A Pleistocene legacy structures variation in modern seagrass ecosystems.

Distribution of Earth's biomes is structured by the match between climate and plant traits, which in turn shape associated communities and ecosystem processes and services. However, that climate-trait match can be disrupted by historical events, with lasting ecosystem impacts. As Earth's environment changes faster than at any time in human history, critical questions are whether and how organismal traits and ecosystems can adjust to altered conditions. We quantified the relative importance of current environmental forcing versus evolutionary history in shaping the growth form (stature and biomass) and associated community of eelgrass (Zostera marina), a widespread foundation plant of marine ecosystems along Northern Hemisphere coastlines, which experienced major shifts in distribution and genetic composition during the Pleistocene. We found that eelgrass stature and biomass retain a legacy of the Pleistocene colonization of the Atlantic from the ancestral Pacific range and of more recent within-basin bottlenecks and genetic differentiation. This evolutionary legacy in turn influences the biomass of associated algae and invertebrates that fuel coastal food webs, with effects comparable to or stronger than effects of current environmental forcing. Such historical lags in phenotypic acclimatization may constrain ecosystem adjustments to rapid anthropogenic climate change, thus altering predictions about the future functioning of ecosystems.

Climate drives the geography of marine consumption by changing predator communities.

The global distribution of primary production and consumption by humans (fisheries) is well-documented, but we have no map linking the central ecological process of consumption within food webs to temperature and other ecological drivers. Using standardized assays that span 105° of latitude on four continents, we show that rates of bait consumption by generalist predators in shallow marine ecosystems are tightly linked to both temperature and the composition of consumer assemblages. Unexpectedly, rates of consumption peaked at midlatitudes (25 to 35°) in both Northern and Southern Hemispheres across both seagrass and unvegetated sediment habitats. This pattern contrasts with terrestrial systems, where biotic interactions reportedly weaken away from the equator, but it parallels an emerging pattern of a subtropical peak in marine biodiversity. The higher consumption at midlatitudes was closely related to the type of consumers present, which explained rates of consumption better than consumer density, biomass, species diversity, or habitat. Indeed, the apparent effect of temperature on consumption was mostly driven by temperature-associated turnover in consumer community composition. Our findings reinforce the key influence of climate warming on altered species composition and highlight its implications for the functioning of Earth's ecosystems.

The biogeography of community assembly: latitude and predation drive variation in community trait distribution in a guild of epifaunal crustaceans.

While considerable evidence exists of biogeographic patterns in the intensity of species interactions, the influence of these patterns on variation in community structure is less clear. Studying how the distributions of traits in communities vary along global gradients can inform how variation in interactions and other factors contribute to the process of community assembly. Using a model selection approach on measures of trait dispersion in crustaceans associated with eelgrass (Zostera marina) spanning 30° of latitude in two oceans, we found that dispersion strongly increased with increasing predation and decreasing latitude. Ocean and epiphyte load appeared as secondary predictors; Pacific communities were more overdispersed while Atlantic communities were more clustered, and increasing epiphytes were associated with increased clustering. By examining how species interactions and environmental filters influence community structure across biogeographic regions, we demonstrate how both latitudinal variation in species interactions and historical contingency shape these responses. Community trait distributions have implications for ecosystem stability and functioning, and integrating large-scale observations of environmental filters, species interactions and traits can help us predict how communities may respond to environmental change.

Latitude, temperature, and habitat complexity predict predation pressure in eelgrass beds across the Northern Hemisphere.

Latitudinal gradients in species interactions are widely cited as potential causes or consequences of global patterns of biodiversity. However, mechanistic studies documenting changes in interactions across broad geographic ranges are limited. We surveyed predation intensity on common prey (live amphipods and gastropods) in communities of eelgrass (Zostera marina) at 48 sites across its Northern Hemisphere range, encompassing over 37° of latitude and four continental coastlines. Predation on amphipods declined with latitude on all coasts but declined more strongly along western ocean margins where temperature gradients are steeper. Whereas in situ water temperature at the time of the experiments was uncorrelated with predation, mean annual temperature strongly positively predicted predation, suggesting a more complex mechanism than simply increased metabolic activity at the time of predation. This large-scale biogeographic pattern was modified by local habitat characteristics; predation declined with higher shoot density both among and within sites. Predation rates on gastropods, by contrast, were uniformly low and varied little among sites. The high replication and geographic extent of our study not only provides additional evidence to support biogeographic variation in predation intensity, but also insight into the mechanisms that relate temperature and biogeographic gradients in species interactions.

