Topography-based modulation of environmental factors as a mechanism for intertidal microhabitat formation: A basis for marine ecological design.

Topographic complexity is often considered to be closely associated with habitat complexity and niche diversity; however, complex topography per se does not imply habitat suitability. Rather, ecologically suitable habitats may emerge if topographic features interact with environmental factors and thereby alter their surrounding microenvironment to the benefit of local organisms (e.g., resource provisioning, stress mitigation). Topography may thus act as a key modulator of abiotic stressors and biotic pressures, particularly in environmentally challenging intertidal systems. Here, we review how topography can alter microhabitat conditions with respect to four resources required by intertidal organisms: a source of energy (light, suspended food particles, prey, detritus), water (hydration, buffering of light, temperature and hydrodynamics), shelter (temperature, wave exposure, predation), and habitat space (substratum area, propagule settlement, movement). We synthesize mechanisms and quantitative findings of how environmental factors can be altered through topography and suggest an organism-centered 'form-follows-ecological-function' approach to designing multifunctional marine infrastructure.

Complexity-functioning relationships differ across different environmental conditions.

Habitat complexity is widely considered an important determinant of biodiversity, and enhancing complexity can play a key role in restoring degraded habitats. However, the effects of habitat complexity on ecosystem functioning - as opposed to biodiversity and community structure - are relatively poorly understood for artificial habitats, which dominate many coastlines. With Greening of Grey Infrastructure (GGI) approaches, or eco-engineering, increasingly being applied around the globe, it is important to understand the effects that modifying habitat complexity has on both biodiversity and ecological functioning in these highly modified habitats. We assessed how manipulating physical (primary substrate) and/or biogenic habitat (bivalves) complexity on intertidal artificial substrata affected filtration rates, net and gross primary productivity (NPP and GPP, respectively) and community respiration (CR) - as well as abundance of filter feeders and macro-algae and habitat use by cryptobenthic fish across six locations in three continents. We manipulated both physical and biogenic complexity using 1) flat or ridged (2.5 cm or 5 cm) settlement tiles that were either 2) unseeded or seeded with oysters or mussels. Across all locations, increasing physical and biogenic complexity (5 cm seeded tiles) had a significant effect on most ecological functioning variables, increasing overall filtration rates and community respiration of the assemblages on tiles but decreasing productivity (both GPP and NPP) across all locations. There were no overall effects of increasing either type of habitat complexity on cryptobenthic fish MaxN, total time in frame or macro-algal cover. Within each location, there were marked differences in the effects of habitat complexity. In Hobart, we found higher filtration, filter feeder biomass and community respiration on 5 cm tiles compared to flat tiles. However, at this location, both macro-algae cover and GPP decreased with increasing physical complexity. Similarly in Dublin, filtration, filter feeder biomass and community respiration were higher on 5 cm tiles compared to less complex tiles. In Sydney, filtration and filter feeder biomass were higher on seeded than unseeded tiles, and fish MaxN was higher on 5 cm tiles compared to flat tiles. On unseeded tiles in Sydney, filter feeder biomass also increased with increasing physical complexity. Our findings suggest that GGI solutions via increased habitat complexity are likely to have trade-offs among potentially desired functions, such as productivity and filtration rates, and variable effects on cryptobenthic fish communities. Importantly, our results show that the effects of GGI practices can vary markedly according to the environmental context and therefore should not be blindly and uniformly applied across the globe.

Developing expert scientific consensus on the environmental and societal effects of marine artificial structures prior to decommissioning.

