Magnetic sense in the Japanese eel, Anguilla japonica, as determined by conditioning and electrocardiography
Faculty of Fisheries, Kagoshima University, Kagoshima 890-0056, Japan
* Author for correspondence (e-mail: nishi{at}fish.kagoshima-u.ac.jp)
Accepted 9 June 2004
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Summary |
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Key words: magnetosensitivity, eel migration, conditioned response, magnetoreceptor, Japanese eel, Anguilla japonica
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Introduction |
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The American eel, Anguilla rostrata, could not be conditioned to
magnetic fields (McCleave et al.,
1971; Rommel and McCleave,
1973
). McCleave and Power
(1978
) examined the turning
behaviour of American eel elvers in an arena where the vertical magnetic
fields could be manipulated and found no differences in behaviour under four
different magnetic field conditions. However, the American eel showed
directional preferences under natural geomagnetic and artificial magnetic
fields in another study (Souza et al.,
1988
).
Japanese, European and American eels are different species, and each
species comprises three populations: the marine population spends the entire
lifetime at sea; the estuarine population migrates between freshwater and
seawater; and the freshwater population grows in the river and migrates to the
ocean for spawning (Tsukamoto et al.,
1998; Jessop et al.,
2002
; Tzeng et al.,
2000
,
2002
). Given the migratory
life history of the anguillid eels, it is possible that marine eels cue to
magnetic fields during spawning migration but freshwater eels do not. The
present study examined the magnetic sense of Japanese eel captured at sea,
from a river and from a farm.
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Materials and methods |
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The eels were handled according to methods prescribed by the Kagoshima University's Guide for the Care and Use of Laboratory Animals.
Experimental apparatus
The experiment was carried out in darkness in the laboratory of the Faculty
of Fisheries, Kagoshima University. The eels were tested in a PVC aquarium (20
cm wide x 105 cm long x 20 cm deep) placed on a vibration-proof
table surrounded by a black curtain, behind which the investigators worked.
The test eels were provided with shelter in PVC pipes (either 46 cm long
x 3.6 cm in diameter or 72 cm long x 5.8 cm in diameter, depending
on eel size) (Fig. 1). The
aquarium, pipe and eel were placed in an east-west orientation (the eel faced
east).
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The test eels from the river and the farm were allowed more than 1 h to acclimate to the holding conditions in the PVC aquarium. The marine eels were directly transferred from seawater into freshwater in the PVC aquarium and allowed 2 h to acclimate. The eel heart beat was monitored by electrocardiogram (see below), and the conditioning tests were started only after the heart beat had become stable (in terms of the time between successive QRS waves). Being euryhaline, the marine eels showed no irregular behaviour when transferred directly into freshwater and the heart beat rate became stable within 30 min.
Flow-through freshwater was continuously supplied to the PVC aquarium through a water purifier (CW-101; NGK, Nagoya, Japan). Water temperatures in the aquarium ranged from 23.6 to 29.0°C during the eel conditioning experiments.
Generating magnetic fields
Around the PVC aquarium, a solenoid 35 cm in diameter was constructed with
74 turns of teflon-coated copper wire (0.3 mm-diameter wire) in a single
layer. The head of the test eel was at the centre of the solenoid. By passing
direct current through the solenoid, a magnetic field parallel to the fish
body was produced. Thus, inside the solenoid, magnetic north was east when the
solenoid was turned on. The magnetic field produced was monitored with a small
compass placed on the solenoid.
The magnitude of the imposed magnetic fields was varied by changing the
electric current from 0.05 A to 0.76 A and was calculated by the formula of
Biot and Savart (Jackson,
1999):
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where B is magnetic flux density (T), µ0 is magnetic permeability (4x10-7 in vacuo), I is electric current (A), r is radius of solenoid (m), and R is distance from a coil to an observation point (m).
The magnetic fields varied from 192 473 nT to 12 663 nT during the tests on eels. These magnetic fields were from 5.92x to 0.38x the horizontal geomagnetic field of 32 524 nT (measured with an Overhauser effect magnetometer; GSM-19-MC; GEM Systems Inc., Richmond Hill, Ontario, Canada) at our laboratory. The solenoid produced a horizontal west-east vector that combined with the earth's south-north vector for a resultant field redirected 80° to 21° easterly from the geomagnetic north, and the resultant magnitude was 187 298 nT to 34 611 nT at the respective directions (Fig. 2).
