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. 2019 Nov 12;58:e34. doi: 10.6620/ZS.2019.58-34

Age, Growth, and Sex Ratios of the Giant Mottled eel, Anguilla marmorata, in Freshwater Habitats Near Its Northern Geographic Limit: A Comparison to Tropical Regions

Ryoshiro Wakiya 1,*, Hikaru Itakura 2, Kenzo Kaifu 3
PMCID: PMC6943202  PMID: 31966335

Abstract

To understand the latitudinal difference in the basic ecology of the giant mottled eel Anguilla marmorata, we measured its age, growth, and sex ratios in freshwater areas of Amami-Oshima Island, Japan (28.223°N–28.332°N and 129.329°E–129.439°E), near the northern geographic limit of its range and compared these biological characteristics with those observed in the tropical regions of Indonesia. A total of 109 A. marmorata were captured from three rivers on Amami-Oshima Island. The total length (TL) and age of sampled individuals varied across an order of magnitude (TL range: 119–1320 mm, mean: 385.5 ± 172.6; age range: 3–30 years, mean: 12.8 ± 4.9 years). Neither TL nor age differed among rivers. Male A. marmorata accounted for 88.5% of sexually differentiated individuals, which it contrary to previous results for males living in Indonesian watersheds where males were only found in small rivers and areas close to estuaries. Moreover, we found no males larger than 700 mm in TL and few males that were older than 20 years. The growth rates of male A. marmorata were significantly lower than those of females, and growth rates of sexually undifferentiated fish were significantly less than those of males. The mean growth rate of all individuals was 25.9 ± 6.6 mm/y, which is considerably lower than what has been found at lower latitudes, suggesting that growth differences occur along a latitudinal cline.

Keywords: Age, Anguilla marmorata, Freshwater, Growth rate, Sex ratio

BACKGROUND

Species in the genus Anguilla consist of catadromous fish that contain leaf-like leptocephalus larvae that migrate from open oceans to freshwater and estuarine habitats (Han et al. 2016; Chen et al. 2018; Higuchi et al. 2018). After metamorphosing into yellow eels, the fish spend most of their life in continental waters until they begin their downstream migration toward spawning grounds in open ocean. The anguillid eel consists of 19 species and subspecies distributed globally, with the exception of polar regions and the west coast of North and South America (Ege 1939; Aoyama 2003; Watanabe et al. 2004). The giant mottled eel A. marmorata is the most broadly distributed species in the genus, with a range from the south-east African coast to Asia and Polynesia (Ege 1939; Marquet and Galzin 1991; Marquet 1996). It is also one of the largest species in the genus, growing up to 2 m and 21 kg (Castle 1984). Despite this prominent ecology, to date, little basic biological information is available on the giant mottled eel, likely because compared with the Japanese eel A. japonica (Lee and Lou 2019) and the European eel A. anguilla, the mottled eel is not a major species in the aquaculture industry.

Previous studies on the ecology of A. marmorata have focused on its population structure (Ishikawa et al. 2004; Minegishi et al. 2008; Watanabe et al. 2008 2009; Gagnaire et al. 2009 2011; Donovan et al. 2012), spawning and recruitment (Arai et al. 1999a b 2001a b 2002a b; Sugeha et al. 2001; Robinet et al. 2003a b c 2007 2008; Kuroki et al. 2005 2009; Aoyama et al. 2007; Réveillac et al. 2008; Han et al. 2012; Leander et al. 2012; Aoyama et al. 2018). These studies found that there are multiple spawning populations in A. marmorata. Moreover, one of their spawning areas is located in the North Equatorial Current region of the western North Pacific Ocean, which is also the spawning area of the Japanese eel A. japonica. In addition, there has been some work on its migratory history, habitat use (Shiao et al. 2003; Chino and Arai 2010; Lin et al. 2012; Arai et al. 2013), and sexual maturation (Robinet et al. 2003c; Hagihara et al. 2012 2018a). To understand the ecology of this widespread species, it is important to examine its basic biological characteristics in not only the central part of its distribution in the tropics but also in the marginal areas in the subtropical and temperate zones. However, its biological characteristics have been studied only in tropical areas at low latitude (Hagihara et al. 2012 2018a b c).

