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The food source of Sargasso Sea leptocephali

  • Review, Concept, and Synthesis
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Abstract

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 stable isotope research have suggested that marine snow detrital-type particles are a food source, but this was difficult to validate. Recent gut-content DNA-sequence analyses indicated that small 4–25 mm Sargasso Sea European eel larvae, Anguilla anguilla, frequently ingest calycophoran siphonophore tissues as well as other taxa not likely to be ingested individually. A high-magnification photographic study of Sargasso Sea leptocephalus gut contents recently detected possible hydrozoan tentacles and apparent fatty acid-rich single-celled, heterotrophic thraustochytrid protists (class Labyrinthulomycetes), which have been found in marine snow in previous studies, but are not amplified by some DNA primers. Calycophoran siphonophores are abundant in the Sargasso Sea and have extensive tentacle arrays and short-lived eudoxid reproductive stages that might be appropriate sizes to be eaten directly or contribute to marine snow aggregates. The two groups may be interrelated because thraustochytrids are ubiquitously present decomposers that colonize detrital materials in oceanic and coastal ecosystems, so both siphonophore tissues and thraustochytrids may be present in marine snow consumed by European eel and other leptocephali. Therefore, future research on what leptocephali consume as food should be approached from a size-scaling perspective using systematic direct gut-content observations in combination with appropriate primers for next-generation DNA sequencing.

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Fig. 1

modified from Miller et al. (2019), and d the whole body of a 14.3 mm A. anguilla. The different sizes of larvae show fewer proportionally longer teeth in the small larvae compared to the larger ones. Scale bars: 1 mm

Fig. 2

modified from Miller et al. (2019). Scale bars 1 mm

Fig. 3

(modified from Manikan et al. 2015), and g aggregates of the thraustochystrid Schizochytrium aggregatum in the laboratory (modified from Boro et al. 2018). Scale bars a, b, d, e 50 μm, f 10 μm, g 20 μm

Fig. 4
Fig. 5
Fig. 6

modified from Mapstone, 2014), a sequential depiction of the movements of Muggiaea atlantica to deploy its tentacle array for feeding on small copepods (b; modified from Blackett 2015-originally drawn by Mackie and Boag, 1963), and the life-cycle stages of Muggiaea kochi that were reared in the laboratory (c; modified from Blackett 2015-originally drawn by Carré and Carré 1991). At 24 °C, the larval development period took 7 days, and after 1–2 days of feeding during the polygastric stage the eudoxid stages were released that matured during the next 5 days and released their eggs and then died. The dead eudoxid bodies would then contribute to POM in the water column and are a likely candidate for being consumed by leptocephali in the same way as discarded appendicularian houses

Fig. 7
Fig. 8

modified from Li et al. (2013), and c a phytoplankton detritus sample from the North Sea viewed with contrast microscopy showing the presence of many round TH cells (modified from Raghukumar and Shaumann, 1993). Scale bar is 5 μm

Fig. 9
Fig. 10

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Acknowledgements

We thank all the scientists in Germany, Japan and Denmark who have conducted research cruises or studies on the gut contents of leptocephali or the biological environment of the Sargasso Sea that have contributed to the information in this review. The efforts of researchers who study siphonophores and thraustochytrid protists are also acknowledged.

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Authors and Affiliations

  1. Department of Marine Science and Resources, College of Bioresource Sciences, Nihon University, 1866 Kameino, Fujisawa-shi, Kanagawa, 252-0880, Japan

    Michael J. Miller & Katsumi Tsukamoto

  2. Department of Aquatic Bioscience, Graduate School of Agricultural and Life Sciences, The University of Tokyo, 1-1-1 Yayoi, Bunkyo, Tokyo, 113-8657, Japan

    Michael J. Miller & Katsumi Tsukamoto

  3. Thünen Institute of Fisheries Ecology, Herwigstraße 31, 27572, Bremerhaven, Germany

    Reinhold Hanel

  4. Laboratoire BOREA (Museum National d’Histoire Naturelle, CNRS, Sorbonne Université, IRD, UniCaen, Univ Antilles Guadeloupe), 57 rue de cuvier, 75005, Paris, France

    Eric Feunteun

  5. Station Marine de Dinard, CRESCO, 38, rue du port Blanc, 35800, Dinard, France

    Eric Feunteun

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  1. Michael J. Miller
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  4. Katsumi Tsukamoto
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Contributions

MJM developed the review concept and conducted the literature research, RH and KT led research cruises that provided information about the gut contents of leptocephali, EF led research efforts on the stable isotopic compositions of leptocephali, other food web components and POM, and authors critically revised the review.

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Correspondence to Michael J. Miller.

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Supplementary Video: Video recording of amorphous materials as they flowed out of the intestine of a 19.0 mm Anguilla anguilla that are seen in still images in Figure 4 just prior to recording the video. Many small round objects and a piece of apparent exoskeletal material can be seen. The video was recorded on 8 April 2015 during a research cruise in the Sargasso Sea (see Miller et al. 2019) (MP4 21705 kb)

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Miller, M.J., Hanel, R., Feunteun, E. et al. The food source of Sargasso Sea leptocephali. Mar Biol 167, 57 (2020). https://doi.org/10.1007/s00227-020-3662-6

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