Reintroducing a keystone bioturbator can facilitate microbial bioremediation in urban polluted sediments.

Anthropogenic environmental stressors have significantly reduced biodiversity and the capacity of remnant natural habitats to deliver ecosystem functions and services in urban areas. To mitigate these impacts and recover biodiversity and function, ecological restoration strategies are needed. While habitat restoration is proliferating in rural and peri-urban areas, strategies purposely designed to succeed under the environmental, social and political pressures of urban areas are lacking. Here, we propose that ecosystem health in marine urban areas can be improved by restoring biodiversity to the most dominant habitat, unvegetated sediments. We reintroduced a native ecosystem engineer, the sediment bioturbating worm Diopatra aciculata, and assessed their effects on microbial biodiversity and function. Results showed that worms can affect the diversity of microbes, but effects varied between locations. Worms caused shifts in microbial community composition and function at all locations. Specifically, the abundance of microbes capable of chlorophyll production (i.e. benthic microalgae) increased and the abundance of microbes capable of methane production decreased. Moreover, worms increased the abundances of microbes capable of denitrification in the site with lowest sediment oxygenation. Worms also affected microbes capable of degrading the polycyclic aromatic hydrocarbon toluene, although the direction of that effect was site-specific. This study provides evidence that a simple intervention such as the reintroduction of a single species can enhance sediment functions important for the amelioration of contamination and eutrophication, although further studies are needed to understand the variation in outcomes between sites. Nevertheless, restoration strategies targeting unvegetated sediments provide an opportunity to combat anthropogenic stressors in urban ecosystems and may be used for precondition before more traditional forms of habitat restoration such as seagrass, mangrove and shellfish restoration.

Assessing the validity and sensitivity of microbial processes within a hydrodynamic model.

Eutrophication due to excess anthropogenic nutrients in waterways is a significant issue worldwide. The pressure-stressor-response of a waterway to excessive nutrient loading is reliant on numerous physical and biological factors, including hydrodynamics and microbial processing. While substantial progress has been made towards simulating these mechanisms there are limited multi-disciplinary studies that relate the physical hydrodynamics of a site with the ecological response from linked laboratory and field studies. This paper presents the development of a coupled hydrodynamic and aquatic ecosystem response model, expanded to include an integrated microbial loop, that allows the explicit representation of heterotrophic bacteria growth and dissolved organic nutrient mineralisation. A unique long-term water quality dataset at an estuary in south-eastern Australia was used to validate and assess the model's sensitivity to complex biophysical processes driving the observed water quality variability. Results indicate that explicit time-varying bacterial mineralisation rates provide a substantially improved understanding of the broader aquatic ecosystem response than assigned fixed bulk rate parameter values, which are typically derived from non-local literature. Implementation of a microbial loop at the study site indicated that the model is sensitive to the boundary conditions, in particular catchment loads, with both net transport rates and the net growth rates of heterotrophic bacteria demonstrating different responses. Under average flow conditions, a smaller net transport and reduced nutrient availability has a pronounced effect of lowering net growth rates through the applied limitation factors. During high flow conditions, freshwater inflows increased net transport and nutrient loads, which resulted in higher net growth rates. Further, temporal variability in water temperature had a compounding effect on the model's response sensitivity. This approach has broader application in other riverine systems subject to eutrophication, and in interrogating linkages in hydrodynamic and microbial mediated processes (e.g., productivity). Future studies are recommended to better understand the sensitivity of aquatic ecosystem response models to microbial net growth rate kinetics at different temperatures and from top-down predation (e.g., zooplankton grazing).

Implications of bacterial mineralisation in aquatic ecosystem response models.

Widespread wastewater pollution is a major barrier to the sustainable management of freshwater and coastal marine ecosystems worldwide. Integrated multi-disciplinary studies are necessary to improve waterway management and protect ecosystem integrity. This study used the Generalised Likelihood Uncertainty Estimation (GLUE) methodology to link microbial community ecotoxicology laboratory data to a mechanistic aquatic ecosystem response model. The generic model provided good predictive skill for major water quality constituents, including heterotrophic bacteria dynamics (r2 = 0.91). The model was validated against observed data across a gradient of effluent concentrations from community whole effluent toxicity (WET) laboratory tests. GLUE analysis revealed that a combined likelihood measure increased confidence in the predictive capability of the model. This study highlights the importance of calibrating aquatic ecosystem response models with net growth rates (i.e., sum of the growth minus loss rate parameter terms) of biological functional groups. The final calibrated net growth rate value of heterotrophic bacteria determined using the GLUE analysis was selected to be 0.58, which was significantly greater than the average literature value of -0.15. This finding demonstrated that use of literature parameter values without a good understanding of the represented processes could create misleading outputs and result in unsatisfactory conclusions. Further, fixed bulk mineralisation rate literature values are typically higher than realistically required in aquatic ecosystem response models. This indicates that explicitly including bacterial mineralisation is crucial to represent microbial ecosystem functioning more accurately. Our study suggests that improved data collection and modelling efforts in real-world management applications are needed to better address nutrients released into the natural environment. Future studies should aim to better understand the sensitivity of aquatic ecosystem response models to bacterial mineralisation rates.

