Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Quantitative species-level ecology of reef fish larvae via metabarcoding

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

Subjects

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.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Get just this article for as long as you need it

$39.95

Learn more

Prices may be subject to local taxes which are calculated during checkout

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.

References

  1. Bellwood, D. R., Hoey, A. S. & Hughes, T. P. Human activity selectively impacts the ecosystem roles of parrotfishes on coral reefs. Proc. R. Soc. B 279, 1621–1629 (2012).

    Article  Google Scholar 

  2. McClanahan, T. R. et al. Critical thresholds and tangible targets for ecosystem-based management of coral reef fisheries. Proc. Natl Acad. Sci. USA 108, 17230–17233 (2011).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  3. Hoegh-Guldberg, O. et al. Coral reefs under rapid climate change and ocean acidification. Science 318, 1737–1742 (2007).

    Article  CAS  PubMed  Google Scholar 

  4. Bellwood, D. R., Hughes, T. P., Folke, C. & Nyström, M. Confronting the coral reef crisis. Nature 429, 827–833 (2004).

    Article  CAS  PubMed  Google Scholar 

  5. Gardner, T. A., Cote, I. M., Gill, J. A., Grant, A. & Watkinson, A. R. Long-term region-wide declines in Caribbean corals. Science 301, 958–960 (2003).

    Article  CAS  PubMed  Google Scholar 

  6. Garpe, K. C., Yahya, S. A. S., Lindahl, U. & Öhman, M. C. Long-term effects of the 1998 coral bleaching event on reef fish assemblages. Mar. Ecol. Prog. Ser. 315, 237–247 (2006).

    Article  Google Scholar 

  7. Campbell, L. M., Gray, N. J., Hazen, E. L. & Shackeroff, J. M. Beyond baselines: rethinking priorities for ocean -conservation. Ecol. Soc. 14, 14 (2009).

    Article  Google Scholar 

  8. Cowen, R. K. & Sponaugle, S. Larval dispersal and marine population connectivity. Annu. Rev. Mar. Sci. 1, 443–466 (2009).

    Article  Google Scholar 

  9. Cowen, R. K. in Coral Reef Fishes: Dynamics and Diversity in a Complex Ecosystem (ed. Sale, P. F.) 149–170 (Academic, London, 2002).

  10. Doherty, P. J., Fowlert, T. & Fowler, T. An empirical test of recruitment limitation in a coral reef fish. Science 263, 935–939 (1994).

    Article  CAS  PubMed  Google Scholar 

  11. Armsworth, P. R. Recruitment limitation, population regulation, and larval connectivity in reef fish metapopulations. Ecology 83, 1092–1104 (2002).

    Article  Google Scholar 

  12. Werner, F. E., Cowen, R. C. & Paris, C. B. Coupled biological and physical models: present capabilities and necessary developments for future studies of population connectivity. Oceanography 20, 54–69 (2007).

    Article  Google Scholar 

  13. Llopiz, J. K. & Cowen, R. K. Variability in the trophic role of coral reef fish larvae in the oceanic plankton. Mar. Ecol. Prog. Ser. 381, 259–272 (2009).

    Article  Google Scholar 

  14. Leis, J. M. Taxonomy and systematics of larval Indo-Pacific fishes: a review of progress since 1981. Ichthyol. Res. 62, 9–28 (2014).

    Article  Google Scholar 

  15. Ko, H. L. et al. Evaluating the accuracy of morphological identification of larval fishes by applying DNA barcoding. PLoS ONE 8, e53451 (2013).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  16. Limouzyparis, C., Mcgowan, M. F., Richards, W. J., Umaran, J. P. & Cha, S. S. Diversity of fish larvae in the Florida-Keys—results from SEFCAR. Bull. Mar. Sci. 54, 857–870 (1994).

    Google Scholar 

  17. Irisson, J., Paris, C., Gulgand, C. & Planes, S. Vertical distribution and ontogenetic ‘migration’ in coral reef fish larvae. Limnol. Oceanogr. 55, 909–919 (2009).

