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Article

Early Life History and Recruitment Processes of a Tropical Anguillid Eel Anguilla marmorata to the Pacific Coast, as Revealed by Otolith Sr:Ca Ratios and Microstructure

Environmental and Life Sciences Programme, Faculty of Science, Universiti Brunei Darussalam, Jalan Tungku Link, Gadong, Bandar Seri Begawan BE 1410, Brunei Darussalam
Submission received: 26 April 2022 / Revised: 22 May 2022 / Accepted: 22 May 2022 / Published: 24 May 2022
(This article belongs to the Special Issue Metals in Biology)

Abstract

:

Simple Summary

Examination of strontium:calcium (Sr:Ca) ratios in otolith has elucidated substantial information on the life history of fishes. This study has found that a drastic decline in otolith Sr:Ca ratios, indicated the initiation of metamorphosis from larva to juvenile in a tropical anguillid eel Anguilla marmorata. Based on the criterion, the current study revealed the early life history and recruitment processes of A. marmorata. Furthermore, the larval transportation, dispersion processes and recruitment dynamics to the Pacific coast of A. marmorata are determined by means of the otolith microchemical analysis in combination with abiotic parameters such as oceanic currents.

Abstract

Recent progress in otolith microchemistry especially in strontium:calcium (Sr:Ca) ratios has revealed significant features of life histories in fishes. A catadromous eel, Anguilla marmorata, has the widest distribution among anguillid eels throughout the Indo-Pacific region. However, its dispersal and recruitment mechanisms in the ocean are still unknown. The temporal and spatial variations of early life history characteristics in a tropical anguillid eel A. marmorata were examined by means of otolith Sr:Ca ratios and microstructure to understand the larval transport and recruitment processes to the coasts in the Pacific region. Durations of the larval stage and age at recruitment to the southern part of Japan ranged from 79 to 157 d and 113 to 192, respectively. No significant differences were found between recruitment months in those parameters. The early life characteristics such as larval duration and age at recruitment were constant throughout the recruitment period in the southern part of Japan. The early life history characteristics in combination with the oceanic current regime possibly determine the larval transportation and dispersion processes and further recruitment dynamics to the Pacific coast of A. marmorata. The present study also provides useful information on its biogeographic distribution in the species as determined by otolith Sr:Ca ratios and microstructure.

1. Introduction

The giant mottled eel Anguilla marmorata is widely distributed in the Indo-Pacific region and is one of the most widespread freshwater eels in the region [1,2]. A. marmorata has several populations throughout the distribution range and grows to much larger sizes than other eels [3,4,5,6]. Similar to other anguillid eels, this tropical species spawns in the ocean. These larvae are then transported by oceanic currents during the larval stage, before experiencing a distinct metamorphosis into glass eels before recruitment to coastal waters [1,7]. The oceanic life characteristics such as the larval (leptocephalus) phase and metamorphosis timing together with oceanic current systems would determine the biogeographical distribution of anguillid eels. The prospective for prolonged larval transportation in combination with oceanic current systems could be responsible for the worldwide distribution and speciation of the species [8]. However, there is currently little information and evidence available on the spawning areas and larval transportation mechanisms of A. marmorata.
Fish otolith is a biomineralized aragonite crystalline structure principally constructed from calcium carbonate with small amount of an organic matrix [9]. Alkaline earth metals and other elements (e.g., Mn, Zn, Pb) likely substitute for calcium (Ca) due to the fact that they have Ca-like properties [9,10,11,12]. These elements are incorporated into otolith growth increments and are affected by environmental factors such as temperature and salinity and physiological factors [9,10,11,12,13]. Furthermore, otolith growth increments are deposited daily in many fish during their larval and juvenile stages [9]. Otoliths are metabolically inert, and hence once the elements are deposited in the otolith, it perpetually records the environmental surroundings encountered by the fish throughout their life history [9,14]. Among elements, strontium (Sr) is widely used to reconstruct fish migration and life history because the Sr concentrations or Sr:Ca ratios in otoliths are positively correlated with salinity in waters [9,10,11,12,13,14].
In the anguillid eels of the genus Anguilla, otolith Sr:Ca can reconstruct the life history, migratory history and habitat use throughout their lives [7,8,11]. The application of otolith Sr:Ca ratios to reconstruct the migratory history has revealed a diverse migration strategy in various species such as A. anguilla [15,16], A. japonica [17,18,19,20,21,22,23,24], A. rostrata [25,26], A. australis schmidtii and A. dieffenbachii [27], A. marmorata [28,29,30,31,32], A. bicolor bicolor [14,33,34,35] and A. bicolor pacifica [31]. Progress in otolith strontoium:calcium (Sr:Ca) ratios techniques in combination with the microstructure has also elucidated many crucial details of the early life histories of anguillid eels such as the timing of onset and length of duration of metamorphosis [36,37,38,39,40,41,42,43,44]. During the early life phase, an abrupt decline in Sr:Ca ratios, coincident with a marked increase in otolith increment widths, indicated the onset of metamorphosis. Metamorphosis is apparently completed before the maximal peak of otolith incremental width. Hence, otolith Sr:Ca ratios are believed to be a powerful tool for reconstructing the life history characteristics in the eels [7,38].
In the present study, life history features such as larval duration and age at recruitment were examined by means of otolith Sr:Ca ratios and microstructure of A. marmorata glass eels recruited to the Japanese coast. Temporal variations of early life history characteristics were examined throughout the recruitment period in the southern part of Japan. Furthermore, to understand the spatial variations, previously published data on the early life characteristics of A. marmorata in Fiji [44], Indonesia [36,37,39,40], Japan [39,41,43], Philippines [36,39,43] and Taiwan [39,41,43] in the Pacific region were also examined. There have been several studies conducted in an attempt to understand the spatial variation in the early life history of A. marmorata [36,37,38,39,40,41,42,43,44]. However, there have been very few studies conducted on the temporal variation throughout the recruitment period in the life history of A. marmorata [37] as well as other anguillid eels. It is indispensable to study the spatial and temporal variation of early life history traits for understanding the valid mechanisms of larval transportation and recruitment in the species. The present results establish the foundation for a discussion of larval transportation and recruitment processes to the Pacific coast in relation to the oceanic current systems in the region.

