ﬀerences in size and growth rates of male and female
migrating Japanese eels in Pearl River, China
W. N. T*‡, H. R. L†, C. H. W* S. N. X*
*Department of Zoology, College of Science, National Taiwan University, No. 1, Sec. 4, Roosevelt Rd., Taipei, Taiwan 106, ROC and †School of Life Science, Zhongshan
(Sun Yet-Sen) University, Guangzhou 510275, PROC (Received 13 January 2000, Accepted 21 June 2000)
The Sr/Ca ratios in otoliths of silver Japanese eels Anguilla japonica in Pearl River, China, indicated that both sexes did not stay in brackish water and grew in fresh water from the glass eel stage until spawning migration. This did not support the hypothesis that females tended to distribute upstream and males might be restricted to estuaries. The back-calculated total length of males at glass eel stage was not significantly diﬀerent from that of females, indicating that the hypothesis that small glass eels became males and larger ones became females may not be true. The mean (..) age and total length of males at migration were 6·41·6 years and 48·34·5 cm, which were significantly smaller than for females, 8·31·6 years and 61·44·1 cm. The age of migration was related inversely to growth rate for both sexes. Growth parameters of the von Bertalanﬀy growth equation were K=0·21 cm year1, L`=55·7 cm and to=0·55 year for males and K=0·14 cm year1, L`=77·5 cm and
to=0·60 year for females. The diﬀerence in asymptotic length (L`) between males and
females may be because females postpone migration to achieve larger size for maximizing reproductive success. 2000 The Fisheries Society of the British Isles
Key words: eel; age; growth; otolith; microchemistry; migration.
The Japanese eel Anguilla japonica Temminck and Schlegel is distributed from the Philippines in the south, through Taiwan, mainland China and Korea to Japan in the north (Tesch, 1977). The eel is a commercially important cultured species in these Asian countries (Tzeng, 1985). It spawns in the Pacific Ocean west of Mariana Islands (14–16 N; 134–143 E) (Tsukamoto, 1992) in June and July (Tzeng, 1990). The eel larvae (leptocephali) migrate on the North Equatorial and the Kuroshio Currents to the coast, metamorphose to glass eels on the continental shelf, and then migrate to estuaries. As they move upriver, they become pigmented and are called elvers. For culture, glass eels are harvested in estuaries during their upstream migration in winter (Tzeng, 1985). The time for eel larvae to migrate from the oceanic spawning ground to the estuaries is c. 5–6 months (Tzeng, 1990; Tzeng & Tsai, 1992, 1994; Cheng &
Tzeng, 1996). Most glass eels migrate upstream and grow in fresh water until
maturation, but some of them may stay in brackish water until maturation
(Tsukamoto et al., 1998; Tzeng et al., 2000). In late autumn when the eels
‡Author to whom correspondence should be addressed. Fax: 886 2 23639570; email: wnt@ ccms.ntu.edu.tw
become mature, they metamorphose from yellow eels to silver eels and migrate downstream to the ocean for spawning (Tesch, 1977).
Otoliths of silver eels provide a complete history of the growth of individual eels, so that variation in growth may be observed between the sexes and within each of the sexes at all stages of their life history (Poole & Reynolds, 1996). Meanwhile the strontium (Sr) : calcium (Ca) ratio in otoliths is correlated positively with the ambient salinity in which fish growth, and it is feasible to track ontogenetic shifts in habitat use, especially by anadromous and catadromous fishes (Kalish, 1990; Tzeng, 1995, 1996; Tzeng et al., 1997, 1999,
In comparison with the American eel A. rostrata (Le Sueur) and the European eel A. anguilla (L.), the growth history of the Japanese eel has not been well studied. The age and growth of Japanese eel have been studied recently for the yellow eel stage, but without discriminating sexes (Guan et al., 1994). Female eels grow faster than males in European eel (Rossi & Colombo, 1976;Vøllestad
& Jonsson, 1986; Poole & Reynolds, 1996) and in the American eel (Helfman
et al., 1987). However, Holmgren & Mosegaard (1996) indicated that males grew faster than females at sizes where the gonads were not completely diﬀerentiated. It is not known if the sexes of the Japanese eel grow at diﬀerent rates. Vladykov (1966)proposed that small glass eels of American eels became males, whereas larger glass eels became females. Helfman et al. (1987)noted that females tended to distribute upstream, while males might be restricted to estuaries. To test these hypotheses, the age and growth of Japanese eels col-lected during their downstream spawning migration were studied by sex. The migratory environmental history of each sex was determined by the Sr : Ca ratios in otoliths.
MATERIALS AND METHODS
Silver Japanese eels were collected during their downstream spawning migration in a bag net along the riverbank at Fan-Yu in the lower Pearl River, c. 200–250 km from the South China Sea, in October and November 1996. The mean water temperature at the study site was 29 C in the summer and 15·4 C in the winter.
