Toward a network perspective in coastal ecosystem management.

Environmental management in coastal ecosystems has been challenged by the complex cumulative effects that occur when many small issues result in large ecological shifts. Current environmental management of these spaces focuses on identifying and limiting problematic stressors via a series of assessment techniques. Whilst there is a strong desire among managers to consider complexity in ecological responses to cumulative effects, current approaches for assessing risk focus on breaking down the issues into multiple cause and effect relationships. However, uncertainty arises when data and information for a place are limited, as is commonly the case, and this creates decision paralysis while more information is generated. Here, we discuss how ecological understanding of network interactions in coastal marine ecosystems can be used as a lens to bring together multiple lines of evidence and create actions. We list and describe four characteristics of marine ecosystem interaction networks including the possibility for; 1) indirect effects, 2) effects that emerge as stressor magnitude increases the number of network components implicated, 3) network interactions that amplify these indirect effects, and 4) feedbacks that reinforce or stabilise against indirect effects. We then link these four characteristics to three case studies of common coastal environmental issues to demonstrate how a general understanding of ecological interaction networks can enhance priorities for stressor management that can be applied even when specific data is limited.

Ecological network analysis of traits reveals variable response capacity to stress.

Response diversity increases the potential 'options' for ecological communities to respond to stress (i.e. response capacity). An indicator of community response diversity is the diversity of different traits associated with their capacity to be resistant to stress, to recover and to regulate ecosystem functions. We conducted a network analysis of traits using benthic macroinvertebrate community data from a large-scale field experiment to explore the loss of response diversity along environmental gradients. We elevated sediment nutrient concentrations (a process that occurs with eutrophication) at 24 sites (in 15 estuaries) with varying environmental conditions (water column turbidity and sediment properties). Macroinvertebrate community response capacity to nutrient stress was dependent on the baseline trait network complexity in the ambient community (i.e. non-enriched sediments). The greater the complexity of the baseline network, the less variable the network response to nutrient stress was; in contrast, more variable responses to nutrient stress occurred with simpler networks. Thus, stressors or environmental variables that shift baseline network complexity also shift the capacity for these ecosystems to respond to additional stressors. Empirical studies that explore the mechanisms responsible for loss of resilience are essential to inform our ability to predict changes in ecological states.

Estimating Effects of Sea Level Rise on Benthic Biodiversity and Ecosystem Functioning in a Large Meso-Tidal Coastal Lagoon.

Estuaries are among the world's most productive ecosystems, but due to their geographic location, they are at the forefront of anthropogenic pressures. Sea level rise (SLR) is one major consequence of climate change that poses a threat to estuaries with extensive intertidal habitats. The ecological implications of intertidal habitat loss have been largely overlooked despite their likely significance. We aimed to address this knowledge gap by investigating how benthic macroinvertebrate communities and their contributions to ecosystem function are likely to respond to SLR. Based on a spatially extensive dataset (119 sites) from a large coastal lagoon, depth, sediment chlorophyll concentrations, mud content, and average current speed were identified as the main drivers of community compositional turnover. Shifts in benthic community structure and associated functional implications were then evaluated using depth as a proxy for SLR. Three main macrofaunal groups representing intertidal, shallow subtidal, and deep subtidal habitats were identified. Functional trait analysis indicated low functional redundancy for a key intertidal suspension-feeding bivalve (Austrovenus stutchburyi) and the lack of a shallow subtidal functional replacement should intertidal habitats become inundated. These findings strongly suggest SLR and the associated environmental changes will alter estuarine macroinvertebrate communities, with implications for future ecosystem function and resilience.

Altered nitrogen transformation pathways and a legacy of sediment organic matter enrichment.

Estuaries are ecologically valuable ecosystems that process nutrients through complex biogeochemical processes. Here we identify drivers and inhibitors of nitrogen removal in unvegetated intertidal sandflats at six sites in Manukau Harbour (37° 2.00'S 174° 42.00'E) to quantify the exchange of solutes across the sediment-water interface, with nitrogen removal rates (NRR) measured at two contrasting sites (PI and CB) near and far, respectively, from an historical wastewater treatment plant. Solute fluxes were paired with sediment and macrofauna community data to identify drivers of ecosystem function. Fluxes of oxygen, nitrogen and phosphorous were found to vary among sites, with differences attributed to variation in sediment characteristics (grain size, chlorophyll a, organic content) and macrofauna community structure. Mean NRR was found to vary between sites (PI = 32.2 vs CB = 217.9 µmol N2/m2/h), with bioturbating macrofauna (bivalves Austrovenus stutchburyi and Macomona liliana), microphytobenthic biomass, and exposure to nutrients likely key contributing drivers.

