Electric and magnetic field detection in elasmobranch fishes
26 Nov 1982-Science (American Association for the Advancement of Science)-Vol. 218, Iss: 4575, pp 916-918
TL;DR: Dogfish and blue sharks were observed to execute apparent feeding responses to dipole electric fields designed to mimic prey, and stingrays showed the ability to orient relative to uniform electric fields similar to those produced by ocean currents.
Abstract: Sharks, skates, and rays receive electrical information about the positions of their prey, the drift of ocean currents, and their magnetic compass headings. At sea, dogfish and blue sharks were observed to execute apparent feeding responses to dipole electric fields designed to mimic prey. In training experiments, stingrays showed the ability to orient relative to uniform electric fields similar to those produced by ocean currents. Voltage gradients of only 5 nanovolts per centimeter would elicit either behavior.
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TL;DR: Direct evidence supporting the coexistence and distribution of multiple ecotypes permits the survival of the population as a whole over a broader range of environmental conditions than would be possible for a homogeneous population is reported.
Abstract: The cyanobacterium Prochlorococcus is the dominant oxygenic phototroph in the tropical and subtropical regions of the world's oceans. It can grow at a range of depths over which light intensities can vary by up to 4 orders of magnitude. This broad depth distribution has been hypothesized to stem from the coexistence of genetically different populations adapted for growth at high- and low-light intensities. Here we report direct evidence supporting this hypothesis, which has been generated by isolating and analysing distinct co-occurring populations of Prochlorococcus at two locations in the North Atlantic. Co-isolates from the same water sample have very different light-dependent physiologies, one growing maximally at light intensities at which the other is completely photoinhibited. Despite this ecotypic differentiation, the co-isolates have 97% similarity in their 16S ribosomal RNA sequences, demonstrating that molecular microdiversity, commonly observed in microbial systems, can be due to the coexistence of closely related, physiologically distinct populations. The coexistence and distribution of multiple ecotypes permits the survival of the population as a whole over a broader range of environmental conditions than would be possible for a homogeneous population.
736 citations
Book•
01 Jan 1995
TL;DR: In this paper, the magnetic effects on spatial behavior in various groups of the animal kingdom from platyhelminths to vertebrates, with an emphasis on birds as the best studied group.
Abstract: This text details animal orientation with the help of information from the geomagnetic field. It reviews the magnetic effects on spatial behaviour in the various groups of the animal kingdom from platyhelminths to vertebrates, with an emphasis on birds as the best studied group. The discussion covers "compass" and "non-compass" effects and different types of responses, for example, alignments, compass orientation and orientation by the spatial distribution of magnetic parameters, which should aid the reader's understanding of the various ways magnetic information may be used.
642 citations
Journal Article•
TL;DR: It is argued that some larvae may use a hierarchy of sensory cues to find suitable settlement sites and that some of the same types of stimuli may be used at more than one spatial scale (as demonstrated for adult salmonid fishes).
Abstract: Models of larval dispersal rarely incorporate the behavior of larvae, yet many potential settlers of marine invertebrates and fishes may navigate toward suitable settlement sites by responding to gradients of environmental stimuli. Accordingly, a variety of stimuli may be used for navigation (directed movements to the source of stimuli) and partial navigation (e.g., migration to a current that may favor transport to a settlement site) in the pelagic environment. A broad diversity of taxa have senses that allow them to detect variation in: water chemistry (biotic sources, e.g., amino acids and abiotic sources, e.g., salinity), sound and vibration (biotic sources, e.g., grunting fishes, abiotic sources, e.g., waves breaking), white light gradients and images, polarized light, current direction, magnetism and water pressure. Some organisms can detect multiple stimuli (e.g., decapods and fishes) and integrated sensory responses are likely to be common; many potential settlers of these taxa are good swimmers. Demonstrations of strong orientation to stimuli and navigation over short (centimeters to meters) and broad spatial scales (tens of meters to tens of kilometers) are most common for these groups. Partial navigation, involving vertical migration, is common for invertebrate larvae. A consequence of vertical migration can be transportation that favors movement to suitable settlement habitat. Navigation over a range of spatial scales may use stimuli that are very predictable regardless of location (e.g., water pressure, gravity). The gradients of other stimuli may be more useful for environment-specific signals and even the location of natal habitats, locations and conspecifics (e.g., using sound or smell of specific taxa). We argue that some larvae may use a hierarchy of sensory cues to find suitable settlement sites and that some of the same types of stimuli may be used at more than one spatial scale (as demonstrated for adult salmonid fishes). There are good demonstrations of the use of cues for orientation and navigation at small spatial scales (less than a few meters). More information, however, is required at spatial scales that are relevant to navigation over kilometers before behavior can be incorporated more accurately into models of larval dispersal.
555 citations
Journal Article•
TL;DR: It is concluded that physical factors that result in a departure from unidirectional, depth-uniform water flow provide the opportunity for retention of larvae, and therefore of self-recruitment.