Wastewater effluents cause microbial community shifts and change trophic status.

Widespread wastewater pollution is one of the greatest challenges threatening the sustainable management of rivers globally. Understanding microbial responses to gradients in environmental stressors, such as wastewater pollution, is crucial to identify thresholds of community change and to develop management strategies that protect ecosystem integrity. This study used multiple lines of empirical evidence, including a novel combination of microbial ecotoxicology methods in the laboratory and field to link pressure-stressor-response relationships. Specifically, community-based whole effluent toxicity (WET) testing and environmental genomics were integrated to determine real-world community interactions, shifts and functional change in response to wastewater pollution. Here we show that wastewater effluents above moderate (>10%) concentrations caused consistent significant shifts in bacterial community structure and function. These thresholds of community shifts were also linked to changes in the trophic state of receiving waters in terms of nutrient concentrations. Differences in the community responses along the effluent concentration gradient were primarily driven by two globally relevant bacterial indicator taxa, namely Malikia spp. (Burkholderiales) and hgcI_clade (Frankiales). Species replacement occurred above moderate effluent concentrations with abundances of Malikia spp. increasing, while abundances of hgcI_clade decreased. The responses of Malikia spp. and hgcI_clade matched gene patterns associated with globally important nitrogen cycling pathways, such as denitrification and nitrogen fixation, which linked the core individual taxa to putative function and ecosystem processes, rarely achieved in previous studies. This study has identified potential indicators of change in trophic status and the functional consequences of wastewater pollution. These findings have immediate implications for both the management of environmental stressors and protection of aquatic ecosystems.

Making seawalls multifunctional: The positive effects of seeded bivalves and habitat structure on species diversity and filtration rates.

The marine environment is being increasingly modified by the construction of artificial structures, the impacts of which may be mitigated through eco-engineering. To date, eco-engineering has predominantly aimed to increase biodiversity, but enhancing other ecological functions is arguably of equal importance for artificial structures. Here, we manipulated complexity through habitat structure (flat, and 2.5 cm, 5 cm deep vertical and 5 cm deep horizontal crevices) and seeding with the native oyster (Saccostrea glomerata, unseeded and seeded) on concrete tiles (0.25 m × 0.25 m) affixed to seawalls to investigate whether complexity (both orientation and depth of crevices) influences particle removal rates by suspension feeders and colonisation by different functional groups, and whether there are any ecological trade-offs between these functions. After 12 months, complex seeded tiles generally supported a greater abundance of suspension feeding taxa and had higher particle removal rates than flat tiles or unseeded tiles. The richness and diversity of taxa also increased with complexity. The effect of seeding was, however, generally weaker on tiles with complex habitat structure. However, the orientation of habitat complexity and the depth of the crevices did not influence particle removal rates or colonising taxa. Colonisation by non-native taxa was low compared to total taxa richness. We did not detect negative ecological trade-offs between increased particle removal rates and diversity and abundance of key functional groups. Our results suggest that the addition of complexity to marine artificial structures could potentially be used to enhance both biodiversity and particle removal rates. Consequently, complexity should be incorporated into future eco-engineering projects to provide a range of ecological functions in urbanised estuaries.

A novel real-world ecotoxicological dataset of pelagic microbial community responses to wastewater.

Real-world observational datasets that record and quantify pressure-stressor-response linkages between effluent discharges and natural aquatic systems are rare. With global wastewater volumes increasing at unprecedented rates, it is urgent that the present dataset is available to provide the necessary information about microbial community structure and functioning. Field studies were performed at two time-points in the Austral summer. Single-species and microbial community whole effluent toxicity (WET) testing was performed at a complete range of effluent concentrations and two salinities, with accompanying environmental data to provide new insights into nutrient and organic matter cycling, and to identify ecotoxicological tipping points. The two salinity regimes were chosen to investigate future scenarios based on a predicted salinity increase at the study site, typical of coastal regions with rising sea levels globally. Flow cytometry, amplicon sequencing of 16S and 18S rRNA genes and micro-fluidic quantitative polymerase-chain reactions (MFQPCR) were used to determine chlorophyll-a and total bacterial cell numbers and size, as well as taxonomic and functional diversity of pelagic microbial communities. This strong pilot dataset could be replicated in other regions globally and would be of high value to scientists and engineers to support the next advances in microbial ecotoxicology, environmental biomonitoring and estuarine water quality modelling.

