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Comparing Environmental DNA Metabarcoding and Underwater Visual Census to Monitor Tropical Reef Fishes

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Comparing Environmental DNA Metabarcoding and Underwater Visual Census to Monitor Tropical Reef Fishes Received: 4 April 2020 | Revised: 6 August 2020 | Accepted: 9 September 2020 DOI: 10.1002/edn3.140 SPECIAL ISSUE ORIGINAL ARTICLE Comparing environmental DNA metabarcoding and underwater visual census to monitor tropical reef fishes Andrea Polanco Fernández1 | Virginie Marques2,3 | Fabian Fopp4,5 | Jean-Baptiste Juhel2 | Giomar Helena Borrero-Pérez1 | Marie-Charlotte Cheutin2 | Tony Dejean6 | Juan David González Corredor1 | Andrés Acosta-Chaparro1 | Régis Hocdé2 | David Eme7 | Eva Maire2,8 | Manuel Spescha4,5 | Alice Valentini6 | Stéphanie Manel3 | David Mouillot2 | Camille Albouy7 | Loïc Pellissier4,5 1Programa de Biodiversidad y Ecosistemas Marinos, Museo de Historia Natural Abstract Marina de Colombia (MHNMC), Instituto Environmental DNA (eDNA) analysis is a revolutionary method to monitor marine de Investigaciones Marinas y Costeras- INVEMAR, Santa Marta, Colombia biodiversity from animal DNA traces. Examining the capacity of eDNA to provide 2MARBEC, CNRS, Ifremer, IRD, University of accurate biodiversity measures in species-rich ecosystems such as coral reefs is a Montpellier, Montpellier, France prerequisite for their application in long-term monitoring. Here, we surveyed two 3EPHE, CNRS, UM, UM3, IRD, UMR5175 CEFE, PSL Research University, Montpellier, Colombian tropical marine reefs, the island of Providencia and Gayraca Bay near France Santa Marta, using eDNA and underwater visual census (UVC) methods. We collected 4 Landscape Ecology, Institute of Terrestrial a large quantity of surface water (30 L per filter) above the reefs and applied a meta- Ecosystems, Department of Environmental Systems Science, ETH Zürich, Zürich, barcoding protocol using three different primer sets targeting the 12S mitochondrial Switzerland DNA, which are specific to the vertebrates Actinopterygii and Elasmobranchii. By 5Unit of Land Change Science, Swiss Federal assigning eDNA sequences to species using a public reference database, we detected Institute for Forest, Snow and Landscape Research WSL, Birmensdorf, Switzerland the presence of 107 and 85 fish species, 106 and 92 genera, and 73 and 57 families 6 SPYGEN, Le Bourget-du-Lac, France in Providencia and Gayraca Bay, respectively. Of the species identified using eDNA, 7 Unité Ecologie et Modèles pour 32.7% (Providencia) and 18.8% (Gayraca) were also found in the UVCs. We further l'Halieutique, EMH, IFREMER, Nantes, France found congruence in genus and species richness and abundance between eDNA and 8Lancaster Environment Centre, Lancaster UVC approaches in Providencia but not in Gayraca Bay. Mismatches between eDNA University, Lancaster, UK and UVC had a phylogenetic and ecological signal, with eDNA detecting a broader Correspondence phylogenetic diversity and more effectively detecting smaller species, pelagic spe- Andrea Polanco Fernández, Programa de Biodiversidad y Ecosistemas Marinos, Museo cies and those in deeper habitats. Altogether, eDNA can be used for fast and broad de Historia Natural Marina de Colombia biodiversity surveys and is applicable to species-rich ecosystems in the tropics, but (MHNMC), Instituto de Investigaciones Marinas y Costeras-INVEMAR, Calle 25 improved coverage of the reference database is required before this new method No.2—55 Playa Salguero, Santa Marta, could serve as an effective complement to traditional census methods. Colombia. Email: [email protected] Andrea Polanco Fernández and Virginie Marques shared first authorship. Camille Albouy and Loïc Pellissier shared senior authorship. This research was financed by the Monaco Explorations Foundation grant "Megafauna" to DM, SM, and LP. The research was further supported by the Swiss National Science Foundation grant n°310030E-164294 to LP. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. © 2020 The Authors. Environmental DNA published by John Wiley & Sons Ltd Environmental DNA. 2020;00:1–15. wileyonlinelibrary.com/journal/edn3 | 1 2 | POLANCO FERNÁNDEZ ET al. Funding information KEYWORDS Monaco Explorations Foundation grant "Megafauna"; Swiss National Science biodiversity, biomonitoring, Caribbean Sea, environmental DNA, reef fishes, underwater visual Foundation grant n° 310030E-164294 census 1 | INTRODUCTION in aquatic systems (Deiner et al., 2017; Harrison et al., 2019). A recent synthesis counted 54 papers on tropical eDNA, whereas only 15 fo- Coral reefs represent the most diverse marine ecosystems on cused on marine systems (Bakker et al., 2019; Huerlimann et al., 2020; the planet (Fisher et al., 2015) and are also the most threatened Sigsgaard et al., 2019; West et al., 