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Images of the intestines of a a 13.0 mm Anguilla anguilla that contain amorphous material, apppendicularian houses and fecal pellets, b a 20.1 mm Avocettina infans that contains translucent and pigmented objects that appear different than typical apppendicularian houses and could be hydrozoan tissues, amorphous materials, appendicularian houses, and fecal pellets inside the intestines of leptocephali of c a 14.0 mm Anguilla rostrata, and d a 43 mm Anarchias similis (Muraenidae) modified from Miller et al. (2019). Scale bars 1 mm
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The mysterious food source of anguilliform leptocephali has been difficult to understand, so this review evaluates potential interrelationships among recent discoveries on this subject. There are typically few identifiable gut-content objects in leptocephalus intestines, which usually contain amorphous materials. Gut content observation studies and...
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... Most of the body is filled with a gelatinous substance that provides a slightly positive buoyancy. Although the diet of leptocephali is not well understood, examination and DNA analysis of the leptocephalus gut contents indicate that marine snow and hydrozoan plankton are important components (Miller et al., 2020). However, a limitation is that all dietary studies have been done on larvae caught during larval surveys in the Sargasso Sea area. ...
... Apparently because of these structural changes to the body, their feeding ceases completely during metamorphosis. This feeding cessation through metamorphosis from leptocephalus to glass eel marks a major shift in diet from consuming marine snow, which consists of a wide range of detrital materials and carbohydrate exudates from plankton and bacteria that form soft aggregates that is floating free in the ocean surface layer (Miller et al., 2020), to eating benthic aquatic animals in estuaries and rivers (Belpaire et al., 1992). ...
... The remarkable elongation of the stomach, and differentiation and numerical increase of gastric glands in post-metamorphic glass eels seems to be related to a rapid development of their ability to digest more protein, which is required in association with a diet shift from the marine snow diet of leptocephali (Miller et al., 2013(Miller et al., , 2020 to feeding on aquatic invertebrates as young eels (Belpaire et al., 1992). Pepsinogen secreted by the gastric glands reacts with gastric acid that is likewise secreted by the gastric glands and is converted to active pepsin, which contributes to proteolysis. ...
... Since the posterior end of the stomach of this species elongates to near the transition between midgut and rectum in the late elver stage just before the yellow eel stage (Hatakeyama et al., 2021), the protein digestive ability in the stomach is expected to further improve after the feeding initiation at the glass eel stage. Incidentally, marine snow, the food of leptocephali, contains detrital materials and carbohydrate exudates from plankton and bacteria (Miller et al., 2020), that are of interest to the digestive physiology of larval eels. However, the high and low expression of trypsin and amylase, and the expressional ratio of proteolytic and carbohydrate digestive enzymes during larval stage varies in each study not only in Japanese eels (Hsu et al., 2015;Murashita et al., 2013), but also in the closely related European eel (Benini et al., 2023;Parmeggiani et al., 2020;Politis et al., 2018). ...
Temporal changes of feeding incidences, digestive organ tissues, and mRNA expression of digestive enzymes
were investigated in artificially reared Anguilla japonica glass eels. Incidences of daily feeding and cumulative
first feeding exceeded 50% at day 40 and 33, respectively, but tended to increase gradually. Time until first
feeding varied from day 11–61 among individuals. Glass eels without food after metamorphosis showed notable
developmental changes in their digestive system that included increases in esophagus goblet cells and blood
vessel diameters, elongation of the stomach, differentiation and increased number of gastric glands, and increases
in gall bladder sizes. A distinct qualitative change, which was gastric gland differentiation, occurred in all
eels until week 2 after metamorphosis. All quantitative character values showed trends of gradual changes in
their averages and had high coefficients of variation, especially for goblet cell numbers. Few deaths and no
histological features related to severe starvation such as notably more hepatocyte necrosis or desquamation of
intestinal epithelial cells were observed even after 9 weeks. Hepatocyte-vacuole stored glycogens and pancreatic
zymogen granules were also found, suggesting that they were not expressing symptoms of starvation. Relative
expressions of five digestive enzymes were lowest at week 0 and increased gradually in their averages with the
passage of weeks, along with large variations among fish. This study found that half of the post-metamorphic
glass eels began feeding after 4 weeks, but that there were large individual variations in the timing of feeding
onset, the degree of developmental of their digestive organs, and in digestive enzyme expressions.
