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Deconvolving feeding niches and strategies of abyssal holothurians from their stable isotope, amino acid, and fatty acid composition

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Abstract

Holothurians are the dominant megabenthic deposit feeders in the Peru Basin (SE Pacific) and feed to various degrees of selectivity on a heterogenous pool of sedimentary detritus, but drivers of feeding selectivity and diet preferences for most holothurian species are unknown. This study reconstructs the diets of 13 holothurian species of the orders Elasipodida, Holothuriida, and Synallactida. Bulk stable isotope analyses (δ13C, δ15N) of holothurian body wall and gut wall tissues, gut contents, and feces were combined with compound-specific stable isotope analyses of amino acids, phospholipid-derived fatty acids, and neutral-lipid-derived fatty acids in the body wall. We further assessed how holothurians in the Peru Basin partition their resources and calculated how much of the daily particulate organic carbon (POC) flux to the area is ingested by them using information about gut contents of nine species. To assess the dependence of holothurians on fresh phytodetritus, we performed in situ pulse-chase experiments using 13C- and 15N-enriched phytodetritus. By measuring the uptake of this phytodetritus in fatty acids and amino acids and by comparing it with the presence of these compounds in the sediment, we calculated net accumulation and net deficiency for specific fatty acids and amino acids and discussed how climate change might affect the dependence on specific compounds. A Sørensen–Dice coefficient-based cluster analysis using data from trophic levels, levels of heterotrophic re-synthesis of amino acids, feeding selectivity, and food sources/diet suggested two major trophic groups with two optional subgroups each. Species-specific traits of locomotion, tentacle morphology, and gut structure likely allow resource partitioning and differences in selectivity among the holothurians, of which a subpopulation of 65% of all specimens can ingest 4 to 27% of the daily POC flux to the Peru Basin. Holothurians are specifically dependent on the uptake of arachidonic acid from phytodetritus, while most essential amino acids are available in the Peru Basin in sufficient concentrations.

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Acknowledgements

The authors thank chief scientist Prof. Antje Boetius, Dr. Felix Janssen, the captain and crew of RV Sonne, and the ROV Kiel 6000 team from Geomar (Kiel) for their excellent support during research cruise SO242-2. The authors thank furthermore Dr. Andrey Gebruk for species identification of holothurians. Pieter van Rijswijk, Jana Stratmann, and Jonas Sonntag are thanked for technical assistance during sample processing. We thank three anonymous reviewers and the editor for valuable feedback that improved the content of this paper.

Funding

The research leading to these results has received funding from the European Union Seventh Framework Program (FP7/2007–2013) under the MIDAS project, grant agreement nr 603418, and by the JPI Oceans—Ecological Aspects of Deep Sea Mining project under NWO-ALW grant 856.14.002 and BMBF grant 03F0707A-G. TS was further supported by the Dutch Research Council NWO (NWO-Rubicon grant no. 019.182EN.012, NWO-Talent program Veni grant no. VI.Veni.212.211).

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Correspondence to Tanja Stratmann.

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The authors declare no competing interests.

Ethical approval

All applicable international, national, and/or institutional guidelines for animal testing, animal care, and use of animals were followed by the authors.

Sampling and field studies

All necessary permits for sampling and observational field studies have been obtained by the authors from the competent authorities and are mentioned in the acknowledgements, if applicable. The study is compliant with CBD and Nagoya protocols.

Data availability

The datasets generated during and/or analyzed during the current study are available in the Zenodo repository, https://doi.org/10.5281/zenodo.10188555.

Author contribution

TS and DvO conceived the study; TS, DvO, and AKS performed fieldwork; TS and PvB performed lab analysis; TS drafted the manuscript; and TS, DvO, PvB, and AKS contributed to revising the manuscript to its final version which was approved by all.

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Communicated by S. Kaiser

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This article is a contribution to the Topical Collection Biodiversity in Abyssal Polymetallic Nodule Areas

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Stratmann, T., van Breugel, P., Sweetman, A.K. et al. Deconvolving feeding niches and strategies of abyssal holothurians from their stable isotope, amino acid, and fatty acid composition. Mar. Biodivers. 53, 80 (2023). https://doi.org/10.1007/s12526-023-01389-2

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  • DOI: https://doi.org/10.1007/s12526-023-01389-2

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