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  • 1. Introduction

    The ecology of larval fish has been studied for many years because of their importance inunderstanding the population dynamics of commercially important fish species around the world.Their interesting morphology and ecology also has been studied to learn about the wide varietyof behavioral and morphological adaptations used by fish larvae, which are often quite differentin appearance than their juveniles and adults (Moser 1981; Leis and McCormick 2002; Leis2006; Masuda 2009). However, one major group of fish larvae that has received less attentionfor various reasons are leptocephali, which are the larvae of marine and freshwater eels and theirclose relatives that live in the ocean (Castle 1984; Smith 1989a; Mochioka 2003; Lecomte-Finiger 2004). There has been increasing concern recently though, that changes in the ocean due

    Aqua-BioSci. Monogr. (ABSM), Vol. 2, No. 4, pp. 194 (2009) 2009 TERRAPUB, Tokyo. All rights reserved. www.terrapub.co.jp/onlinemonographs/absm/

    *Corresponding author at:Ocean Research Institute, The University of Tokyo1-15-1, Minamidai, Nakano-ku, Tokyo 164-8639, JapanPhone: +81-3-5351-6512Fax: +81-3-5351-6514e-mail: miller@ori.u-tokyo.ac.jp

    Received on May 12, 2009Accepted on August 3, 2009Published online on

    October 31, 2009

    Keywords leptocephali Anguilliformes eels fish larvae early life history larval ecology larval growth rates larval distribution metamorphosis recruitment

    Ecology of Anguilliform Leptocephali:Remarkable Transparent Fish Larvaeof the Ocean Surface Layer

    Michael J. Miller*

    Ocean Research Institute, The University of Tokyo1-15-1, Minamidai, Nakano-ku, Tokyo 164-8639, Japan

    AbstractThis review examines the present state of knowledge about the ecology of

    anguilliform leptocephali, which are the unique but poorly understood larvae ofeels. All eels spawn in the ocean and their leptocephali live in the ocean surfacelayer. Their presence worldwide and basic biology have not been extensively studieddue to their strong ability to avoid standard plankton nets and their fragile trans-parent bodies. Leptocephali have laterally compressed bodies and contain a highproportion of transparent energy storage compounds. They have diverse morpho-logical features, but appear to feed only on particulate material, such as marinesnow or discarded larvacean houses. Some information on their chemical compo-sition, respiration, growth rates, depth distributions, swimming ability, metamor-phosis, and recruitment patterns has been reported, which highlights the interest-ing and unique aspects of leptocephalus larvae. Regional zoogeography and re-productive ecology of adults and ocean currents affect the spatial and temporaldistribution patterns of leptocephali, which have long larval durations, but mostlife histories and larval recruitment behaviors remain undocumented. Their trans-parency, feeding strategy, and large size seem to be a unique and successful larvalstrategy, but the abundance and ecological significance of leptocephali in the oceanappear to have been underestimated.

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    to alterations in the oceanatmosphere system may be affecting the survival of anguillid lepto-cephali (see Miller et al. 2009a), so there is a need to gain a greater understanding of the ecologyof leptocephali.

    Leptocephali are poorly known largely because they grow much larger than typical fishlarvae, and they are rarely collected by the standard-sized plankton nets used by fisheries scien-tists and biological oceanographers. As will be reviewed below, they have large eyes,mechanoreceptors, and can actively swim both forwards and backwards, so this in combinationwith their large size appears to make leptocephali well adapted to avoid small plankton nets(1 m diameter) or any sized trawl during the day (Castonguay and McCleave 1987a; Miller andMcCleave 1994; Miller and Tsukamoto 2004; Miller et al. 2006a). Another problem that hasslowed the progress in research on leptocephali is that these larvae typically show no resem-blance to the juvenile or adult forms of each species, so it is extraordinarily difficult to matchlarval forms to adult species using morphological characteristics.

    Leptocephali differ so much from their adult forms that for about a century they werethought to be a unique type of marine fish (Smith 1989a). Eventually it was realized that lepto-cephali are actually the larval forms of the fishes of the superorder Elopomorpha, which in-cludes species with both eel-like and typical fish-like bodies. The true eels of the Anguilliformesall have elongate body forms and swim using typical anguilliform locomotion (Gray 1933) thatenables them to swim in both directions (DAot and Aerts 1999). This order includes about 15families, with all but one family being almost entirely marine species throughout their life histo-ries (Bhlke 1989a). The eels of the Anguillidae are the catadromous eels that live in freshwaterand estuarine habitats as juveniles and adults, but spawn in the ocean and have leptocephaluslarvae (Tesch 2003; Aoyama 2009). The gulper and swallower eels of the historical orderSaccopharyngiformes are also eel-like in body form, and genetically appear to be containedwithin the Anguilliformes (Inoue et al. 2004). The bonefishes and spiny eels of the Albuliformes(including the historical Notacanthiformes), and the tarpons and ladyfishes of the Elopiformeshave more typical fish-like bodies and do not resemble eels even though they all share thecommon larval form of leptocephalus larvae. All of these elopomorph orders are distributedworldwide from tropical to temperate waters and in the deep sea for some species (Nelson 2006),although anguillids are absent in the South Atlantic and eastern Pacific oceans (Aoyama 2009).

    Despite their global distribution and the existence of more than 800 species of eels (Nel-son 2006), little is known about the life histories of most species or the ecology of their lepto-cephali (Bhlke 1989a,b; Smith 1989a; Miller and Tsukamoto 2004). Adults are difficult tostudy due to the nocturnal and often fossorial behavior of most eels, or the deep depths at whichmany species live in the ocean. Leptocephali are difficult to collect unless large trawls are fishedat night (Miller and Tsukamoto 2004, 2006), but even if they are collected, leptocephali rarelysurvive being captured due to their fragile body form.

    Leptocephali are unusual due to their highly laterally compressed bodies, which are al-most totally transparent (Fig. 1). They are transparent as a result of their bodies mostly contain-ing transparent energy storage material consisting primarily of glycosaminoglycan (GAG) com-pounds (Pfeiler 1999; Pfeiler et al. 2002), which also provide structural support for the bodyuntil they are converted into new body tissues when the leptocephali metamorphose into juve-nile eels at the end of their larval phase. These larvae are very fragile though, because their bodyis covered with a thin layer of tissue that is only a few cell layers thick (Hulet 1978; Suzuki andOtake 2000; Nakamura et al. 2002) and is easily damaged.

    Leptocephali exhibit a wide variety of body shapes that range from very long and thin todeep, with rounded or pointed tails (Fig. 2). Head shapes also vary greatly (Fig. 3; but see be-low). Maximum sizes of leptocephali can range from about 50 mm to greater than 300 mm (totallength) (Castle 1984; Smith 1989a; Bhlke 1989b), but they remain transparent and very fragileregardless of their size or body shape until they metamorphose into juvenile eels.

    Research on leptocephali primarily began after expeditions started searching for the spawn-ing place of the Atlantic eels by collecting their leptocephali in the early part of the last century(Schmidt 1922; Botius and Harding 1985; McCleave 2003). During these early surveys foranguillid leptocephali, which expanded into the IndoPacific (Jespersen 1942), various othertaxa were also collected, and some of these marine eel leptocephali were later studied (e.g.

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    Bertin 1938; Bauchot 1959; Castle 1970, 1979, 1997; Castle and Raju 1975; Smith and Castle1982; Karmovskaya 1990; Castle and Smith 1999). Research on leptocephalus morphology andtheir species identifications achieved greater advances as a result of collections made in morerecent years in the western South Pacific (Castle 1963, 1964, 1965a,b,c), the Gulf of Guinea ofwestern Africa (Blache 1977), and to an even greater extent in the western North Atlantic (Smith1969, 1974), where most leptocephali were eventually identified to the species level (Smith1979; Bhlke 1989b). Other more recent studies compared regional catches of leptocephali tothe known distributions of adults (Richardson and Cowen 2004a,b; Ross et al. 2007). In mostparts of the world however, such as in the IndoPacific, the species identifications are still notknown for the majority of leptocephali (Mochioka et al. 1982, 1991; Tabeta and Mochioka1988a; Miller et al. 2002a, 2006a; Miller and Tsukamoto 2004, 2006).

    Fig. 1. Photographs of leptocephali of the Japanese eel, Anguilla japonica, that were artificially spawned and reared in thelaboratory at the IRAGO Institute in Japan. The larvae are approximately 3050 mm long, and about 200 days old. Photo-graphs are courtesy of Yoshiaki Yamada.

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    There has been research on the distributions, life history characteri