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.

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.

Consumers mediate the effects of experimental ocean acidification and warming on primary producers.

It is well known that ocean acidification can have profound impacts on marine organisms. However, we know little about the direct and indirect effects of ocean acidification and also how these effects interact with other features of environmental change such as warming and declining consumer pressure. In this study, we tested whether the presence of consumers (invertebrate mesograzers) influenced the interactive effects of ocean acidification and warming on benthic microalgae in a seagrass community mesocosm experiment. Net effects of acidification and warming on benthic microalgal biomass and production, as assessed by analysis of variance, were relatively weak regardless of grazer presence. However, partitioning these net effects into direct and indirect effects using structural equation modeling revealed several strong relationships. In the absence of grazers, benthic microalgae were negatively and indirectly affected by sediment-associated microalgal grazers and macroalgal shading, but directly and positively affected by acidification and warming. Combining indirect and direct effects yielded no or weak net effects. In the presence of grazers, almost all direct and indirect climate effects were nonsignificant. Our analyses highlight that (i) indirect effects of climate change may be at least as strong as direct effects, (ii) grazers are crucial in mediating these effects, and (iii) effects of ocean acidification may be apparent only through indirect effects and in combination with other variables (e.g., warming). These findings highlight the importance of experimental designs and statistical analyses that allow us to separate and quantify the direct and indirect effects of multiple climate variables on natural communities.

Biodiversity mediates top-down control in eelgrass ecosystems: a global comparative-experimental approach.

Nutrient pollution and reduced grazing each can stimulate algal blooms as shown by numerous experiments. But because experiments rarely incorporate natural variation in environmental factors and biodiversity, conditions determining the relative strength of bottom-up and top-down forcing remain unresolved. We factorially added nutrients and reduced grazing at 15 sites across the range of the marine foundation species eelgrass (Zostera marina) to quantify how top-down and bottom-up control interact with natural gradients in biodiversity and environmental forcing. Experiments confirmed modest top-down control of algae, whereas fertilisation had no general effect. Unexpectedly, grazer and algal biomass were better predicted by cross-site variation in grazer and eelgrass diversity than by global environmental gradients. Moreover, these large-scale patterns corresponded strikingly with prior small-scale experiments. Our results link global and local evidence that biodiversity and top-down control strongly influence functioning of threatened seagrass ecosystems, and suggest that biodiversity is comparably important to global change stressors.

Predation and spatial connectivity interact to shape ecosystem resilience to an ongoing regime shift.

Ecosystem regime shifts can have severe ecological and economic consequences, making it a top priority to understand how to make systems more resilient. Theory predicts that spatial connectivity and the local environment interact to shape resilience, but empirical studies are scarce. Here, we use >7000 fish samplings from the Baltic Sea coast to test this prediction in an ongoing, spatially propagating shift in dominance from predatory fish to an opportunistic mesopredator, with cascading effects throughout the food web. After controlling for the influence of other drivers (including increasing mesopredator densities), we find that predatory fish habitat connectivity increases resilience to the shift, but only when densities of fish-eating top predators (seals, cormorants) are low. Resilience also increases with temperature, likely through boosted predatory fish growth and recruitment. These findings confirm theoretical predictions that spatial connectivity and the local environment can together shape resilience to regime shifts.

Cross-habitat interactions among bivalve species control community structure on intertidal flats.

Increasing evidence shows that spatial interactions between sedentary organisms can structure communities and promote landscape complexity in many ecosystems. Here we tested the hypothesis that reef-forming mussels (Mytilus edulis L.), a dominant intertidal ecosystem engineer in the Wadden Sea, promote abundances of the burrowing bivalve Cerastoderma edule L. (cockle) in neighboring habitats at relatively long distances coastward from mussel beds. Field surveys within and around three mussel beds showed a peak in cockle densities at 50-100 m toward the coast from the mussel bed, while cockle abundances elsewhere in the study area were very low. Field transplantation of cockles showed higher survival of young cockles (2-3 years old) and increased spat fall coastward of the mussel bed compared to within the bed and to areas without mussels, whereas growth decreased within and coastward of the mussel bed. Our measurements suggest that the observed spatial patterns in cockle numbers resulted from (1) inhibition effects by the mussels close to the beds due to preemptive algal depletion and deteriorated sediment conditions and (2) facilitation effects by the mussels farther away from the beds due to reduction of wave energy. Our results imply that these spatial, scale-dependent interactions between reef-forming ecosystem engineers and surrounding communities of sedentary benthic organisms can be an important determinant of the large-scale community structure in intertidal ecosystems. Understanding this interplay between neighboring communities of sedentary species is therefore essential for effective conservation and restoration of soft-bottom intertidal communities.