2. Materials and Methods

2.1. Ethics Statement

Our protocols followed the ethical guidelines for the use of animals of the Universiti Brunei Darussalam (UBD) and were approved by the animal ethics committee at UBD (Approval Code: UBD/RSCH/1.4/FICBF(b)/2021/037; Approval Date: 15 September 2021).

2.2. Animals

A. marmorata glass eels were sampled during the nighttime at the time of the new moon by means of scoop and dip nets on the shore of Tanegashima Island, southern Japan, on 18 December in 1998 and 17 January, 16 February and 17 March in 1999 (Figure 1, Table 1). All specimens were kept for several years in ethanol until ready for experiment. Elemental composition in otolith is not influenced by ethanol preservation [45]. Each total length (TL) was measured and the pigmentation stage was determined following Bertin [46], respectively.

2.3. Otolith Preparation

Otoliths were collected from all fish and were fixed in epoxy resin (Struers, Epofix, Copenhagen, Denmark). All otoliths were ground and polished in the sagittal plane by a grinding machine (Struers, Discoplan-TS, Copenhagen, Denmark) and an automated polishing wheel (Struers, Planopol-V, Copenhagen, Denmark) with 6 µm and 1 µm diamond paste, respectively. After polishing, otoliths were cleaned and rinsed using an ultrasonic bath and Milli-Q water for otolith Sr and Ca analyses.

2.4. Otolith Sr and Ca Analyses

All otoliths were platinum and palladium (Pt-Pd) coated for electron microprobe analyses. Sr and Ca levels in otoliths were determined across the longest axis by means of a wavelength-dispersive X-ray electron microprobe (JEOL JXA-8900R, Tokyo, Japan). Calcite (CaCO3) and strontianite (SrCO3) were used as standards [39,41]. The beam current and accelerating voltage were 12 nA and 15 kv, respectively. The electron beam had a 1 µm diameter while measuring 1 µm space on the otolith. The data depict the mean of three quantifications (4.0 s in each counting time). Microprobe quantification points could be identified along the burning transect on the otolith which were allocated to otolith increments after the otolith increment analysis.

2.5. Otolith Increment Analysis

After the Sr and Ca analyses, all otoliths were etched with 0.05 M HCl after removing the coating. Otolith microstructures were observed by means of scanning electron microscope (SEM, Hitachi S-4500, Kyoto, Japan) on the sagittal plane [39,41]. Because otolith increments in A. marmorata have validated the daily periodicity [52], similar to other anguillid eels such as A. japonica [53,54,55], A. rostrata [56] and A. celebesensis [57], the increment number can be used as the daily age (Table 1).

2.6. Interpretation of Early Life History

Early life history characteristics such as the timing of onset of metamorphosis and duration of the leptocephalus stage were determined using SEM photographs (Figure 2) based on previous studies concerning anguillid eels such as temperate species, A. anguilla [58], A. rostrata [58], A. japonica [38,42,59], A. australis [60,61] and A. dieffenbachii [40] and tropical species, A. marmorata [36,37,38,39,40,41,42,43,44,62], A. celebesensis [36,37,63], A. bicolor bicolor [36], A. bicolor pacifica [37,62,64] and A. reinhardtii [61]. According to these studies, for otolith Sr:Ca ratios and the microstructure of anguillid eels, the age at which an abrupt increase in the widths of the otolith increments can be seen in combination with a drastic decrease in otolith Sr:Ca ratios is defined as the initiation of metamorphosis (Figure 2 and Figure 3). The length of the metamorphosis phase was determined as the period between the initiation of a significant increase in the widths of the otolith increments and the maximal otolith width (Figure 2 and Figure 3). Age at recruitment was examined by counting the increment number from the presumed hatching check and the edge of the otolith (Figure 2 and Figure 3).

2.7. Statistics

Total length, otolith radius and age at the onset of metamorphosis and recruitment among recruitment periods were analyzed by an analysis of variance (ANOVA) to determine if there was significant variation in these parameters between months and thereafter multiple comparison tests were carried out using Scheffe’s test. Significance of the regression slope and correlation coefficient was analyzed by Fisher’s Z-transformation and an analysis of covariance (ANCOVA) which is a model that relies on linear regression wherein the dependent variable is linear to the independent variable.

3. Results

The total lengths and the radii of A. marmorata glass eels ranged from 44.8 to 54.2 mm and from 133.1 to 163.8 µm, respectively (Table 1). There were no statistically significant differences in total length and otolith radius between months (December 1998, January to March 1999) (ANOVA, p > 0.05). Pigmentation stage was determined by either VA or VB, and was limited to only the caudal, rostral and skull parts on the body surface. The pigmentation stage suggests that all glass eels have been newly recruited to the coast.
Durations of larval stage (ages at onset of metamorphosis) ranged from 79 to 157 d (Table 1). There were no statistically significant differences between recruitment months (ANOVA, p > 0.05). Lengths of metamorphosis stage ranged from 10 to 27 d (Table 1). No significant difference was found between the four recruitment months (ANOVA, p > 0.05). Age at recruitment to the coast ranged from 113 to 192. There were no statistically significant differences in the ages between recruitment months (ANOVA, p > 0.05).
Linear relationships were found between the duration of the larval (leptocephalus) stage and recruitment (Fisher’s Z-transformation, p < 0.0001) (Figure 4).