Combined effects of warming and nutrients on marine communities are moderated by predators and vary across functional groups.

Warming, nutrient enrichment and biodiversity modification are among the most pervasive components of human-induced global environmental change. We know little about their cumulative effects on ecosystems; however, even though this knowledge is fundamental to predicting and managing their consequences in a changing world. Here, we show that shifts in predator species composition can moderate both the individual and combined effects of warming and nutrient enrichment in marine systems. However, all three aspects of global change also acted independently to alter different functional groups in our flow-through marine rock-pool mesocosms. Specifically, warming reduced macroalgal biomass and assemblage productivity, whereas enrichment led to increased abundance of meso-invertebrate consumers, and loss of predator species led to increased gastropod grazer biomass. This disparity in responses, both across trophic levels (macroalgae and intermediate consumers), and between detecting additive effects on aggregate measures of ecosystem functioning, yet interactive effects on community composition, illustrates that our forecasting ability depends strongly on the level of ecological complexity incorporated within global change experiments. We conclude that biodiversity change-and loss of predator species in particular-plays a critical and overarching role in determining how ecological communities respond to stressors.

Loss of predator species, not intermediate consumers, triggers rapid and dramatic extinction cascades.

Ecological networks are tightly interconnected, such that loss of a single species can trigger additional species extinctions. Theory predicts that such secondary extinctions are driven primarily by loss of species from intermediate or basal trophic levels. In contrast, most cases of secondary extinctions from natural systems have been attributed to loss of entire top trophic levels. Here, we show that loss of single predator species in isolation can, irrespective of their identity or the presence of other predators, trigger rapid secondary extinction cascades in natural communities far exceeding those generally predicted by theory. In contrast, we did not find any secondary extinctions caused by intermediate consumer loss. A food web model of our experimental system-a marine rocky shore community-could reproduce these results only when biologically likely and plausible nontrophic interactions, based on competition for space and predator-avoidance behaviour, were included. These findings call for a reassessment of the scale and nature of extinction cascades, particularly the inclusion of nontrophic interactions, in forecasts of the future of biodiversity.

Microplastics Affect the Ecological Functioning of an Important Biogenic Habitat.

Biological effects of microplastics on the health of bivalves have been demonstrated elsewhere, but ecological impacts on the biodiversity and ecosystem functioning of bivalve-dominated habitats are unknown. Thus, we exposed intact sediment cores containing European flat oysters (Ostrea edulis) or blue mussels (Mytilus edulis) in seawater to two different densities (2.5 or 25 µg L-1) of biodegradable or conventional microplastics in outdoor mesocosms. We hypothesized that filtration rates of the bivalves, inorganic nitrogen cycling, primary productivity of sediment dwelling microphytobenthos, and the structure of invertebrate benthic assemblages would be influenced by microplastics. After 50 days, filtration by M. edulis was significantly less when exposed to 25 µg L-1 of either type of microplastics, but there were no effects on ecosystem functioning or the associated invertebrate assemblages. Contrastingly, filtration by O. edulis significantly increased when exposed to 2.5 or 25 µg L-1 of microplastics, and porewater ammonium and biomass of benthic cyanobacteria decreased. Additionally the associated infaunal invertebrate assemblages differed, with significantly less polychaetes and more oligochaetes in treatments exposed to microplastics. These findings highlight the potential of microplastics to impact the functioning and structure of sedimentary habitats and show that such effects may depend on the dominant bivalve present.

Navigating the complexity of ecological stability.