For each eel collected, total length was measured to the nearest 0·5 cm. Then the eels were dissected and sexes were determined from the histology of the gonad. The largest pair of otoliths (sagitta) were extracted, dried at 60 C for 10 min, embedded in a silicon rubber mould with petropoxy 154 (Palouse Petro Procuts, U.S.A.). Each otolith was ground and polished from the proximal side with sandpaper until the primordium was revealed, and then coated with carbon. Strontium (Sr) and calcium (Ca) concentrations were measured with a wavelength-dispersive X-ray spectrometer (Shimadzu-ARL-EMX-SM7). In the analyses of Sr and Ca, SrTiO3and CaSO4were used as standards. The
acceleration voltage of electrons was 15 kV and specimen current 0·01 A. The electron beam was focused on an area c. 5 m in diameter at intervals of 20 and 50 m, respectively, along the anterior-posterior axis of the otoliths (Tzeng & Tsai, 1994). The temporal changes in Sr : Ca ratios of eight randomly selected otoliths were used to reconstruct the previous migratory environmental history of each sex of the eels (Tzeng
et al., 1997).
After electron microprobe analysis, the otoliths were repolished and etched with 5% EDTA (ethylene diamine tetra-acetate, pH adjusted with NaOH to 7·4) for 3 min to enhance the annuli (Tzeng et al., 1994). The annuli were discriminated using a transmitted light microscope. Age was determined by counting annuli in the otolith. A total of 74 eels was examined for age determination.
The radii from primordium to glass eel mark (ro), annuli (rn) and the edge of otolith (R)
were measured. Then total lengths at glass eel stage (lo) and at annulus formation period
(ln) were estimated respectively by the Dahl-Lea formula (Francis, 1990):
ln=rnL R1 (1)
where, L is total length of the silver eel at capture. Mean lnwas used to estimate the
growth parameters of the von Bertalanﬀy growth equation by Ford-Walford plot (Ricker, 1958).
The significance of diﬀerence in mean values loand lnbetween the sexes was examined
by the t-test. Mean absolute growth rate (G) of the silver eels was calculated according to the formula:
where, lois total length at glass eel stage as estimated from ro, t is the age of silver eels
estimated from the counts of annuli in the otolith. Then the age of silver eels at downstream spawning migration in relation to their growth rate (G) was calculated by sex.
AGE AND GROWTH
Figure 1shows the glass eel mark located c. 145 m from the primordium, and
the subsequent five annuli on the sagittal plane of a 65-cm female silver eel otolith. The mark was formed as the glass eel arrived at the estuary. Beyond the mark, there are five fast growth opaque zones and five slow growth translucent zones (annuli). The annuli were dark under the transmitted light microscope.
The ages of silver females at downstream spawning migration (5–10 years, mean 8·31·6) were significantly higher than those of males (4–10 years, mean 6·41·6) (P<0·001). Similarly, total lengths of females (50·5–70·5 cm, mean 61·444·05) were significantly greater than lengths of males (42·0– 59·0 cm, mean 48·324·48) (P<0·001). Weights of females (160–490 g, mean 384·1470·91) were also significantly greater than those of males (95–250 g, mean 145·6138·86) (P<0·001) (Table I). These indicate that the male and female eels develop and mature according to diﬀerent life history strategies, males using a time-minimizing strategy and maturing at a smaller size while females using a size-maximizing strategy by postponing the age at migration.
Ages of the eels at downstream spawning migration were correlated negatively with the mean growth rates for both sexes, indicating that faster-growing eels became silver before slower-growing ones (Fig. 2).
The back-calculated mean (..) total length at glass eel stage was not significantly diﬀerent between males (lo=5·230·95 cm) and females (5·620·95 cm) (P=0·107). The back-calculated lowas close to the total length of glass eels during upstream migration in the estuary (Cheng & Tzeng, 1996). In addition, the mean total lengths for each of the ages up to 5 years old were not significantly diﬀerent between males and females (P=0·086–0·300). But beyond 6 years old, the lengths of females were significantly greater than those of males (P<0·001) (Fig. 3).
A theoretical growth curve of the eels was fitted by the von Bertalanﬀy growth equation for both sexes (Fig. 3), and the growth parameters were
K=0·21 cm year1(male) and 0·14 cm year1(female), L
`=55·7 and 77·5 cm,
and to=0·55 and 0·60 years. The K was larger and L`was smaller in males
than females, indicating that males approached the asymptotic length (L`) faster
than females. Ar R Pr 300 µm r5 r4 r3 r2 r1 r0
F. 1. Photograph showing glass eel mark (r0) and annuli (r1-5) on the otolith of a 65 cm female eel, Anguilla japonica (R, rostrum; Ar, antirostrum; Pr, postrostrum).