The impact of cumulative stressor effects on uncertainty and ecological risk.

To enable environmental management actions to be more effectively prioritized, cumulative effects between multiple stressors need to be accounted for in risk-assessment frameworks. Ecological risk and uncertainty are generally high when multiple stressors occur. In the face of high uncertainty, transparent communication is essential to inform decision-making. The impact of stressor interactions on risk and uncertainty was assessed using generalized linear models for additive and multiplicative effect of six anthropogenic stressors on the abundance of estuarine macrofauna across New Zealand. Models that accounted for multiplicative stressor interactions demonstrated that non-additive effects dominated, had increased explanatory power (6 to 73 % relative increase between models), and thereby reduced the risk of unexpected ecological responses to stress. Secondly, 3D-plots provide important insights in the direction, magnitude and gradients of change, and aid transparency and communication of complex stressor effects. Notably, small changes in a stressor can cause a disproportionally steep gradient of change for a synergistic effect where the tolerance to stressors are lost, and would invoke precautionary management. 3D-plots were able to clearly identify directional shifts where the nature of the interaction changed from antagonistic to synergistic along increasing stressor gradients. For example, increased nitrogen load and exposure caused a shift from positive to negative effect on the abundance of a deposit-feeding polychaete (Magelona). Assessments relying on model coefficient estimates, which provide one effect term, could not capture the complexities observed in 3D-plots and are at risk of mis-identifying interaction types. Finally, visualising model uncertainty demonstrated that although error terms were higher for multiplicative models, they better captured the uncertainty caused by data availability. Together, the steep gradients of change identified in 3D-plots and the higher uncertainty in model predictions in multiplicative models urges more conservative limits to be set for management that account for risk and uncertainty in multiple stressor effects.

Who is contributing where? Predicting ecosystem service multifunctionality for shellfish species through ecological principles.

A key challenge in environmental management is determining how to manage multiple ecosystem services (ES) simultaneously, to ensure efficient and sustainable use of the environment and its resources. In marine environments, the spatial assessment of ES is lagging as a result of data-scarcity and modelling complexity. Applying mechanistic models to link ecological processes with ecosystem functions and services to assess areas of high ES potential can bridge this gap and accommodate assessments of functional differences between service providers. Here, we applied an ecosystem principles approach to assess ES potential for food provision, water quality regulation, nitrogen removal, and sediment stabilisation, provided by two estuarine bivalves (Austrovenus stutchburyi and Paphies australis) that differ in habitat association (broad and narrow distributions), to gain insight into the utility of these models for local-scale management. Maps of individual ES displayed differing patterns related to habitat associations of the species providing them, with variation in the quantities of services being delivered and locations of importance. Areas of importance for the provision of multiple services (number of services provided and their combined intensity per species) were assessed using hotspot analyses, which suggested that areas of high shellfish density at the harbour entrances were important for ES multifunctionality. A targeted management approach that includes environmental context, rather than a focus solely on the protection of high-density shellfish areas, is required to sustain the provision of individual ES.

Biogeochemical feedbacks to ocean acidification in a cohesive photosynthetic sediment.