A trait-based framework for seagrass ecology: Trends and prospects.

In the last three decades, quantitative approaches that rely on organism traits instead of taxonomy have advanced different fields of ecological research through establishing the mechanistic links between environmental drivers, functional traits, and ecosystem functions. A research subfield where trait-based approaches have been frequently used but poorly synthesized is the ecology of seagrasses; marine angiosperms that colonized the ocean 100M YA and today make up productive yet threatened coastal ecosystems globally. Here, we compiled a comprehensive trait-based response-effect framework (TBF) which builds on previous concepts and ideas, including the use of traits for the study of community assembly processes, from dispersal and response to abiotic and biotic factors, to ecosystem function and service provision. We then apply this framework to the global seagrass literature, using a systematic review to identify the strengths, gaps, and opportunities of the field. Seagrass trait research has mostly focused on the effect of environmental drivers on traits, i.e., "environmental filtering" (72%), whereas links between traits and functions are less common (26.9%). Despite the richness of trait-based data available, concepts related to TBFs are rare in the seagrass literature (15% of studies), including the relative importance of neutral and niche assembly processes, or the influence of trait dominance or complementarity in ecosystem function provision. These knowledge gaps indicate ample potential for further research, highlighting the need to understand the links between the unique traits of seagrasses and the ecosystem services they provide.

Experimental climate change weakens the insurance effect of biodiversity.

Ecosystems are simultaneously affected by biodiversity loss and climate change, but we know little about how these factors interact. We predicted that climate warming and CO (2) -enrichment should strengthen trophic cascades by reducing the relative efficiency of predation-resistant herbivores, if herbivore consumption rate trades off with predation resistance. This weakens the insurance effect of herbivore diversity. We tested this prediction using experimental ocean warming and acidification in seagrass mesocosms. Meta-analyses of published experiments first indicated that consumption rate trades off with predation resistance. The experiment then showed that three common herbivores together controlled macroalgae and facilitated seagrass dominance, regardless of climate change. When the predation-vulnerable herbivore was excluded in normal conditions, the two resistant herbivores maintained top-down control. Under warming, however, increased algal growth outstripped control by herbivores and the system became algal-dominated. Consequently, climate change can reduce the relative efficiency of resistant herbivores and weaken the insurance effect of biodiversity.

Effects of altered offshore food webs on coastal ecosystems emphasize the need for cross-ecosystem management.

By mainly targeting larger predatory fish, commercial fisheries have indirectly promoted rapid increases in densities of their prey; smaller predatory fish like sprat, stickleback and gobies. This process, known as mesopredator release, has effectively transformed many marine offshore basins into mesopredator-dominated ecosystems. In this article, we discuss recent indications of trophic cascades on the Atlantic and Baltic coasts of Sweden, where increased abundances of mesopredatory fish are linked to increased nearshore production and biomass of ephemeral algae. Based on synthesis of monitoring data, we suggest that offshore exploitation of larger predatory fish has contributed to the increase in mesopredator fish also along the coasts, with indirect negative effects on important benthic habitats and coastal water quality. The results emphasize the need to rebuild offshore and coastal populations of larger predatory fish to levels where they regain their control over lower trophic levels and important links between offshore and coastal systems are restored.

Facultative mutualisms: A double-edged sword for foundation species in the face of anthropogenic global change.