... Eel hatchery research is continuing and has been on-going for many decades, especially in Japan (Yuan et al., 2021). It has been stymied repeatedly (Don and Carlson, 2019) by the challenges of spawning and rearing from leptocephali to the elver stage in captivity because: (1) Eels do not mature spontaneously, sexual maturation of eels is driven by a complex set of environmental cues; (2) Most farmed eels turn out to be males; markets want larger females; (3) Hormonal treatments have been developed and reliable supplies of fertilized eggs can be obtained but few healthy larvae result; (4) Development of leptocephali to glass eels takes 250-300 days in culture versus 110-160 days in the wild, and survival rates are very low <10%; (6) Leptocephali feed on marine snow in nature (Miller et al., 2020) but in a hatchery setting the only effective feeds are formulations of expensive, thick, pinkish pastes made primarily of shark eggs, soy protein, and vitamins, and these are very expensive and cause water quality problems; and (7) Light-wary leptocephali need to be kept in darkened rooms making hatchery management difficult and costly. ...
Capture fisheries and aquaculture are researched, planned, and managed throughout the world as if they are independent entities ignoring their complex and evolving interdependencies. Global attention on "blue foods" as an important part of United Nations Sustainable Development Goals (SDGs) is focused on the restoration of capture fisheries and the sustainable expansion of aquaculture. Such a binary approach does not fit the current realities, opportunities, and innovations in ocean food systems (OFS), and does not integrate enough of the necessary transdisciplinary knowledge across professions. Integration of knowledge across professions is needed as modern ocean foods enter common marketplaces so interventions to increase sustainability must incorporate data on rural economic development, producers and their mixed ocean/land-based livelihoods and seasonal employment patterns, tourism, data on local to regional and global trade, and consumer behaviors. Four case studies detail the status and evolution of OFS typologies of American and spiny lobsters as fed fisheries, salmon as aquaculture-enhanced fisheries, and the capture-based aquacultures for cod and for eels. Objectives of this review were to examine for four OFS cases if there was adequate evidence to show that they were as productive, economically attractive, and as socially beneficial OFS that rival those of binary aquaculture or fisheries systems alone; and did they have significant potential to accelerate innovations as much as those sectors. For the four cases reviewed, productive, social and ecologically valuable, rapidly evolving OFS existed with demonstrable innovation trajectories. In the early part of this century it was estimated that capture-based aquaculture (CBA) accounted for about 20% of the total quantity of food fish production worth US$1.7 billion. Review of just four case studies having a limited number of participating countries found that annual value of the OFS exceeded US$4 billion: the value of eels as a capture-based aquaculture (CBA) was estimated US$2.3 billion for just two countries; for salmon as an aquaculture-enhanced fishery at $1.7 billion for only one state of the USA; and for lobsters as fed fisheries and a CBA, $825 million for the USA and Vietnam. However, OFS are disruptive as they require radically changed science, education, management, and development policies as current binary fisheries and aquaculture management approaches do not fit their current realities, or opportunities, or accelerate innovations, plus poorly integrate knowledge across professions. This was demonstrated by the example of dynamic management/regulatory situation for cod wild fisheries and the growing CBA for cod in Norway. The coming decades of accelerated climate and social changes will cause concomitant changes to ocean foods markets from local to global, and rural ocean foods livelihoods. These two systemic changes will drive the evolution and development of a greater diversity of OFS that will require much more attention of policy-makers and investors.
... Another uncertain aspect of glass eels feeding behaviour is its relationship with migration modus because it is generally believed that digestion and locomotion compete for energy and oxygen allocation, indicating that a feeding individual cannot migrate and vice versa (Edeline et al., 2009;Owen, 2001). First food uptake at the continental stage thus seems a crucial but largely understudied aspect (e.g., Dörner & Berg, 2016;Miller et al., 2020) that might determine the success of the marine/freshwater transition in heavily modified estuaries for many juvenile eels nowadays. ...