4. Discussion

The high Sr:Ca ratios during the larval stage are believed to emanate the substantial accumulation of gelatinous extracellular materials that were incorporated into their bodies just before initiation of metamorphosis [59]. The materials consisted of sulfated glycosaminoglycans (GAG), which are transformed during the metamorphosis [65]. GAG has an affinity to alkaline earth metals especially Sr, and hence, otolith Sr:Ca ratios gradually increased alongside the larval growth. During the metamorphosis stage, GAG is broken down and is excreted outside of the body, leading to the drastic depletion of otolith Sr:Ca ratios [38,59]. In addition, otolith (somatic) growth would accelerate at the initiation of metamorphosis from larva to juvenile [38,59] and hence, otolith growth increments sharply increased as an indication of metamorphosis. After completion of metamorphosis, the growth would gradually decrease to regular growth of the juvenile stage. Otolith Sr:Ca ratios averaged approximately 10 × 10−3 at the core, subsequently increased to a maximum level averaging approximately more than 15 × 10−3 in the second phase and markedly decreased thereafter toward the edge (Figure 3). These fluctuation patterns in otolith Sr:Ca ratios are commonly found in anguillid eels such as A. anguilla and A. rostrata [58], A. australis [60,61] and A. dieffenbachii [40] and tropical eels A. celebesensis [36,37,63], A. marmorata [36,37,38,39,40,41,42,43,44,62], A. bicolor bicolor [36], A. bicolor pacifica [37,62,64] and A. reinhardtii [61]. Therefore, these otolith features could apply to the early life history analyses in anguillid eels.
The correlation between the duration of the larval age and age at recruitment apparently indicated that juveniles that metamorphosed at a younger age tended to recruit to the coast at a younger age (Figure 4). Metamorphosis could be an important biotic cue to larval transportation, migration and recruitment to coastal waters. The same phenomena were also found in the temperate eels, A. anguilla and A. rostrata [58], A. australis [60,61] and A. dieffenbachii [40] and tropical eels A. celebesensis [36,37,63], A. marmorata [36,37,38,39,40,41,42,43,44,62], A. bicolor bicolor [36], A. bicolor pacifica [37,62,64], A. reinhardtii [61], A. obscura and A. megastoma [44]. This correlation between the larval duration and the age at recruitment is a common phenomenon and is a key inshore migration mechanism during the oceanic migration phase in anguillid eels.
The life history traits of the larval period, length of metamorphosis stage and recruitment age to the coast were constant throughout four recruitment months from December 1998 to March 1999 in the southern part of Japan (Table 1), possibly as a consequence of constant larval growth during the periods. There are few reports available on the evaluation of temporal variations in the life history characteristics in anguillid eels. In tropical eels, the early life history parameters of A. marmorata, A. celebesensis and A. bicolor pacifica, which recruited to the Indonesian coast, were constant throughout the year [37]. Their stable larval growth and timing of metamorphosis throughout the year would be the result of constant age at recruitment in tropical anguillid eels. Furthermore, monthly spawning with no seasonal spawning was found in tropical anguillid eels [37,66,67], possibly a result of constant life history traits throughout the year.
The life history traits of A. marmorata were essentially the same in the Pacific region, with the mean length of the larval stage ranging from 110 d (Philippines) to 128 d (Indonesia) and the mean recruitment age ranging from 145 d (Philippines, Taiwan and Japan) to 155 d (Indonesia) (Table 2). The larval duration and age at recruitment of A. marmorata were found to be constant throughout the year along the Indonesian coast [37]. These findings suggest that early life history traits such as age at recruitment and metamorphosis would be consistent in A. marmorata in the Pacific region, regardless of their different geographic locations, oceanic transportation routes and growth histories. However, in Réunion Island, located in the Indian Ocean, mean larval length and mean age at recruitment of A. marmorata were 97 and 120 days, respectively [68], shorter than those found in the Pacific region. Differences in the life history traits of A. marmorata between the Indian Ocean and the Pacific Ocean may suggest different population structures across the Indo-Pacific.
The mean TLs of A. marmorata at recruitment (44.8 to 54.2 mm) were 10 to 20 mm smaller than those of temperate anguillid eels even at the same developmental stage [39]. The smaller sizes of tropical glass eel species, such as A. bicolor bicolor (45.5–54.5 mm) [36,68], A. bicolor pacifica (48.6–54.5 mm) [37,64], A. celebesensis (44.7–52.8 mm) [36,37,63], A. reinhardtii (47.6–52.2 mm) [61], A. bengalensis labiata (51.0–52.5 mm) [68], A. mossambica (43.0–53.5 mm) [68,69], A. obscura (46.9–53.0 mm) [44] and A. megastoma (47.8–53.1 mm) [44], were consistent with the size of A. marmorata, when they recruited to tropical coastal areas. Furthermore, differences in TLs of fully developed larvae have also been found between temperate and tropical species. The TLs of fully developed larvae in temperate anguillid eels were found to be 60 mm in A. japonica [70], 70 mm in A. rostrata [71] and 75 mm in A. anguilla [1]. However, those of tropical anguillid eels in the Indo-Pacific region including A. marmorata have been found to be approximately 50 mm [62]. The larval growth rate of A. marmorata was found to be in the range of 0.38 to 0.43 mm day−1 [62]. Although the durations of the larval stage were similar between A. marmorata and A. japonica [43], the growth rate of A. marmorata is less than that of the temperate eel, A. japonica (0.56–0.59 mm day−1) [72,73]. The smaller larval growth rate found in A. marmorata would be due to the smaller size of the fully developed larval and juvenile at recruitment.
There is little information available on the life history of A. marmorata throughout the geographical distribution range, although the species is a geographically widespread species in the Indo-Pacific [7,8,74]. Information on the reproduction and migration ecology of A. marmorata is still unknown [75], and only one spawning site has been discovered in the North Equatorial Current (NEC) west of the Mariana Islands in the northwest area of the Pacific (Figure 1) [50]. A. marmorata larvae entrapped in the Kuroshio Current (KC) would be further transported northward to northern Philippines and East Asian countries. In contrast, the larvae entrapped in the Mindanao Current (MC) would be transported across the east coast of the southern part of the Philippines. Thereafter, other larvae would be further transported westward by means of water flows from the Mindanao Eddy area in the southeast region of the Philippines to the Celebes Sea [47,48] and then A. marmorata glass eels recruit to the Sulawesi Island in the east of Indonesia and adjacent to the Celebes Sea areas.
These two transportation routes and mechanisms of A. marmorata larvae are supported by the population genetic research [3,4,5,6]. A. marmorata specimens from Indonesia, Japan, Philippines and Taiwan were found to belong to the same northern population, which was apparently separated from five other populations dispersed throughout the distribution range. In the northwest Pacific region, A. marmorata would migrate downstream to spawn in the NEC and then their larvae would be widely transported and dispersed over 30 degrees of latitude. Differences in the length of the larval stage and the age at recruitment among the sites might be due to the different distances from the spawning site in the NEC, seasonal fluctuations in the velocity of NEC, KC and MC [49] or the fluctuations and dynamics of the coastal currents around the recruitment sites.
However, in A. marmorata from Fiji in the South Pacific, larval transportation mechanisms and routes are highly speculated because little research has been conducted [51]. Further intensive research on the early life history by means of otolith Sr:Ca ratios and the microstructure and geographic distribution of A. marmorata larvae in combination with ocean current dynamics and fluctuations is needed to determine the spawning area and larval transportation mechanisms of A. marmorata in the South Pacific Ocean.

