Global conservation outcomes depend on marine protected areas with five key features.

In line with global targets agreed under the Convention on Biological Diversity, the number of marine protected areas (MPAs) is increasing rapidly, yet socio-economic benefits generated by MPAs remain difficult to predict and under debate. MPAs often fail to reach their full potential as a consequence of factors such as illegal harvesting, regulations that legally allow detrimental harvesting, or emigration of animals outside boundaries because of continuous habitat or inadequate size of reserve. Here we show that the conservation benefits of 87 MPAs investigated worldwide increase exponentially with the accumulation of five key features: no take, well enforced, old (>10 years), large (>100 km(2)), and isolated by deep water or sand. Using effective MPAs with four or five key features as an unfished standard, comparisons of underwater survey data from effective MPAs with predictions based on survey data from fished coasts indicate that total fish biomass has declined about two-thirds from historical baselines as a result of fishing. Effective MPAs also had twice as many large (>250 mm total length) fish species per transect, five times more large fish biomass, and fourteen times more shark biomass than fished areas. Most (59%) of the MPAs studied had only one or two key features and were not ecologically distinguishable from fished sites. Our results show that global conservation targets based on area alone will not optimize protection of marine biodiversity. More emphasis is needed on better MPA design, durable management and compliance to ensure that MPAs achieve their desired conservation value.

Integrating abundance and functional traits reveals new global hotspots of fish diversity.

Species richness has dominated our view of global biodiversity patterns for centuries. The dominance of this paradigm is reflected in the focus by ecologists and conservation managers on richness and associated occurrence-based measures for understanding drivers of broad-scale diversity patterns and as a biological basis for management. However, this is changing rapidly, as it is now recognized that not only the number of species but the species present, their phenotypes and the number of individuals of each species are critical in determining the nature and strength of the relationships between species diversity and a range of ecological functions (such as biomass production and nutrient cycling). Integrating these measures should provide a more relevant representation of global biodiversity patterns in terms of ecological functions than that provided by simple species counts. Here we provide comparisons of a traditional global biodiversity distribution measure based on richness with metrics that incorporate species abundances and functional traits. We use data from standardized quantitative surveys of 2,473 marine reef fish species at 1,844 sites, spanning 133 degrees of latitude from all ocean basins, to identify new diversity hotspots in some temperate regions and the tropical eastern Pacific Ocean. These relate to high diversity of functional traits amongst individuals in the community (calculated using Rao's Q), and differ from previously reported patterns in functional diversity and richness for terrestrial animals, which emphasize species-rich tropical regions only. There is a global trend for greater evenness in the number of individuals of each species, across the reef fish species observed at sites ('community evenness'), at higher latitudes. This contributes to the distribution of functional diversity hotspots and contrasts with well-known latitudinal gradients in richness. Our findings suggest that the contribution of species diversity to a range of ecosystem functions varies over large scales, and imply that in tropical regions, which have higher numbers of species, each species contributes proportionally less to community-level ecological processes on average than species in temperate regions. Metrics of ecological function usefully complement metrics of species diversity in conservation management, including when identifying planning priorities and when tracking changes to biodiversity values.

Assessing National Biodiversity Trends for Rocky and Coral Reefs through the Integration of Citizen Science and Scientific Monitoring Programs.

Reporting progress against targets for international biodiversity agreements is hindered by a shortage of suitable biodiversity data. We describe a cost-effective system involving Reef Life Survey citizen scientists in the systematic collection of quantitative data covering multiple phyla that can underpin numerous marine biodiversity indicators at high spatial and temporal resolution. We then summarize the findings of a continental- and decadal-scale State of the Environment assessment for rocky and coral reefs based on indicators of ecosystem state relating to fishing, ocean warming, and invasive species and describing the distribution of threatened species. Fishing impacts are widespread, whereas substantial warming-related change affected some regions between 2005 and 2015. Invasive species are concentrated near harbors in southeastern Australia, and the threatened-species index is highest for the Great Australian Bight and Tasman Sea. Our approach can be applied globally to improve reporting against biodiversity targets and enhance public and policymakers' understanding of marine biodiversity trends.

