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6 January 2025 Indo-Pacific Eels (Anguilla marmorata) from the Caroline Islands Belong to the Micronesia Population Based on Total Number of Vertebrae Counts
Shun Watanabe, Michael J. Miller, Tomoki Honryo, Pierre Sasal
Author Affiliations +
Abstract

The Indo-Pacific eel, Anguilla marmorata Quoy & Gaimard, has the widest geographic distribution of anguillid eels. At least four populations (North Pacific, Micronesia, Indian Ocean and South Pacific) of this species were estimated to exist by previous morphological and molecular genetic studies. Recent mitochondrial control region haplotype analysis of A. marmorata eels from the eastern Caroline Islands and Guam grouped them in two separated lineages with eels from the South Pacific and western Indian Ocean. To examine the composition and possible distribution of the Micronesia population of A. marmorata that may mostly be found in the Mariana (Guam) and Caroline (Palau, Yap, Chuuk, Pohnpei, Kosrae) islands in relation to other populations in the Indo-Pacific region, we statistically compared the total number of vertebrae (TV) of specimens collected from throughout most of the range of A. marmorata including 32 specimens from Kosrae and Pohnpei islands. The TV for 1298 specimens of A. marmorata in combined data from 15 localities ranged from 100 to 110. The mean TV (107.95, 108.03) and range (105–110) of eels from the Mariana and Caroline islands were clearly higher than other localities. The post hoc multiple pairwise comparisons of the 105 pairs of single localities showed that there were 57 significant TV differences between each locality. The most significant differences were between Mariana and Caroline eels and all the other 13 localities. The statistical differences of pooled regional TV data, various genetic studies, and general geography indicate that there are likely six spawning populations of A. marmorata. This study indicates that the Caroline Islands are included in the Micronesia population, but further research is needed to understand the spawning area and life history of the Micronesia population of A. marmorata that seems to live on a relatively small number of islands in Oceania.

Freshwater eels of the genus Anguilla Schrank have now been recognized as comprising 16 species (Ege 1939, Castle and Williamson 1974, Watanabe et al. 2009a), three of which are further divided into two subspecies (Ege 1939). To resolve the inconsistencies in the common names used for some anguillid species, Tsukamoto et al. (2020) proposed a standardized list of the common names of species and subspecies in anguillid eels. The Indo-Pacific eel, Anguilla marmorata Quoy & Gaimard (often referred to previously as the giant mottled eel), is unique among all anguillids because it has the widest geographic distribution of anguillid eels and is found longitudinally from the east coast of Africa to the Marquesas Islands in the southeast Pacific Ocean and as far north as southern Japan (Ege 1939, Figure 1), and so it was given a new common name of the “Indo-Pacific eel” in that paper. Recently this species was found at Palmyra Atoll in the central Pacific (Handler and James 2006) and even farther to the east in the Galapagos Islands (McCosker et al. 2003, Escobar-Camacho et al. 2023), which may indicate that it has an even wider geographic range than previously thought.

Anguillid eels have the unique life history of catadromy, in which most juvenile feeding and growth occur in freshwater or estuaries before reaching maturity when the adult eels migrate to oceanic waters to reproduce. Most anguillid species are distributed in the Indo-Pacific where some make long spawning migrations like the two Atlantic eels, but other species were found to make short migrations to spawn locally, such as in the Indonesian Seas (Aoyama 2009). Larval sampling surveys were able to find the spawning areas of some species in the Pacific and Indian oceans (Kuroki et al. 2009, 2020, Tsukamoto et al. 2011, Miller and Tsukamoto 2017), but many spawning locations have not been clarified (Miller 2023). There seems to be relatively limited variation in the life histories of anguillid eels other than differences in the sizes of species ranges, adult migration distances and larval durations (Aoyama 2009, Kuroki et al. 2014, Righton et al. 2021). However, A. marmorata uniquely developed the ability to expand its species range to overlap with the ranges of most of the other Indo-Pacific anguillid species, possibly because it is a habitat generalist when interacting with other sympatric anguillid species (Miller et al. 2023). The presence of A. marmorata in the Indian Ocean and both the North and South Pacific oceans, a species range that overlaps with all species other than those in Australia and New Zealand (Watanabe 2003, 2023), makes it impossible to have only one spawning population.

FIGURE 1.

Map showing the range of A. marmorata (thick lines on coastlines), with the collection localities of specimens examined by Ege (1939) and Watanabe et al. (2009b) shown with solid and open circles, respectively, and the collection localities of Donovan et al. (2012) with triangles. SUL: Sulawesi; AMB: Ambon; NG: New Guinea; TM: Timor.

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Because of this wide geographic range, various studies have evaluated the possible population structure of A. marmorata. Ege (1939) evaluated the regional morphological variation and suggested that there were three primary races of this species. Ishikawa et al. (2004) recognized five geographically separated populations, which were the North Pacific, Fiji, Tahiti, Madagascar, and Sumatra populations, using 626 base pair segments of the mitochondrial DNA (mtDNA) control region (mtCR) from 162 specimens of A. marmorata collected from 10 localities across their distribution range, but specimens from Guam were not included. Genetic differentiation among populations in the Southern Hemisphere was supported by examination of nuclear DNA with amplified fragment length polymorphism (AFLP) analysis performed on 76 individuals from Madagascar, Sumatra, Fiji, and Tahiti (Ishikawa et al. 2004). Furthermore, Minegishi et al. (2008) examined the population structure of A. marmorata by analyzing the two mtDNA genes of mtCR and cytochrome b and a few nuclear microsatellites of eels from 13 localities. These results generally indicated that A. marmorata has at least four genetically different populations (North Pacific, South Pacific, Indian Ocean, Guam region). The North Pacific population may be fully panmictic (Minegishi et al. 2008), but parts of genomic regions across multiple chromosomes exhibited significant genetic differentiation between the northernmost (Yakushima Island, Southern Japan) and southernmost (Sulawesi, Indonesia) individuals (Hirase et al. 2022), whereas the South Pacific and Indian Ocean populations have metapopulation structures, which both might include more than one spawning population. Interestingly, Guam was suggested to be inhabited by a reproductively isolated population (Minegishi et al. 2008, Watanabe et al. 2008, 2009b) without any information about their spawning area or adult or larval migrations. Further analysis of A. marmorata in the Indian Ocean that also included nuclear DNA, found that there were two genetically distinct populations in the Indian Ocean, with one in the southwestern Indian Ocean and another on the eastern side along Sumatra Island in Indonesia (Gagnaire et al. 2009). Analysis of A. marmorata population structure using AFLP only found three divergent populations that were the North Pacific, the South Pacific, and the southwestern Indian Ocean populations (Gagnaire et al. 2011). By analyzing the genetic diversity of mtCR of A. marmorata from several drainages of Vietnam in comparison to existing sequences from other regions, most of the eels in Vietnam were found to belong to the North Pacific population of that species (Nguyen et al. 2022).