5. Conclusions

The temporal and spatial variations in early life history characteristics in a tropical anguillid eel, A. marmorata, in the Pacific region were revealed using otolith Sr:Ca ratios in combination with the microstructure. The life history traits of the larval period, length of metamorphosis stage and recruitment age to the coast were constant throughout the recruitment period. The life history traits of A. marmorata were overlapped and essentially the same in the Pacific region, with the mean length of the larval stage ranging from 110 d to 128 d and the mean recruitment age ranging from 145 d to 155 d. Metamorphosis at a younger age caused recruitment to the coast at younger ages, suggesting that metamorphosis is a key factor in determining the inshore migration to coastal areas. The early life history characteristics in combination with the oceanic current regime possibly determine the larval transportation, dispersion processes and recruitment dynamics to the Pacific coast of A. marmorata. The present study could provide useful information on its biogeographic distribution in the species based on otolith Sr:Ca ratios and microstructure.

Funding

This work was supported by the Universiti Brunei Darussalam Faculty/Institute/Center Research Grant (UBD/RSCH/1.4/FICBF(b)/2020/029 and UBD/RSCH/1.4/FICBF(b)/2021/037).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Data are provided in the article.

Conflicts of Interest

The author declares no conflict of interest.

References

  1. Tesch, F.W. The Eel, 3rd ed.; Blackwell Science: Oxford, UK, 2003. [Google Scholar]
  2. Arai, T. Taxonomy and Distribution. In Biology and Ecology of Anguillid Eels; Arai, T., Ed.; CRC Press: Boca Raton, FL, USA, 2016; pp. 1–20. [Google Scholar]
  3. Minegishi, Y.; Aoyama, J.; Tsukamoto, K. Multiple population structure of the giant mottled eel, Anguilla marmorata. Mol. Ecol. 2008, 17, 3109–3122. [Google Scholar] [CrossRef] [PubMed]
  4. Gagnaire, P.A.; Minegishi, Y.; Zenboudji, S.; Valade, P.; Aoyama, J.; Berrebi, P. Within-population structure highlighted by differential introgression across semipermeable barriers to gene flow in Anguilla marmorata. Evolution 2011, 65, 3413–3427. [Google Scholar] [CrossRef] [PubMed]
  5. Arai, T.; Taha, H.; Mohd-Riduan, M.N.; Mokti, S.S.A. Molecular and morphological evidence for the identity of the giant mottled eel, Anguilla marmorata in Southeast Asia. Trop. Ecol. 2020, 61, 429–436. [Google Scholar] [CrossRef]
  6. Zan, N.D.; Sarbini, A.; Taha, H.; Tan, I.V.; Azri, A.; Kahar, R.; Metali, F.; Ahmad, N.; Arai, T. Occurrence and ecological implication of a tropical anguillid eel, Anguilla marmorata, in Brunei Darussalam, Borneo Island. Zoologia 2020, 37, e39468. [Google Scholar] [CrossRef]
  7. Arai, T. Migration ecology in the freshwater eels of the genus Anguilla Schrank, 1798. Trop. Ecol. 2022, 63, 155–170. [Google Scholar] [CrossRef]
  8. Arai, T. Ecology and evolution of migration in the freshwater eels of the genus Anguilla Schrank, 1798. Heliyon 2020, 6, e05176. [Google Scholar] [CrossRef]
  9. Campana, S.E. Chemistry and composition of fish otoliths: Pathway, mechanisms and applications. Mar. Ecol. Prog. Ser. 1999, 188, 263–297. [Google Scholar] [CrossRef] [Green Version]
  10. Arai, T.; Sato, H.; Ishii, T.; Tsukamoto, K. Alkaline earth metal and Mn distribution in otoliths of Anguilla spp. glass eels and elvers. Fish. Sci. 2003, 69, 421–423. [Google Scholar] [CrossRef]
  11. Arai, T.; Chino, N. Diverse migration strategy between freshwater and seawater habitats in the freshwater eels genus Anguilla. J. Fish Biol. 2012, 81, 442–455. [Google Scholar] [CrossRef]
  12. Arai, T. Effect of salinity on strontium:calcium ratios in the otoliths of Sakhalin taimen, Hucho perryi. Fish. Sci. 2010, 76, 451–455. [Google Scholar] [CrossRef]
  13. Arai, T.; Chino, N. Influence of water salinity on the strontium:calcium ratios in otoliths of the giant mottled eel, Anguilla marmorata. Environ. Biol. Fish. 2017, 100, 281–286. [Google Scholar] [CrossRef]
  14. Arai, T.; Chino, N. Contribution of migratory types to the reproduction of migrating silver eels in a tropical eel, Anguilla bicolor bicolor. Heliyon 2022, 8, e09491. [Google Scholar] [CrossRef]
  15. Arai, T.; Kotake, A.; McCarthy, T.K. Habitat use by the European eel Anguilla anguilla in Irish waters. Estuar. Coast. Shelf Sci. 2006, 67, 569–578. [Google Scholar] [CrossRef]
  16. Arai, T.; Kotake, A.; Harrod, C.; Morrissey, M.; McCarthy, T.K. Ecological plasticity of the European eel Anguilla anguilla in a tidal Atlantic lake system in Ireland. J. Mar. Biol. Assoc. 2019, 99, 1189–1195. [Google Scholar] [CrossRef]
