Archived DNA reveals marine heatwave‐associated shifts in fish assemblages

• Published in: Environmental DNA (Hoboken, N.J.) N.J.), 2024-01, Vol.6 (1), p.n/a
• Main Authors: Gold, Zachary, Kelly, Ryan P., Shelton, Andrew Olaf, Thompson, Andrew R., Goodwin, Kelly D., Gallego, Ramón, Parsons, Kim M., Thompson, Luke R., Kacev, Dovi, Barber, Paul H.
• Format: Article
• Language: English
• Subjects: amplicon sequencing; CalCOFI; California Current Ecosystem; DNA barcoding; Ecosystems; eDNA; Eggs; Environmental DNA; Environmental impact; Ethanol; Fish; Fisheries; Gene sequencing; Heat waves; Ichthyoplankton; Investigations; joint model; Marine ecosystems; Marine fish; marine heatwave; Modelling; Morphology; Nucleotide sequence; Plankton; Population decline; Preservatives; quantitative metabarcoding; Taxonomy; Temperature; Water temperature
• ISSN: 2637-4943; 2637-4943
• DOI: 10.1002/edn3.400

Marine heatwaves can drive large‐scale shifts in marine ecosystems, but studying their impacts on whole species assemblages is difficult. Analysis combining microscopic observations with environmental DNA (eDNA) metabarcoding of the ethanol preservative of an ichthyoplankton biorepository spanning a 23 years time series captures major and sometimes unexpected changes to fish assemblages in the California Current Large Marine Ecosystem during and after the 2014–2016 Pacific Marine Heatwave. Joint modeling efforts reveal patterns of tropicalization with increases in southern, mesopelagic species and associated declines in commercially important temperate fish species (e.g., North Pacific Hake [Merluccius productus] and Pacific Sardine [Sardinops sagax]). Data show shifts in fisheries assemblages (e.g., Northern Anchovy, Engraulis mordax) even after the return to average water temperatures, corroborating ecosystem impacts found through multiple traditional surveys of this study area. Our innovative approach of metabarcoding preservative eDNA coupled with quantitative modeling leverages the taxonomic breadth and resolution of DNA sequences combined with microscopy‐derived ichthyoplankton identification to yield higher‐resolution, species‐specific quantitative abundance estimates. This work opens the door to economically reconstruct the historical dynamics of assemblages from modern and archived samples worldwide. We reconstruct the fish fauna of the California Current Large Marine Ecosystem before, during, and after the 2014–2016 Pacific Marine Heatwave, integrating DNA amplicons derived eDNA in the ethanol of a 23‐year longitudinal ichthyoplankton sample collection with microscopy‐derived morphological identification through a novel joint model to provide a much higher‐resolution picture of fish assemblages.Consistent with expectations under warming, we find tropicalization of fish assemblages in favor of southern, mesopelagic species during and after the 2014–2016 Pacific Marine Heatwave with declines in important temperate fisheries targets including Northern Pacific Hake (Merluccius productus) and Pacific Sardine (Sardinops sagax).