Ecosystems worldwide depend on habitat-forming foundation species that often facilitate themselves with increasing density and patch size, while also engaging in facultative mutualisms. Anthropogenic global change (e.g., climate change, eutrophication, overharvest, land-use change), however, is causing rapid declines of foundation species-structured ecosystems, often typified by sudden collapse. Although disruption of obligate mutualisms involving foundation species is known to precipitate collapse (e.g., coral bleaching), how facultative mutualisms (i.e., context-dependent, nonbinding reciprocal interactions) affect ecosystem resilience is uncertain. Here, we synthesize recent advancements and combine these with model analyses supported by real-world examples, to propose that facultative mutualisms may pose a double-edged sword for foundation species. We suggest that by amplifying self-facilitative feedbacks by foundation species, facultative mutualisms can increase foundation species' resistance to stress from anthropogenic impact. Simultaneously, however, mutualism dependency can generate or exacerbate bistability, implying a potential for sudden collapse when the mutualism's buffering capacity is exceeded, while recovery requires conditions to improve beyond the initial collapse point (hysteresis). Thus, our work emphasizes the importance of acknowledging facultative mutualisms for conservation and restoration of foundation species-structured ecosystems, but highlights the potential risk of relying on mutualisms in the face of global change. We argue that significant caveats remain regarding the determination of these feedbacks, and suggest empirical manipulation across stress gradients as a way forward to identify related nonlinear responses.

Effects of Recreational Boating on Microbial and Meiofauna Diversity in Coastal Shallow Ecosystems of the Baltic Sea.

Recreational boating can impact benthic ecosystems in coastal waters. Reduced height and cover of aquatic vegetation in shallow Baltic Sea inlets with high boat traffic have raised concerns about cascading effects on benthic communities in these ecosystems. Here, we characterized the diversity and composition of sediment-associated microbial and meiofaunal communities across five bays subjected to low and high degrees of boating activity and examined the community-environment relationships and association with bay morphometry. We found that recreational boating activity altered meiofauna alpha diversity and the composition of both micro- and meiobenthic communities, and there were strong correlations between community structure and morphometric variables like topographic openness, wave exposure, water surface area, and total phosphorous concentrations. Inlets with high boat traffic showed an increase of bacterial taxa like Hydrogenophilaceae and Burkholderiaceae. Several meiofauna taxa previously reported to respond positively to high levels of suspended organic matter were found in higher relative abundances in the bays with high boat traffic. Overall, our results show that morphometric characteristics of inlets are the strongest drivers of benthic diversity in shallow coastal environments. However, while the effects were small, we found significant effects of recreational boating on benthic community structure that should be considered when evaluating the new mooring projects. IMPORTANCE With the increase of recreational boating activity and development of boating infrastructure in shallow, wave-protected areas, there is growing concern for their impact on coastal ecosystems. In order to properly assess the effects and consider the potential for recovery, it is important to investigate microbial and meiofaunal communities that underpin the functioning of these ecosystems. Here, we present the first study that uses DNA metabarcoding to assess how benthic biodiversity in shallow coastal areas is impacted by recreational boating. Our study shows a relatively small, but significant, effect of recreational boating both on meiofauna alpha diversity and meiofauna and bacterial community composition. However, both meiofauna and bacterial community composition in shallow benthic habitats is mediated to a higher degree by abiotic variables, such as topographic openness, area or size of the inlets, and wave exposure. Despite the fact that the effects were small, such impacts on benthic biodiversity should be considered in the management of coastal shallow habitats.

Predator biomass and vegetation influence the coastal distribution of threespine stickleback morphotypes.

Intraspecific niche differentiation can contribute to population persistence in changing environments. Following declines in large predatory fish, eutrophication, and climate change, there has been a major increase in the abundance of threespine stickleback (Gasterosteus aculeatus) in the Baltic Sea. Two morphotype groups with different levels of body armor-completely plated and incompletely plated-are common in coastal Baltic Sea habitats. The morphotypes are similar in shape, size, and other morphological characteristics and live as one apparently intermixed population. Variation in resource use between the groups could indicate a degree of niche segregation that could aid population persistence in the face of further environmental change. To assess whether morphotypes exhibit niche segregation associated with resource and/or habitat exploitation and predator avoidance, we conducted a field survey of stickleback morphotypes, and biotic and abiotic ecosystem structure, in two habitat types within shallow coastal bays in the Baltic Sea: deeper central waters and shallow near-shore waters. In the deeper waters, the proportion of completely plated stickleback was greater in habitats with greater biomass of two piscivorous fish: perch (Perca fluviatilis) and pike (Esox lucius). In the shallow waters, the proportion of completely plated stickleback was greater in habitats with greater coverage of habitat-forming vegetation. Our results suggest niche segregation between morphotypes, which may contribute to the continued success of stickleback in coastal Baltic Sea habitats.

