Effects of the bioturbating lugworm Arenicola marina on the structure of benthic protistan communities

Abstract

Sedimentary coastal ecosystems like the European Wadden Sea in the northeasternAtlantic harbor large populations of burrowing infauna, such as arenicolide polychaetes. These 'ecosystem engineering' macrofaunal organisms destabilize sediments by reworking and irrigating them, leading to a reorganization of sediment physicochemical state and bacterial communities. Here, we tested the effects of the lugworm Arenicola marina on intertidal psammophilic protistan community diversity and structure in a field experiment. We applied pyrosequencing and community structure analyses to samples in which we manipulated lugworm densities. Irrespective of the presence or absence of the lugworm, protistan abundance and diversity (mostly diatoms and ciliates) was higher in oxic surface sediments compared to anoxic subsurface sediments. In the presence of A. marina, protistan abundances and diversity decreased decisively in surface as well as in subsurface bulk sediment. Also, the protistan community composition differed remarkably, with only 28% of all phylotypes (n total = 855) shared between habitats with and without lugworms. Twenty-seven percent of all taxa were detected exclusively in the presence of lugworms, and 62% of the taxa found in the oxic subsurface sediment surrounding the lugworm burrow were limited to this distinct microenvironment. This suggests that lugworm burrows provide an ecological niche potentially hosting protist taxa that are adapted to fluctuating oxygen supply. We conclude that though the activities of A. marina reduce the overall abundance of protists, they select for very specific and well-adapted taxa. This adds to the overall protistan diversity in intertidal sandflats on larger spatial scales. Most likely, the observed effects of lugworms on protistan community structure and composition are due to a combination of direct trophic and indirect sediment-mediated effects, such as disturbance by reworking the sediment, oxygen supply by burrow ventilation and increased pore water exchange due to bioadvection.

Polychaete burrows harbour distinct microbial communities in oil‐contaminated coastal sediments

“…Only one previous study has assessed microbial eukaryote diversity in polychaete burrows (Engel et al ., ). Engel and colleagues () showed that ciliates and diatoms dominate A. marina burrows in non‐polluted coastal sediment. In this study, fungi dominated both H. diversicolor burrow and un‐bioturbated sediment sequence libraries.…”

“…The potential impacts of bioturbation on sediment microbial eukaryote diversity have received much less attention compared with that of bacterial diversity. In one study, 18S rRNA gene pyrosequencing of DNA isolated from Arenicola marina burrows showed that resident protist communities are different to those in un‐bioturbated sediment and at the sediment–water interface (Engel et al ., ).…”

Microeukaryotic Community Structure and Dynamics During Macrobenthos Bioremediation in Intertidal Mudflat Sediments of Sansha Bay, China

“…Previous studies demonstrated that the burrows of Nereids (H. diversicolor or Arenicola marina) harbored different eukaryotic communities compared to the un-bioturbated sediments, and more Nematodes were detected in the burrows (24,25). However, the mentioned studies mainly focused on the burrow environments; the influence of macrobenthos bioturbation on overall microeukaryotes communities in a larger scale environment has not been thus far extensively characterized.…”

“…A previous study (24) also indicated that the activities of lugworm (Arenicola marina) reduced the overall abundance of protists (mainly Cercozoa and Alveolate). The decrease of protists is probably due to the grazing/predation pressure of filter-feeding nereids, bivalves, and altered environmental conditions by macrobenthos bioturbation (28).…”

“…Photosynthetic microeukaryotes are producers of substantial biomass, while heterotrophs play a crucial role in benthic food webs. They are consumers of microorganisms including some protists and are at the same time grazed by benthic invertebrates such as filter-feeding bivalves, thus representing a link between lower and higher trophic levels (24).…”