Environmental DNA metabarcoding reveals and unpacks a biodiversity conservation paradox in Mediterranean marine reserves

Abstract

Although we are currently experiencing worldwide biodiversity loss, local species richness does not always decline under anthropogenic pressure. This conservation paradox may also apply in protected areas but has not yet received conclusive evidence in marine ecosystems. Here, we survey fish assemblages in six Mediterranean no-take reserves and their adjacent fishing grounds using environmental DNA (eDNA) while controlling for environmental conditions. We detect less fish species in marine reserves than in nearby fished areas. The paradoxical gradient in species richness is accompanied by a marked change in fish species composition under different managements. This dissimilarity is mainly driven by species that are often overlooked by classical visual surveys but detected with eDNA: cryptobenthic, pelagic, and rare fishes. These results do not negate the importance of reserves in protecting biodiversity but shed new light on how under-represented species groups can positively react to fishing pressure and how conservation efforts can shape regional biodiversity patterns.

How many replicates to accurately estimate fish biodiversity using environmental DNA on coral reefs?

“…Sampling designs may need to account for the extent that a given water body accumulates sources of eDNA, and the amount of habitat variation that a water sample signal is aggregated over. eDNA statistical analyses may also need to control for habitat variations before reaching conclusions (Boulanger et al ., 2021).…”

“…Despite decades of sampling efforts, biodiversity monitoring still covers only a small fraction of global ecosystems and is particularly challenging in isolated and remote regions across the oceans (Collen et al ., 2009; Webb, Vanden Berghe and O’Dor, 2010; Dornelas et al ., 2018; Letessier et al ., 2019). An emerging tool for rapid biodiversity assessment is environmental DNA (eDNA) metabarcoding (Stat et al ., 2017;Eble et al ., 2020), which is proving to be particularly effective for marine environments (Juhel et al ., 2020; Boulanger et al ., 2021; Holman et al ., 2021). eDNA-based methods rely on the detection of DNA fragments from various sources including faeces, shed skin cells, organelles, or extruded waste of animals, which become suspended in the water (Dejean et al ., 2012; Collins et al ., 2018; Harrison, Sunday and Rogers, 2019).…”

“…In contrast to freshwater systems, marine systems are very open with eDNA particles dispersed by oceanographic dynamics at local (e.g., tides, currents, and water stratification), regional (e.g., eddies) and large (e.g., thermohaline currents) scales in interaction with coastal morphology. Whilst significant dispersal of eDNA from its source may theoretically occur (Andruszkiewicz et al ., 2019; Eble et al ., 2020), many studies also indicate that eDNA detection is limited to a small spatio-temporal sampling window even in highly dynamic marine habitats (Port et al ., 2016; O’Donnell et al ., 2017; Yamamoto et al ., 2017; Jeunen, Knapp, Spencer, Lamare, et al ., 2019; Stat et al ., 2019; West et al ., 2020; Boulanger et al ., 2021). If marine eDNA is sparse, widely transported, and heterogeneously distributed, then biodiversity estimates could be highly variable and eDNA sampling strategies may need to overcome this potentially high noise-to-signal ratio.…”

Biodiversity Monitoring in Mediterranean Marine Protected Areas: Scientific and Methodological Challenges

“…A major advantage of the eDNA approach is that sampling water or sediments is rapid and easier than other methodologies currently used for assessing biodiversity, and can routinely applied on a large scale [60]. Studies on fish showed that eDNA may detect cryptobenthic, pelagic, and rare species that are often overlooked by the traditional visual surveys [61]. The potentiality of the method is still to be fully explored: experiences to date indicate that it is not yet capable of reliably identifying all the species actually present in a given area but anyway provides an important complement to traditional methods [62].…”

Effects of sampling strategies and DNA extraction methods on eDNA metabarcoding: A case study of estuarine fish diversity monitoring

“…At present, most investigations on fishery resources in the PRE are based on traditional survey methods, which can be destructive for both species and habitat ( Hiddink et al, 2019 ; Liu et al, 2018 ). As an effective and non-invasive technology, eDNA metabarcoding is a promising alternative approach for investigating fish diversity in aquatic ecosystems such as the PRE ( Boulanger et al, 2021 ; Gold et al, 2021 ; Prié et al, 2021 ; Sales et al, 2021 ). Because determining differences in DNA detection capabilities among protocols requires a realistic eDNA metabarcoding approach, we explored sampling, filtration, and extraction method combinations to reliably monitor fish diversity in the PRE.…”