Topic: Electroreception in fish, amphibians and monotremes
From an evolutionary point of view, electroreception is particularly intriguing as a sense modality that has been repeatedly lost and reinvented again.
Some animals have evolved a most astonishing sensory capacity – they are able to detect naturally occurring electric fields in the microvolt or even nanovolt range with the help of specialised receptors. The electric signals, which convey information about the structure of the environment and the activity of other animals, are processed in specific regions of the brain. This passive electric sense can be employed for navigation, obstacle avoidance or prey detection and is particularly useful in conditions that limit the use of other senses, e.g. at night or in murky waters. Some fish, known as electric fish, have gone one step further and evolved an active electric sense. With the help of an electric organ, they can generate weak or strong electric fields and use them for electrical communication, active electrolocation or, in case of strong electric discharges, even for stunning prey.
As electroreception needs a conductive medium, it is generally limited to aquatic and partly aquatic species. So far, it has only been convincingly demonstrated in vertebrates – it can be found in many marine and freshwater fishes, some amphibians and, most remarkably, monotreme mammals. Speculations that also the largely aquatic star-nosed mole (Condylura cristata) possesses electroreceptors on the highly touch-sensitive tentacles surrounding its nostrils have not been confirmed (but these animals give as important insights into tactile sensation and specifically a series of striking convergences with the eye). Also the recently reported response to electric fields of two species of freshwater crayfish, Cherax destructor and Procambarus clarkii, is most likely not due to a specialized electric sense as the behavioural thresholds were extremely high and electroreceptors could not be identified. It seems reasonable to predict, however, that, given its potential advantages, electroreception will eventually be demonstrated in other groups of animals as well, possibly birds (e.g. wading birds that probe the soil with their bill to find food, where again tactile sensitivity and the convergence of touch receptors are well known), reptiles or invertebrates.
Electroreceptors can be found in lampreys as well as in many groups of true fish, where they may be limited to the head or distributed across the whole surface of the body. Cartilaginous fish (elasmobranchs: sharks, rays and skates; holocephalans: chimaeras), non-teleost ray-finned fish (polypterids: bichirs and reedfish; acipenseriforms: sturgeons and paddlefish), some teleosts (siluriforms: catfish; gymnotids: American knifefish; gymnarchids: African knifefish; mormyrids: elephantfish), lungfish and coelacanths all are electroreceptive and use this sense mainly for prey capture. Recent studies of the Mississippi River paddlefish (Polyodon spathula), for example, have shown that its huge rostrum functions as an electrical antenna for detecting the electric signals of planktonic crustaceans. It might also help the fish to orientate during migration to their spawning grounds.
Among amphibians, electroreception has been demonstrated in several aquatic caecilians and urodeles (salamanders) but to date not in anurans (frogs). That anurans appear to lack an electric sense might be due to the mainly non-predatory lifestyle of their tadpoles. Examples of electroreceptive urodele species are the giant salamander (Andrias davidianus), the axolotl (Ambystoma mexicanum) and the olm (Proteus anguinus). Particularly for the latter, the value of an electric sense is obvious – it lives in caves and is almost blind, so it can detect and recognise prey items by their electric fields. Generally, the main function of the electrosensory system in amphibians seems to be the localisation of prey objects.
Three living species of monotreme have been shown to be capable of electroreception – the Australian duck-billed platypus (Ornithorhynchus anatinus) as well as two species of echidna, the Australian short-beaked echidna (Tachyglossus aculeatus) and the Western long-beaked echidna (Zaglossus bruijnii) of New Guinea. The electric sense is best studied in the platypus. It had long puzzled scientists how platypuses manage to catch large amounts of invertebrate prey in murky streams at night with their eyes, ears and nostrils closed. The mystery was solved when they discovered that the bill skin is laced with push rod mechanoreceptors and electroreceptors. While the push rods are distributed uniformly across the bill surface, the 40,000 electroreceptors are arranged in a series of stripes, which probably aids the localisation of prey. The platypus electroreceptive system is highly directional, with the axis of greatest sensitivity pointing outwards and downwards. By making short latency 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. This behaviour is comparable to that shown by barn owls that orient towards an acoustic stimulus.