Corrigendum: Assessing National Biodiversity Trends for Rocky and Coral Reefs through the Integration of Citizen Science and Scientific Monitoring Programs.

[This corrects the article DOI: 10.1093/biosci/biw180.].

Environmental heterogeneity and microbial inheritance influence sponge-associated bacterial composition of Spongia lamella.

Sponges are important components of marine benthic communities. High microbial abundance sponges host a large diversity of associated microbial assemblages. However, the dynamics of such assemblages are still poorly known. In this study, we investigated whether bacterial assemblages present in Spongia lamella remained constant or changed as a function of the environment and life cycle. Sponges were collected in multiple locations and at different times of the year in the western Mediterranean Sea and in nearby Atlantic Ocean to cover heterogeneous environmental variability. Co-occurring adult sponges and offsprings were compared at two of the sites. To explore the composition and abundance of the main bacteria present in the sponge mesohyl, embryos, and larvae, we applied both 16S rRNA gene-denaturing gradient gel electrophoresis (DGGE) and sequencing of excised DGGE bands and quantitative polymerase chain reactions (qPCR). On average, the overall core bacterial assemblage showed over 60 % similarity. The associated bacterial assemblage fingerprints varied both within and between sponge populations, and the abundance of specific bacterial taxa assessed by qPCR significantly differed among sponge populations and between adult sponge and offsprings (higher proportions of Actinobacteria in the latter). Sequences showed between 92 and 100 % identity to sequences previously reported in GenBank, and all were affiliated with uncultured invertebrate bacterial symbionts (mainly sponges). Sequences were mainly related to Chloroflexi and Acidobacteria and a few to Actinobacteria and Bacteroidetes. Additional populations may have been present under detection limits. Overall, these results support that both ecological and biological sponge features may shape the composition of endobiont bacterial communities in S. lamella.

Temporal trends in the secondary metabolite production of the sponge Aplysina aerophoba.

Temporal changes in the production of secondary metabolites are far from being fully understood. Our study quantified, over a two-year period, the concentrations of brominated alkaloids in the ectosome and the choanosome of Aplysina aerophoba, and examined the temporal patterns of these natural products. Based on standard curves, we quantified the concentrations of aerophobin-2, aplysinamisin-1, and isofistularin-3: three of the four major peaks obtained through chemical profiling with high-performance liquid chromatography. Our results showed a striking variation in compound abundance between the outer and inner layers of the sponge. The ectosome showed high concentrations of bromocompounds during the summer months, while the choanosome followed no pattern. Additionally, we found that, from the outer layer of the sponge, aerophobin-2 and isofistularin-3 were significantly correlated with water temperature. The present study is one of the first to document quantitative seasonal variations in individual compounds over multiple years. Further studies will clarify the role of environmental, biological, and physiological factors in determining the seasonal patterns in the concentration of brominated alkaloids.

Exploring the links between natural products and bacterial assemblages in the sponge Aplysina aerophoba.

The sponge Aplysina aerophoba produces a large diversity of brominated alkaloids (BAs) and hosts a complex microbial assemblage. Although BAs are located within sponge cells, the enzymes that bind halogen elements to organic compounds have been exclusively described in algae, fungi, and bacteria. Bacterial communities within A. aerophoba could therefore be involved in the biosynthesis of these compounds. This study investigates whether changes in both the concentration of BAs and the bacterial assemblages are correlated in A. aerophoba. To do so, we quantified major natural products using high-performance liquid chromatography and analyzed bacterial assemblages using denaturing gradient gel electrophoresis on the 16S rRNA gene. We identified multiple associations between bacteria and natural products, including a strong relationship between a Chloroflexi phylotype and aplysinamisin-1 and between an unidentified bacterium and aerophobin-2 and isofistularin-3. Our results suggest that these bacteria could either be involved in the production of BAs or be directly affected by them. To our knowledge, this is one of the first reports that find a significant correlation between natural products and bacterial populations in any benthic organism. Further investigating these associations will shed light on the organization and functioning of host-endobiont systems such as Aplysina aerophoba.