Some studies reported that there are negative correlations between growth rates and latitudes in A. anguilla (Vøllestad 1992) and A. rostrata (Oliveira 1999; Jessop 2010). The wide latitudinal distribution range of A. marmorata suggests differences in the basic ecology of their life histories, such as age and growth, between low and high latitudes that cover different climatic zones. To understand the changes in the basic ecology of A. marmorata induced by differences in latitudes, we investigated the age, growth, and sex ratio of this species in freshwater habitats near the northern geographic limit of its range, and compared the results with those obtained in the lower latitude areas.

MATERIALS AND METHODS

Study area and sampling

This study was conducted in the Yakugachi, Sumiyo, and Kawauchi Rivers on Amami-Oshima Island, Kagoshima Prefecture, Japan (Fig. 1). This island is located approximately 380 km south of the southern tip of the Kyushu mainland and 250 km north of Okinawa. The average annual temperature of this island (1981–2010) is 21.6°C, which is 3.0°C higher than that of the mainland of Kagoshima, and the annual fluctuation is small. The annual precipitation is 2837.7 mm, with the monthly precipitation exceeding 150 mm even in winters; moreover, it is a particularly rainy part of Japan (statistics from Japan Meteorological Agency). The island is thought to be near the northern distribution limit of A. marmorata (Jacoby and Gollock 2014).

Fig. 1.

Fig. 1.

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Maps of the study area on Amami-Oshima Island, Kagoshima Prefecture, Japan. (a) Location of the Amami-Oshima Island in Japan. (b) Location of the study area on Amami-Oshima Island. (c) Map of the study area. Open circles indicate sampling sites for Anguilla marmorata.

The lengths of the Yakugachi, Sumiyo, and Kawauchi Rivers are 15.1 km, 16.8 km, and 10.6 km, respectively. They are largest rivers on this island. Nine sampling sites were set up across freshwater areas of each river (27 sites in total). All sampling sites were less than 20 m long and 15 m wide. To avoid sampling bias among study sites, sampling was conducted using a consistent protocol across all sampling sites. Anguillid eels were collected using an electroshocker (LR-20B; Smith-Root, Inc., Vancouver, WA, USA) and hand nets during the daytime, from August to September 2015. Captured fish were exposed to a subzero temperature of approximately -20°C to euthanize them as per previous studies using low temperature anesthesia on eels (Barbin 1998; Han et al. 2003; Fukuda et al. 2009; Itakura et al. 2015) to satisfy both national and institutional standards. Fish were maintained under this low temperature anesthesia until they died and were kept frozen until internal and external measurements were made.

Morphological observation

Each specimen was identified morphologically according to Watanabe et al. (2004). In this study, 5 A. japonica were captured in the Yakugachi River, and they were excluded from data analysis. The total length (TL) was measured to the nearest 1 mm. Sex was categorized as male, female, or undifferentiated (UD) based on visual inspection of gonadal morphology.

Age determination

The extracted sagittal otoliths were embedded in epoxy resin (EpoFix Kit, Struers; www.struers.com) and ground with a grinding machine (Discoplan-TS, Struers) to expose the core along the anterior-posterior direction in the frontal plane. Samples were polished further as described by ICES (2009). The otoliths were etched using 1% HCl for 1 min and stained with 1% Toluidine blue for 1–2 h to define the rings of the otolith (ICES 2009). Age was determined by counting the number of annual rings on the otoliths, according to Hagihara et al. (2018a). The first distinct transition check outside the nucleus (elver mark), which is thought to be associated with inshore recruitment to low salinity areas, was assigned age = 0.

Statistical analysis

All statistical analyses were performed with the R statistical package 3.3.2. To compare TL and age of A. marmorata between sex and rivers, we used a generalized linear model (GLM), which included TL and age as response variables (Gaussian distribution and log-link function) and sex and river as explanatory variables. To evaluate the relationship between growth rate and sex, age, and rivers, we used a GLM that included growth rate as the response variable (gamma distribution and log-link function) and sex, age, and river as the explanatory variables. When the effect of sex was statistically significant, we conducted pairwise multiple comparisons using the Tukey-Kramer method (glht in the package multcomp). To assess the relationship between TL and sex differentiation, we also used a GLM that included sex-differentiated (i.e., male or female) or UD as the response variable (binomial distribution and logit-link function) and TL as the explanatory variable.