    Article  Google Scholar 

  18. Evans, N. T. et al. Quantification of mesocosm fish and amphibian species diversity via environmental DNA metabarcoding. Mol. Ecol. Resour. 16, 29–41 (2016).

    Article  CAS  PubMed  Google Scholar 

  19. Hubert, N., Delrieu-trottin, E., Irisson, J., Meyer, C. & Planes, S. Identifying coral reef fish larvae through DNA barcoding : a test case with the families Acanthuridae and Holocentridae. Mol. Phylogenet. Evol. 55, 1195–1203 (2010).

    Article  CAS  PubMed  Google Scholar 

  20. Hebert, P. D. N., Ratnasingham, S. & Waard, J. Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proc. R. Soc. Lond. B 270, S96–S99 (2003).

    Article  CAS  Google Scholar 

  21. Ratnasingham, S. & Hebert, P. D. N. BOLD : the Barcode of Life Data System (www.barcodinglife.org). Mol. Ecol. Notes 7, 355–364 (2007).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  22. Hubert, N., Espiau, B., Meyer, C. & Planes, S. Identifying the ichthyoplankton of a coral reef using DNA barcodes. Mol. Ecol. Resour. 15, 57–67 (2015).

    Article  CAS  PubMed  Google Scholar 

  23. Leray, M. & Knowlton, N. DNA barcoding and metabarcoding of standardized samples reveal patterns of marine benthic diversity. Proc. Natl Acad. Sci. USA 112, 2076–2081 (2015).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  24. Qiu, X. et al. Evaluation of PCR-generated chimeras, mutations, and heteroduplexes with 16S rRNA gene-based cloning. Appl. Environ. Microbiol. 67, 880–887 (2001).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  25. Galan, M., Pagés, M. & Cosson, J. F. Next-generation sequencing for rodent barcoding: species identification from fresh, degraded and environmental samples. PLoS ONE 7, e48374 (2012).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  26. Bucklin, A., Steinke, D. & Blanco-Bercial, L. DNA barcoding of marine metazoa. Ann. Rev. Mar. Sci. 3, 471–508 (2011).

    Article  PubMed  Google Scholar 

  27. Zhou, X. et al Ultra-deep sequencing enables high-fidelity recovery of biodiversity for bulk arthropod samples without PCR amplification. Gigascience 2, 4 (2013).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  28. Deagle, B. E. et al. DNA metabarcoding and the cytochrome c oxidase subunit I marker: not a perfect match. Biol. Lett. 10, 1789–1793 (2014).

    Article  Google Scholar 

  29. Kiflawi, M., Belmaker, J., Brokovich, E., Einbinder, S. & Holzman, R. The determinants of species richness of a relatively young coral-reef ichthyofauna. J. Biogeogr. 33, 1289–1294 (2006).

    Article  Google Scholar 

  30. Golani, D. & Bogorodsky, S. V. The fishes of the Red Sea—reappraisal and updated checklist. Zootaxa 2463, 1–135 (2010).

    Google Scholar 

  31. Genin, A., Lazar, B. & Brenner, S. Vertical mixing and coral death in the Red Sea following the eruption of Mount Pinatubo. Nature 377, 507–510 (1995).

    Article  CAS  Google Scholar 

  32. Fine, M., Gildor, H. & Genin, A. A coral reef refuge in the Red Sea. Glob. Change Biol. 19, 3640–3647 (2013).

    Article  PubMed  Google Scholar 

  33. Hughes, T. P., Bellwood, D. R. & Connolly, S. R. Biodiversity hotspots, centers of endemicity, and the conservation of coral reefs. Ecol. Lett. 5, 775–784 (2002).

    Article  Google Scholar 

  34. Brokovich, E., Einbinder, S., Shashar, N., Kiflawi, M. & Kark, S. Descending to the twilight-zone: changes in coral reef fish assemblages along a depth gradient down to 65 m. Mar. Ecol. Prog. Ser. 371, 253–262 (2008).

    Article  Google Scholar 

  35. Taberlet, P., Coissac, E., Pompanon, F., Brochmann, C. & Willerslev, E. Towards next-generation biodiversity assessment using DNA metabarcoding. Mol. Ecol. 21, 2045–2050 (2012).

