Low occurrence rates of ubiquitously present leptocephalus larvae in the stomach contents of predatory fish

ICES Journal of Marine Science, Jun 2015

Leptocephali, the larvae of eels, grow to large sizes and are widely distributed in tropical and subtropical oceans. Their role in oceanic food webs is poorly known because they are rarely reported as food items in fish stomach content studies. Data from 13 years of research on the trophic dynamics of Pacific Ocean predatory fish indicate that among 8746 fish of 76 species/taxa (33 families) that had been feeding, only 16 fish of 6 species had remains of 34 leptocephali in their stomachs. Only 0.013% of the 256 308 total prey items were leptocephalus larvae, and 0.03% of the total prey items were juvenile or adult eels (mostly snipe eels: Nemichthyidae). There were 10 fish of 2 species of lancetfish (Alepisaurus spp., n = 152), 2 rainbow runners (Elagatis bipinnulata, n = 222), and 2 yellowfin tuna (Thunnus albacares, n = 3103) that had leptocephali in their stomach contents, but all except one T. albacares (contained 15 leptocephali) had each eaten ≤3 leptocephali. A swallower, Pseudoscopelus sp., and a frigate tuna, Auxis thazard, had eaten single leptocephali. Twenty-eight bigeye tuna, Thunnus obesus, had eaten 76 juvenile/adult nemichthyid or serrivomerid eels. A literature survey found that only 15 out of 75 examined publications listed leptocephali in the stomach contents of a total of 6 species out of ∼ 42 300 predatory fish of 40 species. The transparency of leptocephali and their apparent mimicry of gelatinous zooplankton could contribute to lower rates of predation. Their soft bodies likely digest rapidly, so although this study and existing literature indicate that leptocephali sometimes contribute to predatory fish diets, particularly for fish that do not exclude gelatinous prey types, and fish with low digestion rates in their stomachs such as lancetfish, their levels of contribution to fish diets and the impacts of predators on eel recruitment remain uncertain.

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Low occurrence rates of ubiquitously present leptocephalus larvae in the stomach contents of predatory fish

Miller, M. J., Dubosc, J., Vourey, E., Tsukamoto, K., and Allain, V. Low occurrence rates of ubiquitously present leptocephalus larvae in the stomach contents of predatory fish. - ICES Journal of Marine Science Marine Science Michael J. Miller 1 2 Jeff Dubosc 0 Elodie Vourey 0 Katsumi Tsukamoto 1 Valerie Allain 0 0 Oceanic Fisheries Programme, Secretariat of the Pacific Community , BP D5, 98848 Noumea Cedex, New Caledonia 1 Laboratory of Eel Science, Department of Marine Science and Resources, College of Bioresource Sciences, Nihon University , 1866 Kameino, Fujisawa-shi, Kanagawa 252-0880 , Japan 2 Atmosphere and Ocean Research Institute, The University of Tokyo , 5-1-5 Kashiwanoha, Kashiwa, Chiba 277-8564 , Japan Leptocephali, the larvae of eels, grow to large sizes and are widely distributed in tropical and subtropical oceans. Their role in oceanic food webs is poorly known because they are rarely reported as food items in fish stomach content studies. Data from 13 years of research on the trophic dynamics of Pacific Ocean predatory fish indicate that among 8746 fish of 76 species/taxa (33 families) that had been feeding, only 16 fish of 6 species had remains of 34 leptocephali in their stomachs. Only 0.013% of the 256 308 total prey items were leptocephalus larvae, and 0.03% of the total prey items were juvenile or adult eels (mostly snipe eels: Nemichthyidae). There were 10 fish of 2 species of lancetfish (Alepisaurus spp., n ¼ 152), 2 rainbow runners (Elagatis bipinnulata, n ¼ 222), and 2 yellowfin tuna (Thunnus albacares, n ¼ 3103) that had leptocephali in their stomach contents, but all except one T. albacares (contained 15 leptocephali) had each eaten ≤3 leptocephali. A swallower, Pseudoscopelus sp., and a frigate tuna, Auxis thazard, had eaten single leptocephali. Twenty-eight bigeye tuna, Thunnus obesus, had eaten 76 juvenile/adult nemichthyid or serrivomerid eels. A literature survey found that only 15 out of 75 examined publications listed leptocephali in the stomach contents of a total of 6 species out of 42 300 predatory fish of 40 species. The transparency of leptocephali and their apparent mimicry of gelatinous zooplankton could contribute to lower rates of predation. Their soft bodies likely digest rapidly, so although this study and existing literature indicate that leptocephali sometimes contribute to predatory fish diets, particularly for fish that do not exclude gelatinous prey types, and fish with low digestion rates in their stomachs such as lancetfish, their levels of contribution to fish diets and the impacts of predators on eel recruitment remain uncertain. Alepisaurus; Anguilliformes; leptocephali; Pacific Ocean; predation; predator avoidance; stomach contents Introduction Leptocephali are a ubiquitously present but poorly known type of fish larvae that live in the surface layer of the world’s warm water oceans (Castle, 1984; Bo¨hlke, 1989a; Smith, 1989; Miller, 2009) . They are the larvae of eels of the Anguilliformes and the other