Complex Effects of Ecosystem Engineer Loss on Benthic Ecosystem Response to Detrital Macroalgae

Francesca Rossi,Frederic Gazeau,Britta Gribsholt,Jack J. Middelburg,Valentina Di Santo,Andrew Davies

doi:10.1371/journal.pone.0066650

Abstract

Ecosystem engineers change abiotic conditions, community assembly and ecosystem functioning. Consequently, their loss may modify thresholds of ecosystem response to disturbance and undermine ecosystem stability. This study investigates how loss of the bioturbating lugworm Arenicola marina modifies the response to macroalgal detrital enrichment of sediment biogeochemical properties, microphytobenthos and macrofauna assemblages. A field manipulative experiment was done on an intertidal sandflat (Oosterschelde estuary, The Netherlands). Lugworms were deliberately excluded from 1× m sediment plots and different amounts of detrital Ulva (0, 200 or 600 g Wet Weight) were added twice. Sediment biogeochemistry changes were evaluated through benthic respiration, sediment organic carbon content and porewater inorganic carbon as well as detrital macroalgae remaining in the sediment one month after enrichment. Microalgal biomass and macrofauna composition were measured at the same time. Macroalgal carbon mineralization and transfer to the benthic consumers were also investigated during decomposition at low enrichment level (200 g WW). The interaction between lugworm exclusion and detrital enrichment did not modify sediment organic carbon or benthic respiration. Weak but significant changes were instead found for porewater inorganic carbon and microalgal biomass. Lugworm exclusion caused an increase of porewater carbon and a decrease of microalgal biomass, while detrital enrichment drove these values back to values typical of lugworm-dominated sediments. Lugworm exclusion also decreased the amount of macroalgae remaining into the sediment and accelerated detrital carbon mineralization and CO2 release to the water column. Eventually, the interaction between lugworm exclusion and detrital enrichment affected macrofauna abundance and diversity, which collapsed at high level of enrichment only when the lugworms were present. This study reveals that in nature the role of this ecosystem engineer may be variable and sometimes have no or even negative effects on stability, conversely to what it should be expected based on current research knowledge.

Highlights

It is widely recognized that species loss may affect ecosystem stability and, in turn, have important social and ecological consequences [1,2,3]
The loss of species that are important contributors to bioturbation may greatly change the response to detrital decomposition of sediment biogeochemistry
The exclusion of A. marina from intertidal sediments was expected to modify the biogeochemical response to macroalgal detrital enrichment

Summary

Introduction

It is widely recognized that species loss may affect ecosystem stability and, in turn, have important social and ecological consequences [1,2,3]. Empirical evidence has shown that sometimes species loss can have complex, often idiosyncratic effects on the stability of ecosystem functions and on both their resistance and resilience against disturbance [8,9]. This is especially true for the marine coastal ecosystem, where species identity, functional traits and environmental context may rule ecosystem functions and their response to disturbances [10,11,12]. It seems evident that understanding the role of species loss in marine systems might require a large body of knowledge of the functional role of individual species and of the consequences of losing particular species for ecosystem functions and for their response to disturbance

Methods

Results

Conclusion