Eels: Physiology, Habitat and Conservation : Physiology, Habitat and Conservation [1 ed.] 9781619422421, 9781619422315

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Copyright © 2012. Nova Science Publishers, Incorporated. All rights reserved. Eels: Physiology, Habitat and Conservation : Physiology, Habitat and Conservation, Nova Science Publishers, Incorporated,

Copyright © 2012. Nova Science Publishers, Incorporated. All rights reserved. Eels: Physiology, Habitat and Conservation : Physiology, Habitat and Conservation, Nova Science Publishers, Incorporated,

MARINE BIOLOGY

EELS

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PHYSIOLOGY, HABITAT AND CONSERVATION

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MARINE BIOLOGY

EELS

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PHYSIOLOGY, HABITAT AND CONSERVATION

NAKASHIMA SACHIKO AND

MICHIYO FUJIMOTO EDITORS

Nova Science Publishers, Inc. New York

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Library of Congress Cataloging-in-Publication Data Eels : physiology, habitat, and conservation / editors, Nakashima Sachiko and Michiyo Fujimoto. p. cm. Includes index. ISBN  ((%RRN) 1. Eels--Physiology. 2. Eels--Habitat. 3. Eels--Conservation. I. Sachiko, Nakashima. II. Fujimoto, Michiyo. QL637.9.A5E46 2011 597'.43--dc23 2011043396

Published by Nova Science Publishers, Inc. † New York

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CONTENTS   vii 

Preface Chapter 1

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Chapter 2

Chapter 3

Chapter 4

Chapter 5

Chapter 6

Species, Geographic Distribution, Habitat and Conservation of Freshwater Eels Shun Watanabe and Michael J. Miller 

1 

Ecological Risk for Organotin Accumulation in Relation to Life History in the Anguillid Eels Takaomi Arai 

45 

Habitat Use and Migration in the Japanese Eel Anguilla Japonica and Introduced Anguillid Eels in Japanese Natural Waters Naoko Chino and Takaomi Arai  Early Life History and Recruitment Mechanisms of the Freshwater Eels Genus Anguilla Takaomi Arai  Quality and Vitamin Content of Eggs of Japanese Eel Anguilla Japonica Hirofumi Furuita, Hiroyuki Matsunari and Takeshi Yamamoto  Modulation of Gene Transcriptional Level of Different Ion Transporters in Eel Gill MitochondriaRich Cells Upon Osmotic Stress William Ka Fai Tse and Chris Kong Chu Wong 

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69 

91 

115 

133 

vi Chapter 7

Chapter 8

Contents Wide Geographic Distribution with Little Population Genetic Differentiation: A Case Study of the Japanese Eel Anguilla Japonica Yu-San Han  Differences in Vitamin K Concentration in Japanese Eel Anguilla Japonica from Different Cultured Areas in Japan and Taiwan Miho Udagawa and Yumiko Yamashita 

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Index

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149 

165  173 

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PREFACE This book presents topical research in the study of the physiology, habitat and conservation of eels. Topics discussed in this compilation include the species and geographic distribution of freshwater eels; the ecological risk for organotin accumulation in relation to life history in the anguillid eel; habitat use and migration in the Japanese eel anguilla japonica and quality and vita Chapter 1- Freshwater eels of the genus Anguilla are widely distributed throughout many parts of the world and consist of 16 species including the recently discovered Anguilla luzonensis in the Philippines. Three of the species are divided into separate subspecies that have different morphological characteristics and geographic ranges. The morphology of all anguillid eels is generally similar, but they can be divided into four groups using body marking, maxillary bands of teeth and the position of the dorsal fin, with the number of vertebrae also being important in their taxonomy. There are 5 temperate and 11 tropical anguillid species, but they all have catadromous life histories, with their offshore spawning areas being located at tropical latitudes. Anguillid species vary in maximum body size and in the sizes of their species ranges, with Anguilla marmorata being one of the largest species with the widest geographic distribution, while species such as A. borneensis and A. dieffenbachii have restricted geographic distributions. Some species have single spawning areas and panmictic spawning populations, but others have multiple populations, such as A. marmorata, which is present in 3 different ocean basins. All anguillid species enter freshwater for their juvenile growth period, but many eels remain in estuaries, and brackish lakes or lagoons and may not enter freshwater. In freshwater, anguillids live in rivers, streams and lakes, but the degree of use of different habitats ranging from small streams far inland to the estuary appears to vary among species, especially in regions with

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Nakashima Sachiko and Michiyo Fujimoto

several species living sympatrically. Some eels have been found to switch between habitats, such as moving back downstream to the estuary to complete their juvenile growth period. Their unique catadromous life history has made them vulnerable to the effects of dams that block their migrations, and pollutants, parasites, viruses and overfishing may be affecting some species. Changes in conditions in the ocean may also influence their recruitment success by affecting their larval feeding or transport success. The European eel has been declared to be critically threatened, and a new management plan has been initiated. The conservation status of most freshwater eel species is not well known however, so more effort is needed globally to protect these unique fishes that use both freshwater and the ocean during their life histories. Chapter 2- A number of recent studies found that anguillid eels have never migrated into fresh water, spending their entire life history in the ocean. Furthermore, those studies found an intermediate type between marine and freshwater residents, which appear to frequently move between different environments during their growth phase. The discovery of marine and brackish water residents in the eels suggests that anguillid eels do not all have to be catadromous, and it calls into question the generalized classification of diadromous fishes. It suggests that the ecological risks caused by various contaminants differ among their life histories in a species. However, there is little information available on the ecological risks for contaminants for anguillid eels as well as other diadromous fish. In this chapter, the ecological risks for organotin compounds (OTs) such as tributyltin (TBT) and triphenyltin (TPT) compounds, and their breakdown products, were evaluated in the eels having sea, estuarine and river life histories. There were generally three different life history patterns, which were categorized ‘marine resident’ (spent most of their life in the sea and did not enter freshwater), ‘estuarine resident’ (inhabited estuaries or switched between different habitats), and ‘freshwater resident’ (entered and remained in freshwater river habitats after arrival in the estuary) in the species. There were generally no significant correlations between TBT and TPT accumulation and various biological characteristics such as total length, body weight, age and sex in A. japonica, A. marmorata and A. bicolor pacifica. The concentrations of TBT and TPT in silver eels (mature eels) were significantly higher than those in yellow eels (immature eels), and the percentages of TBT and TPT were also higher in silver eels than in yellow eels. A positive correlation was found between TBT concentration and the gonadosomatic index (GSI). It is thus considered that silver eels have a higher ecological risk of contamination by TBT than yellow eels. TBT and TPT concentrations in marine resident eels were significantly

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Preface

ix

higher than those in freshwater resident eels. In contrast, no significant differences were observed in TBT and TPT concentrations in estuarine resident eels compared to marine and freshwater resident eels. These results suggest that marine resident eels have a higher ecological risk of OT contamination than freshwater resident eels during their life history, and the risk of OTs in estuarine resident eels is considered to be intermediate between that of marine and freshwater resident eels. Positive linear relationships were found between otolith strontium:calcium ratios and the concentrations of TBT and TPT. Therefore, these results suggest that the ecological risk of OTs increase, as the sea residence period in the eel become longer. Even at the same maturation stage, TBT and TPT concentrations in marine resident eels were significantly higher than those in freshwater resident eels. Thus, it is clear that migratory type is a more important factor for OT accumulation than maturation stage. The risks involved in the exposure of marine and estuarine residenct eels to TBT and TPT may in turn influence freshwater resident eels, resulting in a disturbance in the overall population maintenance of the anguillid eels. Chapter 3- The catadromous eels of the genus Anguilla are famous for their remarkable migrations between fresh water and marine habitats. The use of Sr:Ca ratios in fish otoliths to reconstruct historical patterns of fish movement between aquatic habitats of different salinity ranges (fresh, estuarine, marine) can be extended to evaluate the frequency and duration of inter-habitat movements. Otolith microchemistry studies have revealed that some yellow and silver eels of temperate Anguilla japonica never migrate into fresh water, but spend their entire life history in the ocean. The application of otolith Sr:Ca ratios to trace the migratory history of the eel has also revealed otolith signatures intermediate to those of marine and freshwater residents of the eel, all of which appeared to reflect estuarine resident, or showed clear evidence of switching between different salinity environments. It thus appears that a proportion of the eels move frequently between different environments during their growth phase. Therefore, because individuals of the eel species have been found to remain in estuarine or marine habitats, it appears that the Japanese eel does not all enter into fresh water environments and that the species display more of a facultative catadromy. In Japanese natural waters, several non-native species, such as European eel, A. anguilla, American eel, A. rostrata, and Australian shortfinned eel, A. australis, have recently been found. This is due to their escaping from aquaculture operations or intentional release. Analyses of the otolith Sr:Ca ratios of the European eels caught in the water showed that they had been not only typical freshwater resident but also

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Nakashima Sachiko and Michiyo Fujimoto

marine resident before capture. Marine residents that never migrate into fresh water often occur in its own habitat in Europe. This indicates that the European eels retain their own nature despite being far from their original habitat. This further suggests that the authors must consider that the ecological impact of European eels would affect not only fresh water habitats but also coastal ecosystems in and around Japan. The European and American eels had found to begin maturation, and start downstream migration far from its native range. This discovery of introduced eels initiating their spawning migration at the same time as the Japanese eel raises concerns about the potential impact of interbreeding between species and the possible effects on the fishery resources of A. japonica. Chapter 4- The freshwater eels have fascinated biologists because of their spectacular thousands of long-distance migrations between their freshwater habitats and their spawning areas far out in the ocean. However, recent studies indicated that much shorter migrations of a few hundred kilometers are made by tropical eels to spawn in areas near their freshwater habitats, clearly contrasting with the long distance migrations of their counterparts in temperate regions, such as the European eel Anguilla anguilla, the American eel A. rostrata and the Japanese eel A. japonica. Ages at metamorphosis and recruitment were constant throughout year, whereas significant differences were found among species in tropical species. Hatchings were estimated to occur throughout the entire year in the species. In both tropical and temperate species, positive linear relationships were found between age at metamorphosis and age at recruitment, suggesting that early metamorphosing larvae were recruited to freshwater habitats at an early age. Year-round recruitment of tropical glass eels to the river mouth would necessarily follow year-round spawning and stable recruitment age. Such a recruitment mechanism differs from that of temperate eels, the latter having a limited spawning season followed by a limited period of recruitment. This chapter outlines the recent findings on the early life ecology of the freshwater eels such as larval migrations, metamorphosis, recruitment and growth. Based on these findings, the present state of our understanding about the evolution of oceanic migration in the genus Anguilla is discussed. Chapter 5- This chapter describes the relationship between egg vitamin concentrations and egg quality and techniques to improve vitamin levels and quality of eggs in artificially matured Japanese eel Anguilla japonica. Hatching and survival rates of larvae significantly increased with elevated levels of egg vitamin C (VC). In contrast to VC, the relationship between vitamins E (VE) and A (VA) and survival rate showed a clear peak, with

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reduced survival rates at both higher and lower vitamin concentrations. The ratio of VE to lipid or highly unsaturated fatty acid (HUFA) in eggs positively correlated with hatching and survival rates of larvae. Therefore, techniques to increase egg VC and VE levels were investigated, since increasing these vitamins in eggs was expected to improve egg quality of the eel. Supplementation of VC and VE in the broodstock diet, however, did not effectively improve the vitamin concentration and quality of eggs of eel, although in some species supplementation of vitamins to diets of broodstock improves egg quality. In order to improve the egg quality of eel, the effects of direct injection of VC and VE into broodstock during artificial maturation on the vitamin levels of broodstock and eggs and subsequent egg and larval quality was investigated. The levels of both vitamins in eggs and broodstock increased following vitamin injection. Hatching rate, survival and normality of larvae increased with vitamin treatments. Further, combination of supplementation to diet and injection of the vitamins were investigated. Treatment of vitamins to the diet alone significantly increased the egg vitamin level, but did not improve egg quality. Combination of dietary treatment and injection of the vitamins significantly improved both the vitamin level and quality of eggs, compared to the dietary treatment alone and no-vitamin treatment groups. These results suggest that VC and VE concentrations of eggs is one of the factor determining egg quality, and that supplementation of these vitamin to broodstock, especially via vitamin injections, effectively improves egg quality in Japanese eel. Chapter 6- Eels are euryhaline fishes that their life cycles involve the stay in fresh water and seawater. In order to compensate the osmotic challenges in fresh water (ion loss and water gain) and in seawater habitat (ion gain and water loss), eels have developed specific osmoregulatory mechanisms to acclimate rapidly and effectively in such two extreme aquatic environments. Fish gill is the outermost tissue that is in direct contact with the external media. In the gill tissue, two specific osmoregulatory cell types (pavement cells (PVCs) and mitochondria-rich/ chloride cells (MRCs/CCs)) have been identified and characterized. It is generally believed that MRCs, which the authors will focus on, are the essential ion-regulatory cell type in the eel gill. With the recent advances in molecular biology, together with the immunohistochemical staining and electrophysiology studies, more transcriptional and translational profiling data are generated to unfold the molecular nature of the branchial osmoregulatory mechanisms. In this review, they will begin with the general description of eel gill structure and cell types

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(PVCs and MRCs), followed by the discussion on the differential mRNA expressions of different ion transporters in MRCs under hyper/ hypo- tonic stress conditions. Lastly, the authors will provide an opinion on the use of recent advanced genomic transcriptome data to form a public accessible database. To summarize, this chapter provides essential updated information on the expressions of ion channels/ transporters in eel gills acclimated in waters of different salinities, providing new in-sight on the future direction of eel gill studies in modern molecular perspectives. Chapter 7- In general, organisms with wider geographic distributions are usually accompanied by more significant population genetic differentiation due to spawning spatial isolation . The Japanese eel (Anguilla japonica Temminck and Schlegel, 1846), however, does not follow this rule. It has a wide geographic distribution in East Asia, south from the Taiwan and north to Japan, but without a significant population genetic structuring. Recent studies using microsatellite DNA loci indicated no significant genetic differences, either spatially or temporally, among populations of Japanese eels in East Asia. Differences in habitat utilization or larval duration were not found to contribute to population structuring. These results strongly suggest the existence of a single panmictic population of Japanese eels. The maturing silver eels leave continental rivers and migrate more than 2,000 km over several months to spawn in restricted areas (12.5–16°N and 141–143°E) west of Mariana Island during a specific time span (mainly between Jun.-Aug.). Although many spawning patches in the spawning site may form, each batch of larvae could be passively transported via the North Equatorial Current, Kuroshio, and its branch waters to wide East Asian growth habitats. The ''mixed'' growing schools at each location would form the new ‘‘mate aggregates’’ when they migrate together and form a spawning patch. This mode could efficiently prevent the population structuring from occurring and thus maintains the Japanese eel as a panmictic population. Chapter 8 Japanese eel, Anguilla japonica, is major fish throughout Japan, because a large amount of the cultured variety is consumed. Japanese eel is cultured in many areas of Japan, as well as in Taiwan and China. Recently, traceability of produce has become an important issue because quality must be considered as a convergence of the consumers’ wishes and needs and the intrinsic and extrinsic quality attributes of fish. Consumers are more concerned about how the fish are produced, and which type of feed ingredients are used. However, it is difficult to determine the place of origin simply by the appearance of the fish. Vitamin K is well known to have several derivatives, such as phylloquinone (PK), mennaquinone (MK) and menadione (MD).

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The types of vitamin K in Japanese eel cultured in various areas were measured in order to detect differences by area of culture. Except a few analyses, only MK-4 was detected in the tissue of fish cultured in Japan. MK-4 was the major vitamin K in the tissue of Japanese fish, whereas several longchain MKs and PK were detected in the tissue of Taiwan fish. The fish cultured in Japan fed mainly on a commercial diet, whereas the fish cultured in Taiwan fed on benthos or plankton in addition to their commercial diet. This finding suggests that Japanese eel cultured in Japan were raised under the conditions in the controlled room. By contrast, the tissue of the Taiwan fish showed a different pattern of vitamin K concentration from that of Japanese ones.

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In: Eels Editors: N. Sachiko and M. Fujimoto

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Chapter 1

SPECIES, GEOGRAPHIC DISTRIBUTION, HABITAT AND CONSERVATION OF FRESHWATER EELS Shun Watanabe∗ and Michael J. Miller• Copyright © 2012. Nova Science Publishers, Incorporated. All rights reserved.

Atmosphere and Ocean Research Institute, The University of Tokyo, Kashiwa, Chiba, Japan

ABSTRACT Freshwater eels of the genus Anguilla are widely distributed throughout many parts of the world and consist of 16 species including the recently discovered Anguilla luzonensis in the Philippines. Three of the species are divided into separate subspecies that have different morphological characteristics and geographic ranges. The morphology of all anguillid eels is generally similar, but they can be divided into four groups using body marking, maxillary bands of teeth and the position of the dorsal fin, with the number of vertebrae also being important in their taxonomy. There are 5 temperate and 11 tropical anguillid species, but they all have catadromous life histories, with their offshore spawning areas being located at tropical latitudes. Anguillid species vary in maximum body size and in the sizes of their species ranges, with Anguilla ∗ •

E-mail: [email protected]. E-mail: [email protected].

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marmorata being one of the largest species with the widest geographic distribution, while species such as A. borneensis and A. dieffenbachii have restricted geographic distributions. Some species have single spawning areas and panmictic spawning populations, but others have multiple populations, such as A. marmorata, which is present in 3 different ocean basins. All anguillid species enter freshwater for their juvenile growth period, but many eels remain in estuaries, and brackish lakes or lagoons and may not enter freshwater. In freshwater, anguillids live in rivers, streams and lakes, but the degree of use of different habitats ranging from small streams far inland to the estuary appears to vary among species, especially in regions with several species living sympatrically. Some eels have been found to switch between habitats, such as moving back downstream to the estuary to complete their juvenile growth period. Their unique catadromous life history has made them vulnerable to the effects of dams that block their migrations, and pollutants, parasites, viruses and overfishing may be affecting some species. Changes in conditions in the ocean may also influence their recruitment success by affecting their larval feeding or transport success. The European eel has been declared to be critically threatened, and a new management plan has been initiated. The conservation status of most freshwater eel species is not well known however, so more effort is needed globally to protect these unique fishes that use both freshwater and the ocean during their life histories.

INTRODUCTION Freshwater eels of the family Anguillidae are catadromous fishes that are famous for their long migrations to their offshore spawning areas (Schmidt 1922; Tsukamoto 1992). They are members of the order Anguilliformes, the true eels, which also includes more than 10 other families of marine eels consisting of more than 800 species worldwide (Nelson 2006). Recently, a new species Protoanguilla palau has been discovered in a fringing-reef cave in Palau that appears to be ‘living fossil’ of the Anguilliformes and has been assigned to the new family of Protoanguillidae (Johnson et al. 2011). All anguilliform fishes and several other orders of fishes such as the tarpons, bonefishes and notacanths comprise the superorder Elopomorpha, whose species are all similar in having leptocephalus larvae (Inoue et al. 2004), despite having contrasting adult body forms and life histories (Miller and Tsukamoto 2004). The leptocephalus larva is a unique laterally compressed and transparent larval form that has a long duration and a large size increase (Smith 1989; Miller 2009), which is not found in other groups of

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Species, Geographic Distribution, Habitat and Conservation …

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fishes. Although juvenile and adult anguillid eels resemble various other families of benthic marine eels, they are actually phylogenetically related to the mesopelagic eels that live in the deep-sea (Inoue et al. 2010). Anguillid eels are unique among the Elopomorpha fishes however, because they extensively use both true oceanic waters and purely freshwater habitats. They are distributed throughout much of the world, but not in the South Atlantic or eastern Pacific (Figure 1) (Schmidt 1909, 1925; Ege 1939; Tesch 1977, 2003). They can be separated into different species during the juvenile and adult stage using morphological characters such as skin colorations, length of their dorsal fins, and tooth patterns (Figure 2, Table 1), but these characters can overlap in some species from different regions, so genetic identification is often useful especially since some species are being transported around the world due to the trade of glass eels (Watanabe et al. 2004; Tsukamoto et al. 2009). Their leptocephali are all similar morphologically and also usually require DNA identification to separate different species (Aoyama et al. 1999, 2000a, 2003).

Figure 1. The worldwide distribution of the genus Anguilla (areas covered by thick lines), with the number of species or subspecies in each ocean basin shown in parenthesis. The distribution of eels inland away from the coastlines is not shown.

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Freshwater Eels

Figure 2. Types of morphology of anguillid eels that are used to separate the different species that include the position of the dorsal fin, skin coloration, and dentition patterns. The total number of vertebrae of each eel species is also important.

Their leptocephalus larvae live only in the ocean and are transported by ocean currents back to their continental or island growth habitats where the yellow eel stage occurs (Tesch 1977, 2003; Tsukamoto et al. 2002; Aoyama 2009). The leptocephali metamorphose into glass eels as they approach the continental shelves or near islands and then the glass eels enter estuaries or migrate upstream into freshwater habitats (Tsukamoto 1990; Otake 2003). The yellow eels can either remain in the estuary or live in freshwater streams, rivers, or lakes (Moriarty 2003; Tesch 2003). It is becoming well documented though, that many eels can also switch between habitats during their yellow eel stage (Tsukamoto and Arai 2001; Jessop et al. 2002; Morrison et al. 2003; Daverat et al. 2006).

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Table 1. List of all anguillid eels species worldwide that are likely valid species based on both morphological and molecular genetic udies, showing the general morphological characteristics of each species that were recognized by the important revision of the genus by Ege (1939) and the more recent changes or new species Species names

Morphological characters

According to Ege (1939)

As of 2011

Skin coloration pattern

Bands of maxillary teeth

Length of dorsal fin

Mean No. of vertebrae

Region

A. celebesensis Kaup, 1856

A. celebesensis Kaup, 1856

Mottled

Broad

Longfin

103.1

A. interioirs Whitley, 1938

A. interioirs Whitley, 1938

Mottled

Broad

Longfin

104.1

Tropical

A. megastoma Kaup, 1856

A. megastoma Kaup, 1856

Mottled

Broad

Longfin

112.7

Tropical

A. luzonensis Watanabe, Aoyama

Mottled

Broad

Longfin

104.8

Tropical

Tropical

and Tsukamoto, 2009

A. ancestralis Ege, 1939 A. nebulosa nebulosa McClelland, 1844

A. bengalensis bengalensis (Gray, 1831)

Mottled

Narrow

Longfin

105.6

Tropical

A. nebulosa labiata (Peters, 1852)

A. bengalensis labiata (Peters, 1852)

Mottled

Narrow

Longfin

109.1

Tropical

A. marmorata Quoy and Gaimard, 1824

A. marmorata Quoy and Gaimard, 1824

Mottled

Narrow

Longfin

111.3

Tropical

A. reinhardtii Steindachner 1867

A. reinhardtii Steindachner 1867

Mottled

Narrow

Longfin

107.8

Tropical

A. borneensis Popta, 1924

A. borneensis Popta, 1924

Plain

-*

Longfin

105.5

Tropical

A. japonica Temminck and Schlegel, 1846

A. japonica Temminck and Schlegel, 1846

Plain

-

Longfin

115.8

Temperate

A. rostrata (Lesueur, 1817)

A. rostrata (Lesueur, 1817)

Plain

-

Longfin

107.2

Temperate

A. anguilla (Linnaeus, 1758)

A. anguilla (Linnaeus, 1758)

Plain

-

Longfin

114.7

Temperate

A. dieffenbachii Gray, 1842

A. dieffenbachii Gray, 1842

Plain

-

Longfin

112.7

Temperate

A. mossambica (Peters, 1852)

A. mossambica (Peters, 1852)

Plain

-

Longfin

102.9

Tropical

A. bicolor bicolor McClelland, 1844

A. bicolor McClelland, 1844

Plain

-

Shotfin

107.2

Tropical

A. bicolor pacifica Schmidt, 1928

A. bicolor pacifica Schmidt, 1928

Plain

-

Shotfin

109.5

Tropical

A. obscura Günther, 1872

A. obscura Günther, 1872

Plain

-

Shotfin

104.0

Tropical

A. australis australis Richardson, 1841

A. australis Richardson, 1841

Plain

-

Shotfin

112.6

Temperate

Plain

-

Shotfin

111.7

Temperate

A. australis schmidtii Phillipps, 1925 A. australis schmidtii Phillipps, 1925 * Teeth patterns not clear or useful for distinguishing plain skin species.

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After a period of a few years to more than a decade the yellow eels transform into the silver eel stage and then migrate to their offshore spawning areas (Tesch 2003; Aoyama and Miller 2003; Tsukamoto 2009). The spawning areas are located at various distances from their growth habitats with some tropical anguillids having very short migrations and temperate species having long migrations (Aoyama et al. 2003; Aoyama 2009). Spawning and early larval development appears to take place in the upper few hundred meters of the ocean (Tsukamoto et al. 2011), with their late stage leptocephali also residing in the surface layer and shallower than 100 m at night (Castonguay and McCleave 1987; Miller 2009). The life history and biology of anguillid eels is becoming better understood for some species (Aida et al. 2003), but there are increasing concerns in recent years about population declines that have been observed especially for the Northern Hemisphere temperate species (Dekker et al. 2003). There is evidence of declines in recruitment for the Japanese eel, Anguilla japonica (Tatsukawa 2003), the American eel, Anguilla rostrata (Casselman 2003), and the European eel, Anguilla anguilla, has declined so drastically that it has been placed on the IUCN red list (CITES 2006; CITES 2007). Their catadromous life cycle in which they are exposed to anthropogenic influences in their freshwater and estuarine growth habitats, along with their completely separate early life history in the ocean that is difficult to observe, has made it hard to determine what is causing the declines in anguillid eel species. The possible factors affecting them include the effects of dams, pollutants, parasites, viruses and overfishing, and changes in oceanatmosphere conditions also appear to have the potential to affect their recruitment success (Castonguay et al. 1994; Haro et al. 2000; Feunteun 2002; Miller et al. 2009). The uncertainty about what is causing the declines in freshwater eels, calls for increased conservation efforts for these unusual fishes worldwide. The objective of this review is to overview the distribution and species composition of freshwater eels worldwide, to briefly outline what is known about their basic life history and habitat use, and to discuss conservation issues related to anguillid eels. This information can provide a useful introduction to the other chapters contained in this book.