  17. Tsukamoto, K.; Arai, T. Facultative catadromy of the eel, Anguilla japonica, between freshwater and seawater habitats. Mar. Ecol. Prog. Ser. 2001, 220, 365–376. [Google Scholar] [CrossRef]
  18. Arai, T.; Kotake, A.; Ohji, M.; Miller, M.J.; Tsukamoto, K.; Miyazaki, N. Occurrence of sea eels of Anguilla japonica along the Sanriku Coast of Japan. Ichthyol. Res. 2003, 50, 78–81. [Google Scholar] [CrossRef]
  19. Arai, T.; Kotake, A.; Ohji, M.; Miyazaki, N.; Tsukamoto, K. Migratory history and habitat use of Japanese eel Anguilla japonica in the Sanriku Coast of Japan. Fish. Sci. 2003, 69, 813–818. [Google Scholar] [CrossRef] [Green Version]
  20. Arai, T.; Kotake, A.; Ohji, M. Variation in migratory history of Japanese eels, Anguilla japonica, collected in the northernmost part of its distribution. J. Mar. Biol. Assoc. 2008, 88, 1075–1080. [Google Scholar] [CrossRef]
  21. Arai, T.; Chino, N.; Kotake, A. Occurrence of estuarine and sea eels Anguilla japonica and a migrating silver eel Anguilla anguilla in Tokyo Bay area, Japan. Fish. Sci. 2009, 75, 1197–1203. [Google Scholar] [CrossRef]
  22. Kotake, A.; Arai, T.; Ozawa, T.; Nojima, S.; Miller, M.J.; Tsukamoto, K. Variation in migratory history of Japanese eels, Anguilla japonica, collected in coastal waters of the Amakusa Islands, Japan, inferred from otolith Sr/Ca ratios. Mar. Biol. 2003, 142, 849–854. [Google Scholar] [CrossRef]
  23. Kotake, A.; Okamura, A.; Yamada, Y.; Utoh, T.; Arai, T.; Miller, M.J.; Oka, H.P.; Tsukamoto, K. Seasonal variation in migratory history of the Japanese eel, Anguilla japonica, in Mikawa Bay, Japan. Mar. Ecol. Prog. Ser. 2005, 293, 213–221. [Google Scholar] [CrossRef] [Green Version]
  24. Chino, N.; Arai, T. Relative contribution of migratory type on the reproduction of migrating silver eels Anguilla japonica, collected off Shikoku Island, Japan. Mar. Biol. 2009, 156, 661–668. [Google Scholar] [CrossRef]
  25. Lamson, H.M.; Shiao, J.C.; Iizuka, Y.; Tzeng, W.N.; Cairns, D.K. Movement patterns of American eels (Anguilla rostrata) between salt- and freshwater in a coasta watershed, based on otolith microchemistry. Mar. Biol. 2006, 149, 1567–1576. [Google Scholar] [CrossRef]
  26. Jessop, B.M.; Cairns, D.K.; Thibault, I.; Tzeng, W.N. Life history of American eel Anguilla rostrata: New insights from otolith microchemistry. Aquat. Biol. 2008, 1, 205–216. [Google Scholar] [CrossRef] [Green Version]
  27. Arai, T.; Kotake, A.; Lokman, M.; Miller, M.J.; Tsukamoto, K. Evidence of different habitat use by New Zealand freshwater eel Anguilla australis and A. dieffenbachii as revealed by otolith microchemistry. Mar. Ecol. Prog. Ser. 2004, 266, 213–225. [Google Scholar] [CrossRef] [Green Version]
  28. Shiao, J.C.; Iizuka, Y.; Chang, C.W.; Tzeng, W.N. Disparities in habitat use and migratory behavior between tropical eel Anguilla marmorata and temperate eel A. japonica in four Taiwanese rivers. Mar. Ecol. Prog. Ser. 2003, 261, 233–242. [Google Scholar] [CrossRef]
  29. Chino, N.; Arai, T. Migratory history of the giant mottled eel (Anguilla marmorata) in the Bonin Islands of Japan. Ecol. Freshw. Fish. 2010, 19, 19–25. [Google Scholar] [CrossRef]
  30. Lin, Y.J.; Jessop, B.M.; Weyl, O.L.; Iizuka, Y.; Lin., S.H.; Tzeng, W.N.; Sun, C.L. Regional variation in otolith Sr:Ca ratios of African longfinned eel Anguilla mossambica and mottled eel Anguilla marmorata: A challenge to the classic tool for reconstructing migratory histories of fishes. J. Fish Biol. 2012, 81, 427–441. [Google Scholar] [CrossRef]
  31. Arai, T.; Chino, N.; Le, D.Q. Migration and habitat use of the tropical eels Anguilla marmorata and A. bicolor pacifica in Vietnam. Aquat. Ecol. 2013, 47, 57–65. [Google Scholar] [CrossRef]
  32. Arai, T.; Chino, N. Opportunistic migration and habitat use of the giant mottled eel Anguilla marmorata (Teleostei: Elopomorpha). Sci. Rep. 2018, 8, 5666. [Google Scholar] [CrossRef] [Green Version]
  33. Chino, N.; Arai, T. Occurrence of marine resident tropical eel Anguilla bicolor bicolor in Indonesia. Mar. Biol. 2010, 157, 1075–1081. [Google Scholar] [CrossRef]
  34. Chino, N.; Arai, T. Habitat use and habitat transitions in the tropical eel, Anguilla bicolor bicolor. Environ. Biol. Fish. 2010, 89, 571–578. [Google Scholar] [CrossRef]
  35. Arai, T.; Chai, I.J.; Iizuka, Y.; Chang, C.W. Habitat segregation and migration in tropical anguillid eels, Anguilla bengalensis bengalensis and A. bicolor bicolor. Sci. Rep. 2020, 10, 16890. [Google Scholar] [CrossRef] [PubMed]
  36. Arai, T.; Limbong, D.; Otake, T.; Tsukamoto, K. Metamorphosis and inshore migration of tropical eels Anguilla spp. in the Indo-Pacific. Mar. Ecol. Prog. Ser. 1999, 182, 283–293. [Google Scholar] [CrossRef] [Green Version]
