Environmental Biology of Fishes 71: 105–114, 2004.
2004 Kluwer Academic Publishers. Printed in the Netherlands.
Ecological aspects of the downstream migration of introduced European
eels in the Uono River, Japan
Takeshi Miyai, Jun Aoyama, Seji Sasai, Jun G. Inoue, Michael J. Miller & Katsumi Tsukamoto
Ocean Research Institute, The University of Tokyo, Minamidai, Nakano, Tokyo 164-8639, Japan
(e-mail: [email protected])
Received 12 December 2002
Accepted 6 January 2004
Key words: silver eels, Anguilla anguilla, age, growth, lunar cycle
Synopsis
We examined the species composition, timing of downstream migration, and biological characteristics of
eels using catches at three commercial weirs from 1996 to 1998 in the Uono River, Niigata Prefecture,
Japan, which is located farther north in the Japan Sea than where most Japanese eels, Anguilla japonica,
recruit. Analyses of a sub-sample of the 292 eels caught in the weirs found that 93.6% were introduced
European eels, Anguilla anguilla, that were sexually maturing silver phase eels. Their average age based on
otolith annuli was 10.2 years, indicating a relatively high average growth rate of 6.3 cm year)1. Catch
records in 1996 and 1997 indicated that downstream migration occurred sporadically from the middle of
August to the end of November and that catches generally coincided with abrupt increases in water
discharge and drops in water temperature. The highest catches in both years occurred between the last
quarter and new moon. These findings were similar to studies on this species in Europe and indicate that A.
anguilla can grow rapidly, begin maturation, and start downstream migration far from its native range.
This discovery of introduced eels initiating their spawning migration at the same time as A. japonica raises
concerns about the potential impact of interbreeding between species and the possible effects on the fishery
resources of A. japonica.
Introduction
The presence of introduced species of anguillid eels
in Japanese natural waters has been reported in
recent years as a result of their importation from
other parts of the world for aquaculture in Japan
(Tabeta et al. 1976, 1977, Zhang et al. 1999, Aoyama
et al. 2000a, Okamura et al. 2001). Eels are imported primarily during the glass eel stage, which
occurs around the time of recruitment when many
individuals enter freshwater. After becoming pigmented elvers, they then begin the yellow eel
growth phase, and when they begin reproductive
maturation, the silver eel phase occurs, which is
when they start their migration back to their
spawning areas in the ocean. According to the
Japanese Trade Statistics (1995–1997), Japan imports glass eels and cultured juveniles from over 10
countries for eel culture or for stocking in rivers.
Many of these countries are in regions where Anguilla japonica does not occur (e.g., France, Denmark, United States, the Philippines, Indonesia,
the Marshall Islands) and therefore they represent
importation of other species into Japan. There
have now been a total of three species of introduced
eels reported in Japan (Anguilla anguilla, Anguilla
australis, Anguilla rostrata), but additional undetected introduced species may now inhabit Japanese waters.
In some cases, these imported eels have escaped
from culture ponds or have been released for
natural production of eel stocks as alternatives to
106
the Japanese eel, whose glass eel catches have
drastically decreased in some recent years. Previous studies reported their presence in Japanese
waters, but no information is available about their
biological characteristics such as age, growth, and
downstream migration.
Because anguillid eels may be important predators in freshwater benthic habitats, introduced eel
species may not only compete with native Japanese
eels, but may also affect other aspects of the
aquatic communities they enter, especially in the
northern rivers adjacent to the Japan Sea, where
very few native Japanese eels recruit. Effective
conservation and management of these river systems and of the important Japanese eel fishery
resource requires an urgent research effort to
gather fundamental knowledge on the possible
ecological effects of these introduced eels.
Therefore, we examined the downstream migration of eels during the typical fall migration season
of temperate anguillid silver eels in the Uono River,
Niigata Prefecture, Japan, where both native and
introduced eels have been released. We describe the
species composition of a sub-sample of these silver
eels, which were genetically identified in a previous
study (Aoyama et al. 2000a), and present data on
the biological characteristics of body size, eye index, age, and growth of the European eels caught at
one of the weirs in 1997. The temporal patterns of
catches of eels at three weirs in 1996 and 1997 are
evaluated in relation to the environmental factors
of water temperature, water discharge, and lunar
cycle, to determine which factors may influence
their downstream migration in the Uono River.