After decades of stressor research in urban estuarine ecosystems the focus is still on single stressors: A systematic literature review and meta-analysis.

Natural systems are threatened by a variety of anthropogenic stressors and so understanding the interactive threats posed by multiple stressors is essential. In this study we focused on urban stressors that are ubiquitous to urban estuarine systems worldwide: elevated nutrients, toxic chemical contaminants, built infrastructure and non-indigenous species (NIS). We investigated structural (abundance, diversity and species richness) and functional endpoints (productivity, primary production (chlorophyll-a) and metabolism) commonly used to determine responses to these selected stressors. Through a systematic review of global literature, we found 579 studies of our selected stressors; 93% measured responses to a single stressor, with few assessing the effects of multiple stressors (7%). Structural endpoints were commonly used to measure the effects of stressors (49% of the total 579 studies). Whereas, functional endpoints were rarely assessed alone (10%) but rather in combination with structural endpoints (41%). Elevated nutrients followed by NIS were the most studied single stressors (43% and 16% of the 541 single stressor studies), while elevated nutrients and toxic contaminants were overwhelmingly the most common stressor combination (79% of the 38 multiple stressor studies); with NIS and built infrastructure representing major gaps in multi-stressor research. In the meta-analysis, structural endpoints tended to decrease, while functional endpoints increased and/or decreased in response to different types of organisms or groups. We predicted an antagonistic effect of elevated nutrients and toxic contaminants based on the opposing enriching versus toxic effects of this stressor combination. Of note, biodiversity was the only endpoint that revealed such an antagonistic response. Our results highlight the continuing paucity of multiple stressor studies and provide evidence for opposing patterns in the responses to single and interacting stressors depending on the measured endpoint. The latter is of significant consequence to understanding relevant impacts of stressors in coastal monitoring and management.

Artificial structures alter kelp functioning across an urbanised estuary.

Assessments of human impacts on natural habitats often focus on the abundance of component species, yet physiological and/or sub-lethal effects of stressors on functional attributes may be equally important to consider. Here we evaluated how artificial structures, an integral part of urbanisation in the marine environment, affects key functional properties of the habitat-forming kelp Ecklonia radiata. Given that stressors rarely occur in isolation, we assessed the effects of infrastructure across an urbanised estuary. Estuaries are ideal for studying how multiple anthropogenic and natural stressors influence potential impacts of infrastructure on habitat-forming species because these habitats usually face a wide range and levels of stressors. Here, we compared the abundance of habitat-forming macro-algae as well as the growth, erosion and photosynthetic activity of kelp in artificial and natural habitats across one of the largest urbanised estuaries in the word - Sydney Harbour. We predicted that effects of artificial structures on functional attributes of kelps would be stronger in the inner area of the Harbour, characterised by higher levels of human impacts and low flushing. Contrary to our predictions, we found that effects of infrastructure were consistent across the estuary, regardless of the ecological footprint caused by human activities or natural environmental gradients. When differences were observed between areas of the estuary, they mostly occurred independently of impacts of substrate type. Importantly, we found lower erosion rates of kelp on pilings than on reefs, likely resulting in lower production of detritus in estuaries where natural reefs are degraded or lost and pilings added. Such impacts have important implications for the connectivity among coastal habitats and secondary productivity in adjacent and remote habitats, which are highly dependent on the exportation of kelp detritus. Our study is the first to assess potential functional consequences of urbanisation through physiological and/or biomechanical effects on habitat-formers, an often overlooked mechanism of environmental impact on ecosystem functioning.

Uncovering hidden heterogeneity: Geo-statistical models illuminate the fine scale effects of boating infrastructure on sediment characteristics and contaminants.

Infrastructure associated with coastal communities is likely to not only directly displace natural systems, but also leave environmental footprints' that stretch over multiple scales. Some coastal infrastructure will, there- fore, generate a hidden layer of habitat heterogeneity in sediment systems that is not immediately observable in classical impact assessment frameworks. We examine the hidden heterogeneity associated with one of the most ubiquitous coastal modifications; dense swing moorings fields. Using a model based geo-statistical framework we highlight the variation in sedimentology throughout mooring fields and reference locations. Moorings were correlated with patches of sediment with larger particle sizes, and associated metal(loid) concentrations in these patches were depressed. Our work highlights two important ideas i) mooring fields create a mosaic of habitat in which contamination decreases and grain sizes increase close to moorings, and ii) model- based frameworks provide an information rich, easy-to-interpret way to communicate complex analyses to stakeholders.