  37. Arai, T.; Limbong, D.; Otake, T.; Tsukamoto, K. Recruitment mechanisms of tropical eels, Anguilla spp., and implications for the evolution of oceanic migration in the genus Anguilla. Mar. Ecol. Prog. Ser. 2001, 216, 253–264. [Google Scholar] [CrossRef]
  38. Arai, T.; Otake, T.; Tsukamoto, K. Drastic changes in otolith microstructure and microchemistry accompanying the onset of metamorphosis in the Japanese eel Anguilla japonica. Mar. Ecol. Prog. Ser. 1997, 161, 17–22. [Google Scholar] [CrossRef]
  39. Arai, T.; Marui, M.; Miller, M.J.; Tsukamoto, K. Growth history and inshore migration of the tropical eel, Anguilla marmorata in the Pacific. Mar. Biol. 2002, 140, 309–316. [Google Scholar]
  40. Marui, M.; Arai, T.; Miller, M.J.; Jellyman, D.J.; Tsukamoto, K. Comparison of early life history between New Zealand temperate eels and Pacific tropical eels revealed by otolith microstructure and microchemistry. Mar. Ecol. Prog. Ser. 2001, 213, 273–284. [Google Scholar] [CrossRef] [Green Version]
  41. Arai, T.; Marui, M.; Otake, T.; Tsukamoto, K. Inshore migration of a tropical eel, Anguilla marmorata from Taiwanese and Japanese coasts. Fish. Sci. 2002, 68, 152–157. [Google Scholar] [CrossRef] [Green Version]
  42. Réveillac, É.; Feunteun, E.; Berrebi, P.; Gagnaire, P.A.; Lecomte-Finiger, R.; Bosc, P.; Robinet, T. Anguilla marmorata larval migration plasticity as revealed by otolith microstructural analysis. Can. J. Fish. Aquat. Sci. 2008, 65, 2127–2137. [Google Scholar] [CrossRef]
  43. Leander, N.; Tzeng, W.N.; Yeh, N.T.; Shen, K.N.; Han, Y.S. Effects of metamorphosis timing and the larval growth rate on the latitudinal distribution of sympatric freshwater eels, Anguilla japonica and A. marmorata, in the western North Pacific. Zool. Stud. 2013, 52, 30. [Google Scholar] [CrossRef] [Green Version]
  44. Hewavitharane, C.A.; Pickering, T.D.; Rico, C.; Mochioka, N. Early life history of tropical freshwater eels (Anguilla spp.) recruiting to Viti Levu, Fiji Islands, in the western South Pacific. Mar. Freshw. Res. 2020, 71, 452–460. [Google Scholar] [CrossRef]
  45. Hedges, K.J.; Ludsin, S.A.; Fryer, B.J. Effects of ethanol preservation on otolith microchemistry. J. Fish Biol. 2004, 64, 923–937. [Google Scholar] [CrossRef] [Green Version]
  46. Bertin, L. Eels, A Biological Study; Cleaver-Hume Press Ltd.: London, UK, 1956. [Google Scholar]
  47. Miyama, T.; Awaji, T.; Akitomo, K.; Imasato, N. Study of seasonal transport variations in the Indonesian seas. J. Geophys. Res. 1995, 100, 20517–20541. [Google Scholar] [CrossRef]
  48. Godfrey, J.S. The effect of the Indonesian throughflow on ocean circulation and heat exchange with the atmosphere: A review. J. Geophys. Res. 1996, 101, 12217–12237. [Google Scholar] [CrossRef]
  49. Oui, G.; Lukas, R. Seasonal and interannual variability of the North Equatorial Current, the Mindanao Current, and the Kuroshio along the Pacific western boundary. J. Geophys. Res. 1996, 101, 12315–12330. [Google Scholar]
  50. Tsukamoto, K.; Chow, S.; Otake, T.; Kurogi, H.; Mochioka, N.; Miller, M.J.; Aoyama, J.; Kimura, S.; Watanabe, S.; Yoshinaga, T.; et al. Oceanic spawning ecology of freshwater eels in the western North Pacific. Nat. Commun. 2011, 2, 179. [Google Scholar] [CrossRef] [Green Version]
  51. Schabetsberger, R.; Føkland, F.; Kalfatak, D.; Sichrowsky, U.; Meelis, T.; Aarestrup, K.; Gubili, C.; Sarginson, J.; Boufana, B.; Jehle, R.; et al. Genetic and migratory evidence for sympatric spawning of tropical Pacific eels from Vanuatu. Mar. Ecol. Prog. Ser. 2015, 521, 171–187. [Google Scholar] [CrossRef]
  52. Sugeha, H.Y.; Shinoda, A.; Marui, M.; Arai, T.; Tsukamoto, K. Validation of otolith daily increments in the tropical eel Anguilla marmorata. Mar. Ecol. Prog. Ser. 2001, 220, 291–294. [Google Scholar] [CrossRef]
  53. Umezawa, A.; Tsukamoto, K.; Tabeta, O.; Yamakawa, H. Daily growth increments in the larval otolith of the Japanese eel, Anguilla japonica. Jpn. J. Ichthyol. 1989, 35, 440–444. [Google Scholar] [CrossRef]
  54. Tsukamoto, K. Otolith daily growth increments in the Japanese eel. Bull. Jpn. Soc. Sci. Fish. 1989, 55, 1017–1021. [Google Scholar] [CrossRef] [Green Version]
  55. Umezawa, A.; Tsukamoto, K. Factors influencing otolith increment formation in Japanese eel, Anguilla japonica T. and S., elvers. J. Fish Biol. 1991, 39, 211–223. [Google Scholar] [CrossRef]
  56. Martin, M.H. Validation of daily growth increments in otoliths of Anguilla rostrata (Lesueur) elvers. Can. J. Zool. 1995, 73, 208–211. [Google Scholar] [CrossRef]