Human actions challenge nature in many ways. Ecological responses are ineluctably complex, demanding measures that describe them succinctly. Collectively, these measures encapsulate the overall 'stability' of the system. Many international bodies, including the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services, broadly aspire to maintain or enhance ecological stability. Such bodies frequently use terms pertaining to stability that lack clear definition. Consequently, we cannot measure them and so they disconnect from a large body of theoretical and empirical understanding. We assess the scientific and policy literature and show that this disconnect is one consequence of an inconsistent and one-dimensional approach that ecologists have taken to both disturbances and stability. This has led to confused communication of the nature of stability and the level of our insight into it. Disturbances and stability are multidimensional. Our understanding of them is not. We have a remarkably poor understanding of the impacts on stability of the characteristics that define many, perhaps all, of the most important elements of global change. We provide recommendations for theoreticians, empiricists and policymakers on how to better integrate the multidimensional nature of ecological stability into their research, policies and actions.

Wave action modifies the effects of consumer diversity and warming on algal assemblages.

To understand the consequences of biodiversity loss, it is necessary to test how biodiversity-ecosystem functioning relationships may vary with predicted environmental change. In particular, our understanding will be advanced by studies addressing the interactive effects of multiple stressors on the role of biodiversity across trophic levels. Predicted increases in wave disturbance and ocean warming, together with climate-driven range shifts of key consumer species, are likely to have profound impacts on the dynamics of coastal marine communities. We tested whether wave action and temperature modified the effects of gastropod grazer diversity (Patella vulgata, Littorina littorea, and Gibbula umbilicalis) on algal assemblages in experimental rock pools. The presence or absence of L. littorea appeared to drive changes in microalgal and macroalgal biomass and macroalgal assemblage structure. Macroalgal biomass also decreased with increasing grazer species richness, but only when wave action was enhanced. Further, independently of grazer diversity, wave action and temperature had interactive effects on macroalgal assemblage structure. Warming also led to a reversal of grazer-macroalgal interaction strengths from negative to positive, but only when there was no wave action. Our results show that hydrodynamic disturbance can exacerbate the effects of changing consumer diversity, and may also disrupt the influence of other environmental stressors on key consumer-resource interactions. These findings suggest that the combined effects of anticipated abiotic and biotic change on the functioning of coastal marine ecosystems, although difficult to predict, may be substantial.

Key benthic species are affected by predicted warming in winter but show resistance to ocean acidification.

The effects of climate change on coastal biodiversity are a major concern because altered community compositions may change associated rates of ecosystem functioning and services. Whilst responses of single species or taxa have been studied extensively, it remains challenging to estimate responses to climate change across different levels of biological organisation. Studies that consider the effects of moderate realistic near-future levels of ocean warming and acidification are needed to identify and quantify the gradual responses of species to change. Also, studies including different levels of biological complexity may reveal opportunities for amelioration or facilitation under changing environmental conditions. To test experimentally for independent and combined effects of predicted near-future warming and acidification on key benthic species, we manipulated three levels of temperature (winter ambient, +0.8 and +2°C) and two levels of pco 2 (ambient at 450 ppm and elevated at 645 ppm) and quantified their effects on mussels and algae growing separately and together (to also test for inter-specific interactions). Warming increased mussel clearance and mortality rates simultaneously, which meant that total biomass peaked at +0.8°C. Surprisingly, however, no effects of elevated pco 2 were identified on mussels or algae. Moreover, when kept together, mussels and algae had mutually positive effects on each other's performance (i.e. mussel survival and condition index, mussel and algal biomass and proxies for algal productivity including relative maximum electron transport rate [rETRmax], saturating light intensity [I k] and maximum quantum yield [F v/F m]), independent of warming and acidification. Our results show that even moderate warming affected the functioning of key benthic species, and we identified a level of resistance to predicted ocean acidification. Importantly, we show that the presence of a second functional group enhanced the functioning of both groups (mussels and algae), independent of changing environmental conditions, which highlights the ecological and potential economic benefits of conserving biodiversity in marine ecosystems.

On the dimensionality of ecological stability.