The transition from marine to fresh water is a challenging task for juvenile eels. This critical step in the early eels' life is preceded by a metamorphosis from the oceanic larval to the continental glass eel stage, requiring major energy‐demanding morphological, physiological and behavioural modifications during which time these animals do not feed. The success of the glass eels’ inland migration after metamorphosis will largely depend on remaining energy levels, which can be supplemented only by resuming food uptake. Although it is crucial for their survival and the maintenance of the population, the feeding behaviour of glass eels is still an understudied aspect of the eels’ complex life cycle. Many uncertainties about the phenology, diet, potential prey preferences and their relation with migration modus (migratory vs. sedentary) still remain. In this study, the authors analysed the stomach and gut contents of 458 European glass eels (Anguilla anguilla L. 1758) captured in a drainage canal connecting a small mesotidal estuary with an adjacent polder area during the spring migration seasons of 2016 and 2017. They demonstrated that although glass eels started feeding briefly upon arrival in the estuary, food uptake for early arrivals was restricted to a minority that sparsely feed on detritus and some worm‐like benthic invertebrates. Along the season, food uptake intensified eventually engaging all glass eels and their dietary palette diversified including a wide array of planktonic and benthic organisms. Crustacean plankton (mainly cyclopoid copepods) was an important part of the glass eel diet, whereas benthic oligochaetes were less abundant as food source in spite of their high presence in the sediments. No clear differences in feeding behaviour could be observed between migratory and sedentary glass eels. This study showed that glass eels can use highly artificial and dynamic drainage canals as feeding ground during their critical marine/freshwater transition. This outcome is also a plea to improve the accessibility of alternative (unnatural) migration routes between the ocean and suitable freshwater growth habitats for the European eel.
... Recently, particulate organic matter (POM) in the ocean surface layer (Feunteun et al., 2015;Miller et al., 2013;Tomoda et al., 2018;Watanabe et al., 2021) comprising natural materials, zooplankton carcasses and dead phytoplankton (e.g., marine snow) has been described as a main food. Nonetheless, the actual materials that leptocephali feed on in situ, and the distribution of these in time and space in sea water, are mostly undetermined; thus the feeding ecology and dietary preferences of anguilliform leptocephali are still poorly understood (Chow et al., 2019a;Ghinter et al., 2020;Miller et al., 2020;. These reports relate to the anguilliform leptocephali belonging to the multifamily Anguillidae, Chlopsidae, Congridae, Muraenidae, Muraenesocidae, Nemichthyidae, Ophichthidae, Serrivomeridae, etc. ...
The authors observed the feeding behaviour of artificially reared Japanese eel Anguilla japonica leptocephali, 7.5–19 mm total length (10–61 days post‐hatch), fed Synechococcus sp., which is considered a potential food source of anguilliform larvae. Three strains of Synechococcus sp. (NIES‐972, 976 and 979) were tested as the food material. Larvae across the entire length range could effectively ingest a suspension of pico‐sized cyanobacteria (1–3 μm in diameter). Video observations of the mid‐hindgut of larvae under an epifluorescence microscope confirmed that the movement of microvilli of the intestinal epithelium allowed the cell particles to circulate in the mid‐hindgut, before becoming solidified in the anal region. Significant differences in food intake were observed between larvae fed two strains of Synechococcus (NIES‐972 and 976), and among different cell densities, which suggests feeding selectivity and density dependence. Comparisons of feeding behaviour under the light group (9L:15D) and the dark group (24D) showed significantly higher food intake (measured as an index of intestinal fullness) in the light group, although substantial and continuous ingestion was observed in the dark group, indicating continuous feeding by swallowing sea water. The authors hypothesise that the feeding ecology of anguilliform leptocephali is based on a survival strategy whereby the larvae do not compete with various higher‐trophic‐level fishes for food in an oligotrophic environment.
... Many species of marine eels such as those living below 1000 m may be unaffected by climate change, but almost all eel larvae live in the upper few hundred meters and their food source is directly linked to primary production factors that could be affected by climate change. Leptocephali appear to feed on marine snow particles as their primary food source [114,115], and these particles are produced by materials released by phytoplankton and from various sources of detrital materials from planktonic organisms [116]. Therefore, because primary production of eukaryotic phytoplankton appears to be reduced by warm water conditions [116,118], there may be reductions of marine snow production when ocean surface layer temperatures become warmer as a result of global warming. ...