Ecosystem feedbacks in response to ocean acidification can amplify or diminish diel pH oscillations in productive coastal waters. Benthic microalgae generate such oscillations in sediment porewater and here we ask how CO2 enrichment (acidification) of the overlying seawater alters these in the absence and presence of biogenic calcite. We placed a 1-mm layer of ground oyster shells, mimicking the arrival of dead calcifying biota (+Calcite), or sand (Control) onto intact silt sediment cores, and then gradually increased the pCO2 in the seawater above half of +Calcite and Control cores from 472 to 1216 µatm (pH 8.0 to 7.6, CO2:HCO3- from 4.8 to 9.6 × 10-4). Porewater [O2] and [H+] microprofiles measured 16 d later showed that this enrichment had decreased the O2 penetration depth (O2-pd) in +Calcite and Control, indicating a metabolic response. In CO2-enriched seawater: (1) sediment biogeochemical processes respectively added and removed more H+ to and from the sediment porewater in darkness and light, than in ambient seawater increasing the amplitude of the diel porewater [H+] oscillations, and (2) in darkness, calcite dissolution in +Calcite sediment decreased the porewater [H+] below that in overlying seawater, reversing the sediment-seawater H+ flux and decreasing the amplitude of diel [H+] oscillations. This dissolution did not, however, counter the negative effect of CO2 enrichment on O2-pd. We now hypothesise that feedback to CO2 enrichment-an increase in the microbial reoxidation of reduced solutes with O2-decreased the sediment O2-pd and contributed to the enhanced porewater acidification.

Biodiversity breakpoints along stress gradients in estuaries and associated shifts in ecosystem interactions.

Denitrification in coastal sediments can provide resilience to eutrophication in estuarine ecosystems, but this key ecosystem function is impacted directly and indirectly by increasing stressors. The erosion and loading of fine sediments from land, resulting in sedimentation and elevated sediment muddiness, presents a significant threat to coastal ecosystems worldwide. Impacts on biodiversity with increasing sediment mud content are relatively well understood, but corresponding impacts on denitrification are uncharacterised. Soft sediment ecosystems have a network of interrelated biotic and abiotic ecosystem components that contribute to microbial nitrogen cycling, but these components (especially biodiversity measures) and their relationships with ecosystem functions are sensitive to stress. With a large dataset spanning broad environmental gradients this study uses interaction network analysis to present a mechanistic view of the ecological interactions that contribute to microbial nitrogen cycling, showing significant changes above and below a stressor (mud) threshold. Our models demonstrate that positive biodiversity effects become more critical with a higher level of sedimentation stress, and show that effective ecosystem management for resilience requires different action under different scenarios.

Calcium carbonate alters the functional response of coastal sediments to eutrophication-induced acidification.

Coastal ocean acidification research is dominated by laboratory-based studies that cannot necessarily predict real-world ecosystem response given its complexity. We enriched coastal sediments with increasing quantities of organic matter in the field to identify the effects of eutrophication-induced acidification on benthic structure and function, and assess whether biogenic calcium carbonate (CaCO3) would alter the response. Along the eutrophication gradient we observed declines in macrofauna biodiversity and impaired benthic net primary productivity and sediment nutrient cycling. CaCO3 addition did not alter the macrofauna community response, but significantly dampened negative effects on function (e.g. net autotrophy occurred at higher levels of organic matter enrichment in +CaCO3 treatments than -CaCO3 (1400 vs 950 g dw m-2)). By identifying the links between eutrophication, sediment biogeochemistry and benthic ecosystem structure and function in situ, our study represents a crucial step forward in understanding the ecological effects of coastal acidification and the role of biogenic CaCO3 in moderating responses.

Linking Traits across Ecological Scales Determines Functional Resilience.

Under globally accelerating rates of ecosystem degradation, maintaining ecosystem function is a priority to avoid loss of valuable ecosystem services. Two factors are important: changes to the disturbance regime (stresses imposed) and resilience of biodiversity and ecosystem functions (the ecosystem's capacity to respond to change). Various attributes at different scales of ecological organisation confer resilience (from individual species to communities at landscape scales), but it is critical to understand how these attributes interact to inform how ecosystem function changes with disturbances that vary in intensity, spatial extent, and frequency. Individual species attributes influence their resistance, while attributes at the landscape-scale influence recovery of communities and function. Understanding resilience to disturbances requires defining the characteristics of a resilient community at multiple scales.

Effects of CO2 enrichment on benthic primary production and inorganic nitrogen fluxes in two coastal sediments.

