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
108 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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