elopomorph orders of the Albuliformes (including the notacanths) and Elopiformes (Bo¨hlke, 1989b; Inoue et al., 2004; Miller and Tsukamoto, 2004) . The most well-known eels are the freshwater eels of the Anguillidae, which are important fisheries species in some parts of the world (Tesch, 2003; Tsukamoto and Kuroki, 2014) . There are also several important commercially harvested coastal marine eels, particularly of the genera Conger (Congridae) and Muraenosox (Muraenesoscidae), and a wide range of more than 800 species of marine eels are present in all types of tropical to southern temperate habitats down to 4000 m (Bo¨hlke, 1989b; Miller and Tsukamoto, 2004) . Interestingly, despite the anguillid species living in freshwater and estuarine habitats for their juvenile growth stage before spawning offshore in the ocean (Tsukamoto et al., 2002; Tesch, 2003; Aoyama, 2009) and marine eels inhabiting coastal, continental slope, deep-benthic, and mesopelagic habitats, the leptocephalus larvae of all eels, as well as those of the other elopomorphs, inhabit the upper few hundred metres of the ocean (Castonguay and McCleave, 1987; Miller, 2009) . Compared with other fish larvae that also live in the ocean surface layer, leptocephali are unusual because of their extreme transparency, large maximum sizes, unique morphology and physiology, and drastic metamorphosis into completely different body forms as they enter the juvenile stage (Smith, 1989; Pfeiler, 1999; Miller, 2009) . Surveys for leptocephali in various parts of the world show that larvae of a variety of eel families are consistently present in the surface layer of the ocean in tropical and subtropical areas and can sometimes be quite abundant near the edges of continental shelves or within offshore spawning areas (McCleave and Kleckner, 1987; Tsukamoto, 1992; Miller and McCleave, 1994, 2007; Miller et al., 2002, 2006; Richardson and Cowen, 2004; Miller, 2009) . The leptocephali of the European eel, Anguilla anguilla, for example, become distributed all across the North Atlantic after being spawned in the Sargasso Sea, as they are transported to their recruitment areas in Europe and North Africa (Schmidt, 1922; Miller et al., 2015) . The characteristics of anguillid larvae may have been an important component of the evolution and speciation of freshwater eels (Kuroki et al., 2014) , yet their ecological role and those of marine eel leptocephali within marine communities are very poorly known. Leptocephali live in the upper few hundred metres of the ocean and some make diel vertical migrations within the upper 250 m, or deeper near continental shelves (Castonguay and McCleave, 1987; Ross et al., 2007; Miller, 2009) . Unlike most fish larvae, they appear to feed exclusively on particulate organic material, such as marine snow, giving them low trophic isotopic signatures (Otake et al., 1993; Mochioka and Iwamizu, 1996; Miller et al., 2013a) . Some species grow to large sizes of 250 mm or larger, although most taxa reach 60 – 120 mm (Castle, 1984; Bo¨hlke, 1989a; Miller et al., 2013b) . They appear to be capable swimmers (Wuenschel and Able, 2008) and many seem to avoid large plankton nets during the day in clear oceanic waters, with the largest leptocephali potentially avoiding nets even at night (Miller et al., 2013b) . Importantly though in relation to predator – prey relationships, they also appear to use a dynamic form of shape-change behaviour of curling their bodies into fully or partially formed coil shapes, which seems to make them resemble the silhouettes of gelatinous zooplankton (Miller et al., 2013c) . This type of behaviour has been also observed in other marine animals (Robison, 1999) , and may occur because only a limited number of fish seem to feed on gelatinous zooplankton in warmer-water areas (Purcell and Arai, 2001; Arai, 2005) . Because of this, the shape-change behaviour of leptocephali has been hypothesized to reduce predation by acting as a form of Batesian Mimicry (Miller et al., 2013b) . This behaviour might reduce predation by some types of predatory fish, and their laterally compressed transparent bodies and forwards-or-backwards swimming ability probably make leptocephali adapted to avoid detection or actively avoid capture by predators (Miller, 2009). Most food habits studies on predators such as tunas, billfish, and other scombrids that live in the same habitats as eel larvae do not list leptocephali among the types of fish that were found in stomach contents (e.g. Bertrand et al., 2002; Potier et al., 2007; Young et al., 2010; see Supplementary Table S1) . The pelagic top-predators are opportunistic feeders foraging in the epipelagic layer (0 – 200 m) and in deeper waters on micronektonic fish, molluscs, and crustaceans of sizes ranging between ,1 and 20 – 30 cm (Blackburn, 1968; Sund et al., 1981; Me´nard et al., 2006; Dambacher et al., 2010; Young et al., 2010) , so they should have the potential to prey on leptocephali. Most of these predators are considered to be visual hunters (Fritsches and Warrant, 2001; Fritsches et al., 2005) , so their ability to see the highly transparent leptocephali may be a factor in determining the predator – prey relationships between