T I. Diﬀerences in age, total length and body weight of the silver Japanese eels at downstream spawning migration between males and females
Sex n Range Mean .. P-value
Total length (cm) 7 38 42·0–59·0 48·32 4·48 <0·001 8 36 50·5–70·5 61·44 4·05 Body weight (g) 7 38 95·0–250·0 145·61 38·86 <0·001 8 36 160·0–490·0 348·14 70·91 Age (years) 7 32 4–10 6·38 1·62 <0·001 8 30 5–10 8·30 1·62
TEMPORAL CHANGE OF Sr/Ca RATIOS IN OTOLITH
The time-series change of mean (..) Sr : Ca ratios in the otoliths was similar between males and females (Fig. 4). The ratios were higher in the interval from primordium to c. 100 m from the primordium, and ranged from 8 to 16103. The otolith for this interval was deposited during the leptocephalus stage of the marine phase. Thereafter, the ratios decreased gradually to a lower level (<1·0103) as the eels migrated into fresh water. The ratios remained c. 4·0103if the eels had stayed in brackish water (Tzeng et al., 1997). This indicates that both males and females grew in fresh water until the downstream spawning migration.
The growth history of eels is not well understood. It was proposed that females may occur in all appropriate estuarine and fresh waters; while males may be restricted to estuaries (Helfman et al., 1987). If this was true, the Sr : Ca ratios in male otoliths should increase after the glass eel stage (Fig. 4). However,
Growth rate (cm year–1) (b)
Age at migration (year)
0 3 6 9 12 3 6 9 15 12 (a) 0 3 6 9 12 3 6 9
F. 2. Correlation between age at downstream spawning migration and growth rate of the silver Japanese eel, A. japonica, (a) female; (b) male. (a) y=0·87x+14·38; r2=0·84; n=30. (b) y=0·81x+12·13; r2=0·69; n=32.
this was not the case. This indicates that males in this study left the estuary after the glass eel stage. However, it is not known if there is a segment of the male population that stayed in the estuary, because fish caught in the estuary were not examined. 10 80 Age (years) T otal length (cm) 0 60 40 20 9 8 7 6 5 4 3 2 1 * * * * *
F. 3. Growth curves of male () and female () Japanese eel A. japonica with a comparison of mean total length between the sexes at each age (vertical line, standard deviations): lototal length at glass eel stage (age=0); *, the mean total length diﬀered between the sexes at P<0·001.
Distance from primordium (µm) (b) Sr:Ca ratios ( × 10 – 3 ) 0 200 400 600 800 1000 1200 1400 10 5 1600 15 (a) 0 200 400 600 800 1000 1200 1400 10 5
F. 4. Time series changes in mean (..) Sr : Ca ratios in otoliths of silver eels, A. japonica: (a) male, n=4; (b) female, n=4.
The sex of the eel cannot be determined at the glass eel stage (Rossi &
Colombo, 1976). From a geographic decline in size–sex relationship, Vladykov
(1966)proposed that smaller glass eels of American eels became males, whereas
larger glass eels became females. A similar mechanism was proposed also for European eels (Bellini, 1970; Kuhlman, 1975). However, the back-calculated total length of the eel at the glass eel stage (lo) was not significnatly diﬀerent between males and females. This indicates that Vladykov’s (1966) hypothesis may not be true.
Many studies on the European eel indicated that females grew faster than males (Vøllestad & Jonsson, 1986; Vøllestad, 1992; Poole & Reynolds, 1996). On the contrary, Holmgren & Mosegaard (1996) indicated that there was no consistent diﬀerence in absolute length increase between small males and females, but below 40–60 g initial body weights, males displayed on average a faster weight increase than females. In the case of Japanese eel the back-calculated total lengths of males at each of the ages before downstream spawning migration was not significantly diﬀerent from those of females in the correspond-ing ages (Fig. 3). This indicated that the existence of a diﬀerence in growth rates of eels between males and females is still controversial.
The sex diﬀerentiation of the eels is labile and influenced by environmental factors (Colombo & Rossi, 1978) and the testis-like gonad of the yellow eels is primitive and possibly reversible (Colombo et al., 1984). In other words, the sex of eels is determined environmentally (Krueger & Oliveira, 1999). The Sr : Ca ratios in otoliths indicated that the migratory environmental history of the eels during the growing phase was similar between males and females. Accordingly, it is possible that the total length of males at each age before downstream spawning migration was consistent with that of females at the corresponding ages. On the other hand, the mean total length of females over 6 years old was significantly larger than that of males. This is because females postpone the age at migration to achieve larger size while males approach an asymptotic length. The phenomenon that males enter the migrating silver eel stage at lower mean age and size than females was found also in the European eel (Helfman et al.,
1987; Vøllestad, 1992) and other fishes, possibly because larger females can
produce more eggs to maximize their reproductive success (Wenner & Musick,
1974; Wootton, 1984).
This study was financially supported by the National Science Foundation, Republic of China (Contract No. NSC 88-2311-B-002-043). We thank T. F. Tsai and two anonymous reviewers for helpful comments on an early draft of the manuscript.
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