Relevant spatial scales of chemical variation in Aplysina aerophoba.

Understanding the scale at which natural products vary the most is critical because it sheds light on the type of factors that regulate their production. The sponge Aplysina aerophoba is a common Mediterranean sponge inhabiting shallow waters in the Mediterranean and its area of influence in Atlantic Ocean. This species contains large concentrations of brominated alkaloids (BAs) that play a number of ecological roles in nature. Our research investigates the ecological variation in BAs of A. aerophoba from a scale of hundred of meters to thousand kilometers. We used a nested design to sample sponges from two geographically distinct regions (Canary Islands and Mediterranean, over 2500 km), with two zones within each region (less than 50 km), two locations within each zone (less than 5 km), and two sites within each location (less than 500 m). We used high-performance liquid chromatography to quantify multiple BAs and a spectrophotometer to quantify chlorophyll a (Chl a). Our results show a striking degree of variation in both natural products and Chl a content. Significant variation in Chl a content occurred at the largest and smallest geographic scales. The variation patterns of BAs also occurred at the largest and smallest scales, but varied depending on which BA was analyzed. Concentrations of Chl a and isofistularin-3 were negatively correlated, suggesting that symbionts may impact the concentration of some of these compounds. Our results underline the complex control of the production of secondary metabolites, with factors acting at both small and large geographic scales affecting the production of multiple secondary metabolites.

Assessing social-ecological vulnerability of coastal systems to fishing and tourism.

Detecting areas with high social-ecological vulnerability (SEV) is essential to better inform management interventions for building resilience in coastal systems. The SEV framework, developed by the Intergovernmental Panel on Climate Change, is a robust method to identify SEV of tropical coastal systems to climate change. Yet, the application of this framework to temperate regions and other drivers of change remains underexplored. This study operationalizes the SEV framework to assess the social-ecological implications of fishing and tourism in temperate coastal systems. We spatially represented the SEV of coastal systems and identified the social and ecological vulnerability dimensions underpinning this SEV. Our results demonstrate that different dimensions contribute differently to the SEV, suggesting the need for distinctive management intervention to reduce the vulnerability of coastal systems. Our findings also highlight that livelihood diversification and the protection of marine areas may be plausible strategies to build resilience in temperate coastal systems that face fishing and tourism pressures. With this study, we hope to encourage the application of the SEV framework to other drivers of change for building more resilient coastal systems.

Intramolecular modulation of serine protease inhibitor activity in a marine cyanobacterium with antifeedant properties.

Extracts of the Floridian marine cyanobacterium Lyngbya cf. confervoides were found to deter feeding by reef fish and sea urchins (Diadema antillarum). This antifeedant activity may be a reflection of the secondary metabolite content, known to be comprised of many serine protease inhibitors. Further chemical and NMR spectroscopic investigation led us to isolate and structurally characterize a new serine protease inhibitor 1 that is formally derived from an intramolecular condensation of largamide D (2). The cyclization resulted in diminished activity, but to different extents against two serine proteases tested. This finding suggests that cyanobacteria can endogenously modulate the activity of their protease inhibitors.

Marine protected areas are more effective but less reliable in protecting fish biomass than fish diversity.

Marine protected areas (MPAs) provide multiple conservation benefits, thus raising the question of how good and consistent they are at their roles. Here, we quantified three components, namely, diversity, biomass, and other relevant variables, in numerous protected and unprotected areas across four marine ecoregions in south-western Europe. We created a "global conservation status index" (CSIglobal) as the sum of CSIdiversity, CSIbiomass, and CSIrelevant. We then tested whether CSI and its three components varied as a function of protection and marine ecoregion. MPA efficiency, defined as the effect size of protection on CSIglobal, was unreliable and varied with geography. CSIbiomass and CSIrelevant contributed to the unreliability of MPA efficiency, while CSIdiversity was reliable. CSIbiomass showed the major efficiency in protected areas (60%). Biomass of threatened species was the single largest variable that contributed to MPA efficiency. Our easy-to-use approach can identify high- and low-efficient MPAs and help to clarify their actual roles.