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1. TAXONOMY AND PHYLOGENY The taxonomy and species identification of the genus Anguilla Schrank, 1798 has been somewhat complicated over the years because there are relatively few morphological characteristics that have been found to be useful for distinguishing different species. Using skin coloration patterns (mottled vs. plain), length of the dorsal fin (longfin vs. shortfin), and types of tooth patterns (broad vs. narrow bands of maxillary teeth), there are clearly 4 morphological groups of species (Ege 1939; Watanabe 2003; Watanabe et al. 2004) as follows: 1) mottled skin and broad maxillary bands of teeth; 2) mottled skin and narrow maxillary bands of teeth; 3) plain marking and long dorsal fin; 4) plain marking and short dorsal fin. When defining these four groups, Watanabe et al. (2004) did not use the character of a toothless longitudinal groove in the maxillary and mandibular bands of teeth that Ege (1939) used because this character was subjective and unclear. But within these 4 groups the eel species have very similar morphological features making them difficult to distinguish (Watanabe et al. 2004). The total number of vertebrae (TV) is useful for separating some species within each group (Ege 1939; Watanabe et al. 2005), but there are many cases of overlap in this character, and TV can only be counted using difficult procedures such as x-ray or CT (computed tomography) scanning. This lack of useful characters and the overlap of TV among many species has seemingly made this genus a difficult taxonomic group. Surprisingly, these species were only evaluated again quite recently when new tropical eel specimens were obtained from the less accessible parts of the world (Watanabe 2003; Watanabe et al. 2004). The comprehensive revisions of the genus Anguilla were done by Kaup (1856), Guሷnther (1870) and Ege (1939) using morphological analysis. In the last revision by Ege (1939), this genus was classified into 16 species, three of which were divided into two subspecies (Table 1), and the phylogeny of anguillid species were evaluated for the first time. By building on earlier taxonomic works (Schmidt 1915, 1927, 1928a,b), Ege (1939) was able to accomplish a monumental systematic, phylogenetic and geographical study of the freshwater eels. However, there has been a variety of new knowledge accumulated about the taxonomy and phylogeny of anguillid species since his study. The history of the taxonomy of this eel family is somewhat complex, since according to Fishbase (ver.06/2011, www.fishbase.org), there were 116 scientific names of freshwater eels so far. For example, 36 scientific names

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including Anguilla anguilla were given to the European eel, which likely reflects the amount of interest in eels over the years. After Ege’s (1939) taxonomy, Castle and Williamson (1974) reported that based on morphological analysis, A. ancestralis Ege, 1939, which was described by Ege (1939) using only glass eels, was a synonym of A. celebesensis Kaup, 1856. Furthermore, there were descriptions of three new species, A. breviceps Chu and Jin, A. foochowensis Chu and Jin and A. nigricans Chu and Wu, in 1984 based on the external morphology and body proportions of single individual eel specimens (Chu 1984). However, Tabeta (1994) has pointed out the necessity of a reexamination of these unconfirmed species in China. It is likely that A. breviceps and A. nigricans will be a junior synonym of A. japonica and A. foochowensis will be a junior synonym of A. bicolor pacifica. Other taxonomic problems within the genus Anguilla are ongoing even more recently. The Borneo longfin eel, Anguilla borneensis Popta, 1924, that is endemic to eastern Borneo Island of Malaysia and Indonesia has been widely recognized as a valid species since Ege (1939). However, Bauchot et al. (1993) recently revived the name of A. malgumora Kaup, 1856 as a senior synonym of A. borneensis simply according to the principle of priority, but without morphological examination. Smith (1999) also listed A. malgumora Schlegel in Kaup, 1856 for the Borneo longfin eel in his species identification guide, and the name A. malgumora Kaup continues to be treated as valid in some current literature (e. g., Martin-Smith and Tan 1998; Lin et al. 2001, 2002, 2005; Teng et al. 2009) and web compilations (e. g., Catalog of Fishes; Fishbase). Ege (1939) proposed that A. malgumora Schlegel should be treated as a synonym of A. anguilla (Linnaeus). Silfvergrip (2009) argued that the Borneo longfin eel was erroneously cited as A. malgumora Kaup and therefore, its correct name should be A. borneensis. The name A. borneensis as the Borneo longfin eel is used in this chapter, since for various reasons it is probably the valid species name (Watanabe et al. unpublished manuscript). Ege (1939) used the name Anguilla nebulosa McClelland, 1844 for the Indian and African mottled eels, which form two subspecies. However, either the first nomenclatural act or the first published name is given precedence in the International Code of Zoological Nomenclature, so this species name should be Anguilla bengalensis as described by Gray (1831), even if there is no extant type series (Eschmeyer 1998), so A. bengalensis is chosen in this chapter. The most interesting recent change is that using DNA identification a new species, Anguilla luzonensis, has been found in the Pinacanauan River, which is a tributary of the Cagayan River on northern Luzon Island of the Philippines

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(Watanabe et al. 2009a). Historically, this species would have been identified as A. celebesensis when it was encountered on northern Luzon Island before A. luzonensis was discovered. This new species was also detected within glass eels imported into Taiwan from northern Luzon Island by Teng et al. (2009) who named it as Anguilla huangi. These newly described species of eels from Luzon are morphologically similar (Teng et al. 2009; Watanabe et al. 2009a) and were genetically distinct from all known anguillid eel species (Teng et al. 2009; Minegishi et al. 2010) so they are the same species. The first nomenclatural act or the first published name is given precedence and in the case of the new eel species, the name luzonensis was published in March 2009 (Watanabe et al. 2009a) while huangi was published in November 2009 (Teng et al. 2009), so the species name luzonensis has priority and precedence over the second name. More biological and species distribution information is needed for this species though, so it can be better understood. It is clear however that A. luzonensis is a valid new species of the genus, so until any more new species are discovered, there are now 16 valid species of anguillid eels that are recognized in the world, three of which were divided into two subspecies (Table 1). At least two of the three subspecies appear to be morphologically and genetically distinct, but considering the multiple populations that have now been found within Anguilla marmorata (Ishikawa et al. 2004; Minegishi et al. 2008; Watanabe et al. 2008a, 2009b), the taxonomy of these subspecies and populations may need further evaluation (Dijkstra and Jellyman 1999; Shen and Tzeng 2007; Watanabe 2003; Watanabe et al. 2006, 2008b). Ege (1939) used the morphology of the freshwater eel species to propose the phylogenetic relationships of the genus, but recent phylogenetic research using DNA analyses have shown that the morphology is not clearly reflecting the evolutionary history of these eels, since some characters may have evolved separately more than once. The first molecular phylogenetic approaches to the genus Anguilla were conducted by Tagliavini et al. (1995, 1996) and Aoyama et al. (1996). Thereafter, two molecular phylogenetic studies of the genus Anguilla were published, in which Lin et al. (2001) examined mitochondrial 12S rRNA and cytochrome b genes of 12 species and Aoyama et al. (2001) examined 16S rRNA cytochrome b genes from 15 species (Figure 3A). The complete mtDNA sequences of 15 species of the genus Anguilla were then determined to analyze their phylogenetic relationships by Minegishi et al. (2005) (Figure 3B). Furthermore, Teng et al. (2009) showed a DNA phylogeny of 16 species including A. luzonensis (Figure 3C).

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There were slightly different results and interpretations of the phylogeographic histories of anguillid eels among the studies on the phylogeneny of anguillid eels (Aoyama et al. 2001; Lin et al. 2001; Minegishi et al. 2005; Teng et al. 2009). The most ancestral or basal species suggested by these studies were different, and the hypothesized dispersal route of anguillid eels into the Atlantic Ocean was different as well (Tethys Sea route: Aoyama et al. 2001, Panama route: Lin et al. 2001; Teng et al. 2009). However, the 4 sister relationships, between A. anguilla and A. rostrata, among A. dieffenbachii, A. australis australis and A. australis schmidtii, between A. celebesensis and A. megastoma, and among A. obscura, A. bicolor bicolor and A. bicolor pacifica, were the same among the 3 phylogenetic studies (Aoyama et al. 2001; Minegishi et al. 2005; Teng et al. 2009). Both A. borneensis and A. mossambica were suggested to be basal species in these studies though (Aoyama et al. 2001; Minegishi et al. 2005), which suggests that the mtDNA of the genus Anguilla does not include enough information for a robust phylogenetic reconstruction. It seems that lineages of the genus Anguilla have experienced particular evolutionary events such as rapid radiation and extinction of phylogenetically critical species. Careful consideration of the phylogenetic relationships of the anguillid species are needed, not only with statistical supports of the phylogeny, but also considering the geography of landmasses and ocean basins over evolutionary time. The complexity and often unexpected nature of anguillid eels is perhaps best illustrated by the recent discovery that the freshwater eels are not related to other similar appearing eels among the more than 800 species of eels of the order Anguilliformes, but are related to morphologically very different species. Inoue et al. (2010) showed strong evidence that anguillids are directly related only to midwater eel species that live in the deep ocean by conducting phylogenetic analyses of the whole mitochondrial genome sequences from 56 species representing all of the 19 anguilliform families. The freshwater eels occupy an apical position within the anguilliforms, forming a highly supported monophyletic group with various oceanic midwater eel species that mostly live in the mesopelagic zone of the open ocean. Moreover, reconstruction of the growth habitats on the resulting tree unequivovcally indicates an origination of the freshwater eels from the midwater of the deep ocean.

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Figure 3. Phylogenetic trees of anguillid eels in the three previous mitochondrial DNA studies of A) Aoyama et al. (2001), B) Minegishi et al. (2005), C) Teng et al. (2009). The thicker lines show the sister group relationships that are the same in all three studies.

2. SPECIES AND DISTRIBUTION The 16 species of freshwater eels are widely distributed in the world (Figure 1) and have unique catadromous life histories with a long larval duration as leptocephali. Catadromy is one of the three distinct forms of diadromy, which is a specialized migratory phenomenon of fishes involving regular, seasonal, mostly obligatory migrations between fresh and marine waters (McDowall 1988). Catadromous fishes such as the freshwater eels spend most of their life cycles in freshwater or estuaries and mature adults migrate to the sea for the purpose of breeding (McDowall 1988). Because of their catadromous life history that uses the ocean for spawning and larval growth, it appears that some parts of the world are not appropriate for anguillid life histories. Most anguillid species are distributed on the west side of the Pacific Ocean, and on both sides of the Indian and North Atlantic oceans (Figure 1,

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Schmidt 1909, 1925; Ege 1939; Tesch 1977). They are absent from the eastern margins of the Pacific Ocean, apparently because both North and South America have cold currents flowing along their Pacific coasts, and anguillids appear to need warm currents for transporting their leptocephali (Tsukamoto et al. 2002). Therefore, their distribution on continents and islands appears to have a close relationship with warm ocean currents derived from the tropical zone that can be used for larval growth by their leptocephali. However, anguillid eels are absent along the east coast of South America, despite the existence of the warm Brazil Current, so the reasons for the absence of eels in the South Atlantic may include various factors. The European eel, A. anguilla, is able to inhabit Europe and the Mediterranean because of the warm eastward flow of the Gulf Stream and North Atlantic drift. The distribution of each species of anguillid eel in the Pacific, Indian and Atlantic oceans is shown in Figure 4, but for simplicity and lack of consistency in the literature about some anguillid common names, we will primarily use scientific names for most of the anguillid species described in this chapter.

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PACIFIC OCEAN Western North Pacific area The freshwater eels of the western North Pacific include the 4 species of A. luzonensis, A. marmorata, A. japonica, and A. bicolor pacifica (Figure 4A). Anguilla luzonensis yellow eels have only found in the Pinacanauan River system, which is a tributary of the Cagayan River on northern Luzon Island of the Philippines (Watanabe et al. 2009a). In the Cagayan River, this species appears to live in small rivers at higher altitudes, while A. marmorata lives in all habitats in this river system and A. bicolor pacifica is typically only found at lower altitudes or in the estuary. The Japanese eel, Anguilla japonica has its natural distribution in the northwestern Pacific Ocean in East Asia. It is recorded from Vietnam, China, Taiwan, Korea, Japan, and the far northern Philippines. A. bicolor pacifica has its natural distribution in the Philippines and northern Indonesia, but some individuals reach China, Taiwan and far southern Japan.

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Figure 4. The distributions of all the species and subspecies of the genus Anguilla including the newly discovered species Anguilla luzonensis. Some species ranges are shown with shaded ovals and some with various types of lines, or large dots for species with limited known ranges. The depictions of some parts of the ranges, such as A. borneensis, A. luzonensis, and A. interioris are likely not completely accurate due to lack of collection data.

The giant mottled eel, Anguilla marmorata, has the widest geographic distribution of the 16 species of the genus Anguilla (Figure 4). The distribution of this remarkable species extends longitudinally from the east coast of Africa to the Marquesas Islands in the central South Pacific, as far north as southern Japan, and as far south as southern Africa (Ege 1939). Recently it was also found at the Palmyra Atoll in the central Pacific (Handler and James, 2006) and even farther to the east in the Galapagos Islands (McCosker et al., 2003). It clearly has several different populations distributed throughout its wide geographic range with morphological and molecular genetic differences (Ishikawa et al. 2004; Minegishi et al. 2008; Watanabe et al. 2008a, 2009b). One spawning area of A. marmorata has been determined to be in the North Equatorial Current (NEC) region of western North Pacific Ocean (Figure 5B) in about the same place as the spawning area of A. japonica (Kuroki et al.

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2009; Tsukamoto et al. 2011). The leptocephali of this species appear to have a widespread presence, but relatively low abundance in this region of the NEC based on several surveys (Miller et al. 2002; Kuroki et al. 2009). The NEC is probably where the North Pacific population of A. marmorata spawns based on its population structure and the geography of currents along the southwestern margin of the North Pacific Ocean. From this spawning area, their leptocephali are transported westward by the NEC, which bifurcates into both northward (Kuroshio Current) and southward (Mindanao Current) flows (Figure 5B). These two current branches can then transport them to all the recruitment areas of the North Pacific population ranging from southern Japan, Taiwan, the Philippines and northern Indonesia (Miller et al. 2002; Kuroki et al. 2006a, 2009). The North Pacific population of this species can also have larvae that reach southwestern China, Vietnam, Cambodia, Thailand and Malaysia in Kalimantan around the South China Sea. A. marmorata also lives in Guam, Palau and Pohnpei, but these eels belong to a different population because they have different morphological and molecular genetic characters (Minegishi et al. 2008; Watanabe et al. 2008a, 2009b).

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Indonesia and New Guinea The freshwater eels in Indonesia and New Guinea include the 7 species of A. celebesensis, A. interioris, A. bengalensis bengalensis, A. marmorata, A. borneensis, A. obscura, A. bicolor pacifica and some A. bicolor bicolor from the Indian Ocean (Figure 4A). Anguilla interioris is similar to A. luzonensis in having one of the most uncertain geographic distributions of anguillid eels. The type specimen of this species was from the upper Purari River in the Central Mandated Territory of New Guinea at an altitude 1,737 m (Whitley 1938). In the revision of Ege (1939), this species and A. celebesensis were partly sympatric in New Guinea, but Aoyama et al. (2000b) suggested that these species were allopatric in Sulawesi Island and New Guinea using mitochondrial DNA sequence analysis. Furthermore, leptocephali of this species also occurred both near Sulawesi Island and off west Sumatra of Indonesia in the Indian Ocean (Kuroki et al. 2006b; Aoyama et al. 2007; Wouthuyzen et al. 2009). Considering this distribution, the A. celebesensis reported by Ege (1939) and Jespersen (1942) might be A. interioris, because both species have very similar morphological characters (Aoyama et al. 2000b). It is likely that this species has two or three different populations corresponding to Sumatra, Sulawesi Island and New Guinea.

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Anguilla celebesensis also has an uncertain geographic distribution because it may have frequently been confused with A. interioris and A. luzonensis. Aoyama et al. (2003) reported this species has two spawning areas that are located in the Celebes Sea and in Tomini Bay of Sulawesi Island. Therefore, A. celebesensis likely has a species range in the region of Sulawesi Island. Anguilla borneensis has the narrowest geographic distribution of the 16 species of the genus Anguilla. This species was previously known from the Mahakam River, Borneo (Ege 1939). Aoyama et al. (2003) reported that the small leptocephali (8.5 and 13.0 mm) of A. borneensis were collected in the Celebes Sea to the east of Borneo. This report strongly suggests that this species spawns in the Celebes Sea and then their larvae recruit to their growth habitat adjacent to the spawning area. Anguilla bicolor pacifica also lives in localities around the Celebes Sea, southeast Borneo, and the Sulawesi Island region. Ege (1939) reported that this species and A. obscura were sympatric in New Guinea. However, these species have similar morphological characters and a close phylogenetic relationship, so the distributions of these species in New Guinea are unclear. Anguilla bicolor bicolor may sometimes get transported into the southern Indonesian Seas where it has been reported (Ege 1939), but it is primarily found in the Indian Ocean region.

Australia and New Zealand The freshwater eels of Australia and New Zealand include the 3 species of A. reinhardtii, A. dieffenbachii, A. australis australis, and A. australis schmidtii (Figure 4B). Anguilla reinhardtii is found in the southwestern Pacific Ocean, mainly along the east coast of Australia, New Caledonia and Lord Howe Island (Ege 1939). Recently it has also been recorded in northern New Zealand freshwater streams (McDowall et al. 1998). Anguilla dieffenbachii is endemic to New Zealand including the Chatham and Auckland Islands, where it lives in all habitats from the sea to the inland waters at higher altitudes (McDowall 1990; Jellyman 2003; Arai et al. 2004). The sympatric A. australis australis schmidtii is typically only found at lower altitudes, but this subspecies lives in New Zealand, New Caledonia and Norfolk Island. Anguilla australis australis occurs in the subtropical to temperate waters of eastern Australia, in Tasmania, Flinders and Vansittart Islands, and Lord Howe Island

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(Ege 1939). Museum records of this species reported by Ege (1939) from Fiji and Tahiti are doubtful (Smith 1999).

South Pacific Area The freshwater eels of the offshore areas of the western South Pacific include A. megastoma, A. marmorata, A. reinhardtii, and A. obscura (Figure 4B). Anguilla megastoma and A. obscura are distributed across mostly overlapping areas of the western and central Pacific Ocean region (Ege 1939; Watanabe et al. 2011). More information about the detailed patterns of occurrences of these 4 species are given and discussed by Marquet and Galzin (1991) and Jellyman (2003). Considering the findings of the three phylogeny studies (Aoyama et al. 2001; Minegishi et al. 2005; Teng et al. 2009) shown in Figure 3, these species likely radiated out into South Pacific from the center of the distribution of the genus to the west in the Indonesia region, in part by speciation from species in that region (Watanabe et al. 2011).

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INDIAN OCEAN The freshwater eels that live in the regions adjacent to the Indian Ocean all appear to be tropical species and include A. interioirs, A. bengalensis bengalensis, A. bengalensis labiata, A. marmorata, A. mossambica, and A. bicolor bicolor (Figure 4C). Anguilla bengalensis has been separated into two subspecies that occur on either the east or the west side of the Indian Ocean. It occurs as A. bengalensis labiata along the African east coast in drainages from South Africa to Kenya (Ege 1939), including the Malawi and Kariba lakes. It is not reported from the Red Sea or the northwestern Indian Ocean. It occurs as A. bengalensis bengalensis from Pakistan along the south Asian coast and in major drainages to Sumatra. The subspecies Anguilla bicolor bicolor is found on both sides of the Indian Ocean including western Sumatra, southern Java, and northwest Australia and along the east coast of Africa up to the Arabian peninsula and along the east coast of India (Ege 1939). Anguilla mossambica is found in waters around the southwestern Indian Ocean. It is frequently recorded from African streams from eastern South Africa and north to Kenya (Ege 1939). It is also recorded from Madagascar, Réunion, Mauritius and the Mascarene Islands.

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ATLA ANTIC OCEA AN

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Theere are only 2 species of frreshwater eelss in the Atlanttic Ocean, whhich are the European eel,, A. anguilla, and a the Ameriican eel, A. roostrata (Figuree 4) t Sargasso Sea (Figure 5A) 5 and theey both spawnn in overlappiing areas of the (McCleave et al. 19887). Anguilla anguilla is natively n foundd adjacent to the northeastern Atlantic Ocean in riveer systems off Europe and its i Mediterrannean nd along Northh Africa. coast an

Figure 5. The spawningg areas (grey ovvals) of temperate eels in 3 subttropical gyres g the major curreents that transpoort their leptoceephalus larvae to t their recruitm ment showing areas. Th he Florida Curreent (FC), Gulf Stream S (GS), North N Atlantic Drift D (NAD), Noorth Equatoriial Current (NEC), Mindanao Current C (MC), Kuroshio K Curreent, South Equatoriial Current (SEC C), and the Eastt Australian Cuurrent (EAC) aree shown.

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However, it has been transported around the world as glass eels for aquaculture and has been introduced for stocking in some areas, where they could even be harvested as migrating silver eels (Miyai et al. 2004). Due to the longevity of the species, those introductions may be present in nature for decades, but their abundance is decreasing in Japan at least (Okamura et al. 2008). A. rostrata occurs from Greenland to the Atlantic coast of Canada and the United States and along the Gulf Coast to the West Indies and Bermuda. They occur throughout the Mississippi drainage and reach as far upstream as Minnesota unless blocked by dams. The southern limit is not well-known, but this species has been recorded from Panama, the Bahamas and most of the West Indies to northern Brazil (Schmidt 1909; Smith 1989). Less than 10% of the anguillid eels collected in Iceland are typically identified as A. rostrata, with the remainder being suggested to be hybrids (Albert et al. 2006).

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3. LIFE HISTORY AND HABITAT USE Because anguillid eels are catadromous fishes they use both freshwater and marine habitats during various parts of their life histories. All species spawn offshore over the deep ocean and not over the continental shelf (Figure 5, 6) so their larvae are born in the open ocean (Tsukamoto et al. 2002). Temperate species all appear to migrate far offshore to spawn in the subtropical gyres of the Atlantic and Pacific oceans (Figure 5), but some tropical species have been found to spawn over deep water in the local regions near their growth habitats (Aoyama et al. 2003, Aoyama 2009). After being born, their larvae use the habitat of the ocean surface layer for feeding and growth (Castonguay and McCleave 1987; Miller 2009), which is the euphotic zone where the majority of primary production occurs in the ocean. They feed and grow while being transported by ocean currents back to their recruitment areas. What they feed on was a mystery for many years, but eventually it has been determined that they appear to feed on particulate organic material, such as marine snow and discarded larvacean houses, which are readily available in the ocean, but not on zooplankton like normal fish larvae (Otake et al. 1993; Mochioka and Iwamizu 1996; Miller 2009; Miyazaki et al. 2011). When they reach their maximum larval sizes, which varies somewhat among different species (Kuroki et al. 2006a; 2008), and approach the continental shelf, they metamorphose into the glass eel stage and migrate towards estuaries and rivers for recruitment (Tsukamoto 1990).

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Once they have reached estuaries or river mouths, most glass eels likely then begin to migrate upstream into freshwater for their yellow eel growth phase. They then proceed upstream into all available habitats including lakes and small streams (Feunteun et al. 2003). A proportion of anguillid eels also remain in the brackish water habitats of estuaries or even in semi-marine habitats without ever entering freshwater during their life history (Tsukamoto et al. 1998; Tsukamoto and Arai 2001; Daverat et al. 2006). Therefore, anguillid eels can seemingly be found in the whole range of continental aquatic habitats (Figure 6). For example, eels have therefore been studied in large estuaries of rivers (Parker 1995; Morrison and Secor 2003), salt marshes or tidal creeks (Bozeman et al. 1985; Ford and Mercer 1986; Lafaille et al. 2000), brackish lakes or lagoons (Jellyman et al. 1996; Arai et al. 2004; Melia et al. 2006), in rivers and streams (Sloane 1984; Barak and Mason 1992; Smogor et al. 1995; Baras et al. 1998; Oliveira and McCleave 2000; Laffaille et al. 2003), in shallow lakes (Carrs et al. 1999; Jellyman and Chisnall 1999), along the margins of deeper lakes (Fischer and Eckmann 1997; Schulze et al. 2004), as well as deeper parts of lakes (Yokouchi et al. 2009). Tracking or tagging studies have shown that yellow eels generally establish a home range in which they remain for extended periods of time where they feed at night and hide during the day (Bozeman et al. 1985; Ford and Mercer 1986; Chisnall and Kalish 1993; Oliveira 1997; Jellyman and Sykes 2003), although in strongly tidal rivers they can move significant distances for feeding using tidal transport (Parker 1995). In recent decades with dams blocking upstream migration in some areas and population levels decreased, many glass eels appear to stay in the brackish water regions of rivers or in estuaries. Historically however, during high recruitment periods, these lower reaches likely had high densities of eels and have been thought to be where many male eels resided (Bozeman et al. 1985; Helfman et al. 1987). Sex determination appears to environmentally determined in anguillid eels, so the high densities and slow growth in the lower reaches of river systems appears to cause male eels to be produced (Krueger and Oliveira 1997; Davey and Jellyman 2005). The lower densities and faster growth further upstream and deep into river systems or lakes tends to produce female eels (Feunteun et al. 2003; Moriarty 2003; Tesch 2003). This situation may be reversed for some species or in some areas in recent years where growth in the estuaries is faster (see Cairns et al. 2009), but this may be an abnormal situation reflecting human impacts on both the freshwater (lower habitat quality for feeding) and estuarine habitats (fewer large predators due to overfishing) in combination with lower eel recruitment.

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Figure 6. Types of habittats used by angguillid eels duriing their yellow w eel growth phaase in relatio on to their offshhore spawning areas a over the deep d ocean. Angguillid eels live in both the brackish waters of the estuariees of rivers and in brackish lakkes or lagoons (light shaading) or in all types of freshw water habitats (ddark shading). After A their silverr eels spaw wn offshore andd their leptocephhalus larvae traansform into glaass eels, they migrate to t the continenttal margins or too islands wheree they recruit annd start their yellow eel e growth phasee.