Thousands of artificial ('human-made') structures are present in the marine environment, many at or approaching end-of-life and requiring urgent decisions regarding their decommissioning. No consensus has been reached on which decommissioning option(s) result in optimal environmental and societal outcomes, in part, owing to a paucity of evidence from real-world decommissioning case studies. To address this significant challenge, we asked a worldwide panel of scientists to provide their expert opinion. They were asked to identify and characterise the ecosystem effects of artificial structures in the sea, their causes and consequences, and to identify which, if any, should be retained following decommissioning. Experts considered that most of the pressures driving ecological and societal effects from marine artificial structures (MAS) were of medium severity, occur frequently, and are dependent on spatial scale with local-scale effects of greater magnitude than regional effects. The duration of many effects following decommissioning were considered to be relatively short, in the order of days. Overall, environmental effects of structures were considered marginally undesirable, while societal effects marginally desirable. Experts therefore indicated that any decision to leave MAS in place at end-of-life to be more beneficial to society than the natural environment. However, some individual environmental effects were considered desirable and worthy of retention, especially in certain geographic locations, where structures can support improved trophic linkages, increases in tourism, habitat provision, and population size, and provide stability in population dynamics. The expert analysis consensus that the effects of MAS are both negative and positive for the environment and society, gives no strong support for policy change whether removal or retention is favoured until further empirical evidence is available to justify change to the status quo. The combination of desirable and undesirable effects associated with MAS present a significant challenge for policy- and decision-makers in their justification to implement decommissioning options. Decisions may need to be decided on a case-by-case basis accounting for the trade-off in costs and benefits at a local level.

To what extent can decommissioning options for marine artificial structures move us toward environmental targets?

Switching from fossil fuels to renewable energy is key to international energy transition efforts and the move toward net zero. For many nations, this requires decommissioning of hundreds of oil and gas infrastructure in the marine environment. Current international, regional and national legislation largely dictates that structures must be completely removed at end-of-life although, increasingly, alternative decommissioning options are being promoted and implemented. Yet, a paucity of real-world case studies describing the impacts of decommissioning on the environment make decision-making with respect to which option(s) might be optimal for meeting international and regional strategic environmental targets challenging. To address this gap, we draw together international expertise and judgment from marine environmental scientists on marine artificial structures as an alternative source of evidence that explores how different decommissioning options might ameliorate pressures that drive environmental status toward (or away) from environmental objectives. Synthesis reveals that for 37 United Nations and Oslo-Paris Commissions (OSPAR) global and regional environmental targets, experts consider repurposing or abandoning individual structures, or abandoning multiple structures across a region, as the options that would most strongly contribute toward targets. This collective view suggests complete removal may not be best for the environment or society. However, different decommissioning options act in different ways and make variable contributions toward environmental targets, such that policy makers and managers would likely need to prioritise some targets over others considering political, social, economic, and ecological contexts. Current policy may not result in optimal outcomes for the environment or society.

Invasive macroalgae in native seagrass beds - vectors of spread and impacts.

BACKGROUND AND AIMS: Worldwide, invasive species are spreading through marine systems at an unprecedented rate with both positive and negative consequences for ecosystems and biological functioning of organisms. Human activities from shipping to habitat damage and modification are known vectors of spread, although biological interactions including epibiosis are increasingly recognised as potentially important to introduction into susceptible habitats. METHODS: We assessed a novel spread mechanism - limpets as transporters of invasive algae, Sargassum muticum into beds of the seagrass Zostera marina - and the physiological impact of its invasion. The association of S. muticum with three limpet species and other habitats was assessed using intertidal surveys on rocky shores and snorkelling at two seagrass sites in the UK. A 4-yr field study tested the effect of S. muticum on Z. marina shoot density, dry weight and phenolic compounds (caffeic and tannic acid) content, and a laboratory experiment tested the impact of S. muticum on nutrient partitioning (C/H/N/P/Si), photosynthetic efficiency (Fv/Fm) and growth of Z. marina. RESULTS: On rocky shores 15% of S. muticum occurrences were attached to the shells of live limpets. In seagrass beds 5% of S. muticum occurrences were attached to the shells of dead limpets. The remainder were attached to rock, cobblestones, the seagrass matrix or embedded within the sand. Z. marina density and phenolics content was lower when S. muticum co-occurred with it. Over 3-years, photosynthetic response of Z. marina to S. muticum was idiosyncratic, and S. muticum had no effect on nutrient partitioning in Z. marina. CONCLUSIONS: Our results show limpets support S. muticum as an epibiont and may act as a previous unreported transport mechanism introducing invaders into sensitive habitats. S. muticum reduced phenolics production in Z. marina which may weaken its defensive capabilities and facilitate proliferation of S. muticum. The effect of S. muticum on Z. marina photosynthesis requires further work but having no effect on the capacity of Z. marina to sequester nutrients suggests a degree of resilience to this invader.