However, some aspects of these genetic studies on A. marmorata should be interpreted with caution. Differences in types of DNA or genetic analysis techniques have been found to cause mtDNA and AFLP analyses to produce different results (Lucchini 2003, Bensch et al. 2006). There are also problems associated with the maternal inheritance aspect of mtDNA (Rubinoff and Holland 2005) that may cause significant limitations for use in population structure studies on species such as anguillid eels that have long larval durations that probably results in some occasional mixing of larvae and mtDNA lineages among populations over evolutionary time, which could mask some recent population separations. Furthermore, genetic studies usually used mixed individuals of different ages and that could be another problem. Genetic exchange between populations and age differences between individuals may make it impossible to distinguish between populations.

A different method that has been used to examine the population structure of anguillid species such as A. marmorata is statistical analysis of total number of vertebrae (TV). Anguilla marmorata has the largest range of TV in the genus Anguilla, which extends from 100 to 110, with some apparent regional variation (Ege 1939, Watanabe et al. 2008, 2009b). Analyses of the TV among eels in all the different regions of the species range indicate that there are at least four populations (North Pacific, Micronesia, Indian Ocean and South Pacific) of A. marmorata (Watanabe et al. 2009b) as has been indicated previously by molecular genetic research (Minegishi et al. 2008). Analyses of TV have also found statistical differences between A. australis subspecies (Watanabe et al. 2006) and A. megastoma in the eastern and western sides of the South Pacific (Watanabe et al. 2011).

When considering regional differences in meristic characters, it should be noted that there is a tendency for TV to increase with latitude, a relationship known as Jordan's rule (Jordan 1892, e.g., McDowall 2008), which is often regarded as an association between TV and water temperature (Fowler 1970, Hubbs 1922). Furthermore, various other environmental factors such as salinity also influence TV (Tåning 1952, Lindsey 1988). However, in the case of eels of the genus Anguilla, the spawning areas that are known for the temperate species A. anguilla, A. rostrata, and A. japonica (Schmidt 1925, McCleave et al. 1987, Tsukamoto et al. 2011) and the tropical species A. bicolor, A. borneensis, A. celebesensis, and A. marmorata (Jespersen 1942, Miller et al. 2002, Aoyama et al. 2003) are all in tropical to subtropical regions with similar water temperatures. In addition, both A. anguilla and A. rostrata spawn in the same area (McCleave et al. 1987, Miller et al. 2015), but their TV are different with very little overlap (A. anguilla: range 110–119, mean 114.7; A. rostrata: range 103–111, mean 107.2; Ege 1939, European material: range 104–120, mean 114.6; American material: range 103–112, mean 107.2; Boëtius 1980). Therefore, because of the similar temperatures that occur at the spawning areas of most anguillids, it seems likely that variations of TV in anguillid eels are derived from genetic rather than environmental factors and that differences in TV may be useful for detecting the existence of different populations of A. marmorata (Watanabe et al. 2008, 2009b). Possible reasons for genetically-based changes in TV ranges within and among species might be related to body elongation for enhanced swimming performance or more random factors such as genetic drift (Tibblin et al. 2016), but this has only begun to be evaluated for anguillid eels (Forsman and Berggren 2016).

One of the most interesting findings of both the TV and the most detailed genetic study of Minegishi et al. (2008) that included both mitochondrial and nuclear DNA, is that the eels collected in Guam of the Mariana Islands formed a separate population, which has been referred to as the Micronesia Population. Micronesia consists of four major archipelagos as follows: Mariana Islands, the Caroline Islands, Gilbert Islands, and Marshall Islands (Figure 2A). Myers and Donaldson (2003) reported this species from the Mariana Islands and all of the larger or “high islands” of the Caroline Islands, which include from west to east: Palau, Yap, Chuuk (Truk), Pohnpei, and Kosrae (Figure 2).

To test if the A. marmorata eels occurring in the eastern Caroline Islands are part of the same Micronesia population as those in Guam, Donovan et al. (2012) obtained 39 specimens of A. marmorata from Kosrae and Pohnpei (Figures 1 and 2) and sequenced their entire mtCR. They also compared the Micronesia eels to 267 previously sequenced haplotypes from across the Indo-Pacific (Minegishi et al. 2008). Their analysis found two distinctive lineages for the eastern Caroline Islands and Guam that were mostly grouped with two clusters of South Pacific Ocean eels and the western Indian Ocean and South Pacific Ocean eels (Figure 3; Donovan et al. 2012). Although that clustering pattern is likely related to the limitations of mtDNA for population studies mentioned above, their findings supported the likelihood of the existence of a Micronesia spawning population.

To further examine if the eels of Guam and the eastern Caroline Islands are actually both part of the Micronesia population A. marmorata in the Indo-Pacific, we statistically analyzed the TV of specimens collected from throughout most of the range of A. marmorata including 32 specimens collected on Kosrae and Pohnpei islands, which are some of the specimens used by Donovan et al. (2012) and also some data of Ege (1939). Furthermore, another objective of the present study was to determine how TV variation may be related to the findings of population genetic studies.

MATERIALS AND METHODS

The TV data of the specimens of A. marmorata used in this study are mainly from the studies of Ege (1939) and Watanabe et al. (2009b), and newly obtained TV data from the eels used in the study of Donovan et al. (2012). The present study used 19 of 39 specimens of A. marmorata used in Donovan et al. (2012) and an additional five specimens of this species, all of which were obtained from collections made in May–June 2007 and June–July 2008 at Pohnpei and Kosrae (Figures 1 and 2) by those authors using handlines, spears, Hawaiian slings, and a Smith-Root Model LR-24 electrofisher. There were 24 specimens from Pohnpei (n = 11) and Kosrae (n = 13) that were radio-graphed by an X-ray apparatus (MA-60, Hitex Co.) and a Digital X-ray imaging sensor (Naomi-NX04H, RF Co.) to count their TV (Table 1). These TV data are referred to as “Donovan's TV data.”

FIGURE 2.

Bathymetric maps showing Micronesia and the surrounding region including Palau, Northern Mariana Islands (including Guam), Federated States of Micronesia, Marshall Islands, and Gilbert Islands, with small circles showing locations where A. marmorata Micronesia population specimens of this study were from at Guam, Pohnpei, and Kosrae (A), and the Caroline Islands region separated (by vertical dashed lines) into island groups (Yap, Chuuk, Pohnpei, Kosrae) (B), with some atolls labeled, but only the islands of Chuuk Atoll are large enough to have any surface freshwater.

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FIGURE 3.

Part of a Bayesian tree (excluding the Northern Population of A. marmorata) based on 277 mtCR haplotypes of A. marmorata from throughout the Indo-Pacific that shows that the eels from Guam (Mariana Islands) and Pohnpei and Kosrae (Caroline Islands) were grouped in separated lineages, which was modified from Donovan et al. (2012).