In recent r years reesearchers havve been using otolith Sr/Ca ratio analysess to study th he habitat use of anguillid eels, because the salinity leevel of the waater has beeen found to be reflectedd in the eel otoliths in the form or Sr concenttration (Kawakkami et al. 1998). This has shown that eeels have a variiety of habittat use patternns after they reeach continenttal waters in teemperate regions (Tsukam moto and Araii 2001; Tzengg et al. 2000, 2002, 2 2003; Jeessop et al. 20002, 2006, 2008; Cairns et e al. 2004; Kootake et al. 20005; Daverat et e al. 2005, 20006; M attention has h focused onn eels in the estuaries e or low wer Kaifu ett al. 2010). Most reaches of rivers wheere it has beenn found that soome eels switcch between tyypes mple many eels that initiallyy enter freshw water as glass eels e of habittats. For exam or youn ng eels eventuaally move back down to thee estuary and remain r there until u they beecome silver eels. e Others may m stay in thhe estuary forr a period beffore entering g freshwater as a young yelloow eels. This type t of variatiion in habitat use may allso be presennt to some degree d in troopical eels based on limiited observaations using these otolithh chemistry techniques t (C Chino and Arai A 2010a,b b). The factorss affecting thesse movementss are not yet cllearly understoood

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and likely depend on the conditions in each river system, but they may be related to the feeding conditions and densities of eels in particular habitats. In northern areas, cold winter temperatures appear to cause eels to leave freshwater and return to the estuary where the water is warmer (Thibault et al. 2007). Understanding the exact patterns of habitat use of anguillid eels within the various habitats they use is somewhat difficult due to their generally cryptic hiding and nocturnal behavior. Determining the habitat preferences of anguillid eels is also complicated by their ability to adapt to many kinds of habitat conditions and their general opportunistic behavior. In estuaries where there are often muddy substrates, eels can create burrows in the mud in which they reside when they are not feeding (Aoyama et al. 2005). In other habitats eels tend to hide in cover created by rocks or other structures. In regions where more than one species live sympatrically, some differences in habitat use have been detected. In New Zealand, the shortfin species, Anguilla australis, appears to be more common in the lower reaches of rivers, and the lonfin species, Anguilla dieffenbachii, is widespread including in upper reaches (McDowall 1990; Jellyman 2003). Various studies have examined habitat preferences or behaviors in these species that show some differences (Glova et al. 1988; Jowett and Richardson 1995; Glova 1999). There may also be differing habitat preferences by the two species in eastern Australia (Silberschneider et al. 2004). In the western South Pacific, field sampling programs have indicated that there is also a zonation pattern in habitat use by several species that can be found on the same islands, such as New Caledonia or the smaller islands of French Polynesia (Marquet and Galzin 1991). In Taiwan, the Japanese eel, Anguilla japonica, seems to prefer the lower reaches of rivers, with the much larger tropical eel, Anguilla marmorata, tending to be found in upper reaches (Shiao et al. 2003). The mechanisms that cause these apparent habitat segregations are not yet known, since anguillid eels so far appear to be feed opportunistically on whatever prey types are available to them. Aquatic insect larvae, crustaceans, various types of worms and other invertebrates are typical prey for all species that have been studied, but small fishes tend to increase in the diet in larger eels or in places where fishes are abundant (Pantulu 1957; Sloane 1984; Ryan 1986; Barak and Mason 1992). They may feed primarily on a few types of organisms such as snails or amphipods in various habitats (Moriarty 1972, 1973) or a single type of fish (Jellyman 1991) if that is what is most available. For many species, such as those in tropical regions, many aspects of the biology and habitat use have not yet been studied much yet. In areas where

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different species are found in the same river system, further research is needed to examine how and why these eels appear to show habitat segregation.

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4. INFLUENCES ON DECLINING RESOURCES Concerns about the health of anguillid eel populations worldwide have increased in recent decades because of declines in recruitment that have occurred in some areas in the last 30 years (Haro et al. 2000; Dekker et al. 2003). There is no clear explanation for why northern temperate anguillids began to show declines starting after the late 1970’s, but various possible influences have been discussed in the literature. Overfishing, habitat loss, pollutants, parasite introductions, and virus infections are factors related to human activities that could negatively affect eel species (Robinet and Feunteun 2002; Kirk 2003; van Ginneken et al. 2004; Palstra et al. 2007; Belpaire and Goemans 2007; Jakob et al. 2009a,b). Implementation of dams along the rivers of eastern North America for example, has reduced the amount of effective habitat for these species greatly (Haro et al. 2000), and much of the river habitat that is now left available for recruitment and safe outmigration of the adults could have been impacted by development and pollution in urbanized or agricultural areas. Fishing pressure on the recruiting glass eel stage also increased in recent decades as a result of the export trade for aquaculture in Asia (Tsukamoto et al. 2009), although this is now being restricted in Europe. Contaminants accumulating in their bodies during the yellow eel stage (Robinet and Feunteun 2002; Belpaire and Goemans 2007; Geeraerts and Belpaire 2010) could also affect the silver eels during their migration as fat reserves are used or they might affect the viability of the eggs or sperm during spawning. The swim bladder parasite, Anguillicola crassus, was introduced into Europe (Kirk 2003) where it can infect eels in freshwater, but not in saline habitats (Jacob et al. 2009a). Because these parasites affect the functioning of the swim bladder that is important for migration through the ocean, they likely impair the migratory ability of silver eels (Palstra et al. 2007). Virus infections of the European eel (van Ginneken et al. 2004; Jacob et al. 2009b) may also impair their migration ability (van Ginneken et al. 2005a). Declines of northern temperate anguillids also have been hypothesized to be related at least in part to changes that occur in the ocean due to regime shifts in the ocean atmosphere system of the earth (Castonguay et al. 1994; Knights 2003; Miller et al. 2009). Changes in spawning location of silver eels

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or alteration of currents that transport their larvae could affect recruitment by preventing successful larval migration back to their recruitment areas (Kimura et al. 2001; Kimura and Tsukamoto, 2006; Friedland et al. 2007; Zenimoto et al. 2009). It is also possible that changes in the productivity of the ocean surface layer could affect larval survival by reducing the feeding success of leptocephali because several recent studies have found correlations between recruitment and productivity-related factors (Knights 2003; Friedland et al. 2007; Bonhommeau et al. 2008a,b). Correlations also have been found between the North Atlantic Oscillation index and recruitment of A. anguilla to the Netherlands (Knights 2003; Friedland et al. 2007) or other parts of Europe (Kettle et al. 2008; Durif et al. 2011). The North Atlantic Oscillation appears to be related to a variety of changes in the North Atlantic, so an effect on productivity or community structure may be the mechanism behind these correlations, which then results in reduced feeding success of leptocephali. Correlations between sea surface temperature or productivity fluctuations and recruitment in both of the northern hemisphere subtropical gyres (Bonhommeau et al. 2008a,b) suggest this may be possible. Increasing ocean temperatures tend to reduce productivity, so sea surface temperature increases in the global ocean (e.g. Levitus et al. 2000) have the potential to reduce productivity, which could affect the feeding success of leptocephali. In the North Pacific however, El Niño events or other ocean-atmosphere interactions have the potential to affect the spawning location or larval transport of the Japanese eel, which could reduce recruitment success. This species appears to spawn to the south of a salinity front (Tsukamoto 1992; Tsukamoto et al. 2011), but the location of the salinity front can move southward during some years (Kimura et al. 2001), which causes spawning to shift to the south (Kimura and Tsukamoto 2006). This could be a problem because the westward flowing North Equatorial Current in which the Japanese eel spawns bifurcates into both northward (towards its recruitment areas in East Asia) and southward (away from its recruitment areas) flows (Figure 5B). Modeling studies indicate that a southward shift in spawning location can increase the proportion of larvae entering the southward current flow (Kim et al. 2007; Zenimoto et al. 2009) and the chance of a southward shift of the front due to decreased tropical rainfall may be greater during El Niño years (Kimura et al. 2001), but the front appears to be frequently in the south in recent years (Tsukamoto et al. 2011). These types of changes in the ocean possibly reducing recruitment by affecting larval transport or larval feeding success due to lower ocean productivity, may be one type of factor, but the other more anthropogenic-

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related factors affecting the yellow and silver eels listed above may also be important for some species. Thus a combination of all these factors may be responsible for the declines of anguillid eels (Starkie 2003), with some factors being more important for particular species. The European eel seems to be the most heavily affected species and there is speculation that part of this may be related to its long spawning migration, which may be at the outer limit of what is physiologically possible for eels of that size. For example it is possible that if eels don’t accumulate enough fat reserves due to poor habitat quality, or the effects of heavy metals such as cadmium (Pierron et al. 2007), they may not be able to make it to the spawning area (Svedäng and Wickström 1997; Belpaire et al. 2009). Experimental evidence suggests that large healthy eels have enough fat reserves to reach the spawning area (van Ginneken and van den Thillart 2000; van Gineken et al. 2005b), but it may be more questionable for smaller eels at greater distances from the spawning area (Clevestam et al. 2011). Thus if smaller eels and those with parasites or heavy contaminant levels in their bodies have migration problems, then the number of silver eels reaching the spawning area may have steadily declined for the European eel. More information about the factors related to the declines of some species or about the status of others is needed to help to solve these problems.

5. CONSERVATION EFFORTS Historically it seems that little attention was given by fisheries managers to eels and their fisheries in most part of the world, and only recently as recruitment has drastically declined in some regions, has awareness been raised about eel conservation issues. The declines and recent concerns about the European eel is the best example of this situation as overviewed by Feunteun (2002). Early management efforts in Europe included the transportation of glass eels primarily to northern regions of Europe where natural recruitment was low, restrictions on fishing, fishing gear control, imposing size limits or requiring fishing licenses, and facilitating the passage of glass eels over dams (Moriarty and Dekker 1997). More general fisheries regulations such as habitat restoration or establishing freshwater protection areas have been considered also (Feunteun 2002; Cucherousset et al. 2007). After this species continued to show drastic recruitment declines in some areas and was listed in the Appendix II of the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES Red List) there has been an increase in research and management efforts within the European Union

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countries (ICES 2010). The European Commission proposed and implemented a Community Action Plan for the protection and recovery of the European eel (Council Regulation (EC) No 1100/2007), which includes preparation of management plans for eels in each river basin by the member states associated with the river. The objective of the regulation is to reduce anthropogenic mortalities to permit the escapement of at least 40% of the silver eel biomass relative to the best estimate of escapement that would have existed without anthropogenic influences. How each country will deal with this regulation will be seen in the coming years, but will likely include drastic reductions in the amount of fishing pressure on yellow and silver eels, or measures such as trapping and transporting silver eels around dams so they are not harmed by passing through the turbines of the dams. The new regulation also severely restricts all collections of glass eels and only allows glass eels to be collected for restocking in other areas of Europe. The international trade in glass eels has become increasingly global in its influences in recent decades, due in part to more extensive eel aquaculture efforts in China (Tsukamoto et al. 2009; Li et al. 2011). Many European eel glass eels have been sent to Asia to support aquaculture operations, and especially to China in recent decades. Prices for glass eels have also fluctuated greatly among years depending on the recruitment levels of the Japanese eel in East Asia, causing “gold rush” style glass eel harvesting in certain places. However, with the once steady supply of European eel glass eels now reduced by the new regulation in Europe, there will likely be increasing efforts to obtain glass eels of other species where their collection is not yet illegal. This could potentially cause new conservation problems for these other species whose population stability is not known. There is seemingly a wide range of levels of management and conservation efforts for anguillid eels in different parts of the world. Much greater attention has been focused on the European eel (Moriarty and Dekker 1997; Feunteun 2002; Rosell et al. 2005; ICES 2010), but also recently for the American eel in North America, due in part to a drastic decrease in recruitment to the northern limit of their species range at the St. Laurence River (Casselman 2003). The effect of dams on these species and what should be done about them has remained an important issue being considered (e.g. McCleave 2001; McCarthy et al. 2008). Within East Asia there historically have been minimal large-scale management efforts for anguillid eels, so increasing effort and coordination is needed, since recruitment of the Japanese eel continues to be low in some years (Tatsukawa et al. 2003; Tsukamoto et al. 2009). There are primarily two anguillid species in New Zealand where

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fisheries are conducted by indigenous fishers for personal consumption and also export, but marked changes in the population structure have been observed and various management efforts have been undertaken to protect these species in recent years (Beentjes et al. 2006; Boubée et al. 2008). Throughout the rest of the Indo-Pacific, the levels of management probably ranges from regulated fisheries such as in Australia, to minimal, or a complete lack of protection from overharvest, including in critically important places such as Indonesia where many tropical species are present (Miller et al. 2009). Because management and conservation efforts for anguillid eels may be at an early stage of development in some regions where eels are eaten or harvested for export, increased efforts are needed worldwide to help prevent further decreases in these eel populations.

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CONCLUSION Anguillid eels are widely distributed in many parts of the world and they are economically important in some regions where they have been increasingly studied in recent years. The majority of species are very poorly known scientifically in other regions of the world, however. Some problems still exist in their taxonomy and one new species has recently been discovered in the northern Philippines. There are relatively few morphological features that can be used to identify species, so DNA analysis is often needed. Their spawning areas and habitat use patterns are generally known for some species, but many species in the Indo-Pacific have not been studied yet. Anguillid eels all spawn over deep water in the ocean, with their larvae feeding and growing in the ocean surface layer, so they may be vulnerable to changes in ocean productivity or altered larval transport patterns. During their yellow eel growth phase in freshwater and brackish habitats they seem to occupy all types of different aquatic habitats and so they may be vulnerable to a variety of anthropogenic factors including habitat loss, overfishing, pollutants, and parasite introductions or infectious agents. Their catadromous life histories are very different than other fisheries species making it difficult to know what is causing the population declines of various species in recent decades. This makes developing management plans complicated. There is increasing effort to conserve these unusual fishes in some countries, but greater conservation activities are likely needed in many other regions of the world.

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REFERENCES Aida, K., Tsukamoto, K., & Yamauchi, K. (Eds.). (2003). Eel biology. Tokyo, Japan: Springer Verlag. Albert, V., Jónsson, B., & Bernatchez, L. (2006). Natural hybrids in Atlantic eels (Anguilla anguilla, A. rostrata): evidence for successful reproduction and fluctuating abundance in space and time. Molecular Ecology, 15, 1903–1916. Aoyama, J. (2009). Life history and evolution of Migration in Catadromous eels (Genus Anguilla). Aqua-BioScienc Monographs, 2, 1–42. Aoyama, J., & Miller, M. J. (2003). The silver eel stage. In K. Aida, K. Tsukamoto, & K. Yamauchi (Eds.), Eel Biology: (pp.107–117). Tokyo, Japan: Springer Verlag. Aoyama, J., Kobayashi, T., & Tsukamoto, K. (1996). Phylogeny of eels suggested by mitochondrial DNA sequences. Nippon Suisan Gakaishi, 68, 312–370. (in Japanese with English abstract). Aoyama, J., Mochioka, N., Otake, T., Ishikawa, S., Kawakami, Y., Castle, P. H. J., Nishida, M., & Tsukamoto, K. (1999). Distribution and dispersal of anguillid leptocephali in the western Pacific Ocean revealed by molecular analysis. Marine Ecology Progress Series, 188, 193–200. Aoyama, J., Watanabe, S., Nishida, M., & Tsukamoto, K. (2000a). Discrimination of catadromous eel species, genus Anguilla, using PCRRFLP analysis of the mitochondrial 16SrRNA domain. Transactions of the American Fisheries Society, 129, 873–878. Aoyama, J., Watanabe, S., Ishikawa, S., Nishida, M., & Tsukamoto, K. (2000b). Are morphological characters distinctive enough to discriminate between two species of freshwater eels, Anguilla celebesensis and A. interioris? Ichthyological Research, 47, 157–162. Aoyama, J., Nishida, M., & Tsukamoto, K. (2001). Molecular phylogeny and evolution of the Freshwater eel, Genus Anguilla. Molecular Phylogenetics and Evolution, 20, 450-459. Aoyama, J., Wouthuyzen, S., Miller, M. J., Inagaki, T., & Tsukamoto, K. (2003). Short-distance spawning migration of tropical freshwater eels. Biological Bulletin, 204, 104–108. Aoyama, J., Shinoda, A., Sasai, S., Miller, M. J., & Tsukamoto, K. (2005). First observations of the burrows of the Japanese eel, Anguilla japonica. Journal of Fish Biology, 67, 1534–1543. Aoyama, J., Wouthuyzen, S., Miller, M. J., Minegishi, Y., Minagawa, G., Kuroki, M., Suharti, S. R., Kawakami, T., Sumardiharga, K. O., &

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Cairns, D. K., Shiao, J. C., Iizuka, Y., Tzeng, W. N., & MacPherson, C. D. (2004). Movement patterns of American eels in an impounded watercourse, as indicated by otolith microchemistry. North American Journal of Fisheries Management, 24, 452–458. Cairns, D. K., Secor, D. A., Morrison, W. E., & Hallett, J. A. (2009). Salinitylinked growth in anguillid eels and the paradox of temperate-zone catadromy. Journal of Fish Biology, 74, 2094–2114. Carss, D. N., Elston, D. A., Nelson, K. C., & Kruuk, H. (1999). Spatial and temporal trends in unexploited yellow eel stocks in two shallow lakes and associated streams. Journal of Fish Biology, 55, 636–654. Casselman, J. M. (2003). Dynamics of resources of the American eel, Anguilla rostrata: declining abundance in the 1990s. In K. Aida, K. Tsukamoto, & K. Yamauchi (Eds.), Eel Biology: (pp. 255–274). Tokyo, Japan: Springer Verlag. Castle, P. H. J., & Williamson, G. R. (1974). On the validity of the freshwater eel species Anguilla ancestralis Ege from Celebes, Copeia, 1974, 569– 570. Castonguay, M., & McCleave, J. D. (1987). Vertical distributions, diel and ontogenetic vertical migrations and net avoidance of leptocephali of Anguilla and other common species in the Sargasso Sea. Journal of Plankton Research, 9, 195–214. Castonguay, M., Hodson, P. V., Moriarty, C., Drinkwater, K. F., & Jessop, B. M. (1994). Is there a role of ocean environment in American and European eel decline? Fisheries Oceanography, 3, 197-203. Chino, N., & Arai, T. (2010a). Migratory history of the giant mottled eel (Anguilla marmorata) in the Bonin Islands of Japan. Ecology of Freshwater Fish, 19, 19–25. Chino, N., & Arai, T. (2010b). Occurrence of marine resident tropical eel Anguilla bicolor bicolor in Indonesia. Marine Biology, 157, 1075–1081. Chisnall, B. L., & Kalish, J. M. (1993). Age validation and movement of freshwater eels (Anguilla dieffenbachii and A. australis) in a New Zealand pastoral stream. New Zealand Journal of Marine & Freshwater Research, 27, 333–338. Chu, Y. T. (1984) Fishes of Fujian Province. Part 1. Fujian, China: Fujian Science and Technology Press. (In Chinese). CITES. (2006). Inclusion of Anguilla anguilla in Appendix II in Accordance with Article II, Paragraph 2 (A). Proposal for CITES Consultation Process. Twenty-second meeting of the Animals Committee Lima (Peru). AC22 Inf. 7. 38 pp.

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from laboratory experiments. Environmental Biology of Fishes, 71, 395– 402. Silfvergrip, A. M. C. (2009). CITES Identification Guide to Freshwater Eels (Anguillidae), with Focus on the. European Eel Anguilla anguilla. Stockholm, Sweden: Swedish Environmental Protection Agency. Sloane, R. D. (1984). Distribution and abundance of freshwater eels (Anguilla spp.) in Tasmania. Australian Journal of Marine and Freshwater Research, 35, 463–470. Smith, D. G. (1989). Introduction to leptocephali. In E. B. Böhlke, (Ed.), Fishes of the Western North Atlantic, Part 9, Volume 2 (pp. 657–668). New Haven, U. S. A.: Sears Foundation for Marine Research. Smith, D. G. (1999). Anguillidae: Freshwater eels. In K. E. Carpenter, & V. H. Niem, (Eds.), FAO species identification guide for fishery puroposes: The living marine resources of the western central Pacific, volume 3 (pp.1630–1636). Rome: Food and agriculture organization of the united nations. Smogor R. A., Angermeier, P. L., & Gaylord, C. K. (1995). Distribution and abundance of American eels in Virginia streams: tests of null models across spatial scales. Transactions of the American Fisheries Society, 124, 789–803. Starkie, A. (2003). Management issues relating to the European eel, Anguilla anguilla. Fisheries Management and Ecology, 10, 361–364. Svedäng, H., & Wickström, H. (1997). Low fat contents in female silver eels: indications of insufficient energetic stores for migration and gonadal development. Journal of Fish Biology, 50, 475–486. Tabeta, O. (1994). Eel research in the world. Kaiyo monthly, 287, 270–273. (in Japanese). Tagliavini, J., Gandolfi, G., Cau, A., Salvadori, S., Deiana, A. M., & Gandolfi, G. (1995). Mitochondrial DNA variability in Anguilla anguilla and phylogenetical relationships with congeneric species. Bollettino di Zoologia. 62: 147–151. Tagliavini, J., Gandolfi, G., Deiana, A. M., & Salvadori, S. (1996). Phylogenetic relationship among two Atlantic and three Indo-Pacific Anguilla species (Osteichtyes, Anguillidae). Italian Journal of Zoology, 63, 271–276. Tatsukawa, T. (2003). Eel resources in East Asia. In K. Aida, K. Tsukamoto, & K. Yamauchi (Eds.), Eel Biology: (pp. 293–298). Tokyo, Japan: Springer Verlag.

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Teng, H.-Y., Lin, Y.-S., & Tzeng, C.-S. (2009). A new Anguilla species and a reanalysis of the phylogeny of freshwater eels. Zoological Studies, 46, 808-822. Tesch, F. W. (1977). The eel, Biology and management of anguillid eels. London, U. K.: Chapman & Hall. Tesch, F. W. (2003). The eel. Oxford, U. K.: Blackwell Publishing. Thibault, I., Dodson, J. J., Caron, F., Tzeng, W.-N., Iizuka, Y., & Shiao, J.-C. (2007). Facultative catadromy in American eels: testing the conditional strategy hypothesis. Marine Ecology Progress Series, 344, 219–229. Tsukamoto, K. (1990). Recruitment mechanism of the Japanese eel, Anguilla japonica, to the Japanese coast. Journal of Fish Biology, 36, 659–671. Tsukamoto, K. (1992). Discovery of the spawning area for the Japanese eel. Nature, 356, 789–791. Tsukamoto, K. (2009). Oceanic migration and spawning of anguillid eels. Journal of Fish Biology, 74, 1833–1852. Tsukamoto, K., & Arai, T. (2001). Facultative catadromy of the eel Anguilla japonica between freshwater and seawater habitats. Marine Ecology Progress Series, 220, 265–276. Tsukamoto, K., Nakai, I., & Tesch, W. V. (1998). Do all freshwater eels migrate? Nature, 396, 635–636. Tsukamoto, K., Aoyama, J., & Miller, M. J. (2002). Migration, speciation and the evolution of diadromy in anguillid eels. Canadian Journal Fisheries and Aquatic Science, 59, 1989–1998. Tsukamoto, K., Aoyama, J., & Miller, M. J. (2009). The present status of the Japanese eel: resources and recent research. American Fisheries Society Symposium, 58, 21–35. Tsukamoto, K., Chow, S., Otake, T., Kurogi, H., Mochioka, N., Miller, M. J., Aoyama, J., Kimura, S., Watanabe, S., Yoshinaga, T., Shinoda, A., Kuroki, M., Oya, M., Watanabe, T., Hata, K., Ijiri, S., Kazeto, Y., Nomura, K., & Tanaka, H. (2011). Oceanic spawning ecology of freshwater eels in the western North Pacific. Nature Communication, DOI: 10.1038/ncomms1174. Tzeng, W. N., Wang, C. H., Wickström, H., & Reizenstein M. (2000). Occurrence of the semi-catadromous European eel Anguilla anguilla in the Baltic Sea. Marine Biology, 137, 93–98. Tzeng, W. N., Shiao, J. C., & Iizuka, Y. (2002). Use of otolith Sr:Ca ratios to study the riverine migratory behaviors of Japanese eel Anguilla japonica. Marine Ecology Progress Series, 245, 213–221.

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Tzeng, W. N., Iizuka, Y., Shiao, J. C., Yamada, Y., & Oka, H. P. (2003). Identification and growth rates comparison of divergent migratory contingents of Japanese eel (Anguilla japonica). Aquaculture, 216, 77– 86. Watanabe, S. (2003). Taxonomy of the freshwater eels, genus Anguilla Schrank, 1798. In K. Aida, K. Tsukamoto, & K. Yamauchi (Eds.), Eel Biology: (pp. 3–18). Tokyo, Japan: Springer Verlag. Watanabe, S., Aoyama, J., & Tsukamoto, K. (2004). Reexamination of Ege's (1939) use of taxonomic characters of the genus Anguilla. Bulletin of Marine Science. 74, 337–351. Watanabe, S., Aoyama, J., Nishida, M., & Tsukamoto, K. (2005). A molecular genetic evaluation of the taxonomy of eels of the genus Anguilla (Pisces: Anguilliformes). Bulletin of Marine Science, 76, 675–690. Watanabe, S., Aoyama, J., & Tsukamoto, K. (2006). Reconfirmation of morphological differences between A. australis australis Richardson and A. australis schmidtii Phillipps. New Zealand Journal of Marine and Freshwater Research, 40, 325–331. Watanabe, S., Aoyama, J., Miller, M. J., Ishikawa, S., Feunteun, E., & Tsukamoto, K. (2008a). Evidence of population structure in the giant mottled eel, Anguilla marmorata, using total number of vertebrae. Copeia; 2008, 680–688. Watanabe, S., Aoyama, J., & Tsukamoto, K. (2008b). The use of morphological and molecular genetic variations to evaluate subspecies issues in the genus Anguilla. Coastal Marine Science, 32, 19–29. Watanabe, S., Aoyama, J., & Tsukamoto, K. (2009a). A new species of freshwater eel, Anguilla luzonensis (Teleostei: Anguillidae) from Luzon Island of the Philippines. Fishries Science, 75, 387–392. Watanabe, S., Miller, M. J., Aoyama, J., & Tsukamoto, K. (2009b). Morphological and meristic evaluation of the population structure of Anguilla marmorata across its range. Journal of Fish Biology, 74, 2069– 2093. Watanabe, S., Miller, M. J., Aoyama, J., & Tsukamoto, K. (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. Environmental Biology of Fishes, 91, 353–360. Whitley, G. P. (1938). Descriptions of some New Guinea fishes. Records of the Australian Museum, 20, 223–233.