Lastly, the ecological implications of the apparently normal freshwater growth phase of these
introduced eels and their initial reproductive
migration are discussed.
Study area
We conducted the study at three commercial weirs
(Urasa, Horinouchi, & Kawaguchi) set in the
Uono River, the largest tributary of the Shinano
River system in Niigata Prefecture, Japan
(Figure 1). The Uono River originally had no eels
because it is located beyond the northern range of
recruitment of the Japanese eel on the Japan Sea
or western side of Japan, but the stocking of
Figure 1. Study area and the locations of the commercial weirs
in the Uono River, a tributary of the Shinano River system, in
Niigata Prefecture of western Japan. Stars show the locations of
the three weirs, and the black circle shows the location of the
water temperature observation station at Nagaoka. The uppermost Urasa weir is about 130 km upstream from the river
mouth.
juveniles of both Japanese eels and introduced eel
species has been carried out since the 1960’s (F.
Isobe, personal communication). The weirs on the
Uono River were located in the middle part of the
river system, with the uppermost Urasa weir being
about 130 km upstream from the river mouth. The
other two weirs were about 10 km apart along the
lower part of the Uono River.
Methods and materials
Collection of eels
The eels were collected by weirs in the Uono River
that covered about 70–80% of the width of the
river (100–150 m). Each weir had a large fish guide
made of rocks in the center, and the current flow
near the cod end of each fish trap was strong enough that it would be difficult for eels to avoid
being caught. The cod ends of the capture nets had
a mesh size of 1.0 cm that would enable juvenile
yellow eels to be caught. The data on catches of
eels in the weirs were collected by the fisherman
that operated the weirs. For the species composition and biological characteristics analyses, we
sub-sampled eels directly from the weir catches,
107
measured, and weighed them and removed only
their heads and retained those for genetic species
identification and otolith analyses.
Species composition
Although Ege’s (1939) morphological characters
are used as a general method of species identification for the genus Anguilla, they have been recently shown to be unsatisfactory due to
underestimates of intraspecific variation (Aoyama
et al. 2000b, Watanabe 2003). We therefore applied polymerase chain reaction-restriction fragment length polymorphism (PCR-RFLP) analysis
of the mtDNA 16s rRNA gene, which has recently
been established as an effective method for species
identification in the genus Anguilla (Aoyama et al.
2000a,b). In 1997 we randomly sampled most of
the eels collected from July to November at the
Horinouchi weir (n ¼ 49) and obtained 9 additional specimens at that weir in September and
November in 1998, for a total of 58 specimens that
we used for PCR-RFLP analysis of species composition.
Characteristics of eels
We used the 36 individuals of A. anguilla caught at
the Horinouchi weir in 1997 for biological analyses. We measured total length (TL) and body mass
of all these eels at the weir to the nearest 1 cm and
10 g, respectively. We used 34 individuals of the
above sample for eye index analysis, which appears to be one of the best indicators of the onset
of reproductive maturation in silver eels of this
species (Pankhurst 1982). We classified eels with
an eye index less than 6.5 as sexually immature
adults, and those over 6.5 as sexually mature
adults (Pankhurst 1982).
We also determined the age of the same 34
specimens based on their number of otolith annuli.
We removed sagittal otoliths and stored them dry
at room temperature for several days before
embedding them in epoxy resin (SpeciFix-20,
Struers) and mounting them on glass slides. Subsequently, we ground the otoliths on both sides
along a longitudinal axis using 70 and 13 lm
whetstones to expose the core. We polished the
otolith slices with 6 lm diamond paste on a polishing wheel (Planopol-V, Struers), etched them
Figure 2. Otolith of an Anguilla anguilla silver eel (80 cm TL)
caught at the Horinouchi weir in 1997. TRZ shows the ‘transition zone’ corresponding to the beginning of the freshwater
growth phase. The annuli are marked with black dots.
with 1% HCl for 1–2 min and stained them with
1% toluidine blue (Figure 2). We counted the
numbers of annuli with a microscope, while
regarding the first clearly marked ring, or the
transition zone (Lecomte-Finiger 1992), as year
zero. The transition zone is assumed to correspond
to the beginning of the freshwater growth phase
(Lecomte-Finiger 1992). Therefore, the ‘age’ in
this study represents the number of years each eel
lived in freshwater.