Dramatic decline of northern bat Eptesicus nilssonii in Sweden over 30 years.

We monitored northern bat Eptesicus nilssonii (Keyserling & Blasius, 1839) acoustically along a 27 km road transect at weekly intervals in 1988, 1989 and 1990, and again in 2016 and 2017. The methodology of data collection and the transect were the same throughout, except that the insect-attracting mercury-vapour street-lights along parts of the road were replaced by sodium lights between the two survey periods. Counts along sections of the transect with and without street-lights were analysed separately. The frequency of bat encounters in unlit sections showed an average decline of 3.0% per year, corresponding to a reduction of 59% between 1988 and 2017. Sections with street-lights showed an 85% decline over the same period (6.3% per year). The decline represents a real reduction in the abundance of bats rather than an artefact of changed distribution of bats away from roads. Our study conforms with another long-term survey of the same species on the Baltic island of Gotland. Our results agree with predictions based on climate change models. They also indicate that the decline was caused directly by the disuse of the insect-attracting mercury-vapour street-lights, which may have resulted in lower availability of preferred prey (moths). In the 1980s, E. nilssonii was considered the most common bat in Sweden, but the subsequent decline would rather qualify it for vulnerable or endangered status in the national Red List of Threatened Species.

A spatial regime shift from predator to prey dominance in a large coastal ecosystem.

Regime shifts in ecosystem structure and processes are typically studied from a temporal perspective. Yet, theory predicts that in large ecosystems with environmental gradients, shifts should start locally and gradually spread through space. Here we empirically document a spatially propagating shift in the trophic structure of a large aquatic ecosystem, from dominance of large predatory fish (perch, pike) to the small prey fish, the three-spined stickleback. Fish surveys in 486 shallow bays along the 1200 km western Baltic Sea coast during 1979-2017 show that the shift started in wave-exposed archipelago areas near the open sea, but gradually spread towards the wave-sheltered mainland coast. Ecosystem surveys in 32 bays in 2014 show that stickleback predation on juvenile predators (predator-prey reversal) generates a feedback mechanism that appears to reinforce the shift. In summary, managers must account for spatial heterogeneity and dispersal to better predict, detect and confront regime shifts within large ecosystems.

Recreational boating degrades vegetation important for fish recruitment.

Recreational boating increases globally and associated moorings are often placed in vegetated habitats important for fish recruitment. Meanwhile, assessments of the effects of boating on vegetation, and potential effects on associated fish assemblages are rare. Here, we analysed (i) the effect of small-boat marinas on vegetation structure, and (ii) juvenile fish abundance in relation to vegetation cover in shallow wave-sheltered coastal inlets. We found marinas to have lower vegetation cover and height, and a different species composition, compared to control inlets. This effect became stronger with increasing berth density. Moreover, there was a clear positive relationship between vegetation cover and fish abundance. We conclude that recreational boating and related moorings are associated with reduced cover of aquatic vegetation constituting important habitats for juvenile fish. We therefore recommend that coastal constructions and associated boating should be allocated to more disturbance tolerant environments (e.g. naturally wave-exposed shores), thereby minimizing negative environmental impacts.

Global challenges for seagrass conservation.