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Wouthuyzen, S., Aoyama, J., Sugeha, H. Y., Miller, M. J., Kuroki, M., Minegishi, Y., Suharti, S., & Tsukamoto, K. (2009). Seasonality of spawning by tropical anguillid eels around Sulawesi Island, Indonesia. Naturwissenshaften, 96, 153–158. Yokouchi, K., Aoyama, J., Miller, M. J., Tsukamoto, K., & McCarthy, T. K. (2009). Depth distribution and biological characteristics of the European eel (Anguilla anguilla) in Lough Ennell, Ireland. Journal of Fish Biology, 74, 857–871. Zenimoto, K., Kitagawa, T., Miyazaki, S., Sasai, Y., Sasaki, H., & Kimura, S. (2009). The effects of seasonal and interannual variability of oceanic structure in the western Pacific North Equatorial Current on larval transport of the Japanese eel Anguilla japonica. Journal of Fish Biology, 74, 1878–1890.

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Chapter 2

ECOLOGICAL RISK FOR ORGANOTIN ACCUMULATION IN RELATION TO LIFE HISTORY IN THE ANGUILLID EELS Takaomi Arai∗

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Department of Biology, Faculty of Science, Universiti Putra Malaysia, UPM Serdang, Selangor, Malaysia

ABSTRACT A number of recent studies found that anguillid eels have never migrated into fresh water, spending their entire life history in the ocean. Furthermore, those studies found an intermediate type between marine and freshwater residents, which appear to frequently move between different environments during their growth phase. The discovery of marine and brackish water residents in the eels suggests that anguillid eels do not all have to be catadromous, and it calls into question the generalized classification of diadromous fishes. It suggests that the ecological risks caused by various contaminants differ among their life histories in a species. However, there is little information available on the ecological risks for contaminants for anguillid eels as well as other diadromous fish. In this chapter, the ecological risks for organotin compounds (OTs) such as tributyltin (TBT) and triphenyltin (TPT) compounds, and their breakdown products, were evaluated in the eels ∗

E-mail: [email protected].

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Takaomi Arai having sea, estuarine and river life histories. There were generally three different life history patterns, which were categorized ‘marine resident’ (spent most of their life in the sea and did not enter freshwater), ‘estuarine resident’ (inhabited estuaries or switched between different habitats), and ‘freshwater resident’ (entered and remained in freshwater river habitats after arrival in the estuary) in the species. There were generally no significant correlations between TBT and TPT accumulation and various biological characteristics such as total length, body weight, age and sex in A. japonica, A. marmorata and A. bicolor pacifica. The concentrations of TBT and TPT in silver eels (mature eels) were significantly higher than those in yellow eels (immature eels), and the percentages of TBT and TPT were also higher in silver eels than in yellow eels. A positive correlation was found between TBT concentration and the gonadosomatic index (GSI). It is thus considered that silver eels have a higher ecological risk of contamination by TBT than yellow eels. TBT and TPT concentrations in marine resident eels were significantly higher than those in freshwater resident eels. In contrast, no significant differences were observed in TBT and TPT concentrations in estuarine resident eels compared to marine and freshwater resident eels. These results suggest that marine resident eels have a higher ecological risk of OT contamination than freshwater resident eels during their life history, and the risk of OTs in estuarine resident eels is considered to be intermediate between that of marine and freshwater resident eels. Positive linear relationships were found between otolith strontium:calcium ratios and the concentrations of TBT and TPT. Therefore, these results suggest that the ecological risk of OTs increase, as the sea residence period in the eel become longer. Even at the same maturation stage, TBT and TPT concentrations in marine resident eels were significantly higher than those in freshwater resident eels. Thus, it is clear that migratory type is a more important factor for OT accumulation than maturation stage. The risks involved in the exposure of marine and estuarine residenct eels to TBT and TPT may in turn influence freshwater resident eels, resulting in a disturbance in the overall population maintenance of the anguillid eels.

INTRODUCTION Organotins (OTs) are used in a variety of consumer and industrial products such as marine antifouling paints, agricultural pesticides, preservatives, and plastic stabilizers. In particular, butyltins (BTs) and phenyltins (PTs) have been extensively used in boat paints because of their excellent and long-lasting antifouling properties. TBT and TPT are responsible for many deleterious effects on non-target aquatic life (Fent and Meier 1994,

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Ohji et al. 2006a, b, Grzyb et al. 2003). In spite of regulation of their use in antifouling paints, high concentrations of TBT and TPT are still detected in the aquatic ecosystem (Arai and Harino 2009). In fish, OTs accumulate various kinds of fish such as marine, freshwater, diadromous and even in deep sea fishes (Arai 2009). Recently, it was reported that TBT accumulation in diadromous fish such as salmon and freshwater eel was significantly different between their life histories in a species (Ohji et al. 2006a, b, 2009, 2010, 2011). TBT concentrations in sea-run masu salmon, brown trout and whitespotted charr were significantly higher than those in freshwater-residents, and the proportions of TBT in the total butyltin in these anadromous salmonid fishes were significantly higher than those in their freshwater-resident types (Ohji et al. 2006a, 2010, 2011). These results suggest that the anadromous Oncorhynchus masou, Salmo trutta and Salvelinus leucomaenis had a higher ecological risk than their freshwater-resident ones to TBT exposure during their life histories, even though both anadromous and freshwater resident belong to the same species. Therefore, the differences in TBT accumulation, as well as TPT, between migratory types in the catadromous eel could also be considered similar to salmonid fish. The freshwater eels of the genus Anguilla are widely distributed throughout the world. The are found in most tropical, subtropical and temperate areas except for the South Atlantic and the west coasts of North and South America (Ege 1939). The freshwater eels are also highly valued cultured species because of their high market price, high yield and high survival rate. Among Anguilla species, the Japanese eel Anguilla japonica and the European eel Anguilla anguilla are the most important in East Asia (mainly Japan, Taiwan, and China) and Europe (mainly Italy and the Netherlands) (Liao 2002). Anguillid eel species display a remarkable similarity in their life history traits. The eels all spawn in deep oceanic waters. They perform a spectacular migration between its freshwater and estuarine habitats, and its offshore spawning area. These larvae (leptocephali) drift from the spawning area toward the coastal waters, and then metamorphose into juveniles (glass eels) and begin their inshore migration. The glass eels start to become pigmented elvers when they enter estuaries, and in general, large numbers of elvers typically migrate up freshwater streams and rivers or enter lakes. After yellow eel (immature) growth phase, they metamorphose into the silver eel (mature) stage, characterized by mature gonads and enlarged eyes, and move back downstream to the ocean to begin the journey to the spawning area. Recently, the migratory history of several species of anguillid eels has been studied using microchemical analytical techniques to determine the ratios

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of strontium to calcium (Sr:Ca) in the otoliths of fishes. The Sr:Ca ratio in the otoliths of fishes such as anguillid eels differs depending on the amount of time they spend in freshwater vs. seawater (Arai et al. 2004, 2006, Chino and Arai 2010a, b, c).Thus, the Sr:Ca ratios of otoliths may enable us to determine whether or not individual eels actually move between different habitats with differing salinity regimes. Chino and Arai (2010b, c) used these Sr:Ca ratios to classify the migratory histories of anguillid eels into three migratory types: (1) ‘marine resident’ (spent most of their life in the sea and did not enter freshwater), (2) ‘estuarine resident’ (inhabited estuaries or switched between different habitats), and (3) ‘freshwater resident’ (entered and remained in freshwater river habitats after arrival in the estuary). Therefore, it could be considered that there were different ecological risks for pollutants including OTs among the three migration types of the species. Such information is important to understand the aquatic contamination levels and bioaccumulation in the eels to conserve their population in ecosystem. In this chapter, differences in the accumulation patterns of butyltin compounds (BTs) including TBT and its derivatives, dibutyltin (DBT) and monobutyltin (MBT), and phenyltin compounds (PTs) including TPT and its derivatives, diphenyltin (DPT) and monophenyltin (MPT), in the different migratory types of a catadromous eel of the genus Anguilla were discussed. The environmental histories of these eels were reconstructed by means of the ontogenic changes in otolith Sr:Ca ratios along the life history transect emphasized previously for determining the details of eel migration. This chapter may provide valuable clues for understanding the ecological risk of OTs and its variations according to life history and migration in catadromous fish.

MATERIALS AND METHODS This chapter synthesizes information following publications regarding OCs accumulation in the freshwater eels: Ohji et al. (2006a, 2009) in Anguilla japonica from Japan and Arai et al. (2011) in A. marmorata and A. bicolor pacifica from Vietnam.

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LIFE HISTORY ANALYSIS

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In all studies, sagittal otoliths were extracted, and the otoliths were embedded in epoxy resin (Struers, Epofix). These otoliths were then ground to expose the core along the anterior-posterior direction in the frontal plane, using a grinding machine equipped with a diamond cup-wheel (Struers, Discoplan-TS), and polished further with oxide polishing suspension on an automated polishing wheel (Struers, PdM-Force-20). Finally, they were cleaned using distilled water and ethanol, and dried at 50ºC in an oven prior to examination. The ground surfaces of the otoliths were examined at 200 x with a light microscope, and photographs were taken to measure the “radius” of the elver mark (the distance from the otolith core to the elver check) (Figure 2). For otolith microchemical analyses, all otoliths were Pt-Pd coated by a high vacuum evaporator.

Figure 1. Butyltin (left) and phenyltin (right) concentrations (A) and compositions (B) in the livers of yellow and silver eels in Japanese eel Anguilla japonica (Ohji et al. 2009).

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Figure 2. Relationship between total butyltin (left) and total phenyltin (right) concentrations in the livers and otolith Sr:Ca ratio of Anguilla marmorata and A. bicolor pacifica from Vietnam (A; Arai et al. 2011) and relationship between tributyltin (left) and triphenyltin (right) concentrations in the livers and otolith Sr:Ca ratios in the Japanese eel Anguilla japonica (B; Ohji et al. 2006a). The higher Sr:Ca ratios indicate the eel depends sea water environment.

Otoliths from all specimens were used for life-history transect analyses of Sr and Ca concentrations, which were measured along a line down the longest axis of each otolith from the core to the edge (Figure 2) using a wavelength dispersive X-ray electron microprobe (JEOL JXA-8900R). We described the detail of the analytical procedure in Chino and Arai (2011). We calculated the average Sr:Ca ratios for the values outside the elver mark. According to the criteria of Tsukamoto and Arai (2001), Anguilla japonica specimens were categorized into “marine resident” (Sr:Ca ≥ 6.0 x 103 ), “estuarine resident” (2.5 x 10-3 ≤ Sr:Ca < 6.0 x 10-3) and “freshwater resident” (Sr:Ca < 2.5 x 10-3). In other eel species, specimens were categorized into “marine resident” (Sr:Ca ≥ 6.0 x 10-3), “estuarine resident” (2.0 x 10-3 ≤ Sr:Ca < 6.0 x 10-3) and “freshwater resident” (Sr:Ca < 2.0 x 10-3) following Chino and Arai (2010b, c). Following the electron microprobe analysis, the otoliths were repolished to remove the coating, etched with 1% HCl and thereafter stained with 1 %

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toluidine blue. The age of the specimens was determined by counting the number of blue-stained transparent zones following the method of Chino and Arai (2009).

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Chemical Analysis of Organotin Compounds One gram of homogenated liver of each eel was placed in a centrifuge tube and 100 µl of mixed acetone solution including 1 µg ml-1 of each tributyltin monochloride (TBTCl)-d27, dibutyltin dichloride (DBTCl)-d18, monobutyltin trichloride (MBTCl)-d9, triphenyltin monochloride (TPTCl)-d15, diphenyltin dichloride (DPTCl)-d10, and monophenyltin trichloride (MPTCl)d5 was added to the centrifuge tube as a surrogate standard. The mixture was extracted with 25 ml of 1 M HCl-methanol/ethyl acetate (1/1) by shaking for 10 min. After centrifugation for 10 min, the residue was extracted and centrifuged again in the same way. The combined supernatants and 70 ml of saturated NaCl solution were transferred to a separatory funnel. The analytes were extracted twice using 30 ml of ethyl acetate/hexane (3/2) solution. A fifty milliliter of hexane was mixed with the combined organic layers and the mixture was allowed to stand for 20 min. After removal of the aqueous layer, the organic layer was dried with anhydrous Na2SO4 and was concentrated up to trace level by a rotary evaporator, and further concentrated by means of a nitrogen purge. The analytes were diluted with 5 ml of acetic acid-sodium acetate buffer (pH 5.0) and ethylated using 1 ml of 5% NaBEt4. The lipids were saponificated with 10 ml of 1 M KOH–ethanol solution by shaking for 1 h. Forty ml of distilled water and 40 ml of hexane were added to the solution, and ethylated OTs in the mixed sample solution were extracted to an organic layer by shaking for 10 min. The ethylated OT residue in an aqueous layer was extracted again by shaking for 10 min with 40 ml of hexane. The combined organic layers were dried with anhydrous Na2SO4. After being concentrated up to 1 ml by a rotary evaporator and nitrogen gas, the solution was cleaned using a florisil Sep-Pak column (Waters Associates Inc.) The analytes were eluted with 5% diethyl ether/hexane, and TeBT-d36 and TePT-d20 were then added as an internal standard. The final solution was then concentrated up to 0.5 ml. A Hewlett-Packard 6890 series gas chromatography equipped with a mass spectrometry (5973 N) was used for analysis of OTs with selected ion monitoring. The separation was carried out in a capillary column coated with 5% phenyl methyl silicone (JandW Scientific Inc., 30 m length x 0.25 mm i.d., 0.25 µm film thickness). The column temperature was held at 60˚C for the first

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2 min, then increased to 130˚C at 20˚C/min, to 210˚C at 10˚C/min, to 260˚C at 5˚C/min, and to 300˚C at 10˚C/min. Finally, the column temperature was maintained at 300˚C for 2 min. The interface temperature, ion source temperature and ion energy were 280˚C, 230˚C and 70 eV, respectively. Selected ion monitoring was performed under this program. Splitless injection (1 µl) of the sample was employed. The concentrations of OTs in this study are expressed as Sn4+ on a wet weight basis for the biological samples.

RESULTS Environmental Habitat Use of Eels

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The Sr:Ca ratios in the transects along the radius of each otolith showed the same common features in all specimens, but there were generally three different patterns outside the otolith core (Figure 3 in Chapter X in this book; Chino and Arai submitted). The high Sr:Ca ratios in the central core region, inside the elver mark, corresponded to the leptocephalus and early glass eel stages during their oceanic life (Arai et al. 1997).

Taken from Chapter title “Habitat Use And Migration In The Japanese Eel Anguilla Japonica And Introduced Anguillid Eels In Japanese Natural Waters” by (Chino & Arai). Figure 3. Fluctuation of otolithSr:Ca ratios along a transect line from the core to the edge of the otolith with reference to growth stages and habitat uses in the life history of Anguilla japonica.

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Taken from Chapter title “Habitat Use And Migration In The Japanese Eel Anguilla Japonica And Introduced Anguillid Eels In Japanese Natural Waters” by (Chino and Arai). Figure 4. Plots of the otolithSr:Ca ratios along transect lines from the core to the edge of the otolith for three representative specimens of Anguilla japonica. Migratory patterns showedeither marine resident (a), estuarine resident (b) or freshwater resident(c). The solid line in each panel indicates marine water life period (≥ 6.0 x 10-3 in Sr:Ca ratios), and the dotted line in each panel indicates fresh water life period (< 2.5 x 10-3 in Sr:Ca ratios).

The life history transects of Sr:Ca ratios outside the elver mark in the otolith showed three distinctive patterns: (1) constantly living in freshwater (freshwater resident); (2) constantly living in brackish water with no freshwater life (estuarine resident); and (3) constantly living in sea water with no freshwater life (marine resident) (Figure 4 in Chapter X in this book; Chino

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and Arai 2012). The wide range of otolith Sr:Ca ratios indicated that the habitat use of Anguilla japonica, A. marmorata and A. bicolor pacifica were variable after their recruitment to the coastal waters as glass eels.

Relationship between Organotin Accumulation and Each Biological Characteristic

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There were generally no significant correlations between TBT and TPT accumulation and various biological characteristics such as total length (TL), body weight (BW), age and sex in Anguilla japonica, A. marmorata and A. bicolor pacifica. The concentrations of TBT and TPT in silver eels (mature eels) were significantly higher than those in yellow eels (immature eels), and the percentages of TBT and TPT were also higher in silver eels than in yellow eels in A. japonica (Figure 1). A positive correlation was found between TBT concentration and the gonadosomatic index (GSI). It is thus considered that silver eels have a higher risk of contamination by TBT than yellow eels.

Bioaccumulation of Organotin in Eels with Different Habitat Use TBT and TPT concentrations in marine resident eels were significantly higher than those in river eels. In contrast, no significant differences were observed in TBT and TPT concentrations in estuarine resident eels compared to marine and freshwater resident eels. These results suggest that marine residents have a higher ecological risk of OTs contamination than freshwater residents during their life history, and the risk of OTs in estuarine residents is considered to be intermediate between that of sea and river eels. Positive linear relationships were found between Sr:Ca ratios and the concentrations of TBT and TPT (Figure 2). Therefore, these results suggest that the ecological risk of OTs increase, as the sea residence period in the eel become longer. Even at the same maturation stage, TBT and TPT concentrations in sea eels were significantly higher than those in river eels. Thus, it is clear that migratory type is a more important factor for OT accumulation than maturation stage.

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DISCUSSION

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Relationship between Organotin Accumulation and Each Biological Characteristic TBT and TPT accumulations in three anguillid eels such as Anguilla japonica, A. marmorata and A. bicolor pacifica did not generally depend on TL, BW and age (Ohji et al. 2006a, 2009, Arai et al. 2011). It is reported that concentrations of TBT in liver were independent of TL and BW in European eel A. anguilla collected in Thames Estuary and the Weston Canal in United Kingdom (Harino et al. 2002). It is also reported that TBT concentration and fish length were no correlation in Japanese sea perch Lateolabrax japonicus, white crocker Pennehia argentatu and yellowtail Seriola quinqueradiata (Harino et al. 2000). BT residues in fish are not greatly affected by size, but more likely to reflect the recent history of TBT contamination in their environment. In the previous study, TBT concentration was less affected by TL and age in perch and ruffe, although TPT concentrations increased with length and age (Stäb et al. 1994). This indicates that TBT is more easily metabolized or eliminated as the di- and mono-OT levels than TPT. These suggest that TPT might accumulate throughout the life history, whereas TBT do not show such accumulation trend.

Relationship between Organotin Accumulation and Maturation Variation in accumulation of TBT and TPT occur depending on maturation stage in the anguillid eels. TBT and TPT concentrations in silver eels were significantly higher than those in yellow eels. Furthermore, positive correlation was found between each total BT and TBT concentrations, and GSI value (Ohji et al. 2006a, 2009, Arai et al. 2011). The percentages of TBT and TPT in silver eels were higher than those in yellow eels. It is considered that silver eels have higher risk of TBT than that in yellow eels. Biochemical features of ready-to-migrate silver and pre-migratory yellow stages of the shortfin eel Anguilla australis of southeastern Australian waters were reported (De Silva et al. 2002). The percent of moisture, protein and ash content of the liver of silver eels was significantly lower than in yellow eels, but lipid content was significantly higher in the former (36%). Higher amounts of fatty acid in total lipid, and saturates and monoenes were found in silver eels. Eels that they just before spawning migrationare not thought to feed, and at that time of

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migration, oocytes are not fully developed (Lokman et al. 1998), and certain proportion of the reserves will need to be channeled from the reserves for this purpose. Therefore, biochemical changes including the build up of potential large energy reserves take place in the transformation of yellow to silver eel in preparation for long oceanic spawning migration. Similar situation regarding lipid content in A. australis might be considered in A. japonica due to the same genus. Since TBT is a hydrophobic compound, TBT is considered to unite to the lipids in liver. Therefore, higher lipid content in silver eels than yellow eels might lead to be elevated concentration of TBT in silver eels in A. japonica.

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Differences in Organotin Accumulation Depending on Migration TBT and TPT were detected in all migratory types, i.e. marine, estuarine and freshwater residents, in the anguillid eels. The residue of TBT and TPT in marine residents indicates continuous input of TBT and TPT into the sea despite of the ban of its usage. It is reported that yellow eels are territorial and maintain local home-ranges in river, lake, estuaries, and sea, residing in mud, weed beds or shady pools during the day (Naismith and Knights 1990). Eels have been known to feed on benthic invertebrates and other aquatic fauna occurring within the area (Slayter 1981). Because of their benthic feeding habitat and close association with sediment which is known to be a persistent sink of OTs (Langston and Pope 1995), eels have significant potential for bioaccumulation of OTs in all migratory types. The distribution of sedimentbound TBT has been reported to be very similar to that in livers in A. anguilla collected along Thames tideway (Langston et al. 2000, Harino et al. 2002), which implies that sediment is an important vector for TBT uptake for these benthic fish. Extremely high concentrations of TBT were detected in several individuals in marine resident eels in the previous study in Anguilla japonica (564 – 1060 ng g-1 wet wt) (Ohji et al. 2006a). Such relative high concentration were reported in anguillid eels in Vietnam (Arai et al. 2011). The yellow eels are known to have a restricted home range, although sometimes moving to different areas (Bozeman et al. 1985, Ford and Mercer 1986, Parker 1995, Oliveira 1997). In the migratory histories, diverse migratory patterns were observed within the same category of marine and estuarine dependents as follows. Marine eels showed constant high Sr:Ca ratio through their life history, which indicated that the specimen spent long-term in the sea. There was a marine resident showed a change of Sr:Ca ratio from low

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to high levels, that indicated the specimen moved to the sea after spend for several period in the brackish water. Estuarine dependents exhibited the consistent intermediate values in Sr:Ca ratio from the high Sr core out to the otolith edge, suggesting that they stayed for long-term in the brackish water habitat. A estuarine resident showed frequent change of Sr:Ca ratio, which indicated the specimen moved between freshwater, estuarine, or seawater habitats. Another estuarine resident specimen showed the change of Sr:Ca ratio from high to low levels, which indicated the specimen stayed in freshwater after sea or brackish waters. These results suggest that constant ratio of Sr:Ca means staying in small home range, and frequent change of Sr:Ca ratio indicate moving between different habitats. Therefore, even in the same category, there are various levels of risk of OTs for anguillid eels. High concentration in some individuals of marine residents might result from their spending for the long period with only movement of short distance in the sediment that might be considered the hot spot of OTs. TBT and TPT concentrations in marine residents were significantly higher than those in river eels even within the same maturation stage. Since TBT and TPT are mainly used in the coastal area, marine resident eels might be exposed to OTs throughout whole life history. In contrast, since freshwater residents remain in a freshwater environment throughout their life history, they might be little exposed to OTs. TBT and TPT concentrations increased significantly with increasing Sr:Ca ratio. Therefore, it is considered that risk of TBT and TPT in marine residents were higher than those in freshwater residents. In estuarine residents, no significant differences were observed in TBT and TPT concentrations compared to marine and freshwater residents. Since the estuarine residents are considered to move between freshwater and marine habitats during their yellow phase, it is considered that OT exposure varies during their life history. Therefore, the risk of OTs in estuarine resident eels might be considered to be in intermediate level between sea and river eels. Thus, the risk of OTs varies within the same migratory type. Although TBT and TPT concentrations in estuarine and freshwater residents were lower than those in marine residents, the levels of TBT and TPT in estuarine and river can still be toxic to susceptible organisms. There were differences in the compositions between BTs and PTs. In BTs, TBT and its metabolites, DBT and MBT were found to be approximately equal percentages (Ohji et al. 2006a). In contrast, the percentage of TPT was the predominant compounds. Similar situations were found in the previous study (Stäb et al. 1996). High DBT and MBT levels were detected in liver in

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pike, while high concentration of TPT was found. A different metabolic capacity to degrade TBT and TPT in European eel Anguilla anguilla and rainbow trout Oncorhynchus mykiss was found in the previous in vitro experiment (Fent and Bucheli 1994). The liver microsomes in eel and rainbow trout were affected by TBT and TPT, and TPT inhibited the metabolic system more strongly than did TBT. At TBT concentrations of 98 µg ml-1 for eel and 20 µg ml-1 for rainbow trout, the cytochrome P-450 enzymes of each eel and rainbow trout were 50% inactivated, while both fish sowed higher sensitivity to TPT, with 50% P-450 inhibition at a concentration of only 9 µg ml. Therefore, high concentration of degradation products of TBT, and high concentration of TPT in the present study might result from that TBT is more easily dealkylated in the liver and excreted via the bile than TPT because metabolic capacity to degrade TBT in liver is higher than that of TPT in anguillid eel. Since it is clear that there are differences in risk of TBT and TPT among migratory patterns in anguillid eels, the comparison in the contamination level of OTs in anguillid eels between different regions should be conducted within the same migratory types.

Regional Variation in Organotin Level A few studies are available for TBT concentration in anguillid eels for the roughly comparison of the scale of impact. TBT and TPT concentrations ranged from 113 to 1050 and from 480 to 1500 ng g-1 dry wt, respectively, in livers of eels from marinas on Lake Grote Poel, the Netherlands (Stäb et al. 1996). The concentration of TBT in Thames Estuary and Weston Canal in the United Kingdom were from 180.0 to 1349 and from 292.6 to 319.8 ng g-1 wet wt, respectively (Harino et al. 2002). TPT concentrations in Thames Estuary and Weston Canal were from under detection limit to 676.0 and from 998.4 to 1394.6 ng g-1 wet wt, respectively (Harino et al. 2002). In Japanese waters, TBT concentration ranged from 1.1 to 1060.5 ng g-1 wet wt in Tokushima Region of the Shikoku Island, and these values are similar to those in the Netherlands and in the Thames Estuary in the United Kingdom. TBT concentrations in Miyako Region and Lake Ogawara in northern Japan were lower than those in the other regions investigated. TPT concentration in Anguilla japonica from Japan ranged from under the detection limit to 566.2 ng g-1 wet wt in Tokushima Region, and these values are lower than that in the Netherlands, and similar to the level in the United Kingdom. TBT and TPT

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were ranged from 1.53 to 197.4 ng g-1wet wt and from < 0.001 ng g-1wet wt to 45.22 ng g-1wet wt, respectively in A. marmorata and A. bicolor pacifica from Vietnam, and these values seems to be less than the previous reports, although the values are overlapped to those reports. However, these levels are considerable level to induce chronic effect on sensitive aquatic organisms.