Metrics matter: Multiple diversity metrics at different spatial scales are needed to understand species diversity in urban environments.

Worldwide, natural habitats are being replaced by artificial structures due to urbanisation. Planning of such modifications should strive for environmental net gain that benefits biodiversity and ecosystems. Alpha (α) and gamma (γ) diversity are often used to assess 'impact' but are insensitive metrics. We test several diversity measures across two spatial scales to compare species diversity in natural and artificial habitats. We show γ-diversity indicates equivalency in biodiversity between natural and artificial habitats, but natural habitats support greater taxon (α) and functional richness. Within-site ß-diversity was also greater in natural habitats, but among-site ß-diversity was greater in artificial habitats, contradicting the commonly held view that urban ecosystems are more biologically homogenous than natural ecosystems. This study suggests artificial habitats may in fact provide novel habitat for biodiversity, challenges the applicability of the urban homogenisation concept and highlights a significant limitation of using just α-diversity (i.e., multiple metrics are needed and recommended) for assessing environmental net gain and attaining biodiversity conservation goals.

Challenges of evidence-informed offshore decommissioning: an environmental perspective.

Many offshore artificial structures are at or nearing their ends of life, and society faces the considerable challenge that is decommissioning. Current scientific evidence of the ecological and environmental consequences of decommissioning is insufficient to reliably and accurately inform decision-making and policy development. Thus, we must strengthen the scientific basis for evidence-informed decommissioning.

Epibionts provide their basibionts with associational resistance to predation but at a cost.

Epibiosis is increasingly considered a survival strategy in space-limited environments. However, epibionts can create a new interface between its host, environment and potential predators which may alter predator-prey relationships and biological functioning. Ex-situ experiments investigated the potential costs and benefits of epibiont barnacles on mortality and feeding rate of the mussel, Mytilus edulis, and its predator, the whelk Nucella lapillus. Mussels with living epibiont barnacles suffered no mortality from whelk predation, but when barnacles were absent, mortality was ∼21% over 48 days. Further comparisons revealed the structural complexity of barnacles provided mussels with protection from whelk predation, while the presence of living barnacles increased predator-prey encounters but led to predators targeting barnacles over mussels. Feeding trials revealed feeding rate increased by ∼24% in mussels with living epibionts over mussels with dead or without epibionts, indicating potential costs of hosting epibionts. Our results show that epibionts provide important associational resistance for mussels against whelk predation but a potential cost to the mussel of hosting epibionts requiring increased energy acquisition. These findings advance our understanding of associational resistance derived from epibionts and serve to highlight the potential trade-offs affecting basibiont functioning while showing the importance of positive ecological interactions in ecosystem structure and functioning.

Science paper or big data? Assessing invasion dynamics using observational data.

Non-native species are spreading at an unprecedented rate over large spatial scales, with global environmental change and growth in commerce providing novel opportunities for range expansion. Assessing the pattern and rate of spread is key to the development of strategies for safeguarding against future invasions and efficiently managing existing ones. Such assessments often depend on spatial distribution data from online repositories, which can be spatially biased, imprecise, and lacking in quantity. Here, the influence of disparities between occurrence records from online data repositories and what is known of the invasion history from peer-reviewed published literature on non-native species range expansion was evaluated using 6693 records of the Pacific oyster, Magallana gigas (Thunberg, 1793), spanning 56 years of its invasion in Europe. Two measures of spread were calculated: maximum rate of spread (distance from introduction site over time) and accumulated area (spatial expansion). Results suggest that despite discrepancies between online and peer-reviewed data sources, including a paucity of records from the early invasion history in online repositories, the use of either source does not result in significantly different estimates of spread. Our study significantly improves our understanding of the European distribution of M. gigas and suggests that a combination of short- and long-range dispersal drives range expansions. More widely, our approach provides a framework for comparison of online occurrence records and invasion histories as documented in the peer-reviewed literature, allowing critical evaluation of both data sources and improving our understanding of invasion dynamics significantly.

Differential effects of ocean acidification and warming on biological functioning of a predator and prey species may alter future trophic interactions.

