Coastal rocky reef fish monitoring in the context of the Marine Strategy Framework Directive: Environmental DNA metabarcoding complements underwater visual census

Afzali, 2021, Comparing environmental metabarcoding and trawling survey of demersal fish communities in the Gulf of St. Lawrence, Canada, Environ. DNA, 3, 22, 10.1002/edn3.111 Aglieri, 2020, Environmental DNA effectively captures functional diversity of coastal fish communities, Mol. Ecol., 30, 3127, 10.1111/mec.15661 Altschul, 1990, Basic local alignment search tool, J. Mol. Biol., 215, 403, 10.1016/S0022-2836(05)80360-2 Anderson, 2008 Andruszkiewicz, 2017, Biomonitoring of marine vertebrates in Monterey Bay using eDNA metabarcoding, PLoS One, 12, 10.1371/journal.pone.0176343 Arthington, 2016, Fish conservation in freshwater and marine realms: status, threats and management, Aquat. Conserv. Mar. Freshw. Ecosyst., 26, 838, 10.1002/aqc.2712 Bajjouk, 2019, Map of intertidal habitats for the natura 2000 FR5300015 site – Morlaix bay, Ifremer Baker, 2016, Comparative analysis of different survey methods for monitoring fish assemblages in coastal habitats, PeerJ, 4, 10.7717/peerj.1832 Baudrier, 2018, Optimising French fisheries surveys for Marine Strategy Framework Directive integrated ecosystem monitoring, Mar. Pol., 94, 10, 10.1016/j.marpol.2018.04.024 Bessey, 2020, Maximizing fish detection with eDNA metabarcoding, Environ. DNA, 2, 493, 10.1002/edn3.74 Biggs, 2015, Using eDNA to develop a national citizen science-based monitoring programme for the great crested newt (Triturus cristatus), Biol. Conserv., 183, 19, 10.1016/j.biocon.2014.11.029 Bosch, 2017, “How” and “what” matters: sampling method affects biodiversity estimates of reef fishes, Ecol. Evol., 7, 4891, 10.1002/ece3.2979 Boulanger, 2021, Environmental DNA metabarcoding reveals and unpacks a biodiversity conservation paradox in Mediterranean marine reserves, Proc. R. Soc. B Biol. Sci., 288 Boussarie, 2018, Environmental DNA illuminates the dark diversity of sharks, Sci. Adv., 4, 10.1126/sciadv.aap9661 Boyer, 2016, obitools: a unix-inspired software package for DNA metabarcoding, Mol. Ecol. Resour., 16, 176, 10.1111/1755-0998.12428 Bracken, 2019, Identifying spawning sites and other critical habitat in lotic systems using eDNA "snapshots": a case study using the sea lamprey Petromyzon marinus L, Ecol. Evol., 9, 553, 10.1002/ece3.4777 Caldwell, 2016, Reef fish survey techniques: assessing the potential for standardizing methodologies, PLoS One, 11, 10.1371/journal.pone.0153066 Callahan, 2016, DADA2: high-resolution sample inference from Illumina amplicon data, Nat. Methods, 13, 581, 10.1038/nmeth.3869 Clarke, K.R., Gorley, R.N., 2006. PRIMER v6: User Manual/Tutorial (Ed. Plymouth Marine Laboratory), Plymouth, UK. Collins, 2019, Non-specific amplification compromises environmental DNA metabarcoding with COI, Methods Ecol. Evol., 10, 1985, 10.1111/2041-210X.13276 Collins, 2021, Meta-Fish-Lib: a generalised, dynamic DNA reference library pipeline for metabarcoding of fishes, J. Fish. Biol., 99, 1446, 10.1111/jfb.14852 Collins, 2018, Persistence of environmental DNA in marine systems, Commun. Biol., 1, 1, 10.1038/s42003-018-0192-6 Costello, 2017, Methods for the study of marine biodiversity, 129 Couton, 2022, Water eDNA metabarcoding is effective in detecting non-native species in marinas, but detection errors still hinder its use for passive monitoring, Biofouling, 38, 367, 10.1080/08927014.2022.2075739 Danovaro, 2016, Implementing and innovating marine monitoring approaches for assessing marine environmental