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The Risk of Organotin Compounds in the Anguillid Eels The catadromous eels have a different risk of TBT and TPT accompanying intraspecies variation of the migratory pattern and maturation stage, while the accumulation of OTs did not depend on body size, age and sex. Furthermore, Ohji et al. (2006a) suggested that the differences in the migratory history were more effective compare to maturation in the accumulation of organotin. Therefore, the comparison in the contamination level of OTs in anguillid eel between different regions should be conducted in consideration of migratory histories. It has been reported that TBT has adverse effects on many fishes even at ambient water levels, i.e. TBT caused thymus atrophy, increase in granulocytes, accumulation of glycogen and fat in the liver, and changes in cornea, retina, and skin in guppy (Wester and Canton 1987). Furthermore, TBT cause a number of histopathological effects in rainbow trout Oncorhynchus mykiss and European minnow Phoxinus phoxinus in early life stages (De Vries et al. 1991, Fent and Meier 1992, Schwaiger et al. 1992). Survival reduction, survival reduction, morphological and histopathological alterations were found in response to exposure to TPT in European minnow Phoxinus phoxinus in larval stages (Fent and Meier 1994). Exposure of TPT induced chronic effect such as growth and survival in fathead minnow larvae Pimephales promelas (Jarvinen et al. 1988). Thus, the higher ecological risk of marine residents than that of the freshwater residents to TBT and TPT exposure may result in the former being more conspicuously affected by TBT and TPT. Furthermore, estuarine and marine resident eels inhabiting the coastal area make a larger reproductive contribution to the next generation than that of freshwater eel (Chino and Arai 2009). These results seem to indicate that marine and estuarine residents are more affected by TBT than freshwater residents. However, the effects of TBT might not be only on marine and/or estuarine resident eels, but also freshwater eels. In Anguilla japonica, after 5 to 15 yr of yellow eel growth phase in the river or lake, river eels metamorphose into the silver stage, and they move back downstream to the

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ocean to begin the journey to the same spawning area to sea and estuarine eels. It implies that eels from freshwater, brackish water and marine habitats can mix together during the spawning migration, and participate in reproductive activity with marine and/or estuarine resident eels, and potentially contribute to the next generation together. It has been reported that TBT exposure detrimentally affects the reproductive activity of spermatozoa, i.e. decrease the duration and intensity of motility, as well as reduces the ATP levels in the Afrian catfish (Rurangwa et al. 2002), and decrease the viability of herring spermatozoa (Grzyb et al. 2003). It is also reported that fecundity and hatching success were significantly reduced in Japanese medaka Oryzias latipes (Walker et al. 1989). Embryonic exposure of TBT as well as TPT has been reported to result in delaying of hatching, decrease of hatching success and increase of mortality in European minnow Phoxinus phoxinus (Fent 1992, Fent and Meier 1992, 1994). A similar phenomenon of toxicity of TBT and TPT to sperm cell and embryo in the Mediterranean sea urchin Paracentrotus lividus has been reported (Novelli et al. 2002), and the mechanisms of effect of triorganotin in sperm and embryo in sea urchin are considered as follows. High sensitivity of embryos toward triorganotins was to be expressed because different targets (inhibition of DNA and protein synthesis, alteration of cellular Ca2+ homeostasis) are involved during embryonic development (Girard et al. 1997). Sperm toxicity presumably involves both the inhibition of the acrosomal reaction (Giudice 1986) and a direct inhibition of the energy functions of cells (Argese et al. 1998). Those inhibitions of reproduction might occur in A. japonica, resulting in population disturbance. Masculinization (imposex) induced in female gastropods by TBT and TPT exposure leads to reproductive failure and consequently population decline (Bryan et al. 1986, Gibbs and Bryan 1986, 1987, Bettin et al. 1996, Matthiessen and Gibbs 1998, Horiguchi et al. 1997). Therefore, TBT and TPT exposure might also affect the reproduction systems of marine resident eels, resulting in a decline of its population of anguillid eel species. The risks involved in the exposure of the marine and estuarine resident eels to TBT and TPT may in turn influence river eels, resulting in a disturbance in the maintenance of population of anguillid eels.

CONCLUSION The freshwater eels of genus Anguilla are widely used as a bioindicator for environmental monitoring of pollutants. The eel does not reproduce in

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freshwater. Therefore, body burdens are not affected by a reproduction cycle and associated changes in lipid metabolism (Maes et al. 2008). Further, yellow eel has high lipid content, increasing with age and reaching a maximum prior to silvering and emigration. They generally show life-long accumulation and low depuration rates (Larsson et al. 1991, Tulonen and Vuorinen 1996, Knights 1997). Prior to their downstream migration to the offshore spawning area, yellow eels are territorial and maintain local homeranges in rivers and estuaries, residing in mud, weed beds or shady pools during the day (Naismith and Knights 1990). Eels have been known to feed on benthic invertebrates and other aquatic fauna occurring within the area (Tesch 2003). These typical life history characteristics warrant the use of eel as an indicator for the presence of hazardous chemicals in the environment and, in particular, of those substances with a low solubility in water. Thus, the eel tissue concentration and body burden reflect well environmental exposure and that tissue concentration are related to pollution levels of prey species, surface waters and sediments. However, there have been few studies to date on the relationship between OT accumulations and different migratory histories in this species. To understand correctly and minutely of bioaccumulation and biomagnification of pollutants on the eels, such ecotoxicological approach is mandatory. TBT and TPT were detected in all migratory types, i.e. marine, estuarine and freshwater dependents, in the anguillid eels. However, TBT and TPT concentrations increased significantly with increasing Sr:Ca ratio. The accumulation of OTs did not depend on body size, age and sex. These suggest that risk of TBT and TPT in marine residents were higher than those in freshwater residents. Therefore, the comparison in the contamination level of OTs in anguillid eel between different regions should be conducted in consideration of migratory histories. TBT and TPT exposure might also affect the reproductive systems of marine and estuarine resident eels, resulting in a decline of the eel population. The higher accumulation of OTs found in both marine and estuarine resident eels may affect on freshwater dependent eels during reproductive activity, and the scenario consequently might lead to the fluctuation of resource in the anguillid eel.

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Parker, S. J. (1995) Homing ability and home-range of yellow phase American eels in a tidal dominated estuary. Journal of the Marine Biological Association of the United Kingdom 75:127-140. Rurangwa, E., Biegniewska, A., Slominska, E., Skorkowski, E. F. and Ollevier, F. (2002) Effect of tributyltin on adenylate content and enzyme activities of teleost sperm: A biochemical approach to study the mechanisms of toxicant reduced spermatozoa motility. Comparative Biochemistry and Physiology 131C:335-344. Schwaiger, J., Bucher, F., Ferling, H., Kalbus, W. and Negele, R.D. (1992) A prolonged toxicity study on the effects of sublethal concentrations of bis(tri-n-butyltin) oxide (TBTO): histopathological and histochemical findings in rainbow trout (Oncorhynchus mykiss). Aquatic Toxicology 23:31-48. Slayter, E. M. (1981) Unravelling the eel. Oceans, January 1981, 26-31. Stäb, J.A., Brinkman, U.A.T., Cofino, W.P. (1994) Validation of the analysis of organotin compounds in biological tissues using alkylation and gas chromatography. Applied Organometallic Chemistry 8: 577–585. Stäb, J. A., Traas, T. P., Stroomberg, G., van Kesteren, J., Leonards, P., van Hattum, B., Brinkman, U. A., Cofino, W. P. (1996) Determination of organotin compounds in the Foodweb of a shallow freshwater lake in the Netherlands. Archives of Environmental Contamination and Toxicology 31:319-328. Tesch, F. W. (2003) The Eel. Biology and management of anguillid eels. London, Chapman and Hall. Tsukamoto, K. and Arai, T. (2001) Facultative catadromy of the eel, Anguilla japonica, between freshwater and seawater habitats. Marine Ecology Progress Series 220: 365-376. Tulonen, J. and Vuorinen, P.J. (1996) Concentrations of PCBs and other organochlorine compounds in eels (Anguilla anguilla L.) of the Vanajavesi watercourse in southern Finland, 1990–1993. Science of the Total Environment 187: 11–18. Walker, W. W., Heard, C. S., Lotz, K., Lytle, T. F., Hawkins, W. E., Barnes, C. S., Barnes, D. H. and Overstreet, R. M. (1989) Tumorigenic, growth, reproductive and developmental effects in medaka exposed to bis(tri-nbutyltin) oxide. In Proceedings of the Organotin Symposium, Oceans ‘89 Conference, vol.2, pp. 516-524. Seattle, Washington, USA: the Marine Technology Society and the Institute of Electrical and Electronics Engineers Council on Oceanic Engineering.

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Wester, P. W. and Canton, J. H. (1987) Histopathological study of Poecilia reticulata (guppy) after long-term exposure to bis(tri-n-butyltin) oxide (TBTO) and di-n-butyltin dichloride (DBTC). Aquatic Toxicology 10:143165.

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Chapter 3

HABITAT USE AND MIGRATION IN THE JAPANESE EEL ANGUILLA JAPONICA AND INTRODUCED ANGUILLID EELS IN JAPANESE NATURAL WATERS Naoko Chino∗ and Takaomi Arai Copyright © 2012. Nova Science Publishers, Incorporated. All rights reserved.

Atmosphere and Ocean Research Institute, The University of Tokyo, Akahama, Otsuchi, Iwate, Japan

ABSTRACT The catadromous eels of the genus Anguilla are famous for their remarkable migrations between fresh water and marine habitats. The use of Sr:Ca ratios in fish otoliths to reconstruct historical patterns of fish movement between aquatic habitats of different salinity ranges (fresh, estuarine, marine) can be extended to evaluate the frequency and duration of inter-habitat movements. Otolith microchemistry studies have revealed that some yellow and silver eels of temperate Anguilla japonica never migrate into fresh water, but spend their entire life history in the ocean. The application of otolith Sr:Ca ratios to trace the migratory history of the eel has also revealed otolith signatures intermediate to those of marine and freshwater residents of the eel, all of which appeared to reflect estuarine resident, or showed clear evidence of switching between different salinity environments. It thus appears that a proportion of the ∗

Corresponding author: N. Chino, E-mail: [email protected].

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eels move frequently between different environments during their growth phase. Therefore, because individuals of the eel species have been found to remain in estuarine or marine habitats, it appears that the Japanese eel does not all enter into fresh water environments and that the species display more of a facultative catadromy. In Japanese natural waters, several non-native species, such as European eel, A. anguilla, American eel, A. rostrata, and Australian shortfinned eel, A. australis, have recently been found. This is due to their escaping from aquaculture operations or intentional release. Analyses of the otolith Sr:Ca ratios of the European eels caught in the water showed that they had been not only typical freshwater resident but also marine resident before capture. Marine residents that never migrate into fresh water often occur in its own habitat in Europe. This indicates that the European eels retain their own nature despite being far from their original habitat. This further suggests that we must consider that the ecological impact of European eels would affect not only fresh water habitats but also coastal ecosystems in and around Japan. The European and American eels had found to begin maturation, and start downstream migration far from its native range. This discovery of introduced eels initiating their spawning migration at the same time as the Japanese eel raises concerns about the potential impact of interbreeding between species and the possible effects on the fishery resources of A. japonica.

INTRODUCTION The Japanese eel Anguilla japonica Temminck and Schlegel, generally has been considered a catadromous fish species (McDowall 1988). It is widely cultivated in the inland fresh water of Japan, Taiwan and China. The eel A. japonica spawns in waters west of the Mariana Islands, and its transparent leaf-like larvae, or leptocephali, move within the North Equatorial and Kuroshio currents to the east Asian coasts of Taiwan, China, Korea and Japan. They leave these currents after metamorphosing into glass eels, and all are generally thought to migrate up fresh water streams where they grow to the pre-adult silver eel stage. During the silver eel stage, their gonads begin maturing and they start their downstream migration into the ocean and back out to the spawning area, where they spawn and die. A similar life cycle is believed to occur in the Atlantic species, the American eel A. rostrata and the European eel A. anguilla. Both species spawn in the Sargasso Sea, and their larvae move westward within the southern Sargasso Sea. They enter the Gulf Stream and the North Atlantic Drift and are distributed throughout the coasts of North America and Europe, respectively, before their glass eels enter the

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rivers. These spectacular life histories are the subject of a large literature on biology, and are so well accepted that the life cycle of freshwater eels goes without question. However, otolith microchemistry studies have revealed that some yellow and silver eels of Anguilla japonica never migrated into fresh water, but spent their entire life history in the ocean (Tsukamoto and Arai 2001, Arai et al. 2003a, b, 2008, 2009, Kotake et al. 2003, 2005, Chino and Arai 2008, 2009). Recently, the migratory history of several species of anguillid eels have been studied using analytical microchemical techniques to determine the ratios of strontium to calcium (Sr:Ca ratio) in the otoliths of fish (Campana 1999, Arai 2002). The Sr:Ca ratio in the otoliths of fishes differs between the time they spend in fresh water and sea water and this also has been found to be true for anguillid eels (Arai 2002). Thus, the Sr:Ca ratios of otoliths may help in determining whether or not individual eels actually enter into fresh water at the elver stage and whether they remained in fresh water, estuarine or marine environments until the silver eel stage, or if they moved between different habitats with differing salinity regimes. Furthermore, application of otolith Sr:Ca ratios to trace the migratory history of eels revealed otolith signatures that were intermediate to those of marine and freshwater residents of Anguilla anguilla (Tzeng et al. 1997, Arai et al. 2006), A. rostrata (Thibalut et al. 2007 ), A. australis and A. dieffenbachii (Arai et al. 2004), A. marmorata (Chino and Arai 2010a) and A. bicolor (Chino and Arai 2010b, c) and appeared to reflect estuarine resident, or showed clear evidence of switching between different salinity environments. It thus appears that a proportion of eels move frequently between different environments during their growth phase. Chino and Arai (2010b) used these Sr:Ca ratios to divide the migratory histories of anguillid eels collected into 3 migratory types: (1) ‘marine resident’ (spent most of their life in the sea and did not enter fresh water), (2) ‘estuarine resident’ (inhabited estuaries or switched between different habitats), and (3) ‘freshwater resident’ (entered and remained in fresh water river habitats after arrival in the estuary). Therefore, because the individuals of several anguillid species have been found to remain in estuarine or marine habitats, it appears that anguillid eels do not all enter into fresh water environments and these species have been suggested to display more of an apparent facultative catadromy (Chino and Arai 2011). In Japanese waters, two freshwater eel species, Japanese eel Anguilla japonica and giant mottled eel A. marmorata occur naturally. However, several non-native species, such as European eel, A. anguilla, American eel A. rostrata and Australian shortfinned eel A. australis have recently been found

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in these waters (Okamura et al. 2008). This is probably due to their escaping from aquaculture operations or intentional release, although the precise pathway for introduction of these species into natural waters is still unclear. After 1968, a number of non-native glass eels were imported into Japan from more than 23 countries as alternatives to the seedlings for aquaculture of the Japanese eel (Okamura et al. 2008) However, information regarding the ecological status of non-native eels in Japan remains only at rudimental level (Miyai et al. 2004, Okamura et al. 2008, Arai et al. 2009). These data are necessary to estimate whether non-native eels would adapt in East Asia and to predict their unknown effects on ecosystems.

Figure 1. Study sites showing the geographical range of the Japanese eel Anguilla japonica used in this chapter. The source of information is Arai et al. (2003a, b), Kotake et al. (2003, 2005), Chino et al. (2008) and Chino and Arai (2009). Relative migratory patterns, marine resident, estuarine resident and freshwater resident is shown for four sites in Japan. R1: Otsuchi Bay, Miyako Bay and off Sanriku Coast, R2: Mikawa Bay, R3: Kii Channel, and R4: coastal waters of Amakusa Island.

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Figure 2. Procedures of life-history transect analyses of Sr and Ca concentrations in the freshwater eel, which were measured along a line down the longest axis of otolith from the core to the edge using a wavelength dispersive X-ray electron microprobe and age determination by otolith.

In this chapter, we examined and discussed for habitat use and migration between fresh water and sea water habitats by Anguilla japonica in Japanese waters. We also discussed the implications of these findings in relation to the possible contribution of their migratory types, i.e., marine resident, estuarine resident and freshwater resident to the spawning population of A. japonica. Further, we discussed the life history of non-native eel Anguilla spp. to understand their adaptation in Japanese environments far from their original habitat and the ecological impact for A. japonica.

MATERIALS AND METHODS This chapter synthesizes information following our publications in Anguilla japonica: Tsukamoto and Arai (2001), Arai et al. (2003a, b, 2008, 2009), Kotake et al. (2003, 2005), Chino et al. (2008) and Chino and Arai (2009) (Figure 1). In all studies, sagittal otoliths were extracted, and the otoliths were embedded in epoxy resin (Struers, Epofix). These otoliths were then ground to expose the core along the anterior-posterior direction in the frontal plane,

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using a grinding machine equipped with a diamond cup-wheel (Struers, Discoplan-TS), and polished further with oxide polishing suspension on an automated polishing wheel (Struers, PdM-Force-20). Finally, they were cleaned using distilled water and ethanol, and dried at 50ºC in an oven prior to examination. The ground surfaces of the otoliths were examined at 200x with a light microscope, and photographs were taken to measure the “radius” of the elver mark (the distance from the otolith core to the elver check) (Figure 2).

Figure 3. Fluctuation of otolith Sr:Ca ratios along a transect line from the core to the edge of the otolith with reference to growth stages and habitat uses in the life history of Anguilla japonica.

For otolith microchemical analyses, all otoliths were Pt-Pd coated by a high vacuum evaporator. Otoliths from all specimens were used for lifehistory transect analyses of Sr and Ca concentrations, which were measured along a line down the longest axis of each otolith from the core to the edge (Figure 2) using a wavelength dispersive X-ray electron microprobe (JEOL JXA-8900R). We describe the detail of the analytical procedure in Chino and Arai (2011).

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We calculated the average Sr:Ca ratios for the values outside the elver mark. According to the criteria of Tsukamoto and Arai (2001) and Chino and Arai (2010b), these specimens were categorized into “marine resident” (Sr:Ca ≥ 6.0 x 10-3), “estuarine resident” (2.5 x 10-3 ≤ Sr:Ca < 6.0 x 10-3) and “freshwater resident” (Sr:Ca < 2.5 x 10-3). Following the electron microprobe analysis, the otoliths were repolished to remove the coating, etched with 1% HCl and thereafter stained with 1 % toluidine blue. The age of the specimens was determined by counting the number of blue-stained transparent zones following the method of Chino and Arai (2009) (Figure 2).

RESULTS

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Migratory History in Anguillid Eels during Oceanic Migration Period The Sr:Ca ratios in the transects along the radius of each otolith showed the same common feature in all specimens (Figure 3). All otoliths had a common peak of high values of Sr:Ca ratios at the center of the otolith inside the elver mark (ca 150 µm), which roughly corresponded to the leptocephalus and early glass eel stages during their oceanic life (Arai et al. 1997). Outside of the high Sr core, there was a great variation in the change of the Sr:Ca ratios in the otoliths of eels from different habitats. The high Sr content in the central core region during the leptocephalus stage may derive from the large amounts of gelatinous extracellular matrix that fills the body until metamorphosis. This material is composed of sulfated glycosaminoglycans (GAG), which are converted into other compounds during metamorphosis (Pfeiler 1984). The drastic decrease in Sr at the outer otolith region in both river and sea water samples after metamorphosis to glass eels, may occur because these sulfated polysaccharides have an affinity to alkali earth elements, and are particularly high in Sr, suggesting that a high Sr content in the body has a significant influence on otolith Sr content through saccular epithelium in the inner ear, and the sudden loss of Sr-rich GAG during metamorphosis probably results in the lower Sr concentration in otoliths after metamorphosis (Arai et al. 1997).

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Figure 4. Plots of the otolith Sr:Ca ratios along transect lines from the core to the edge of the otolith for three representative specimens of Anguilla japonica. Migratory patterns showed either marine resident (a), estuarine resident (b) or freshwater resident (c). The solid line in each panel indicates marine water life period (≥ 6.0 x 10-3 in Sr:Ca ratios), and the dotted line in each panel indicates fresh water life period (< 2.5 x 10-3 in Sr:Ca ratios).

Migratory History in Anguilla japonica after Recruitment to Coastal Waters Outside of the high Sr:Ca core, there was great variation in the Sr:Ca ratios in the otoliths of Anguilla japonica from different habitats. The change

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in Sr:Ca values outside the elver mark in the constant type was generally divided into three types (Figure 4a, b , c): (1) relatively high values of more than 6.0 x 10-3 with no movement into fresh water (Figure 4a), (2) intermediate values of 2.5-6.0 x 10-3 (Figure 4b), and (3) constantly low values less than 2.5 x 10-3 (Figure 4c). In addition to these typical migratory histories, we also found switch type with Sr:Ca ratios shifting between two phases from a low phase (less than 2.0 x 10-3) to a middle phase (range: 2.5-6.0 x 10-3), from a low phase to a high phase (more than 6.0 x 10-3), or from a middle phase to a high phase, which suggests that these specimens shifted their resident environment. Further, specimens showed multiple shifts, with several low and high Sr:Ca ratio phases along the life history transect, which suggests that these specimens moved to different environments several times in their lives. Based on our previous studies, we apparently examined specimens from four regions through Japan (Figure 1). The northernmost region includes the samples from Otsuchi Bay, Miyako Bay and off Sanriku Coast (R1), northern part of middle one does Mikawa Bay (R2), southern part of middle one does Kii Channel (R3) and southernmost one does coastal waters of Amakusa Islands (R4). In R1, 22 yellow and 6 silver eels showed 8 marine, 14 estuarine and 0 freshwater residents and 4 marine, 2 estuarine and 0 freshwater residents, respectively (Table 1). A total of 198 eels were examined in R2. These showed 80 marine, 85 estuarine and 33 freshwater residents. All samples of 37 specimens were silver eels showing 7 marine, 23 estuarine and 7 freshwater residents in R3. In R4, 6 yellow and 16 silver eels showed 2 marine, 3 estuarine and 1 freshwater residents and 3 marine, 9 estuarine and 4 freshwater residents, respectively (Table 1).

Migratory History in Anguilla anguilla in Japanese Waters Regarding non-native eels in Japanese waters, Anguilla anguilla (Okamura et al. 2008, Arai et al. 2009) was examined in the otolith Sr:Ca ratios to trace their migratory histories. In 17 A. anguilla specimens examined from Mikawa Bay of Aichi Prefecture (Figure 1), the patterns of the Sr:Ca ratios were classified into two types (Okamura et al. 2008). The first type (n = 8) had consistently low Sr:Ca values outside of the high Sr:Ca core and the mean values outside the high Sr core to the otolith edge of each specimen ranged from 1.5 to 2.6 x 10-3, suggesting that they had lived in fresh water throughout the growth phase. The second type (n = 9) had relatively high values of the Sr:Ca ratios and the mean values ranged from 6.0 to 9.2 x 10-3,

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suggesting that they had lived in sea water throughout almost the entire growth phase. According to the criteria of Chino and Arai (2010b), A. anguilla has three migratory patterns, marine resident, esuarine resident and freshwater resident in Japanese waters. In a silver stage of A. anguilla from Tokyo Bay, the life history transect of otolith Sr:Ca showed constantly low values with a mean of 1.7. The fluctuation pattern suggested that the eel spent its entire life in a fresh water environment only, with no movement either to the sea or a brackish environment just before spawning migration. Table 1. Migratory types from each region through Japan Sampling sites R1 (Sanriku) R2 (Mikawa) R3 (Kii)

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R4 (Amakusa)

Deveropmenta l stages Yellow Silver

Sample size 22 6

Marine 8 4

Residents Estuarine Freshwater 14 0 2 0

Yellow/Silver Yellow Silver Yellow Silver

198 0 37 6 16

80 0 7 2 3

85 0 23 3 9

33 0 7 1 4

Index of Habitat Use in Anguilla japonica In order to quantitatively estimate the general habitat use of each specimen based on its mean Sr:Ca ratio values, we calculated an index for the degree of sea water residence as follows. Since all specimens had experienced the same common marine life as a preleptocephalus, leptocephalus, metamorphosing larva and early glass eel during their long trip from the spawning area to coastal waters, the values of Sr:Ca inside the elver mark could be excluded from each life-history transect (see Figure 3) when estimating the degree of sea water residence for the juvenile stages of each individual after arrival in coastal waters at the early glass eel stage. The mean Sr:Ca ratio values outside the elver mark in each eel indicated that the habitat use was variable with interspecific variations after their recruitment to the coastal waters as glass eels (Figure 5).