We estimated the growth history of each individual based on a theoretical back-calculation.
Since we considered the transition zone as year
zero, the length at that time was uniformly set at
7.0 cm, which is the approximate length of glass
eels of this species when they recruit to freshwater
(Nagiec & Bahnsawy 1990, Svedang et al. 1996).
We defined the amount of growth attained during
the freshwater phase as TL-7.0 (cm), and we calculated the growth rate of each individual during
its freshwater life using the following formula:
growth rate ¼ (TL)7.0) age)1. We calculated the
theoretical body length at each age according to the
method described by Nagiec & Bahnsawy (1990).
Environmental conditions
To examine the relationship between environmental conditions and the onset of downstream
migration, we compared catch records of eels with
environmental data in the river system and with
daily and lunar cycles. The date and time of day
when eels were caught were recorded at the three
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weirs from July to November in 1996 and 1997.
We chose water discharge, water temperature, and
lunar phase as other environmental variables.
Water discharge was automatically measured
every hour at the Horinouchi Branch Office,
Hokuriku Regional Construction Bureau, Ministry of Construction, and the water discharge each
day was expressed by its mean value. Water temperature was measured in the same way at the
Nagaoka Branch Office (see Figure 1), and the
mean value was used as the daily water temperature. Short-term change in water temperature (T)
on a certain day (i) was represented as: DT(i) ¼
T(i + 1))T(i)1) where T(i) was the mean water
temperature of the day(i). Moon phase was
determined using a tide table.
Results
Catches of silver eels
A total of 292 specimens were caught at the three
commercial weirs during the study period, with
118 eels being caught in 1996 and 174 in 1997.
There were either very few or no eels caught in
July, and in both years more than 90% of the total
catch occurred between the middle of August and
the end of November, with the greatest numbers
being caught in September (42 eels, 35.6%) in 1996
and in October (76 eels, 43.7%) in 1997 (Figure 3).
The timing of catches showed sporadic patterns
in both years, with most of the catch being concentrated during relatively few days each year.
Because the timing of big catches tended to
approximately coincide among the three weirs, all
catch data of the three weirs were combined for
further analyses.
Species identification of migrating silver eels
Of the 58 specimens examined, 47 (38 in 1997, and
9 in 1998) individuals were successfully identified
using PCR. Of the 1997 specimens, 36 individuals
showed the haplotypes of the European eel, A.
anguilla, and the remaining two showed those of
the Japanese eel, A. japonica. In the 1998 specimens, eight individuals were identified as A. anguilla and one as the American eel, A. rostrata.
Thus, A. anguilla appeared to be the dominant
Figure 3. The daily catch of eels at the three weirs in the Uono
River in 1996 and 1997.
species in the Uono River. The eels analyzed by
PCR-RFLP were taken randomly throughout the
fishing season, so the high percentage of A. anguilla (93.6%) strongly suggests this species was the
most abundant downstream migrant in the Uono
River in 1997 and 1998.
Body size, eye index, age, and growth
The body sizes of the A. anguilla caught at the
Horinouchi weir in 1997 varied widely in TL from
49 to 87 cm (mean ± SD ¼ 69.4 ± 11.3 cm) and
in body mass from 250–1500 g (mean ¼
913 ± 331.0 g; Figure 4). The eye index exceeded
6.5 in all eels examined (range ¼ 6.9–13.9,
mean ¼ 9.2 ± 1.7), indicating that all eels were
sexually maturing, migrating silver eels (Pankhurst
1982). The frequency distribution of eye index was
skewed to lower values with a mode of 8.0–9.0
(Figure 4).
Estimated age of the eels also varied widely from
7 to 15 years, and there was considerable variation
in their growth rates. The frequency distribution of
age was skewed to lower values, with a mean of
10.2 ± 2.0 years and a mode at 8 years old, but
109
Figure 4. Total length, body mass, eye index, and age of Anguilla anguilla caught at the Horinouchi weir in the Uono River from July
to November in 1997.
only one specimen was 7 years old (Figure 4).