    Article  CAS  PubMed  Google Scholar 

  36. Leis, J. M. & Mccormick, M. I. in Coral Reef Fishes: Dynamics and Diversity in a Complex Ecosystem (ed. Sale, P. F.) 171–200 (Academic, London, 2002).

  37. Paris, C. B. & Cowen, R. K. Direct evidence of a biophysical retention mechanism for coral reef fish larvae. Limnol. Oceanogr. 49, 1964–1979 (2004).

    Article  Google Scholar 

  38. Ottosson, U., Sandberg, R. & Pettersson, J. Orientation cage and release experiments with migratory Wheatears (Oenanthe oenanthe) in Scandinavia and Greenland: the importance of visual cues. Ethology 86, 57–70 (1990).

    Article  Google Scholar 

  39. Pineda, J., Porri, F., Starczak, V. & Blythe, J. Causes of decoupling between larval supply and settlement and consequences for understanding recruitment and population connectivity. J. Exp. Mar. Biol. Ecol. 392, 9–21 (2010).

    Article  Google Scholar 

  40. Dibattista, J. D. et al. A review of contemporary patterns of endemism for shallow water reef fauna in the Red Sea. J. Biogeogr. 43, 423–439 (2016).

    Article  Google Scholar 

  41. Matasuura, K. & Tyler, J. C. Resultats DES Campagnes Musorstom Vol. 17 (ed. Séret, B.) 173–208 (Museum National d’Histoire Naturelle, Paris, 1997).

  42. Turan, C. & Yaglioglu, D. First record of the spiny blaasop Tylerius spinosissimus (Regan, 1908) (Tetraodontidae) from the Turkish coasts. Mediterr. Mar. Sci. 12, 247–252 (2011).

    Article  Google Scholar 

  43. Clayton, D. Replication of animal mitochondrial DNA. Cell 28, 693–705 (1982).

    Article  CAS  PubMed  Google Scholar 

  44. Chu, H. T. et al. Quantitative assessment of mitochondrial DNA copies from whole genome sequencing. BMC Genomics 13, S5 (2012).

    Article  PubMed Central  PubMed  Google Scholar 

  45. Munwes, I., Geffen, E., Friedmann, A., Tikochinski, Y. & Gafny, S. Variation in repeat length and heteroplasmy of the mitochondrial DNA control region along a core-edge gradient in the eastern spadefoot toad (Pelobates syriacus). Mol. Ecol. 20, 2878–2887 (2011).

    Article  PubMed  Google Scholar 

  46. Blaser, M., Bork, P., Fraser, C., Knight, R. & Wang, J. The microbiome explored: recent insights and future challenges. Nat. Rev. Microbiol. 11, 213–217 (2013).

    Article  CAS  PubMed  Google Scholar 

  47. Cowles, T. in Handbook of Scaling Methods in Aquatic Ecology: Measurement, Analysis, Simulation (eds Seuront, L. & Strutton, P. G.) 31–49 (CRC Press, Boca Raton, 2003).

  48. Wiebe, P. H. et al. New development in the MOCNESS, an apparatus for sampling zooplankton and micronekton. Mar. Biol. 87, 313–323 (1985).

    Article  Google Scholar 

  49. Leis, J. & Carson-Ewart, B. M. (eds) The Larvae of Indo-Pacific Coastal Fishes: An Identification Guide to Marine Fish Larvae (Brill, Leiden, 2000).

  50. Richards, W. J. Early Stages of Atlantic Fishes: An Identification Guide for the Western Central North Atlantic (CRC Press, Boca Raton, 2005).

  51. Ivanova, N. V., Zemlak, T. S., Hanner, R. H. & Hebert, P. D. N. Universal primer cocktails for fish DNA barcoding. Mol. Ecol. Notes 7, 544–548 (2007).