451 citations
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...Chemical stimuli, with directional information, may be found in estuarine and reefal plumes (Crossland et al., 1980; Wolanski and Hamner, 1988; Grimes and Kingsford, 1996), from sandy beaches (Kalmun, 1982) and perhaps algae (Walters and DiFiori, 1996)....
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Journal Article•
TL;DR: In this article, the authors evaluate direct and indirect evidence to predict the relationship between these biophysical variables and the degree of self-recruitment in benthic marine organisms.
Abstract: Mounting evidence suggests that some populations of benthic marine organisms may be less demographically 'open' than previously thought. The degree to which a population receives recruits from local sources versus other populations has important ecological and management ramifications. For either of these reasons, it is often desirable to estimate the degree to which a population of interest is self-recruiting. Although methods for actual estimation of population self-recruitment are limited and often difficult to employ, the presence of several biological and physical conditions may improve our estimates of self-recruitment for particular populations. Biological traits of benthic adults (relative fecundity, spatial and temporal patterns of spawning and larval release, parental investment), as well as pelagic larvae (stage of development at hatching, pelagic larval duration, vertical migration behavior, horizontal swimming ability, and sensory capabilities) influence where and when larvae are released, where and how they are transported, their ability to move actively in the pelagic realm, and finally, spatial and temporal settlement patterns. Physical variables potentially influencing self-recruitment include site isolation, coastal complexity and flow variability. Within these physical variables we discuss explicit mechanisms by which larvae may be retained in proximity to their natal population. We provide examples from specific locations such as coral reefs, isolated islands and seamounts, and semi-enclosed embayments such as lagoons and estuaries, as well as characteristic oceanographic features such as upwelling systems, fronts, moving convergences, eddies and counter currents. We evaluate direct and indirect evidence to predict the relationship between these biophysical variables and the degree of self-recruitment in benthic marine organisms. We conclude that physical factors that result in a departure from unidirectional, depth-uniform water flow provide the opportunity for retention of larvae, and therefore of self-recruitment. These physical factors are common in the ocean and vary in intensity among locations and times. Some enable retention of passive larvae (physical retention), whereas others lead to retention only with active behavioral input by the larvae (biophysical retention). Larval behavior that can contribute to or result in retention or return to natal sites ranges from simple vertical orientation (within the capabilities of the larvae of most taxa) to complex sensory abilities and strong swimming (known to occur in larvae of a few taxa, particularly decapod crustaceans and fishes). For all taxa, both the pelagic larval duration and the time to behavioral competency will have a strong influence on likelihood of self-recruitment. Understanding the biophysical mechanisms by which larvae are retained near or return to their natal population will be necessary before generalizations can be made. Examples highlight the importance of each variable to processes controlling self-recruitment. For most correlates, further study is clearly warranted. Although certain variables hold promise for predicting self-recruitment, complex, non-linear interactions among these biophysical variables must be considered.
412 citations
References
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TL;DR: The experiments described demonstrate clearly that the shark Scyliorhinus canicula and the ray Raja clavata make a biologically significant use of their electrical sensitivity and are justified in accrediting the animals with an electric sense and in designating the ampullae of Lorenzini as electroreceptors.
Abstract: 1. Previous experiments have demonstrated that ( a ) the shark Scyliorhinus canicula and the ray Raja clavata are extremely sensitive to weak electric fields; ( b ) their electrical sensitivity is due to the ampullae of Lorenzini; ( c ) the sharks and rays can be stimulated by the bioelectric fields emanating from the flatfish Pleuronectes platessa .
2. When hungry, Scyliorhinus and Raja perform well-aimed feeding responses to flatfish, even if the prey have covered themselves with sand. The object of the present study was to determine whether the sharks and rays use the bioelectric fields of the flatfish to detect the position of their prey.
3. To analyse the feeding responses of the sharks and rays, a flatfish was put into an agar chamber. The predators responded to the so screened prey from the same distance, and tried to feed on it in the same way as if there were no agar at all. As the flatfish in the agar chamber was completely hidden from view, the sharks and rays were thus shown not to need visual contact to locate the prey.
4. If the agar chamber was filled with cut-up pieces of whiting, the sharks and rays did not respond to the food, although the odour of whiting juice normally attracts them strongly. Therefore, the sharks and rays did not detect the position of the agarscreened flatfish by smell.
5. The feeding responses to the flatfish could be entirely abolished by covering the agar chamber with a very thin sheet of plastic. The mechanical attenuation offered by the plastic film was too weak to explain its dramatic inhibitory effect, and, thus, a purely mechanical detection of the agar-screened flatfish without plastic film was also ruled out.
6. As the responses to the agar-screened flatfish were not merely due to visual, chemical, or mechanical stimuli, it was tentatively concluded that the sharks and rays perceived the prey electrically. This conclusion was fully in agreement with the results of the experiments, for the agar chamber did not appreciably distort the bioelectric fields of the flatfish, and the electrical impedance of the plastic film was extremely high.