status, Front. Mar. Sci., 3, 213, 10.3389/fmars.2016.00213 Deiner, 2017, Environmental DNA metabarcoding: transforming how we survey animal and plant communities, Mol. Ecol., 26, 5872, 10.1111/mec.14350 DiBattista, 2017, Assessing the utility of eDNA as a tool to survey reef-fish communities in the Red Sea, Coral Reefs, 36, 1245, 10.1007/s00338-017-1618-1 DiBattista, 2019, Digging for DNA at depth: Rapid universal metabarcoding surveys (RUMS) as a tool to detect coral reef biodiversity across a depth gradient, PeerJ, 7, e6379, 10.7717/peerj.6379 Doi, 2019, Evaluation of detection probabilities at the water-filtering and initial PCR steps in environmental DNA metabarcoding using a multispecies site occupancy model, Sci. Rep., 9, 3581, 10.1038/s41598-019-40233-1 Dray, 2018 Dray, 2007, The ade4 package: implementing the duality diagram for ecologists, J. Stat. Software, 22, 1, 10.18637/jss.v022.i04 Dunn, 2003, The occurrence of Symphodus bailloni on the south coast of England, Mar. Biol. Assoc. U. K. J. Mar. Biol. Assoc. U. K., 83, 875, 10.1017/S002531540300794Xh Eble, 2020, Chapter two - marine environmental DNA: approaches, applications, and opportunities, 141, 10.1016/bs.amb.2020.01.001 Edgar, 2020, Reef Life Survey: establishing the ecological basis for conservation of shallow marine life, Biol. Conserv., 252, 10.1016/j.biocon.2020.108855 Escoufier, 1973, Le Traitement des Variables Vectorielles, Biometrics, 29, 751, 10.2307/2529140 Figueroa-Pico, 2020, Turbidity: a key factor in the estimation of fish species richness and abundance in the rocky reefs of Ecuador, Ecol. Indicat., 111, 10.1016/j.ecolind.2019.106021 Fraija-Fernandez, 2020, Marine water environmental DNA metabarcoding provides a comprehensive fish diversity assessment and reveals spatial patterns in a large oceanic area, Ecol. Evol., 10, 7560, 10.1002/ece3.6482 Franco, 2012, Assessment of fish assemblages in coastal lagoon habitats: effect of sampling method, Estuar. Coast. Shelf Sci., Assessing Ecological Quality in Estuarine and Coastal Systems – Functional Perspective, 112, 115 Froese, 2019 Frøslev, 2017, Algorithm for post-clustering curation of DNA amplicon data yields reliable biodiversity estimates, Nat. Commun., 8, 1188, 10.1038/s41467-017-01312-x Furlan, 2019, eDNA surveys to detect species at very low densities: a case study of European carp eradication in Tasmania, Australia, J. Appl. Ecol., 56, 2505, 10.1111/1365-2664.13485 Gilbey, 2021, Life in a drop: sampling environmental DNA for marine fishery management and ecosystem monitoring, Mar. Pol., 124, 10.1016/j.marpol.2020.104331 Göktürk, 2012, A new record for occurrence of Symphodus bailloni (osteichthyes: perciformes: Labridae) in the western black sea coast of Turkey, Sci. World J., 2012, 10.1100/2012/615318 Harmelin, 1987, Structure et variabilité de I’ichtyofaune d’une zone rocheuse protégée en Méditerranée (Pare national de Port-Cros, France), Mar. Ecol., 8, 263, 10.1111/j.1439-0485.1987.tb00188.x Harrison, 2019, Predicting the fate of eDNA in the environment and implications for studying biodiversity, Proc. R. Soc. B Biol. Sci., 286 Henderson, 1984, Long-term stability of a sand smelt (Atherina presbyter Cuvier) population subject to power station cropping, J. Appl. Ecol., 21, 1, 10.2307/2403034 Holmlund, 1999, Ecosystem services generated by fish populations, Ecol. Econ., 29, 253, 10.1016/S0921-8009(99)00015-4 Hsieh, 2016, iNEXT: an R package for rarefaction and extrapolation of species diversity (Hill numbers), Methods Ecol. Evol., 7, 1451, 10.1111/2041-210X.12613 Hughes, 2018, Comprehensive phylogeny of