leptocephali and predators that forage in areas where they are present. Other types of fish larvae are known to be preyed on by both invertebrate and fish predators (Bailey and Houde, 1989) , but leptocephali grow to much larger sizes than most fish larvae, which along with their extreme transparency, makes them a special case among fish larvae. There is a general lack of information about the predator – prey dynamics of leptocephali (Appelbaum, 1982; Miller, 2009) , and the consumption of substantial numbers of leptocephali has only been reported in a few rare cases (Grassi, 1896; Matsui et al., 1970) . One modelling study examined the theoretical effect of mortality of European eel leptocephali presumably from predation or other factors, but the model parameters were not based on any information directly related to leptocephali (Bonhommeau et al., 2009) . Our study used an ongoing research programme and database on the trophic ecology of predatory fish in the western and central Pacific Ocean region described in Allain et al. (2012) to examine the general occurrence of leptocephali in the stomach contents of mostly pelagic top-predator fish. A literature review of previous studies on these types of fish was also conducted to examine the presence of leptocephali in the stomach contents. This provides the opportunity to assess the prevalence of leptocephali in stomach contents of a range of mostly oceanic predatory fish species and to begin to evaluate the possible contribution of leptocephali to oceanic food webs as prey, and if predators may have much influence on the recruitment of eel populations. The presence of juvenile and adult eels in the stomach contents database and in the previous studies examined is also briefly evaluated. Methods The stomach contents of predatory fish collected from tuna fishing vessels catching fish near the surface (purse-seine and poleand-line) and at greater depths within the upper 400 m (longline) between 2001 and 2014 were examined in the laboratory as part of previous studies (Allain et al., 2012) or ongoing research of the Oceanic Fisheries Programme of the Secretariat of the Pacific Community (SPC). These collections were made across a wide region of the southwest Pacific Ocean ranging from just offshore of northeastern Indonesia, eastward offshore of Papua New Guinea (PNG), through southern Micronesia and the Solomon Islands, near New Caledonia, Fiji, the Cook Islands, New Zealand, and across French Polynesia (Figure 1a). A wide range of fish were caught and sampled for stomach contents that included 8 species/ taxa of tunas and other Scombridae, 6 billfish, 7 Carangidae, 6 Gempylidae, 19 sharks or rays, and 39 other species, with the common commercial species of tuna (yellowfin, Thunnus albacares; skipjack, Katsuwonus pelamis; albacore, Thunnus alalunga; bigeye, Thunnus obesus), wahoo (Acanthocybium solandri), and dolphinfish (Coryphaena hippurus) being caught in the greatest abundances, with substantial numbers of lancetfish (Alepisaurus spp.) and rainbow runners (Elagatis bipinnulata) also being caught (Table 1; Figure 2). Prey were identified to lowest taxonomic level, counted, and weighed and measured when digestion was not too advanced. Leptocephali in the Indo-Pacific usually have not been matched with their adult species yet (Miller and Tsukamoto, 2004, 2006) , and leptocephali in this research effort were only sometimes identified to family or species level or measured for length because they were typically in poor condition due to partial digestion. Juvenile or adult eels were classified to family, genus or species using their distinctive features. The abundance of leptocephali in the stomach contents of predatory fish was evaluated using individuals with nonempty stomachs (74.0% of 11 814 fish examined; 76 of 85 predator species/taxa; 33 of 36 families). Examination of the literature about the food contents of predatory fish was also conducted using 75 published papers or reports that included 40 species (Supplementary Table S1). This literature review included mostly pelagic predatory fish that are of commercial or recreational importance, and did not include many of the smaller mesopelagic fish or coastal fish that may sometimes overlap in their distributions with leptocephali. Therefore, it is not intended to be a comprehensive literature review of this broad subject for all types of predatory fish. However, the diets of 184 species of coastal or continental shelf fish along the southeast US coast that overlap with the habitats of some types of leptocephali such as the Ophichthidae have been overviewed previously (Marancik and Hare, 2005) , as well as the diets of 50 species of fish along the northeast US coast (Smith and Link, 2010) and 52 fish species along the US west coast (Dufault et al., 2009). Randall (1967) reported on the stomach contents of 50 predatory reef and inshore fish species from Puerto Rico and the Virgin Islands. In addition, most mesopelagic fish appear to feed on crustaceans or other invertebrates (Clarke, 1980; Roe and Badcock, 1984; Bernal et al., 2013) , or sometimes other mesopelagic fish (Butler et al., 2001) , and the stomach contents of 1000 mesopelagic fish 25 