Ecological stability is touted as a complex and multifaceted concept, including components such as variability, resistance, resilience, persistence and robustness. Even though a complete appreciation of the effects of perturbations on ecosystems requires the simultaneous measurement of these multiple components of stability, most ecological research has focused on one or a few of those components analysed in isolation. Here, we present a new view of ecological stability that recognises explicitly the non-independence of components of stability. This provides an approach for simplifying the concept of stability. We illustrate the concept and approach using results from a field experiment, and show that the effective dimensionality of ecological stability is considerably lower than if the various components of stability were unrelated. However, strong perturbations can modify, and even decouple, relationships among individual components of stability. Thus, perturbations not only increase the dimensionality of stability but they can also alter the relationships among components of stability in different ways. Studies that focus on single forms of stability in isolation therefore risk underestimating significantly the potential of perturbations to destabilise ecosystems. In contrast, application of the multidimensional stability framework that we propose gives a far richer understanding of how communities respond to perturbations.

Distinguishing between direct and indirect effects of predators in complex ecosystems.

1. Global declines in biodiversity have stimulated much research into the consequences of species loss for ecosystems and the goods and services they provide. Species at higher trophic levels are at greater risk of human-induced extinction yet remarkably little is known about the effects of consumer species loss across multiple trophic levels in natural complex ecosystems. Previous studies have been criticized for lacking experimental realism and appropriate temporal scale, running for short periods that are not sufficient to detect many of the mechanisms operating in the field. 2. We manipulated the presence of two predator species and two groups of their prey (primary consumers) and measured their independent and interactive effects on primary producers in a natural marine benthic system. The presence of predators and their prey was manipulated in the field for 14 months to distinguish clearly the direct and indirect effects of predators on primary producers and to identify mechanisms driving responses. 3. We found that the loss of either predator species had indirect negative effects on species diversity and total cover of primary producers. These cascading effects of predator species loss were mediated by the presence of intermediate consumers. Moreover, the presence of different intermediate consumers, irrespective of the presence or absence of their predators, determined primary producer assemblage structure. We identified direct negative effects of predators on their prey and several indirect effects of predators on primary producers but not all interactions could have been predicted based on trophic level. 4. Our findings demonstrate the importance of trophic cascade effects coupled with non-trophic interactions when predicting the effects of loss of predator species on primary producers and consequently for ecosystem functioning. There is a pressing need for improved understanding of the effects of loss of consumers, based on realistic scenarios of diversity loss, to test conceptual frameworks linking predator diversity to variation in ecosystem functioning and for the protection of biodiversity, ecosystem functioning and related services.

What does the future look like for kelp when facing multiple stressors?

As primary producers and ecosystem engineers, kelp (generally Order Laminariales) are ecologically important, and their decline could have far-reaching consequences. Kelp are valuable in forming habitats for fish and invertebrates and are crucial for adaptation to climate change by creating coastal defenses and in providing key functions, such as carbon sequestration and food provision. Kelp are threatened by multiple stressors, such as climate change, over-harvesting of predators, and pollution. In this opinion paper, we discuss how these stressors may interact to affect kelp, and how this varies under different contexts. We argue that more research that bridges kelp conservation and multiple stressor theory is needed and outline key questions that should be addressed as a priority. For instance, it is important to understand how previous exposure (either to earlier generations or life stages) determines responses to emerging stressors, and how responses in kelp scale up to alter food webs and ecosystem functioning. By increasing the temporal and biological complexity of kelp research in this way, we will improve our understanding allowing better predictions. This research is essential for the effective conservation and potential restoration of kelp in our rapidly changing world.

Seasonal and spatial variability in rates of primary production and detritus release by intertidal stands of Laminaria digitata and Saccharina latissima on wave-exposed shores in the northeast Atlantic.