Building up marine biodiversity loss: Artificial substrates hold lower number and abundance of low occupancy benthic and sessile species.

Ocean sprawl is replacing natural substrates with artificial alternatives. We hypothesized that, after submersion, high occupancy, high mobility species colonize artificial substrates faster than low occupancy, low mobility species, a biodiversity divergence that will slowly fade out with time. Using quantitative visual census of species in 10 artificial and their adjacent natural substrates, we tested for the existence and temporal evolution of this divergence. Assigning species to one of three occupancy and one of three mobility categories, we found that artificial substrates increased the performance of high mobility, high occupancy species while decreased the performance of low occupancy species with medium and low mobility. This biodiversity divergence remained unchanged over the 50-year underwater timespan of the artificial substrates investigated. Our results suggest that proliferation of artificial substrates is building up a biodiversity loss driven by the least conspicuous and uncommon benthic and sessile species that is undermining coastal marine biodiversity.

Siliceous spicules and skeleton frameworks in sponges: origin, diversity, ultrastructural patterns, and biological functions.

Silica deposition is a fundamental process in sponges. Most sponges in the Classes Demospongiae and Hexactinellida secrete siliceous elements, which can subsequently fuse, interlock with each other, or form three-dimensional structures connected by spongin. The resulting skeletal frameworks allow sponges to grow upwards and facilitate water exchange with minimal metabolic cost. Several studies on sponge skeletogenesis have been published. We are beginning to understand the mechanisms of spicule secretion and the role of spicules and skeletal frameworks in the biology, ecology, and evolution of sponges. Molecular techniques and ecological experiments have demonstrated the genetic control of the process and the contribution of environmental factors to the expression of a sponge spicule, respectively. However, other classic topics such as the role of membranes in silicon transport or whether spicules are formed in situ or secreted anywhere in the sponge mesohyl and then transported to the skeletal framework require further investigation. We review the process of silica deposition in sponges at the molecular and cellular levels, as well as the biological and ecological functions of spicules and skeletons. The genetic control of spicule shapes makes them useful in the reconstruction of sponge phylogeny, although recent experiments have demonstrated the influence of environmental factors in modulating spicule size, shape, and the presence or absence of one or more spicule types. The implications of such variations in sponge taxonomy may be important. Besides supporting sponge cells, spicules can help larvae stay buoyant while in the plankton or reach the bottom at settlement, enhance reproduction success, or catch prey. Conversely, the role of spicules and skeletons in deterring predation has not been demonstrated. Knowledge of several aspects is still based on a single or a few species and extrapolations should be made only with caution. With the advent of new molecular techniques, new lines of research are presently open and active in this field.

Small-scale association measures in epibenthic communities as a clue for allelochemical interactions.

The small-scale associations in a rocky subtidal community in the northwestern Mediterranean were studied by a development of the continuous line transect method. This method allowed the overall measurement of non-randomness in interspecific contacts and the assignment of an association index to each species-pair, whose, significance was tested by Monte Carlo procedures. At the same time, the continuous recording allowed the study of the weakening of the interactions with increasing distances. Our purpose was to uncover evidence for allelochemical mechanisms of space occupation and maintenance. A strong non-randomness was found in the interspecific associations. This was mostly due to the interactions of the poecilosclerid sponge Crambe crambe (Schmidt) with its neighbours, especially its negative associations with other sponge species. The strength of the relationships fell drastically over the first few centimeters from the contact borders of the different species. The results pointed strongly to an allelochemical mechanism. The extracts of this sponge featured high bioactivity in laboratory assays, and field experiments demonstrated that the sponge can inhibit the growth of species in the community studied. Standard sampling techniques would have overlooked the spatial structure present in the data. The study emphasizes the need for both contact data and distance data in order to identify the underlying processes reliably. The line transect method provides both types of information easily and allows testing of models and identification of organisms likely to use chemical defenses in space competition. Its use as a preliminary step in studies of chemical ecology might help to detect presumptive allelochemical processes prior to experimental work on the potentially active species.