Ocean acidification may alter the cycling of nitrogen in coastal sediment and so the sediment-seawater nitrogen flux, an important driver of pelagic productivity. To investigate how this perturbation affects the fluxes of NOX- (nitrite/nitrate), NH4+ and O2, we incubated estuarine sand and subtidal silt in recirculating seawater with a CO2-adjusted pH of 8.1 and 7.9. During a 41-day incubation, the seawater kept at pH 8.1 lost 97% of its NOX- content but the seawater kept at pH 7.9 lost only 18%. Excess CO2 increased benthic photosynthesis. In the silt, this was accompanied by a reversal of the initial NOX- efflux into influx. The estuarine sand sustained its initial NOX- influx but, by the end of the incubation, released more NH4+ at pH 7.9 than at pH 8.1. We hypothesise that these effects share a common cause; excess CO2 increased the growth of benthic microalgae and so nutrient competition with ammonia oxidising bacteria (AOB). In the silt, diatoms likely outcompeted AOB for NH4+ and photosynthesis increased the dark/light fluctuations in the pore water oxygenation inhibiting nitrification and coupled nitrification/denitrification. If this is correct, then excess CO2 may lead to retention of inorganic nitrogen adding to the pressures of increasing coastal eutrophication.

Modelling interactive effects of multiple disturbances on a coastal lake ecosystem: Implications for management.

Coastal lakes, also known as temporarily open/closed estuaries or intermittently closed and open lakes and lagoons, are common worldwide, are typically sites of high biodiversity and often contain abundant macrophyte populations. Anthropogenic stressors such as increased nutrient and sediment loading have adverse effects on submerged macrophytes, and when closed, the lack of tidal flushing makes coastal lakes highly susceptible to eutrophication. Lake openings to the sea may occur naturally, but many coastal lakes are also opened artificially, often to reduce inundation of surrounding land. Here we used a coupled hydrodynamic-ecological model (DYRESM-CAEDYM), modified to include dynamic feedback between submerged macrophyte biomass and sediment resuspension, to explore the interactive effects of multiple disturbances (openings, eutrophication and climate change) on the dynamics of primary producers in a coastal lake (Waituna Lagoon) in South Island, New Zealand. Our results indicate that with exposure to high external nutrient loads, the frequent disturbances caused by artificial openings prevent sustained dominance by algae (algal biomass averaged 192 g C m-2 with artificial openings compared to 453 g C m-2 with no openings). However, under current nutrient loading, climate change is likely to enhance the effects of eutrophication on the system (algal biomass averaged 227 g C m-2 with climate change compared with 192 g C m-2 for current climate). The model provides a decision-support tool to guide lake management in setting limits for nutrient loads and managing the opening regime, in order to prevent eutrophication and the potential collapse of the macrophyte community.

Estimating the effect of burrowing shrimp on deep-sea sediment community oxygen consumption.

Sediment community oxygen consumption (SCOC) is a proxy for organic matter processing and thus provides a useful proxy of benthic ecosystem function. Oxygen uptake in deep-sea sediments is mainly driven by bacteria, and the direct contribution of benthic macro- and mega-infauna respiration is thought to be relatively modest. However, the main contribution of infaunal organisms to benthic respiration, particularly large burrowing organisms, is likely to be indirect and mainly driven by processes such as feeding and bioturbation that stimulate bacterial metabolism and promote the chemical oxidation of reduced solutes. Here, we estimate the direct and indirect contributions of burrowing shrimp (Eucalastacus cf. torbeni) to sediment community oxygen consumption based on incubations of sediment cores from 490 m depth on the continental slope of New Zealand. Results indicate that the presence of one shrimp in the sediment is responsible for an oxygen uptake rate of about 40 µmol d-1, only 1% of which is estimated to be due to shrimp respiration. We estimate that the presence of ten burrowing shrimp m-2 of seabed would lead to an oxygen uptake comparable to current estimates of macro-infaunal community respiration on Chatham Rise based on allometric equations, and would increase total sediment community oxygen uptake by 14% compared to sediment without shrimp. Our findings suggest that oxygen consumption mediated by burrowing shrimp may be substantial in continental slope ecosystems.

Changes in the location of biodiversity-ecosystem function hot spots across the seafloor landscape with increasing sediment nutrient loading.

