Paraguay–Paraná River, including the Amazon Basin. They are popular in aquaria. The fish is all black except for two white rings on its tail, and a white blaze on its nose, which can occasionally extend into a stripe down its back. It moves mainly by undulating a long fin on its underside. It will grow to a maximum length of 50 cm (20 in).

Magnetoreception Biological ability to perceive magnetic fields

Magnetoreception is a sense which allows an organism to detect the Earth's magnetic field. Animals with this sense include arthropods, molluscs, and vertebrates. The sense is mainly used for orientation and navigation, but it may help some animals to form regional maps. Experiments on migratory birds suggest that they make use of a cryptochrome protein in the eye, relying on the quantum radical pair mechanism to perceive magnetic fields. This effect is extremely sensitive to weak magnetic fields, and readily disturbed by radio-frequency interference, unlike a conventional iron compass.

Ampullae of Lorenzini Sensory organs in some fish that detect electrical fields

The ampullae of Lorenzini are special sensing organs called electroreceptors, where they can form a network of mucus-filled pores. They are mostly found in cartilaginous fish ; however, they are also found in basal actinopterygians such as reedfish and sturgeon. Lungfish have also been reported to have them.

Mormyridae Family of fishes

The Mormyridae, sometimes called "elephantfish", are a family of freshwater fish in the order Osteoglossiformes native to Africa. It is by far the largest family in the order with around 200 species. Members of the family can be popular, if challenging, aquarium species. These fish are also known for having large brain size and unusually high intelligence.

Peterss elephantnose fish Species of fish

Peters's elephant-nose fish is an African freshwater elephantfish in the genus Gnathonemus. Other names in English include elephantnose fish, long-nosed elephant fish, and Ubangi mormyrid, after the Ubangi River. The Latin name petersii is probably for the German naturalist Wilhelm Peters. The fish uses electrolocation to find prey, and has the largest brain-to-body oxygen use ratio of all known vertebrates.

Electric organ (biology) Organ common to all electric fish used to create an electric field

In biology, the electric organ is an organ common to all electric fish used for the purposes of creating an electric field. The electric organ is derived from modified nerve or muscle tissue. The electric discharge from this organ is used for navigation, communication, mating, defense and also sometimes for the incapacitation of prey.

Knollenorgan

A Knollenorgan is an electroreceptor in the skin of weakly electric fish of the family Mormyridae (Elephantfish) from Africa. The structure was first described by Viktor Franz (1921), a German anatomist unaware of its function. They are named after "Knolle", German for "tuberous root" which describes their structure.

Magnetic shark repellents utilize permanent magnets, which exploit the sensitivity of the Ampullae of Lorenzini in sharks and rays (electrosense). This organ is not found on bony fish (teleosts), therefore, this type of shark repellent is selective to sharks and rays. Permanent magnets do not require power input, making them practical for use in fisheries and as bycatch reduction devices. Sharkbanz, released in 2014, is a wearable commercially available device intended for recreational users. Its manufacturers cite numerous scientific papers which support the effectiveness of permanent magnets in a range of contexts. A field study of a range of shark deterrents in 2018 found that Sharkbanz were ineffective when used in a temperate oceanic setting with berley-attracted Great white sharks.

Sternarchogiton nattereri is a species of weakly electric knifefish in the family Apteronotidae. It is native to the Amazon River system and feeds on sponges. Unlike other members of the genus Sternarchogiton, there is pronounced sexual dimorphism in S. nattereri, with reproductively mature males developing strong external teeth on tips of their jaws. These males are so different from the females and juveniles that they were thought to be a different genus and species, the "tooth-lip knifefish" Oedemognathus exodon, for over 40 years.

Sternarchogiton porcinum is a species of weakly electric knifefish in the family Apteronotidae. It is native to deep river channels in the Río Huallaga, Río Napo, and Río Amazonas in Peru, and in the Río Orinoco in Venezuela. Many specimens once identified as S. porcinum from the Brazilian Amazon Basin and the Venezuelan Orinoco are now known to be a different species, S. preto.

Monotreme Order of egg-laying mammals

Monotremes are prototherian mammals of the order Monotremata. They are one of the three main groups of living mammals, along with placentals (Eutheria) and marsupials (Metatheria). Monotremes are typified by structural differences in their brains, jaws, digestive tract, reproductive tract, and other body parts compared to the more common mammalian types. In addition, they lay eggs rather than bearing live young, but, like all mammals, the female monotremes nurse their young with milk.

Mormyrinae Subfamily of fishes

The subfamily Mormyrinae contains all but one of the genera of the African freshwater fish family Mormyridae in the order Osteoglossiformes. They are often called elephantfish due to a long protrusion below their mouths used to detect buried invertebrates that is suggestive of a tusk or trunk. They can also be called tapirfish.

Jamming avoidance response Behavior performed by weakly electric fish to prevent jamming of their sense of electroreception

Jamming avoidance response (JAR) is a behavior performed by some species of weakly electric fish. The JAR occurs when two electric fish with wave discharges meet – if their discharge frequencies are very similar, each fish will shift its discharge frequency to increase the difference between the two fish's discharge frequencies. By doing this, both fish prevent jamming of their sense of electroreception.

Bioelectrogenesis

Bioelectrogenesis is the generation of electricity by living organisms, a phenomenon that belongs to the science of electrophysiology. In biological cells, electrochemically active transmembrane ion channel and transporter proteins, such as the sodium-potassium pump, make electricity generation possible by maintaining a voltage imbalance from an electrical potential difference between the intracellular and extracellular space. The sodium-potassium pump simultaneously releases three sodium ions away from, and influxes two potassium ions towards, the intracellular space. This generates an electrical potential gradient from the uneven charge separation created. The process consumes metabolic energy in the form of ATP.

Hydrodynamic reception

Hydrodynamic reception refers to the ability of some animals to sense water movements generated by biotic or abiotic sources. This form of mechanoreception is useful for orientation, hunting, predator avoidance, and schooling. Frequent encounters with conditions of low visibility can prevent vision from being a reliable information source for navigation and sensing objects or organisms in the environment. Sensing water movements is one resolution to this problem.

Most fish possess highly developed sense organs. Nearly all daylight fish have color vision that is at least as good as a human's. Many fish also have chemoreceptors that are responsible for extraordinary senses of taste and smell. Although they have ears, many fish may not hear very well. Most fish have sensitive receptors that form the lateral line system, which detects gentle currents and vibrations, and senses the motion of nearby fish and prey. Sharks can sense frequencies in the range of 25 to 50 Hz through their lateral line.

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Further reading