  57. Arai, T.; Daniel, L.; Tsukamoto, K. Validation of otolith daily increments in the tropical eel, Anguilla celebesensis. Can. J. Zool. 2000, 78, 1078–1084. [Google Scholar] [CrossRef]
  58. Arai, T.; Otake, T.; Tsukamoto, K. Timing of metamorphosis and larval segregation of the Atlantic eels Anguilla rostrata and A. anguilla, as revealed by otolith microstructure and microchemistry. Mar. Biol. 2000, 137, 39–45. [Google Scholar] [CrossRef]
  59. Otake, T.; Ishii, T.; Nakahara, M.; Nakamura, R. Drastic changes in otolith strontium/calcium ratios in leptocephali and glass eels of Japanese eel Anguilla japonica. Mar. Ecol. Prog. Ser. 1994, 112, 189–193. [Google Scholar] [CrossRef]
  60. Arai, T.; Otake, T.; Jellyman, D.J.; Tsukamoto, K. Differences in the early life history of the Australasian shortfinned eel, Anguilla australis from Australia and New Zealand, as revealed by otolith microstructure and microchemistry. Mar. Biol. 1999, 135, 381–389. [Google Scholar] [CrossRef]
  61. Shiao, J.C.; Tzeng, W.N.; Collins, A.; Iizuka, Y. Role of marine larval duration and growth rate of glass eels in determining the distribution of Anguilla reinhardtii and A. australis on Australian eastern coasts. Mar. Freshw. Res. 2002, 53, 687–695. [Google Scholar] [CrossRef]
  62. Arai, T.; Aoyama, J.; Ishikawa, S.; Miller, M.J.; Otake, T.; Inagaki, T.; Tsukamoto, K. Early life history of tropical Anguilla leptocephali in the western Pacific Ocean. Mar. Biol. 2001, 138, 887–895. [Google Scholar]
  63. Arai, T.; Miller, M.J.; Tsukamoto, K. Larval duration of the tropical eel, Anguilla celebesensis, from the Indonesian and Philippine coasts. Mar. Ecol. Prog. Ser. 2003, 251, 255–261. [Google Scholar] [CrossRef] [Green Version]
  64. Arai, T.; Otake, T.; Limbong, D.; Tsukamoto, K. Early life history and recruitment of the tropical eel Anguilla bicolor pacifica, as revealed by otolith microstructure and microchemistry. Mar. Biol. 1999, 133, 319–326. [Google Scholar] [CrossRef]
  65. Pfeiler, E. Glycosaminoglycan breakdown during metamorphosis of larval bonefish Albla. Mar. Biol. Lett. 1984, 5, 241–249. [Google Scholar]
  66. Arai, T.; Abdul Kadir, S.R.; Chino, N. Year-round spawning by a tropical catadromous eel Anguilla bicolor bicolor. Mar. Biol. 2016, 163, 37. [Google Scholar] [CrossRef]
  67. Arai, T.; Abdul Kadir, S.R. Opportunistic spawning of tropical anguillid eels Anguilla bicolor bicolor and A. bengalensis bengalensis. Sci. Rep. 2017, 7, 41649. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  68. Robinet, T.; Lecomte-Finiger, R.; Escoubeyrou, K.; Feunteun, E. Tropical eels Anguilla spp. recruiting to Réunion Island in the Indian Ocean: Taxonomy, patterns of recruitment and early life histories. Mar. Ecol. Prog. Ser. 2003, 259, 263–272. [Google Scholar] [CrossRef]
  69. Réveillac, É.; Robinet, T.; Rabenevanana, M.W.; Valade, P.; Feunteun, É. Clues to the location of the spawning area and larval migration characteristics of Anguilla mossambica as inferred from otolith microstructural analyses. J. Fish Biol. 2009, 74, 1866–1877. [Google Scholar] [CrossRef]
  70. Tabeta, O.; Konishi, Y. An anguillid leptocephalus Anguilla japonica from the waters of Miyako Island, Okinawa, Japan. Bull. Jpn. Soc. Sci. Fish. 1986, 52, 1935–1937. [Google Scholar] [CrossRef] [Green Version]
  71. Kleckner, R.C.; McCleave, J.D. Spatial and temporal distribution of American eel larvae in relation to North Atlantic Ocean current systems. Dana 1985, 4, 67–92. [Google Scholar]
  72. Umezawa, A.; Tsukamoto, K. Age and birth date of the glass eel, Anguilla japonica, collected in Taiwan. Bull. Jpn. Soc. Sci. Fish. 1990, 56, 1199–1202. [Google Scholar] [CrossRef] [Green Version]
  73. Tsukamoto, K. Recruitment mechanism of the eel, Anguilla japonica, to the Japanese coast. J. Fish Biol. 1990, 36, 659–671. [Google Scholar] [CrossRef]
  74. Arai, T.; Taha, H. Contrasting patterns of genetic population structure in tropical freshwater eels of genus Anguilla in the Indo-Pacific. Heliyon 2021, 7, e07097. [Google Scholar] [CrossRef] [PubMed]
  75. Arai, T. Evidence of local short-distance spawning migration of tropical freshwater eels, and implications for the evolution of freshwater eel migration. Ecol. Evol. 2014, 4, 3812–3819. [Google Scholar] [CrossRef] [PubMed]
Figure 1. Map showing the Tanegashima Island (red circle) and other sites examined early life history in the previous studies (blue circle), surface currents and a spawning site (green circle) [47,48,49,50] in the North Equatorial Current and an estimated spawning site (yellow circle) [51] in the South Equatorial Current of Anguilla marmorata in the Pacific Ocean. The base map was downloaded from the OpenStreetMap (open access) at https://www.openstreetmap.org (accessed on 10 August 2021).