Declining biodiversity and loss of ecosystem function threatens the ability of habitats to contribute ecosystem services. However, the form of the relationship between biodiversity and ecosystem function (BEF) and how relationships change with environmental change is poorly understood. This limits our ability to predict the consequences of biodiversity loss on ecosystem function, particularly in real-world marine ecosystems that are species rich, and where multiple ecosystem functions are represented by multiple indicators. We investigated spatial variation in BEF relationships across a 300 000 m2 intertidal sandflat by nesting experimental manipulations of sediment pore water nitrogen concentration into sites with contrasting macrobenthic community composition. Our results highlight the significance of many different elements of biodiversity associated with environmental characteristics, community structure, functional diversity, ecological traits or particular species (ecosystem engineers) to important functions of coastal marine sediments (benthic oxygen consumption, ammonium pore water concentrations and flux across the sediment-water interface). Using the BEF relationships developed from our experiment, we demonstrate patchiness across a landscape in functional performance and the potential for changes in the location of functional hot and cold spots with increasing nutrient loading that have important implications for mapping and predicating change in functionality and the concomitant delivery of ecosystem services.

Density of Key-Species Determines Efficiency of Macroalgae Detritus Uptake by Intertidal Benthic Communities.

Accumulating evidence shows that increased biodiversity has a positive effect on ecosystem functioning, but the mechanisms that underpin this positive relationship are contentious. Complete extinctions of regional species pools are comparatively rare whereas compositional changes and reductions in abundance and biomass are common, although seldom the focus of biodiversity-ecosystem functioning studies. We use natural, small-scale patchiness in the density of two species of large bivalves with contrasting feeding modes (the suspension-feeding Austrovenus stutchburyi and deposit-feeding Macomona liliana) to examine their influence on the uptake of nitrogen from macroalgae detritus (i.e. measure of ecosystem function and food web efficiency) by other infauna in a 10-d laboratory isotope-tracer experiment. We predicted that densities of these key bivalve species and functional group diversity (calculated as Shannons H, a density-independent measure of community composition) of the intact infaunal community will be critical factors explaining variance in macroalgal per capita uptake rates by the community members and hence determine total uptake by the community. Results show that only two species, M. liliana and a large orbiniid polychaete (Scoloplos cylindrifer) dominated macroalgal nitrogen taken up by the whole community due to their large biomass. However, their densities were mostly not important or negatively influenced per capita uptake by other species. Instead, the density of a head-down deposit-feeder (the capitellid Heteromastus filiformis), scavengers (mainly nemertines and nereids) and species and functional group diversity, best explained per capita uptake rates in community members. Our results demonstrate the importance of species identity, density and large body size for ecosystem functioning and highlight the complex interactions underlying loss of ecological functions with declining biodiversity and compositional changes.

In situ soft sediment nutrient enrichment: A unified approach to eutrophication field experiments.

Adding fertiliser to sediments is an established way of studying the effects of eutrophication but a lack of consistent methodology, reporting on enrichment levels, or guidance on application rates precludes rigorous synthesis and meta-analysis. We developed a simple enrichment technique then applied it to 28 sites across an intertidal sandflat. Fertiliser application rates of 150 and 600gNm(-2) resulted in pore water ammonium concentrations respectively 1-110 and 4-580×ambient, with greater elevations observed in deeper (5-7cm) than surface (0-2cm) sediments. These enrichment levels were similar to eutrophic estuaries and were maintained for at least seven weeks. The high between-site variability could be partially explained by the sedimentary environment and macrofaunal community (42%), but only at the high application rate. We suggest future enrichment studies should be conducted in situ across large environmental gradients to incorporate real world complexity and increase generality of conclusions.

Same pattern, different mechanism: Locking onto the role of key species in seafloor ecosystem process.

Seafloor biodiversity is a key mediator of ecosystem functioning, but its role is often excluded from global budgets or simplified to black boxes in models. New techniques allow quantification of the behavior of animals living below the sediment surface and assessment of the ecosystem consequences of complex interactions, yielding a better understanding of the role of seafloor animals in affecting key processes like primary productivity. Combining predictions based on natural history, behavior of key benthic species and environmental context allow assessment of differences in functioning and process, even when the measured ecosystem property in different systems is similar. Data from three sedimentary systems in New Zealand illustrate this. Analysis of the behaviors of the infaunal ecosystem engineers in each system revealed three very different mechanisms driving ecosystem function: density and excretion, sediment turnover and surface rugosity, and hydraulic activities and porewater bioadvection. Integrative metrics of ecosystem function in some cases differentiate among the systems (gross primary production) and in others do not (photosynthetic efficiency). Analyses based on behaviors and activities revealed important ecosystem functional differences and can dramatically improve our ability to model the impact of stressors on ecosystem and global processes.