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TABLE 1

Comparison of Frequency Distributions of Total Number of Vertebrae (TV) of Anguilla marmorata from Pohnpei and Kosrae Island and Ege' Data That Were Used in This Study

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TABLE 2

Frequency Distributions for Total Number of Vertebrae (TV) in A. marmorata from 21 Locations in Data of (A) Ege (1939) and (B) Watanabe et al. (2009b): Madagascar (MAD), Réunion Island (REU), Nias Island (NIA), Sumatra (SUM), Timor (TIM), Japan (JPN), Philippines (PHI), Luzon Island (LUZ), Sulawesi (Celebes) (SUL), Ambon Island (AMB), Mariana Islands (MAR), Guam Island (GUA), Caroline Islands (CAR), New Guinea (NGU), Papua New Guinea (PMG), New Caledonia (NCA), Fiji (FIJ), Samoa (SAM), Tahiti (TAH) Marquesas (MQU), and French Polynesia (FPN)

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The TV data in Ege (1939) were obtained from Madagascar, Réunion, Nias (off west Sumatra), Sumatra, Timor, the Philippines, Celebes (Sulawesi Island), the Mariana Islands, Caroline Islands, New Guinea, New Caledonia, Fiji, Samoa, Tahiti, and the Marquesas Islands (Figure 1). A total of 793 specimens including TV data from examinations of museum specimens were used for “Ege's TV data” (Table 2A). The TV data in Watanabe et al. (2009b) were obtained from Madagascar, Réunion, Sumatra, Japan, Luzon Island of the Philippines, Sulawesi Island (Celebes), Ambon Island, Guam, Papua New Guinea, New Caledonia, Fiji, and Raiatea, Tahiti, and Moorea islands in French Polynesia (Figure 1). A total of 481 specimens including TV data were used for “Watanabe's TV data” (Table 2B).

The nonparametric Kruskal–Wallis test was applied to the TV data among Pohnpei (n = 11) and Kosrae (n = 13) specimens whose vertebral counts were examined in this study along with the Caroline Islands (n = 8) from Ege's data using Prism (version 8.4.3) for macOS (GraphPad Software, LLC), which showed no significant differences (P = 0.175). Therefore, these data were combined as TV data from the Caroline Islands (n = 32, Tables 1 and 3).

Donovan's, Ege's and Watanabe's TV data were also combined to have 15 localities in the Indo-Pacific, which resulted in a total of 1298 specimens as shown in Table 3 that were analyzed statistically. The TV data from Nias Island (n = 16) in Ege's TV data were included with the TV data from Sumatra in both Ege's and Watanabe's TV data, because this island is very near Sumatra. The TV data from Tahiti and Marquesas in Ege's TV data and Watanabe's TV data were all combined into the TV data from French Polynesia.

TABLE 3

Comparison of Frequency Distributions of the Combined Data Set of Total Number of Vertebrae (TV) of A. marmorata from the 15 Localities Analyzed in This Study: Madagascar (MAD), Réunion Island (REU), Sumatra (SUM), Timor (TIM), Japan (JPN), Philippines (PHI), Sulawesi (Celebes) (SUL), Ambon Island (AMB), Mariana Islands (MAR), Caroline Islands (CAR), New Guinea (NGU), New Caledonia (NCA), Fiji (FIJ), Samoa (SAM), and French Polynesia (FPN)

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All 15 localities in the combined TV data sets did not have normal distributions (Shapiro–Wilk test, P < 0.05, Table 3) using JMP (version 14.2) for macOS (SAS Institute Inc.). The TV data among each location were tested using the nonparametric Kruskal–Wallis test followed by pairwise comparisons with Dunn's test using Prism (version 8.4.3) for macOS (GraphPad Software, LLC).

Based on the difference in TV among 15 localities and the results of molecular genetic studies (Ishikawa et al. 2004, Minegishi et al. 2008, Gagnaire et al. 2009), the validity of the estimated six regional populations (West Indian Ocean, East Indian Ocean, North Pacific, Micronesia, West South Pacific, East South Pacific) was examined using normal distributions (Shapiro–Wilk test) and the nonparametric Kruskal–Wallis test followed by pairwise comparisons with Dunn's test.

TABLE 4

Result of Each Pairwise Comparison (P 0.05, Dunn's Test) of the TV of A. marmorata at 15 Localities: Madagascar (MAD), Réunion Island (REU), Sumatra (SUM), Timor (TIM), Japan (JPN), Philippines (PHI), Sulawesi (Celebes) (SUL), Ambon Island (AMB), Mariana Islands (MAR), Caroline Islands (CAR), New Guinea (NGU), New Caledonia (NCA), Fiji (FIJ), Samoa (SAM), and French Polynesia (FPN)

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RESULTS

The TV for 1298 specimens of A. marmorata in the combined data from 15 localities ranged from 100 to 110 and overlapped at least at 105 and 106 vertebrae in all locations (Table 3). The mean TV at each location ranged from 104.39 to 108.03 (Table 3). While the mean TV in Timor, Japan, Philippines, and Sulawesi were lower (104.39–104.72) than other localities, the mean TV in the Mariana and Caroline islands were higher (107.95, 108.03) than other localities (Table 3). The statistical analysis of the TV data found a significant difference among the 15 localities (Kruskal–Wallis test, P < 0.0001). The post hoc multiple pairwise comparisons of the 105 pairs of localities showed that there were 57 significant differences (Dunn's test, P < 0.0001–0.05) in the TV data between each locality (Table 4). The most significant differences were between the Mariana and Caroline specimens compared to each of all the other 13 localities, except for between Mariana and Caroline, which resulted in those two localities forming a statistically independent group (Table 4, Figure 4). There were 15 significant differences between Japan, Philippines, and Sulawesi in the North Pacific Ocean region and all localities (New Guinea, New Caledonia, Fiji, Samoa, and French Polynesia) in the South Pacific Ocean region (Table 4). The specimens from French Polynesia had the third highest mean TV (106.41, Table 3) and were significantly different from all 12 other localities except for between Madagascar and New Caledonia (Table 4). The significant differences other than the above were between Réunion and each of Timor, Japan, Philippines, and Sulawesi, between Sumatra and Philippines, between Timor and New Guinea, New Caledonia, and Fiji, and between Ambon and New Caledonia (Table 4).

FIGURE 4.

Diagrammatic summary of the results of the statistical comparisons of the total number of vertebrae (TV) data of A. marmorata between each locality (see Table 4). Lines connecting two localities indicate no statistically significant differences between those localities (P ≥ 0.05). Localities that are not connected by lines were statistically different (P < 0.05). Abbreviations of locations are from Table 4.

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There were no significant differences between Madagascar and the other 12 localities except for between Madagascar and the Mariana and Caroline islands or between Ambon and 10 other localities except for between Ambon and Mariana, Caroline, New Caledonia, and French Polynesia (Table 4, Figure 4). There were no significant differences among Madagascar, Réunion, Sumatra, and Timor in the Indian Ocean region, except for between Réunion and Timor. There were also no significant differences among Japan, Philippines, Sulawesi, and Ambon in the North Pacific Ocean region or among New Guinea, New Caledonia, Fiji, and Samoa in the South Pacific Ocean region (Table 4, Figure 4). The four localities in the Indian Ocean region (Madagascar, Réunion, Sumatra, and Timor) showed almost no significant differences from the four localities in the North Pacific Ocean region (Japan, Philippines, Sulawesi, and Ambon), except for between Réunion and three localities (Japan, Philippines, and Sulawesi) and between Sumatra and Philippines, or among the four localities in the South Pacific Ocean region (New Guinea, New Caledonia, Fiji, and Samoa), except for between Timor and three localities (New Guinea, New Caledonia, and Fiji) (Table 4, Figure 4).

