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First published online January 3, 2006
Journal of Experimental Biology 209, 200-201 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.10.1242/jeb.02012
JEB Classics |
A NEW SENSE FOR MUDDY WATER
University of Leeds r.m.alexander{at}leeds.ac.uk
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). He did not see how
their electric organs could have evolved, as his theory required, by natural
selection of small variations. They appeared to be derived from muscles, which
were already known to produce the weak electric pulses now known as action
potentials, but what selective advantage could have driven the early stages of
their evolution? A strong electric discharge would be a formidable defence,
and possibly an aid to catching prey, but a weak one would be utterly useless
for either of these functions.
Late in the nineteenth century and early in the twentieth, weak electric
organs were discovered in several groups of freshwater fishes, notably the
African Mormyridae and the South American Gymnotidae (reviewed by
Lissmann, 1958). They produced
pulses of a few volts, stronger than action potentials but much weaker than
the discharges of the strong electric fishes. Various suggestions of possible
functions were made, but none were convincing until Hans Lissmann and Ken
Machin carried out the research that is the subject of this article.
Both these scientists had remarkable careers. Hans Lissmann (1909-1995) was
the son of German parents living in Russia
(Alexander, 1996). He and his
family were interned as aliens during the First World War. After it, they set
out on foot for Germany to escape the Russian Revolution, but after a 300 mile
trek found themselves stuck in a refugee camp, still in Russia. Eventually
they got to Hamburg, where Lissmann was able to train as a zoologist,
obtaining his doctorate (on fish behaviour) in 1932. He worked briefly in
Hungary and India, and (though not Jewish) was unwilling to return to Hitler's
Germany. He wrote to James Gray in the Zoology Department at Cambridge, and
was offered a post there. Gray was engaged on his pioneering research on
animal locomotion. Lissmann worked closely with him on the locomotion of
leeches, earthworms and amphibians, and independently on slugs and snails
(summarised in Gray, 1968). In
the Second World War, Lissmann was again interned as an alien, and was sent to
Canada. He was allowed to return in 1943, and continued his career in
Cambridge. He was elected to the Royal Society in 1954.
Ken Machin (1924-1988) took a BA in physics, followed by a PhD in
radio-astronomy. After that, in a remarkably astute move, Gray appointed him
to a post in the Cambridge Zoology Department. His role was to collaborate
with the zoologists on the physical aspects of their research. He worked with
Pringle on the asynchronous flight muscles of insects, showing how they will
drive any resonant system at its natural frequency of vibration
(Machin and Pringle, 1959).
This and his work with Lissmann were Machin's finest scientific
achievements.
Before Machin joined the Zoology Department, Lissmann had been sent a
living specimen of Gymnarchus. Despite the similarity of name between
this African fish and the South American gymnotids, Gymnarchus is not
related to them, but to the mormyrids. Lissmann became interested in its weak
electric discharges, pulses of 3-7 volts. He wondered whether they could be
the basis of a previously unknown sense, which might enable the animal to
detect objects in the water around it
(Lissmann, 1951). The story
told in Cambridge was that the first clue to the electric sense had come when
a student combed her hair near its tank, and the Gymnarchus went
wild. This may have been a myth, but Lissmann did indeed find that the fish
reacted to electrostatic charges outside its tank
(Lissmann, 1958). More
generally, he showed that the fish was sensitive to any change in the electric
field around it.
The first Gymnarchus died, but others were obtained, and Machin joined forces with Lissmann. I was a research student, sharing a laboratory with Machin, so I was well placed to watch their progress. To test Lissmann's hypothesis, they needed to show that objects in the water around the fish would affect its electric field in ways that could provide information about the objects' positions, and that the fish was sensitive enough to detect these changes in its field.
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They needed to show that the fish could tell the difference between objects that were indistinguishable by sight, touch, smell or any other known sense. They chose porous earthenware pots with contents of different electrical conductivity. They eventually showed that the fish could distinguish a pot filled with aquarium water, from an identical pot containing 75% aquarium water plus 25% distilled water. They also showed that it could distinguish between pots filled with aquarium water, with and without a glass tube of 2 mm diameter down its centre. It could not, however, distinguish between a pot of diluted aquarium water and an electrically equivalent pot of undiluted aquarium water with a glass tube in it.
While Lissmann concentrated on training the fish to make ever-finer discriminations, Machin built an electrical model of it. This model had a Perspex body immersed in a shallow tank of tapwater. Two electrodes on the long axis of the body were used to establish an electric field like the one produced by the fish. Recording electrodes around the edge of the body proved capable of recording distortions of the field like the ones shown in Fig. 1, when objects of higher or lower conductivity were placed in the water. There was a feeling of rivalry between Machin and the fish; which could make the finer discriminations? The fish won hands down, but the experiments with the model showed that the postulated mechanism for object location was feasible.
Gymnarchus lives in extremely turbid rivers. Lissmann
(1958) showed that the weakly
electric gymnotid fish, which are active mainly at night, have similar
sensitivity to electric fields. The value of a non-visual means of locating
objects is evident, both in turbid water and in darkness.
Lissmann and Machin had discovered and explained a new sense, utterly
unlike anything that we humans can experience. Here was something at least as
remarkable as the echolocation of bats, a discovery of the previous decade
(see Griffin, 1958). It has
generated a huge and diverse literature, both before and after Moller's
(1995) book. Physiologists have
shown in great detail how the electric organs and electroreceptors work.
Neurobiologists have investigated the processing of receptor output in the
brain. Researchers in animal behaviour have shown how fish use the electric
sense in their natural environments, and how they interact with neighbouring
electric fishes to avoid being confused by their signals. Electrolocation has
been shown to be a remarkably refined sense, enabling fish to discern the
shapes, distances and, to some extent, the composition of objects
(von der Emde, 2004). We can
now appreciate the major part it plays in the lives of the two large groups of
fish that possess it.
Footnotes
R. McNeill Alexander writes about H. W. Lissmann and K. E. Machin's 1958 paper `The mechanism of object location in Gymnarchus niloticus and similar fish.'
References
Alexander, R. McN. (1996). Hans Werner Lissmann 30 April 1909-21 April 1995. Biog. Mem. R. Soc. Lond. 42,234 -245.
Darwin, C. R. (1872). Of the Origin of Species by Means of Natural Selection, sixth edition. London: J. Murray.
Gray, J. (1968). Animal Locomotion. London: Weidenfeld and Nicolson.
Griffin, D. R. (1958) Listening in the Dark. The Acoustic Orientation of Bats and Men. New York: Yale University Press.
Lissmann, H. W. (1951). Continuous electrical signals from the tail of a fish, Gymnarchus niloticus Cuv. Nature 167,201 -202.[CrossRef][Medline]
Lissmann, H. W. (1958). On the function and
evolution of the electric organs of fishes. J. Exp.
Biol. 35,156
-191.
Lissmann, H. W. and Machin, K. E. (1958). The mechanism of object location in Gymnarchus niloticus and similar fish. J. Exp. Biol. 35,451 -486.[Abstract]
Machin, K. E. and Pringle, J. W. S. (1959). The physiology of insect fibrillar muscle. II. Mechanical properties of a beetle flight muscle. Proc. R. Soc. Lond. B 151,204 -225.
Moller, P. (1995). Electric Fishes: History and Behaviour. London: Chapman and Hall.
Von der Emde, G. (2004). Distance and shape: perception of the 3-dimensional world by weakly electric fish. J. Physiol., Paris 98,67 -80.[CrossRef][Medline]
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