RESULTS

A total of 109 Anguilla marmorata were captured in the three rivers on Amami-Oshima Island: 36 individuals from the Yakugachi River, 24 individuals from the Sumiyo River, and 49 individuals from the Kawauchi River. The total length of captured A. marmorata ranged from 119 to 1320 mm across rivers, with mean ± SD = 385.5 ± 172.6 mm. Age ranged from 3 to 30 years old after recruitment, with mean ± SD = 12.8 ± 4.9 years old (Fig. 2; Table 1).

Fig. 2.

Fig. 2.

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Frequency distributions of total length and age of A. marmorata collected from three rivers in Amami-Oshima Island, Japan. UD = sexually undifferentiated.

Table 1. Total length (TL), age, and growth rate of A. marmorata analyzed from each river in the Amami-Oshima Island, Japan. UD = sexually undifferentiated.

River name Sex n LT (mm) Age (years) Growth rate (mm year-1)
Mean ± SD Range Mean ± SD Range Mean ± SD Range
Yakugachi Female 0 - - - - - -
Male 15 439.1 ± 102.0 280–615 15.8 ± 2.7 11–20 24.7 ± 5.5a 17.7–35.3
UD 21 249.9 ± 63.0 148–381 8.5 ± 2.7 4–14 23.9 ± 4.1a 15.9–32.9
Sumiyo Female 3 862.0 ± 420.6 493–1320 20.3 ± 8.4 15–30 39.0 ± 8.3a 29.5–45.2
Male 12 451.2 ± 87.2 355–655 14.4 ± 2.2 10–18 28.6 ± 8.5a 17.9–50.2
UD 9 349.4 ± 96.8 200–521 12.7 ± 3.5 7–18 24.0 ± 5.8a 17.2–36.1
Kawauchi Female 3 738.7 ± 43.9 688–766 23.0 ± 4.0 19–27 30.6 ± 6.2ab 26.4–37.7
Male 19 499.6 ± 89.9 342–655 16.0 ± 3.4 11–23 28.7 ± 6.0a 19.6–40.4
UD 27 271.5 ± 84.1 119–435 9.4 ± 3.3 3–16 23.7 ± 6.2b 15.8–47.3
Total Female 6 800.3 ± 275.9 493–1320 21.7 ± 6.1 15–30 34.8 ± 8.0a 26 4–45.2
Male 46 467.2 ± 95.4 280–655 15.5 ± 2.9 10–23 27.4 ± 6.7b 17.7–50.2
UD 57 275.8 ± 84.7 119–521 9.6 ± 3.4 3–18 23.8 ± 5.3c 15.8–47.3
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Male A. marmorata were more abundant in our samples than females (female: 5.5%; male: 42.2%; UD: 52.3%), with 88.5% of the sexually differentiated individuals being male (Fig. 3B). This trend was consistent across all three rivers. The percent of females, males, and UD in our samples for the Yakugachi River were 0.0%, 41.7%, and 58.3%, respectively. For the Sumiyo River, percentages were 12.5%, 50.0%, and 37.5%, respectively, and for the Kawauchi River, they were 6.1%, 38.8%, and 55.1%, respectively (Table 1).

Fig. 3.

Fig. 3.

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Difference between Amami-Oshima Island and Sulawesi Island (Hagihara et al. 2018a) in growth rate and sex ratio of A. marmorata. A, Mean growth rate and SD of female, male, and UD in Amami-Oshima Island and Sulawesi Island. B, Sex ratio of sexually differentiated individuals in Amami-Oshima Island and Sulawesi Island.

Because both TL and age were not significantly different among rivers (TL: χ2 = 4.37, d.f. = 2, p > 0.05; age: χ2 = 1.43, d.f. = 2, p > 0.05), data obtained from the three rivers were combined. After combining, TL was significantly different among sex classifications (GLM: χ2 = 164.34, d.f. = 2, p < 0.001), with the TL of female A. marmorata being significantly larger than that of male A. marmorata (Tukey multiple comparisons test, p < 0.001). The ages also differed significantly among sex classifications (GLM: χ2 = 112.61, d.f. = 2, p < 0.001), with females being older than males of UD (Tukey multiple comparisons test, p < 0.001).

