Spatial insurance against a heatwave differs between trophic levels in experimental aquatic communities.

Climate change-related heatwaves are major threats to biodiversity and ecosystem functioning. However, our current understanding of the mechanisms governing community resistance to and recovery from extreme temperature events is still rudimentary. The spatial insurance hypothesis postulates that diverse regional species pools can buffer ecosystem functioning against local disturbances through the immigration of better-adapted taxa. Yet, experimental evidence for such predictions from multi-trophic communities and pulse-type disturbances, like heatwaves, is largely missing. We performed an experimental mesocosm study to test whether species dispersal from natural lakes prior to a simulated heatwave could increase the resistance and recovery of plankton communities. As the buffering effect of dispersal may differ among trophic groups, we independently manipulated the dispersal of organisms from lower (phytoplankton) and higher (zooplankton) trophic levels. The experimental heatwave suppressed total community biomass by having a strong negative effect on zooplankton biomass, probably due to a heat-induced increase in metabolic costs, resulting in weaker top-down control on phytoplankton. While zooplankton dispersal did not alleviate the negative heatwave effects on zooplankton biomass, phytoplankton dispersal enhanced biomass recovery at the level of primary producers, providing partial evidence for spatial insurance. The differential responses to dispersal may be linked to the much larger regional species pool of phytoplankton than of zooplankton. Our results suggest high recovery capacity of community biomass independent of dispersal. However, community composition and trophic structure remained altered due to the heatwave, implying longer-lasting changes in ecosystem functioning.

Wavelength-dependent effects of artificial light at night on phytoplankton growth and community structure.

Artificial light at night (ALAN) is a disruptive form of pollution, impacting physiological and behavioural processes that may scale up to population and community levels. Evidence from terrestrial habitats show that the severity and type of impact depend on the wavelength and intensity of ALAN; however, research on marine organisms is still limited. Here, we experimentally investigated the effect of different ALAN colours on marine primary producers. We tested the effect of green (525 nm), red (624 nm) and broad-spectrum white LED ALAN, compared to a dark control, on the green microalgae Tetraselmis suesica and a diatom assemblage. We show that green ALAN boosted chlorophyll production and abundance in T. suesica. All ALAN wavelengths affected assemblage biomass and diversity, with red and green ALAN having the strongest effects, leading to higher overall abundance and selective dominance of specific diatom species, some known to cause harmful algal blooms. Our findings show that green and red ALAN should be used with caution as alternative LED colours in coastal areas, where there might be a need to strike a balance between the effects of green and red light on marine primary producers with the benefit they appear to bring to other organisms.

Lumpy species coexistence arises robustly in fluctuating resource environments.

The effect of life-history traits on resource competition outcomes is well understood in the context of a constant resource supply. However, almost all natural systems are subject to fluctuations of resources driven by cyclical processes such as seasonality and tidal hydrology. To understand community composition, it is therefore imperative to study the impact of resource fluctuations on interspecies competition. We adapted a well-established resource-competition model to show that fluctuations in inflow concentrations of two limiting resources lead to the survival of species in clumps along the trait axis, consistent with observations of "lumpy coexistence" [Scheffer M, van Nes EH (2006) Proc Natl Acad Sci USA 103:6230-6235]. A complex dynamic pattern in the available ambient resources arose very early in the self-organization process and dictated the locations of clumps along the trait axis by creating niches that promoted the growth of species with specific traits. This dynamic pattern emerged as the combined result of fluctuations in the inflow of resources and their consumption by the most competitive species that accumulated the bulk of biomass early in assemblage organization. Clumps emerged robustly across a range of periodicities, phase differences, and amplitudes. Given the ubiquity in the real world of asynchronous fluctuations of limiting resources, our findings imply that assemblage organization in clumps should be a common feature in nature.

Everything is not everywhere: can marine compartments shape phytoplankton assemblages?

The idea that 'everything is everywhere, but the environment selects' has been seminal in microbial biogeography, and marine phytoplankton is one of the prototypical groups used to illustrate this. The typical argument has been that phytoplankton is ubiquitous, but that distinct assemblages form under environmental selection. It is well established that phytoplankton assemblages vary considerably between coastal ecosystems. However, the relative roles of compartmentalization of regional seas and site-specific environmental conditions in shaping assemblage structures have not been specifically examined. We collected data from coastal embayments that fall within two different water compartments within the same regional sea and are characterized by highly localized environmental pressures. We used principal coordinates of neighbour matrices (PCNM) and asymmetric eigenvector maps (AEM) models to partition the effects that spatial structures, environmental conditions and their overlap had on the variation in assemblage composition. Our models explained a high percentage of variation in assemblage composition (59-65%) and showed that spatial structure consistent with marine compartmentalization played a more important role than local environmental conditions. At least during the study period, surface currents connecting sites within the two compartments failed to generate sufficient dispersal to offset the impact of differences due to compartmentalization. In other words, our findings suggest that, even for a prototypical cosmopolitan group, everything is not everywhere.

Interplay between r- and K-strategists leads to phytoplankton underyielding under pulsed resource supply.

Fluctuations in nutrient ratios over seasonal scales in aquatic ecosystems can result in overyielding, a condition arising when complementary life-history traits of coexisting phytoplankton species enables more complete use of resources. However, when nutrient concentrations fluctuate under short-period pulsed resource supply, the role of complementarity is less understood. We explore this using the framework of Resource Saturation Limitation Theory (r-strategists vs. K-strategists) to interpret findings from laboratory experiments. For these experiments, we isolated dominant species from a natural assemblage, stabilized to a state of coexistence in the laboratory and determined life-history traits for each species, important to categorize its competition strategy. Then, using monocultures we determined maximum biomass density under pulsed resource supply. These same conditions of resource supply were used with polycultures comprised of combinations of the isolated species. Our focal species were consistent of either r- or K-strategies and the biomass production achieved in monocultures depended on their efficiency to convert resources to biomass. For these species, the K-strategists were less efficient resource users. This affected biomass production in polycultures, which were characteristic of underyielding. In polycultures, K-strategists sequestered more resources than the r-strategists. This likely occurred because the intermittent periods of nutrient limitation that would have occurred just prior to the next nutrient supply pulse would have favored the K-strategists, leading to overall less efficient use of resources by the polyculture. This study provides evidence that fluctuation in resource concentrations resulting from pulsed resource supplies in aquatic ecosystems can result in phytoplankton assemblages' underyielding.