2020). Compared to freshwater sys- (Williams et al., 2019). Due to their structural complexity, they host tems, the marine environment has a larger water volume to fish bio- a large diversity of fish species, from tiny cryptic species to large mi- mass ratio, the movement of molecules in suspension is influenced by gratory species (Collins et al., 2019; Darling et al., 2017). Because of various currents, and reef systems can contain up to hundreds of spe- this high species diversity, coral reefs have generally been difficult to cies, which might challenge the detection of individual species (Collins inventory using traditional survey methods (Plaisance et al., 2011). et al., 2019; Hansen et al., 2018; Harrison et al., 2019). Several appli- Moreover, global changes, including exploitation, pollution, or cli- cations demonstrated that eDNA can recover multiple components mate change, are degrading biodiversity on reefs (Cinner et al., 2016; of marine ecosystems, including species richness (Jerde et al., 2019), Descombes et al., 2015), but it is difficult to quantify and monitor seasonal composition variation (Djurhuus et al., 2020), rare species these impacts because describing species diversity and composi- (Weltz et al., 2017), abundance or biomass (Knudsen et al., 2019; tion is generally demanding (Costello et al., 2015; Mora et al., 2008). Thomsen et al., 2016), and the occurrence of invasive species (Nevers The monitoring of the biodiversity of coral reefs under global et al., 2018). Nevertheless, a range of methodological challenges still changes could benefit from novel solutions with lower costs and hampers the broad use of eDNA for the reliable monitoring of ma- broader applicability complementing traditional methods (Thomsen rine ecosystems, linked to the choice of markers (Collins et al., 2019; et al., 2012; West et al., 2020). Freeland, 2017), primers sets (Stat et al., 2017), laboratory and se- Traditionally, monitoring fishes on coral reefs has been per- quencing protocols (Deiner et al., 2017; Goldberg et al., 2016), and bio- formed using underwater visual censuses (UVC) or video surveys informatic analyses (Calderón-Sanou et al., 2020; Juhel et al., 2020), (Stat et al., 2019), which offer a partial view of the dynamics of reef which implies further testing of the eDNA methodology in situ. biodiversity, from their degradation under global changes to their Tropical ecosystems have historically been underrepresented in recovery (Bozec et al., 2011; Cinner et al., 2016). These methods research (Collen et al., 2008), and increased monitoring efforts in are limited in both spatial and temporal coverage and are biased these regions are urgently needed, particularly under ongoing global toward certain categories of species (Boussarie et al., 2018). UVC is change (Barlow et al., 2018). Different abiotic conditions and high traditionally used to monitor fish diversity on coral reefs (Samoilys species richness might challenge the application of eDNA in the & Carlos, 2000). However, besides logistical difficulties to orga- tropics (Huerlimann et al., 2020; Jerde et al., 2019). Studies of eDNA nize underwater sampling in remote locations, UVC can suffer on coral reefs have shown a strong potential for biodiversity detec- from several observer biases, such as overlooking cryptobenthic tion (Nguyen et al., 2020; Sigsgaard et al., 2019; West et al., 2020), (Bozec et al., 2011) or wideranged species such as sharks (Juhel but the scope of methodological testing remains narrow. Dibattista et al., 2018). One of the most effective approaches to circumvent et al. (2017) used fish-specific 16S mitochondrial DNA to monitor the limitations of traditional survey methods in highly diverse eco- fish diversity in the Red Sea, but captured only a fraction of the local systems is environmental DNA (eDNA) metabarcoding (Cilleros fish species pool. Stat et al. (2019) compared the signal of eDNA et al., 2019; Gomes et al., 2017). eDNA is a noninvasive method with observations from baited videos and detected >30% more demonstrating higher detection capabilities and cost-effectiveness generic richness using the combination of approaches than when compared to traditional methods, especially when deployed in re- either method was used alone. Sigsgaard et al. (2019) used eDNA mote locations (Dejean et al., 2011; Kelly et al., 2014; Thomsen & with fish-specific 12S mitochondrial DNA across a network of sites Willerslev, 2015). Before it can effectively complement traditional in the Gulf of Oman and recovered sequences from a diverse as- sampling methods, the ability of eDNA to recover signals of diver- semblage of marine vertebrates, which covered approximately one- sity and composition of marine systems should be evaluated. third of the bony fish genera previously recorded in this area. Using
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