Deposit-feeding worms control subsurface ecosystem functioning in intertidal sediment with strong physical forcing

Abstract

Intertidal sands are global hotspots of terrestrial and marine carbon cycling with strong hydrodynamic forcing by waves and tides and high macrofaunal activity. Yet, the relative importance of hydrodynamics and macrofauna in controlling these ecosystems remains unclear. Here we compare bacterial, archaeal, and eukaryotic communities in upper intertidal sands dominated by subsurface deposit-feeding worms (Abarenicola pacifica) to adjacent worm-free areas. We show that hydrodynamic forcing controls organismal assemblages in surface sediments, while in deeper layers selective feeding by worms on fine, algae-rich particles strongly decreases the abundance and richness of all three domains. In these deeper layers, bacterial and eukaryotic network connectivity decreases, while percentages of taxa involved in degradation of refractory organic macrostructures, oxidative nitrogen and sulfur cycling, and macrofaunal symbioses, increase. Our findings reveal macrofaunal activity as the key driver of ecosystem functioning and carbon cycling in intertidal sands below the mainly physically controlled surface layer. Significance StatementHydrodynamics and bioturbation are the main forces controlling chemical exchanges between sediment and seawater in coastal environments. However, little is known about the relative impact of both processes on sediment biological communities. We show that intertidal sand ecosystems dominated by lugworms can be divided into vertically distinct hydrodynamically and biologically controlled layers. Hydrodynamic forcing controls biological communities in surface layers by regulating organic carbon and electron acceptor inputs. By contrast, lugworms structure subsurface ecosystems through the selective consumption of fine particles, which diminishes microbial and eukaryotic populations and weakens ecological networks, while promoting the burial of, mostly terrestrial, macrodetritus. Our study demonstrates that globally distributed marine invertebrates control intertidal sand ecosystems below the physically controlled surface layer.