The probability of sex-differentiated A. marmorata was positively related to TL (GLM: coefficient ± SE = 0.024 ± 0.005, z = 4.96, p < 0.01). We found that 50% of individuals were sexually differentiated at 374 mm TL and 95% were differentiated when they attained a length of 494 mm.

The growth rate of A. marmorata was 25.9 ± 6.6 mm/y (mean ± SD), and they were significantly differentiated by sex (GLM: χ2 = 26.45, d.f. = 2, p < 0.001); the growth rate of male A. marmorata was significantly slower than in females, whereas the growth rates of UD were significantly slower than those of others (Tukey multiple comparisons test, p < 0.001) (Fig. 3A). In addition, the mean growth rate decreased significantly with age (χ2 = 9.13, d.f. = 1, p < 0.01), but they were not different among rivers (p > 0.05).

DISCUSSION

Growth rate

As expected, the estimated growth rates of A. marmorata in this study (Female: 34.8 ± 8.0 mm/y, Male: 27.4 ± 6.7 mm/y, UD: 23.8 ± 5.3 mm/y) were approximately one third lower than those of the same species from Sulawesi Island, Indonesia (Female: 94.2 ± 18.9 mm/y, Male: 82.2 ± 12.2 mm/y, UD: 74.1 ± 17.1 mm/y; Hagihara et al. 2018a) (Fig. 3A). A potential explanation for this pattern is that growth rates vary along a latitudinal cline, a results of differences in annual water temperatures and productivity of rivers. In fact, because Sulawesi Island is located on and near the equator, the average annual temperature is around 27°C (JICA 2008), much higher than 21.6°C on Amami- Oshima Island, although there are seasonal temperature differences. In particular, since the Central Sulawesi region, which was the main study area of Hagihara et al. (2018a), has an annual precipitation of 2500 mm or more, similar to Amami-Oshima Island. The difference in growth rates between the two regions is considered to be due to the difference in temperature. Some studies also show that there is a negative correlation between the latitude of habitats during the growth stage and growth rate in anguillid eels (A. anguilla: Vøllestad 1992; A. rostrata: Oliveira 1999; Jessop 2010). Physiological activity tends to increase with higher water temperatures at lower latitudes (Clarke 2003), suggesting that productivity may be higher at lower latitudes than in temperate rivers (Gross et al. 1988). This might explain the differences in growth rate of A. marmorata at lower latitudes compared with results in this study from the northern geographic limit.

On the other hand, the mean growth rate of female A. marmorata in this study was greater than that of males, consistent with previous reports on the same species inhabiting lower latitudes (Hagihara et al. 2018a), as well as other anguillid species (A. anguilla: Panfili et al. 1994; Svedäng 1999; A. rostrata: Oliveira 1999; Oliveira and McCleave 2002; Jessop et al. 2004; A. japonica: Tzeng et al. 2003). Furthermore, the mean growth rate of A. marmorata with undetermined sexual anatomy was lower than that in the other groups, indicating that growth rates are higher following sexual differentiation than during the few years after recruitment but before sexual differentiation. Another possible explanation for these findings is that individuals with lower growth rates in the UD group may not survive until sexual differentiation, indicating that only individuals with relatively greater growth survive long enough to differentiate into male or female.

Sex ratio

Although more than half of the collected A. marmorata were sexually undifferentiated, males accounted for 88.5% of the sexually differentiated individuals we sampled. This pattern differs substantially from what was found in multiple watersheds in the Central Sulawesi Island, Indonesia, where 22.8% of collected specimens were male (Hagihara et al. 2018a) (Fig. 3B).

This may be due to differences in river size rather than differences in latitude because Hagihara et al. (2018a b) found that the proportion of males was negatively correlated with increasing distance between the river mouth and the sampling area, and that high proportions of males were also observed at low latitudes. In a study by Hagihara et al. (2018a), the length of Poso River is approximately 100 km, whereas the length of each river conducted in this study is less than 20 km, which may explain the higher ratio of males. Consistent with this conclusion, studies in other anguillid eels also reported higher ratios of females at sites located at greater distances from the river mouth (A. anguilla: Sinha and Jones 1967; A. rostrata: Oliveira 1999).

