Acknowledgments
General: We especially thank the Indonesian Institute of
Sciences (LIPI) for promoting our collaboration and the Sorong
Polytechnic of Marine and Fisheries (Politeknik KP Sorong, West Papua)
for providing the vessel Airaha 02 that we used in this campaign. We are
grateful to the crew of the Aihara 02 for assisting us during the
operations and SPYGEN staff for the technical support in the laboratory.
Funding: Fieldwork and laboratory activities were supported by
the Lengguru 2017 Project (www.lengguru.org), conducted by the French
National Research Institute for Sustainable Development (IRD), the
Indonesian Institute of Sciences (LIPI) with the Research Center for
Oceanography (RCO, the Politeknik KP Sorong), the University of Papua
(UNIPA) with the help of the Institut Français in Indonesia (IFI) and
with corporate sponsorship from the Total Foundation and TIPCO company.
The sequencing was funded by the “Explorations de Monaco”.
Author contributions: J.B.J, I.B.V., K., L.P., D.M. and R.H.
designed research; J.B.J and R.H. design the specific research methods
of data collection and the sampling strategy; J.B.J, R.S.U., K., and
R.H. collected samples and data; T.D. coordinated the biomolecular
analyses; J.B.J., R.S.U. and V.M. performed the bioinformatics analyses;
J.B.J, R.S.U., V.M., T.D., L.P., D.M. and R.H. defined sequencing
strategy, analyzed and interpreted data; J.B.J wrote the initial draft
and designed the figures; J.B.J, R.S.U., V.M., I.B.V., Y.H.S., K., T.D.,
L.P., D.M. and R.H. wrote the paper and approved the final draft; and
L.P., D.M. and R.H. acquired funding to conduct the study.
Competing interests: The authors declare no competing
interests.
Data and materials availability: The sequencing run that
supports the findings of this study will be available in Dryad digital
repository and the metabarcoding pipelines available in GitLab will be
stored in a long-term open access archive following paper acceptance.
References
- Costello, M.J. & Chaudhary, C. (2017) Marine biodiversity,
biogeography, deep-sea, and conservation. Current Biology,27: R511-R527. DOI: 10.1016/j.cub.2017.04.060.
- Barlow, J., França, F., Gardner, T.A., Hicks, C.C., Lennox, G.D.,
Berenguer, E., Castello, L., Economo, E.P., Ferreira, J., Guénard, B.,
Gontijo Leal, C., Isaac, V., Lees, A.C., Parr, C.L., Wilson, S.K.,
Young, P.J. & Graham, N.A.J. (2018) The future of hyperdiverse
tropical ecosystems. Nature, 559: 517–526. DOI:
10.1038/s41586-018-0301-1.
- Lees, A.C. & Pimm, S.L. (2015) Species, extinct before we know them.Current Biology, 5: R177-R180. DOI:
10.1016/j.cub.2014.12.017.
- Díaz, S., Pascual, U., Stenseke, M., Martín-lópez, B., Watson, R.T.,
Molnár, Z., Hill, R., Chan, K.M.A. et al (2018) Assessing nature’s
contributions to people. Science, 359: 270-272. DOI:
10.1126/science.aap8826.
- Duffy, J.E., Godwyn, C.M. & Cardinale, B.J. (2017) Biodiversity
effects in the wild are common and as strong as key drivers of
productivity. Nature, 0: 1-4. DOI:
10.1038/nature23886.
- Juhel, J.B., Vigliola, L., Wantiez, L., Letessier, T.B., Meeuwig, J.J.
& Mouillot, D. (2019) Isolation and no-entry marine reserves mitigate
anthropogenic impacts on grey reef shark behavior. Scientific
reports, 9: 2897. DOI: 10.1038/s41598-018-37145-x.
- Brandl, S.J., Goatley, C.H.R., Bellwood, D.R. & Tornabene, L., (2018)
The hidden half: ecology and evolution of cryptobenthic fishes on
coral reefs. Biological Reviews, 93: 1846-1873. DOI:
10.1111/brv.124233.
- Garlapati, D., Charankumar, B., Ramu, K., Madeswaran, P. & Ramana
Murthy, M.V. (2019) A review on the applications and recent advances
in environmental DNA (eDNA) metagenomics. Reviews in
Environmental Science and Bio/Technology. 18: 389. DOI:
10.1007/s11157-019-09501-4.
- Boussarie, G., Bakker, J., Wangensteen, O.S., Mariani, S., Bonin, L.,
Juhel, J.-B., Kiszka, J.J., Kulbicki, M., Manel, S., Robbins, W.D.,
Vigliola, L. & Mouillot, D. (2018) Environmental DNA illuminates the
dark diversity of sharks. Science Advances, 4:
eaap9661. DOI: 10.1126/sciadv.aap9661.
- Fukumoto, S., Ushimaru, A. & Minamoto, T. (2015) A basin-scale
application of environmental DNA assessment for rare endemic species
and closely related exotic species in rivers: a case study of giant
salamanders in Japan. Journal of Applied Ecology, 52:
358-365. DOI: 10.1111/1365-2664.12392.
- Ruppert, K.M., Kline, R.J. & Rahman, Md S. (2019) Past, present, and
future of environmental DNA (eDNA) metabarcoding: a systematic review
in methods, monitoring, and applications of global eDNA. Global
Ecology and Conservation, 17: e00547. DOI:10.1016/j.gecco.2019.e00547.
- Mahé, F., Rognes, T., Quince, C., de Vargas, C. & Dunthorn, M. (2014)
Swarm: robust and fast clustering method for amplicon-based studies.PeerJ, 2: e593. DOI: 10.7717/peerj.593.
- Brandl, S.J., Rasher, D.B., Côté, I.M., Casey, J.M., Darling, E.S.,
Lefcheck, J.S. & Duffy, J.E. (2019) Coral reef ecosystem functioning:
eight core processes and the role of biodiversity. Frontiers in
Ecology and the Environment. 17:445-454. DOI:
10.1002/fee.2088.
- Veron, J.E.N., Devantier, L.M., Turak, E., Green, A.L., Kininmonth,
S., Stafford-Smith, M. & Peterson, N. (2009) Delineating the Coral
Triangle. Galaxea, Journal of Coral Reef Studies, 11:
91-100. DOI: 10.3755/galaxea.11.91.
- Allen, G.R. & Erdmann, M.V. (2012) Reef fishes of the East Indies.
Volumes I-III. Tropical Reef Research, Perth, Australia. ISBN:
978-0-9872600-0-0. 1,292 p.
- Mangubhai, S., Erdman, M.V., Wilson, J.R., Huffard, C.L., Ballamu, F.,
Hidayat, N.I., Hitipeuw, C., Lazuardi, M.E., Muhajir, Pada, D., Purba,
G., Rotinsulu, C., Rumetna, L., Sumolang, K. & Wen, W. (2012) Papuan
Bird’s Head seascape: Emerging threats and challenges in the global
center of marine biodiversity. Marine Pollution Bulletin,64: 2279-2295. DOI: 10.1016/j.marpolbul.2012.07.024.
- Kulbicki, M., Parravicini, V., Bellwood, D.R., Arias-Gonzalez, E.,
Chabanet, P., Floeter, S.R., Friedlander, A., McPherson, J., Myers,
R.E., Vigliola, L., Mouillot, D. (2013) Global Biogeography of Reef
Fishes: A Hierarchical Quantitative Delineation of Regions. Plos
One, 8: e81847. DOI: 10.1371/journal.pone.0081847.
- Mora, C., Chittaro, P.M., Sale, P.F., Kritzer, J.P. & Ludsin, S.A.
(2003) Patterns and processes in reef fish diversity. Nature,421: 933-936. DOI: 10.1038/nature01393.
- Hubert, N., Dettai, A., Pruvost, P., Cruaud, C., Kulbicki, M., Myers,
R. & Borsa, P. (2017) Geography and life
history traits account for the accumulation of cryptic diversity among
Indo-West Pacific coral reef fishes. Marine Ecology Progress
Series, 583: 179-193. DOI: 10.3354/meps12316.
- Leprieur, F., Descombes, P., Gaboriau, T., Cowman, P.F., Parravicini,
V., Kulbicki, M., Melian, C.J., de Santana, C.N., Heine, C., Mouillot,
D., Bellwood, D.R. & Pellissier, L. (2016) Plate tectonics drive
tropical reef biodiversity dynamics. Nature Communications,7: 11461. DOI: 10.1038/ncomms11461.
- Gaboriau, T., Albouy, C., Descombes, P., Mouillot, D., Pellissier, L.
& Leprieur, F. (2019) Ecological constraints coupled with deep_time
habitat dynamics predict the latitudinal diversity gradient in reef
fishes. Proceedings of the Royal Society B, 286:
20191506. DOI: 0.1098/rspb.2019.1506.
- Pelissier, L., Leprieur, F., Parravicini, V., Cowman, P.F. &
Kulbicki, M. (2014) Quaternary coral reef refugia preserved fish
diversity. Science, 344: 1016-109. DOI:
10.1126/science.1249853.
- Exton, D.A., Ahmadia, G.N., Cullen-Unsworth, L.C., Jompa, J., May, D.,
Rice, J., Simonin, P.W., Unsworth, R.K.F. & SmithD.J. (2019)
Artisanal fish fences pose broad and unexpected threats to the
tropical coastal seascape. Nature Communications, 10:
2100. DOI: 10.1038/s41467-019-10051-0.
- Jones, L.A., Mannion, P.D., Farnsworth, A., Valdes, P.J., Kelland,
S.-J. & Allison, P.A. (2019) Coupling of palaeontological and
neontological reef coral data improves forecasts of biodiversity
responses under climatic change. Royal Society Open Science,6: 182111. DOI: 10.1098/rsos.182111.
- Ainsworth, C.H., Pitcher, T.J. & Rotinsulu, C. (2008) Evidence of
fishery depletions and shifting cognitive baselines in Eastern
Indonesia. Biological Conservation, 141: 848-859. DOI:
10.1016/j.biocon.2008.01.006.
- Valentini, A., Taberlet, P., Miaud, C., Civade, R., Herder, J.,
Thomsen, P.F., Bellemain, E., Besnard, A., Coissac, E., Boyer, F.,
Gaboriaud, C., Jean, P., Poulet, N., Roset, N., Copp, G.H., Geniez,
P., Pont, D., Argillier, C., Baudoin, J.-M., Peroux, T., Crivelli,
A.J., Olivier, A., Acqueberge, M., Le Brun, M., Møller, P.R.,
Willerslev, E. & Dejean, T. (2016) Next-generation monitoring of
aquatic biodiversity using environmental DNA metabarcoding.Molecular Ecology, 25: 929–942. DOI:
10.1111/mec.13428.
- Goldberg, C.S., Turner, C.R., Deiner, K., Klymus, K.E., Thomsen, P.F.,
Murphy, M.A., Spear, S.F., McKee, A., Oyler-McCance, S.J., Cornman,
R.S., Laramie, M.B., Mahon, A.R., Lance, R.F., Pilliod, D.S.,
Strickler, K.M., Waits, L.P., Fremier, A.K., Takahara, T., Herder,
J.E. & Taberlet, P. (2016) Critical considerations for the
application of environmental DNA methods to detect aquatic species.Methods in Ecology and Evolution, 7: 1299-1307. DOI:
10.1111/2041-210X.12595.
- Pont, D., Rocle, M., Valentini, A., Civade, R., Jean, P., Maire, A.,
Roset, N., Schabuss, M., Zornig, H., Dejean, T. (2018) Environmental
DNA reveals quantitative patterns of fish biodiversity in large rivers
despite its downstream transportation. Scientific Reports,8: 10361. DOI: 10.1038/s41598-018-28424-8.
- Ficetola, G.T., Coissac, E., Zundel, S., Riaz, T., Shehzad, W.,
Bessière, J., Taberlet, P. & Pompanon, F. (2010) An in silicoapproach for the evaluation of DNA barcodes. BMC Genomics,11: 434. DOI: 10.1186/1471-2164-11-434.
- Baker, W., van den Broek, Camon, E., Hingamp, P., Sterk, P., Stoesser,
G. & Tuli, M.A. (2000) The EMBL nucleotide sequence database.Nucleic Acids Research, 28: 19-23. DOI:
10.1093/nar/gki098.
- Boyer, F., Mercier, C., Bonin, A., Le Bras, Y., Taberlet, P. &
Coissac, E. (2016) OBITOOLS: a UNIX-inspired software package for DNA
metabarcoding. Molecular Ecology Resources, 16:
176-182. DOI: 10.1111/1755-0998.12428.
- Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettan,
P.A., McWilliams, H., Valentin, F., Wallace, I.M., Wilm, A., Lopez,
R., Thompson, J.D., Gibson, T.J. & Higgins, D.G. (2007) Clustal W and
Clustal X version 2.0. Bioinformatics, 23: 2947-2948.