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Conditioning of eels to magnetic fields
Classical conditioning was done on the Japanese eel to determine its
sensitivity to a magnetic field. The method depended on establishing a
conditioned response, in this case a change in the heart beat of the eel when
exposed to a magnetic field (the conditioning stimulus) accompanied by flashes
of light. A light flash is a commonly used stimulus that scares and stresses
fishes (Kawamura et al., 2002).
The light flash in this experiment came from a halogen lamp placed in front of
the solenoid; the light intensity was 7300 lux at the head of the test
eel.
A conditioning run consisted of exposing an eel to an artificial magnetic field of 192 473 nT for 10 s, with three light flashes at 1 s intervals during the latter 5 s. One set of 10 conditioning runs (at irregular intervals of 1-5 min) was done on each eel. 1 min after a set of conditioning runs was finished, a conditioning test was done on the same eel to record the conditioned response - i.e. a change in the eel heart beat (see below). A conditioning test consisted of re-exposing the eel to the same magnetic field (192 473 nT) for 10 s but without the three light flashes. Eleven heart beats were recorded before the conditioning test to measure 10 interbeat intervals (mean and confidence interval) for each eel. Only four heart beats were recorded during the conditioning test because the conditioned response was evident as soon as the magnetic field was turned on and it was enough to measure three interbeat intervals.
A significant slowing down of the heart beat was obtained at 192 473 nT, so the magnitude of the imposed magnetic field was reduced in three steps to 12 663 nT during the conditioning tests to see if the Japanese eel still responded to small redirected resultant magnetic fields. For six marine eels, the smallest magnetic field used was 12 663 nT, equivalent to 0.38x the south-north horizontal geomagnetic field at Kagoshima, and redirection was 21° easterly.
Recording and measuring eel electrocardiograms
Electrodes are usually implanted close to the heart to record the
electrocardiogram uncontaminated by muscle potentials and movement artefacts.
However, the eel heart has a high electromotive force, and electrocardiograms
could be recorded by electrodes placed in the water but not in the fish's body
(Yamamori et al., 1971). Thus,
in this study, the eel heart beat was recorded while the test eel rested
inside a PVC pipe shelter - that is, the eel experienced minimum handling, no
anaesthesia and, presumably, little or no stress. Electrodes (1.5 m-long
teflon-coated copper wires, 1 mm diameter) were attached to the two ends of
the PVC pipe and twisted together and connected to the probe of an amplifier
(Ab-601G; Nihonkoden). The electrocardiograms were recorded with a thermal
array recorder (RTA-4100, Nihonkoden).
Ten heart beats before the conditioning test and three heart beats after
the test were measured for interbeat intervals. For the statistical analysis,
the interbeat intervals were normalized by logarithmic transformation
following the formula of Kawamura et al.
(1981): normalized
interval=log10(1+T), where T is the raw value of
the interbeat interval (s). Each test interbeat interval was then compared
with the mean pre-test interbeat interval (by t-test).
The cardiac deceleration ratio was computed to assess the strength of the
conditioned response (Northmore and Yagar,
1974). This ratio was defined as: (test interbeat interval - mean
pre-test interbeat interval)/mean pre-test interbeat interval, and was
computed from the raw values of the interbeat intervals. In this paper, the
largest value of the interbeat intervals during the test (either T1, T2 or T3)
was used in computing the maximum cardiac deceleration ratio.
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Results |
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The highest cardiac deceleration ratios ranged from 0.11 to 2.60 in 10
marine eels, from 0.10 to 1.47 in two river eels, and from 0.16 to 2.27 in
five farmed eels (Fig. 4). The
ratios varied widely even at the same imposed magnetic field (the correlation
coefficients between the intensity of imposed magnetic field and the highest
cardiac deceleration ratios were not statistically significant by the
F-test). The variation was not due to the magnitude of the imposed
magnetic field nor the number of conditioning runs (Wilcoxon-Mann-Whitney
test, P>0.10) (Siegel and
Castellan, 1988) but was probably due to individual differences in
physiological condition. These statistics meant that the maximum cardiac
deceleration ratio was not a good indicator of the strength of the conditioned
response of Japanese eels to magnetic fields. Thus, no such comparison was
made among the marine, riverine and farmed Japanese eels in this study.
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The Japanese eel could detect a 21° easterly shift in the horizontal magnetic field (Fig. 2). The solenoid produced horizontal vector south-east, which combined with the earth's vector for a resultant field redirected horizontally 21° easterly with 34 611 nT in resultant magnitude (6% increment) at the centre of the solenoid where the test eels were placed.
