Cross-ocean patterns and processes in fish biodiversity on coral reefs through the lens of eDNA metabarcoding

Abstract

Increasing speed and magnitude of global change threaten the world's biodiversity and particularly coral reef fishes. A better understanding of large-scale patterns and processes on coral reefs is essential to prevent fish biodiversity decline but it requires new monitoring approaches. Here, we use environmental DNA metabarcoding to reconstruct well-known patterns of fish biodiversity on coral reefs and uncover hidden patterns on these highly diverse and threatened ecosystems. We analysed 226 environmental DNA (eDNA) seawater samples from 100 stations in five tropical regions (Caribbean, Central and Southwest Pacific, Coral Triangle and Western Indian Ocean) and compared those to 2047 underwater visual censuses from the Reef Life Survey in 1224 stations. Environmental DNA reveals a higher (16%) fish biodiversity, with 2650 taxa, and 25% more families than underwater visual surveys. By identifying more pelagic, reef-associated and crypto-benthic species, eDNA offers a fresh view on assembly rules across spatial scales. Nevertheless, the reef life survey identified more species than eDNA in 47 shared families, which can be due to incomplete sequence assignment, possibly combined with incomplete detection in the environment, for some species. Combining eDNA metabarcoding and extensive visual census offers novel insights on the spatial organization of the richest marine ecosystems.

Estimating the extended and hidden species diversity from environmental DNA in hyper‐diverse regions

“…Such mobile and elusive species are often missed by traditional methods that involve divers and are dependent on water visibility. This result confirms the significant and valuable contribution eDNA metabarcoding can provide for the monitoring of such species (Mathon et al 2022). Additionally, a large number of species were recorded with our fishing effort alone and added to the checklist during the development of the reference database.…”

“…With 92 water samples, eDNA captured 54.8% of the sequenced fish biodiversity in the extended checklist. This detection capacity outperforms that of traditional methods such as visual surveys that can miss elusive, highly mobile or cryptobenthic species (Boussarie et al 2018, Mathon et al 2022 or destructive fishing surveys that target restricted habitats and small sets of species. Unlike UVC, eDNA monitoring is less restricted by logistical constraints and can be performed at depths inaccessible to divers.…”

“…Beyond taxonomic assignment, impaired by the actual incompleteness of genetic reference databases and the unperfect taxonomic resolution of genetic markers, eDNA metabarcoding can be analyzed by generating MOTUs that can be defined as distinct taxonomic entities and act as a proxy of taxonomic diversity following adequate curation (Marques et al 2020b). They can provide a more exhaustive biodiversity estimation, albeit not taxonomically assigned, to revisit biogeographic patterns (Juhel et al 2020, Mathon et al 2022). Implementing comprehensive, large‐scale and long‐term biodiversity observatories will thus significantly complement or challenge many known ecological patterns and processes from the local to the global scale (Boulanger et al 2021, Mathon et al 2022).…”

“…They can provide a more exhaustive biodiversity estimation, albeit not taxonomically assigned, to revisit biogeographic patterns (Juhel et al 2020, Mathon et al 2022). Implementing comprehensive, large‐scale and long‐term biodiversity observatories will thus significantly complement or challenge many known ecological patterns and processes from the local to the global scale (Boulanger et al 2021, Mathon et al 2022).…”

“…Moreover, the detection potential of eDNA is conditional to fish behavior (Thalinger et al 2021) and the persistence of eDNA in the environment (Harrison et al 2019) so some species can be missed (Stat et al 2019). In this case, asymptotic estimates can be inferred using species or MOTU accumulation curves (Juhel et al 2020, Mathon et al 2022). Yet, these asymptotes cannot provide the level of species dissimilarity between methods so cannot estimate the asymptotic extended or hidden species diversity.…”