ray-finned fishes (Actinopterygii) based on transcriptomic and genomic data, Proc. Natl. Acad. Sci. USA, 115, 6249, 10.1073/pnas.1719358115 Iglesias, 2020 Jackson, 2006, Seagrass complexity hierarchies: influence on fish groups around the coast of Jersey (English Channel), J. Exp. Mar. Biol. Ecol., 330, 38, 10.1016/j.jembe.2005.12.016 Jeunen, 2019, Environmental DNA (eDNA) metabarcoding reveals strong discrimination among diverse marine habitats connected by water movement, Mol. Ecol. Resour., 19, 426, 10.1111/1755-0998.12982 Jeunen, 2020, Water stratification in the marine biome restricts vertical environmental DNA (eDNA) signal dispersal, Environ. DNA, 2, 99, 10.1002/edn3.49 Juhel, 2020, Accumulation curves of environmental DNA sequences predict coastal fish diversity in the coral triangle, Proc. R. Soc. B Biol. Sci., 287 Kelly, 2018, The effect of tides on nearshore environmental DNA, PeerJ, 6, 10.7717/peerj.4521 Kelly, 2016, Genetic signatures of ecological diversity along an urbanization gradient, PeerJ, 4, e2444, 10.7717/peerj.2444 Lamb, 2019, How quantitative is metabarcoding: a meta-analytical approach, Mol. Ecol., 28, 420, 10.1111/mec.14920 Lamy, 2021, Environmental DNA reveals the fine-grained and hierarchical spatial structure of kelp forest fish communities, Sci. Rep., 11, 10.1038/s41598-021-93859-5 Legendre, 2013, Beta diversity as the variance of community data: dissimilarity coefficients and partitioning, Ecol. Lett., 16, 951, 10.1111/ele.12141 Legendre, 2012 Livore, 2021, Biodiversity monitoring in rocky shores: challenges of devising a globally applicable and cost-effective protocol, Ocean Coast Manag., 205, 10.1016/j.ocecoaman.2021.105548 Mahé, 2015, Swarm v2: highly-scalable and high-resolution amplicon clustering, PeerJ, 3, 10.7717/peerj.1420 Maran, 2011, Observations du crénilabre de Baillon Symphodus bailloni (Valenciennes, 1839), Labridae, dans et autour de la rade de Brest (Nord Bretagne, France), Bull. Société Sci. Nat. Ouest Fr., 33, 57 Marques, 2021, Use of environmental DNA in assessment of fish functional and phylogenetic diversity, Conserv. Biol., 35, 1944, 10.1111/cobi.13802 Marques, 2021, GAPeDNA: assessing and mapping global species gaps in genetic databases for eDNA metabarcoding, Divers. Distrib., 27, 1880, 10.1111/ddi.13142 Martin, 2011, Cutadapt removes adapter sequences from high-throughput sequencing reads, EMBnet.journal, 17, 10, 10.14806/ej.17.1.200 McClenaghan, 2020, Validating metabarcoding-based biodiversity assessments with multi-species occupancy models: a case study using coastal marine eDNA, PLoS One, 15, 10.1371/journal.pone.0224119 McColl‐Gausden, 2020, Multispecies models reveal that eDNA metabarcoding is more sensitive than backpack electrofishing for conducting fish surveys in freshwater streams, Mol. Ecol., 30, 3111, 10.1111/mec.15644 McElroy, 2020, Calibrating environmental DNA metabarcoding to conventional surveys for measuring fish species richness, Front. Ecol. Evol., 8, 276, 10.3389/fevo.2020.00276 Miya, 2022, Environmental DNA metabarcoding: a novel method for biodiversity monitoring of marine fish communities, Ann. Rev. Mar. Sci, 14, 161, 10.1146/annurev-marine-041421-082251 Miya, 2015, MiFish, a set of universal PCR primers for metabarcoding environmental DNA from fishes: detection of more than 230 subtropical marine species, R. Soc. Open Sci., 2, 10.1098/rsos.150088 Mora, 2008, The completeness of taxonomic inventories for describing the global diversity and distribution of marine fishes, Proc. R. Soc. B Biol. Sci., 275, 149, 10.1098/rspb.2007.1315 Moreno, 2005, Reproductive