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DISCUSSION

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Migratory History of Anguilla japonica The most significant finding of migration of Anguilla japonica was that the occurrence of marine resident eels that had never migrated into fresh water habitat was confirmed at many localities in Japanese coastal waters. Another significant result was the finding of estuarine resident of eel migration. These findings strongly suggested that A. japonica has a flexible migration strategy with a high degree of behavioral plasticity and an ability to utilize the full range of salinity as juveniles. In detail, however, some specimens were difficult to classify into 1 of these patterns because of a complex life-history transect or an intermediate change in values. Such diverse behaviour is the same as that of A. japonica from Taiwan (Shiao et al. 2003) and other anguillid eels A. anguilla (Tzeng et al. 2000; Arai et al. 2006), A. rostrata (Daverat et al. 2006), A. australis and A. dieffenbachii (Arai et al. 2004), A. marmorata (Chino and Arai 2010a) and A. bicolor (Chino and Arai 2010b, c) which migrate flexibly among fresh water, brackish water, and sea water environments. It is less studied to use otolith Sr:Ca ratio analysis to document the migratory history of anguillid eels in conjunction with age and gonadsomatic index (GSI) analyses of eels collected continuously at a fixed location throughout the year. Previous studies using the same technique to determine the migratory history of anguillid eels have shown that many anguillid eels live in marine and estuarine habitats, in addition to those that show the typical catadromous migration pattern of entering fresh water. The analysis of the Sr:Ca ratios in the otoliths of almost 200 eels collected using set nets in the brackish water of Mikawa Bay showed that all 3 of the general migratory types of eels (marine, estuarine and freshwater residents) were present, but that there were some seasonal differences in their occurrences (Kotake et al. 2005). The majority of eels were caught during the typical spawning migration season in the autumn, but those that were caught in other months were all sea or estuarine eels. This seasonal occurrence pattern of each migratory type could correspond with their migratory behaviour throughout the year.

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Figure 5. Frequency distribution of the mean values of Sr:Ca ratio outside the elver mark (150 µm in radius) in each otolith of the specimens. The source of information is Arai et al. (2003a, b), Kotake et al. (2003), Chino et al. (2008) and Chino and Arai (2009). A: all data for both yellow and silver eels, B: data for yellow eel, C: data for silver eel.

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Considering that there were estuarine residents at all the localities of Japanese coasts (Figure 1), it appears that it is not unusual for Anguilla japonica to live in estuarine or sea water habitats for long periods of time, and this appears to be a geographically widespread phenomenon that is not limited to A. japonica. It is well known among fishermen that large numbers of immature yellow eels occur in estuarine waters in Japan. In addition, male yellow eels of the American eel A. rostrata are common in estuarine habitats in the southeastern USA (Helfman et al. 1987), and over 80% of European eels in the commercial ocean catch in the North Sea are yellow, i.e. not yet in the silver phase (Tsukamoto and Arai 2001). It has been generally assumed that the yellow eels found in coastal waters have been washed out of rivers by floods, but this has not been tested. Tagging studies have shown that some sea eels in the North Sea migrated into brackish or fresh water areas (Lowenberg 1980), suggesting a secondary movement after first settlement. Thus, the classification of anguillid eels in all major ichthyology texts as being catadromous and having a fresh water growth stage clearly needs revision, because it is now evident that their movement into fresh water is not an obligate migratory pathway, and should be defined as a facultative catadromy, with ocean and estuarine residents as ecophenotypes.

Habitat Use of Anguilla japonica Anguilla japonica may use sea water habitats on a widespread basis, that it appears to mature in the habitats in the same way as in fresh water, and that the silver phase estuarine and sea eels presumably migrate to the spawning areas to reproduce just as do typical freshwater resident eels. A number of marine resident eels and estuarine eels were in the silver phase, indicating that they were close to migrating or were in the early stages of migration. To make an estimation of the contribution of marine resident eels to spawning stock, we used as many specimens as possible in this chapter from various habitats around Japan. As a result we obtained a frequency distribution for the degree of sea water residence (Figure 5), which shows the relative proportion of the 3 types based on these samples. It indicates that eels which utilize the marine and brackish water environments to various degrees during their juvenile growth phase may make a substantial contribution to the spawning stock each year. Thus, estuarine and marine habitats are important for eels around Japan. The habitat use of female eels included a high percentage of sea eels (24 %), while the migratory male eels were either river or estuarine eels with no

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occurrence of sea eels in Kii Channel (Chino and Arai 2008). Kotake et al. (2003) also reported that female silver eels caught near the Amakusa Islands of western Japan included many sea eels (44 %) and that males were mainly river eels (43 %). A similar finding, a high percentage of sea eels (45 %), while the migratory male eels were mainly river (42 %) and estuarine eels (42 %), is also reported in Mikawa Bay along the east coast of central Japan (Kotake et al. 2005). Krueger and Oliveira (1999) concluded that increases in population density, and the resulting slower growth, favored the production of males in Anguilla rostrata. Wiberg (1983) concluded that warm temperatures induce maleness in A. anguilla, but long–term experiments in Sweden produced a small but significant increase in the number of females with increasing temperature (Holmgern and Mosegaard 1996). In A. japonica, Sasai et al. (2001) reported that in the East China Sea, females were more abundant (n = 71) than males (n = 18). Tzeng et al. (1995) also reported that A. japonica collected near the estuary and at down-, mid- and up-stream sites of rivers in northern Taiwan were mainly made up of smaller individuals whose sex was undetermined whereas the eels whose sex could be determined were mainly female. They concluded that overcrowding and poor feeding would give to rise male eels, and low population densities with rich feeding would favor females. Thus, the potentially food rich and low population density environment in the coastal waters of Shikoku Island might favor the production of females, while river habitats with poor food and higher population density might favor males.

Cause of Occurrence of Marine Resident Eels Han et al. (2010) examined genetic differentiation using characteristics of the 6 analyzed microsatellite loci for three migratory types, marine, estuarine and freshwater residents in Anguilla japonica. No genetic differentiation was found among eel groups possessing different habitat uses. Thus, the diverse habitat usage by Japanese eels could be due to behavioral plasticity that allows the utilization of different ecological niches, rather than a heritable character that can cause genetic differentiation among populations. In anadromous salmon, freshwater residents or landlocked populations that do not migrate to the ocean often occur, especially near the southern limit of their geographical distribution (McDowall 1988). The ancestors of salmon, which originated in fresh water, expanded their growth habitat into the ocean while their breeding place remained in fresh water. Since reproduction is physiologically costly, it was hypothesized that the migratory behaviour

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remained conservative through its evolutionary process (Tcharnavin 1939). Freshwater eels of the genus Anguilla are considered to have originated from a marine ancestor, and all anguilliform fishes except Anguilla are marine species; thus, the marine breeding habits of Anguilla are probably a conservative trait. This suggests the hypothesis that a number of species of catadromous eels have never lost the ability to be resident in marine habitats during the juvenile growth phase, but it is unknown whether this is due to a remnant genetic trait that determines if an individual will enter fresh water or not, or if it is simply due to behavioral plasticity that enables each species to use the maximum range of habits. Another hypothesis for the occurrence of marine resident anguillid eels would be ecological competition with other species (Moriarty 1978). In the case of European eels, they may have strong competition with the conger eel Conger conger, especially in regard to predation at lower latitudes, and thus there are few reports of the occurrence of European eels in the ocean from the Central and South European and Mediterranean coasts where conger eels are plentiful. In contrast, the North Sea and Baltic Sea have no conger eels, but European eels are abundant and commercially exploited (Lowenberg 1980). Marine resident eels occur in the East China Sea, however, in spite of a huge stock of C. myriaster. In A. japonica, there may be other species-specific factors in each geographic area that determine the distribution and abundance of marine resident eels.

Life History of European Eel in Japanese Waters The otolith Sr:Ca ratios of the European eels caught in Mikawa Bay showed that they had been not only freshwater residents but also marine and estuarine habitats (Okamura et al. 2008). Arai et al. (2009) also found that an eel spent its entire life in a fresh water environment just before spawning migration in Tokyo Bay, as was shown by the value of the Sr:Ca ratio, which showed a low level during the glass eel and yellow eel stages. Futhermore, the fact that Anguilla anguilla was found in Japanese waters, and that the eel matured and began its spawning migration. Marine resident eels that never migrate into fresh water often occur in its own habitat in Europe such as the Baltic Sea (Tzeng et al. 2000). Estuarine resident eels are also found in European countries from Ireland (Arai et al. 2006) and France (Daverat et al. 2006). This indicates that the European eels retain their own nature despite

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being far from their original habitat. European eel could adapt and utilize in Japanese environments migrating various water environments. The GSI values of the European eel specimens in Japanese waters (n = 40) ranged from 0.7 to 4.8 with (Okamura et al. 2008). The histological examination revealed no abnormalities in their gonads. Further, most of the European eel specimens possessed relatively mature oocytes at the oil droplet stage (67.5%) or primary yolk globule stage (15%), while the remainder (17.5%) possessed immature oocytes at the peri-nucleolus stage. Miyai et al. (2004) also found that the eye index exceeded 6.5 in 36 European eels collected from Niigata Prefecture, Japan with ranging 6.9 to 13.9. It indicates that all eels were sexually maturing, migrating silver eels (Pankhurst1982). These results suggest that the European eels studied in those studies had already begun to metamorphose into silver eels, which are possible candidates as spawners. Thus, the European eel could show normal physiological development in the Japanese environment. Such ‘normality’ shown by introduced species could cause serious problems for the conservation of the fisheries resources of native species. Interspecies competition for habitat and food might occur between introduced eels species and native eels or other aquatic animals. The possibility also exists that introduced eels could successfully migrate to the spawning area located to the west of the Mariana Islands and interbreed with Anguilla japonica. In fact, a sexually maturing silver eel of A. anguilla was found in the East China Sea together with A. japonica migrating to the spawning area (Sasai et al. 2001). If introduced eels can migrate and eventually spawn with A. japonica, it is possible that they could form hybrids, as has been suggested for the two Atlantic anguillid eels (Avise et al. 1990). The potential ecological and genetic impacts of introduced eels on the fisheries resources of A. japonica in East Asia are unclear, but the possibility of negative affects should not be ignored, nor should the potential impacts on fish assemblages in rivers that have not historically contained eels.

CONCLUSION Otolith microchemistry studies have revealed that a number of yellow and silver eels of the Japanese eel Anguilla japonica never migrate into fresh water, but spend their entire life history in the ocean. Application of otolith Sr:Ca ratios to trace the migratory history of eels has also revealed otolith signatures intermediate to those of marine and freshwater residents, all of which appeared to reflect estuarine resident, or showed clear evidence of

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switching between different salinity environments. It thus appears that a proportion of eels move frequently between different environments during their growth phase. The wide range of otolith Sr:Ca ratios indicated that the habitat preference of A. japonica during their growth phases would be facultative and not obligatory. These findings strongly suggested that A. japonica has a flexible migration strategy with a high degree of behavioral plasticity and an ability to utilize the full range of salinity. Otolith analyses of European, American and Australasian yellow and silver eels and those of tropical eels A. marmorata and A. bicolor have also shown evidence of marine and estuarine residents (Tzeng et al. 2000, Arai et al. 2004, 2006, Daverat et al. 2006, Thibault et al. 2007, Cino and Arai 2010a, b, c). Therefore, because individuals of several anguillid species have been found to remain in estuarine or marine habitats, it appears that anguillid eels do not all enter into fresh water environments and that these species display more a facultative catadromy. Both marine, estuarine and freshwater resident eels began their spawning migration toward the open ocean at about the same time. This type of synchronization of migration and gonadal maturation, and the apparent predominance of estuarine and marine habitats found in A. japonica, has important implications for the conservation of this species. It implies that eels from both fresh water and marine habitats can mix together during the spawning migration and potentially contribute to the next generation, and that estuarine and marine habitats may be very important for eels around Japan. In Japanese waters, several introduced eels were found, especially the European eel Anguilla anguilla is one of the wide spread species in the waters. The eel might have either escaped from a culture pond or been released into a river. The eel could spend its entire life in various water environments between fresh and marine waters just before spawning migration, as was shown by the value of the Sr:Ca ratio (Okamura et al. 2008, Arai et al. 2009). Futhermore, the fact that A. anguilla was found in Japanese waters, and that the eel matured and began its spawning migration, suggests that the introduced eel could adapt and survive in a foreign environment far from their original habitat. Although the number of introduced eels such as A. anguilla has recently decreased (Okamura et al., 2008), it is important to study the life history and behaviour of eels introduced in Japanese waters to conserve the A. japonica population in the ecosystem of Japanese waters.

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REFERENCES Arai, T., Otake, T., Tsukamoto, K. (1997) Drastic changes in otolith microstructure and microchemistry accompanying the onset of metamorphosis in the Japanese eel Anguilla japonica. Marine Ecology Progress Series 161: 17-22. Arai, T. (2002)) Migratory history of fishes: present status and perspectives of the analytical methods. Japanese Journal of Ichthyology 49: 1-23. Arai, T., Kotake, A., Ohji, M., Miyazaki, N., Tsukamoto, K. (2003a) Migratory history and habitat use of Japanese eel Anguilla japonica in the Sanriku Coast of Japan. Fisheries Science 69: 813-818. Arai, T., Kotake, A., Ohji, M., Miller, M. J., Tsukamoto, K., Miyazaki, N. (2003b) Occurrence of sea eels of Anguilla japonica along the Sanriku Coast of Japan. Ichthyological Research 50: 78-81. Arai, T., Kotake, A., Lokman, P. M., Miller, M. J., Tsukamoto, K. (2004) Evidence of different habitat use by New Zealand freshwater eels, Anguilla australis and A. dieffenbachii, as revealed by otolith microchemistry. Marine Ecology Progress Series 266: 213-225. Arai, T., Kotake, A., McCarthy, T. K. (2006) Habitat use by the European eel Anguilla anguilla in Irish waters. Estuarine, Coastal and Shelf Science 67: 569-578. Arai, T., Kotake, A., Ohji, M. (2008) Variation in migratory history of Japanese eels, Anguilla japonica, collected in the northernmost part of its distribution. Journal of the Marine Biological Association of the United Kingdom 88: 1075-1080. Arai, T., Chino, N., Kotake, A. (2009) Occurrence of estuarine and sea eels Anguilla japonica and a migrating silver eel Anguilla anguilla in Tokyo Bay area, Japan. Fisheries Science 75: 1197-1203. Avise, J. C., Nelson, W. S., Arnold, J., Koehn, R. K., Williams, G. C., Thorsteinsson, V. T. (1990) The evolutionary genetic status of Icelandic eels. Evolution 44: 1254-1262. Campana, S. E. (1999) Chemistry and composition of fish otoliths: pathways, mechanisms and applications Marine Ecology Progress Series 188: 263297. Chino, N., Yoshinaga, T., Hirai, A., Arai, T. (2008) Life history patterns of silver eels Anguilla japonica collected in the Sanriku Coast of Japan. Coastal Marine Science 32: 54-56.

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Chino, N., Arai, T. (2009) Relative contribution of migratory type on the reproduction of migrating silver eels, Anguilla japonica, collected off Shikoku Island, Japan. Marine Biology 156: 661-668. Chino, N., Arai, T. (2010a) Migratory history of the giant mottled eel (Anguilla marmorata) in the Bonin Islands of Japan. Ecology of Freshwater Fish 19: 19-25. Chino, N., Arai, T. (2010b) Occurrence of marine resident tropical eel Anguilla bicolor bicolor in Indonesia. Marine Biology 157: 1075-1081. Chino, N., Arai, T. (2010c) Habitat use and habitat transitions in the tropical eel, Anguilla bicolor bicolor. Environmental Biology of Fishes 89: 571578. Chino, N., Arai, T. (2011) Facultative catadromy in the freshwater eel genus Anguilla between fresh water and sea water habitats. In: Fish Ecology, Editor: Dempsey SP, p. -114, Nova Science Publishers, New York 192pp. Daverat, F., Limberg, K. E., Thibault, I., Shiao, J. C., Dodson, J. J., Caron, F., Tzeng, W. N., Iizuka, Y., Wickström, H. (2006) Phenotypic plasticity of habitat use by three temperate eel species, Anguilla anguilla, A. japonica and A. rostrata. Marine Ecology Progress Series 308: 231-241. Dingle, H. (1980) Ecology of juvenile grey mullet: a short review. Aquaculture 19: 21-36. Ege, V. (1939) A revision of the Genus Anguilla Shaw. Dana Report 16: 8256. Gross, M. R. (1985) Disruptive selection for alternative life histories in salmon. Nature 313: 47-48. Gross, M. R. (1987) Evolution of diadromy in fishes. American Fisheries Society Symposium 1: 14-25. Han, Y. S., Iizuka, Y., Tzeng, W. N. (2010) Does Variable Habitat Usage by the Japanese Eel Lead to Population Genetic Differentiation? Zoological Studies 49: 392-397. Helfman, G. S., Facey, D. E., Hales, L. S. Jr, Bozeman, E. L. Jr (1987) Reproductive ecology of the American eel. American Fisheries Society Symposium 1: 42-56. Kotake, A., Arai, T., Ozawa, T., Nojima, S., Miller, M. J., Tsukamoto, K. (2003) Variation in migratory history of Japanese eels, Anguilla japonica, collected in coastal waters of the Amakusa Islands, Japan, inferred from otolith Sr/Ca ratios. Marine Biology 142: 849-854. Kotake, A., Okamura, A., Yamada, Y., Utoh, T., Arai, T., Miller, M. J., Oka, H. P., Tsukamoto, K. (2005) Seasonal variation in migratory history of the

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Japanese eel, Anguilla japonica, in Mikawa Bay, Japan. Marine Ecology Progress Series 293: 213-221. Krueger, W. H., Oliveira, K. (1999) Evidence for environmental sex determination in the American eel, Anguilla rostrata. Environmental Biology of Fishes 55: 381–389. Lowenberg, U. (1980) An assessment of the eel (Anguilla anguilla) stock in the German Bight as evaluated by commercial and experimental fishery. International Council for the Exploration of the Sea, Committee Meeting 1980/M: 5 1-9. McDowall, R. M. (1988) Diadromy in fishes. Croom Helm, London. Miyai, T., Aoyama, J., Sasai, S., Inoue, J. G., Miller, M. J. Tsukamoto, K. (2004) Ecological aspects of the downstream migration of introduced European eels in the Uono River, Japan. Environmental Biology of Fishes 71: 105-114. Moriarty, C. (1978) Eels, a natural and unnatural history. David and Charles, Newton Abbot. Myers, G. S. (1949) Usage of anadromous, catadromous and allied terms for migratory fishes. Copeia 1949: 89-97. Nordeng, H. (1983) Solution to the char problem based on arctic char (Salvelinus alpinus) in Norway. Canadian Journal of Fisheries and Aquatic Sciences 40: 1372-1387. Okamura, A., Zhang, H., Mikawa, N., Kotake, A., Yamada, Y., Utoh, T., Horie, N., Tanaka, S., Oka, H. P. Tsukamoto, K. (2008) Decline in nonnative freshwater eels in Japan: ecology and future perspectives. Environmental Biology of Fishes 81: 347-358. Pankhurst, N. W. (1982) Relation of visual changes to the onset of sexual maturation in the European eel Anguilla anguilla (L.). Journal of Fish Biology 21: 127-140. Pfeiler, E. (1984) Glycosaminoglycan breakdown during metamorphosis of larval bone fish Albula. Marine Biology Letters 5: 241-249. Sasai, S., Aoyoma, J., Watanabe, S., Kaneko, T., Miller, M. J., Tsukamoto, K. (2001) The occurrence of migrating silver eels, Anguilla japonica, in the East China Sea. Marine Ecology Progress Series 212: 305-310. Schaffer, W. N., Elson, P. F. (1975) The adaptative significance of variations in life history among local populations of Atlantic salmon in North America. Ecology 56: 577-590. Shiao, J. C., Iizuka, Y., Chang, C. W., Tzeng, W. N. (2003) Disparities in habitat use and migratory behaviour between tropical eel Anguilla

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marmorata and temperate eel A. japonica in four Taiwanese rivers. Marine Ecology Progress Series 261: 233-242. Stearns, S. C. (1977) The evolution of life history traits-a critique of the theory and a review of the data. Annual Review of Ecology and Systematics 8: 145-171. Tcharnavin, V. (1939) The origin of salmon its ancestry marineor freshwater? Trout and Salmon Magazine 95: 120-140. Tesch, F. W. (2003) The Eel. Biology and management of anguillid eels. Chapman and Hall, London. Thibault, I., Dodson, J. J., Caron, F., Tzeng, W. N., Iizuka, Y., Shiao, J. C. (2007) Facultative catadromy in American eels: testing the conditional strategy hypothesis. Marine Ecology Progress Series 344: 219-229. Tsukamoto, K. Arai, T. (2001) Facultative catadromy of the eel, Anguilla japonica, between freshwater and seawater habitats. Marine Ecology Progress Series 220: 365-376. Tzeng, W. N., Cheng, P. W., Lin, F. Y. (1995) Relative abundance, sex ratio and population structure of the Japanese eel Anguilla japonica in the Tanshui River system of northern Taiwan. Journal of Fish Biology 46:183-201. Tzeng, W. N., Wang, C. H., Wickström, H., Reizenstein, M. (2000) Occurrence of the semi-catadromous European eel Anguilla anguilla in the Baltic Sea. Marine Biology 137: 93-98. Wiberg, U. H. (1983) Sex determination in European eel (Anguilla anguilla L.): a hypothesis based on cytogenetic results, correlated with findings of skewed sex ratio. Cytogenet Cell Genet 36: 589-598.

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Chapter 4

EARLY LIFE HISTORY AND RECRUITMENT MECHANISMS OF THE FRESHWATER EELS GENUS ANGUILLA Takaomi Arai∗

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Department of Biology, Faculty of Science, Universiti Putra Malaysia, UPM Serdang, Selangor Darul Ehsan, Malaysia

ABSTRACT The freshwater eels have fascinated biologists because of their spectacular thousands of long-distance migrations between their freshwater habitats and their spawning areas far out in the ocean. However, recent studies indicated that much shorter migrations of a few hundred kilometers are made by tropical eels to spawn in areas near their freshwater habitats, clearly contrasting with the long distance migrations of their counterparts in temperate regions, such as the European eel Anguilla anguilla, the American eel A. rostrata and the Japanese eel A. japonica. Ages at metamorphosis and recruitment were constant throughout year, whereas significant differences were found among species in tropical species. Hatchings were estimated to occur throughout the entire year in the species. In both tropical and temperate species, positive linear relationships were found between age at metamorphosis ∗

E-mail: [email protected]

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Takaomi Arai and age at recruitment, suggesting that early metamorphosing larvae were recruited to freshwater habitats at an early age. Year-round recruitment of tropical glass eels to the river mouth would necessarily follow year-round spawning and stable recruitment age. Such a recruitment mechanism differs from that of temperate eels, the latter having a limited spawning season followed by a limited period of recruitment. This chapter outlines the recent findings on the early life ecology of the freshwater eels such as larval migrations, metamorphosis, recruitment and growth. Based on these findings, the present state of our understanding about the evolution of oceanic migration in the genus Anguilla is discussed.

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INTRODUCTION The freshwater eels of the genus Anguilla consist of 16 species and three subspecies and are widely distributed in most tropical and subtropical areas of the world. They all have catadromous life histories, spawn in tropical ocean waters, and their larvae are transported back to their growth habitats in freshwater or estuarine areas by warm subtropical currents (Schmidt 1922, 1925, Tesch, 2003). The continental distributions of the temperate species appear to be related to the subtropical circulation of the oceans, with most species being located along the west sides of the Atlantic, Indian, and Pacific Oceans, except for the European eel, A. anguilla (Ege 1939). However, anguillid eels are absent along the east coast of South America, despite the existence of the warm Brazil Current. Based on this geographic pattern, the Atlantic species (A. anguilla and A. rostrata) are geographically separated from their other congeners in the Pacific and Indian Oceans. Such a unique geographic distribution has recently attracted the attention of biologists, and numerous studies have been conducted. Among their various life history events, metamorphosis from leptocephalus to glass eel is one of the most interesting phenomena. The timing of metamorphosis, i. e., the duration of the leptocephalus stage, is an important biological key for determining the geographical distribution of eels. Long term larval migration in the sea might have been involved in the worldwide distribution of the genus and consequent speciation of Anguilla species. In fifteen species of Anguilla, ten being known from tropical regions (Ege 1939). Of the latter, seven species/subspecies occur in the western Pacific around Indonesia, i. e. A. celebesensis, A. interioris, A. nebulosa nebulosa, A. marmorata, A. borneensis, A. bicolor bicolor and A. bicolor pacifica (Ege 1939, Castle and Williamson 1974, Arai et al. 1999a). Mitochondrial DNA

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analysis has revealed that A. borneensis from Borneo Island was closest to the ancestral form among the 16 presently-known species (Aoyama et al. 2001). Further, based on the whole mitochondrial genome sequences for all species of the genus Anguilla, their phylogenetic relationships suggested that A. mossambica was the most likely basal species, and the other species (except for A. borneensis) formed three geographic clades: Atlantic, Oceania, and Indo-Pacific (Minegishi et al. 2005). These findings suggest that the tropical species seem to be more closely related to the ancestral form than their temperate counterparts. Thus, studying larval migration and metamorphosis in tropical eels may provide some clues to understanding the nature of primitive forms of catadromous migration in freshwater eels and how the large-scale migration of temperate species became established. Examination of otolith microstructure and microchemistry have revealed considerable information on the early life history of Anguilla species. Arai et al. (1997) have revealed that a marked increase in otolith increment width, coincident with a drop in Sr:Ca ratios, indicated the onset of metamorphosis, the latter apparently being completed before the maximum peak of otolith increment width (Arai et al. 1997). Based on these criteria, a number of studies regarding the early life history and recruitment such as larval growth and metamorphosis, migration and recruitment of glass eels to estuarine habitats are conducted for both temperate and tropical anguillid eel species. In this chapter, the early life history such as the timing and duration of metamorphosis, inshore migration period, age at recruitment and hatching date based on the otolith microstructure and microchemistry analyses in the anguillid eels are summarized. The results provided a basis for discussion on the larval migration mechanisms in the eels. Further, oceanic migration, evolution and distribution of Anguilla species are also discussed.

MATERIALS AND METHODS This chapter synthesizes information following publications regarding early life history of freshwater eels: A. anguilla (Lecomte-Finiger 1992, Wang and Tzeng 2000, Arai et al. 2000a, Kuroki et al. 2008), A. japonica (Cheng and Tzeng 1996, Arai et al. 1997), A. rostrata (Wang and Tzeng 1998, 2000, Arai et al. 2000a, Kuroki et al. 2008), A. australis (Arai et al. 1999b, Marui et al. 2001, Shiao et al. 2001, 2002), A. bicolor pacifica (Arai et al. 1999c, 2001), A. celebesensis (Arai et al. 1999d, 2001, 2003), A. marmorata (Arai et al. 1999d, 2001, 2002a, b, Robinet et al. 2003, Reveillac et al. 2008), A. bicolor

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bicolor (Arai et al. 1999d), A. reinhardtii (Shiao et al. 2002) and A. mossambica (Robinet et al. 2003, Reveillac et al. 2009). The methods for both otolith microstructure and microchemistry are described following Arai et al. (1997, 2001).

