Effects of Non-Indigenous Oysters on Microbial Diversity and Ecosystem Functioning

Just Cebrian,Bas Boots,Dannielle S Green,Tasman P Crowe

doi:10.1371/journal.pone.0048410

Abstract

Invasive ecosystem engineers can physically and chemically alter the receiving environment, thereby affecting biodiversity and ecosystem functioning. The Pacific oyster, Crassostrea gigas, invasive throughout much of the world, can establish dense populations monopolising shorelines and possibly altering ecosystem processes including decomposition and nutrient cycling. The effects of increasing cover of invasive C. gigas on ecosystem processes and associated microbial assemblages in mud-flats were tested experimentally in the field. Pore-water nutrients (NH4 + and total oxidised nitrogen), sediment chlorophyll content, microbial activity, total carbon and nitrogen, and community respiration (CO2 and CH4) were measured to assess changes in ecosystem functioning. Assemblages of bacteria and functionally important microbes, including methanogens, methylotrophs and ammonia-oxidisers were assessed in the oxic and anoxic layers of sediment using terminal restriction length polymorphism of the bacterial 16S rRNA, mxaF, amoA and archaeal mcrA genes respectively. At higher covers (40 and 80%) of oysters there was significantly greater microbial activity, increased chlorophyll content, CO2 (13 fold greater) and CH4 (6 fold greater) emission from the sediment compared to mud-flats without C. gigas. At 10% cover, C. gigas increased the concentration of total oxidised nitrogen and altered the assemblage structure of ammonia-oxidisers and methanogens. Concentrations of pore-water NH4 + were increased by C. gigas regardless of cover. Invasive species can alter ecosystem functioning not only directly, but also indirectly, by affecting microbial communities vital for the maintenance of ecosystem processes, but the nature and magnitude of these effects can be non-linear, depending on invader abundance.

Highlights

Biological invasions by non-indigenous species are among the most serious threats to biodiversity, ecosystem functioning and the provision of ecosystem services in terrestrial, freshwater and marine environments [1]
The link between invasive species, microbial diversity and nutrient cycling in the marine environment has not been explicitly explored until now
Nutrient cycling and microbial assemblage structure and diversity were altered, but the nature and magnitude of effects were dependent on the cover of C. gigas

Summary

Introduction

Biological invasions by non-indigenous species are among the most serious threats to biodiversity, ecosystem functioning and the provision of ecosystem services in terrestrial, freshwater and marine environments [1]. Repairing the damage caused by invasive species is estimated to cost nearly 5% of the world’s economy per year [2]. Many of these costs are due to a deterioration of ecosystem services [1], but the costs of prevention, management and mitigation can be substantial [3]. The nature and magnitude of their effects on receiving ecosystems may vary spatially and over the course of establishment as a result of variation in abundance [5]. Knowledge of how their impacts on receiving ecosystems vary with invader abundance is lacking [6], concerning how ecosystem functioning is affected [7]. Studies on the impacts of invasive species typically compare presence or absence of invaders, but in order to improve predictions, it is advantageous to relate invader effects directly to their abundance [6]

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