However, comparisons among many different sites among likely population regions may mask the overall TV patterns statistically, so we also pooled the TV data of sites in regions that might represent different populations with no significant differences among the sites in each region (Figure 4). Based on the above results of this study and the results of molecular genetic studies (Ishikawa et al. 2004, Minegishi et al. 2008, Gagnaire et al. 2009), there is the possibility of six regional populations (West Indian Ocean, East Indian Ocean, North Pacific, Micronesia, West South Pacific, East South Pacific) (Table 5, Figure 5). The six estimated populations in the combined TV data sets (Figure 5) did not have normal distributions (Shapiro–Wilk test, P < 0.0001, Table 5), but the statistical analysis of their TV data found a significant difference among them (Kruskal–Wallis test, P < 0.0001). The post hoc multiple pairwise comparisons of the 15 pairs among six populations showed 13 significant differences (Dunn's test, P < 0.0001–0.01), and that there were no significant differences between West Indian Ocean and West South Pacific or between East Indian Ocean and North Pacific (Table 6).

FIGURE 5.

Frequency distributions of the combined TV data of six known or likely regional populations of A. marmorata in the west Indian Ocean (A), the east Indian Ocean (B), North Pacific (C), Micronesia (D), the west South Pacific (E), and the east South Pacific (F). Abbreviations of locations are from Table 4.

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TABLE 5

Comparison of Frequency Distributions of Total Number of Vertebrae (TV) of A. marmorata from Six Populations

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TABLE 6

Result of Each Pairwise Comparison (P 0.05, Dunn's Test) of the TV of A. marmorata among Six Populations

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DISCUSSION

The analysis of the TV data of A. marmorata in the present study using data from Ege (1939), Watanabe et al. (2009b), and newly obtained data of eels from Pohnpei and Kosrae of the Caroline Islands (Donovan et al. 2012) provide new evidence for the existence of a population of this species that lives on the larger islands of the Micronesia region. The specimens of A. marmorata from the Mariana and Caroline islands showed a remarkable difference in TV range and mean from those collected at the 13 other localities and there was no significant difference between the Mariana and Caroline islands specimens. Ege (1939) also showed that the TV of a specimen from Palau (a museum specimen), was 108, which is within the higher TV range of the Mariana and Caroline islands specimens. From a morphological viewpoint, this supports that individuals from the Mariana, Caroline, and Palau islands are included in the same population, which has been referred to as the Micronesia population (Minegishi et al. 2008, Watanabe et al. 2008). The TV data from the Caroline Islands also had the exact same range of TV (105–110) as the eel specimens from Guam and their two means (107, 108) and modal values of 108 were the highest of all the localities. The pooled TV frequency distributions of six likely regional populations in Figure 5 clearly show how different the Micronesia population is. In contrast, all the means (104–106) and modes (104–106) of all the other localities included direct overlaps even among widely separated sites in different ocean basins, and there was a wide range of statistical differences or no differences found in our study and in previous TV or other morphological analyses (Watanabe et al. 2008, 2009b).

Therefore, in some respects, the distinctly different TV data for the Micronesia population based on samples from three separate islands show more definitive evidence of it being a highly distinct population than was illustrated in the genetic analyses. For example, the analysis of Donovan et al. (2012) that used sequences of the entire control region mtDNA for 39 eels from Kosrae and Pohnpei and compared them to 267 previously sequenced haplotypes (Minegishi et al. 2008) from across the Indo-Pacific Ocean, found that some of the Mariana and Caroline islands specimens occurred in their own clade of a cluster of South Pacific and Indian Ocean eels (Figure 3). Other Mariana and Caroline Islands specimens were placed in their own branch in a South Pacific cluster, but four others were in different branches of that cluster. The analyses of Minegishi et al. (2008) found a similar pattern of a single distinct clade of only Guam specimens, with other specimens from Guam being placed in other clusters with eels from other regions. Ishikawa et al. (2004) did not include any Micronesia specimens, but were able to find a distinct Northern Population clade, and a distinct Madagascar clade. Eels from other areas were in various clusters and a cluster formed with only Fiji and French Polynesia eels, but other clusters were highly mixed. Gagnaire et al. (2009, 2011) also showed a distinct western Indian Ocean population, which supports the likelihood that those eels spawn on the western side of the Indian Ocean and that there is a different spawning population on the east side.

Therefore, the results in this study, the population genetic study of this species (Minegishi et al. 2008), and all the other gathered information generally indicate that there are undoubtedly at least four regional populations (Indian Ocean, North Pacific, Micronesia, and South Pacific), but it is more likely that there are six spawning populations of A. marmorata, with different spawning populations being present in the Indian (east and west) and South Pacific (French Polynesia and western region) oceans based in part on the wide longitudinal zones of those ocean basins and the statistical analysis of the regionally pooled TV data (Table 5, Figure 5). That is also consistent with Ishikawa et al. (2004) that suggested that sequence differences in mtDNA and nuclear DNA with AFLP analysis among geographic samples revealed the existence of four geographic populations around Madagascar, Sumatra, Fiji, and Tahiti in the South Pacific and Indian Ocean regions. Minegishi et al. (2008) showed significant differences in FST between four of the localities (Madagascar, Sumatra, Fiji, and Tahiti), but Fiji and Tahiti showed no significant genetic differences in mtCR, and Réunion (an additional sampling location in that study) in the western Indian Ocean showed no significant difference with Sumatra in the eastern Indian Ocean in the microsatellite analysis. Gagnaire et al. (2009) supported the existence of three divergent populations (the southwestern Indian Ocean, the South Pacific Ocean, and the North Pacific Ocean populations) in A. marmorata and provided a new interpretation for the genetic distinctiveness of Sumatra and Guam. These three populations identified from the AFLP dataset (Gagnaire et al. 2009) mostly correspond to the three main mitochondrial lineages previously found in A. marmorata (Ishikawa et al. 2004, Minegishi et al. 2008).

Similar to the DNA studies, the statistical analyses of TV probably have a limited ability to clearly distinguish all the likely spawning populations that may exist in A. marmorata. Using individual collection site TV data, significant differences in the TV data were found between the North Pacific Ocean region, except Ambon Island, and South Pacific Ocean regions, while there were few differences between specimens from the Indian and the North or South Pacific Ocean region. The regionally pooled TV confirmed most regional differences (Table 6), but as can be seen in their similar TV distributions in Figure 5, each of the Indian Ocean regional populations were not statistically different from at least one of the Pacific populations (the west Indian Ocean vs. the west South Pacific and the east Indian Ocean vs. North Pacific, Table 6), even though they cannot be part of the same spawning populations. Similarly, the specimens from French Polynesia showed a significant difference of TV from those collected at 10 other localities, but not Madagascar and New Caledonia. French Polynesia was different than all the regionally pooled locations however, which suggests that the nonparametric statistical comparisons may have limitations to find significant differences within overlapping TV distributions. Most importantly though, the regionally pooled data support the hypothesis that there are different spawning populations on each side of both the Indian Ocean and the South Pacific, and there are two spawning populations in the North Pacific.