Otolith Preparation Sagittal otoliths were extracted from each fish, embedded in epoxy resin (Struers, Epofix) and mounted on glass slides. After the radius was measured, otoliths were ground to expose the core using a grinding machine equipped with a diamond cup-wheel (Struers, Discoplan-TS), and further polished with 6 µm and 1 µm diamond paste on an automated polishing wheel (Struers, Planopol-V). They were then cleaned in an ultrasonic bath and rinsed with deionized water for the following microchemical and microstructual examinations.

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Otolith X-Ray Microprobe Analysis For electron microprobe analyses, Sr and Ca concentrations were measured along the longest axis of the otolith using a wavelength dispersive X-ray electron microprobe. Calcite (CaCO3) and Strontianite (SrCO3) were used as standards. Accelerating voltage and beam current were 15 kV and 7 nA, respectively. The electron beam was focused on a point about 1µm in diameter, with measurements taken at 1µm intervals. Each datum point represents the average of three measurements of 4.0 seconds each. Microprobe measurement points were taken along a burn transect from the otolith core to the outer margin. The average of successive data of Sr and Ca concentrations were pooled for every 10 successive growth increments, and used for the lifehistory transect analysis.

Otolith Increment Analysis Following the electron microprobe analysis, the otoliths were etched with 0.05 M HCl and vacuum coated with Pt-Pd in an ion-sputterer for scanning electron microscope (SEM) observations. Otoliths that were not used for chemical analyses were also ground, the resulting surfaces being etched and

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coated by the same procedure as above for SEM observation. SEM photographs taken at various magnifications (150 x, 180 x, 1000 x, 1500 x) were used for counting the number of growth increments and measuring their width. The average of every 10 successive rings between the hatch check and the edge were used to analyze otolith growth. Based on the findings of Martin (1995), Arai et al. (2000b) and Sugeha et al. (2001a), the growth rings in Anguilla rostrata, A. celebesensis and A. marmorata were formed daily, the equivalent rings in other anguillid eel species were also considered to be formed daily.

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Early Life History Analyses

Figure 1. Conceptual model showing changes in otolith incremental widths and Sr:Ca ratios during the early life history of Anguilla spp.. Solid and broken lines represent increment widths and Sr:Ca ratios, respectively. Age at M indicates the timing of metamorphosis.

Based on previous data for otolith increment width and Sr:Ca ratios in Anguilla japonica (Arai et al. 1997), A. rostrata (Wang and Tzeng 1998, Arai et al. 2000a), A. australis (Arai et al. 1999b), A. bicolor pacifica (Arai et al. 1999c), A. celebesensis, A. marmorata and A. bicolor bicolor (Arai et al. 1999d), and A. anguilla (Arai et al. 2000a), age at Point M (Figure 1), at which a marked increase occurred in otolith increment width, coincident with a drop

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in Sr:Ca ratios, was regarded as the onset of metamorphosis in each species examined here.

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Figure 2. SEM photograph showing otolith growth increments of a glass eel. H: hatch check, E: otolith edge.

Duration of the metamorphosis stage was regarded as the period between the onset of a marked increase in otolith increment width and the maximum width recorded. The increments outside the maximum recorded otolith increment width were interpreted as representing the inshore migration period. The number of increments between the hatch check and otolith edge (Figure 2) was determined as the age at recruitment.

RESULTS Otolith Microstructure The otolith morphology of all glass eels in the anguillid eels was oval, similar to all species. The otolith core was observed as a deep hole in the center of the etched otolith surface, a hatch check being visible as a deep circular groove surrounding the hole (Figure 2). Distinct concentric growth increments were observed in all otoliths examined. These concentric rings were similar in configuration to those previously reported in A. anguilla

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(Lecomte-Finiger 1992; Wang and Tzeng 2000; Arai et al. 2000a, Kuroki et al. 2008), A. japonica (Cheng and Tzeng 1996, Arai et al. 1997), A. rostrata (Wang and Tzeng 1998, 2000; Arai et al. 2000a, Kuroki et al. 2008), A. australis (Arai et al. 1999b, Marui et al. 2001, Shiao et al. 2001, 2002), A. bicolor pacifica (Arai et al. 1999c, 2001), A. celebesensis (Arai et al. 1999d, 2001, 2003), A. marmorata (Arai et al. 1999d, 2002a, b, Robinet et al. 2003, Reveillac et al. 2008), A. bicolor bicolor (Arai et al. 1999d), A. reinhardtii (Shiao et al. 2002) and A. mossambica (Robinet et al. 2003, Reveillac et al. 2009). Although a metamorphosis check (Figure 2) was observed consistent with the onset of metamorphosis in A. anguilla (Lecomte-Finiger 1992) and A. japonica (Cheng and Tzeng 1996), such a check occurrence was different among species.

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Otolith Growth Pattern Patterns of change in otolith increment widths from the core to the edge relative to the life-history transects of each species are shown in Figure 3. The common pattern observed in all species comprised four phases with drastic changes occurring in the last two, similar to the patterns previously reported for all anguillid eel species. Otolith increment widths increased between the hatch check and age about 20-40 d in each species (first phase), thereafter becoming constant or gradually decreasing (average widths less than 0.5 µm) (second phase). Thereafter, increment widths increased sharply to a maximum (mostly more than 2 µm) (third phase), followed by a rapid drop (fourth phase).

Otolith Sr:Ca ratios Otolith Sr:Ca ratios changed dramatically along the life-history transect in all species (Figure 3), a common pattern of microchemical changes being observed in all of the glass eels. Sr:Ca ratios, averaging approximately 10 x 10-3 at the core, dropped slightly over what approximated the first phase of otolith growth, subsequently increased to a maximum level (average approximately more than 15 x 10-3) in the second phase and markedly decreased thereafter toward the edge.

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Figure 3. Profiles of otolith incremental widths from the core to the edge (circles) and otolith Sr:Ca concentration ratios measured with a wavelength dispersive electron microprobe from the core to the edge (triangles) in Anguilla marmorata (Arai et al. 2002). Each point represents the average of data for every 10 days. Numbers at the upper right indicate age (days). The dotted and straight lines indicate age at metamorphosis and age at termination of metamorphosis, respectively.

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Metamorphosis and Recruitment The last phase of changing Sr:Ca ratios coincided with the onset of the third phase of otolith growth. The minimum average Sr:Ca values were recorded in the outermost region of the otolith in each species. The ages at the onset of metamorphosis differed among all species and were greatest in A. anguilla (Table 1). In general, the temperate anguillid eels metamorphosed at greater ages than the tropical eels. The average age at recruitment also differed significantly among all the species and was greatest in A. anguilla. A. anguilla recruited to estuary at the oldest age, and A. bicolor bicolor at the youngest age (Table 1). The age at metamorphosis and ages at recruitment showed a similar linear relationship among eel species in that the individuals that metamorphosed at younger ages recruited at younger ages (Figure 4). In monthly observation, the mean ages at metamorphosis of tropical eels Anguilla celebesensis, A. marmorata and A. bicolor pacifica in each month ranged from 84 (October) to 95 d (February), 114 (June) to 158 d (August) and 129 (January) to 171 d (December), respectively (Arai et al. 2001). No significant difference was found among months in each species, although significant differences occurred in all combinations among species (Arai et al. 2001). Further, the mean ages at recruitment of Anguilla celebesensis, A. marmorata and A. bicolor pacifica in each month ranged from 104 (October) to 118 d (February), 144 (November) to 182 d (August) and 158 (January) to 201 d (December), respectively (Arai et al. 2001). No significant difference occurred among months in each species, while significant differences occurred in all combinations among species (Arai et al. 2001)). However, the earlier recruitment glass eels were younger and later recruitment individuals were older in temperate eel A. japonica (Kawakami et al. 1999).

Hatching Period In the studies of monthly observations, the estimated hatching dates, backcalculated from sampling date and ages were distributed throughout the year for Anguilla marmorata and similarly in A. celebesensis. The hatching dates ranged for six months in A. japonica.

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Table 1. Age at metamorphosis (days) of the anguillid eels genus Anguilla Species

Mean

Minimum

Maximum

Source

184

178

196

Lecomte-Finiger 1992

198

163

235

Arai et al. 2000a

350

319

397

Wang and Tzeng 2000

287

220

340

Kuroki et al. 2008

128

116

138

Cheng and Tzeng 1996

136

125

144

Kawakami et al. 1999

200

189

214

Wang and Tzeng 1998

156

132

191

Arai et al. 2000a

254

160

330

Kuroki et al. 2008

186

138

208

Arai et al. 1999b

174

160

189

Shiao et al. 2001

204

151

265

Marui et al. 2001

174

130

245

Shiao et al. 2002

241

189

294

Marui et al. 2001

124

104

147

Arai et al. 1999d

88

84

95

Arai et al. 2001

104

74

147

Arai et al. 2003

120

96

147

Arai et al. 1999d

128

114

158

Arai et al. 2001

146

112

183

Marui et al. 2001

122

92

155

Arai et al. 2002a

119

92

155

Arai et al. 2002b

97

60

135

Robinet et al. 2003

123

91

180

Reveillac 2008

Temperate species A. anguilla

A. japonica

A. rostrata

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A. australis

A. dieffenbachii Tropical species A. celebesensis

A. marmorata

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Early Life History and Recruitment Mechanisms … Species A. bicolor pacifica

Mean

Minimum

Maximum

Source

135

101

172

Arai et al. 1999c

141

129

171

Arai et al. 2001

161

132

208

Marui et al. 2001

139

119

171

Arai et al. 1999d

46

39

57

Robinet et al. 2003

A. reinhardtii

145

96

177

Shiao et al. 2002

A. mossambica

102

72

130

Robinet et al. 2003

93

64

152

Reveillac 2009

118

115

120

Robinet et al. 2003

A. bicolor bicolor

A. nebulosa labiata

101

Table 2. Age at recruitment (days) of the anguillid eels genus Anguilla Species

Mean

Minimum

Maximum

Source

237

191

276

Lecomte-Finiger 1992

249

220

281

Arai et al. 2000a

448

420

468

Wang and Tzeng 2000

336

260

416

Kuroki et al. 2008

166

155

182

Cheng and Tzeng 1996

175

143

206

Arai et al. 1997

171

150

188

Kawakami et al. 1999

255

220

283

Wang and Tzeng 1998

206

171

252

Arai et al. 2000a

319

248

365

Kuroki et al. 2008

235

186

266

Arai et al. 1999b

268

216

326

Marui et al. 2001

239

214

261

Shiao et al. 2001

229

169

317

Shiao et al. 2002

289

240

332

Marui et al. 2001

Temperate species Copyright © 2012. Nova Science Publishers, Incorporated. All rights reserved.

A. anguilla

A. japonica

A. rostrata

A. australis

A. dieffenbachii

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Takaomi Arai Table 2. (Continued)

Species

Mean

Minimum

Maximum

Source

157

130

177

Arai et al. 1999d

109

104

118

Arai et al. 2001

130

92

177

Arai et al. 2003

153

129

178

Arai et al. 1999d

155

144

182

Arai et al. 2001

174

147

219

Marui et al. 2001

153

116

189

Arai et al. 2002a

149

116

189

Arai et al. 2002b

120

86

160

Robinet et al. 2003

160

128

196

Reveillac 2008

167

124

202

Arai et al. 1999c

173

158

201

Arai et al. 2001

199

165

256

Marui et al. 2001

177

148

202

Arai et al. 1999d

80

68

96

Robinet et al. 2003

A. reinhardtii

183

140

227

Shiao et al. 2002

A. mossambica

124

96

151

Robinet et al. 2003

117

80

181

Reveillac 2009

144

143

145

Robinet et al. 2003

Tropical species A. celebesensis

A. marmorata

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A. bicolor pacifica

A. bicolor bicolor

A. nebulosa labiata

The duration of spawning season back-calculated from the daily age was also reported approximately six months for A. rostrata (March-October) and A. anguilla (November-July) (Wang and Tzeng 2000).

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DISCUSSION

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Metamorphosis and Recruitment Arai et al. (2001) suggested that age at metamorphosis and duration of the metamorphosis stage of the tropical eels, Anguilla celebesensis, A. marmorata and A. bicolor pacifica, were constant throughout the year regardless of differing recruitment seasons in each species. A. celebesensis, A. marmorata and A. bicolor pacifica leptocephali were determined as taking about 3 - 5 months to metamorphose after hatching. In temperate eels, for example, A. japonica, it has been reported that the earlier-hatching individuals are recruited to estuarine habitats relatively earlier in the recruitment season (Kawakami et al. 1999). In temperate eels, A. anguilla, A. rostrata and A. japonica, recruitment occurs over a limited period (winter and spring) (Matsui 1972, Tesch 2003), with the spawning period also being limited (Kawakami et al. 1999, Arai et al. 1999b, 2000a, Wang and Tzeng 1998, 2000). Individuals with earlier hatching dates and faster growth rates begin metamorphosis earlier, the age at metamorphosis therefore possibly changing as a result of the differences in time of spawning. By comparison, tropical eels, in which spawning persists throughout the year, have a constant age at recruitment throughout the year and most likely constant larval growth rates throughout the year. Ages at metamorphosis (duration of leptocephalus stage) of tropical eels, A. celebesensis (Arai et al. 1999d, 2001, 2003), A. marmorata (Arai et al. 1999d, 2001, 2002a, b, Robinet et al. 2003, Reveillac et al. 2008) A. bicolor pacifica (Arai et al. 1999c, 2001), A. bicolor bicolor (Arai et al. 1999d, Robinet et al. 2003) and A. mossambica (Robinet et al. 2003, Reveillac et al. 2009), were 1 to 11 months younger than those of temperate eels, A. anguilla (7-12 months) (Lecomte-Finiger 1992; Arai et al. 2000a, Wang and Tzeng 2000, Kuroki et al. 2008), A. rostrata (6 - 8 months) (Wang and Tzeng 1998; Arai et al. 2000a, Kuroki et al. 2008), A. australis (6 months) (Arai et al. 1999b) and A. dieffenbachii (8 months) (Marui et al. 2001), except for A. japonica (5 months) (Cheng and Tzeng 1996, Arai et al. 1997) (Table 1). The relationship between the timing of metamorphosis and age at recruitment clearly showed that glass eels metamorphosing earlier tended to migrate to a coastal region at a younger age, indicating that early metamorphosing larvae are recruited relatively sooner (Figure 4) in anguillid eel species (Arai et al. 1999a, b, c, d, 2000a, b, 2001, 20002a, b, 2003, Marui et al. 2001). These considerations suggest that timing of metamorphosis is a key factor in larval migration of anguillid eels.

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Figure 4. Relationship between age at metamorphosis (days) and age at recruitment (days) of Anguilla celebesensis glass eels collected from the coasts of Sulawesi Island Indonesia and the northern Philippines (Marui et al. 2001, Arai et al 2003).

The leptocephali of tropical and temperate eels probably experience different environmental temperatures during their migration from spawning areas to estuarine habitats. This would likely lead to differences in the timing of the onset and duration of metamorphosis. Typical vertical temperatures in open ocean waters at the surface and 200 m, where Anguilla leptocephali have been collected (Castonguay and McCleave 1987), are 20 to 25 °C in tropical areas and 10 to 20 °C in temperate areas (Apel 1987, Pickard and Emery 1990), the spawning areas of both tropical and temperate eels being in tropical areas (Schmidt 1925). The former experience high tropical temperature environments during migration, whereas the latter experience drastic changes in temperature environments during migration. Lower temperature environments may lead to those slower growth in the latter, resulting in delayed metamorphosis. Subsequently, those species may be transported for greater distances in temperate areas. Ages at recruitment of Anguilla celebesensis, A. marmorata and A. bicolor pacifica were constant throughout the year in each species, possibly a result of the constant age at the onset of metamorphosis throughout the year (Arai et al. 2001).

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The differences in age at recruitment among the species, 4 months in A. celebesensis, 5 months in A. marmorata and 6 months in A. bicolor pacifica, might be due to the differences in age at the beginning of metamorphosis of each. Furthermore, ages at recruitment of those tropical eels with A. bicolor bicolor (Arai et al. 1999d, Robinet et al. 2003) and A. mossambica (Robinet et al. 2003) were 1 to 12 months less than those of temperate eels, A. anguilla (815 months) (Lecomte-Finiger 1992; Arai et al. 2000a), A. rostrata (7 - 8 months) (Wang and Tzeng 1998; Arai et al. 2000a), A. australis (7 months) (Arai et al. 1999b) and A. dieffenbachi (10 months) (Marui et al. 2001), respectively, except for A. japonica (6 months) (Cheng and Tzeng 1996, Arai et al. 1997) (Table 1). This may be a result of the ages at metamorphosis in the former being 1 to 11 months less than in the latter.

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Hatching The spawning seasons of Anguilla celebesensis and A. marmorata were found to extend throughout the year (Arai et al. 2001). A. bicolor pacifica was estimated to be about six months (Arai et al. 2001). Based on occurrence in the monthly samples, glass eels of that species have been found throughout the year (Sugeha et al. 2001b), and early life history parameters such as duration of the leptocephalus stage and age at recruitment being found to be constant throughout the year (Arai et al. 2001), the spawning season of A. bicolor pacifica may occur throughout the year. In temperate species spawning occurs over a limited period, i. e. February to April in A. rostrata (McCleave aet al. 1987), March to June in A. anguilla (McCleave et al. 1987), July to November in A. japonica (Kawakami et al. 1999), August to December in A. dieffenbachii (Jellyman 1987) and September to February in A. australis (Jellyman 1987). The difference in spawning season duration and timing between tropical and temperate species might be due to differences in the seaward migration seasons of maturing adult eels. The temperate species are known to start spawning migrations over a limited period, August to November in A. rostrata (Hain 1975), August to December in A. anguilla (Haraldstad et al. 1985), August to December in A. japonica (Matsui 1952), April to May in A. dieffenbachi (Jellyman 1987) and February to April in A. australis (Jellyman 1987). In the tropical species, such may occur throughout the year related to yearround spawning, although nothing is known yet of seaward migration seasons

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of tropical maturing adult eels. Year-round spawning of tropical species and constant larval growth throughout the year may extend the period of recruitment to estuarine habitats to year-round in tropical eel species, as found in previous studies (Tabeta et al. 1976, Arai et al. 1999a, Arai 2001).

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Oceanic Migration The tropical anguillid eel species including Anguilla celebesensis, A. marmorata, A. bicolor pacifica, A. bicolor bicolor and A. mossambica were determined as taking about 2 - 6 months to migrate from their spawning areas to estuarine habitats (Arai et al. 1999a, b, c, d, 2001, 2002a, b, 2003, Marui et al. 2001, Robinet et al. 2003). In temperate eels, the duration of oceanic migration seems to be related to the distance and complexity of the current systems between the spawning areas and their freshwater destinations. According to Jespersen (1942), the spawning areas of tropical eels, including A. bicolor bicolor and A. celebesensis from Indonesia, distributed off Java and the North Sulawesi Islands, respectively, were possibly situated off the southwestern coast of Sumatra for the former and the Celebes Sea for the latter, both being close to their distribution areas. Recently, Aoyama et al. (2003) have conducted to collect small leptocephali from around Sulawesi, Indonesia, and have used species-specific genetic markers to identify them as larvae 12 A.marmorata (34.0–50.7 mm in total length and one glass eel of 47.8 mm), 41 A. celebesensis (13.0–47.8 mm), 3 A. borneensis (8.5, 13.0, 35.4 mm), 4 A. bicolor (42.6–49.2 mm), and 1 A. interioris (48.9 mm), which provides the first definitive information about the general spawning areas of these tropical eels. Of particular interest the study were the small leptocephali of A. borneensis that were 8.5 and 13.0 mm with age of about 16 and 26 days after hatching, which were collected in the Celebes Sea to the east of Borneo Island, and the specimen (35.4 mm) that was collected to the south in Makassar Strait, where water from the Celebes Sea is transported. The freshwater growth habitat of A. borneensis is limited to the east-central part of Borneo (Ege 1939), which strongly suggests that this species spawns in the Celebes Sea and then migrates back to its growth habitat adjacent to the spawning area. Another tropical anguillid species, Anguilla celebesensis, has a wider distribution that extends from Luzon Island of the Philippines to across Sulawesi Island. Interestingly, the small leptocephali of this species collected about 25 days after hatching were found in two different seasons and in two different areas separated by the northern arm of Sulawesi (Aoyama et al.

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2003). Further, the collection of nine A. celebesensis in Tomini Bay ranged in total length from 13 to 48.9 mm (fully grown larval stage). These facts indicate that individuals of A. celebesensis inhabiting the watershed of Tomini Bay spawn over a relatively long period and that their leptocephali are retained in Tomini Bay. The distances between possible spawning area and the freshwater distribution (recruitment area) for the tropical eels A. celebesensis and A. borneensis were 80-300 km and 480-650 km, respectively (Aoyama et al. 2003). However, those in temperate eels A. anguilla (McCleave et al. 1987), A. rostrata (McCleave et al. 1987) and A. japonica were 4000-8000 km, 900-5500 km and 2000-3500 km, respectively. This discrepancy between tropical and temperate eels related to distance between spawning area and their freshwater distribution indicate that, in contrast to the long migrations made by temperate eels, tropical eels make much shorter migrations to spawn in areas near their freshwater habitats. The occurrence of leptocephali of various sizes and stages, including preleptocephalus to metamorphosing stages and oceanic glass eel stage, in waters off Sumatra (Jespersen 1942) and Tomini Bay (Aoyama et al. 2003) support that supposition. This situation is quite different to that of temperate eels, suggesting that the migration mechanisms of tropical eel larvae are not as simple as those of temperate eels. The spawning areas of the genus Anguilla are all located in tropical regions (Schmidt 1925), indicating that freshwater eels may have originated in the tropics. Leptocephali have a long duration (2 - 12 months) and appear to be highly adapted to a marine planktonic life. As the result of their slow growth and passive transport by oceanic currents and wind, it is likely that global dispersal of freshwater eels might have occurred from the Indonesian region. Accidental drift of larvae in a global circum-equatorial current and variations in early development may have resulted in a variation of the larval phase, that is, expansion of their growth habitat. For temperate eels, retention of their spawning areas in the tropics would require their migrating thousands of kilometers.

CONCLUSION The early life history parameters found in all tropical species were overlapped with the range of those in a temperate species, Anguilla japonica, although the former was a little shorter than those of A. anguilla, A. rostrata, A. australis and A. dieffenbachii. A. celebesensis, A. marmorata and A. bicolor bicolor leptocephali were defined to take about 3 - 6 months to migrate from

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their spawning area to the estuarine parts, and A. bicolor bicolor pacifica took also same period in the previous study (Arai et al. 1999c). In temperate eels, which migrate via oceanic current systems (Schmidt 1922, 1925, Tsukamoto 1992), the duration of oceanic migration seems to be related to the distance and complexity of the current systems between the spawning areas and their destinations to freshwater habitats.

Figure 5. Conceptual model showing the scenario of evolutionary pathway of the oceanic migration in the anguillid eels genus Anguilla. The ancestral eels most likely underwent diadromous migration from a local short distance movement in complex currents in tropical coastal waters, subsequently developing the long distant migration characteristic of present-day temperate eels, well-established as occurring in a subtropical gyre in both hemispheres.

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The spawning areas of tropical eels are possibly situated close to their distribution area. Therefore, the rather long migration period of those species relative to short distance between growth habitat and spawning area may due to the complicated local current systems around spawning areas. The occurrence of leptocephali of various sizes including even preleptocephalus to metamorphosing stages and glass eel in the waters (Jespersen 1942, Aoyama et al. 2003) support that supposition. This situation is quite different from those of temperate eels, suggesting that the migration mechanisms of tropical eel larvae is not so simple as those of temperate eels which can be interpreted as simple transportation by stable current systems. These results all lead to the conclusion that ancestral eels most likely underwent diadromous migration from a local short distance movement in complex currents in tropical coastal waters, subsequently developing the long distant migration characteristic of present-day temperate eels, well-established as occurring in a subtropical gyre in both hemispheres (Figure 5).

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from Australia and New Zealand, as revealed by otolith microstructure and microchemistry. Marine Biology 135: 381-389. Arai, T., Aoyama, J., Limbong, D. and Tsukamoto, K. (1999a) Species composition and inshore migration of the tropical eels, Anguilla spp., recruiting to the estuary of the Poigar River, Sulawesi Island. Marine Ecology Progress Series 188: 299-303. Arai, T., Limbong, D. and Tsukamoto, K. (2000b) Validation of otolith daily increments in the tropical eel, Anguilla celebesensis. Canadian Journal of Zoology 78: 1078-1084. Arai, T., Otake, T. and Tsukamoto, K. (2000a) Timing of metamorphosis and larval segregation of the Atlantic eels Anguilla rostrata and A. anguilla, as revealed by otolith microstructure and microchemistry. Marine Biology 137: 39-45. Arai, T., Limbong, D., Otake, T. and Tsukamoto, K. (2001) Recruitment mechanisms of tropical eels, Anguilla spp., and implications for the evolution of oceanic migration in the genus Anguilla. Marine Ecology Progress Series 216: 253-264. Arai, T., Marui, M., Miller, M. J. and Tsukamoto, K. (2002a). Growth history and inshore migration of the tropical eel, Anguilla marmorata in the Pacific. Marine Biology 140: 309-316. Arai, T., Marui, M., Otake, T. and Tsukamoto, K. (2002b) Inshore migration of a tropical eel, Anguilla marmorata, from Taiwanese and Japanese coasts. Fisheries Science 68: 152-157. Arai, T., Miller, M. J. and Tsukamoto, K. (2003) Larval duration of the tropical eel, Anguilla celebesensis, from the Indonesian and Philippine coasts. Marine Ecology Progress Series 251: 255-261. Castle, P. H. J. and Williamson, G. R. (1974) On the validity of the freshwater eel species Anguilla ancestralis Ege from Celebes. Copeia 2: 569-570. Castonguay, M. and McCleave, J. D. (1987). Vertical distributions, diel and ontogenetic vertical migrations, and net avoidance of leptocephali of Anguilla spp. and other common species in the Sargasso Sea. Journal of Plankton Research 9: 195-214. Cheng, P. W. and Tzeng, W. N. (1996) Timing of metamorphosis and estuarine arrival across the dispersal range of the Japanese eel Anguilla japonica. Marine Ecology Progress Series 131:87-96. Ege V (1939) A revision of the Genus Anguilla Shaw. Dana Report 16: 8-256. Hain, J. H. W. (1975) The behavior of migratory eels, Anguilla rostrata, in response to current, salinity and lunar period. Helgoländer Meeresunters 27: 211-233.