The Indonesian Seas are at the center of the Coral Triangle, which has the highest marine biodiversity in the world, and the region is under threat from climate change. Freshwater habitats in the region have a high number of anguillid eels compared to other regions of the world, but it is more difficult to capture marine eels to assess their biodiversity. Catches of leptocephali from 5 internationally collaborative surveys for eel larvae (leptocephali) in the Coral Triangle have collected about 126-169 species of larvae, which indicates that the Coral Triangle region likely has the highest marine eel biodiversity in the world based on comparisons to similar larval surveys in the Indian, Pacific, and Atlantic oceans (29-107 species). These marine eel species inhabit a wide range of benthic and pelagic habitats, but how they might be affected by climate changes such as ocean warming has not been considered. Anguillid eels in the Coral Triangle region could be affected mainly by changes in rainfall patterns that could affect their freshwater growth stage or their reproductive maturation patterns and migration. Effects on marine eels would depend on the types of habitats where they live, with the least impacts occurring for deep benthic or pelagic species. Marine eels that live in shallow habitats would be most affected if warming seas and coral bleaching reduce the types of prey species they depend on. Based on their possible association with coral reef habitats, eels of the families Muraenidae and Chlopsidae appear to the most likely types of eels to be impacted by changes in community structure resulting from coral bleaching. All leptocephali species live in the ocean surface layer where they feed on marine snow, so warmer ocean temperatures might reduce the amount or quality of marine snow that is available, resulting in lower larval survival rates. Further studies on eel biodiversity and habitat use will provide more insight into the possible loss of endemic species in the Coral Triangle due to climate change, but presently it is unclear how many species of eels may be directly affected by climate change.
... The larval stage is assumed to last for about 1-2 years (van Ginneken and Maes, 2005;Bonhommeauz et al., 2009;Munk et al., 2010). However, many aspects of their life cycle and the biology of the early life stages are still scarcely described from nature (Righton et al., 2016;Miller et al., 2020). ...
... One hypothesis suggests gelatinous plankton as an important part of the diet. This is based on recent studies using rRNA sequencing and DNA-sequence analyses of gut content of European eel larvae which showed a dominance of Hydrozoa taxa (phylum Cnidaria), suggesting that gelatinous plankton is an important part of the diet for these leptocephalus larvae Miller et al., 2020). Further, studies on vertical distribution in the area of European eel spawning (Castonguay and McCleave, 1986) showed correspondence between vertical patterns in distribution of the leptocephalus larvae and of small hydrozoans, supporting this proposed predator-prey linkage . ...
... Further, studies on vertical distribution in the area of European eel spawning (Castonguay and McCleave, 1986) showed correspondence between vertical patterns in distribution of the leptocephalus larvae and of small hydrozoans, supporting this proposed predator-prey linkage . Another hypothesis proposes that marine snow particles, i.e., flocculated dead organic matter could be major components of the leptocephalus diet, (Miller et al., 2011(Miller et al., , 2018(Miller et al., , 2020. This is supported by isotope studies indicating low trophic position of gut contents (Miller et al., 2012) and by visual observations of the contents showing discarded larvacean houses, as well as plankton fecal pellets which could be part of the marine snow (Mochioka and Iwamizu, 1996;Riemann et al., 2010). ...