Although, both molecular genetic and TV studies have some limitations for clearly distinguishing all the likely spawning populations (e.g., some Indian Ocean vs. Pacific Ocean populations were not different for TV), the geography of the six suggested spawning populations seem consistent with the general patterns of ocean currents that would be needed to transport their leptocephalus larvae to their recruitment areas. In the western North Pacific, there must be a spawning area of the Micronesian population in addition to that of the North Pacific population, which appears likely to spawn to the west of the Mariana Islands (Miller et al. 2002, Kuroki et al. 2006, Chow et al. 2017). The spawning area of the Micronesia population is not known, but the North Equatorial Current (NEC) flows westward throughout the year at latitudes from about 8 to 16°N (Reverdin et al. 1994), and part of this water enters the eastward flowing North Equatorial Countercurrent (NECC; Lukas et al. 1991). Therefore, a spawning area in the NEC east of the Mariana and Caroline Islands could also transport leptocephali to the Palau Islands (Figure 2A). Eastward transport of leptocephali in the NECC could also explain the presence of this species in other more eastern Micronesian islands, including Palmyra Atoll (Handler and James 2006) (Figure 1). The specimen of A. marmorata collected from an artificial freshwater pond Palmyra Atoll (Handler and James 2006) had 110 TV (A. Y. Suzumoto, unpubl. data), which is the maximum number of vertebrae that has been observed in this species that has been seen in the Micronesian population (Tables 2 and 3), except for at Marquesas in Ege's TV data. Therefore, this specimen may have arrived at Palmyra Atoll naturally without assistance from humans. This Palmyra Atoll specimen suggests that freshwater eels have begun to be noticed in new locations, possibly also because of possible recent shifts in oceanic currents (McCosker et al. 2003, Escobar-Camacho et al. 2023).

Other types of information have been obtained about possible spawning populations of A. marmorata, but not for the Micronesia population. Net sampling of larvae (Miller et al. 2002, Kuroki et al. 2009) and trawl captures of spawning-condition adults (Chow et al. 2009, Tsukamoto et al. 2011) have found that the North Pacific population of A. marmorata spawns in an area in the NEC overlapping with the Japanese eel spawning area. Both pop-up satellite transmitting tags (PSAT; Schabetsberger et al. 2013, 2015) and catches of small larvae (16–18 mm; Miller et al. 2022) have indicated that there is an offshore spawning area of A. marmorata to the northeast of Vanuatu (northwest of Fiji) presumably for the western South Pacific population. In contrast, local spawning near Samoa was suggested by PSAT studies (Schabetsberger et al. 2019, 2021) and the capture of a small larva (7.8 mm) near those islands is consistent with that (Kuroki et al. 2020). However, the distance between those possible spawning areas (northwest of Fiji and near Samoa) and the island archipelagos of French Polynesia (∼2,300 km from Samoa to Tahiti), suggest that separate spawning areas likely occur in those far eastern areas even if DNA studies cannot definitively demonstrate that. These various types of information suggest that both long- or medium-distance (North Pacific population, possibly Vanuatu-Fiji region in South Pacific) and local (Samoa, Madagascar, Sumatra) migration and spawning strategies can be used by A. marmorata, which are difficult to detect by existing DNA studies or using TV. Only by studying the same cohorts for several years from different places, could research provide a clear answer on genetical structures. However, this kind of data is difficult to obtain.

The patterns found in the DNA studies seem to highlight the limitations of using mtDNA in population structure studies of a relatively old widespread species that has expanded its range across the entire Indo-Pacific. For example, A. marmorata does not appear to be one of the oldest species of anguillid eels, but may be about 10 million years old (Myr) (Barth et al. 2020) and seems to have originated within an Indo-Pacific clade after A. celebesensis and A. megastoma appeared (Minegishi et al. 2005). The long larval duration of anguillid eels, including A. marmorata (∼3–7 months; Kuroki et al. 2014), would have enabled eventual dispersal of the species across the Indo-Pacific. The maternal inheritance of mtDNA with no recombination (Rubinoff and Holland 2005) has likely resulted in a situation where each regional spawning population retains some ancestral haplotypes, some new ones occur in each population, and some mixing of haplotypes occurs over evolutionary time, which results in the population structure in the South Pacific being obscured in mtDNA studies. Minegishi et al. (2008) suggested that the ancestral population of A. marmorata originated somewhere in the western Pacific Ocean and then invaded the central South Pacific and Indian oceans, which is consistent with those 2 ocean regions having similar overall TV ranges as seen in Table 4 and Figure 5. It is possible that the Micronesia population of this species was derived from two lineages with origins in the Indian and South Pacific oceans as suggested by the clustering patterns of Donovan et al. (2012) as seen in Figure 3.

The Micronesia population seems unique in some other respects however, because it is the only anguillid to have colonized the relatively few larger islands of that region. However, A. bicolor pacifica has been reported in Palau, the Mariana Islands and Pohnpei along with A. marmorata (Myers and Donaldson 2003), whereas in the South Pacific, A. marmorata co-occurs with A. megastoma and A. obscura (Marquet and Galzin 1991). The larger islands such as Palau, Guam, Pohnpei, and Kosrae have been documented to have the same types of aquatic faunas of amphidromous snails, shrimp, and gobies and freshwater insect larvae (Nelson et al. 1996, 1997, Buden et al. 2001, Leberer and Nelson 2001, March et al. 2003, Myers and Donaldson 2003) that form the main part of the diets of anguillids on the islands of Oceania in the South Pacific (Marquet and Lamarque 1986, Miller et al. 2023). Therefore, these islands with freshwater streams (Palau, Yap, Guam, Chuuk, Pohnpei, Kosrae, Figure 2) appear to be the core habitats of the Micronesia population, because there is little apparent surface water in the archipelagos of the Marshall and Gilbert islands (Figure 2A), which consist entirely of atoll islands that are part of fringing reefs and only have small ponds or brackish water bodies (Myers and Donaldson 2003).

Although there is basically no clear understanding of all aspects of the life histories of any population of A. marmorata yet, the early life histories have been examined in some regions (reviewed by Kuroki et al. 2014). There were many studies of the hatching dates, the leptocephalus durations, and the age at recruitment of glass eels of A. marmorata in areas such as Japan, Taiwan, Philippines, and Indonesia for the North Pacific population (e.g., Arai et al. 1999, 2002, Kuroki et al. 2006, 2020), Réunion, Mauritius, and Mayotte for the Indian Ocean population (Robinet et al. 2003, Réveillac et al. 2008), and Fiji for the South Pacific population (Hewavitharane et al. 2020). Helme et al. (2018) documented the seasonal occurrence of recruiting glass eels of A. marmorata in two estuaries of French Polynesia (Tahiti and Moorea islands) from 2009 to 2017. The recruitment was seasonal and occurred between November and March during the rainy season, with peaks in December and January. There is no information on the occurrence of glass eels of the Micronesia population, or other aspects of their eels in freshwater. Further research on the spawning areas, distributions of leptocephali, and the recruitment patterns in the Micronesia population will be required to fully understand the population structure and life history of this widespread anguillid species that has established a unique population on a relatively small number of islands of Oceania.