species of 10 families in the North Atlantic were previously checked for the presence of leptocephali (Appelbaum, 1982) . Results The stomach contents of 11 814 fish of 85 species/taxa (36 families) were checked from fish that were caught in many areas of the western Pacific mostly between 108N and 258S, and also near New Zealand (Figure 1). The 8746 fish of 76 species/taxa (33 families) with food in their stomachs contained 256 308 prey items of 598 taxa. Among those fish, 16 individuals (ind.) of 6 species had from 1 to 15 leptocephali in their gut contents. There were 34 leptocephali in total that were eaten by lancetfish Alepisaurus ferox (7 ind.: 9 larvae), Alepisaurus brevirostris (1 ind.: 1 larvae), and Alepisaurus sp. (2 ind.: 2 larva), rainbow runners, E. bipinnulata (2 ind.: 4 larvae), yellowfin tuna, T. albacares (2 ind.: 16 larvae), a frigate tuna, Auxis thazard (1 ind.: 1 larva), and a swallower, Pseudoscopelus sp. (1 ind.: 1 larva) as shown in Table 1. The percentage of individuals of each of these types of fish that had eaten leptocephali was 0.06% for yellowfin tuna, 3.2% for the less abundant frigate tuna, 6.6% for the lancetfish in general, and 0.9% for rainbow runners (Table 1). Although most leptocephali were identified as Anguilliformes larvae only, some were identified as belonging to the Bathymyrinae (Congridae; Ariosoma-type: Miller et al., 2013d) eaten by a rainbow runner and a lancetfish, Congrinae (Congridae) eaten by the swallower, and Ophichthidae eaten by the frigate tuna and lancetfish. It is also possible that a few individuals of bigeye and skipjack tuna may have had leptocephali in their stomach contents, but were only labelled as Anguilliformes, with no stage listed in the database. The developmental stage or taxa of anguilliform fish (n ¼ 14) eaten by two great barracuda (Sphyraena barracuda) were also not specified. Most of the fish that had leptocephali in their stomach contents were collected in the region to the northeast of PNG, except for the lancetfish, which were mostly caught around New Caledonia, and The number or percentage of fish (with food contents) that had leptocephalus larvae or juvenile/adult eels in their stomach contents is shown (number of leptocephali or eels eaten is shown in parentheses). Species that included leptocephali or juvenile/adult eels in previous studies are also noted (see Supplementary Table S1 for details). Poorly sampled species for some families shown are pooled at the bottom of the table within the “other families” category. the swallower that was caught northwest of Fiji (Figure 1). Yellowfin tuna were caught all across the sampling region, but the two fish that contained leptocephali were in the PNG region. The yellowfin tuna caught in the vicinity (4.988S, 159.598E) of the large atoll called Frindsbury Reef was the only fish that had many leptocephali (n ¼ 15) in its stomach contents. Frigate tuna were only collected near PNG (not shown), and the one fish that had a leptocephalus was caught near the coast (Figure 1a). The swallower that contained a leptocephalus was caught near Fiji (Figure 1a). The examination of stomach contents in previous studies of mostly oceanic predators found that out of 75 published papers or reports including 128 datasets about individual species (some papers include data on more than one species) 42 387 predatory fish of 40 species, only 15 papers listed the presence of leptocephalus larvae in the stomach contents (Supplementary Table S1). This included 8 out of 16 studies on lancetfish (A. ferox) that listed leptocephali in the stomach contents. Only 1 out of 21 studies on yellowfin tuna reported leptocephali being in stomach contents, but 2 out of 7 studies on skipjack tuna included leptocephali. Only 1 (bullet tuna) out of 26 studies on other species of tuna, and 1 (white marlin) out of 22 datasets on 10 species of billfish reported leptocephali being present. Two out of 11 studies on dolphinfish listed leptocephali as prey. These various studies that listed leptocephali in the stomach contents were conducted in a wide range of ocean areas including the Pacific, Indian Ocean, Atlantic, and the Mediterranean Sea. A few leptocephali might have been present among the gut contents examined in some studies if they were included in categories such as “unidentified fish” or “fish larvae”. Some juvenile/adult eels had been eaten by 28 bigeye tuna, T. obesus, which mostly consisted of snipe eels of the family Nemichthyidae (n ¼ 74) and a few sawtooth eels of the family Serrivomeridae (n ¼ 2). Two individual bigeye had each eaten 16 or 17 snipe eels. Single individuals of albacore and yellowfin tuna, a moonfish (Lampris guttatus), and a lancetfish had also eaten 1 – 3 juvenile/adult eels. In the literature survey of 75 papers, the studies with juvenile/adult eels present in stomach contents included 5 species of tuna in 9 studies and 7 species of other types of fish in 9 studies (Supplementary Table S1). Similar to leptocephali, these studies listing eels as prey items were conducted in all the ocean basins where this type of research has been conducted. Discussion This study evaluated how frequently leptocephali are present in the stomach