Eel migration to the Sargasso: remarkably high swimming efficiency and low energy costs
1 Institute of Evolutionary and Ecological Sciences, Integrative Zoology,
Leiden University, POB 9516, 2300 RA Leiden, The Netherlands
2 Department of Experimental Zoology, Wageningen Agricultural University,
Marijkeweg 40, 6709 PG Wageningen, The Netherlands
3 Department of Fishculture and Fisheries, Wageningen Agricultural
University, Marijkeweg 40, 6709 PG Wageningen, The Netherlands
* Author for correspondence (e-mail: ginneken{at}LUMC.NL)
Accepted 27 January 2005
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Summary |
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Key words: eel, Anguilla anguilla, trout, swimming efficiency, metabolic costs, muscle performance, swimtunnel, cost of transport
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Introduction |
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Materials and methods |
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Animals
For experiment 1, 3 year old hatchery eels Anguilla anguilla L.
(N=30, 860±81.9 g, 73.1±3.8 cm BL) were used.
In experiment 2, we used eels A. anguilla (N=5,
155.0±18.3 g, 43.2±3.2 cm) and trout Oncorhynchus
mykiss Walbaum (N=5, 161.5±21.5 g, 24.6±1.0 cm) of
the same body mass. The eels used in both experiments 1 and 2 were in the
non-migratory yellow stage. Eels were obtained from Royal B.V., Helmond, The
Netherlands, and trout were obtained from the Dutch Organization of Fisheries,
O.V.B. Geertruidenberg, The Netherlands.
Flow tank experiments
In experiment 1, the oxygen consumption rates of eels (N=9)
swimming at 0.5 BL s1 were measured over a period
of 173 days in 2 m Blazka-type flow tanks with a volume of 127.1±0.9 l.
In addition, to establish the routine metabolic rate (RMR), we measured the
oxygen consumption, over the same period of 173 days, of six eels resting in
Blazka-type flow tanks with continuous water refreshment. The cross section of
the flow tanks is circular with an inner diameter of 190 mm. Outside the
boundary layer the flow speed is constant over the cross section of the inner
tube. The flow tanks were calibrated using a Laser Doppler method. Thus the
eels swam at a constant known speed with negligible wall effects
(van den Thillart et al.,
2004). Swimming experiments were performed over 173 days under a
12 h:12 h day:night light cycle at a temperature of 19.0±0.3°C at
0.5 BL s1. The illumination in the climatized room
was switched to 670 nm light (bandwidth 20 nm) during experiments. Based on
pigment changes during silvering it is assumed that this far-red light is
invisible for eels (Pankhurst and Lythgoe,
1983
). The time lapse between the start of migration and the first
leptocephali in the Sargasso Sea is about 6 months. Thus to cover a distance
of 50006000 km in 6 months requires a mean swimming speed of 0.4 m
s1 (Ellerby et al.,
2001
).
For experiment 2, five eels and five trout were placed in the same 127 l
flow tanks at a constant temperature of 18±0.3°C under the same
illumination protocol. Eels swam at 0.5 BL s1
(21.5±1.6 cm s1), whereas the trout swam at a
slightly higher speed of 0.7 BL s1 (17.2±0.7
cm s1). We ensured that both species swam at their maximum
range or optimal swimming speed, which is the relevant speed for migration, to
facilitate the comparison between costs of transport of eel and trout. The
optimal swimming speed of trout is available in the literature
(Webb, 1971), whereas the
value for eel is based on a study of eel muscle efficiency
(Ellerby et al., 2001
; for a
more detailed explanation, see Discussion).
Swimming behavior was recorded at regular intervals during the entire period using an infrared video camera (frame rate 25 Hz) during the dark period to document the position of the animal in the flow tank as well as to detect possible long-term changes in swimming behavior.
Before sampling, the animals were quickly anaesthetized with 300 p.p.m. MS222 (3-aminobenzoic-acid-ethyl-ester methane sulfonate salt; Sigma, St Louis, MO, USA). All experiments were approved by the local committee on animal experimentation.
Oxygen consumption
The oxygen level in the tunnel was measured continuously using an oxygen
electrode (Mettler Toledo, Tiel, The Netherlands). The oxygen consumption rate
was calculated from the oxygen decline after automatic closure of the
water-inlet by a magnetic valve. The oxygen levels changed between 85 and 75%
air saturation. The valve was normally open allowing a refreshment rate of
57 l min1 and automatically operated between 14:00 h
and 17:00 h to measure oxygen consumption. The oxygen value was not allowed to
fall below 75% in order to prevent the animals from becoming hypoxic
(van den Thillart and van Waarde,
1985).