ACKNOWLEDGMENTS

This work was supported by Kindai University. Thanks are due to Dr. Frank Pezold and Dr. Shaun Donovan for providing us with A. marmorata specimen loans from Pohnpei and Kosrae. We thank Prof. Y. Sawada for permission to make radiographs using the X-ray apparatus and Digital X-ray imaging sensor in his laboratory to count the TV of A. marmorata. We are also grateful to Y. Kawai and K. Ikuta for assistance with parts of the data analysis and to Dr. T. Higuchi for assistance with parts of the figures.

© 2024 by University of Hawai‘i Press. All rights reserved.

Literature Cited

1.

Aoyama, J. 2009. Life history and evolution of migration in catadromous eels (Genus Anguilla). Aqua-BioSci. Monogr. 2:1–42. Google Scholar

2.

Aoyama, J., S. Wouthuyzen, M. J. Miller, T. Inagaki, and K. Tsukamoto. 2003. Short-distance spawning migration of tropical freshwater eels. Biol. Bull. 204:104–108. Google Scholar

3.

Arai, T., D. Limbong, T. Otake, and K. Tsukamoto. 1999. Metamorphosis and inshore migration of tropical eels Anguilla spp. in the Indo-Pacific. Mar. Ecol. Prog. Ser. 182:283–293. Google Scholar

4.

Arai, T., M. Marui, T. Otake, and K. Tsukamoto. 2002. Inshore migration of a tropical eel, Anguilla marmorata, from Taiwanese and Japanese coasts. Fish. Sci. 68:152–157. Google Scholar

5.

Barth, J. M. I., C. Gubili, M. Matschiner, O. K. Trresen, S. Watanabe, B. Egger, Y.-S. Han, E. Feunteun, R. Sommaruga, R. Jehle, and R. Schabetsberger. 2020. Stable species boundaries despite ten million years of hybridization in tropical eels. Nat. Commun. 11:1433. Google Scholar

6.

Bensch, S., D. E. Irwin, J. H. Irwin, L. Kvist, and S. Åkesson. 2006. Conflicting patterns of mitochondrial and nuclear DNA diversity in Phylloscopus warblers. Mol. Ecol. 15: 161–171. Google Scholar

7.

Boëtius, J. 1980. Atlantic Anguilla. A presentation of old and new data of total numbers of vertebrae with special reference to the occurrence of Anguilla rostrata in Europe. Dana 1:93–112. Google Scholar

8.

Buden, D. W., B. Lynch, J. W. Short, and T. Leberer. 2001. Decapod crustaceans of the headwater streams of Pohnpei, Eastern Caroline Islands, Federated States of Micronesia. Pac. Sci. 55:257–265. Google Scholar

9.

Castle, P. H. J., and G. R. Williamson. 1974. On the validity of the freshwater eel species Anguilla ancestralis Ege from Celebes. Copeia 1974:569–570. Google Scholar

10.

Chow, S., H. Kurogi, N. Mochioka, S. Kaji, M. Okazaki, and K. Tsukamoto. 2009. Discovery of mature freshwater eels in the open ocean. Fish. Sci. 75:257–259. Google Scholar

11.

Chow, S., H. Kurogi, T. Yamamoto, T. Tomoda, N. Mochioka, F. Shirotori, T. Yoshinaga, D. Ambe, M. Okazaki, S. Nagai, and T. Yanagimoto. 2017. Reproductive isolation between sympatric Anguilla japonica and Anguilla marmorata. J. Fish Biol. 91:517–1525 Google Scholar

12.

Donovan, S., F. Pezold, Y. Chen, and B. Lynch. 2012. Phylogeography of Anguilla marmorata (Teleostei:Anguilliformes) from the eastern Caroline Islands. Ichthyol. Res. 59:70–76. Google Scholar

13.

Ege, V. 1939. A revision of the genus Anguilla Shaw, a systematic, phylogenetic and geographical study. Dana Report 16:1–256. Google Scholar

14.

Escobar-Camacho, D., W. Andrade, N. Valencia, A. C. Encalada, and D. A. Pazmiño. 2023. Validating the occurrence of the giant mottled eel (Anguilla marmorata) in the Galápagos Islands J. Fish Biol. 103(1):183–188. Google Scholar

15.

Forsman, A., and H. Berggren. 2016. Can spatial sorting associated with spawning migration explain evolution of body size and vertebral number in Anguilla eels? Ecol. Evol. 7:751–761. Google Scholar

16.

Fowler, J. A. 1970. Control of vertebral number in teleosts—an embryological problem. Q. Rev. Biol. 45:148–167. Google Scholar

17.

Gagnaire, P. A., Y. Minegishi, J. Aoyama, E. Réveillac, T. Robinet, P. Bosc, K. Tsukamoto, E. Feunteun, and P. Berrebi. 2009. Ocean currents drive secondary contact between Anguilla marmorata populations in the Indian Ocean. Mar. Ecol. Prog. Ser. 379:267–278. Google Scholar

18.

Gagnaire, P. A., Y. Minegishi, S. Zenboudji, P. Valade, J. Aoyama, and P. Berrebi. 2011. Within-population structure highlighted by differential introgression across semipermeable barriers to gene flow in Anguilla marmorata. Evolution 65:3413–3427. Google Scholar

19.

Handler, A., and S. A. James. 2006. Anguilla marmorata (giant mottled eel) discovered in a new location: natural range expansion or recent human introduction? Pac. Sci. 60: 109–115. Google Scholar

20.

Helme, H., F. Bertucci, R. M. Moussa, Y. Wolff, and P. Sasal. 2018. Temporal dynamics of the recruitment of glass eels in two valleys of French Polynesia (Tahiti and Moorea Islands). Cybium 42:341–348. Google Scholar

21.

Hewavitharane, C. A., T. D. Pickering, C. Rico, and N. Mochioka. 2020. Early life history of tropical freshwater eels (Anguilla spp.) recruiting to Viti Levu, Fiji Islands, in the western South Pacific. Mar. Freshw. Res. 71:452–460. Google Scholar

22.

Hirase, S., Y. Kumai, S. Kato, S. Hagihara, K. Kikuchi, and M. Kuroki. 2022. Genomic signatures for latitudinal selection in the tropical eel Anguilla marmorata. J. Evol. Biol. 35:763–771. Google Scholar

23.

Hubbs, C. L. 1922. Variations in the number of vertebrae and other meristic characters of fishes correlated with the temperature of water during development. Am. Nat. 56:360–372. Google Scholar

24.

Ishikawa, S., K. Tsukamoto, and M. Nishida. 2004. Genetic evidence for multiple geographic populations of the giant mottled eels Anguilla marmorata in the Pacific and Indian oceans. Ichthyol. Res. 51:343–353. Google Scholar

25.