Seagrasses, flowering marine plants that form underwater meadows, play a significant global role in supporting food security, mitigating climate change and supporting biodiversity. Although progress is being made to conserve seagrass meadows in select areas, most meadows remain under significant pressure resulting in a decline in meadow condition and loss of function. Effective management strategies need to be implemented to reverse seagrass loss and enhance their fundamental role in coastal ocean habitats. Here we propose that seagrass meadows globally face a series of significant common challenges that must be addressed from a multifaceted and interdisciplinary perspective in order to achieve global conservation of seagrass meadows. The six main global challenges to seagrass conservation are (1) a lack of awareness of what seagrasses are and a limited societal recognition of the importance of seagrasses in coastal systems; (2) the status of many seagrass meadows are unknown, and up-to-date information on status and condition is essential; (3) understanding threatening activities at local scales is required to target management actions accordingly; (4) expanding our understanding of interactions between the socio-economic and ecological elements of seagrass systems is essential to balance the needs of people and the planet; (5) seagrass research should be expanded to generate scientific inquiries that support conservation actions; (6) increased understanding of the linkages between seagrass and climate change is required to adapt conservation accordingly. We also explicitly outline a series of proposed policy actions that will enable the scientific and conservation community to rise to these challenges. We urge the seagrass conservation community to engage stakeholders from local resource users to international policy-makers to address the challenges outlined here, in order to secure the future of the world's seagrass ecosystems and maintain the vital services which they supply.

Age of enlightenment: long-term effects of outdoor aesthetic lights on bats in churches.

We surveyed 110 country churches in south-western Sweden for presence of brown long-eared bats Plecotus auritus in summer 2016 by visual inspection and/or evening emergence counts. Each church was also classified according to the presence and amount of aesthetic directional lights (flood-lights) aimed on its walls and tower from the outside. Sixty-one of the churches had previously been surveyed by one of us (J.R.) between 1980 and 1990, before lights were installed on Swedish churches, using the same methods. Churches with bat colonies had decreased significantly in frequency from 61% in 1980s to 38% by 2016. All abandoned churches had been fitted with flood-lights in the period between the two surveys. The loss of bat colonies from lit churches was highly significant and most obvious when lights were applied from all directions, leaving no dark corridor for the bats to leave and return to the roost. In contrast, in churches that were not lit, all of 13 bat colonies remained after 25+ years between the surveys. Lighting of churches and other historical buildings is a serious threat to the long-term survival and reproduction of light-averse bats such as Plecotus spp. and other slow-flying species. Bat roosts are strictly protected according to the EU Habitats Directive and the EUROBATS agreement. Lighting of buildings for aesthetic purposes is becoming a serious environmental issue, because important bat roosts are destroyed in large numbers, and the problem should be handled accordingly. As a start, installation of flood-lights on historical buildings should at least require an environmental impact assessment (EIA).

Marine protected areas increase temporal stability of community structure, but not density or diversity, of tropical seagrass fish communities.

Marine protected areas (MPAs) have been shown to increase long-term temporal stability of fish communities and enhance ecosystem resilience to anthropogenic disturbance. Yet, the potential ability of MPAs to buffer effects of environmental variability at shorter time scales remains widely unknown. In the tropics, the yearly monsoon cycle is a major natural force affecting marine organisms in tropical regions, and its timing and severity are predicted to change over the coming century, with potentially severe effects on marine organisms, ecosystems and ecosystem services. Here, we assessed the ability of MPAs to buffer effects of monsoon seasonality on seagrass-associated fish communities, using a field survey in two MPAs (no-take zones) and two unprotected (open-access) sites around Zanzibar (Tanzania). We assessed the temporal stability of fish density and community structure within and outside MPAs during three monsoon seasons in 2014-2015, and investigated several possible mechanisms that could regulate temporal stability. Our results show that MPAs did not affect fish density and diversity, but that juvenile fish densities were temporally more stable within MPAs. Second, fish community structure was more stable within MPAs for juvenile and adult fish, but not for subadult fish or the total fish community. Third, the observed effects may be due to a combination of direct and indirect (seagrass-mediated) effects of seasonality and, potentially, fluctuating fishing pressure outside MPAs. In summary, these MPAs may not have the ability to enhance fish density and diversity and to buffer effects of monsoon seasonality on the whole fish community. However, they may increase the temporal stability of certain groups, such as juvenile fish. Consequently, our results question whether MPAs play a general role in the maintenance of biodiversity and ecosystem functioning under changing environmental conditions in tropical seagrass fish communities.