for decades , tracking studies with eels have been conducted to reveal the oceanic migration routes to their mysterious spawning areas6,000  km from the european coast  by using acoustic and archival tags ( tesch 2003 ) .
recently , the use of pop - up satellite tags ( psats ) , developed for tracking large animals ( > 50  kg ) , were used in several studies for tracking eels ( aarestrup et al .
although the oceanic migration routes were partially obtained this way , the assumed spawning areas have never been reached .
results showed a much lower travel speed than required for reaching the spawning areas in time .
the minimal speed for european silver eels is 0.4  m  s , 6,000  km within 6  months  the time between leaving the coast and the occurrence of the first larvae ( tesch 2003 ) .
2009 ) found an average horizontal migration speed of 13.8  km  day , which corresponds to ca .
the effect of psats on the swimming efficiency and swimming behaviour of eels has not been tested before .
eels have been shown to be very efficient swimmers ; they are some five times more efficient than salmonids with respect to the energy cost of swimming ( van ginneken and van den thillart 2000 ; van den thillart et al .
particularly this extreme high swimming efficiency must have been a strong selection force during evolution ; as a consequence , any interference with shape and movement must have a serious impact on the cost of transport ( cot ) and thus interferes with successful spawning migration .
current psats have almost the same cross section as that of an eel of 1  kg , which therefore almost doubles the hydrodynamic drag .
the psat resists not only forward but also sideward motion , which must have an additional disturbing effect on the anguilliform mode of swimming .
furthermore due to the positive buoyancy of the psat , there will be an additional constant pull upwards , which also impairs the swimming mode .
thus , one may expect a strong interference of a psat with swimming mode , swimming capacity and swimming efficiency . in this study we tested the effect of a small psat on the swimming efficiency of female european eels of about 1  kg .
swim performance tests ( trial 15 ) were carried out in 127-l blazka - type swimming tunnels ( van den thillart et al . 2004 ) with running natural seawater ( 35  ppt ) at 18    1c under red light according to the speed test protocol of palstra et al .
five different trials were performed on each of eight farmed female silver eels ( 1,026    31  g ; 76.5    1.0  cm ) .
every trial included a 1-day swim performance test ( speed test ) after appropriate conditioning .
the trials were performed in the following order : ( 1 ) no tag ( control ) ; ( 2 ) no tag , after operation ( to check the effect of the operation ) ; ( 3 ) positive buoyant tag ; ( 4 ) neutral buoyant tag ; ( 5 ) no tag , after removal of the tag ( to test handling and training effects ) .
the 1-day speed test was carried out in five steps from 0.4 to 0.8  m  s with increments of 0.1  m  s at 2-h intervals .
the optimal swimming speed  speed with lowest cot  is within this range of speeds , as demonstrated in a previous study ( palstra et al .
it was calculated from the decline of the oxygen concentration in the closed swimming tunnel .
the oxygen levels were kept between 95% and 75% air saturation . to restore the initial saturation level ,
the swimming tunnel was flushed with air - saturated water during the last 30  min of each interval .
the swimming tunnels were calibrated with a doppler flow technique to determine the correct water flow in the tunnel ( van den thillart et al .
table  1protocol swim performance testdayaction1adaptation ; overnight at 0.4  m  s2trial 1 : no tag , before operation  speed test ; overnight at 0.4  m  s3  +  4operation , attach base ; 2  days at 0.4  m  s5trial 2 : no tag , after operation  speed test ; overnight at 0.4  m  s6psat attached ; overnight at 0.3  m  s7trial 3 : positive buoyant tag 
speed test ; overnight at 0.3  m  s8added metal weight to tag ; overnight at 0.3  m  s9trial 4 : neutral buoyant tag  speed test ; overnight at 0.3  m  s10tag removed ; overnight at 0.4  m  s11trial 5 : no tag , final test  speed test ; endspeed test includes five 2-h intervals 0.40.8  m  s in steps of 0.1  m  s. after the last step , the eels were kept at 0.1  m  s for 1.5  h to measure the resting rate .
the oxygen consumption was measured over the first 90  min of the interval ; thereafter , the tunnel was flushed for 30  min to restore the oxygen level . before introduction to the tunnels and before the operation , the eels were anaesthetized with 1  ml  l clove oil solution ( 10% clove oil dissolved in 96% ethanol ) protocol swim performance test speed test includes five 2-h intervals 0.40.8  m  s in steps of 0.1  m  s. after the last step , the eels were kept at 0.1  m  s for 1.5  h to measure the resting rate .
the oxygen consumption was measured over the first 90  min of the interval ; thereafter , the tunnel was flushed for 30  min to restore the oxygen level . before introduction to the tunnels and before the operation , the eels were anaesthetized with 1  ml  l clove oil solution ( 10% clove oil dissolved in 96% ethanol ) the eels were introduced in the tunnels 1  day before each trial , and left overnight while swimming at 0.4  m  s. after trial 1 , a 20    9-mm teflon plate ( 1.5  mm thick ) was placed under the skin of the experimental animal about 30  mm in front of the dorsal fin , the same location as used by jellyman and tsukamoto ( 2002 ) .
a silk line was pulled through the plate and skin on either side ; the line was left outside the body .
after the operation , the eels were placed back into the swimming tunnels and swam for 2  days at 0.4  m  s. trial 2 was carried out 2  days after the operation .
thereafter a psat was attached to the teflon plate , leaving about 20  mm between the fish and the tag .