Jespersen, P. 1942. Indo-Pacific leptocephali of the genus Anguilla. Dana Report 22: 1–128. Google Scholar

26.

Jordan, D. S. 1892. Relations of temperature to vertebrae in fishes. Proc. U. S. Natl. Mus. 1891:107–120. Google Scholar

27.

Kuroki, M., J. Aoyama, M. J. Miller, S. Wouthuyzen, T. Arai, and K. Tsukamoto. 2006. Contrasting patterns of growth and migration of tropical anguillid leptocephali in the western Pacific and Indonesian Seas. Mar. Ecol. Prog. Ser. 309:233–246. Google Scholar

28.

Kuroki, M., J. Aoyama, M. J. Miller, T. Yoshinaga, A. Shinoda, S. Hagihara, and K. Tsukamoto. 2009. Sympatric spawning of Anguilla marmorata and Anguilla japonica in the western North Pacific Ocean. J. Fish Biol. 74:1835–1865. Google Scholar

29.

Kuroki, M., M. J. Miller, and K. Tsukamoto. 2014. Diversity of early life-history traits in freshwater eels and the evolution of their oceanic migrations. Can. J. Zool. 92:749–770. Google Scholar

30.

Kuroki, M., M. J. Miller, E. Feunteun, P. Sasal, T. Pikering, Y.-S. Han, E. Faliex, A. Acou, A. Dessier, R. Schabetsberger, S. Watanabe, T. Kawakami, H. Onda, T. Higuchi, A. Takeuchi, M. Shimizu, C. A. Hewavitharane, S. Hagihara, T. Taka, S. Kimura, N. Mochioka, T. Otake, and K. Tsukamoto. 2020. Distribution of anguillid leptocephali and possible spawning areas in the South Pacific Ocean. Prog. Oceanogr. 180:102310. Google Scholar

31.

Leberer, T., and S. G. Nelson. 2001. Factors affecting the distribution of atyid shrimps in two tropical insular rivers. Pac. Sci. 55: 389–398. Google Scholar

32.

Lindsey, C. C. 1988. Factors controlling meristic variation. Pages 197–274 in W. S. Hoar and D. J. Randall, eds. Fish physiology. Volume 11B. Academic Press, New York. Google Scholar

33.

Lucchini, V. 2003. AFLP: a useful tool for biodiversity conservation and management. C. R. Biol. 326:43–48. Google Scholar

34.

Lukas, R., E. R. Firing, P. Hacker, P. L. Richardson, C. A. Collins, R. Fine, and R. Gammon. 1991. Observations of the Mindanao Current during the Western Equatorial Pacific Ocean Circulation Study. J. Geophys. Res. 96:7089–7104. Google Scholar

35.

March, J. G., J. P. Benstead, and C. M. Pringle. 2003. Benthic community structure and invertebrate drift in a Pacific Island stream, Kosrae, Micronesia. Biotropica 35:125–130. Google Scholar

36.

Marquet, G., and R. Galzin. 1991. The eels of French Polynesia: taxonomy, distribution and biomass. La mer 29:8–17. Google Scholar

37.

Marquet, G., and P. Lamarque. 1986. Acquisitions recentes sur la biologie des anguillies de Tahiti et de Moorea (Polynesia Francaise): A. marmorata, A. megastoma, A. obscura. Vie Milieu 36:311–315. Google Scholar

38.

McCleave, J. D., R. C. Kleckner, and M. Castonguay. 1987. Reproductive sympatry of American and European eels and implications for migration and taxonomy. Am. Fish. Soc. Symp. 1:286–297. Google Scholar

39.

McCosker, J. E., R. H. Bustamante, and G. M. Wellington. 2003. The freshwater eel, Anguilla marmorata, discovered at Galapagos. Not. Galapagos 62:2–6. Google Scholar

40.

McDowall R. M. 2008. Jordan's and other ecogeographical rules, and the vertebral number in fishes. J. Biogeogr. 35:501–508. Google Scholar

41.

Miller, M. J. 2023. Spawning areas. Pages 52–64 in K. Tsukamoto, M. Kuroki, and S. Watanabe. Eel science. Springer Nature, Singapore. Google Scholar

42.

Miller, M. J., and K. Tsukamoto. 2017. The ecology of oceanic dispersal and survival of anguillid leptocephali. Can. J. Fish. Aquat. Sci. 74:958–971. Google Scholar

43.

Miller, M. J., N. Mochioka, T. Otake, and K. Tsukamoto. 2002. Evidence of a spawning area of Anguilla marmorata in the western North Pacific. Mar. Biol. 138:887–895. Google Scholar

44.

Miller, M. J., S. Bonhommeau, P. Munk, M. Castonguay, R. Hanel, and J. D. McCleave. 2015. A century of research on the larval distributions of the Atlantic eels: a reexamination of the data. Biol. Rev. 90: 1035–1064. Google Scholar

45.

Miller, M. J., M. Shimizu, J. Aoyama, S. Watanabe, M. Kuroki, E. Feunteun, T. Higuchi, A. Takeuchi, Y.-S. Han, P. Sasal, C. Dupuy, D. Jellyman, R. Schabetsberger, S. Kimura, N. Mochioka, T. Otake, and K. Tsukamoto. 2022. Distribution and abundance of leptocephali in the western South Pacific region during two large-scale sampling surveys. Prog. Oceanogr. 206:102853. Google Scholar

46.

Miller, M. J., P. Sasal, R. Schabetsberger, M. Kuroki, A. Acou, Y.-L. K. Chang, T. Higuchi, S. Watanabe, J. Aoyama, and E. Feunteun. 2023. The South Pacific: a unique geological and oceanographic region of freshwater island-oasis habitats for anguillid eel population interactions. Cybium 48(1):5–33. Google Scholar

47.

Minegishi, Y., J. Aoyama, J. G. Inoue, M. Miya, M. Nishida, and K. Tsukamoto. 2005. Molecular phylogeny and evolution of the freshwater eels genus Anguilla based on the whole mitochondrial genome sequences. Mol. Phylogenet. Evol. 34:134–146. Google Scholar

48.

Minegishi, Y., J. Aoyama, and K. Tsukamoto. 2008. Multiple population structure of the giant mottled eel, Anguilla marmorata. Mol. Ecol. 17:3109–3122. Google Scholar

49.

Myers, R. F., and T. J. Donaldson. 2003. The fishes of the Mariana Islands. Micronesica 35–36:598–652. Google Scholar

50.

Nelson, S. G., F. A. Camacho, J. E. Parham, R. B. Tibbatts, T. Leberer, and B. D. Smith. 1996. Surveys of the macrofauna of the Nanpil Kiepw and Lehn Mesi Rivers of Pohnpei. Univ. Guam Mar. Lab. Tech. Rep. 103:1–22. Google Scholar

51.

Nelson, S. G., J. E. Parham, R. B. Tibbatts, F. A. Camacho, T. Leberer, and B. D. Smith. 1997. Distributions and microhabitats of the amphidromous gobies in streams of Micronesia. Micronesica 30:83–91. Google Scholar

52.