There was a significant positive correlation between the age and the TL (p < 0.01; Figure 5). A
large variation in both age and TL indicated that
the eels did not start their downstream migration
at a certain fixed age or body size. The growth rate
of A. anguilla in the Uono River ranged from 4.0
to 8.9 cm year)1, with a mean of 6.3 cm year)1.
The growth history of each individual estimated
through back-calculation showed no evidence of a
reduction in growth during freshwater life
(Figure 6), and every individual appeared to start
its downstream migration during an active growth
phase.
Figure 5. Relationship between age and total length of
migrating silver eels of Anguilla anguilla caught at the Horinouchi weir in the Uono River, July–November 1997.
Environmental conditions during downstream
migration
We could obtain data on the exact time of day of
collection of 245 (83.9%) out of the 292 eels that
were collected. Eel catches were highly concentrated during night time (Figure 7) and 82.4% of
the eels were caught between 18:00 and 06:00 h.
The largest catches occurred between 18:00 and
21:00 h, soon after sunset. Only 43 individuals
(17.6%) were caught during the daytime between
06:00 and 18:00 h, and in the time periods of
Figure 6. Estimated growth histories of Anguilla anguilla in the
Uono River based on otolith back-calculation.
110
Figure 7. Time of day when eels were caught at the three weirs
in the Uono River in 1996 and 1997. Bar at the bottom of the
figure shows nighttime (black) and daytime (white).
09:00–12:00 and 12:00–15:00 h, only one and six
eels were caught, respectively.
Water discharge varied greatly both in 1996
(48.2–287.4 m3 s)1) and 1997 (50.7–649.9 m3 s)1),
and the timing of eel catches appeared to coincide
with increases in water discharge (Figure 8). In
1996, eel catches coincided with spikes in water
discharge after mid-August when the first eels were
caught, and in 1997 eels were caught earlier at the
beginning of July, with a similar apparent corre-
spondence between discharge spikes and the catches of eels. During the period from August to
November when over 90% of total catch occurred,
the water discharges on positive catch days with
more than one eel being caught were significantly
larger than on negative catch days without eel
catches in both years (U-test, 1996: p < 0.0001,
1997: p < 0.05).
Water temperature peaked at about 25C in the
middle of August, and then dropped gradually to
below 10C at the end of November (Figure 8).
The temperature at which eel catches occurred
varied greatly from 9 to 24 C, corresponding to
the wide variation of the water temperature of the
river. However, the timing of catches tended to
coincide with drops in water temperature. The
short-term changes in water temperature (DT) on
the days of positive eel catches had significantly
lower values than those on the negative catch days
in both years (U-test, p < 0.01).
Eel catches were greatest between the last
quarter and new moon in both years, although
some eels were caught during almost all lunar
phases (Figure 9). There were relatively large catches of eels between the last quarter and new moon
in August, October and November in 1996, but
Figure 8. Water discharge (lower bold line), water temperature (upper line), lunar phase, and the eel catch (bars) at the three weirs in
the Uono River from July–November in 1996 and 1997.
111
Southern Hemisphere species, that were found in
Nagata River in Yamaguchi Prefecture, and by
Tabeta et al. (1977) about A. anguilla being found
in several rivers, suggesting that introduced eels
may have been prevalent in some Japanese waters
even at that time. Recently, Zhang et al. (1999)
showed that 31.4% of eels from Shinjiko Lake
and 12.4% from Mikawa Bay were A. anguilla. In
addition, Aoyama et al. (2000a) found one
migrating A. anguilla silver eel off Goto Island in
an area where Japanese silver eels were also collected (Sasai et al. 2001). Eels identified as A.
anguilla also appear to have been initiating a
spawning migration in the coastal region of
Mikawa Bay on the Pacific side of Japan (Okamura et al. 2002).
Biological characteristics of downstream migrating
A. anguilla
Figure 9. CPUE (catch per unit effort) of eels during each lunar
phase at three weirs in the Uono River from July to November
in 1996 and 1997. CPUE was calculated as the total number of
eels caught on the xth day of the lunar cycle divided by the total
number of each xth day from July to November of both years.
these catches also corresponded to spikes in river
discharge (Figure 8). In 1997, the period with the
largest catch also occurred between the last quarter and new moon when there was a spike in river
discharge. The largest catches of eels that were
made at other periods of the lunar cycle, such as
close to the full moon, were also associated with at
least moderate increases in water discharge.
