Environmental DNA (eDNA) detects temporal and habitat effects on community composition and endangered species in ephemeral ecosystems: A case study in vernal pools

Abstract

Vernal pools are temporary wetlands that can form during a rainy season, often in Mediterranean climates, and serve as ideal testing grounds to understand species detection using eDNA and how biological communities may shift across time and spatial and environmental heterogeneity. Most vernal pools exhibit high plant and animal diversity and endemism, but due to their ephemeral nature, they are understudied, especially their microorganisms. Habitat destruction and fragmentation creates an urgent need to monitor their biodiversity, but traditional species surveys require time and taxonomic expertise. We conducted a community science‐enabled examination of soil environmental DNA (eDNA) in California's Great Central Valley and assessed the capacity of eDNA to aid biomonitoring. We used metabarcoding of 16S, ITS1, CO1, 18S, and ITS2 marker regions to quantify and compare differences in pool communities across two sampling periods (during years with disparate precipitation) and to estimate variation among pools and inundation zones (vernal pool bottom, transitional edge, and grassland upland). We found differences in beta diversity among sampling periods, pools, and inundation zones; alpha diversity was mainly affected by sampling period and zone, but this differed by marker. Numerous taxonomic families varied in abundance and composition among samples, yet vernal pool communities remained distinct from upland grass communities, even between sampling periods differing by 1 year. Turnover in ecologically co‐occurring taxon pairs varied by over 90% between sampling periods in all metabarcodes but plants, which were more stable. Finally, we confirmed substantial concordance between eDNA and traditional inventories of the reserve's plants and presented a case in which we detected one endangered plant species, Colusa grass (Neostapfia colusana), in advance of its emergence. This initial study adds hundreds of new taxon records for California vernal pools and discusses benefits and challenges of using eDNA for biomonitoring within stressful, temporary, or otherwise challenging ecosystems.

Critical considerations for communicating environmental DNA science

“…Correlations can provide quantitative estimates of organism abundance (Shelton et al, 2022); however, the precise relationship between eDNA concentration and organismal abundance currently lacks the accuracy required for many applications (Spear et al, 2021) and may need to be calibrated to the location sampled. Environmental DNA analysis can also describe biodiversity (community richness, evenness, composition, and functions), but the resolution varies based on the assay, environmental conditions of the sampled system, and the sampling intensity (Mächler et al, 2019; Pont et al, 2018; Ruiz‐Ramos et al, 2023; Zhang et al, 2020). Therefore, the choice of assays and sampling design should be validated based on the management objective.…”

Environmental determinants of phylogenetic diversity in vernal pool habitats

“…Vernal pools are ephemerally aquatic habitats underlain by an impermeable claypan that promotes the cyclical filling of water during the winter and evaporation during the spring (Keeley & Zedler, 1998 ; Smith & Verrill, 1998 ; Solomeshch et al., 2007 ). Approximately 95% of vernal pool habitats in the Central Valley of California have been destroyed (Ruiz‐Ramos et al., 2023 ) and continue to be threatened by altered climate and persistent invasions. To date, no phylogenetic diversity assessment has been performed on the habitat, and thus, the ecological factors that maintain phylogenetic diversity and the human impacts that disrupt phylogenetic structure are not currently understood.…”

Species identification method by a new non-invasive technique in Korean endangered terrestrial snail, Koreanohadra koreana (Castropoda: Mollusca)

“…Recently, various genetic analyzes using environmental DNA (eDNA) that comes from organisms has been studied to identify their presence or absence in the habitat (Weltz et al 2017;Mizumoto et al 2020;Ruiz-Ramos et al 2023) and to verify host plants (Milla et al 2022). These studies con rmed that large amounts of residual gDNA from organisms exists in the environment, and on this basis it was established that genetic research could be su ciently conducted using eDNA.…”