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Quantitative species-level ecology of reef fish larvae via metabarcoding

Nature Ecology & Evolution volume 2, pages 306–316 (2018)Cite this article

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Abstract

The larval pool of coral reef fish has a crucial role in the dynamics of adult fish populations. However, large-scale species-level monitoring of species-rich larval pools has been technically impractical. Here, we use high-throughput metabarcoding to study larval ecology in the Gulf of Aqaba, a region that is inhabited by >500 reef fish species. We analysed 9,933 larvae from 383 samples that were stratified over sites, depth and time. Metagenomic DNA extracted from pooled larvae was matched to a mitochondrial cytochrome c oxidase subunit I barcode database compiled for 77% of known fish species within this region. This yielded species-level reconstruction of the larval community, allowing robust estimation of larval spatio-temporal distributions. We found significant correlations between species abundance in the larval pool and in local adult assemblages, suggesting a major role for larval supply in determining local adult densities. We documented larval flux of species whose adults were never documented in the region, suggesting environmental filtering as the reason for the absence of these species. Larvae of several deep-sea fishes were found in shallow waters, supporting their dispersal over shallow bathymetries, potentially allowing Lessepsian migration into the Mediterranean Sea. Our method is applicable to any larval community and could assist coral reef conservation and fishery management efforts.

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Fig. 1: Larval sampling.
Fig. 2: COI sequences in the reference barcode set provide distinctive species identification.
Fig. 3: Size-based model for quantitative inference of species abundance.
Fig. 4: Spatio-temporal distribution of species from the five most abundant families of reef-associated fish in our study.
Fig. 5: The relationship between larval and adult abundance in six common families within our data set.
Fig. 6: The relationship between larval incidence and density for demersal and reef-associated species.

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Acknowledgements

We thank M. McGrouther from the Australian Museum, P. L. Munday from James Cook University, J. Herler from the University of Vienna and P. Borsa from Universitas Udayana for providing tissue samples for this study, the staff of the Inter-University Institute for Marine Sciences in Eilat, Israel, and the Marine Science Station of The University of Jordan and Yarmouk University for their help in conducting the research. This study was supported by the United States–Israel Binational Science Foundation (BSF grant 2008/144 to M.K. and C.B.P.), the Israeli Ministry of the Environment (grant 111-51-6 to M.K. and R.H.), the Angel Faivovich Foundation (to R.S.) and by the Nancy & Stephen Grand Israel National Center for Personalized Medicine. Field sampling was supported in part by the World Bank, as part of the Red Sea–Dead Sea Water Conveyance Study Program.

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Author notes

  1. Rachel Armoza-Zvuloni

    Present address: Dead Sea and Arava Science Center, Yotvata, Israel

  2. Naama Kimmerling, Omer Zuqert and Gil Amitai contributed equally to this work.

Authors and Affiliations

  1. Marine Biology Program, Eilat Campus, Department of Life Sciences, Ben-Gurion University, Eilat, Israel

    Naama Kimmerling & Igal Berenshtein

  2. Interuniversity Institute for Marine Sciences, Eilat, Israel

    Naama Kimmerling, Tamara Gurevich, Rachel Armoza-Zvuloni, Irina Kolesnikov, Igal Berenshtein, Asaph Rivlin, Moti Ohavia, Roi Holzman & Moshe Kiflawi

  3. Department of Molecular Genetics, Weizmann Institute of Science, Rehovot, Israel

    Omer Zuqert, Gil Amitai, Sarah Melamed & Rotem Sorek

  4. The Nancy and Stephen Grand Israel National Center for Personalized Medicine (INCPM), Weizmann Institute of Science, Rehovot, Israel

    Shlomit Gilad & Sima Benjamin

  5. Department of Ocean Sciences, Rosenstiel School of Marine and Atmospheric Science, University of Miami, Miami, FL, USA

    Claire B. Paris

  6. Department of Zoology, Faculty of Life Sciences, Tel Aviv University, Tel Aviv, Israel

    Roi Holzman

  7. Department of Life Sciences, Ben-Gurion University, Eilat, Israel

    Moshe Kiflawi

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Contributions

M.K., C.B.P., R.S. and R.H. designed the study. N.K., I.K., I.B., A.R. and M.O. performed the field sampling of larvae. N.K., O.Z., G.A., T.G., R.A.-Z., I.K., S.M., C.B.P., M.K. and R.H. processed the field samples and collected data for the COI database. O.Z., G.A., S.G., S.B. and R.S. performed and analysed the high-throughput sequencing. O.Z., N.K., M.K., R.H. and R.S. analysed the data. M.K., R.H., R.S., O.Z. and N.K. wrote the paper. All authors contributed to writing the manuscript through comments and discussions.

Corresponding authors

Correspondence to Roi Holzman, Moshe Kiflawi or Rotem Sorek.

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Supplementary information

Supplementary Information

Supplementary Table 1, Supplementary Figure 1

Life Sciences Reporting Summary

Supplementary Table 2

Metagenomic and ecological features of larvae samples

Supplementary Table 3

Gulf of Aqaba/Red Sea fish and their available COIs

Supplementary Table 4

Occurrence and abundance of classified larvae

Supplementary Data 1

Fasta file of all reference COI barcodes in our set

Supplementary Data 2

Fasta file of all COI-mapped reads in our set

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Kimmerling, N., Zuqert, O., Amitai, G. et al. Quantitative species-level ecology of reef fish larvae via metabarcoding. Nat Ecol Evol 2, 306–316 (2018). https://doi.org/10.1038/s41559-017-0413-2

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