Marine environmental DNA biomonitoring reveals seasonal patterns in biodiversity and identifies ecosystem responses to anomalous climatic events

Abstract

Marine ecosystems are changing rapidly as the oceans warm and become more acidic. The physical factors and the changes to ocean chemistry that they drive can all be measured with great precision. Changes in the biological composition of communities in different ocean regions are far more challenging to measure because most biological monitoring methods focus on a limited taxonomic or size range. Environmental DNA (eDNA) analysis has the potential to solve this problem in biological oceanography, as it is capable of identifying a huge phylogenetic range of organisms to species level. Here we develop and apply a novel multi-gene molecular toolkit to eDNA isolated from bulk plankton samples collected over a five-year period from a single site. This temporal scale and level of detail is unprecedented in eDNA studies. We identified consistent seasonal assemblages of zooplankton species, which demonstrates the ability of our toolkit to audit community composition. We were also able to detect clear departures from the regular seasonal patterns that occurred during an extreme marine heatwave. The integration of eDNA analyses with existing biotic and abiotic surveys delivers a powerful new long-term approach to monitoring the health of our world’s oceans in the context of a rapidly changing climate.

Author summary

All environments contain genetic remnants of the life they contain and support. For example, samples collected from the ocean contain biological material such as microscopic organisms, shed cells, excrement and saliva—the DNA from which reveals the surrounding marine biodiversity. Environmental DNA (eDNA) approaches have the ability to identify marine species that are notoriously difficult to identify using morphology alone. Here we develop, and apply, a DNA ‘toolkit’ to five years of samples collected from a single site in the Indian ocean. It is rare to find a temporal series of samples of this duration that are also suitable for DNA analysis. We show that eDNA techniques have the capacity to monitor ocean biology in fine detail. We demonstrate how the biological communities of plankton and fish respond to normal seasonal changes and, more importantly, to that of an uncharacteristic heatwave. The methods embodied in this paper are applicable to marine studies across the globe and, as such, pave the way for the design of long-term monitoring programs using eDNA.