    Article  CAS  Google Scholar 

  52. Klöppel, A., Brümmer, F., Schwabe, D. & Morlock, G. Detection of bioactive compounds in the mucus nets of Dendropoma maxima, Sowerby 1825 (Prosobranch Gastropod Vermetidae, Mollusca). J. Mar. Biol. 2013, 283506 (2013).

    Article  Google Scholar 

  53. Khalaf, M. Fish fauna of the Jordanian coast, Gulf of Aqaba, Red Sea. J. King Abdulaziz Univ. Mar. Sci. 15, 23–50 (2004).

    Article  Google Scholar 

  54. Hensley, D. A. Two new flatfish records from the Red Sea, an Indopacific samarid (Samariscus inornatus) and the European plaice (Pleuronectes platessa). Isr. J. Zool. 39, 371–379 (1993).

    Google Scholar 

  55. Russell, B. C. & Golani, D. A review of the fish genus Parascolopsis (Nemipteridae) of the western Indian Ocean, with description of a new species from the northern Red Sea. Isr. J. Zool. 39, 337–347 (1993).

    Google Scholar 

  56. Ben-Tuvia, A. A review of the Indo-West Pacific congrid fishes of genera Rhynchoconger and Bathycongrus with the description of three new species. Isr. J. Zool. 39, 349–370 (1993).

    Google Scholar 

  57. Randall, J. E. & Golani, D. Review of the moray eels (Anguilliformes: Muraenidae) of the Red Sea. Bull. Mar. Sci. 56, 849–880 (1995).

    Google Scholar 

  58. Kimura, S., Golani, D., Iwatsuki, Y., Tabuchi, M. & Yoshino, T. Redescriptions of the Indo-Pacific atherinid fishes Atherinomorus forskalii, Atherinomorus lacunosus, and Atherinomorus pinguis. Ichthyol. Res. 54, 145–159 (2007).

    Article  Google Scholar 

  59. Golani, D. Upeneus Davidaromi, a new deep water goatfish (Osteichthyes, Mullidae) from the Red Sea. Isr. J. Zool. 47, 111–121 (2001).

    Article  Google Scholar 

  60. Golani, G. & Lerner, A. A long-term study of the sandy shore icthyofauna in the northern Red Sea (Gulf of Aqaba) with reference to adjacent mariculture activity. Raffles Bull. Zool. 14, 255–264 (2007).

    Google Scholar 

  61. Baranes, A. & Golani, D. An annotated list of deep-sea fishes collected in the northern Red-Sea, Gulf-of-Aqaba. Isr. J. Zool. 39, 299–336 (1993).

    Google Scholar 

  62. Herler, J., Bogorodsky, S. V. & Suzuki, T. Four new species of coral gobies (Teleostei: Gobiidae: Gobiodon), with comments on their relationships within the genus. Zootaxa 3709, 301–329 (2013).

    Article  PubMed Central  PubMed  Google Scholar 

  63. Khalaf, M. A. & Kochzius, M. Community structure and biogeography of shore fishes in the Gulf of Aqaba, Red Sea. Helgol. Mar. Res. 55, 252–284 (2002).

    Article  Google Scholar 

  64. Randall, J. E. & van Egmond, J. in Results of the ‘Oceanic Reefs' Expedition to the Seychelles (1992–1993) Vol. 1 (ed. van der Land, J.) 1–70 (Nationaal Natuurhistorisch Museum, Leiden, 1994).

  65. Freinschlag, M. & Patzner, R. A. Shrimp-gobies in the southern Gulf of Aqaba (Red Sea). Zool. Middle East 55, 41–46 (2012).

    Article  Google Scholar 

  66. Fricke, R., Golani, D., Appelbaum-Golani, B. & Zajonz, U. New record of the spiny pufferfish, Tylerius spinossissimis (Regan, 1908), from Israel, Gulf of Aqaba, Red Sea (Actinopterygii : Tetraodontiformes: Tetraodontidae). Acta Ichthyol. Piscat. 46, 115–118 (2016).

    Article  Google Scholar 

  67. Pietsch, T. W. & Grobecker, D. B. Frogfishes of the World: Systematics, Zoogeography, and Behavioral Ecology (Stanford Univ. Press, Stanford, 1987).