Independently, ocean warming (OW) and acidification (OA) from increased anthropogenic atmospheric carbon dioxide are argued to be two of the greatest threats to marine organisms. Increasingly, their interaction (ocean acidification and warming, OAW) is shown to have wide-ranging consequences to biological functioning, population and community structure, species interactions and ecosystem service provision. Here, using a multi-trophic experiment, we tested the effects of future OAW scenarios on two widespread intertidal species, the blue mussel Mytilus edulis and its predator Nucella lapillus. Results indicate negative consequences of OAW on the growth, feeding and metabolic rate of M. edulis and heightened predation risk. In contrast, Nucella growth and metabolism was unaffected and feeding increased under OAW but declined under OW suggesting OA may offset warming consequences. Should this differential response between the two species to OAW, and specifically greater physiological costs to the prey than its predator come to fruition in the nature, fundamental change in ecosystem structure and functioning could be expected as trophic interactions become disrupted.

Material type influences the abundance but not richness of colonising organisms on marine structures.

Urbanisation of coastal areas and growth in the blue economy drive the proliferation of artificial structures in marine environments. These structures support distinct ecological communities compared to natural hard substrates, potentially reflecting differences in the materials from which they are constructed. We undertook a meta-analysis of 46 studies to compare the effects of different material types (natural or eco-friendly vs. artificial) on the colonising biota on built structures. Neither the abundance nor richness of colonists displayed consistent patterns of difference between artificial and natural substrates or between eco-friendly and standard concrete. Instead, there were differences in the abundance of organisms (but not richness) between artificial and natural materials, that varied according to material type and by functional group. When compared to biogenic materials and rock, polymer and metal supported significantly lower abundances of total benthic species (in studies assessing sessile and mobile species together), sessile invertebrates and corals (in studies assessing these groups individually). In contrast, non-indigenous species were significantly more abundant on wood than metal. Concrete supported greater abundances of the general community, including habitat-forming species, compared to wood. Our results suggest that the ecological requirements of the biological community, alongside economic, logistic and engineering factors should be considered in material selection for multifunctional marine structures that deliver both engineering and ecological (enhanced abundance and diversity) benefits.

On the diversity and distribution of a data deficient habitat in a poorly mapped region: The case of Sabellaria alveolata L. in Ireland.

Data that can be used to monitor biodiversity through time are essential for conservation and management. The reef-forming worm, Sabellaria alveolata (L. 1767) is currently classed as 'Data Deficient' due to an imbalance in the spread of data on its distribution. Little is known about the distribution of this species around Ireland. Using data archaeology, we collated past and present distribution records and discovered that S. alveolata has a discontinuous distribution with large gaps between populations. Many regions lack data and should be targeted for sampling. Biodiversity surveys revealed that S. alveolata supported diverse epibiotic algal communities. Retrograding (declining) reefs supported greater infaunal diversity than prograding (growing) reefs or sand, suggesting that S. alveolata is a dynamic ecosystem engineer that has a lasting legacy effect. Similar research should be carried out for other Data Deficient species, habitats and regions. Such data are invaluable resources for management and conservation.

Seascape genomics reveals population isolation in the reef-building honeycomb worm, Sabellaria alveolata (L.).

BACKGROUND: Under the threat of climate change populations can disperse, acclimatise or evolve in order to avoid fitness loss. In light of this, it is important to understand neutral gene flow patterns as a measure of dispersal potential, but also adaptive genetic variation as a measure of evolutionary potential. In order to assess genetic variation and how this relates to environment in the honeycomb worm (Sabellaria alveolata (L.)), a reef-building polychaete that supports high biodiversity, we carried out RAD sequencing using individuals from along its complete latitudinal range. Patterns of neutral population genetic structure were compared to larval dispersal as predicted by ocean circulation modelling, and outlier analyses and genotype-environment association tests were used to attempt to identify loci under selection in relation to local temperature data. RESULTS: We genotyped 482 filtered SNPs, from 68 individuals across nine sites, 27 of which were identified as outliers using BAYESCAN and ARLEQUIN. All outlier loci were potentially under balancing selection, despite previous evidence of local adaptation in the system. Limited gene flow was observed among reef-sites (FST = 0.28 ± 0.10), in line with the low dispersal potential identified by the larval dispersal models. The North Atlantic reef emerged as a distinct population and this was linked to high local larval retention and the effect of the North Atlantic Current on dispersal. CONCLUSIONS: As an isolated population, with limited potential for natural genetic or demographic augmentation from other reefs, the North Atlantic site warrants conservation attention in order to preserve not only this species, but above all the crucial functional ecological roles that are associated with their bioconstructions. Our study highlights the utility of using seascape genomics to identify populations of conservation concern.