From the decrease in O2 concentration, the rate of oxygen
consumption O2
(mg O2 h1 kg1) was calculated
from the formula:
O2=127
[O]
t1,
where
[O2]
t1 is the
decrease in oxygen content per hour. Oxygen consumption data were corrected
for the decline in mass of the animals.
Carcass analyses
To quantify the energy cost of transportation by a second method,
independently from our respiratory measurements, we analyzed the changes in
body composition. Carcass analyses were performed according to ISO-standards
(International Organization for Standardization, Animal feeding stuffs; ISO
5983 and ISO/DIS 6492, Geneva, Switzerland). After weighing, fish samples were
cut into pieces of about 3 cm and nearly submerged in water in a glass beaker.
The samples were autoclaved at 2 atm (2.013x105 Pa) at
120°C for 4 h. They were then homogenized and subsequently sampled in
triplicate for dry matter, protein and fat analyses. Dry matter content was
measured by freeze drying of the sub-samples to constant mass. Protein was
measured according to procedures described in ISO 5983 (1979). For fat
determination, freeze dried sub-samples were extracted as described in ISO/DIS
6492 (1996).
Calculations and statistics
In order to calculate the cost of transportation (COT: mean gross energy
costs of transportation; Schmidt-Nielsen,
1972), total energy consumption was first calculated from oxygen
consumption by multiplying the mean measured rate of oxygen consumption
(Table 1, in ml O2
kg1 fish h1) with the number of swimming
hours (4152 h = 173 days) and the applied energy conversion factor for
respirometry of 18.89 kJ ml1 O2
(Elliot and Davison, 1975
).
This gives a total energy consumption of 2316.58 kJ kg1 fish
over 5533.2 km or a COT of 0.42 kJ kg1
km1. Alternatively the energy used during the 5533 km run
was calculated by bomb-calorimetry. Bomb-calorimetry could be only used once
on eels at the start of the experiment, so a control group of 15 animals was
also measured for comparison with the swim- and the rest-groups
(Table 2).
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The calculations for the bomb-calorimetry were as follows:
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Results |
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We obtained two independent estimates for cost of transport. From the first
method, oxygen uptake (using the oxycaloric value of the three substrates;
Elliot and Davison, 1975), we
obtained a value of 2317 kJ kg1 fish for the energy cost of
6 months swimming covering a distance of 5500 km. This corresponds to a COT
value of 0.42 kJ kg1 km1. The swimming
group lost more total body mass than the resting group (180.3 g compared with
103.9 g; Table 1). Hence, based
on the second method, which uses mass loss, body composition and energy
conversion factors (Brafield and Llewellyn,
1982
), we calculated that energy used for swimming was 3450 kJ
kg1 fish, corresponding to a COT value of 0.62 kJ
kg1 km1. The two COT estimates obtained
independently (Table 1) are of
the same order of magnitude.
In experiment 2, where eels and trout swam in identical experimental set-ups, we measured an oxygen consumption of 43.9±8.42 mg O2 kg1 h1 and 130.4±9.49 mg O2 kg1 h1, respectively. During 7 days the eels and trout covered a mean distance of 132.5±12.1 km and 102.8±2.3 km, respectively. From these data we calculated COT values for eel and trout of 0.68 and 2.73 kJ kg1 km1, respectively. Our video recordings of the fish swimming in the flow tank show that the fish were swimming in the free-stream and did not benefit from wall effects: the fish swam mostly in the centre of the flow tank and therefore are more than 2 (eel) up to 3 (trout) tail heights removed from the wall (results not shown).
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Discussion |
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There are various levels of energy conversion in a swimming animal. The overall metabolic efficiency (how much heat is generated at a given swimming speed) comprises the efficiencies of various processes, e.g. propeller efficiency (how much momentum is gained by the animal and wasted in the wake) and the muscle efficiency (how many ATP molecules are used per myosin-head cycle). The concept of efficiency used here corresponds to overall metabolic efficiency and encompasses propeller and muscle efficiency, for example. During locomotion, propeller and muscle efficiency are likely to contribute significantly to overall metabolic efficiency, so it is interesting to compare the hydrodynamic and muscle performance of eel to those of other undulatory swimmers.
To reduce costs of transport and increase overall metabolic efficiency, all or some of the processes that determine the costs of transport can be optimized. Efficiency can be improved most effectively by improving those processes in which efficiency increases nonlinearly and progressively with a given performance parameter. Performance parameters that only weakly or linearly affect efficiency are less likely to bring about a drastic increase in efficiency.