  68. Brokovich, E. The Community Structure and Biodiversity of Reef Fishes at the Northern Gulf of Aqaba (Red Sea) with Relation to their Habitat. MSc thesis, Tel Aviv Univ. (2001).

  69. Blecher-Gonen, R. et al. High-throughput chromatin immunoprecipitation for genome-wide mapping of in vivo protein–DNA interactions and epigenomic states. Nat. Protoc. 8, 539–554 (2013).

    Article  PubMed  Google Scholar 

  70. Dondoshansky, I. & Wolf, Y. Blastclust (NCBI Software Development Toolkit) (NCBI, Bethesda, 2002).

    Google Scholar 

  71. Zerbino, D. R. & Birney, E. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 18, 821–829 (2008). 

  72. Standley, K. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772–780 (2013).

    Article  PubMed Central  PubMed  Google Scholar 

  73. Price, M. N., Dehal, P. S. & Arkin, A. P. Fasttree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol. Biol. Evol. 26, 1641–1650 (2009).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  74. Matsen, F. A., Kodner, R. B. & Armbrust, E. V. pplacer: linear time maximum-likelihood and Bayesian phylogenetic placement of sequences onto a fixed reference tree. BMC Bioinformatics 11, 538 (2010).

    Article  PubMed Central  PubMed  Google Scholar 

  75. Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012).

    Article  CAS  PubMed  Google Scholar 

  76. R Development Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna, 2011).

  77. Hufbauer, R. A., Rutschmann, A., Serrate, B., Vermeil de Conchard, H. & Facon, B. Role of propagule pressure in colonization success: disentangling the relative importance of demographic, genetic and habitat effects. J. Evol. Biol. 26, 1691–1699 (2013).

    Article  CAS  PubMed  Google Scholar 

  78. Iwasaki, W. et al. MitoFish and MitoAnnotator: a mitochondrial genome database of fish with an accurate and automatic annotation pipeline. Mol. Biol. Evol. 30, 2531–2540 (2013).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  79. Palumbi, S. in Molecular Systematics 2nd edn (eds Hillis, D.M., Moritz, C. & Mable, B.K.) 205–247 (Sinauer Associates, Sunderland, 1996).

  80. Baldwin, C. C., Mounts, J. H., Smith, D. G. & Weigt, L. A. Genetic identification and color descriptions of early life-history stages of Belizean Phaeoptyx and Astrapogon (Teleostei: Apogonidae) with comments on identification of adult Phaeoptyx. Zootaxa 2008, 1–22 (2009).

    Google Scholar 

  81. Hebert, P. D. N., Penton, E. H., Burns, J. M., Janzen, D. H. & Hallwachs, W. Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proc. Natl Acad. Sci. USA 101, 14812–14817 (2004).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  82. Ivanova, N. V., Dewaard, J. R. & Hebert, P. D. N. An inexpensive, automation-friendly protocol for recovering high-quality DNA. Mol. Ecol. Notes 6, 998–1002 (2006).

    Article  CAS  Google Scholar 

  83. Ward, R. D., Zemlak, T. S., Innes, B. H., Last, P. R. & Hebert, P. D. N. DNA barcoding Australia’s fish species. Phil. Trans. R. Soc. B 360, 1847–1857 (2005).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  84. Sade, A. R. et al. The Israel National Bathymetric Survey: northern Gulf of Aqaba/Eilat poster. Isr. J. Earth Sci. 57, 139–144 (2008).

    Article  Google Scholar 

Download references

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.

Author information

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

Authors
  1. Naama Kimmerling
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Omer Zuqert
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gil Amitai
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tamara Gurevich
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Rachel Armoza-Zvuloni
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Irina Kolesnikov
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Igal Berenshtein
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Sarah Melamed
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Shlomit Gilad
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Sima Benjamin
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Asaph Rivlin
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Moti Ohavia
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Claire B. Paris
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Roi Holzman
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Moshe Kiflawi
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Rotem Sorek
    View author publications

    You can also search for this author in PubMed Google Scholar

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.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41559-017-0413-2

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing