Pan-regional marine benthic cryptobiome biodiversity patterns revealed by metabarcoding Autonomous Reef Monitoring Structures.
biodiversity
climate change
dispersal limitation
ecological monitoring
ecological niche
ecosystem connectivity
metapopulation
mitochondrial cytochrome oxidase I (COI)
Journal
Molecular ecology
ISSN: 1365-294X
Titre abrégé: Mol Ecol
Pays: England
ID NLM: 9214478
Informations de publication
Date de publication:
12 2020
12 2020
Historique:
received:
24
10
2019
revised:
10
09
2020
accepted:
08
10
2020
pubmed:
17
10
2020
medline:
22
6
2021
entrez:
16
10
2020
Statut:
ppublish
Résumé
Autonomous Reef Monitoring Structures (ARMS) have been applied worldwide to characterize the critical yet frequently overlooked biodiversity patterns of marine benthic organisms. In order to disentangle the relevance of environmental factors in benthic patterns, here, through standardized metabarcoding protocols, we analyse sessile and mobile (<2 mm) organisms collected using ARMS deployed across six regions with different environmental conditions (3 sites × 3 replicates per region): Baltic, Western Mediterranean, Adriatic, Black and Red Seas, and the Bay of Biscay. A total of 27,473 Amplicon Sequence Variants (ASVs) were observed ranging from 1,404 in the Black Sea to 9,958 in the Red Sea. No ASVs were shared among all regions. The highest number of shared ASVs was between the Western Mediterranean and the Adriatic Sea (116) and Bay of Biscay (115). Relatively high numbers of ASVs (103), mostly associated with the genus Amphibalanus, were also shared between the lower salinity seas (Baltic and Black Seas). We found that compositional differences in spatial patterns of rocky-shore benthos are determined slightly more by dispersal limitation than environmental filtering. Dispersal limitation was similar between sessile and mobile groups, while the sessile group had a larger environmental niche breadth than the mobile group. Further, our study can provide a foundation for future evaluations of biodiversity patterns in the cryptobiome, which can contribute up to 70% of the local biodiversity.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
4882-4897Informations de copyright
© 2020 John Wiley & Sons Ltd.
Références
Alberto, F., Raimondi, P. T., Reed, D. C., Watson, J. R., Siegel, D. A., Mitarai, S., Coelho, N., & Serrão, E. A. (2011). Isolation by oceanographic distance explains genetic structure for Macrocystis pyrifera in the Santa Barbara Channel. Molecular Ecology, 20(12), 2543-2554. https://doi.org/10.1111/j.1365-294X.2011.05117.x
Al-Rshaidat, M. M. D., Snider, A., Rosebraugh, S., Devine, A. M., Devine, T. D., Plaisance, L., Knowlton, N., & Leray, M. (2016). Deep COI sequencing of standardized benthic samples unveils overlooked diversity of Jordanian coral reefs in the northern Red Sea. Genome, 59(9), 724-737. https://doi.org/10.1139/gen-2015-0208
Andersen, J. H., Halpern, B. S., Korpinen, S., Murray, C., & Reker, J. (2015). Baltic Sea biodiversity status vs. cumulative human pressures. Estuarine, Coastal and Shelf Science, 161, 88-92. https://doi.org/10.1016/j.ecss.2015.05.002
Andrews, S. (2010). FastQC: A quality control tool for high throughput sequence data.
Arnaud-Haond, S., Migliaccio, M., Diaz-Almela, E., Teixeira, S., Vliet, M. S. V. D., Alberto, F., Procaccini, G., Duarte, C. M., & Serrão, E. A. (2007). Vicariance patterns in the Mediterranean Sea: East-west cleavage and low dispersal in the endemic seagrass Posidonia oceanica. Journal of Biogeography, 34(6), 963-976. https://doi.org/10.1111/j.1365-2699.2006.01671.x
Assis, J., Tyberghein, L., Bosch, S., Verbruggen, H., Serrão, E. A., & Clerck, O. D. (2018). Bio-ORACLE v2.0: Extending marine data layers for bioclimatic modelling. Global Ecology and Biogeography, 27(3), 277-284. https://doi.org/10.1111/geb.12693
Bahri-Sfar, L., Lemaire, C., Hassine, O. K. B., & Bonhomme, F. (2000). Fragmentation of sea bass populations in the western and eastern Mediterranean as revealed by microsatellite polymorphism. Proceedings of the Royal Society of London B: Biological Sciences, 267(1446), 929-935.
Barbier, E. B., Hacker, S. D., Koch, E. W., Stier, A. C., & Silliman, B. R. (2011). Estuarine and coastal ecosystems and their services.
Benović, A. (1997). The history, present condition, and future of the molluscan fisheries of Croatia. In C.L. MacKenzie V.G. Burrel A. Rosenfield & W.L. Hobar (Eds.), The history, present condition, and future of the molluscan fisheries of North and Central America and Europe (pp. 217-226). U.S. Department of Commerce.
Bestová, H., Munoz, F., Svoboda, P., Škaloud, P., & Violle, C. (2018). Ecological and biogeographical drivers of freshwater green algae biodiversity: From local communities to large-scale species pools of desmids. Oecologia, 186(4), 1017-1030. https://doi.org/10.1007/s00442-018-4074-x
Borja, A., Aguirrezabalaga, F., Martínez, J., Sola, J. C., García-Arberas, L., & Gorostiaga, J. M. (2004). Benthic communities, biogeography and resources management. Oceanography and Marine Environment of the Basque Country, 70(18), 455-492.
Borja, A., Amouroux, D., Anschutz, P., Gómez-Gesteira, M., Uyarra, M. C., & Valdés, L. (2019). The Bay of Biscay. In C. Sheppard (Eds.), World Seas: An environmental evaluation (pp. 113-152). Elsevier: Academic Press.
Borsa, P., Naciri, M., Bahri, L., Chikhi, L., Garcia de Leon, F. J., Kotoulas, G., & Bonhomme, F. (1997). Infraspecific zoogeography of the Mediterranean: population genetic analysis on sixteen Atlanto-Mediterranean species (fishes and invertebrates). Vie et Milieu (France).
Burgess, S. C., Baskett, M. L., Grosberg, R. K., Morgan, S. G., & Strathmann, R. R. (2016). When is dispersal for dispersal? Unifying marine and terrestrial perspectives. Biological Reviews, 91(3), 867-882. https://doi.org/10.1111/brv.12198
Cahill, A. E., Pearman, J. K., Borja, A., Carugati, L., Carvalho, S., Danovaro, R., Dashfield, S., David, R., Féral, J.-P., Olenin, S., Šiaulys, A., Somerfield, P. J., Trayanova, A., Uyarra, M. C., & Chenuil, A. (2018). A comparative analysis of metabarcoding and morphology-based identification of benthic communities across different regional seas. Ecology and Evolution, 8(17), 8908-8920. https://doi.org/10.1002/ece3.4283
Callahan, B. J., McMurdie, P. J., Rosen, M. J., Han, A. W., Johnson, A. J. A., & Holmes, S. P. (2016). DADA2: High-resolution sample inference from Illumina amplicon data. Nature Methods, 13(7), 581. https://doi.org/10.1038/nmeth.3869
Carvalho, S., Aylagas, E., Villalobos, R., Kattan, Y., Berumen, M. L., & Pearman, J. K. (2019). Beyond the visual: Using metabarcoding to characterize the hidden reef cryptobiome. Proceedings of the Royal Society B: Biological Sciences, 286(1896), 20182697. https://doi.org/10.1098/rspb.2018.2697
Chave, J. (2004). Neutral theory and community ecology. Ecology Letters, 7(3), 241-253. https://doi.org/10.1111/j.1461-0248.2003.00566.x
Chust, G., Villarino, E., Chenuil, A., Irigoien, X., Bizsel, N., Bode, A., Broms, C., Claus, S., Fernández de Puelles, M. L., Fonda-Umani, S., Hoarau, G., Mazzocchi, M. G., Mozetič, P., Vandepitte, L., Veríssimo, H., Zervoudaki, S., & Borja, A. (2016). Dispersal similarly shapes both population genetics and community patterns in the marine realm. Scientific Reports, 6, 28730. https://doi.org/10.1038/srep28730
Coen, L. D. (1988). Herbivory by Caribbean majid crabs: Feeding ecology and plant susceptibility. Journal of Experimental Marine Biology and Ecology, 122(3), 257-276. https://doi.org/10.1016/0022-0981(88)90127-X
Coll, M., Piroddi, C., Steenbeek, J., Kaschner, K., Ben Rais Lasram, F., Aguzzi, J., Ballesteros, E., Bianchi, C. N., Corbera, J., Dailianis, T., Danovaro, R., Estrada, M., Froglia, C., Galil, B. S., Gasol, J. M., Gertwagen, R., Gil, J., Guilhaumon, F., Kesner-Reyes, K., … Voultsiadou, E. (2010). The Biodiversity of the Mediterranean Sea: Estimates, Patterns, and Threats. PLoS One, 5(8), e11842. https://doi.org/10.1371/journal.pone.0011842
Cordes, E. E., Jones, D. O. B., Schlacher, T. A., Amon, D. J., Bernardino, A. F., Brooke, S., Carney, R., DeLeo, D. M., Dunlop, K. M., Escobar-Briones, E. G., Gates, A. R., Génio, L., Gobin, J., Henry, L.-A., Herrera, S., Hoyt, S., Joye, M., Kark, S., Mestre, N. C., … Witte, U. (2016). Environmental impacts of the deep-water oil and gas industry: A review to guide management strategies. Frontiers in Environmental Science, 4, https://doi.org/10.3389/fenvs.2016.00058
Costanza, R., d'Arge, R., de Groot, R., Farber, S., Grasso, M., Hannon, B., Limburg, K., Naeem, S., O'Neill, R. V., Paruelo, J., Raskin, R. G., Sutton, P., & van den Belt, M. (1997). The value of the world’s ecosystem services and natural capital. Nature, 387(6630), 253. https://doi.org/10.1038/387253a0
Costello, M. J., & Wilson, S. P. (2011). Predicting the number of known and unknown species in European seas using rates of description. Global Ecology and Biogeography, 20(2), 319-330. https://doi.org/10.1111/j.1466-8238.2010.00603.x
Cowen, R., Gawarkiewicz, G., Pineda, J., Thorrold, S., & Werner, F. (2007). Population connectivity in marine systems: An overview. Oceanography, 20(3), 14-21. https://doi.org/10.5670/oceanog.2007.26
Danovaro, R., Carugati, L., Berzano, M., Cahill, A. E., Carvalho, S., Chenuil, A., Corinaldesi, C., Cristina, S., David, R., Dell'Anno, A., Dzhembekova, N., Garcés, E., Gasol, J. M., Goela, P., Féral, J.-P., Ferrera, I., Forster, R. M., Kurekin, A. A., Rastelli, E., … Borja, A. (2016). Implementing and innovating marine monitoring approaches for assessing marine environmental status. Frontiers in Marine Science, 3, 213. https://doi.org/10.3389/fmars.2016.00213
David, R., Uyarra, M. C., Carvalho, S., Anlauf, H., Borja, A., Cahill, A. E., Carugati, L., Danovaro, R., De Jode, A., Feral, J.-P., Guillemain, D., Martire, M. L., D'Avray, L. T. D. V., Pearman, J. K., & Chenuil, A. (2019). Lessons from photo analyses of Autonomous Reef Monitoring Structures as tools to detect (bio-)geographical, spatial, and environmental effects. Marine Pollution Bulletin, 141, 420-429. https://doi.org/10.1016/j.marpolbul.2019.02.066
Debes, P. V., Zachos, F. E., & Hanel, R. (2008). Mitochondrial phylogeography of the European sprat (Sprattus sprattus L., Clupeidae) reveals isolated climatically vulnerable populations in the Mediterranean Sea and range expansion in the northeast Atlantic. Molecular Ecology, 17(17), 3873-3888. https://doi.org/10.1111/j.1365-294X.2008.03872.x
Deiner, K., Bik, H. M., Mächler, E., Seymour, M., Lacoursière-Roussel, A., Altermatt, F., Creer, S., Bista, I., Lodge, D. M., de Vere, N., Pfrender, M. E., & Bernatchez, L. (2017). Environmental DNA metabarcoding: Transforming how we survey animal and plant communities. Molecular Ecology, 26(21), 5872-5895. https://doi.org/10.1111/mec.14350
Dray, S., Blanchet, G., Borcard, D., Guenard, G., Jombart, T., Larocque, G., Legendre, P., Madi, N., & Wagner, H. (2016). adespatial: Multivariate Multiscale Spatial Analysis. R package version 0.0-4.
Elbrecht, V., & Leese, F. (2015). Can DNA-based ecosystem assessments quantify species abundance? Testing primer bias and biomass-sequence relationships with an innovative metabarcoding protocol. PLoS One, 10(7), e0130324. https://doi.org/10.1371/journal.pone.0130324
Elliott, M. (2014). Integrated marine science and management: Wading through the morass. Marine Pollution Bulletin, 1(86), 1-4. https://doi.org/10.1016/j.marpolbul.2014.07.026
Enochs, I. C., Toth, L. T., Brandtneris, V. W., Afflerbach, J. C., & Manzello, D. P. (2011). Environmental determinants of motile cryptofauna on an eastern Pacific coral reef. Marine Ecology Progress Series, 438, 105-118. https://doi.org/10.3354/meps09259
Finlay, B. J. (2002). Global dispersal of free-living microbial eukaryote species. Science, 296(5570), 1061-1063.
Fox, J., & Weisberg, S. (2019). An R companion to applied regression (3rd ed.). Sage. Retrieved from https://us.sagepub.com/en-us/nam/an-r-companion-to-applied-regression/book246125
Geller, J., Meyer, C., Parker, M., & Hawk, H. (2013). Redesign of PCR primers for mitochondrial cytochrome c oxidase subunit I for marine invertebrates and application in all-taxa biotic surveys. Molecular Ecology Resources, 13(5), 851-861.
Gratwicke, B., & Speight, M. R. (2005). The relationship between fish species richness, abundance and habitat complexity in a range of shallow tropical marine habitats. Journal of Fish Biology, 66(3), 650-667. https://doi.org/10.1111/j.0022-1112.2005.00629.x
Halpern, B. S., Walbridge, S., Selkoe, K. A., Kappel, C. V., Micheli, F., D’Agrosa, C., Bruno, J. F., Casey, K. S., Ebert, C., Fox, H. E., Fujita, R., Heinemann, D., Lenihan, H. S., Madin, E. M. P., Perry, M. T., Selig, E. R., Spalding, M., Steneck, R., & Fox, H. E. (2008). A global map of human impact on marine ecosystems. Science, 319(5865), 948-952.
Hayward, P. J., & McKinney, F. K. (2002). Northern Adriatic Bryozoa from the vicinity of Rovinj, Croatia. Bulletin of the American Museum of Natural History, 2002(270), 1-139.
Hazeri, G., Rahayu, D. L., Subhan, B., Sembiring, A., Anggoro, A. W., Ghozali, A. T., & Madduppa, H. H. (2019). Latitudinal species diversity and density of cryptic crustacean (Brachyura and Anomura) in micro-habitat Autonomous Reef Monitoring Structures across Kepulauan Seribu, Indonesia. Biodiversitas Journal of Biological Diversity, 20(5), https://doi.org/10.13057/biodiv/d200540
Hervé, M. (2017). RVAideMemoire: Diverse basic statistical and graphical functions (version 0.9-66). Retrieved from https://CRAN.R-project.org/package=RVAideMemoire
Hubbell, S. P. (1997). A unified theory of biogeography and relative species abundance and its application to tropical rain forests and coral reefs. Coral Reefs, 16(1), S9-S21. https://doi.org/10.1007/s003380050237
Hubbell, S. P. (2001). The Unified Neutral Theory of Biodiversity and Biogeography. Princeton University Press.
Hutchinson, G. E. (1957). Concluding remarks, Cold Spring Harbor Symposium. Quantitative Biology, 22, 415-427. https://doi.org/10.1101/SQB.1957.022.01.039
Igić, L. (2007). Cirripedia of Adriatic. Studia Marina, 24(2), 1-168.
Jönsson, B. F., & Watson, J. R. (2016). The timescales of global surface-ocean connectivity. Nature Communications, 7, 11239. https://doi.org/10.1038/ncomms11239
Kelly, R. P. (2016). Making environmental DNA count. Molecular Ecology Resources, 16(1), 10-12. https://doi.org/10.1111/1755-0998.12455
Kinlan, B. P., & Gaines, S. D. (2003). Propagule dispersal in marine and terrestrial environments: A community perspective. Ecology, 84(8), 2007-2020. https://doi.org/10.1890/01-0622
Klymus, K. E., Richter, C. A., Chapman, D. C., & Paukert, C. (2015). Quantification of eDNA shedding rates from invasive bighead carp Hypophthalmichthys nobilis and silver carp Hypophthalmichthys molitrix. Biological Conservation, 183, 77-84. https://doi.org/10.1016/j.biocon.2014.11.020
Korpinen, S., & Andersen, J. H. (2016). A global review of cumulative pressure and impact assessments in marine environments. Frontiers in Marine Science, 3, 153. https://doi.org/10.3389/fmars.2016.00153
Lanzén, A., Lekang, K., Jonassen, I., Thompson, E. M., & Troedsson, C. (2017). DNA extraction replicates improve diversity and compositional dissimilarity in metabarcoding of eukaryotes in marine sediments. PLoS One, 12(6), e0179443. https://doi.org/10.1371/journal.pone.0179443
Legendre, P., & De Caceres, M. (2013). Beta diversity as the variance of community data: Dissimilarity coefficients and partitioning. Ecology Letters, 16(8), 951-963. https://doi.org/10.1111/ele.12141
Legendre, P., & Legendre, L. (2012). Chapter 1 - Complex ecological data sets. In P. Legendre & L. Legendre (Eds.), Developments in environmental modelling (pp. 1-57). Elsevier.
Leray, M., & Knowlton, N. (2015). DNA barcoding and metabarcoding of standardized samples reveal patterns of marine benthic diversity. Proceedings of the National Academy of Sciences of the United States of America, 112(7), 2076-2081. https://doi.org/10.1073/pnas.1424997112
Leray, M., Yang, J. Y., Meyer, C. P., Mills, S. C., Agudelo, N., Ranwez, V., Boehm, J. T., & Machida, R. J. (2013). A new versatile primer set targeting a short fragment of the mitochondrial COI region for metabarcoding metazoan diversity: Application for characterizing coral reef fish gut contents. Frontiers in Zoology, 10, 34. https://doi.org/10.1186/1742-9994-10-34
Loreau, M. (2000). Biodiversity and ecosystem functioning: Recent theoretical advances. Oikos, 91(1), 3-17. https://doi.org/10.1034/j.1600-0706.2000.910101.x
Lotze, H. K., Guest, H., O’Leary, J., Tuda, A., & Wallace, D. (2018). Public perceptions of marine threats and protection from around the world. Ocean & Coastal Management, 152, 14-22. https://doi.org/10.1016/j.ocecoaman.2017.11.004
Machida, R. J., Leray, M., Ho, S.-L., & Knowlton, N. (2017). Metazoan mitochondrial gene sequence reference datasets for taxonomic assignment of environmental samples. Scientific Data, 4(1), 1-7. https://doi.org/10.1038/sdata.2017.27
Magurran, A. E., Baillie, S. R., Buckland, S. T., Dick, J. M. P., Elston, D. A., Scott, E. M., Smith, R. I., Somerfield, P. J., & Watt, A. D. (2010). Long-term datasets in biodiversity research and monitoring: Assessing change in ecological communities through time. Trends in Ecology & Evolution, 25(10), 574-582. https://doi.org/10.1016/j.tree.2010.06.016
Martin, M. (2011). Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.Journal, 17(1), 10-12. https://doi.org/10.14806/ej.17.1.200
McMurdie, P. J., & Holmes, S. (2013). phyloseq: An R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One, 8(4), e61217. https://doi.org/10.1371/journal.pone.0061217
Micheli, F., Halpern, B. S., Walbridge, S., Ciriaco, S., Ferretti, F., Fraschetti, S., Lewison, R., Nykjaer, L., & Rosenberg, A. A. (2013). Cumulative human impacts on Mediterranean and Black Sea marine ecosystems: Assessing current pressures and opportunities. PLoS One, 8(12), e79889. https://doi.org/10.1371/journal.pone.0079889
Milišić, N. (2007). Glavonošci, puževi i školjke Jadrana. Marjan Tisak.
Mouquet, N., & Loreau, M. (2003). Community patterns in source-sink metacommunities. The American Naturalist, 162(5), 544-557. https://doi.org/10.1086/378857
Narayanaswamy, B. E., Coll, M., Danovaro, R., Davidson, K., Ojaveer, H., & Renaud, P. E. (2013). Synthesis of knowledge on marine biodiversity in European Seas: From census to sustainable management. PLoS One, 8(3), e58909. https://doi.org/10.1371/journal.pone.0058909
Nikula, R., & Väinölä, R. (2003). Phylogeography of Cerastoderma glaucum (Bivalvia: Cardiidae) across Europe: A major break in the Eastern Mediterranean. Marine Biology, 143(2), 339-350. https://doi.org/10.1007/s00227-003-1088-6
Normand, S., Ricklefs, R. E., Skov, F., Bladt, J., Tackenberg, O., & Svenning, J. C. (2011). Postglacial migration supplements climate in determining plant species ranges in Europe. Proceedings of the Royal Society B: Biological Sciences, 278(1725), 3644-3653. https://doi.org/10.1098/rspb.2010.2769
Oksanen, J., Kindt, R., Legendre, P., O’Hara, B., Stevens, M. H. H., Oksanen, M. J., & Suggests, M. (2007). The Vegan Package. Community Ecology Package, 10, 631-637.
Pante, E., & Simon-Bouhet, B. (2013). marmap: A package for importing, plotting and analyzing bathymetric and topographic data in R. PLoS One, 8(9), e73051. https://doi.org/10.1371/journal.pone.0073051
Papadopoulos, L. N., Peijnenburg, K., & Luttikhuizen, P. C. (2005). Phylogeography of the calanoid copepods Calanus helgolandicus and C. euxinus suggests Pleistocene divergences between Atlantic, Mediterranean, and Black Sea populations. Marine Biology, 147(6), 1353-1365.
Pearman, J. K., Anlauf, H., Irigoien, X., & Carvalho, S. (2016). Please mind the gap - Visual census and cryptic biodiversity assessment at central Red Sea coral reefs. Marine Environmental Research, 118, 20-30. https://doi.org/10.1016/j.marenvres.2016.04.011
Pearman, J. K., Aylagas, E., Voolstra, C. R., Anlauf, H., Villalobos, R., & Carvalho, S. (2019). Disentangling the complex microbial community of coral reefs using standardized Autonomous Reef Monitoring Structures (ARMS). Molecular Ecology, 28(15), 3496-3507. https://doi.org/10.1111/mec.15167
Pearman, J. K., Leray, M., Villalobos, R., Machida, R. J., Berumen, M. L., Knowlton, N., & Carvalho, S. (2018). Cross-shelf investigation of coral reef cryptic benthic organisms reveals diversity patterns of the hidden majority. Scientific Reports, 8, 8090. https://doi.org/10.1038/s41598-018-26332-5
Pennesi, C., & Danovaro, R. (2017). Assessing marine environmental status through microphytobenthos assemblages colonizing the Autonomous Reef Monitoring Structures (ARMS) and their potential in coastal marine restoration. Marine Pollution Bulletin, 125(1-2), 56-65. https://doi.org/10.1016/j.marpolbul.2017.08.001
Pereira, J. C., Chaves, R., Bastos, E., Leitão, A., & Guedes-Pinto, H. (2011). An efficient method for genomic DNA extraction from different molluscs species. International Journal of Molecular Sciences, 12(11), 8086-8095. https://doi.org/10.3390/ijms12118086
Plaisance, L., Caley, M. J., Brainard, R. E., & Knowlton, N. (2011). The diversity of coral reefs: What are we missing? PLoS One, 6(10), e25026. https://doi.org/10.1371/journal.pone.0025026
Pocheville, A. (2015). The ecological niche: History and recent controversies. In T. Heams, P. Huneman, G. Lecointre, & M. Silberstein (Eds.), Handbook of evolutionary thinking in the sciences (pp. 547-586). : Springer Netherlands.
R Core Team. (2018). R: A language and environment for statistical computing. : R Foundation for Statistical Computing; 2014.
Ransome, E., Geller, J. B., Timmers, M., Leray, M., Mahardini, A., Sembiring, A., Collins, A. G., & Meyer, C. P. (2017). The importance of standardization for biodiversity comparisons: A case study using autonomous reef monitoring structures (ARMS) and metabarcoding to measure cryptic diversity on Mo’orea coral reefs, French Polynesia. PLoS One, 12(4), e0175066. https://doi.org/10.1371/journal.pone.0175066
Ranwez, V., Harispe, S., Delsuc, F., & Douzert, E. J. P. (2011). MACSE: Multiple Alignment of Coding SEquences accounting for frameshifts and stop codons. PLoS One, 6, e22594. https://doi.org/10.1371/journal.pone.0022594
Ratnasingham, S., & Hebert, P. D. N. (2007). BOLD: The Barcode of Life Data System (www.barcodinglife.org). Molecular Ecology Notes, 7, 355-364. https://doi.org/10.1111/j.1471-8286.2006.01678.x
Reaka, M. L. (1987). Adult-juvenile interactions in benthic reef crustaceans. Bulletin of Marine Science, 41(2), 108-134.
Reaka-Kudla, M. I. (1997). The global biodiversity of coral reefs: A comparison with rain forests. In E.O. Wilson D.E. Wilson & M. I. Reaka-Kudla (Eds.), Biodiversity II: Understanding and protecting our biological resources (pp. 83-108).
Reiss, H., Birchenough, S., Borja, A., Buhl-Mortensen, L., Craeymeersch, J., Dannheim, J., Darr, A., Galparsoro, I., Gogina, M., Neumann, H., Populus, J., Rengstorf, A. M., Valle, M., van Hoey, G., Zettler, M. L., & Degraer, S. (2015). Benthos distribution modelling and its relevance for marine ecosystem management. ICES Journal of Marine Science, 72(2), 297-315. https://doi.org/10.1093/icesjms/fsu107
Richter, C., Wunsch, M., Rasheed, M., Kötter, I., & Badran, M. I. (2001). Endoscopic exploration of Red Sea coral reefs reveals dense populations of cavity-dwelling sponges. Nature, 413, 725-730. https://doi.org/10.1038/35099547
Rodríguez-Prieto, C., & Vergés, A. (2001). Geographical Distribution, habitat and reproductive phenology of the genus Kallymenia (Gigartinales, Rhodophyta) from Catalonia, Spain. Botanica Marina, 44(5), 479-492. https://doi.org/10.1515/BOT.2001.054
Rombouts, I., Beaugrand, G., Ibanez, F., Gasparini, S., Chiba, S., & Legendre, L. (2009). Global latitudinal variations in marine copepod diversity and environmental factors. Proceedings of the Royal Society B-Biological Sciences, 276(1670), 3053-3062. https://doi.org/10.1098/rspb.2009.0742
Rothans, T. C., & Miller, A. C. (1991). A link between biologically imported particulate organic nutrients and the detritus food web in reef communities. Marine Biology, 110(1), 145-150. https://doi.org/10.1007/BF01313101
Sammarco, P. W., Kolian, S. R., Warby, R. A. F., Bouldin, J. L., Subra, W. A., & Porter, S. A. (2013). Distribution and concentrations of petroleum hydrocarbons associated with the BP/Deepwater Horizon Oil Spill, Gulf of Mexico. Marine Pollution Bulletin, 73(1), 129-143. https://doi.org/10.1016/j.marpolbul.2013.05.029
Scheffers, S. R., de Goeij, J., van Duyl, F. C., & Bak, R. P. M. (2003). The cave-profilier: A simple tool to describe the 3-D structure of inaccessible coral reef cavities. Coral Reefs, 22, 49-53. https://doi.org/10.1007/s00338-003-0285-6
Seddon, A. W. R., Mackay, A. W., Baker, A. G., Birks, H. J. B., Breman, E., Buck, C. E., Ellis, E. C., Froyd, C. A., Gill, J. L., Gillson, L., Johnson, E. A., Jones, V. J., Juggins, S., Macias-Fauria, M., Mills, K., Morris, J. L., Nogués-Bravo, D., Punyasena, S. W., Roland, T. P., … Witkowski, A. (2014). Looking forward through the past: Identification of 50 priority research questions in palaeoecology. Journal of Ecology, 102(1), 256-267. https://doi.org/10.1111/1365-2745.12195
Selkoe, K. A., & Toonen, R. J. (2011). Marine connectivity: A new look at pelagic larval duration and genetic metrics of dispersal. Marine Ecology Progress Series, 436, 291-305. https://doi.org/10.3354/meps09238
Shanks, A. L. (2009). Pelagic larval duration and dispersal distance revisited. The Biological Bulletin, 216(3), 373-385. https://doi.org/10.1086/BBLv216n3p373
Sherman, K., Okemwa, E. N., & Ntiba, M. J. (2009). Large marine ecosystems of the Indian Ocean: Assessment, sustainability and management. John Wiley & Sons.