Several aspects of the biology of European eel (Anguilla anguilla) larvae are still unknown; particularly, information about their functional development and feeding is sparse. In the present study, we histologically characterize the digestive system of wild caught specimens of European eel leptocephalus larvae. The aim was to provide more understanding about how food may be ingested and mechanically processed in the leptocephalus larvae, and to discuss this in the context of its hypothesized feeding strategy. Larvae were caught in the Sargasso Sea during the “Danish Eel Expedition 2014” with the Danish research vessel Dana. The larval sizes ranged from 7.0 to 23.3 mm standard length (SL) at catch. We found that the mouth/pharynx, especially the anterior esophagus, was surrounded by a multi-layered striated muscle tissue and that the epithelium in the mouth/pharynx had a rough filamentous surface, followed by epithelial columnar cells with multiple cilia in the anterior esophagus. This suggests an expandable pharynx/esophagus, well-suited for the transportation of ingested food and likely with a food-crushing or grinding function. The digestive tract of the larvae consisted of a straight esophagus and intestine ventrally aligned within the larval body, and its length was linearly correlated to the larval length (SL). The length of the intestinal part constituted up to 63% of the total length of the digestive tract. The intestinal epithelium had a typical absorptive epithelium structure, with a brush border and a well-developed villi structure. Some cilia were observed in the intestine, but any surrounding muscularis was not observed. The liver was observed along the posterior part of the esophagus, and pancreatic tissue was located anterior to the intestine. Our findings support the hypothesis that the eel leptocephalus may ingest easily digestible gelatinous plankton and/or marine snow aggregates. The muscular esophagus and the ciliated epithelium appear sufficient to ensure nutrient transport and absorption of the ingested food through the digestive tract.
... Further, analyses of fatty acids and lipids 17,18 and stable isotopes [20][21][22] , indicate that leptocephali feed on POM originating from organisms at lower trophic levels [13][14][15][16][19][20][21][22] . These observations suggest that marine snow detrital-type particles in the POM are a food source 23 . ...
... Artificially cultured Japanese eel survived by eating small POM (53 and 25 µm) from seawater 22 ; however, they died upon eating large POM (> 350 µm), strongly suggesting that relatively large zooplankton and/or phytoplankton, specifically those with hard or sharp bodies, seriously damaged the digestive organs of leptocephali. Smaller particles may therefore be of importance for these larvae 16 , and this corresponds with the food source known as marine snow detrital-type particles 23 . Small spherical particles (2-40 µm in diameter) of marine snow comprising polysaccharides and proteins within the aggregate is a common finding in both the gut contents of anguilliform leptocephali 15,16,23,55 and environmental water 16 , suggesting that marine snow particles originating from phytoplankton and cyanobacteria are a food source for the leptocephali 16 . ...
... Smaller particles may therefore be of importance for these larvae 16 , and this corresponds with the food source known as marine snow detrital-type particles 23 . Small spherical particles (2-40 µm in diameter) of marine snow comprising polysaccharides and proteins within the aggregate is a common finding in both the gut contents of anguilliform leptocephali 15,16,23,55 and environmental water 16 , suggesting that marine snow particles originating from phytoplankton and cyanobacteria are a food source for the leptocephali 16 . Thus, food sources of eel larvae in the marine environment are assumed to be small or soft marine snow particles in POM 56 . ...
Eel larvae apparently feed on marine snow, but many aspects of their feeding ecology remain unknown. The eukaryotic 18S rRNA gene sequence compositions in the gut contents of four taxa of anguilliform eel larvae were compared with the sequence compositions of vertically sampled seawater particulate organic matter (POM) in the oligotrophic western North Pacific Ocean. Both gut contents and POM were mainly composed of dinoflagellates as well as other phytoplankton (cryptophytes and diatoms) and zooplankton (ciliophoran and copepod) sequences. Gut contents also contained cryptophyte and ciliophoran genera and a few other taxa. Dinoflagellates (family Gymnodiniaceae) may be an important food source and these phytoplankton were predominant in gut contents and POM as evidenced by DNA analysis and phytoplankton cell counting. The compositions of the gut contents were not specific to the species of eel larvae or the different sampling areas, and they were most similar to POM at the chlorophyll maximum in the upper part of the thermocline (mean depth: 112 m). Our results are consistent with eel larvae feeding on marine snow at a low trophic level, and feeding may frequently occur in the chlorophyll maximum in the western North Pacific.
... ght in the western NEC in the western North Paci c . The diversity of organisms contributing to or colonizing marine snow (Alldredge and Silver 1988;Shanks and Walters 1997;Kiørboe 2000) is consistent with the diversity of molecular sequences of taxa from marine snow in the Sargasso Sea, including hydrozoans (Ayala et al. 2018;Lundgreen et al. 2019). Miller et al. (2020 reviewed gut content studies based on a variety of analyses, such as those using DNA, morphology, and stable isotopes. ...
