Fish environmental DNA in lake sediment overcomes the gap of reconstructing past fauna in lake ecosystems

Abstract

Underwater sediments are a natural archive of biological information. Reconstruction of past fauna has been conducted for various taxonomic groups using morphological remains and DNA derived from these remains. However, information on past occurrences of fish species, the top predator of lake ecosystems, could have been reproduced only in exceptional environments, and past quantitative information on fish, particularly in lake ecosystems, has been a knowledge gap in reconstructing past fauna. Tracking the quantitative fluctuations of fish is essential for reconstructing multiple trophic levels of organisms in lake ecosystems. To acquire past quantitative fish information from lake sediments, we collected approximately 30 cm-length of underwater sediments in Lake Biwa. We extracted sedimentary environmental DNA (eDNA) and measured temporal fluctuations in the eDNA concentration of the native and fishery target species Plecoglossus altivelis and Gymnogobius isaza. For P. altivelis, we examined the possibility of tracking quantitative fluctuations by comparing sedimentary eDNA with recorded catch per unit effort (CPUE). The chronology of the sediments allowed us to obtain information on sediments collected in Lake Biwa over the past 100 years. The deepest depths at which sedimentary eDNA was detected were 30 and 13 cm for P. altivelis and G. isaza from the surface, corresponding to approximately 100 and 30 years ago, respectively. In the comparison of sedimentary eDNA concentrations and biomass, we found a significant correlation between the CPUE of P. altivelis and its sedimentary eDNA concentration adjusted to compensate for DNA degradation. Sedimentary eDNA fluctuations were observed in P. altivelis, possibly reflecting the abundance fluctuation due to variations in the main food resources of zooplankton. Our findings provide essential pieces for the reconstruction of past fauna of lake ecosystems. The addition of quantitative information on fish species will reach a new phase, for instance, by investigating population shifts or biological interactions in the reconstruction of past fauna in lake ecosystems.

Detection of fish sedimentary DNA in aquatic systems: A review of methodological challenges and future opportunities

“…False‐negative results can be reduced by using IntegritE‐DNA™, which evaluates DNA samples for their capacity to support amplification from ubiquitous endogenous plant chloroplast DNA as a measure of sample integrity that includes identifying inhibited and/or degraded samples (Hobbs et al, 2019; Veldhoen et al, 2016). As an internal positive control to investigate inhibition, the sedDNA samples can also be spiked with exogenous DNA, such as lambda phage DNA (Sakata et al, 2022; Xu et al, 2009). These steps are considered crucial because older DNA is preserved in the sediment matrix with a high likelihood of PCR inhibitor co‐precipitation.…”

“…In sedDNA studies focusing specifically on fish, the quantification of fish DNA copies in younger core sections compared to older sections may provide a useful measure of the degradation of fish sedDNA through time (Sakata et al, 2022; Thomson‐Laing et al (under review); Lopez et al (under review)). However, this method may only be valid if the population size remains constant over time and should still be validated with independent catch data.…”

“…Matisoo‐Smith et al (2008) first detected fish sedDNA matching the native common bully ( Gobiomorphus cotidianus ) in an 1800‐year‐old sediment core from a New Zealand Lake. Fish sedDNA has since been used to estimate colonization histories (Olajos et al, 2018; Stager et al, 2015), confirm species introductions (Nelson‐Chorney et al, 2019), and reconstruct quantitative time series (Kuwae et al, 2020; Sakata et al, 2022) in multiple ecosystems.…”

Opposite trends in environmental DNA distributions of two freshwater species under climate change

“…Primers and probes were established in previous studies (Appendix S1: Table S3). The specificity of each assay has been evaluated in previous studies using tissue DNA, including target and nontarget species, and sequencing the positive amplification of eDNA samples (Sakata et al, 2022; Wu et al, 2018). The PCR conditions were the same for the two species.…”

“…The limit of detection (LOD) and limit of quantification (LOQ) for each assay have been confirmed in previous studies. The LOD and LOQ were determined as one copy and three copies per reaction, respectively, for P. paucidens and as one copy per reaction for G. isaza (Sakata et al, 2022; Wu et al, 2018). As it has been reported that quantifying eDNA concentrations below the LOQ could be meaningful (Takeshita et al, 2020), we employed some data below the LOQ.…”