Discussion
Introduced eels in Japanese natural waters
PCR-RFLP analysis of the silver eels from the
Uono River revealed that about 94% of the eels
examined were introduced A. anguilla. This is the
first report of such a high proportion of introduced
eels, and the individual A. rostrata is the first reported American eel in natural waters in Japan.
There have been several previous reports of the
presence of introduced eel species in Japanese
waters, including those by Tabeta et al. (1976)
about three individuals of A. australis, which is a
The eels examined during this study appear to
have been female silver phase A. anguilla that were
moving downstream during their spawning
migration. According to Pankhurst’s (1982) criteria, all individuals examined here were regarded as
sexually maturing adult silver phase eels, because
they all had an eye index of 6.5 or greater. The
silver eels examined during this study ranged from
49 to 87 cm TL and were probably almost all females, because previous studies have indicated that
males of A. anguilla over 50 cm TL are quite rare
(e.g. Frost 1950, Tesch 1977, Vollestad & Jonsson
1986, Pool & Reynolds 1996).
Based on a number of previous studies, Tesch
(1977) concluded that the TL of female European
silver eels during their downstream migration were
typically 54–61 cm and their age was 8–12 years,
and this is similar to the findings of more recent
studies (Vollestad & Jonsson 1986, Vollestad 1992,
Holmgren et al. 1997). In the Uono River, the TL
of the sub-sample of migrating silver eels was
considerably larger than those mentioned above,
but the estimated age was almost the same.
Therefore, the mean growth rate of A. anguilla
examined in the Uono River of 6.3 cm year)1 was
higher than other results reported for this species
in its native habitats in Europe (Table 1). One
possible reason for a high growth rate A. anguilla
in the Uono River may be that the water temperature during the summer (Figure 8) conforms to
112
Table 1. Growth rates of Anguilla anguilla from several areas within its native range and for the introduced eels in Japan of the present
study.
Study area
Growth rate (cm year)1)
Reference
Uono River (Japan)
Lake Constance (Germany)
River Barrow (N. Ireland)
Jeziorak Lake (Poland)
Camargue (France)
Burrishoole system (N. Ireland)
Imsa River (Norway)
6.3 (4.1–8.9)
4.8
3.3 (2.5–4.6)
4.1
5.3 (6.6 cm in 15 months)
1.4–1.5
6.2
The present study
Berg (1985)
Moriarty (1983)
Nagiec & Bahnsawy (1990)
Panfili et al. (1994)
Pool & Reynolds (1996)
Vollestad & Johnsson (1986)
the optimum range for growth of A. anguilla
(Kuhlmann 1979, Degani et al. 1988). Another
possible reason is that population densities of anguillid eels in the Uono River may be lower than in
their native European habitats, which could result
in a faster growth rate. This potentially lower
density of eels would be the result of the fact that
very few A. japonica glass eels recruit that far
north in the Japan Sea, and therefore most eels in
the Uono River may have originated from the
releases of juveniles by aquaculture facilities.
Environmental conditions and the onset of the
downstream migration
Our data showed that the downstream migration
of silver eels in the Uono River at the same latitude
as the southern part of the natural range of the
European eel, occurred mainly at night from the
middle of August to November, with a peak in
September or October, which agrees with observations in Europe (Tesch 1977). The large fluctuation of the daily catch suggested that there were
certain environmental factors that caused silver
eels to migrate at particular times during the
migration season. It is generally accepted that
downstream migration occurs mainly at night, and
this was the case in the present study, with almost
all eels being caught during night-time, especially a
few hours after sunset. Vollestad et al. (1986) and
Tesch (1977) also reported similar results.
It is widely recognized among scientists and
fishermen that water discharge also greatly influences the downstream migration of European silver eels (Frost 1950, Lowe 1952, Deelder 1954,
1970, Vollestad et al. 1986, Jonsson 1991). In our
study, the timing of catch clearly coincided with
the increase of water discharge, suggesting that the
downstream migration of silver eels in the Uono
River was closely related to increases in water
discharge in both years.