Coastal habitats are increasingly recognized as fundamentally important components of global carbon cycles, but the rates of carbon flow associated with marine macrophytes are not well resolved for many species in many regions. We quantified density, rates of primary productivity, and detritus production of intertidal stands of two common intertidal kelp species-Laminaria digitata (oarweed) and Saccharina latissima (sugar kelp)-on four NE Atlantic rocky shores over 22 months. The density of L. digitata was greater at exposed compared to moderately exposed shores but remained consistently low for S. latissima throughout the survey period. Individual productivity and erosion rates of L. digitata did not differ between exposed and moderately exposed shores but differed across exposure levels throughout the year at moderately exposed sites only. Productivity and erosion of S. latissima remained low on moderately exposed shores and showed no clear seasonal pattern. Patterns of productivity and total detrital production (erosion and dislodgement) per m2 of both L. digitata and S. latissima followed closely that of densities per m2, peaking in May during both survey years. Temperature and light were key factors affecting the productivity rates of L. digitata and S. latissima. Erosion rates of L. digitata were affected by wave exposure, temperature, light, grazing, and epiphyte cover, but only temperature-affected erosion of S. latissima. Production of biomass and detritus was greater in L. digitata than in S. latissima and exceeded previous estimates for subtidal and warmer-water affinity kelp populations (e.g., Laminaria ochroleuca). These biogenic habitats are clearly important contributors to the coastal carbon cycle that have been overlooked previously and should be included in future ecosystem models. Further work is required to determine the areal extent of kelp stands in intertidal and shallow subtidal habitats, which is needed to scale up local production estimates to entire coastlines.

Joint effects of patch edges and habitat degradation on faunal predation risk in a widespread marine foundation species.

Human activities degrade and fragment coastal marine habitats, reducing their structural complexity and making habitat edges a prevalent seascape feature. Though habitat edges frequently are implicated in reduced faunal survival and biodiversity, results of experiments on edge effects have been inconsistent, calling for a mechanistic approach to the study of edges that explicitly includes indirect and interactive effects of habitat alteration at multiple scales across biogeographic gradients. We used an experimental network spanning 17 eelgrass (Zostera marina) sites across the Atlantic and Pacific oceans and the Mediterranean Sea to determine (1) if eelgrass edges consistently increase faunal predation risk, (2) whether edge effects on predation risk are altered by habitat degradation (shoot thinning), and (3) whether variation in the strength of edge effects among sites can be explained by biogeographical variability in covarying eelgrass habitat features. Contrary to expectations, at most sites, predation risk for tethered crustaceans (crabs or shrimps) was lower along patch edges than in patch interiors, regardless of the extent of habitat degradation. However, the extent to which edges reduced predation risk, compared to the patch interior, was correlated with the extent to which edges supported higher eelgrass structural complexity and prey biomass compared to patch interiors. This suggests an indirect component to edge effects in which the impact of edge proximity on predation risk is mediated by the effect of edges on other key biotic factors. Our results suggest that studies on edge effects should consider structural characteristics of patch edges, which may vary geographically, and multiple ways that humans degrade habitats.

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.

Individual species provide multifaceted contributions to the stability of ecosystems.

Exploration of the relationship between species diversity and ecological stability has occupied a prominent place in ecological research for decades. Yet, a key component of this puzzle-the contributions of individual species to the overall stability of ecosystems-remains largely unknown. Here, we show that individual species simultaneously stabilize and destabilize ecosystems along different dimensions of stability, and also that their contributions to functional (biomass) and compositional stability are largely independent. By simulating experimentally the extinction of three consumer species (the limpet Patella, the periwinkle Littorina and the topshell Gibbula) from a coastal rocky shore, we found that the capacity to predict the combined contribution of species to stability from the sum of their individual contributions varied among stability dimensions. This implies that the nature of the diversity-stability relationship depends upon the dimension of stability under consideration, and may be additive, synergistic or antagonistic. We conclude that, although the profoundly multifaceted and context-dependent consequences of species loss pose a significant challenge, the predictability of cumulative species contributions to some dimensions of stability provide a way forward for ecologists trying to conserve ecosystems and manage their stability under global change.

Simulated predator extinctions: predator identity affects survival and recruitment of oysters.