... Although Chow et al. (2019) reported possible contamination of these larval gut samples from the Sargasso Sea, they also reported hydrozoan DNA sequences from leptocephalus gut contents in the western North Paci c. These siphonophores occur widely in the upper few hundred meters of the water column in subtropical gyres, including in the NEC (Lo et al. 2012), and they have a temporary reproductive stage that dies after releasing eggs (Carré and Carré 1991) which could contribute to marine snow and possibly be ingested by leptocephali (Miller et al. 2020). ...
The diets of larval (leptocephali) anguillid and marine eels are poorly understood, despite studies on their gut contents or stable isotope ratios suggesting marine snow particles represent a food source. Concerns for Japanese eel Anguilla japonica stock conservation necessitate an improved knowledge of their larval ecology to better understand the causes of their recent decline in numbers and fluctuating recruitment into East Asia. To understand the distribution of and variation in size of leptocephali in relation to their feeding, we examine carbon and nitrogen stable isotope ratios of larvae from seven research cruises (2002–2013) in the North Equatorial Current spawning area. Preleptocephali (2–3 days old, ~5 mm total length) isotope ratios reflect maternal ratios, but feeding-stage leptocephali (8–56 mm) tend to have higher ∂15N values with decrease of latitude typically in areas south of a salinity front. Neither ∂15N nor ∂13C ratios are clearly related to longitude or larval size < 30 mm, but ∂13C values of larvae > 40 mm are lower further downstream in the North Equatorial Current and Subtropical Countercurrent. Differences in ∂13C values might be a function of varying spatial baselines in the two currents apart from the spawning area. Although among-year larval isotope ratio differences may reflect temporal baseline variation related to the location of the salinity front, more research with much wider range observations in the spawning season is required because ingested marine snow particles might differ with larval growth and location.
... Different depth distributions have also been considered as possible reasons for different stable isotopic signatures that have been observed in leptocephali of different taxa including Ariosoma Liénart et al., 2016;Ghinter et al., 2020). Leptocephali appear to mostly feed on materials that are classified as marine snow (see Miller et al., 2019bMiller et al., , 2020aTsukamoto and Miller, 2021), but the depths where they feed are not yet known. Marine snow can be most abundant near the surface (e.g., offshore in the Sargasso Sea; Munk et al., 2018), so residing at shallow depths might increase the amount of food available to leptocephali. ...
Small-sized eels of the Tropical Conger, Ariosoma scheelei, appear to be common in shallow Indo-Pacific tropical sheltered-bay and lagoon-type habitats when they are sampled appropriately and their larvae are abundant offshore of these areas, but little is known about their biology. Collections of about 7800 likely A. scheelei larvae in May 1997 using a 2-mm mesh 70 m² mouth-opening trawl with a multiple opening-and-closing codend system at 13 Northwest Coral Sea (NWCS) areas (5 upper-200 m sampling depth-layers, 2 nighttime trawl-deployments/area) and a surface net were used to examine the vertical and geographic distributions of abundance and size of the leptocephali and metamorphosing larvae. 76.5% of trawl-caught A. scheelei leptocephali (33–169 mm, 95.3 ± 22.9 mm) were collected in the 0–12 m depth-layer and 927 (43–151 mm, 83.6 ± 19.5 mm) were examined from surface catches. Some larvae were caught at 12–25 m (12.3%) and 25–50 m (10.1%), but few were caught at 50–100 m (0.77%) and 100–200 m (0.12%). Leptocephali were most abundant offshore in the southeast and metamorphosing larvae (N=532, 82–146 mm) were most abundant in the northwest near the large shelf areas of Torres Strait and the Gulf of Papua. Regional size variations, proportions of metamorphosing larvae, and currents entering/exiting the NWCS suggested that larvae experience transport among areas, and have potential for retention by the Coral Sea Gyre or other recirculations. The high larval abundance of this small-size eel that reaches reproductive maturity at sizes <200 mm suggest it is more abundant in shallow tropical areas than is widely known.