Coastal urban lighting has ecological consequences for multiple trophic levels under the sea.

Urban land and seascapes are increasingly exposed to artificial lighting at night (ALAN), which is a significant source of light pollution. A broad range of ecological effects are associated with ALAN, but the changes to ecological processes remain largely unstudied. Predation is a key ecological process that structures assemblages and responds to natural cycles of light and dark. We investigated the effect of ALAN on fish predatory behaviour, and sessile invertebrate prey assemblages. Over 21days fish and sessile assemblages were exposed to 3 light treatments (Day, Night and ALAN). An array of LED spotlights was installed under a wharf to create the ALAN treatments. We used GoPro cameras to film during the day and ALAN treatments, and a Dual frequency IDentification SONar (DIDSON) to film during the night treatments. Fish were most abundant during unlit nights, but were also relatively sedentary. Predatory behaviour was greatest during the day and under ALAN than at night, suggesting that fish are using structures for non-feeding purposes (e.g. shelter) at night, but artificial light dramatically increases their predatory behaviour. Altered predator behaviour corresponded with structural changes to sessile prey assemblages among the experimental lighting treatments. We demonstrate the direct effects of artificial lighting on fish behaviour and the concomitant indirect effects on sessile assemblage structure. Current and future projected use of artificial lights has the potential to significantly affect predator-prey interactions in marine systems by altering habitat use for both predators and prey. However, developments in lighting technology are a promising avenue for mitigation. This is among the first empirical evidence from the marine system on how ALAN can directly alter predation, a fundamental ecosystem process, and have indirect trophic consequences.

Building 'blue': An eco-engineering framework for foreshore developments.

Urbanisation in terrestrial systems has driven architects, planners, ecologists and engineers to collaborate on the design and creation of more sustainable structures. Examples include the development of 'green infrastructure' and the introduction of wildlife corridors that mitigate urban stressors and provide positive ecological outcomes. In contrast, efforts to minimise the impacts of urban developments in marine environments have been far more restricted in their extent and scope, and have often overlooked the ecological role of the built environment as potential habitat. Urban foreshore developments, i.e. those built on the interface of intertidal and/or subtidal zones, have the potential to incorporate clear multi-functional outcomes, by supporting novel ecosystems. We present a step-by-step eco-engineering framework for 'building blue' that will allow coastal managers to facilitate planning and construction of sustainable foreshore developments. Adopting such an approach will incorporate ecological principles, thereby mitigating some of the environmental impacts, creating more resilient urban infrastructure and environments, and maximising benefits to the multiple stakeholders and users of marine urban waterfronts.

Shallow moving structures promote marine invader dominance.

Global increases in urban development have resulted in severe habitat modification in many estuaries. Most are now dominated by artificial structures, which might have a myriad of effects on native species. The provision of extra hard substrata presents additional free space, and recent research suggests non-indigenous epifauna may be able to exploit these artificial structures (particularly pontoons) more effectively than native species. The early development of fouling assemblages was compared on settlement plates attached to fixed or moving experimental structures at depths of 0.5 m and 2 m. Invertebrate invaders as a group were disproportionately more numerous on shallow, moving plates (essentially floating surfaces) than on deeper plates, whereas native epifauna were less numerous than invaders in all treatments. Importantly, however, individual invasive species showed differing effects of movement and depth. Future management strategies should take into account the potential for shallow, moving structures to enhance invader dominance and strongly consider using fixed structures to reduce opportunities for invaders.

Differential effects of tributyltin and copper antifoulants on recruitment of non-indigenous species.

Maritime transport is a primary vector for many marine invaders. For the past two decades, most commercial vessels have used tributyltin (TBT) antifouling (AF) paint, whereas recreational vessels have been restricted to alternatives, most commonly containing copper. Settlement plates painted with a collar of copper or TBT AF paint, and unpainted control plates, were deployed in commercial and recreational embayments in Port Jackson, Australia, and sampled photographically after 5 and 10 months. Copper enhanced early recruitment of several non-indigenous species (NIS), whereas recruitment of indigenous species was typically reduced by copper. TBT limited the recruitment of NIS for just 5 months and indigenous species, for the entire study. The results suggest that the use of toxic AF paints, and the possible accumulation of AF biocides in embayments, may be negatively affecting indigenous epibiota. Conversely, copper antifoulants on recreational vessels may be facilitating the transport and establishment of copper tolerant NIS into disturbed estuarine habitats.