Size at sex differentiation

Size at the time of sexual differentiation appears to differ among anguillid eel species. Based on the visual inspection of gonadal morphology, the results of GLM showed that by, the time the TL of Anguilla marmorata reached 494 mm, 95% of individuals were sexually differentiated (Fig. 4). In a study that visually inspected gonadal morphology of 413 individuals of A. japonica, 95% of fish were sexually differentiated at a TL of 406 mm (Ministry of Environment 2015 2016). A. marmorata becomes sexually differentiated at a body size relatively larger than the temperate species, A. japonica. Moreover, Oliveira and McCleave (2000) reported that the sexual differentiation of A. rostrata was complete at a TL of 270 mm based on histological analysis. Although the method for sex determination used in Oliveira and McCleave (2000) was slightly different from that used in the present study, the results of these studies suggest that A. marmorata is sexually differentiated at a larger body size than A. rostrata. Because data on the size at which sexual differentiation occurs in A. marmorata in different regions is limited, the latitudinal variation in the size at sexual differentiation should be investigated in future studies.

Fig. 4.

Fig. 4.

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Probability of sexual differentiation related to total length of A. marmorata collected from three rivers on Amami-Oshima Island, Japan. The black lines and shaded areas indicate the regression lines and 95% confidential intervals, respectively.

Size and age at downstream migration of male

The male A. marmorata collected in this study were less than 700 mm long, and the majority of them were less than 20 years old (range 10–23 years old). This finding, at least in terms of TL, is consistent with the results of previous studies, in which downstream migrating male A. marmorata were captured on Réunion Island, France (708 mm and 10 years; Robinet et al. 2003c) and Sulawesi Island, Indonesia (683 mm and 7 years; Hagihara et al. 2018a). This pattern suggests that many of the A. marmorata collected on Amami- Oshima Island may represent individuals migrating downstream. Given that downstream migration of anguillid eels is thought to be related to size rather than age (Aoyama and Miller 2003), downstream migration of A. marmorata may also be related to body size.

The biggest male A. marmorata captured on Amami-Oshima Island was 655 mm, which was smaller than 5 of the 6 females, including the largest individual (1320 mm). There have been many reports of other anguillid eels that also found females grew to larger sizes than males (A. anguilla: Vøllestad 1992; Poole and Reynolds 1996; A. rostrata: Oliveira 1999; Jessop 1987; A. japonica: Lin and Tzeng 2009). Therefore, the results from this study may represent a general pattern of sexual dimorphism in anguillid eels.

CONCLUSIONS

The present study is the first to provide information on the size, age, sex ratio, and growth rate of Anguilla marmorata from Amami-Oshima Island, Japan, which is close to the northern limit of its distribution, and to compare these biological characteristics with those previously obtained at a lower latitude. A. marmorata collected in Japan showed slower growth rate and longer longevity in males than those collected in Indonesia. Despite the widespread distribution of A. marmorata, regions where studies on this species were conducted are still limited. Further studies should investigate the basic biological characteristics of A. marmorata from different regions, which will provide a more comprehensive understanding of the ecology of this species, as well as anguillid eels in general. This type of comparison of life history studies based on latitudes is especially important to provide baseline data for predicting changes in the ecology of angullid eels under the effects of global climatic changes.

Acknowledgments

Acknowledgments: We thank T. Shiosaki for the useful information of the rivers and the fisheries cooperative association of Naze in Amami-Oshima Island for storing our samples. We also thank K. Yonekubo and T. Yoshinaga for the otolith preparation and helpful comments on earlier drafts of the manuscript.

Footnotes

Authors’ contributions: All authors conceived the ideas, designed the methodology, and collected the data; RW analyzed the otolith samples; RW and HI analyzed the data; RW led the writing of the manuscript. All authors contributed critically to the drafts and gave final approval for publication.

Competing interests: The authors declare no competing interests.

Availability of data and materials: Relevant data are not currently available because we are drafting another manuscript using some parts of these data.

Consent for publication: Not applicable.

Ethics approval consent to participate: Captured fish were exposed to a subzero temperature of approximately -20°C to euthanize them, as per previous studies using low temperature anesthesia on eels, to satisfy both national and institutional standards.

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