the eels were placed back in the tunnel and left swimming overnight at 0.3  m  s. the lower speed was necessary , as the eels could not swim faster overnight with a psat attached . at the end of trial 3 , a small metal weight ( 10.9  g )
the eels were placed back in the tunnel and left swimming overnight at 0.3  m  s. after trial 4 the psat was removed and the eels were introduced in the tunnel and left overnight swimming at 0.4  m  s. the last trial ( 5 ) was carried out to control whether the handling and previous swim tests changed the swim performance . at the end of each trial , the speed was set at 0.1  m  s for 1.5  h to measure resting conditions .
this low speed was necessary to keep the water well mixed , while low enough for the eels to stay at rest .
the optimal swimming speed ( cot ) and critical swimming speed were calculated according to brett ( 1964 ) . according to this method , the swimming speed is increased in intervals of > 30  min , in 810 equal steps up to collapse ; the critical speed is then interpolated from the last two speeds .
dimensions of the psat were : body length 115  mm , diameter first part 20  mm , diameter second part non - functional 40  mm , length of antenna 170  mm and weight in air 53  g. the used tags were not functional but corresponded in size and buoyancy with minipat from wildlife computers .
the experiments were carried out according to the dutch law on animal experimentation with approval # dec-10089 .
in this study , female silver eels swam at 0.10.8  m  s , with and without a psat .
the swimming performance was tested with the 1-day speed test at five different conditions ( table  1 ) .
there were no significant differences in oxygen consumption rates ( at all speeds ) between the conditions without tag ; i.e. trials 1 , 2 , 5 ( fig . 
therefore , we can infer that there was no negative effect of the operation on the swimming efficiency of the eels .
thus the results of trial 1 , 2 and 5 can be considered as controls .
in contrast , when a psat was attached to the eels ( trials 3 and 4 ) , the oxygen consumption during swimming was more than twofold higher compared to the control groups ( p  <  0.001 , fig . 
even when the psat was made neutrally buoyant ( trial 4 ) , the oxygen consumption during swimming was still ca .
as there were no significant differences found between the positive vs the neutrally buoyant psat ( p  >  0.05 ) , the results suggests that the drag more than the lift of the psat may have been the most crucial factor impairing swimming performance .
although , the vertical migration as observed for eels in the wild ( aarestrup et al . 2009 ) could not be simulated during this study . 
 fig . 
1effect of pop - up satellite tags on a oxygen consumption ( in milligram o2 per kilogram per hour ) and b cost of transport ( in milligram o2 per kilogram per kilometer ) for swimming 1  kg european eels ( n  =  8) .
treatment levels were : no tag , before operation ( filled square , black ) ; no tag , after operation ( filled triangle , blue ) , with positive buoyant tag ( multiplication sign , green ) ; with neutral buoyant tag ( filled diamond , orange ) ; no tag , final test ( filled circle , red ) .
asterisk indicates significant difference from control at p  <  0.05 effect of pop - up satellite tags on a oxygen consumption ( in milligram o2 per kilogram per hour ) and b cost of transport ( in milligram o2 per kilogram per kilometer ) for swimming 1  kg european eels ( n  =  8) .
treatment levels were : no tag , before operation ( filled square , black ) ; no tag , after operation ( filled triangle , blue ) , with positive buoyant tag ( multiplication sign , green ) ; with neutral buoyant tag ( filled diamond , orange ) ; no tag , final test ( filled circle , red ) .
asterisk indicates significant difference from control at p  <  0.05 also the cot was significantly higher when eels were swimming with a psat ( p  <  0.001 , fig . 
1b ) , i.e. a change from 25 to 75  mg o2  kg  h. eels with a psat showed irregular swimming at 0.5  m  s and fatigued after a few minutes when the speed was raised to 0.6  m  s. as eels have a very regular swimming mode with a nearly constant wave frequency , irregular swimming was immediately visible . the calculated critical swimming speed with a psat was significantly lower compared to the control groups ; i.e. 0.48    0.02 and 0.73    0.02  m  s respectively ( p  <  0.001 ) . in contrast , during the trials without psat , all eels were able to swim up to 0.8  m  s. the results of trials 1 , 2 , and 5 ( without psat ) were comparable to those published recently ( palstra et al .
in a recent study , steinhausen et al ( 2006 ) observed that an external tag increased the oxygen consumption of cod at high swimming speeds , while optimal and critical swimming speeds were significantly decreased . in our study , with the much bigger psat , we observed severely impaired swimming already at low speeds .
the difference between the two studies may be due to the different mode of swimming , i.e. subcarangiform vs anguilliform , but more likely due to the rather large difference in extra drag ( corresponding to the cross section surface of the tag , i.e. 2 vs 13  cm respectively ) .
although tag technology is advancing , tags show negative effects in several studies on swimming performance , survival , behaviour and growth rates ( bridger and booth 2003 ; makiguchi and ueda 2009 ) .
negative effects of external tags on swimming performance are also found in other animals like penguins ( saraux et al . 2011 ) and seals ( hazekamp et al . 2010 ) .
our results show a dramatic effect of the smallest available psat on the swimming efficiency of european eels : a more than twofold higher oxygen consumption at all tested cruising speeds and a severely reduced swimming performance .
hence , smaller psats with much less interference on swimming performance are required to unravel the still mysterious journey to the spawning areas of european eels .
 the journey of the european eel to the spawning area in the sargasso sea is still a mystery . 
 several trials have been carried out to follow migrating eels with pop - up satellite tags ( psats ) , without much success . 
 as eels are very efficient swimmers , tags likely interfere with their high swimming efficiency . here 
 we report a more than twofold increase in swimming cost caused by a regular small satellite tag . 
 the impact was determined at a range of swimming speeds with and without tag in a 2-m swimming tunnel . 
 these results help to explain why the previous use of psats to identify spawning sites in the sargasso sea was thus far unsuccessful . 
Introduction
Materials and methods
Results and discussion