In order to explain the remarkable difference in cost of transport between eel and trout, it is important to identify the processes that cause it. To this end, we have studied the literature on propeller efficiency and muscle efficiency in undulatory swimmers.
Hydrodynamic performance and propeller efficiency
A fish can alter its propeller efficiency by changing its structural design
and its motion pattern. Both carangiform and anguilliform swimmers undulate
their body, the former with a narrower amplitude envelope than the latter. How
the shape of the body undulations affect locomotory efficiency has been
estimated using analytical approximations. Lighthill's elongated body theory
(EBT) concludes that efficient swimmers should undulate only the most
posterior section of their body in the ideal case only their trailing
edge to maximise propeller efficiency
(Lighthill, 1971;
Tytell and Lauder, 2004
).
Daniel's predictions (Daniel,
1991
) differ in part: the propeller efficiency of undulatory
swimming decreases linearly as the rearward speed of the body wave increases
relative to the swimming speed, and it is independent of the frequency and the
amplitude of the body wave. Given that the swimming kinematics of trout and
eel mainly differ in the amplitude envelope of their body wave, but have a
similar range of body wave speeds (for a review, see
Videler, 1993
), it is unlikely
that kinematic differences between trout and eel can explain the difference in
their overall metabolic efficiency.
The combined effect of propeller shape and motion on performance can be
studied by visualising the flow generated by anguilliform and carangiform
swimmers. The ratio of forward to total momentum of the entire wake provides
the mean propeller efficiency over a complete tail beat. This approach,
whether using experimental or computational flow fields, requires the
quantification of the three-dimensional flow in the complete wake, which so
far has not been done. The currently available two-dimensional slices through
the wake suggest that eels generate considerable lateral momentum, which do
not contribute to the forward motion and therefore reduce efficiency
(Müller et al., 2001;
Tytell and Lauder, 2004
).
Tytell estimated a hydrodynamic efficiency of 0.5 to possibly up to 0.87
(Tytell and Lauder, 2004
).
Equivalent estimates for carangiform fish are reported in the range
0.740.97 (Drucker and Lauder,
2001
; Müller et al.,
2001
; Nauen and Lauder,
2002a
,b
).
These values suggest that trout has a higher propeller efficiency than eel,
which does not explain the higher overall metabolic efficiency of eels.
Efficiency is also inversely related to thrust
(Lighthill, 1971;
Daniel, 1991
). However, a 25%
difference in swimming speed is insufficient to explain a fourfold difference
in efficiency. So, the currently existing evidence on the hydrodynamics of
undulatory swimming contradicts rather than explains the high swimming
efficiency of eels.
Muscle performance and efficiency
The efficiency with which a muscle converts chemical energy into mechanical
work is important in prolonged aerobic locomotion, such as migration. Cruising
is characterized by cyclic contractions at a well-defined frequency. Swimming
speed depends linearly on tail-beat frequency, and tail-beat frequency
corresponds to contraction frequency. The mechanical efficiency of muscle
contractions depends on contraction speed in a non-linear fashion. This
relationship can be predicted from Hill's model of muscle contractions
(McMahon, 1984) and has also
been documented in fish swimming muscles
(Curtin and Woledge, 1993
).
There is a narrow range of contraction frequencies over which efficiency
remains high. At contraction frequencies above and below this range,
efficiency drops off progressively
(McMahon, 1984
;
Curtin and Woledge, 1993
).
McMahon's calculations (McMahon,
1984
) show that maximum efficiency occurs at a contraction speed
at 13% of the maximum contraction speed of the muscle, which is a slightly
lower speed than the speed at maximum power. To swim at maximum muscle
efficiency, the fish should maintain a tail-beat frequency that allows the
muscle to contract at this optimal speed.
If we take the contraction frequency that maximizes power as a first
approximation of the contraction speed that maximizes efficiency, we can
compare eel aerobic swimming muscles to those of trout. Eel muscles deliver
peak power at much lower contraction frequencies (0.50.8 Hz in silver
eel, measured at 14°C; Ellerby et al.,
2001) than the muscles of trout (23 Hz, measured at
11°C; Hammond et al.,
1998
). The swimming speeds that correspond to these contraction
frequencies are 0.5 l s1 for eel and 0.41.0 l
s1 for trout (Webb,
1971
). These values confirm that in our experiments both eel and
trout were swimming at close to their optimal swimming speed, and hence the
much higher COT of trout is probably not due to the trout having been forced
to swim under considerably suboptimal conditions for its swimming muscles.