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Discussion |
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In the present study, Japanese eels responded to a 12 663 nT east-west
horizontal geomagnetic field equivalent to 0.38x the north-south
horizontal geomagnetic field at Kagoshima. This result indicates that Japanese
eels have higher sensitivity to magnetic fields than other migratory fish that
have been studied. More significantly, Japanese eels have sufficient
sensitivity to detect existing environmental magnetic fields. In earlier
experiments, investigators applied magnetic field stimuli much higher than the
ambient magnetic field. East-west magnetic fields of 50 000 nT and 100 000 nT
were used for American eel (Souza et al.,
1988), and a vertical magnetic field with a peak intensity of 125
000 nT (an artificial field of 70 000 nT added to the earth's magnetic field
of 55 000 nT) was used for rainbow trout
(Walker et al., 1997
). For
yellowfin tuna, Thunnus albacares, a non-uniform vertical magnetic
field of 10 µT to 50 µT was used against a background 30 000 nT
(Walker, 1984
). It is possible
that these fishes would have sensed lower magnetic fields if these had been
presented to them.
Given that Japanese eels are sensitive to magnetic fields, they could use
the geomagnetic field as a cue for their long-distance migration to the
spawning area. The spawning area of Japanese eels has been found in the North
Equatorial Current, west of the Marianas
(Tsukamoto, 1992). After 5-8
years(Tzeng et al., 2002
)
growing at sea, off eastern and northeastern Asia, adult eels migrate
thousands of kilometres to the spawning area.
In contrast to the Japanese eels, American eels (A. rostrata)
showed no conditioned response to a magnetic field applied parallel to the
body or to a reversal of the vertical magnetic field
(McCleave et al., 1971;
Rommel and McCleave, 1973
).
The difference in the conditioned response to magnetic fields between American
eels and Japanese eels may simply be due to the recording method (electrodes
were implanted in the body of the American eel under anaesthesia). American
eels did perceive, and responded to, magnetic fields during another set of
tank experiments, in which the eels showed a preference for a northeast
direction under the earth's magnetic field (50 000 nT) and for a southeast
direction under the -50 000 nT and -100 000 nT fields
(Souza et al., 1988
).
Magnetic fields are relatively simple stimuli with two dimensions - direction and intensity - and it is not clear which is more important to Japanese eels for orientation. Direction may be a more critical cue for migrating fishes since direction can change rapidly in space and time as the body moves from side to side during swimming. Its sensitivity to a 21° easterly shift in the horizontal magnetic field could well guide Japanese eels.
In most fishes, behaviour depends on more than one source of stimulation,
and often the stimuli operate sequentially
(Blaxter, 1988). The presence
of more than one orientation system has been shown in migrating O.
nerka fry in a lake (Quinn,
1980
). Rommel and McCleave
(1972
) demonstrated that
American eels are sensitive to electric fields of 0.167x10-3
µA cm-2 applied perpendicular to the body axis in freshwater,
and that this intensity is within the range of naturally occurring oceanic
electric fields. Fricke and Kaese
(1995
) suggested that different
hydrographic regimes could be used as a rough orientating mechanism in eel
migration in the ocean. Thus, magnetosensitive eels may also use geoelectric
stimuli and hydrographic regimes as orientating cues during migration.
Recent studies have demonstrated the importance of olfaction rather than
magnetic sense in the migration of American eels and European eels. Tagged
European eels were inhibited in either the visual, magnetic or olfactory
sense, and it was observed that the group that had been made anosmic by
injection of elastomer into the nasal cavity behaved differently from the
control group and from the other experimental groups in that they showed
irregular swimming behaviour, slower speed and no common direction
(Tesch et al., 1991;
Westin, 1990
). Ultrasonic
telemetry showed the importance of olfaction in the estuarine migration of
silver-phase American eels - the anosmic eels with nares filled with petroleum
jelly spent more time in the estuary whereas the control eels moved upstream
and downstream with the tides (Barbin et
al., 1998
). In these studies, the perceived absence of a magnetic
sense in the European eel and the American eel may be an artefact of the
method used to induce anosmia, where boiling petroleum jelly (>150°C)
was injected into the nares (Keefe,
1992
). If these eels have magnetoreceptor cells in the nose, as
does the rainbow trout (Walker et al.,
1997
), then the anosmia treatment may have damaged the
magnetoreceptor cells or the nerves [the superficial ophthalmic ramus (ros V)
of the trigeminal nerve] such that the eels could also not detect the
geomagnetic field. The fine branches of the ros V nerve (ros V rami) that
surround the nasal capsule form a complex network from which very fine
processes penetrate the capsule wall and terminate in the lamina propria of
the olfactory lamellae (Walker et al.,
1997
). This thin nerve structure might be very vulnerable to heat
at high temperature.
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Acknowledgments |
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