Figure 1. Map showing the Tanegashima Island (red circle) and other sites examined early life history in the previous studies (blue circle), surface currents and a spawning site (green circle) [47,48,49,50] in the North Equatorial Current and an estimated spawning site (yellow circle) [51] in the South Equatorial Current of Anguilla marmorata in the Pacific Ocean. The base map was downloaded from the OpenStreetMap (open access) at https://www.openstreetmap.org (accessed on 10 August 2021).
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Figure 2. A SEM image shows the otolith microstructure of a A. marmorata glass eel collected on the beach on Tanegashima Island, Japan. H, hatch check; M1, initiation of metamorphosis; M2, completion of metamorphosis; E, otolith edge.
Figure 2. A SEM image shows the otolith microstructure of a A. marmorata glass eel collected on the beach on Tanegashima Island, Japan. H, hatch check; M1, initiation of metamorphosis; M2, completion of metamorphosis; E, otolith edge.
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Figure 3. A profile shows fluctuations in otolith Sr:Ca ratios (blue line) and widths of otolith increments (orange line) across the line history transect. The solid and dashed lines suggest age at onset of metamorphosis and age at completion of metamorphosis, respectively.
Figure 3. A profile shows fluctuations in otolith Sr:Ca ratios (blue line) and widths of otolith increments (orange line) across the line history transect. The solid and dashed lines suggest age at onset of metamorphosis and age at completion of metamorphosis, respectively.
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Figure 4. Relationship between larval duration (days) and age at recruitment (days) of Anguilla marmorata glass eel recruited to southern Japan.
Figure 4. Relationship between larval duration (days) and age at recruitment (days) of Anguilla marmorata glass eel recruited to southern Japan.
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Table 1. Early life history characteristics of Anguilla marmorata recruited to southern Japan examined in this study.
Table 1. Early life history characteristics of Anguilla marmorata recruited to southern Japan examined in this study.
MonthNumber of SpecimensTotal Length (mm)Otolith Radius (µm)Duration of Larval Stage (Days)Duration of Metamorphosis Stage (Days)Age at Recruitment (Days)
Mean ± SDRangeMean ± SDRangeMean ± SDRangeMean ± SDRangeMean ± SDRange
December 19981849.9 ± 1.248.0–52.1149.7 ± 8.4137.1–163.3120.1 ± 25.579–15715.9 ± 3.210–20150.1 ± 22.9113–184
January 1999450.7 ± 0.849.8–51.5141.1 ± 6.9133.1–149.3122.3 ± 15.5103–13821.8 ± 5.714–27161.8 ± 12.4148–175
February 19992549.2 ± 2.044.9–54.2151.6 ± 6.6138.6–162.7123.1 ± 13.4100–15517.2 ± 4.012–24154.3 ± 17.0133–189
March 19992149.1 ± 1.844.8–52.0148.6 ± 6.8138.2–163.8123.5 ± 12.8100–15220.6 ± 3.413–27160.3 ± 10.7148–192
Table 2. Early life history characteristics of Anguilla marmorata recruited to Pacific coast.
Table 2. Early life history characteristics of Anguilla marmorata recruited to Pacific coast.
CountryTotal Length (mm)Duration of Larval Stage (Days)Age at Recruitment (Days)Reference
MeanRangeMeanRangeMeanRange
Fiji51.0–51.548.0–56.3115–113101–146152–154124–183[44]
Indonesia50.947.9–54.812096–147152129–177[36]
47.9–52.3 128114–158155144–182[37]
Japan49.2–49.745.1–54.2123100–155154133–189[39,41]
46.7 118 145 [43]
Philippines49.947.2–51.6120105–140154136–178[36]
49.5 110 145 [43]
Taiwan50.2–50.348.0–53.411692–145145116–167[39,41]
51.6 112 134 [43]
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Arai, T. Early Life History and Recruitment Processes of a Tropical Anguillid Eel Anguilla marmorata to the Pacific Coast, as Revealed by Otolith Sr:Ca Ratios and Microstructure. Biology 2022, 11, 803. https://0-doi-org.brum.beds.ac.uk/10.3390/biology11060803

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Arai T. Early Life History and Recruitment Processes of a Tropical Anguillid Eel Anguilla marmorata to the Pacific Coast, as Revealed by Otolith Sr:Ca Ratios and Microstructure. Biology. 2022; 11(6):803. https://0-doi-org.brum.beds.ac.uk/10.3390/biology11060803

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Arai, Takaomi. 2022. "Early Life History and Recruitment Processes of a Tropical Anguillid Eel Anguilla marmorata to the Pacific Coast, as Revealed by Otolith Sr:Ca Ratios and Microstructure" Biology 11, no. 6: 803. https://0-doi-org.brum.beds.ac.uk/10.3390/biology11060803

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