The electroreceptive system of echidnas is structurally similar to that of platypus but far less complex. In contrast to the 40,000 electroreceptors found on the platypus bill, Western long-beaked echidnas possess only 2,000 receptors and short-beaked echidnas merely 400 that are concentrated in the tip of the snout. Thus, echidnas have obviously experienced a reduction in their electroreceptive abilities, most likely due to the environment they live in. While platypus is largely aquatic, echidnas are terrestrial, although their terrestrial lifestyle is probably secondarily derived from a semi-aquatic ancestor, as suggested in a recent paper on monotreme phylogenetic relationships (Phillips et al. 2009, PNAS). Western long-beaked echidnas live in wet tropical montane forests, where they feed on earthworms in damp leaf litter. So their habitat is probably still quite favourable to the reception of electrical signals, contrary to the varied but generally more arid habitat of their short-beaked relative. However, short-beaked echidnas are particularly active after rain and readily feed on termites and ants, digging tunnels into their nests, where it might be humid enough to detect electric fields. Furthermore, the tip of their snout is constantly wet, which might enhance electroreception. So although it seems likely that echidnas use electroreception at close range to identify live objects, it remains to be shown how behaviourally relevant their electric sense actually is.
Evidence of convergence
From an evolutionary point of view, electroreception is particularly intriguing as a sense modality that has been repeatedly lost and reinvented again. As an electric sense is found in phylogenetically old groups such as sturgeons, it is generally considered to be no more recent than other vertebrate sensory systems, although its real evolutionary origin is still unknown. It is, however, fairly safe to assume that electroreception evolved once in basal vertebrates, was lost in the common ancestor of holosteans (gars and bowfin) and teleosts and then re-evolved independently at least twice in teleost fish. Electroreception has been demonstrated in two distantly related teleost lineages, the osteoglossomorphs, which contain the African mormyrids and gymnarchids, and the ostariophysans, which include the South American gymnotids and the widely distributed catfish. While amphibians most likely inherited their electric sense from their fish ancestors and some groups then lost it, monotreme mammals almost certainly acquired electroreception independently. These separate evolutionary origins are reflected by differences in the morphology of the electroreceptors and processing of the electric signals in the brain.
In all fish and amphibians, the electroreceptors are a secondary cell system (such as in the eye and ear), where a specialized receptor hair cell responds to a stimulus by producing a receptor potential, which then activates a primary sensory neuron. However, there are differences between different groups, e.g. with respect to receptor type and the nature of the stimulating signals. Most fish and amphibians possess cathodally sensitive ampullary receptors (known as “Ampullae of Lorenzini” in elasmobranchs). They consist of a jelly-filled canal, which opens to the surface by a pore in the skin, and are excited by negative pulses and inhibited by positive ones. In contrast, the electroreceptive teleosts have evolved anodally sensitive ampullary electroreceptors as well as tuberous receptors. Tuberous receptors are not connected to the surface and able to respond to the discharges of the electric organs of these electric fish.
The electroreceptors of monotremes are completely different in that they are modified mucous and serous glands. This is ideal for animals that are not fully aquatic, because the association with a gland helps to maintain conductivity and prevent desiccation. In contrast to fish and amphibians, the nerve endings, which are arranged in a daisy chain around the pore of the gland, are naked and not tipped by a sensory cell. Thus, there is no peripheral synapse involved in the transduction of the electric stimuli. The receptors are excited by negative pulses.
Innervation and brain structures
What all electroreceptors have in common is that only afferent nerves are present, which carry nerve impulses to the brain. However, while in all fish and amphibians the receptors are derived from the acoustic-lateralis system and innervated by the 8th cranial nerve (lateral line nerve), the receptors of monotremes are supplied by the 5th cranial nerve (trigeminal nerve). This provides further evidence for independent evolutionary origins.
The afferents project to particular regions of the brain, which also differ between groups. In non-teleost fish and amphibians, the electroreceptor region of the brain is the dorsal nucleus of the medulla. This dorsal nucleus is not found in teleosts. Instead, their electroreceptor afferents are received in a special portion of the medial nucleus known as the electrosensory lateral line lobe (ELLL), which has evolved at least twice independently. In monotremes, the electrical signals are processed in the somatosensory neocortex of the forebrain.
In the elaborate neocortex of platypus, a detailed topographic representation of the bill surface exists, which, in combination with a representation of different field strengths at each point on the bill, allows for highly sophisticated signal processing. Another special feature of the platypus brain is the intimate association between mechano- and electroreceptive neurons (in fish and amphibians, such an association is not prominent). There are alternating rows of mechanosensory neurons and bimodal neurons, which receive electrosensory and mechanical input (so there are no neurons that only respond to electrical input). This stripe-like array is evocative of the primary visual cortex in primates, which integrates input from the two eyes. It has been speculated that the bimodal neurons allow the platypus to estimate the absolute distance of prey: The electrical signal generated by a moving prey organism will reach the bill before the mechanical waves. Thus, there will be a certain time delay between the two signals that changes with distance to the prey. If the bimodal neurons in the neocortex were sensitive to a certain time-of-arrival difference, this would provide a direct read-out of distance (quite similar to echolocating bats).
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Map of Life - "Electroreception in fish, amphibians and monotremes"
January 21, 2017