Removal of intertidal grazers by human harvesting leads to alteration of species interactions, community structure and resilience to climate change.

Extreme fluctuations in abiotic conditions can induce a biological stress response (e.g. bleaching) detrimental to an organism's health. In some instances, organisms can recover if conditions are alleviated, such as through co-occurrence with other species that confer protection. Biodiverse, multitrophic communities are increasingly recognised as important promoters of species persistence and resilience under environmental change. On intertidal shores, the role of grazers as top-down determinants of algal community structure is well recognised. Similarly, the harvesting of grazers for human consumption is increasingly prevalent with potential to greatly alter the community dynamics. Here, we assess how differences in harvesting pressure of grazers under three management regimes (no-take; managed access; open-access) alters the trophic interactions between grazers, and algal communities. Grazer density and body size frequencies were different among regimes leading to changes in the photosynthetic performance and recovery of crustose coralline algae (CCA) post-bleaching, as well as their presence altering the strength of interactions between species. The exclusion of grazers from patches using cages led to different emergent communities and reduced negative correlations between taxa. The absence of larger grazers (>9 cm) at the managed access site led to macroalgal overgrowth of bleached CCA negatively affecting its recovery, whereas no-take or open-access led to a moderated algal growth and a shift from competitive to facilitative interactions between algal species. Given that CCA play an important role in the population growth and development of other species, the choice of management measure should be carefully considered before implementation, depending on objectives.

Indications of future performance of native and non-native adult oysters under acidification and warming.

Globally, non-native species (NNS) have been introduced and now often entirely replace native species in captive aquaculture; in part, a result of a perceived greater resilience of NSS to climate change and disease. Here, the effects of ocean acidification and warming on metabolic rate, feeding rate, and somatic growth was assessed using two co-occurring species of oysters - the introduced Pacific oyster Magallana gigas (formerly Crassostrea gigas), and native flat oyster Ostrea edulis. Biological responses to increased temperature and pCO2 combinations were tested, the effects differing between species. Metabolic rates and energetic demands of both species were increased by warming but not by elevated pCO2. While acidification and warming did not affect the clearance rate of O. edulis, M. gigas displayed a 40% decrease at 750 ppm pCO2. Similarly, the condition index of O. edulis was unaffected, but that of M. gigas was negatively impacted by warming, likely due to increased energetic demands that were not compensated for by increased feeding. These findings suggest differing stress from anthropogenic CO2 emissions between species and contrary to expectations, this was higher in introduced M. gigas than in the native O. edulis. If these laboratory findings hold true for populations in the wild, then continued CO2 emissions can be expected to adversely affect the functioning and structure of M. gigas populations with significant ecological and economic repercussions, especially for aquaculture. Our findings strengthen arguments in favour of investment in O. edulis restoration in UK waters.

The effects of elevated CO2 on shell properties and susceptibility to predation in mussels Mytilus edulis.

For many species, ocean acidification (OA) is having negative physiological consequences on their fitness and resilience to environmental change, but less is known about the ecosystem effects of these changes. Here, we assess how OA conditions predicted for 2100 affects the biological functioning of an important habitat-forming species Mytilus edulis and its susceptibility to predation by a key predator, the gastropod Nucella lapillus. Change in three physiological parameters in Mytilus were assessed: (1) shell thickness and cross-sectional surface area, (2) body volume and (3) feeding rate, as well as susceptibility to predation by N. lapillus. Shell thickness and cross-section area, body volume and feeding rate of Mytilus all reduced under OA conditions indicating compromised fitness. Predation risk increased by ∼26% under OA, suggesting increased susceptibility of mussels to predation and/or altered predator foraging behaviour. Notably, predation of large Mytilus - that were largely free from predation under control conditions - increased by more than 8x under OA, suggesting that body size was no longer a refuge. Our results suggest OA will impact upon ecosystem structure and functioning and the continued provision of ecosystem services associated with Mytilus reefs and the communities associated with them.