Out of sight, out of mind: threats to the marine biodiversity of the Canary Islands (NE Atlantic Ocean).

Lack of knowledge of the marine realm may bias our perception of the current status and threats to marine biodiversity. Less than 10% of all ecological literature is related to the ocean, and the information we have on marine species that are threatened or on the verge of extinction is scarce. This lack of information is particularly critical for isolated areas such as oceanic archipelagos. Here we review published and grey literature on the current status of marine organisms in the Canary Islands as a case description of the consequences that current out-of-sight out-of-mind attitudes may have on this unique environment. Global change, as represented by coastal development, pollution, exotic species and climate change, are currently affecting the distribution and abundance of Canarian marine organisms, and pose multiple threats to local species and communities. Environmental risks are significant at community and species levels, particularly for threatened species. Failure to address these trends will result in shifts in local biodiversity with important ecological, social, and economic consequences. Scientists, policy makers, educators, and relevant societal groups need to collaborate to reverse deleterious coastal biodiversity trends.

Patterns of chemical diversity in the Mediterranean sponge Spongia lamella.

The intra-specific diversity in secondary metabolites can provide crucial information for understanding species ecology and evolution but has received limited attention in marine chemical ecology. The complex nature of diversity is partially responsible for the lack of studies, which often target a narrow number of major compounds. Here, we investigated the intra-specific chemical diversity of the Mediterranean sponge Spongia lamella. The chemical profiles of seven populations spreading over 1200 km in the Western Mediterranean were obtained by a straightforward SPE-HPLC-DAD-ELSD process whereas the identity of compounds was assessed by comparison between HPLC-MS spectra and literature data. Chemical diversity calculated by richness and Shannon indexes differed significantly between sponge populations but not at a larger regional scale. We used factor analysis, analysis of variance, and regression analysis to examine the chemical variability of this sponge at local and regional scales, to establish general patterns of variation in chemical diversity. The abundance of some metabolites varied significantly between sponge populations. Despite these significant differences between populations, we found a clear pattern of increasing chemical dissimilarity with increasing geographic distance. Additional large spatial scale studies on the chemical diversity of marine organisms will validate the universality or exclusivity of this pattern.

Variation in multiple traits of vegetative and reproductive seagrass tissues influences plant-herbivore interactions.

Plant-herbivore interactions have strong ecological and evolutionary consequences, but have been traditionally overlooked in marine higher plants. Despite recent advances in seagrass ecology that highlight the importance of herbivory, the mechanisms that regulate the feeding behaviour of seagrass consumers remain largely unknown. Herbivores have been shown to reduce the sexual reproductive success of seagrasses through direct consumption of inflorescences and seeds, but we know little about intraspecific variation in susceptibility to grazing of different seagrass tissues. We contrasted the relative palatability of reproductive and vegetative tissues of the temperate seagrass Posidonia oceanica in the field, and we assessed the feeding preferences among these tissues of the main consumers of the plant, the fish Sarpa salpa and the urchin Paracentrotus lividus. Moreover, we identified the plant traits that explained the observed feeding behaviour. We provide strong evidence for herbivore selectivity among seagrass tissues. In the field, 70-90% of inflorescences were damaged by herbivores compared to 3-60% of leaves of similar age. In feeding assays, the urchin P. lividus showed over a twofold preference for reproductive tissue at various stages of development. By contrast, we detected no feeding activity on either leaves or inflorescences from the fish S. salpa, which is known to migrate to deeper waters soon after flowering starts and during the period of fruit maturation. Despite being the preferred food of urchins, inflorescences were chemically defended, had higher levels of phenolics and lower nutrient and calorific content than leaves. We experimentally demonstrated that leaf structural defences are the primary factor in determining urchin feeding preferences. Removal of plant structure results in a drastic shift in urchin selectivity towards the most nutritious and less chemically defended leaf tissue, indicating that multiple mechanisms of defence to herbivory may coexist in seagrasses.