Eels were caught in a wide range of water temperature (9–24C) and did not show a threshold of
low temperature that initiated downstream
migration, as has been suggested by Haraldstad
et al. (1985) and Vollestad et al. (1986) in Imsa
River, Norway. A long-term effect of water temperature on downstream migration was suggested
by Vollestad et al. (1986) who used 10 years of
continuous observation in a Nordic river to suggest that downstream migration started earlier in
years with a lower mean temperature during the
summer. Although we cannot evaluate this
hypothesis with our data, local fishermen also report observing this phenomenon (F. Isobe, personal communcation). Water temperature may act
as a long-lasting ‘priming factor’ (Baggerman
1960) controlling a preparatory physiological
condition for migration such as metamorphosis
from the yellow to silver phase (Vollestad et al.
1986). Once the migration season had started in
the Uono River, the timing of catches of silver eels
appeared to coincide with abrupt drops in water
temperature. However, these decreases in temperature appeared to be closely related with the increases in water discharge caused by rainfall.
Because our field data can not clearly separate the
short term influences of these two factors, experimental studies in the laboratory are needed on this
subject.
Lunar phase appears to be another factor
influencing the downstream migration of silver
eels, but its effects may be overridden by other
environmental factors. In our study, the largest
numbers of eels were caught between the last
quarter and new moon both years, which was
113
consistent with previous reports (Frost 1950, Lowe
1952, Deelder 1954, Todd 1981, Pursiainen &
Tulonen 1986), but some eels were caught during
all lunar phases. Boetius (1967) experimentally
demonstrated an apparent innate rhythm in silver
eels that was synchronized to the lunar phase,
which resulted in an increase in escape activity of
male silver eels from an artificial tank. This
activity was at a maximum in the last quarter,
which agrees with this study and numerous field
observations that show increased catches of
migrating silver eels during this lunar phase (Frost
1950, Lowe 1952, Deelder 1954, Todd 1981, Pursiainen & Tulonen 1986). However, the effect of
cloudy weather that blocks much of the moonlight
and of increases in water discharge associated with
storms may result in some eels moving downstream regardless of the lunar cycle, as was observed during September of both years of this
study, when there were spikes of discharge close to
the full moon that coincided with catches of silver
eels.
et al. 2001). If introduced eels can migrate and
eventually spawn with A. japonica, it is possible
that they could form hybrids, as has been suggested for the two Atlantic anguillid eels (Avise
et al. 1990). The potential ecological and genetic
impacts of introduced eels on the fisheries resources of A. japonica in East Asia are unclear, but
the possibility of negative affects should not be
ignored, nor should the potential impacts on fish
assemblages in rivers that have not historically
contained eels.
Therefore, more ecological studies of the introduced eels in Japanese waters are needed, along
with studies on the formation and potential viability of hybrids, to ensure the conservation of
A. japonica. Finally, regulations prohibiting the
deliberate release of non-native anguillids (and
other fishes) in Japan should be instituted and
safeguards against accidental escape should be
strengthened.
Acknowledgements
Ecological implications of introduced eels
The most significant finding in this study was that
A. anguilla can grow rapidly, begin sexual maturation, and start its spawning migration as an
introduced species in the Uono River, far from its
native range. The characteristics of downstream
migration in the Uono River are similar to those
reported in Europe, implying that downstream
migration in the Uono River is ‘normal’ for A.
anguilla. This suggests that the same phenomena
could happen in other waters in Japan, as has been
apparently observed by Okamura et al. (2002), and
for other species of introduced eels.
Such ‘normality’ shown by introduced species
could cause serious problems for the conservation
of the fisheries resources of native species. Interspecies competition for habitat and food might
occur between introduced eels species and native
eels or other aquatic animals. The possibility also
exists that introduced eels could successfully migrate to the spawning area located to the west of
the Mariana Islands (Tsukamoto 1992) and interbreed with A. japonica. In fact, a sexually maturing
silver eel of A. anguilla was found in the East
China Sea together with A. japonica migrating to
the spawning area (Aoyama et al. 2000a, Sasai
The authors are grateful to F. Isobe (Urasa weir),
S. Nozawa (Horinouchi weir), the late K. Seki
(Kawaguchi weir) and all the staff at the weirs for
their kind cooperation in recording the catch data
and providing samples. We also thank Y. Seki of
Koide Branch of Niigata Prefectural Inland Water
Fisheries Experimental Station for his help in
sampling and valuable information.
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