contents of predatory pelagic fish using the large 2001 – 2014 SPC database also used by Allain et al. (2012) in the southwestern Pacific Ocean region and by examining the presence or absence of these larvae in other previously published stomach contents studies. The stomach contents of 9000 fish examined from the western Pacific in the present study indicated that there were only 16 fish of 6 species that had eaten leptocephali recently enough to be distinguished in their stomach contents. This database included 40 species that seemingly could prey on leptocephali based on their feeding ecology or the habitats they use, as well as 34 species such as sharks and rays, triggerfish, or smaller coastal predatory fish that might not be expected to feed on leptocephali. Similarly, only 12% of the datasets about individual species that were examined listed leptocephali as being in the stomach contents of more than 42 300 predatory fish of 40 species that might have the chance to feed on these larvae, but more than half of those papers including leptocephali were about the lancetfish, A. ferox (Supplementary Table S1). These two types of information indicate that leptocephali are very rarely encountered in studies of the stomach contents of most large predatory fish from tropical to southern temperate latitudes where leptocephali are present. In addition, detailed summaries of 113 papers about the food habits of 184 species of coastal or continental shelf fish in the western North Atlantic that were compiled by Marancik and Hare (2005) and the lists of stomach contents of 50 reef and inshore predatory fish species of the West Indies (Randall, 1967) did not mention leptocephali or eel larvae. This, and because other major data summaries of the food contents of many species of coastal fish also do not mention leptocephali (Dufault et al., 2009; Smith and Link, 2010) indicates leptocephali have not been detected as being an important food item in many species of coastal fish. The same may be at least partly true for fish larvae in general, because only 10 of the 75 papers examined in the literature survey in Supplementary Table S1 listed fish larvae as being present in their stomach contents data. However, fish larvae were more commonly found in the SPC database examined in this study than were leptocephali, with 351 fish of 16 species having fish larvae in their stomach contents. The majority of the 3508 larvae were eaten by 303 tuna of 6 species, but 25 lancetfish, 12 rainbow runners, and 3 dolphinfish, species which had also eaten leptocephali, had eaten fish larvae. In addition, the database included 908 fish of 17 species that ate 4577 fish with an uncertain larvae/juvenile development stage designation. Most fish larvae are quite small compared with the sizes of the predators examined, and juvenile fish were listed more frequently in the database (2527 fish of 35 species ate 21 463 juvenile fish) and in the literature survey (19 studies listed juveniles), since these would be larger and would digest less rapidly than fish larvae or leptocephali. Determining the development stage of small fish is often difficult though, and the terminology of the early developmental stages of fish is not universally established and accepted (Leis and Carson-Ewart, 2004) due to the diversity in ways fish develop. Consequently, the number of larvae extracted from the database examined in this study and the number of studies from the literature mentioning fish larvae are uncertain and should be considered with caution. Even though leptocephali grow as large as or larger than many juvenile fish, their body form is quite different from juvenile eels, so it is not difficult to distinguish between the larval and juvenile stages of eels. Although leptocephali seem to be rare or absent in the food contents of oceanic predatory fish as noted previously (Appelbaum, 1982; Miller, 2009) , as well as in coastal fish (Randall, 1967; Marancik and Hare, 2005; Dufault et al., 2009; Smith and Link, 2010) , the large SPC stomach contents database and the examination of many previous studies indicate that leptocephali are sometimes eaten by several types of fish. More than one individual of lancetfish, yellowfin tuna, and rainbow runners had consumed leptocephali according to the database, along with single individuals of three other species. However, one yellowfin tuna in the western equatorial Pacific had consumed 15 leptocephali and 2 skipjack tuna near the coast of PNG had eaten “many” Anguilla obscura leptocephali (41 – 48 mm; Matsui et al., 1970), which proves that at least individual fish will feed on leptocephali beyond just a random encounter with a single larva if the circumstances are favourable to do so. Among the 39 studies on tuna stomach contents that were examined, leptocephali were listed in only 1 study on yellowfin tuna, 2 on skipjack tuna and 1 on bullet tuna (Ronquillo, 1953; Nakamura, 1965; Mostarda et al., 2007; Supplementary Table S1) , and no leptocephali were listed for bigeye tuna or for 8 other tuna species. For dolphinfish, two papers listed leptocephali (Wu et al., 2006; Varghese et al., 2014) . Only 1 species of billfish was reported to have eaten leptocephali (J u´nior et al., 2004) , and none of the papers on wahoo or mostly single papers on 14 other species listed any leptocephali (Supplementary Table S1). However, if leptocephali were common in stomach contents of these predators, they would have been reported, and none of the studies on these large predatory fish have ever mentioned or discussed leptocephali as prey of these fish, except for listing them in the tables. One type of fish whose stomach contents more frequently contain leptocephali are lancetfish, of the genus Alepisaurus. The long-snouted lancetfish, A. ferox, is often caught on pelagic fisheries longlines and its food habits have been studied in several areas. In the present study, in addition to 1 of the 8 shortsnouted lancetfish, A. brevirostris, and 2 of the 5 Alepisaurus sp. having eaten a leptocephalus, 6% of the 165 A. ferox had eaten 1 – 2 leptocephali. This is consistent with the finding that 8 of the 16 studies on A. ferox included leptocephali, which were conducted in the Atlantic (Haedrich, 1964) , eastern Pacific (Haedrich and Nielsen, 1966) , Hawaii (Moteki et al., 1993; Choy et al., 2013) , southwest Pacific (Fourmanoir, 1969) , eastern Indian Ocean and Coral Sea (Fujita and Hattori, 1976) , and Surga Bay Japan (Kubota and Uyeno, 1970; Ito et al., 2005) . The most detailed information about the leptocephali consumed by lancetfish was that of Fourmanoir (1969), which reported that 110 A. ferox had eaten 32 leptocephali of the Congridae (17 larvae, 8 species), Nemichthyidae (14, 2 species), and Muraenidae (1) families along with 610 other fish prey of 92 non-eel species. Haedrich (1964) reported that the five leptocephali eaten by four lancetfish (772 – 1276 mm) near Bermuda were 60 mm in length. There were five Ariosoma and one Muraenesox leptocephali eaten near Hawaii (Moteki et al., 1993) . The leptocephali eaten by lancetfish in the eastern Pacific were two large ( 350 – 400 mm) notacanthid leptocephali (Albuliformes), which were a species referred to as Leptocephalus giganteus (Haedrich and Nielsen, 1966) that grow to large sizes of .1.5 m (Castle, 1984) . Seemingly, the highest rates of leptocephalus consumption by lancetfish were the 160 Conger myriaster leptocephali that were eaten by 44 A. ferox in Surga Bay, Japan (Ito et al., 2005) , and the 27 “young anguilliforms” (97 – 220 mm) that were found in 30 of the 35 A. ferox stomachs examined from the eastern Indian Ocean and Coral Sea by Fujita and Hattori (1976) . Leptocephali were not among the prey categories listed for lancetfish in eight other studies though (e.g. Potier et al., 2007; Varghese et al., 2014; Supplementary Table S1) . To be able to carefully assess the meaning of the low rates of occurrence of leptocephali in the stomach contents of the predatory fish examined here and the higher rates of occurrence in lancetfish, several factors need to be considered. Leptocephali are highly transparent when alive (Miller, 2009) , which might provide a form of camouflage (Johnsen, 2001) , thus reducing their frequency of detection by mobile predators. Because leptocephali appear to be able to avoid being captured even by large plankton nets during the day (Miller and McCleave, 1994; Miller et al., 2006, 2013b) , they also may be able to use their swimming ability to move away from approaching predators before they are seen. In addition, the factor of leptocephali using shape-change behaviour of curling their bodies into various coil shapes that may make them resemble the silhouettes of gelatinous zooplankton (Miller et al., 2013c) also should be considered. This behaviour could reduce predation by some types of fish by acting as a form of Batesian Mimicry (Ruxton et al., 2004) , because relatively few fish species seem to extensively feed on gelatinous zooplankton in warmer-water areas (Purcell and Arai, 2001; Arai, 2005) . For example, a recent study including 1518 fish of 12 predator species including tuna, billfish, dolphinfish, barracuda, and lancetfish in the eastern Arabian Sea does not even mention gelatinous zooplankton, because only low percentages of jellyfish were found in one species (silky shark, Carcharhinus falciformis) and salps were only found in another species (yellowfin tuna; Varghese et al., 2014) . Considering the likely presence of the gelatinous zooplankton where these fish were feeding, the predators may have search images for prey items that help them exclude gelatinous zooplankton from their diet. If this is true, they may also exclude leptocephali that have curled up in front of them because they resemble their search images of gelatinous zooplankton (Miller et al., 2013c) . This tactic of shape-change by leptocephali would not work for predator species that are thought to feed on gelatinous zooplankton such as ocean sunfish (Pope et al., 2010) , which in one case has been found to feed on many European eel leptocephali in the Straits of Messina of Italy (Grassi, 1896) . That observation indirectly suggests that the leptocephali had been curling up using the shape-change behaviour when they detected the larger fish, because ocean sunfish appear poorly adapted to actively pursue and capture swimming larvae that were approaching