Effects of Detrital Subsidies on Soft-Sediment Ecosystem Function Are Transient and Source-Dependent.

Detrital subsidies from marine macrophytes are prevalent in temperate estuaries, and their role in structuring benthic macrofaunal communities is well documented, but the resulting impact on ecosystem function is not understood. We conducted a field experiment to test the effects of detrital decay on soft-sediment primary production, community metabolism and nutrient regeneration (measures of ecosystem function). Twenty four (2 m(2)) plots were established on an intertidal sandflat, to which we added 0 or 220 g DW m(-2) of detritus from either mangroves (Avicennia marina), seagrass (Zostera muelleri), or kelp (Ecklonia radiata) (n = 6 plots per treatment). Then, after 4, 17 and 46 d we measured ecosystem function, macrofaunal community structure and sediment properties. We hypothesized that (1) detrital decay would stimulate benthic primary production either by supplying nutrients to the benthic macrophytes, or by altering the macrofaunal community; and (2) ecosystem responses would depend on the stage and rate of macrophyte decay (a function of source). Avicennia detritus decayed the slowest with a half-life (t50) of 46 d, while Zostera and Ecklonia had t50 values of 28 and 2.6 d, respectively. However, ecosystem responses were not related to these differences. Instead, we found transient effects (up to 17 d) of Avicennia and Ecklonia detritus on benthic primary production, where initially (4 d) these detrital sources suppressed primary production, but after 17 d, primary production was stimulated in Avicennia plots relative to controls. Other ecosystem function response variables and the macrofaunal community composition were not altered by the addition of detritus, but did vary with time. By sampling ecosystem function temporally, we were able to capture the in situ transient effects of detrital subsidies on important benthic ecosystem functions.

Detecting Subtle Shifts in Ecosystem Functioning in a Dynamic Estuarine Environment.

Identifying the effects of stressors before they impact ecosystem functioning can be challenging in dynamic, heterogeneous 'real-world' ecosystems. In aquatic systems, for example, reductions in water clarity can limit the light available for photosynthesis, with knock-on consequences for secondary consumers, though in naturally turbid wave-swept estuaries, detecting the effects of elevated turbidity can be difficult. The objective of this study was to investigate the effects of shading on ecosystem functions mediated by sandflat primary producers (microphytobenthos) and deep-dwelling surface-feeding macrofauna (Macomona liliana; Bivalvia, Veneroida, Tellinidae). Shade cloths (which reduced incident light intensity by ~80%) were deployed on an exposed, intertidal sandflat to experimentally stress the microphytobenthic community associated with the sediment surface. After 13 weeks, sediment properties, macrofauna and fluxes of oxygen and inorganic nutrients across the sediment-water interface were measured. A multivariate metric of ecosystem function (MF) was generated by combining flux-based response variables, and distance-based linear models were used to determine shifts in the drivers of ecosystem function between non-shaded and shaded plots. No significant differences in MF or in the constituent ecosystem function variables were detected between the shaded and non-shaded plots. However, shading reduced the total explained variation in MF (from 64% in non-shaded plots to 15% in shaded plots) and affected the relative influence of M. liliana and other explanatory variables on MF. This suggests that although shade stress may shift the drivers of ecosystem functioning (consistent with earlier investigations of shading effects on sandflat interaction networks), ecosystem functions appear to have a degree of resilience to those changes.

Post-settlement dispersal: the neglected link in maintenance of soft-sediment biodiversity.

Seafloor integrity is threatened by disturbances owing to human activities. The capacity of the system to recover from disturbances, as well as maintain resilience and function, depends on dispersal. In soft-sediment systems, dispersal continues after larval settlement, but there are very few measurements of how far the post-settlers disperse in nature. Spatial scales of post-settlement dispersal are, however, likely to be similar to pelagic larval dispersal because of continued, frequent, small-scale dispersal over longer periods. The consequences of this dispersal may be more important for the maintenance of biodiversity and metacommunity dynamics than is pelagic larval dispersal, because of the greater size and competency of the dispersers. We argue that an increased empirical understanding of post-settlement dispersal processes is key for predicting how benthic communities will respond to local disturbances and shrinking regional species pools, with implications for monitoring, managing and conserving biodiversity.