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Haraldstad, O., Vollestad, L. A. and Jonsson, B. (1985) Descent of European silver eels, Anguilla anguilla L., in a Norwegian watercourse. Journal of Fish Biology 26: 37-41. Jellyman, D. J. (1987) Review of the marine life history of Australasian temperate species of Anguilla. American Fisheries Society Symposium 1: 276-285. Jespersen, P. (1942) Indo-Pacific leptocephali of the Genus Anguilla. Dana Report 22: 1-128. Kuroki, M., Kawai, M., Jonson, B., Aoyama, J., Miller, M. J., Noakes, D. L. G. and Tsukamoto, K. (2008) Inshore migration and otolith microstructure/microchemistry of anguillid glass eels recruited to Iceland. Environmental Biology of Fishes 83: 309-325. Kawakami, Y., Mochioka, N. and Nakazono, A. (1999) Immigration Patterns of Glass-eels Anguilla japonica entering river in northern Kyushu, Japan. Bulletin of Marine Science 64 : 315–327. Lecomte-Finiger, R. (1992) Growth history and age at recruitment of European glass eels (Anguilla anguilla) as revealed by otolith microstructure. Marine Biology 114:205-210. Martin, M. H. (1995) Validation of daily growth increments in otoliths of Anguilla rostrata (Lesueur) elvers. Canadian Journal of Zoology 73: 208211. Marui, M., Arai, T., Miller, M.J., Jellyman, D. J. and Tsukamoto, K. (2001) Comparison of early life history between New Zealand temperate eels and Pacific tropical eels revealed by otolith microstructure and microchemistry. Marine Ecology Progress Series 213: 273-284. Matsui, I. (1952) Morphology, ecology and culture of the Japanese eel. Journal of the Shimonoseki University of Fisheries 2: 1-245. Matsui, I. (1972) Eel Biology - Biological Study. Koseisha-Koseikaku, Tokyo. McCleave, J. D., Kleckner, R. C. and Castonguay, M. (1987) Reproductive sympatry of American and European eels and implications for migration and taxonomy. American Fisheries Society Symposium 1: 286-297. Minegishi, Y., Aoyama, J., Inoue, J. G., Miya, M., Nishida, M. and Tsukamoto, K. (2005) Molecular phylogeny and evolution of the freshwater eels genus Anguilla based on the whole mitochondrial genome sequences. Molecular Phylogenetics and Evolution 34:134–146. Pickard, G. L. and Emery, W. J. (1990) Descriptive physical oceanography. Pergamon Press, Oxford. Re´ veillac, E., Feunteun, E., Berrebi, P., Gagnaire, P. A., Lecomte-Finiger, R., Bosc, P. and Robinet, T. (2008) Anguilla marmorata larval migration

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plasticity as revealed by otolith microstructural analysis. Canadian Journal of Fisheries and Aquatic Sciences 65, 2127–2137. R´eveillac, E., Robinet, T., Rabenevanana, M. W., Valade, P. and Feunteun, E. (2009) Clues to the location of the spawning area and larval migration characteristics of Anguilla mossambica as inferred from otolith microstructural analyses. Journal of Fish Biology (2009) 74, 1866–1877. Robinet, T., Lecomte-Finiger, R., Escoubeyrou, K. and Feunteun, E. (2003). Tropical eels Anguilla spp. recruiting to Reunion Island in the Indian Ocean: taxonomy, patterns of recruitment and early life histories. Marine Ecology Progress Series 259: 263–272. Schmidt J (1922) The breeding places of the eel. Philosophical Transactions of the Royal Society (Ser B) 211: 178-208. Shiao, J. C., Tzeng, W. N., Collins, A. and Jellyman, D. J. (2001). Dispersal pattern of glass eel stage of Anguilla australis revealed by otolith growth increments. Marine Ecology Progress Series 219: 241–250. Schmidt J (1925) The breeding places of the eel. Annual Report of the Smithsonian Institution 1924: 279-316. Shiao, J. C., Tzeng, W. N., Collins, A. and Iizuka, Y. (2002). 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. Marine and Freshwater Research 53: 687–695. Sugeha, H. Y., Arai, T., Miller, M. J., Limbong, D. and Tsukamoto, K. (2001b) Inshore migration of the Tropical eels Anguilla spp. recruiting to the Poigar River estuary on north Sulawesi Island. Marine Ecology Progress Series 221: 233-243. Sugeha, H. Y., Shinoda, A., Marui, M., Arai, T. and Tsukamoto, K. (2001a) Validation of otolith daily Increments in the tropical eel Anguilla marmorata. Marine Ecology Progress Series 220:291-294. Tabeta, O., Tanimoto, T., Takai, T., Matsui, I. and Imamura, T. (1976) Seasonal occurrence of anguillid elvers in Cagayan River, Luzon Island, the Philippines. Bulletin of the Japanese Society of Scientific Fisheries 42: 421-426. Tabeta, O., Tanaka, K., Yamada, J. and Tzeng, W. N. (1987). Aspects of the early life history of the Japanese eel Anguilla japonica determined from otolith microstructure. Bulletin of the Japanese Society of Scientific Fisheries 53:1727-1734. Tesch, F. W. (2003) The Eel. Biology and management of anguillid eels. London, Chapman and Hall.

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Wang, C. H. and Tzeng, W. N. (1998) Interpretation of geographic variation in size of American eel Anguilla rostrata elvers on the Atlantic coast of North America using their life history and otolith ageing. Marine Ecology Progress Series 168: 35-43. Wang, C.H. and Tzeng, W.N. (2000) The timing of metamorphosis and growth rates of American and European eel leptocephali: a mechanism of larval segregative migration. Fisheries Research 46: 191–205.

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In: Eels Editors: N. Sachiko and M. Fujimoto

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Chapter 5

QUALITY AND VITAMIN CONTENT OF EGGS OF JAPANESE EEL ANGUILLA JAPONICA Hirofumi Furuita,1,* Hiroyuki Matsunari1 and Takeshi Yamamoto2

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1

National Research Institute of Aquaculture, Fisheries Research Agency, Minami-ise, Japan 2 Tamaki Station, National Research Institute of Aquaculture, Fisheries Research Agency, Tamaki, Japan

ABSTRACT This chapter describes the relationship between egg vitamin concentrations and egg quality and techniques to improve vitamin levels and quality of eggs in artificially matured Japanese eel Anguilla japonica. Hatching and survival rates of larvae significantly increased with elevated levels of egg vitamin C (VC). In contrast to VC, the relationship between vitamins E (VE) and A (VA) and survival rate showed a clear peak, with reduced survival rates at both higher and lower vitamin concentrations. The ratio of VE to lipid or highly unsaturated fatty acid (HUFA) in eggs positively correlated with hatching and survival rates of larvae. Therefore, techniques to increase egg VC and VE levels were investigated, since increasing these vitamins in eggs was expected to improve egg quality of the eel. Supplementation of VC and VE in the *

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Hirofumi Furuita, Hiroyuki Matsunari and Takeshi Yamamoto broodstock diet, however, did not effectively improve the vitamin concentration and quality of eggs of eel, although in some species supplementation of vitamins to diets of broodstock improves egg quality. In order to improve the egg quality of eel, the effects of direct injection of VC and VE into broodstock during artificial maturation on the vitamin levels of broodstock and eggs and subsequent egg and larval quality was investigated. The levels of both vitamins in eggs and broodstock increased following vitamin injection. Hatching rate, survival and normality of larvae increased with vitamin treatments. Further, combination of supplementation to diet and injection of the vitamins were investigated. Treatment of vitamins to the diet alone significantly increased the egg vitamin level, but did not improve egg quality. Combination of dietary treatment and injection of the vitamins significantly improved both the vitamin level and quality of eggs, compared to the dietary treatment alone and no-vitamin treatment groups. These results suggest that VC and VE concentrations of eggs is one of the factor determining egg quality, and that supplementation of these vitamin to broodstock, especially via vitamin injections, effectively improves egg quality in Japanese eel.

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1. INTRODUCTION Since techniques for mass production of high quality glass eels have not yet been firmly established, all fry used for cultivation of Japanese eel are wild elvers, although eel is the most important cultured freshwater species and its production is almost 20 000 tons in Japan. Egg quality is the limiting factor for the successful production of the eel fry (Tanaka et al., 2003). Several parameters exist for the determination of egg quality. The biochemical composition of eggs is one of the factors determining egg quality since eggs must contain all the nutrients required for normal development during embryonic and yolk-sac larval stages. Several nutrients such as vitamins and essential fatty acids (EFA) have been suggested to be related to egg quality in both freshwater and marine fishes (Watanabe, 1985). In order to obtain an optimum level of each nutrient in eggs, it is necessary to feed broodstock with diets having an optimum composition since egg nutrient concentrations reflect the broodstock nutritional status (Watanabe et al., 1984; Furuita et al., 2000). However, little is known about the interaction between egg quality and egg biochemical composition in Japanese eel. More information on the relationship between egg composition and egg quality is needed for the improvement of egg quality.

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Vitamins have important roles in reproduction and development of fish as well as mammals. High concentrations of vitamin C (VC) in fish ovaries have been reported by many authors. The overall high levels of and seasonal variations of VC in ovaries have been suggested to reflect the requirement of VC in hydroxylation reaction in steroidogenesis in the ovarian follicle cells (Sandnes, 1991). High levels of vitamin E (VE) have been also found in ovaries of several fish species. The VE concentration is generally high in fish eggs and low in broodstock tissues after the spawning period, suggesting the importance of VE in eggs (Hamre, 2011). Vitamin A (VA) is also considered important for embryonic and larval development due to its important role in bone and retinal development, and differentiation of immune cells (Izquierdo et al. 2001). This chapter describes the relationship between egg quality and egg vitamins, with emphasis on VA, VC, and VE, and techniques to improve egg vitamin levels and the subsequent egg quality by supplementation of vitamins to broodstock in Japanese eel.

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2. EGG QUALITY AND EGG VITAMINS Vitamins are classified into two types, water-soluble and fat-soluble vitamins. The former includes VC, and VA and VE are included in the latter. The fat-soluble vitamins differ from the water-soluble vitamins in their accumulative properties. Little evidence has been reported for hypervitaminosis with water-soluble vitamins, since these compounds are rapidly metabolized and excreted when intake exceeds the tissue storage capacity, but hypervitaminosis commonly occurrs in fish when large quantities of fat-soluble vitamins are ingested (Halver and Hardy, 2002). The different modes in accumulation between water-soluble and fat-soluble vitamins affect patterns between egg quality and vitamin levels in eggs of Japanese eel.

2.1. Fertility and Vitamins The relationship between the vitamin concentration and egg quality depends on the type of vitamin, or the egg quality parameter in the eel. An improved fertilization rate was observed with elevated levels of VE in eggs when the egg VE concentration was relatively low (Furuita et al., 2003). However, no clear relationship was found between the fertilization rate and

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VE, when eggs contained VE at levels higher than 200 μg/g (Furuita et al., 2009b). Diets deficient in VE show a decreased percentage of egg buoyancy in gilthead seabream Sparus aurata, and viability of eggs in red seabream Pagrus major (Fernandez-Palacios et al., 2011). On the other hand, VA and VC have no clear relationship with fertilization rate. These results suggest that a moderate level of VE is one of the factors for the improvement of fertilization rate, and that VA and VC in eggs have no effect on fertilization rate in Japanese eel. In other fish species such as sea bass Dicentrarchus labrax and gilthead seabream, supplementation of VC to broodstock diet increased egg VC level, but fertility was not different between VC supplemented and nonsupplemented groups. Fertility does not seem to be influenced much by nutrient contents in eggs (Terova et al., 1998), whereas supplementation of VC to male broodstock diet increases fertility, and seminal plasma ascorbate concentration seems to concern with fertility in fish (Dabrowski and Ciereszko, 2001). VE deficiency in male fish is also suggested to decrease fertility related to number and motility of the spermatozoa (FernandezPalacios et al., 2011). In Japanese eel, effects of these vitamins in males on motility of spermatozoa and fertility have not been investigated.

2.2. Hatching, Survival and Vitamins Hatching rate showed no correlation with VA in eggs as well as fertilization rate. Survival rate of larvae at 8 DPH (days post hatching, first feeding larvae) tended to decrease with an increase of VA in case of high VA levels, indicating high VA level negatively affects larval survival (Furuita et al., 2009b). The necessity of VA for growth and embryonic development is well known and the effect on larval development has been documented in flatfish (Fernandez and Gisbert, 2011). The requirement of VA-active compounds for cellular functions is generally ascribed to their role as physiological regulation of cell growth and differentiation. Survival rate of 3 day-old larvae is significantly improved by supplementation of VA in bighead carp Aristichthys nobilis (Santiago and Gonzal, 2000). Additional VA to the diet of flounder improves normality in skin color of the ocular side. However, excess VA in feed for larvae of flatfish induces skeletal deformity (Fernandez and Gisbert, 2011). It is also suggested that a deficient or excess level of VA in eel eggs tends to depress hatching and survival rates. Relationship between VE in eggs and hatching and survival rates showed a similar tendency with that between VA and egg quality. The relationship

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between VE concentration and hatching rate or survival rate of eel larvae showed a clear peak at ca. 200μg/g with lower rates at both higher and lower VE concentrations, suggesting that a deficiency or excess of VE in eggs depresses hatching and survival rates (Figure 1). That is, it is necessary that eggs contain the optimum level of VE to produce larvae which have high hatching and survival rates, the same as VA (Furuita et al., 2009b). VE acts as antioxidant nutrient in the lipid phase. It is well known that the requirement of VE increases with the increase of lipid or polyunsaturated fatty acids. Fish eggs are usually rich in VE to prevent tissues from oxidative effects since eggs contain a high level of HUFA. Ratios of VE to lipid and HUFA positively correlated with all egg quality parameters examined in the eel, but no notable difference was found by the regression analysis between VE/HUFA ratio and any egg quality parameters of eel (Furuita et al., 2009b). However, the ratios of VE to lipids or HUFA in eggs were significantly higher in high quality eggs (with hatching rate > 80 %) than in low quality eggs (unable to hatch), although there was no significant difference in the VE level between high quality eggs and low quality eggs (Furuita et al., 2009b). This indicates that VE plays important roles in protecting the embryos of the eel against oxidation by free radicals since HUFA is easy oxidized. Eel eggs are rich in lipids (>40%, d.b.; Furuita et al., 2003) compared to pelagic eggs of other species; 20-32 % for Japanese flounder Paralichthys olivaceus (Furuita et al., 2000; 2002); 22-31 % for red seabream Pagrus major (Watanabe et al., 1985); 19-25 % for gilthead seabream (Almansa et al., 1999). This indicates that anti oxidative nutrients are more important in eel eggs than other fish eggs for preventing lipids or HUFAs from oxidation. Fontagne et al. (2008) demonstrated an active anti-oxidant system exists in developing rainbow trout until yolk-sac absorption, from the changes in gene expression of major antioxidant enzymes. Since the mRNA expressions could be influenced by oxidized lipids, it would not be surprising if the status of anti-oxidants could impact the enzyme activities and thereby the overall antioxidant capacity. However, negative effects of high levels of VE on egg quality were observed. Therefore, it is necessary to take care that excess levels of VE in eggs as well as deficiency does not occur for optimal egg quality using egg VE concentration in the eel. On the other hand, VC concentration in eggs showed a different pattern from VA or VE in correlation with hatching and survival rates (Figure 2). Increased hatching and survival rates were found with elevated levels of VC in eggs. The hatching rate of eggs was positively correlated with the VC concentration, and a more significant correlation was found between the

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survival rate and the VC level (Furuita et al., 2009b). VC acts as a cofactor of certain enzymes, which catalyzes the hydroxylation of proline and lysine in the procollagen molecule, contributing to bone and skin formation and thereby to growth (Sandnes, 1991). Low maternal input of VC to eggs produces larvae with spinal deformities. Low hatchability was reported in tilapia Oreochromis mossambicus and rainbow trout Oncorhynchus mykiss when females were fed a diet without VC, as VC was deficient in eggs (Sandnes et al., 1984; Soliman et al., 1986).

Figure 1. Relationship between vitamin E (VE) concentration in eggs and survival rate at the first feeding of Japanese eel.

Figure 2. Relationship between vitamin C (VC) concentration in eggs and survival rate at the first feeding of Japanese eel.

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Sea bass eggs from broodstock fed a diet with VC sufficient for normal growth showed a lower VC concentration than eggs from fish that were fed a diet with an extra addition of VC (Terova et al., 1998). However, they showed that egg quality parameters, such as fertilization and hatching rate did not show significant differences between treatments (Terova et al., 1998). In eel, it was found that the egg VC concentration correlated with hatching and survival rates although there was no notable relation between VC and fertilization rate. Terova et al. (1998) mentioned that the optimum dietary level of VC for normal growth might not be sufficient for broodstock when the goal is the transfer of VC to the embryos. Survival rate of 3 day-old larvae from broodstock fed a VC deficient diet was significantly lower than that from fish fed a VC supplemented diet although no notable difference was found in fertilization and hatching rates in bighead carp (Santiago and Gonzal, 2000). No significant effect of ascorbate was found on fertilization rate and survival of embryos in Atlantic cod (Mangor-Jensen et al. 1994). On the other hand, Sandnes et al. (1984) reported that an increased number of females with high progeny survival rates occurred with increased concentrations of ascorbic acid in eggs of rainbow trout. VC seems to be more important for larval survival than for embryogenesis, but this seems to depend on the fish species. Interactions between VE and VC are observed in fish and mammals. The regeneration of VE from the tocopheryl radical by VC has been well characterized by in vitro studies (Mukai et al., 1991). VC deficiency developed earlier in Atlantic salmon Salmo salar fed a high amount of VE. Thus, high levels of VE appear to have prooxidant effects when VC is low (Hamre, 2011). These indicate that fish eggs need to contain a high level of VC as an anti-oxidant vitamin, in addition to functioning for steridogenesis and as a cofactor in enzyme pathways, since fish eggs contain high levels of VE. Furuita et al. (2009b) found that eggs contained high levels of VE showed lower VC levels in eel. Although it is unclear whether low VC concentration had a relation with high level of VE or not, low VC concentrations may affect the quality of eggs containing high VE, in addition to the effects of excess VE.

3. IMPROVEMENT OF EGG QUALITY 3.1. Supplementation of Vitamins to Broodstock Diet VC and VE concentrations in eggs are shown as possible factors determining egg quality in Japanese eel; e.g., eggs with a low VC or VE

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concentration had low hatchability and productivity of the larvae at the first feeding stage (Furuita et al., 2009b). Several studies have demonstrated that the composition of diet for broodstock greatly affects their egg quality and biochemical composition (Watanabe, 1985; Izquierdo et al., 2001). Addition of vitamins to broodstock diet increases the vitamin level in eggs and improves the egg quality in gilthead seabream and rainbow trout (Izquierdo et al., 2001). These results suggest that supplementation of VC and VE to the diet for eel broodstock before spawning may increase the VC and VE concentration in eggs and result in an improvement of egg quality. In batch spawners with up to 6 months of vitellogenesis, such as salmonids, broodstock must be fed a good quality diet for several months before the spawning season to improve their reproductive performance (Izquierdo et al., 2001). In repeat spawners with short vitellogenesis periods, such as red seabream and gilthead seabream, egg quality is influenced by feed quality fed to broodstock both before and during the spawning period (Izquierdo et al., 2001). As eel broodstock do not feed during the period of artificial maturation which requires a period of 2-3 months, improvement of egg quality is expected by feeding eel broodstock with a diet supplemented with VC and VE for several months before induction of maturation. However, no egg quality parameter was improved, although broodstock were fed a VC and VE supplemented diet for 3 months before induction of maturation (Furuita et al., unpublished data). VE levels in eggs and liver increased with elevated level of dietary VE. Feeding broodstock with a VC-supplemented diet, unexpectedly, did not increase the egg VC concentration. VC is not stored in large amounts in fish tissue if additional VC is fed to broodstock, since VC is a water-soluble vitamin. It is suggested that the vitamins, especially VC, which had been accumulated in eel broodstock before maturation may have been consumed prior to spawning (Yoshikawa, 1998). It is known that stress to fish increases VC and VE requirement. For instance, requirement of VC in channel catfish Ictalurus punctatus increased in high stocking density (Sandnes, 1991). High serum lysozyme activity and lowered serum alternative complement pathway (ACP) caused by crowded stress were normalized by high dietary VC and VE in gilthead seabream (Hamre, 2011). Eel broodstock are induced to maturation by injections of hormone weekly for ca. 10 weeks of induction of maturation. Stress induced by weekly injections may lead to consumption of vitamins stored in broodstock and results in low vitamin concentrations in eggs even if they received extra vitamins before induction of maturation. This suggests that improvement of techniques for vitamin supplementation to eel broodstock is

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required, different from feeding with vitamin-enriched diet used in other fish species.

3.2. Injection of Vitamins into Broodstock

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3.2.1. Effect on Egg Quality Supplementation of VC and VE to broodstock diet did not improve egg quality of eel, although VC and VE levels in eggs is one of the factors influencing egg quality of eel. Thiamin deficiency, termed Cayuga Syndrome, causes reproductive failure in landlocked Atlantic salmon (Fisher et al., 1996). Maternal blood and egg thiamin levels correlated with larval survival of Atlantic salmon. Wooster et al. (2000) showed remediation of Cayuga Syndrome by bath treatment in thiamin hydrochloride. It is also found that injection of thiamin into adult females were more effectively improved egg thiamin levels than immersion of eggs in a thiamin solution (Fitzsimons et al., 2005). These findings indicate that injection of deficient nutrients into female eel can effectively increase the vitamin level in eggs and improve egg and larval quality.

Figure 3. Effect of vitamin injection on egg quality of eel. Control, no vitamin injection; Early; vitamin injected during early part of artificial maturation; Latter, vitamin injected during latter part of artificial maturation.

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Injection of vitamins into eel broodstcok during artificial induction of maturation was conducted by Yoshikawa (1998) and resulted in increase of VC and VE in broodstock liver and muscle. This result suggests the possibility to improve egg quality following the increase of vitamin content in eggs by VC and VE injection into broodstock. Yoshikawa (1998), however, did not examine the effect of the injection of vitamins on egg vitamin levels and egg quality, because he could not obtain fertilized eggs in the experiment. Furuita et al. (2009a) demonstrated that injection of a VC and VE emulsion into eel broodstock during artificial maturation increases vitamin levels in eggs and subsequent egg quality (Figure 3). The fertilization rate was not different among treatments irrespective of vitamin injection. Importance of vitamins for hatching and survival of eel, which was observed in the relationship between egg quality and egg vitamin levels, was confirmed in the vitamin injection experiment.

3.2.2. Vitamin Level in Broodstock and Eggs Both VC and VE concentrations in the liver and the muscle were significantly increased by vitamin injection. However, the extent of the accumulation in broodstock was larger in VE than in VC, although the same amount of both vitamins was injected. In addition, variation in concentration was larger in VC than in VE. Egg VE concentration was correlated with that of the muscle of broodstock, but no correlation was found for VC concentration between eggs and muscle or liver. However, no significant correlation was found between egg quality parameters and vitamin concentrations in eggs or muscle. In addition, eggs having high quality in the vitamin treated groups, however, did not always contain the vitamin at higher levels than in the control group. On the other hand, the VC content of the liver was positively correlated with larval survival and normality, suggesting that the maternal VC level can be an indicator of egg quality as well as the egg VC level. Broodstock in the control group had a significantly lower VC level in the liver and the muscle than in the vitamin treatment groups even if the eggs of the control group contained VC at relatively high levels. Dabrowski et al. (1995) found that the concentration of testosterone, which is an important female hormone, at the time of ovulation in rainbow trout decreased with reduced intake of dietary VC. It would be most intriguing to analyze differences in estrogen concentration in concert with ascorbic acid during fish vitellogenesis as cytochrome P450 aromatases in microsomes are VC dependent in mammals (Kanazawa et al., 1991). This suggests that VC deficiency in female eels reduces the production of important hormones for

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reproduction and fish may ovulate eggs that are either unripe or over ripe, which induces lower egg quality, even if the eggs have high VC. VE content in eggs or broodstock did not have a relation to egg quality in the vitamin injection experiment. This is because the eggs of the control contained relatively high VE, at a level which is considered to satisfy the minimum VE content for high egg quality of the eel (Furuita et al., 2009a,b). It seems that VE in eggs is not deficient if broodstock had been fed diet supplemented with pollack oil as is commonly done, because VE is a fatsoluble vitamin. VC level in the liver decreased as days passed after the end of vitamin injections, whereas the VE level was independent of days after the vitamin injections. These differences may be due to different properties of the vitamins. In order to increase the VC level in eggs of Japanese eel under artificial maturation, injection of VC just before spawning may be effective whereas the effects of VE injection may be independent of timing. Active transfer of ascorbate occurs from yolk reserves into the larval fish body. The mass transfer and loss of VC from the yolk sac to the larval body during development was studied in a population of healthy Atlantic halibut Hippoglossus hippoglossus larvae (Rønnestad et al., 1999). The fate of VC during embryogenesis has been studied in several fish species and the concentration has been shown to decline until the start of feeding (Waagbø, 2010). A decrease of approximately 20±50% was observed during embryonic development and endogenous feeding (Knox et al., 1988; Blom and Dabrowski, 1998). In Atlantic halibut, VC is more rapidly transferred to the larval body from yolk than VE (Rønnestad et al., 1999). At hatching ca. 80% of the VC and 97% of the VE were contained within the yolk-sac compartment. At 200 D°PH (day degrees post hatch; first feeding) >95% of VC and