7. Further, the bioelectric field of a flatfish was simulated with a pair of electrodes, buried in the sand. Now, the sharks and rays displayed exactly the same feeding responses to the electrodes as they did previously to the real prey. This crucial experiment confirmed the electrical hypothesis in a very direct way.
8. The experiments described demonstrate clearly that the shark Scyliorhinus canicula and the ray Raja clavata make a biologically significant use of their electrical sensitivity. Therefore, we now are justified in accrediting the animals with an electric sense and in designating the ampullae of Lorenzini as electroreceptors .
9. When the sharks and rays were offered a piece of whiting in the vicinity of two electrodes simulating a flatfish, they were attracted by the odour of the food but usually performed their well-aimed responses to the electrodes. Thus, at short range, the electric fields act as a much stronger directive force than do the visual and chemical stimuli. Only direct mechanical contact dominates over the electrical stimuli.
10. Theoretically, the sharks and rays can detect the electric fields resulting from ceanic and tidal currents. Whether they make use of the available information for orientation in the open sea is not yet known. Furthermore, the observations and measurements described indicate that, in studying shark attacks, the electric fields of the prey and the electric sense of the predators should be taken into account.
Present address: Department of Neurosciences, School of Medicine, University of California, San DiegoLa Jolla, California 92037.
420 citations
TL;DR: The ampullae of Lorenzini are sensitive to weak tactile stimulation applied to the ends of their jelly-filled tubes, and either an increase or a decrease in their resting discharge frequency may be caused, each with an opposite after-effect.
Abstract: 1 The ampullae of Lorenzini are sensitive to weak tactile stimulation applied to the ends of their jelly-filled tubes
2 Either an increase or a decrease in their resting discharge frequency may be caused, each with an opposite after-effect
3 ‘Adaptation’ is total, being three-quarters completed in 3-8 sec This ‘adaptation’ probably includes accommodative changes of the tissues
4 The function of the ampullae is discussed, but no definite conclusion can yet be reached
199 citations
TL;DR: Partition of the ampullary system makes the head of Scyliorhinus canicula insensitive to weak electrical stimuli in the area where the eliminated ampullae open, and this affects the biological significance of the electro-perception in sharks and rays.
Abstract: SHARKS and rays are extremely sensitive to alternating electric fields. A potential gradient of only 0.1 µV/cm is sufficient to evoke in Scyliorhinus canicula a reflex contraction of the eyelids (“winking of the eyes”), and to affect the respiratory rhythm of Raia clavata (“spiraculum reflex”)1,2. Such a weak electric field is perceived with the ampullae of Lorenzini. The ampullae are not only very sensitive to thermal and mechanical influences as found electrophysiologically3–5, but also respond to electrical stimuli6–8. Partial denervation of the ampullary system makes the head of Scyliorhinus canicula insensitive to weak electrical stimuli in the area where the eliminated ampullae open9. In the past few years, our investigations have been focused on the biological significance of the electro-perception in sharks and rays.
168 citations
TL;DR: In biology, the study of geomagnetic orientation has gained new momentum since the discovery of magnetic field detectors in aquatic organisms and the ability of sharks and rays to orient to the earth's magnetic field has been demonstrated in behavioral experiments as discussed by the authors.
Abstract: In biology, the study of geomagnetic orientation has gained new momentum since the discovery of magnetic field detectors in aquatic organisms. Sharks and rays respond to dc and low frequency voltage gradients of 0.005 μV/cm. By moving through the earth's magnetic field, they induce electric fields well within the sensitivity range of their keen electric sense. As these fields depend on the direction in which the animal is heading, the induced voltage gradients may serve as the biophysical basis of an electromagnetic compass sense. The ability of sharks and rays to orient to the earth's magnetic field has been demonstrated in behavioral experiments. Also, various marine and freshwater mud bacteria are endowed with permanent magnetic dipole moments, directed parallel to the axis of motility. When separated from the sediments, these bacteria return to the mud by migrating downward along the earth's inclined magnetic field lines. Their orientation is largely determined by the principles of statistical mechanics and may be expressed in terms of the directive magnetic force, the randomizing effect of thermal agitation, and the cells' flagellar thrust. Observations on live bacteria yield individual dipole moments circa 15 × kT/G.
113 citations
TL;DR: Investigation has shown that the ampullæ of Lorenzini of elasmobranch fishes are sensitive both to slight changes of temperature and to weak mechanical stimuli, but neither sensory modality is convincing as the biologically adequate stimulus.
Abstract: ELECTROPHYSIOLOGICAL investigation has shown that the ampullae of Lorenzini of elasmobranch fishes are sensitive both to slight changes of temperature1 and also to weak mechanical stimuli2. But neither sensory modality is convincing as the biologically adequate stimulus, for the temperature-sensitive regions are buried deep in the body (there being no apparent reason for the great anatomical development of the tube system), and the mechanical sensitivity is quantitatively less than that of the lateral line without being qualitatively very distinct.
69 citations