DOI: 10.1093/bioinformatics/btm404.
- Kearse, M., Moir, R., Wilson, A., Stones-Havas,
S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz,
Duran, C., Thierer, T., Ashton, B., Meintjes, P. & Drummond, A.
(2012) Geneious basic: an integrated and extendable desktop
software platform for the organization and analysis of sequence
data. Bioinformatics, 28: 1647–1649.DOI: 10.1093/bioinformatics/bts19.
- Aho, K., Derryberry, D. & Peterson, T. (2014) Model selection for
ecologists: the worldviews of AIC and BIC. Ecology,95: 631-636. DOI: 10.1890/13-1452.1.
- Deiner, K., Bik, H.M., Mächler, E., Seymour, M., Lacoursière-Roussel,
A., Altermatt, F., Creer, S., Bista, I., Lodge, D.M., de Vere, N.,
Pfendrer, M.E. & Bernatchez, L. (2017) Environmental DNA
metabarcoding: Transforming how we survey animal and plant
communities. Molecular Ecology, 26:5872-5895. DOI:
10.1111/mec.14350.
- Collins, R.A., Bakker, J., Wangensteen, O.S., Soto, A.Z., Corrigan,
L., Sims, D.W., Genner, M.J. & Mariani, S. (2019) Non-specific
amplification compromises environmental DNA metabarcoding with COI.Methods in Ecology and Evolution, 10: 1985-2001. DOI:
10.1111/2041-210X.13276.
- Wadrop, E., Hobbs, J.-P., Randall, J.E., DiBattista, J.D., Rocha,
L.A., Kosaki, R.K., Berumen, M.L. & Bowen, B.W. (2016)
Phylogeography, population structure and evolution of coral-eating
butterflyfishes (Family Chaetodontidae, genus Chaetodon,
subgenus Corallochaetodon). Journal of Biogeography,43: 1116-1129. DOI: 10.1111/jbi.12680.
- Pinheiro, H.T., Moreau, S., Daly, M. & Rocha, L. A. (2019) Will DNA
barcoding meet taxonomic needs? Science, 365:
873–875. DOI: 10.1126/science.aay7174.
- Pawlowski, J., Kelly-Quinn, M., Altermatt, F.,
Apothéloz-Perret-Gentil, L., Beja, P., Boggero, A., …, Kahlert,
M. (2018). The future of biotic indices in the ecogenomic era:
Integrating (e)DNA metabarcoding in biological assessment of aquatic
ecosystems. Science of the Total Environment, 637-638:
1295-1310. DOI: 10.1016/j.scitotenv.2018.05.002.
- Lladó Fernández, S., Větrovský, T. & Baldrian, P. (2019) The concept
of operational taxonomic units revisited: genomes of bacteria that are
regarded as closely related are often highly dissimilar. Folia
Microbiologica, 64: 19–23. DOI: 10.1007/s12223-018-0627-y.
- Cordier, T., Esling, P., Lejzerowicz, F., Visco, J., Ouadahi, A.,
Martins, C., Cedhagen, T. & Pawlowski, J. (2017) Predicting the
ecological quality status of marine environments from eDNA
metabarcoding data using supervised machine learning.Environmental Science & Technology, 51: 9118-9126.
DOI: 10.1021/acs.est.7b01518.
- Wangensteen, O., Palacín, C., Guardiola, M. & Turon, X. (2018) DNA
metabarcoding of littoral hard-bottom communities: high diversity and
database gaps revealed by two molecular markers. PeerJ,6: e4705. DOI: 10.7717/peerj.4705.
- Stat, M., Jeffrey, J., DiBattista, J.D., Newman, S.J., Bunce, M. &
Harvey, E.S. (2018) Combined use of eDNA metabarcoding and video
surveillance for the assessment of fish biodiversity.Conservation Biology, 33: 196-205. DOI:
10.1111/cobi.13183.
- Duffy, J.E., Lelcheck, J.S., Stuart-Smith, R.D., Navarrete, S.A. &
Edgar, G.J. (2016) Biodiversity enhances reef fish biomass and
resistance to climate change. Proceedings of the National
Academy of Sciences, 113: 6230-6235. DOI:
10.1073/pnas.1524465113.