Predicting free-space occupancy on novel artificial structures by an invasive intertidal barnacle using a removal experiment.

Artificial structures can create novel habitat in the marine environment that has been associated with the spread of invasive species. They are often located in areas of high disturbance and can vary significantly in the area of free space provided for settlement of marine organisms. Whilst correlation between the amount of free space available and recruitment success has been shown in populations of several marine benthic organisms, there has been relatively little focus on invasive species, a group with the potential to reproduce in vast numbers and colonise habitats rapidly. Invasion success following different scales of disturbance was examined in the invasive acorn barnacle, Austrominiusmodestus, on a unique art installation located in Liverpool Bay. Population growth and recruitment success were examined by comparing recruitment rates within disturbance clearings of 4 different sizes and by contrasting population development with early recruitment rates over a 10 week period. Disturbed areas were rapidly recolonised and monocultures of A. modestus formed within 6 weeks. The size of patch created during disturbance had no effect on the rate of recruitment, while a linear relationship between recruit density and patch size was observed. Density-dependent processes mediated initial high recruitment resulting in population stability after 8-10 weeks, but densities continued to greatly exceed those reported in natural habitats. Given that artificial structures are likely to continue to proliferate in light of climate change projections, free-space is likely to become more available more frequently in the future supporting the expansion of fast-colonising species.

Identifying common pressure pathways from a complex network of human activities to support ecosystem-based management.

The marine environment is heavily exploited, but unintentional consequences cause wide-ranging negative effects to its characteristics. Linkage frameworks (e.g., DPSIR [driver-pressure-state-impact-response]) are commonly used to describe an interaction between human activities and ecological characteristics of the ecosystem, but as each linkage is viewed independently, the diversity of pressures that affect those characteristics may not be identified or managed effectively. Here we demonstrate an approach for using linkages to build a simple network to capture the complex relationships arising from multiple sectors and their activities. Using data-analysis tools common to ecology, we show how linkages can be placed into mechanistically similar groups. Management measures can be combined into fewer and more simplified measures that target groups of pressures rather than individual pressures, which is likely to increase compliance and the success of the measure while reducing the cost of enforcement. Given that conservation objectives (regional priorities) can vary, we also demonstrate by way of a case study example from the Marine Strategy Framework Directive, how management priorities might change, and illustrate how the approach can be used to identify sectors for control that best support the conservation objectives.

Interactions between multiple recruitment drivers: post-settlement predation mortality and flow-mediated recruitment.

BACKGROUND: Dispersal is a primary driver in shaping the future distribution of species in both terrestrial and marine systems. Physical transport by advection can regulate the distance travelled and rate of propagule supply to a habitat but post-settlement processes such as predation can decouple supply from recruitment. The effect of flow-mediated recruitment and predation on the recruitment success of an intertidal species, the eastern oyster Crassostrea virginica was evaluated in two-replicated field experiments. Two key crab species were manipulated to test predator identity effects on oyster mortality. FINDINGS: Recruitment was ∼58% higher in high flow compared to low flow, but predation masked those differences. Predation mortality was primarily attributed to the blue crab Callinectes sapidus, whilst the mud crab Panopeus herbstii had no effect on recruit mortality. Recruit mortality from predation was high when recruit densities were high, but when recruit density was low, predation effects were not seen. Under high recruitment (supply), predation determined maximum population size and in low flow environments, recruitment success is likely determined by a combination of recruitment and resource limitation but not predation. CONCLUSIONS: Four processes are demonstrated: (1) Increases in flow rate positively affect recruitment success; (2) In high flow (recruitment) environments, resource availability is less important than predation; (3) predation is an important source of recruit mortality, but is dependent upon recruit density; and (4) recruitment and/or resource limitation is likely a major driver of population structure and functioning, modifying the interaction between predators and prey. Simultaneous testing of flow-mediated recruitment and predation was required to differentiate between the role of each process in determining population size. Our results reinforce the importance of propagule pressure, predation and post-settlement mortality as important determinants of population growth and persistence, but demonstrate that they should not be considered mutually exclusive.