Soininen, J., McDonald, R., & Hillebrand, H. (2007). The distance decay of similarity in ecological communities. Ecography, 30(1), 3-12. https://doi.org/10.1111/j.0906-7590.2007.04817.x
Spagnolo, A., Cuicchi, C., Punzo, E., Santelli, A., Scarcella, G., & Fabi, G. (2014). Patterns of colonization and succession of benthic assemblages in two artificial substrates. Journal of Sea Research, 88, 78-86. https://doi.org/10.1016/j.seares.2014.01.007
Tittensor, D. P., Mora, C., Jetz, W., Lotze, H. K., Ricard, D., Berghe, E. V., & Worm, B. (2010). Global patterns and predictors of marine biodiversity across taxa. Nature, 466(7310), 1098-1101. https://doi.org/10.1038/nature09329
Tyberghein, L., Verbruggen, H., Pauly, K., Troupin, C., Mineur, F., & De Clerck, O. (2012). Bio-ORACLE: A global environmental dataset for marine species distribution modelling: Bio-ORACLE marine environmental data rasters. Global Ecology and Biogeography, 21(2), 272-281. https://doi.org/10.1111/j.1466-8238.2011.00656.x
Villarino, E., Watson, J. R., Jönsson, B., Gasol, J. M., Salazar, G., Acinas, S. G., Estrada, M., Massana, R., Logares, R., Giner, C. R., Pernice, M. C., Olivar, M. P., Citores, L., Corell, J., Rodríguez-Ezpeleta, N., Acuña, J. L., Molina-Ramírez, A., González-Gordillo, J. I., Cózar, A., … Chust, G. (2018). Large-scale ocean connectivity and planktonic body size. Nature Communications, 9(1), 142. https://doi.org/10.1038/s41467-017-02535-8
Wang, Q., Garrity, G. M., Tiedje, J. M., & Cole, J. R. (2007). Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology, 73(16), 5261-5267.
Wangensteen, O. S., & Turon, X. (2015). Metabarcoding techniques for assessing biodiversity of marine animal forests. In S. Rossi L. Bramanti A. Gori & C. Orejas (Eds.), Marine animal forests: The ecology of benthic biodiversity hotspots (pp. 1-29).
Weersing, K., & Toonen, R. J. (2009). Population genetics, larval dispersal, and connectivity in marine systems. Marine Ecology Progress Series, 393, 1-12. https://doi.org/10.3354/meps08287
Wickham, H. (2016). ggplot2: Elegant graphics for data analysis. Springer.
Wilson, E. O., & MacArthur, R. H. (1967). The theory of island biogeography.
Wrange, A.-L., André, C., Lundh, T., Lind, U., Blomberg, A., Jonsson, P. J., & Havenhand, J. N. (2014). Importance of plasticity and local adaptation for coping with changing salinity in coastal areas: A test case with barnacles in the Baltic Sea. BMC Evolutionary Biology, 14(1), 156. https://doi.org/10.1186/1471-2148-14-156
Wrange, A.-L., Charrier, G., Thonig, A., Alm Rosenblad, M., Blomberg, A., Havenhand, J. N., Jonsson, P. R., & André, C. (2016). The story of a hitchhiker: Population Genetic patterns in the invasive barnacle balanus (Amphibalanus) improvisus Darwin 1854. PLoS One, 11(1), e0147082. https://doi.org/10.1371/journal.pone.0147082
Zaitsev, Y., & Mamaev, V. (1997). Marine biological diversity in the Black Sea. A Study of Change and Decline United Nations Publications New York, 208.
Zimmerman, T. L., & Martin, J. W. (2004). Artificial reef matrix structures (ARMS): An inexpensive and effective method for collecting coral reef-associated invertebrates. Gulf and Caribbean Research, 16(1), 59-64. https://doi.org/10.18785/gcr.1601.08
Zinger, L., Bonin, A., Alsos, I. G., Bálint, M., Bik, H., Boyer, F., Chariton, A. A., Creer, S., Coissac, E., Deagle, B. E., De Barba, M., Dickie, I. A., Dumbrell, A. J., Ficetola, G. F., Fierer, N., Fumagalli, L., Gilbert, M. T. P., Jarman, S., Jumpponen, A., … Taberlet, P. (2019). DNA metabarcoding-Need for robust experimental designs to draw sound ecological conclusions. Molecular Ecology, 28(8), 1857-1862. https://doi.org/10.1111/mec.15060
Zuur, A., Ieno, E. N., Walker, N., Saveliev, A. A., & Smith, G. M. (2009). Mixed effects models and extensions in ecology with R. Springer-Verlag.