their recruitment areas (Miller et al., 2013c) . The curling strategy may not work very well with lancetfish either, which appear to be ambush predators (Romanov and Zamorov, 2002) that may not be highly selective in their search images for prey, because non-food debris is often present in their stomachs (Kubota and Uyeno, 1970; Ito et al., 2005) . They have higher rates of ingestion of marine debris of anthropogenic origin than other fish, with clear or white plastic having the highest rate of ingestion (Choy and Drazen, 2013) . Lancetfish can be cannibalistic if other food types are not abundant (Romanov et al., 2008) and also sometimes eat transparent organisms such as salps, polychaetes, and heteropods (Haedrich, 1964; Kubota and Uyeno, 1970; Fujita and Hattori, 1976; Ito et al., 2005; Potier et al., 2007; Romanov and Zamorov, 2007) . Interestingly, they frequently consume Phronima amphipods that live inside transparent barrel-shaped chambers made from gelatinous zooplankton (Laval, 1978) , especially in the Atlantic Ocean (Satoh, 2004) . One 1265 mm fish contained 32 Phronima, seemingly 29 chambers (salp tests) along with 146 salps (Haedrich, 1964) . Satoh (2004) showed that lancetfish were consuming the 20 – 40 mm Phronima along with their chambers in the Atlantic where they were the most important food item. An appropriate sized curling leptocephalus would have a similar silhouette as these chambers, so this may be another case of when the shape-change of leptocephali would not deter predation. Similarly, the diet of Ceratoscopelus warmingii, which had eaten leptocephali (five fish had eaten single leptocephali; Appelbaum, 1982) , has an unusually diverse diet compared with other mesopelagic fish (Robison, 1984) , because they have been found to eat siphonophores, ctenophores, and heteropods along with many other taxa (Clarke, 1980) . It was unclear however, if some of the C. warmingii in the study of Appelbaum (1982) had consumed the leptocephali within the net, since some of the leptocephali were found partly in the mouth or in the oesophagus. Net feeding is not a consideration for predators such as tuna and lancetfish that are not caught in plankton nets though. The higher frequency of lancetfish consumption of leptocephali may also be partly related to their digestive system structure, because they digest their prey in the intestine, not the stomach, making them have good-condition food contents (Rofen, 1966) . Leptocephali have little ossification and are filled with jelly-like glucosaminoglycan materials (GAG) overlain by a thin layer of muscle (Smith, 1989; Pfeiler, 1999; Miller, 2009) , so they likely digest quickly, making them unrecognizable shortly after being eaten if they are exposed to digestive fluids. Therefore, the occurrence of leptocephali in stomach contents might depend on how soon they were eaten before the predator was captured to a greater degree than for prey species with hard parts or large muscle masses. Tuna have high metabolic rates and digest their food two to five times faster than most fish (Magnuson, 1969) , so this may further reduce the occurrence of leptocephali in studies of their stomach contents. Experiments conducted by Olson and Boggs (1986) indicate that prey with low lipid content and non-compact musculature were completely evacuated from stomachs 6 h after feeding. Prey lost up to 20% of their weight within a few minutes after ingestion by yellowfin tuna (Olson and Boggs, 1986) , so leptocephali, with only a thin layer of epidermis and muscle tissue outside of the mucinous pouch containing the GAG, might become unrecognizable very quickly. Small semi-transparent fish larvae in general may digest rapidly and become un-identifiable with 15 – 30 min after consumption (Christensen, 2010) . Rapid digestion has also been hypothesized to be occurring for gelatinous zooplankton that might be consumed by tunas and billfish in the Mediterranean Sea, after stable isotope mixing model results suggested that gelatinous zooplankton were being consumed in greater numbers than expected (Cardona et al., 2012) . Consumption of leptocephali that have a lower trophic position than gelatinous zooplankton (Miller et al., 2013b) could also cause a similar result in isotope studies on predators. This potential for rapid digestion and also the transparency of leptocephali in combination with their apparent ability to mimic gelatinous zooplankton makes it difficult to assess the degree to which these unusual larvae are consumed by predatory fish. One possibility is that they are eaten by some species such as yellowfin tuna in some areas more frequently than stomach contents data indicate, but they are not consumed as much by the wide range of predatory fish as would be expected from the widespread presence and abundances of leptocephali, because of their various apparent predator avoidance adaptations. Leptocephali should directly overlap in the upper 250 m of the ocean with a wide range of predators such as tunas and billfish (Young et al., 2010) , because leptocephali likely show diel vertical migrations from the upper 100 m at night to depths of 250 – 300 m during the day in open ocean areas (Castonguay and McCleave, 