Nguyen, A. T., H. T. Dao, H. T. Quang, S. Hagihara, P. M. Lokman, and E. L. Damsteegt. 2022. Genetic diversity and population structure of the giant mottled eel, Anguilla marmorata Quoy & Gaimard, 1824 in central Vietnam. Fishes 7:286. Google Scholar

53.

Réveillac, E., E. Feunteun, P. Berrebi, P.-A. Gagnaire, R. R. Lecomte-Finiger, P. Bosc, and T. Robinet. 2008. Anguilla marmorata larval migration plasticity as revealed by otolith microstructural analysis. Can. J. Fish. Aquat. Sci. 65:2127–2137. Google Scholar

54.

Reverdin, G., C. Frankignoul, E. Kestenare, and M. J. McPhaden. 1994. Seasonal variability in the surface currents of the equatorial Pacific. J. Geophys. Res. 99: 20323–20344. Google Scholar

55.

Righton, D., A. Piper, K. Aarestrup, E. Amilhat, C. Belpaire, J. Casselman, M. Castonguay, E. Díaz, H. Dörner, E. Faliex, E. Feunteun, N. Fukuda, R. Hanel, C. Hanzen, D. Jellyman, K. Kaifu, K. McCarthy, M. J. Miller, T. Pratt, P. Sasal, R. Schabetsberger, H. Shiraishi, G. Simon, N. Sjöberg, K. Steele, K. Tsukamoto, A. Walker, H. Westerberg, K. Yokouchi, and M. Gollock. 2021. Important questions to progress science and sustainable management of anguillid eels. Fish Fish. 22:762–788. Google Scholar

56.

Robinet, T., R. Lecomte-Finiger, K. Escoubeyrou, and E. Feunteun. 2003. Tropical eels Anguilla spp. recruiting to Réunion Island in the Indian Ocean: taxonomy, patterns of recruitment and early life histories. Mar. Ecol. Prog. Ser. 259:263–272. Google Scholar

57.

Rubinoff, D., and B. S. Holland. 2005. Between two extremes: mitochondrial DNA is neither the panacea nor the nemesis of phylogenetic and taxonomic inference. Syst. Biol. 54:952–961. Google Scholar

58.

Schabetsberger, R., F. Økland, K. Aarestrup, D. Kalfatak, U. Sichrowsky, M. Tambets, G. Dall'Olmo, R. Kaiser, and P. I. Miller. 2013. Oceanic migration behaviour of tropical Pacific eels from Vanuatu. Mar. Ecol. Prog. Ser. 475:177–190. Google Scholar

59.

Schabetsberger, R., F. Økland, D. Kalfatak, U. Sichrowsky, M. Tambets, K. Aarestrup, C. Gubili, J. Sarginson, B. Boufana, R. Jehle, G. Dall'Olmo, M. J. Miller, A. Scheck, R. Kaiser, and G. Quartly. 2015. Sympatric spawning of tropical Pacific eels from Vanuatu. Mar. Ecol. Prog. Ser. 521:171–187. Google Scholar

60.

Schabetsberger, R., A. Scheck, R. Kaiser, R. Leaana, C. Gubili, and F. Økland. 2019. Oceanic migration behaviour of Pacific eels from Samoa. Fish. Manag. Ecol. 26: 53–56. Google Scholar

61.

Schabetsberger, R., Y. L. K. Chang, and M. J. Miller. 2021. Spawning migration and larval dispersal of tropical Pacific eels (Anguilla spp.) in the centre of their distribution ranges. Mar. Ecol. Prog. Ser. 670:167–184. Google Scholar

62.

Schmidt, J. 1925. The breeding places of the eel. Smithsonian Institute Annual Report 1924:279–316. Google Scholar

63.

Tåning, A. V. 1952. Experimental study of meristic characters in fishes. Biol. Rev. 271:169–193. Google Scholar

64.

Tibblin, P., H. Berggren, O. Nordahl, P. Larsson, and A. Forsman. 2016. Causes and consequences of intra-specific variation in vertebral number. Sci. Rep. 6:26372. Google Scholar

65.

Tsukamoto, K., S. Chow, T. Otake, H. Kurogi, N. Mochioka, M. J. Miller, J. Aoyama, S. Kimura, S. Watanabe, T. Yoshinaga, A. Shinoda, M. Kuroki, M. Oya, T. Watanabe, K. Hata, S. Ijiri, Y. Kazeto, K. Nomura, and H. Tanaka. 2011. Oceanic spawning ecology of freshwater eels in the western North Pacific. Nat. Commun. 2: 1–9. Google Scholar

66.

Tsukamoto, K., M. Kuroki, and S. Watanabe. 2020. Common names for all species and subspecies of the genus Anguilla. Environ. Biol. Fish. 103:985–991. Google Scholar

67.

Watanabe, S. 2003. Taxonomy of the freshwater eels, genus Anguilla Schrank, 1798. Pages 3–18 in K. Aida, K. Tsukamoto, and K. Yamauchi, eds. Eel biology. Springer, Tokyo. Google Scholar

68.

Watanabe, S. 2023. Morphology and taxonomy. Pages 3–21 in K. Tsukamoto, M. Kuroki, and S. Watanabe, eds. Eel science. Springer, Tokyo. Google Scholar

69.

Watanabe, S., J. Aoyama, and K. Tsukamoto. 2006. Reconfirmation of morphological differences between A. australis australis Richardson and A. australis schmidtii Phillipps. N. Z. J. Mar. Freshwater Res. 40: 325–331. Google Scholar

70.

Watanabe, S., J. Aoyama, M. J. Miller, S. Ishikawa, E. Feunteun, and K. Tsukamoto. 2008. Evidence of population structure in the giant mottled eel, Anguilla marmorata, using total number of vertebrae. Copeia 2008:681–689. Google Scholar

71.

Watanabe, S., J. Aoyama, and K. Tsukamoto. 2009a. A new species of freshwater eel Anguilla luzonensis (Teleostei: Anguillidae) from Luzon Island of the Philippines. Fish. Sci. 75:387–392. Google Scholar

72.

Watanabe, S., M. J. Miller, J. Aoyama, and K. Tsukamoto. 2009b. Morphological and meristic evaluation of the population structure of Anguilla marmorata across its range. J. Fish Biol. 74:2069–2093. Google Scholar

73.

Watanabe, S., M. J. Miller, J. Aoyama, and K. Tsukamoto. 2011. Analysis of vertebral counts of the tropical anguillids, Anguilla megastoma, A. obscura, and A. reinhardtii, in the western South Pacific in relation to their possible population structure and phylogeny. Environ. Biol. Fish. 91:353–360. Google Scholar
Shun Watanabe, Michael J. Miller, Tomoki Honryo, and Pierre Sasal "Indo-Pacific Eels (Anguilla marmorata) from the Caroline Islands Belong to the Micronesia Population Based on Total Number of Vertebrae Counts," Pacific Science 78(2), 219-238, (6 January 2025). https://doi.org/10.2984/78.2.6
Accepted: 24 April 2023; Published: 6 January 2025
KEYWORDS
Anguilla marmorata
evolutionary history
Kosrae
MTDNA LINEAGES
Pohnpei
spawning area
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