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

This review examines the present state of knowledge about the ecology of anguilliform leptocephali, which are the unique but poorly understood larvae of eels. All eels spawn in the ocean and their leptocephali live in the ocean surface layer. Their presence worldwide and basic biology have not been extensively studied due to their strong ability to avoid standard plankton nets and their fragile transparent bodies. Leptocephali have laterally compressed bodies and contain a high proportion of transparent energy storage compounds. They have diverse morphological features, but appear to feed only on particulate material, such as marine snow or discarded larvacean houses. Some information on their chemical composition, respiration, growth rates, depth distributions, swimming ability, metamorphosis, and recruitment patterns has been reported, which highlights the interesting and unique aspects of leptocephalus larvae. Regional zoogeography and reproductive ecology of adults and ocean currents affect the spatial and temporal distribution patterns of leptocephali, which have long larval durations, but most life histories and larval recruitment behaviors remain undocumented. Their transparency, feeding strategy, and large size seem to be a unique and successful larval strategy, but the abundance and ecological significance of leptocephali in the ocean appear to have been underestimated. 2 Ecology of Anguilliform Leptocephali: Remarkable Transparent Fish Larvae of the Ocean Surface Layer Aqua-BioScience Monographs VOL. 2 NO. 4 2009 to alterations in the ocean–atmosphere system may be affecting the survival of anguillid leptocephali (see Miller et al. 2009a), so there is a need to gain a greater understanding of the ecology of leptocephali. Leptocephali are poorly known largely because they grow much larger than typical fish larvae, and they are rarely collected by the standard-sized plankton nets used by fisheries scientists and biological oceanographers. As will be reviewed below, they have large eyes, mechanoreceptors, and can actively swim both forwards and backwards, so this in combination with 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 and McCleave 1994; Miller and Tsukamoto 2004; Miller et al. 2006a). Another problem that has slowed the progress in research on leptocephali is that these larvae typically show no resemblance to the juvenile or adult forms of each species, so it is extraordinarily difficult to match larval forms to adult species using morphological characteristics. Leptocephali differ so much from their adult forms that for about a century they were thought to be a unique type of marine fish (Smith 1989a). Eventually it was realized that leptocephali are actually the larval forms of the fishes of the superorder Elopomorpha, which includes species with both eel-like and typical fish-like bodies. The true eels of the Anguilliformes all have elongate body forms and swim using typical anguilliform locomotion (Gray 1933) that enables them to swim in both directions (D’Août and Aerts 1999). This order includes about 15 families, with all but one family being almost entirely marine species throughout their life histories (Böhlke 1989a). The eels of the Anguillidae are the catadromous eels that live in freshwater and estuarine habitats as juveniles and adults, but spawn in the ocean and have leptocephalus larvae (Tesch 2003; Aoyama 2009). The gulper and swallower eels of the historical order Saccopharyngiformes are also eel-like in body form, and genetically appear to be contained within 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 Elopiformes have more typical fish-like bodies and do not resemble eels even though they all share the common larval form of leptocephalus larvae. All of these elopomorph orders are distributed worldwide 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 (Nelson 2006), little is known about the life histories of most species or the ecology of their leptocephali (Böhlke 1989a,b; Smith 1989a; Miller and Tsukamoto 2004). Adults are difficult to study due to the nocturnal and often fossorial behavior of most eels, or the deep depths at which many species live in the ocean. Leptocephali are difficult to collect unless large trawls are fished at night (Miller and Tsukamoto 2004, 2006), but even if they are collected, leptocephali rarely survive being captured due to their fragile body form. Leptocephali are unusual due to their highly laterally compressed bodies, which are almost totally transparent (Fig. 1). They are transparent as a result of their bodies mostly containing transparent energy storage material consisting primarily of glycosaminoglycan (GAG) compounds (Pfeiler 1999; Pfeiler et al. 2002), which also provide structural support for the body until they are converted into new body tissues when the leptocephali metamorphose into juvenile eels at the end of their larval phase. These larvae are very fragile though, because their body is covered with a thin layer of tissue that is only a few cell layers thick (Hulet 1978; Suzuki and Otake 2000; Nakamura et al. 2002) and is easily damaged. Leptocephali exhibit a wide variety of body shapes that range from very long and thin to deep, with rounded or pointed tails (Fig. 2). Head shapes also vary greatly (Fig. 3; but see below). Maximum sizes of leptocephali can range from about 50 mm to greater than 300 mm (total length) (Castle 1984; Smith 1989a; Böhlke 1989b), but they remain transparent and very fragile regardless of their size or body shape until they metamorphose into juvenile eels. Research on leptocephali primarily began after expeditions started searching for the spawning place of the Atlantic eels by collecting their leptocephali in the early part of the last century (Schmidt 1922; Boëtius and Harding 1985; McCleave 2003). During these early surveys for anguillid leptocephali, which expanded into the Indo–Pacific (Jespersen 1942), various other taxa were also collected, and some of these marine eel leptocephali were later studied (e.g. Ecology of Anguilliform Leptocephali: Remarkable Transparent Fish Larvae of the Ocean Surface Layer 3 Aqua-BioScience Monographs VOL. 2 NO. 4 2009 Bertin 1938; Bauchot 1959; Castle 1970, 1979, 1997; Castle and Raju 1975; Smith and Castle 1982; Karmovskaya 1990; Castle and Smith 1999). Research on leptocephalus morphology and their species identifications achieved greater advances as a result of collections made in more recent years in the western South Pacific (Castle 1963, 1964, 1965a,b,c), the Gulf of Guinea of western Africa (Blache 1977), and to an even greater extent in the western North Atlantic (Smith 1969, 1974), where most leptocephali were eventually identified to the species level (Smith 1979; Böhlke 1989b). Other more recent studies compared regional catches of leptocephali to the known distributions of adults (Richardson and Cowen 2004a,b; Ross et al. 2007). In most parts of the world however, such as in the Indo–Pacific, the species identifications are still not known for the majority of leptocephali (Mochioka et al. 1982, 1991; Tabeta and Mochioka 1988a; 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 the laboratory at the IRAGO Institute in Japan. The larvae are approximately 30–50 mm long, and about 200 days old. Photographs are courtesy of Yoshiaki Yamada. 4 Ecology of Anguilliform Leptocephali: Remarkable Transparent Fish Larvae of the Ocean Surface Layer Aqua-BioScience Monographs VOL. 2 NO. 4 2009 There has been research on the distributions, life history characteristics, and assemblage structure of leptocephali in a variety of regions of the world using various levels of identification. In the western North Atlantic, the distributions of anguillid leptocephali were studied in more detail to help define the spawning areas of the two species, the European eel, Anguilla anguilla, and the American eel, Anguilla rostrata, which have overlapping spawning areas in the southern Sargasso Sea (Schoth and Tesch 1982; Kleckner et al. 1983; McCleave et al. 1987; Kleckner and McCleave 1988; Tesch and Wegner 1990). These surveys for anguillid leptocephali also collected many marine eel species whose life histories were examined (McCleave and Miller 1994; Miller and McCleave 1994; Miller 1995, 2002a; Wippelhauser et al. 1996). Studies on the assemblages of leptocephali in these areas were conducted as well (Miller and McCleave 1994, 2007; Miller 1995). Leptocephali also have been collected in the Gulf of Mexico (Smith 1989a; Crabtree et al. 1992), over or along the edge of the continental shelf of the southeastern US east coast (Fahay and Obenchain 1978; Ross et al. 2007), and around Barbados in the eastern Caribbean Sea region (Richardson and Cowen 2004a). In the northeastern North Atlantic, research has mostly focused on leptocephali of anguillids (Tesch 1980; Bast and Strehlow 1990; McCleave et al. 1998) and a few other taxa of leptocephali (e.g. Strehlow et al. 1998; Correia et al. 2002a,b, 2003). A few taxa have been reported from the east coast of South America in recent years (De Castro and Bonecker 2005; Figueroa and Ehrlich 2006). Fig. 2. Photographs of freshly caught leptocephali of 13 families of the Anguilliformes, which show the wide variety of body shapes of leptocephali. Members of the three subfamilies of the Congridae are also shown. Sizes of leptocephali are not prop