Exploring the links between nutrient cycling, macrofauna and environmental influences in estuarine sediments

In the short-term hypoxia experiment labile metals accumulated in the pore-waters of surface sediments, intensifying the concentration gradient of metals across the sediment-water interface and increasing the likelihood of diffusive flux from the sediments. Therefore, I measured metal fluxes to the water column during the extended O2 depletion experiment. Manganese and Fe, which are known to significantly regulate the release of other divalent cations from sub-oxic sediments, fluxed from sediments from all sites as hypoxia developed. However, the release of As, Cd, Cu and Zn was comparatively low and unrelated to the degree of sediment contamination, although As release increased significantly under anoxic conditions. Importantly, the most significant release of Cu and Zn occurred within the first few days of hypoxia, suggesting that brief and recurring episodes of O2 depletion may present a greater risk for metal release than periods of extended hypoxia.

The direct effects of reduced DO conditions on macrofauna assemblages were not measured, but I performed an experiment to assess whether the functional traits of a key and locally relevant macrofauna species, Cirriformia filigera, a metal-tolerant bioturbating polychaete worm, might alter the nutrient dynamics of highly contaminated sediments in this system. The presence of C. filigera resulted in a doubling of sediment metabolism and a tripling of denitrification, possibly as a result of C. filigera burrow construction and bioturbation. Oxygen enriched burrows infiltrate into deeper anoxic sediments resulting in a 3-D matrix of overlapping aerobic and anaerobic regions facilitating micro-organism activity and promoting nitrifier-denitrifier coupling. The large increases in NH4+ efflux measured most likely reflected the combined flushing of existing NH4+ from the sediment due to bioturbation, the diffusive and advective release of the products of OM hydrolysis in burrow walls plus excreted wastes.

To understand the effects of extended hypoxia on nutrient cycling and metal availability and test if the effects would vary according to local environmental conditions within the estuary, I measured the flux of nutrients and metals between the sediment and water column in sealed cores incubated without O2 replenishment for 40 days using sediments collected from 3 sites with varying concentrations of contaminants, organic enrichment and macrofauna functional properties. There was an apparent relationship between how quickly the cores became hypoxic and the presence of different macrofauna functional groups. The presence of large numbers of benthic epifauna at one site, compared with infauna at another, potentially accelerated the onset of hypoxia. Further reductions in DO resulted in the mortality, decomposition and mineralisation of the macrofauna. Decomposition of epifauna was more rapid than infauna with an earlier and larger pulse of bioavailable nutrients (NH4+ and PO4+) to the water column at the epifauna dominated site. In contrast, sediments from a site containing little macrofauna and a high proportion of terrigenous organic material showed limited release of these nutrients.

Benthic environments form a key component of estuarine ecosystems; mediating the mineralization of organic matter and the recycling of nutrients whilst providing an important habitat for an array of fauna and flora. Estuarine environments tend to be more urbanised and industrialised than other coastal ecosystems, often becoming enriched with nutrients and subject to elevated loads of pollutants, such as heavy metals. The negative effects of these anthropogenic stressors have led to concerns regarding the condition and stability of estuarine environments. Excess nutrients interfere with the complex biogeochemical interactions that control the benthic nitrogen cycle, potentially leading to algal blooms and the sedimentation of high loads of organic matter which can subsequently deplete oxygen in bottom waters. Heavy metal contaminants impact the diversity and functioning of macrofauna communities and may interfere with biogeochemical microbial processes. Interactions between increased nutrients and heavy metal contaminants are complex: macrofauna influence the nitrogen cycle via bioirrigation and bioturbation activities, thus contaminant impacts on macrofauna diversity can also indirectly impact nutrient cycling. In this research project I explored the interactions between the effects of heavy metal contaminants, algal blooms, macrofauna functional activities and oxygen depletion and benthic biogeochemical processes in a multi-use temperate estuary, the Derwent, in south-eastern Australia, using a combination of spatial surveys and experimental approaches.

Surveys found that variation in nutrient flux was best explained by dissolved oxygen (DO) conditions, total carbon (TC), benthic microalgae and macrofauna abundance. A positive relationship between DO concentration and NOx (nitrate + nitrite) and N2 fluxes and a negative relationship between DO and NH4+ and PO4- production was also indicated. Macrofauna distribution was best explained by depth, salinity, DO and bioavailable Zn and Pb as measured by diffusive gradient in thin-films metal sampling units (DGTs). Based on the results of the spatial survey, I ran manipulative laboratory experiments that tested the effects of short (< 24 hours) and long term (40 days) O2 depletion on nutrient fluxes and on the bioavailability of metals in Derwent sediments. Twenty-four hours of O2 depletion was sufficient to rapidly decrease the oxygenation and the O2 penetration depth of sediments within experimental laboratory cores. As a result NH4+ release from the sediment increased whereas NOx flux out of the sediment decreased, suggesting reduced nitrification efficiency. In addition, DGT sampling devices, which measure labile metals within sediments, detected a two-fold increase in pore-water Cd and a five-fold increase in Cu in surface sediments under reduced DO conditions.

The key findings of this study are 1) DO declines compromise critical nutrient cycling processes within benthic sediments and the effects are modified by local biological and environmental conditions; 2) reduced DO concentrations can lead to an increase in metal availability in surface sediments resulting in small effluxes to the water column; 3) metal availability influences the distribution of macrofauna and 4) changes to the functional diversity of macrofauna communities are likely to have an effect on nutrient cycling. This work has worldwide application to urbanised coastal environments that are increasingly subject to anthropogenic stressors such as nutrient and organic enrichment, metal contamination and periods of hypoxia. In addition these results will assist environmental managers to identify sensitivities in the Derwent estuary and more reliably direct monitoring.