biology of the sand smelt Atherina presbyter cuvier, 1829 (pisces: atherinidae) in the central-East Atlantic, Fish. Res., 72, 121, 10.1016/j.fishres.2004.06.016 Nelson, 2016 Nester, 2020, Development and evaluation of fish eDNA metabarcoding assays facilitate the detection of cryptic seahorse taxa (family: syngnathidae), Environ. DNA, 2, 614, 10.1002/edn3.93 Oka, 2021, Environmental DNA metabarcoding for biodiversity monitoring of a highly diverse tropical fish community in a coral reef lagoon: estimation of species richness and detection of habitat segregation, Environ. DNA, 3, 55, 10.1002/edn3.132 Oksanen, 2013, Package ‘vegan.’ community ecol, Package Version, 2, 1 Pais, 2018, Effect of underwater visual survey methodology on bias and precision of fish counts: a simulation approach, PeerJ, 6, e5378, 10.7717/peerj.5378 Pelletier, 2011, Comparison of visual census and high definition video transects for monitoring coral reef fish assemblages, Fish. Res., 107, 84, 10.1016/j.fishres.2010.10.011 Perera-Valderrama, 2020, A new long-term marine biodiversity monitoring program for the knowledge and management in marine protected areas of the Mexican caribbean, Sustainability, 12, 7814, 10.3390/su12187814 Pita, 2018, Spatiotemporal variation in the structure of reef fish and macroalgal assemblages in a north-east Atlantic kelp forest ecosystem: implications for the management of temperate rocky reefs, Mar. Freshw. Res., 69, 525, 10.1071/MF17193 Pita, 2014, Short-term performance of three underwater sampling techniques for assessing differences in the absolute abundances and in the inventories of the coastal fish communities of the Northeast Atlantic Ocean, Mar. Freshw. Res., 65, 105, 10.1071/MF12301 Polanco Fernández, 2021, Comparing environmental DNA metabarcoding and underwater visual census to monitor tropical reef fishes, Environ. DNA, 3, 142, 10.1002/edn3.140 Polanco Fernández, 2021, Comparing the performance of 12S mitochondrial primers for fish environmental DNA across ecosystems, Environ. DNA, 3, 1113, 10.1002/edn3.232 Pont, 2021, The future of fish‐based ecological assessment of European rivers: from traditional EU Water Framework Directive compliant methods to eDNA metabarcoding‐based approaches, J. Fish. Biol., 98, 354, 10.1111/jfb.14176 Port, 2016, Assessing vertebrate biodiversity in a kelp forest ecosystem using environmental DNA, Mol. Ecol., 25, 527, 10.1111/mec.13481 Pörtner, 2010, Niche dimensions in fishes: an integrative view, Physiol. Biochem. Zool., 83, 808, 10.1086/655977 Rozanski, 2022, Disentangling the components of coastal fish biodiversity in southern Brittany by applying an environmental DNA approach, Envir. DNA, 4, 920, 10.1002/edn3.305 Ruppert, 2019, Past, present, and future perspectives of environmental DNA (eDNA) metabarcoding: a systematic review in methods, monitoring, and applications of global eDNA, Glob. Ecol. Conserv., 17 Sassoubre, 2016, Quantification of environmental DNA (eDNA) shedding and decay rates for three marine fish, Environ. Sci. Technol., 50, 10456, 10.1021/acs.est.6b03114 Schnell, 2015, Tag jumps illuminated--reducing sequence-to-sample misidentifications in metabarcoding studies, Mol. Ecol. Resour., 15, 1289, 10.1111/1755-0998.12402 Shu, 2020, Standards for methods utilizing environmental DNA for detection of fish species, Genes, 11, 296, 10.3390/genes11030296 Sigsgaard, 2017, Seawater environmental DNA reflects seasonality of a coastal fish community, Mar. Biol., 164, 128, 10.1007/s00227-017-3147-4 Sigsgaard, 2020, Using vertebrate environmental DNA from seawater in biomonitoring