Muscle fibre type recruitment and swimming speed
At the low speeds used in this study, the eels will recruit only the
posterior red muscle to swim continuously. As demonstrated in the work of
Gillis (1998), muscle fiber
type recruitment was clearly dependent upon swimming speed. A pattern of
`posterior-to-anterior' recruitment within a fiber type was observed as eels
increased their swimming speed (figs 2, 3A,F in
Gillis, 1998
). For example,
eels typically used mainly posteriorly located red muscle (at 0.75 and 0.6
BL) to power slow-speed swimming, but would then additionally recruit
more anteriorly located red muscle (at 0.45 and 0.3 BL) to swim at
the higher speeds (figs 2, 3A in Gillis,
1998
). These unusual muscle activation pattern and kinematics may
explain the low COT in eels compared with trout, in which most of the red
muscle on each side of the body is stimulated during a tail-beat cycle
assuming that the European and American eels are similar in this regard.
In contradiction to this theory/hypothesis of Gillis
(1998) to explain the low
swimming efficiency of eel by recruitment patterns of muscle, Wardle et al.
(1995
) showed that the muscle
activity pattern (% time active during one tail-beat cycle) does not differ
substantially between different undulatory swimmers. Wardle's values for eel
(based on Williams et al.,
1989
) agree with those mentioned by Gillis
(1998
). Compared with trout
and other fish, recruitment in eel is certainly not less by a factor of
24. Hence it is not likely that more posterior muscle recruitment in
eel can explain the many-fold difference in efficiency between eel and
trout.
Metabolism and non-locomotory influences on costs of transport
Overall metabolic efficiency is also influenced by the efficiency of the
respiration and energy-conversion processes themselves. The whole-organism
locomotory performance is determined by its metabolic machinery, bringing us
to the whole-body oxygen consumption (routine metabolic rate, RMR) of the
animal. In this study, we found a RMR for eel of 29.55±4.2 ml
O2 kg1 h1, which corresponds to
42.21±6.0 mg O2 kg1 h1.
This value is similar to values reported in literature: 35 mg
kg1 h1 (for the similar sized animals at
18°C; Degani et al., 1989;
McKenzie et al., 2000
) for eel
and also the RMR measurements of other fish species
(Winberg, 1956
). Hence, we may
conclude that, based on metabolic rate comparisons with other fish species,
the mitochondrial capacity remains the same. However, in the wild, eel do not
migrate at the surface but in the deep sea: a migrating eel has been
photographed in the Bahamas at a depth of 2000 m
(Robins et al., 1979
). There,
they experience considerably larger pressures, which might further increase
metabolic efficiency at the mitochondrial level by increasing the efficiency
of their oxidative phosphorylation (Theron
et al., 2000
). In a laboratory study in which eels were exposed
for 21 days to 10.1 MPa hydrostatic pressure, Theron et al.
(2000
) demonstrated that the
ADP/O ratios, calculated from mitochondrial respiration measurements, were
significantly increased.
Eels actually performing the migration will not only experience higher pressures, but also lower temperatures, which will also affect their efficiency. Furthermore, eels might adapt their migratory route to take advantage of favorable sea currents, which would further reduce the energy requirements. However, with the migratory routes unknown, nothing can be said about the possible energy savings from pressure, temperature and sea-current effects.
Metabolic costs and efficiency compared
Our respiratory measurements and the carcass analyses suggest that eels
have a much higher metabolic efficiency than trout. In eel, the COT values
obtained from oxygen consumption data and carcass analyses are 0.42 and 0.62
kJ kg1 km1, respectively, whereas trout
has much higher COT values (respirometry only) of 2.73 kJ
kg1 km1, respectively. The COT in trout
matches the value measured by Webb
(1971), and is similar to
other salmonids (Brett, 1973
)
and many adult fish species (for a review, see
Videler, 1993
). This means
that eel swim 46 times more efficiently than many other fish species,
even across swimming styles.
In conclusion, we demonstrate in this study that fasting European eels are able to swim 5500 km, a distance corresponding to their supposed spawning area in the Sargasso Sea, with a remarkably high swimming efficiency and at low energy costs. At this moment, this high efficiency can be explained neither by propeller nor muscle efficiency. How the extremely low optimal contraction frequency of eel aerobic muscle affects muscle efficiency has not yet been studied. So far, the only evidence that eels have a remarkably high swimming efficiency comes from metabolic energy costs. The source of the eel's remarkably high efficiency remains at present unknown, providing ample stimulation for biomechanists and physiologists alike to investigate eel migratory swimming performance.
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Acknowledgments |
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