The rate of species loss is increasing at a global scale, and human-induced extinctions are biased toward predator species. We examined the effects of predator extinctions on a foundation species, the eastern oyster (Crassostrea virginica). We performed a factorial experiment manipulating the presence and abundance of three of the most common predatory crabs, the blue crab (Callinectes sapidus), stone crab (Menippe mercenaria), and mud crab (Panopeus herbstii) in estuaries in the eastern United States. We tested the effects of species richness and identity of predators on juvenile oyster survival, oyster recruitment, and organic matter content of sediment. We also manipulated the density of each of the predators and controlled for the loss of biomass of species by maintaining a constant mass of predators in one set of treatments and simultaneously using an additive design. This design allowed us to test the density dependence of our results and test for functional compensation by other species. The identity of predator species, but not richness, affected oyster populations. The loss of blue crabs, alone or in combination with either of the other species, affected the survival rate of juvenile oysters. Blue crabs and stone crabs both affected oyster recruitment and sediment organic matter negatively. Mud crabs at higher than ambient densities, however, could fulfill some of the functions of blue and stone crabs, suggesting a level of ecological redundancy. Importantly, the strong effects of blue crabs in all processes measured no longer occurred when individuals were present at higher-than-ambient densities. Their role as dominant predator is, therefore, dependent on their density within the system and the density of other species within their guild (e.g., mud crabs). Our findings support the hypothesis that the effects of species loss at higher trophic levels are determined by predator identity and are subject to complex intraguild interactions that are largely density dependent. Understanding the role of biodiversity in ecosystem functioning or addressing practical concerns, such as loss of predators owing to overharvesting, remains complicated because accurate predictions require detailed knowledge of the system and should be drawn from sound experimental evidence, not based on observations or generalized models.

Habitat with small inter-structural spaces promotes mussel survival and reef generation.

Spatially complex habitats provide refuge for prey and mediate many predator-prey interactions. Increasing anthropogenic pressures are eroding such habitats, reducing their complexity and potentially altering ecosystem stability on a global scale. Yet, we have only a rudimentary understanding of how structurally complex habitats create ecological refuges for most ecosystems. Better informed management decisions require an understanding of the mechanisms underpinning the provision of physical refuge and this may be linked to prey size, predator size and predator identity in priority habitats. We tested each of these factors empirically in a model biogenic reef system. Specifically, we tested whether mortality rates of blue mussels (Mytilus edulis) of different sizes differed among: (i) different forms of reef structural distribution (represented as 'clumped', 'patchy' and 'sparse'); (ii) predator species identity (shore crab, Carcinus maenas and starfish, Asterias rubens); and (iii) predator size. The survival rate of small mussels was greatest in the clumped experimental habitat and larger predators generally consumed more prey regardless of the structural organisation of treatment. Small mussels were protected from larger A. rubens but not from larger C. maenas in the clumped habitats. The distribution pattern of structural objects, therefore, may be considered a useful proxy for reef complexity when assessing predator-prey interactions, and optimal organisations should be considered based on both prey and predator sizes. These findings are essential to understand ecological processes underpinning predation rates in structurally complex habitats and to inform future restoration and ecological engineering practices.

Hierarchical structuring of genetic variation at differing geographic scales in the cultivated sugar kelp Saccharina latissima.

The cultivation of macroalgae for biofuels, food and fertilisers has increased dramatically in recent years. The demand for such algal-derived products means that large scale cultivation in coastal waters will become necessary to provide sufficient algal biomass. As part of the process of establishing new macroalgal farms, the potential for gene flow between cultivated specimens and natural populations needs to be taken into consideration. Consequently, in the present study we have used a combined population genetic and hydrodynamic modelling approach to determine potential levels and patterns of gene flow in the kelp Saccharina latissima. Microsatellite analysis of 14 populations sampled across the northern part of the Irish Sea indicated four distinct genetic clusters. These were consistent with dispersal patterns indicated by the particle tracking model and show a combination of isolation by distance and genetic structuring due to local hydrodynamic conditions. At smaller scales (less than a few 10s of km), gene flow appears to be fairly extensive, with evidence of local population connectivity due to local currents. At larger scales, however, factors such as freshwater efflux and open water would appear to represent barriers to gene flow. Together, these patterns suggest that factors other than simple geographical distance and proximity need to be taken into account when planning the siting of kelp farms with the aim of minimizing gene flow to and from natural populations.