of marine habitats, Conserv. Biol., 34, 697, 10.1111/cobi.13437 Stat, 2019, Combined use of eDNA metabarcoding and video surveillance for the assessment of fish biodiversity, Conserv. Biol., 33, 196, 10.1111/cobi.13183 Stauffer, 2021, How many replicates to accurately estimate fish biodiversity using environmental DNA on coral reefs?, Ecol. Evol., 11, 14630, 10.1002/ece3.8150 Stoeckle, 2020, Trawl and eDNA assessment of marine fish diversity, seasonality, and relative abundance in coastal New Jersey, USA, ICES J. Mar. Sci., 78, 293, 10.1093/icesjms/fsaa225 Stoeckle, 2020, Improved environmental DNA reference library detects overlooked marine fishes in New Jersey, United States, Front. Mar. Sci., 7, 226, 10.3389/fmars.2020.00226 Stoeckle, 2017, Aquatic environmental DNA detects seasonal fish abundance and habitat preference in an urban estuary, PLoS One, 12, 10.1371/journal.pone.0175186 Taberlet, 2018 Taberlet, 2012, Environmental DNA, Mol. Ecol., 21, 1789, 10.1111/j.1365-294X.2012.05542.x Thalinger, 2019, Monitoring spawning migrations of potamodromous fish species via eDNA, Sci. Rep., 9, 10.1038/s41598-019-51398-0 Thanopoulou, 2018, How many fish? Comparison of two underwater visual sampling methods for monitoring fish communities, PeerJ, 6, 10.7717/peerj.5066 Thiriet, 2016, Abundance and diversity of crypto- and necto-benthic coastal fish are higher in marine forests than in structurally less complex macroalgal assemblages, PLoS One, 11, 10.1371/journal.pone.0164121 Thompson, 1997, Observer effects and training in underwater visual surveys of reef fishes, Mar. Ecol. Prog. Ser., 154, 53, 10.3354/meps154053 Thomsen, 2012, Detection of a diverse marine fish fauna using environmental DNA from seawater samples, PLoS One, 7, 10.1371/journal.pone.0041732 Thomsen, 2016, Environmental DNA from seawater samples correlate with trawl catches of subarctic, deepwater fishes, PLoS One, 11, 10.1371/journal.pone.0165252 Tsuji, 2021, Identifying spawning events in fish by observing a spike in environmental DNA concentration after spawning, Environ. DNA, 3, 190, 10.1002/edn3.153 Valentini, 2016, Next-generation monitoring of aquatic biodiversity using environmental DNA metabarcoding, Mol. Ecol., 25, 929, 10.1111/mec.13428 Villéger, 2017, Functional ecology of fish: current approaches and future challenges, Aquat. Sci., 79, 783, 10.1007/s00027-017-0546-z Wafar, 1983, Nutrients and primary production in permanently well-mixed temperate coastal waters, Estuar. Coast Shelf Sci., 17, 431, 10.1016/0272-7714(83)90128-2 Wang, 2007, Naïve bayesian classifier for Rapid assignment of rRNA sequences into the new bacterial taxonomy, Appl. Environ. Microbiol., 73, 5261, 10.1128/AEM.00062-07 West, 2021, Large-scale eDNA metabarcoding survey reveals marine biogeographic break and transitions over tropical north-western Australia, Divers. Distrib., 27, 1942, 10.1111/ddi.13228 West, 2020, eDNA metabarcoding survey reveals fine-scale coral reef community variation across a remote, tropical island ecosystem, Mol. Ecol., 29, 1069, 10.1111/mec.15382 Yamamoto, 2017, Environmental DNA metabarcoding reveals local fish communities in a species-rich coastal sea, Sci. Rep., 7, 10.1038/srep40368 Yamamoto, 2016, Environmental DNA as a ‘snapshot’ of fish distribution: a case study of Japanese jack mackerel in maizuru bay, sea of Japan, PLoS One, 11 Zou, 2020, eDNA metabarcoding as a promising conservation tool for monitoring fish diversity in a coastal wetland of the Pearl River Estuary compared to bottom trawling, Sci. Total Environ., 702, 10.1016/j.scitotenv.2019.134704