1987; Miller, 2009) . Overlap could also occur where leptocephali can be abundant at specific times and places such as along the edge of the continental shelf after marine eels have been spawning (Miller et al., 2002; Miller and McCleave, 2007) , in the offshore spawning areas of mesopelagic eels (Miller and McCleave, 1994; Miller et al., 2006) , or within some anguillid eel spawning areas (McCleave and Kleckner, 1987; Tsukamoto, 1992) . They also appear ubiquitously present throughout the subtropical gyres and boundary currents of the world’s oceans and in warm inland seas (Miller, 1995; Wouthuyzen et al., 2005; Ross et al., 2007; Miller et al., 2006, 2015; Miller and Tsukamoto, unpublished data) . Although leptocephali are likely present where fish predators feed from tropical to southern temperate latitudes, it is difficult to clearly assess their likely abundances in the places where predators were feeding in this and previous studies. The observations of Grassi (1896; A. anguilla larvae eaten by ocean sunfish) and Matsui et al. (1970; many A. obscura larvae eaten by 2 skipjack tuna) and the one yellowfin tuna in the present study that ate 15 eel larvae indicate that leptocephali may be consumed in large numbers at specific times and places, but this may only be detected when predators are captured immediately after feeding on the leptocephali because of the rapid digestion of larvae. Another problem for understanding the amount of predation on leptocephali is that their distribution and behaviour is not well understood yet, because they are sometimes present at the surface (,1 m) at night (Ross et al., 2007; Miller, 2009) and apparently even near the surface during the day where they have been captured by seabirds, including one gannet and two noddy species in the Atlantic and Pacific Oceans (Seki and Harrison, 1989; Figueroa, 1997; Naves et al., 2002) . Some species of leptocephali may vertically migrate more than others (Castonguay and McCleave, 1987) , so leptocephali may be exposed to predators at various depths and light levels. Predation might also occur on the metamorphosing leptocephali that use tidal currents to enter shallow water during recruitment to some tropical areas (see Miller, 2009), but leptocephali were not reported in the diets of 50 predatory reef and inshore fish species by Randall (1967) or in coastal predatory carangid jacks or triggerfish (Supplementary Table S1) possibly due to ingress at night. Other types of marine predators may also spatially overlap with leptocephali, such as squid species that include fish in their diets, but leptocephali do not appear present in their stomach contents (e.g. Rosas-Luis et al., 2014) or those of marine mammals such as dolphins that also eat fish (e.g. Amir et al., 2005; Pusineri et al., 2007; Wang et al., 2011) . Sea turtles feeding in the epipelagic zone may also overlap spatially with leptocephali, and some species are known to feed on gelatinous zooplankton in warm-water areas (e.g. Tomas et al., 2001) . A diver-caught siphonophore was observed to have eaten an Ariosoma leptocephalus though (Page`s and Madin, 2010) , and a net-caught chaetognath was found with a small nemichthyid leptocephalus in its gut (Johnson et al., 2006), but we are currently unaware of other reports of leptocephali being consumed by marine animals. The juveniles and adults of mesopelagic or sometimes coastal eels are eaten by pelagic or coastal predators, as was shown by the 28 bigeye tuna that had eaten eels in the present study and by 11 species in the 75 previous studies we examined also having eels in their stomach contents data (10 of the 21 studies on yellowfin and bigeye tuna included eels; Supplementary Table S1). Some marine mammals and sea snakes feed on benthic marine eels of the Congridae and Muraenidae families (Wang et al., 2011; Amir et al., 2005; Ineich et al., 2007; Longenecker, 2010) , so eels and their larvae clearly contribute to some marine foodwebs. However, the degree to which rapidly digestible, but possibly highly predator avoidance adapted leptocephali are consumed by marine fish appears to remain an open question that will require further studies with various types of approaches to help better understand the predator – prey relationships of these fascinating and highly transparent fish larvae. At present, however, there seems to be little indication that predation is major factor regulating recruitment in fish that have a leptocephalus larva. Supplementary data Supplementary material is available at the ICESJMS online version of the manuscript. Acknowledgements This research was funded by the Pacific Islands Oceanic Fisheries Management Project supported by the Global Environment Facility. Co-funding was provided by the Australian Government Overseas Aid Programme (AusAid) and the New Caledonian Zone Economique de Nouvelle-Caledonie (ZoNeCo) programme. 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Michael J. Miller, Jeff Dubosc, Elodie Vourey, Katsumi Tsukamoto, Valerie Allain. Low occurrence rates of ubiquitously present leptocephalus larvae in the stomach contents of predatory fish, ICES Journal of Marine Science, 2015, 1359-1369, DOI: 10.1093/icesjms/fsv034