The effects of artificial light at night (ALAN) on the gaping activity and feeding of mussels.

Artificial Light at Night (ALAN) is a common environmental pollutant which affects >22 % of the world's coastlines. However, the impact of ALAN wavelengths on coastal organisms is under-investigated. Here, we tested the impact of red, green, and white ALAN on the gaping activity and phytoplankton consumption of Mytilus edulis mussels and compared these to dark night. Mussels exhibited a semi-diel activity pattern. Although ALAN did not significantly affect the time open nor the phytoplankton consumption, it did have a colour-specific effect on the gaping frequency with red and white ALAN resulting in lower activity compared to the dark night. Green ALAN caused higher gaping frequency and a negative relationship between consumption and proportion of time open compared to the other treatments. Our findings suggest colour-specific ALAN effects on mussels and call for further investigation on the associated physiological mechanisms and potential ecological consequences.

Increased contribution of parasites in microbial eukaryotic communities of different Aegean Sea coastal systems.

Background-Aim: Protistan communities have a major contribution to biochemical processes and food webs in coastal ecosystems. However, related studies are scarce and usually limited in specific groups and/or sites. The present study examined the spatial structure of the entire protistan community in seven different gulfs and three different depths in a regional Mediterranean Sea, aiming to define taxa that are important for differences detected in the marine microbial network across the different gulfs studied as well as their trophic interactions. Methods: Protistan community structure analysis was based on the diversity of the V2-V3 hypervariable region of the 18S rRNA gene. Operational taxonomic units (OTUs) were identified using a 97% sequence identity threshold and were characterized based on their taxonomy, trophic role, abundance and niche specialization level. The differentially abundant, between gulfs, OTUs were considered for all depths and interactions amongst them were calculated, with statistic and network analysis. Results: It was shown that Dinophyceae, Bacillariophyta and Syndiniales were the most abundant groups, prevalent in all sites and depths. Gulfs separation was more striking at surface corroborating with changes in environmental factors, while it was less pronounced in higher depths. The study of differentially abundant, between gulfs, OTUs revealed that the strongest biotic interactions in all depths occurred between parasite species (mainly Syndiniales) and other trophic groups. Most of these species were generalists but not abundant highlighting the importance of rare species in protistan community assemblage. Conclusion: Overall this study revealed the emergence of parasites as important contributors in protistan network regulation regardless of depth.

Widespread extinction debts and colonization credits in United States breeding bird communities.

Species extinctions and colonizations in response to land cover change often occur with time lags rather than instantaneously, leading to extinction debts and colonization credits. These debts and credits can lead to erroneous predictions of future biodiversity. Recent attempts to measure debts and credits have been limited to small geographical areas and have not considered multiple land cover types, or the directionality of land cover change. Here we quantify the relative contribution of past and current landscapes on the current effective number of species of 2,880 US bird communities, explicitly measuring the response of biodiversity to increases and decreases in five land cover types. We find that the current effective number of species is still largely explained by the past landscape composition (legacy effect), depending on the type, magnitude and directionality of recent land cover change. This legacy effect leads to widespread extinction debts and colonization credits. Specifically, we reveal debts across 52% of the United States, particularly in recently urbanized areas, and colonization credits in the remaining 48%, which are primarily associated with grassland decrease. We conclude that biodiversity policy targets risk becoming rapidly obsolete unless past landscapes are considered and debts and credits accounted for.

Microalgae show a range of responses to exometabolites of foreign species.

Studies on microalgae interspecific interactions have so far focused either on nutrient competition or allelopathic effects due to excreted substances from Harmful Algal Bloom (HAB) species. Evidence from plants, bacteria and specific microalgae groups, point to a range of responses mediated by sensing or direct chemical impact of exometabolites from foreign species. Such processes remain under-investigated, especially in non-HAB microalgae, despite the importance of such knowledge in ecology and industrial applications. Here, we study the directional effect of exometabolites of 4 "foreign" species Heterosigma akashiwo, Phaeocystis sp., Tetraselmis sp. and Thalassiosira sp. to each of three "target" species across a total of 12 treatments. We disentangle these effects from nutrient competition by adding cell free medium of each "foreign" species into our treatment cultures. We measured the biomass response, to the foreign exometabolites, as cell number and photosynthetic biomass (Chla), whereas nutrient use was measured as residual phosphorus (PO4) and intracellular phosphorus (P). Exometabolites from filtrate of foreign species were putatively annotated by untargeted metabolomics analysis and were discussed in association to observed responses of target species. Among others, these metabolites included L-histidinal, Tiliacorine and dimethylsulfoniopropionate (DMSP). Our findings show that species show a range of responses with the most common being biomass suppression, and less frequent biomass enhancement and intracellular P storage. Filtrate from the green microalgae Tetraselmis caused the most pronounced negative effects suggesting that non-HAB species can also cause negative chemical interference. A candidate metabolite inducing this response is L-histidinal which was measured in high abundance uniquely in Tetraselmis and its L-histidine form derived from bacteria was previously confirmed as a microalgal algicidal. H. akashiwo also induced biomass suppression on other microalgae and a candidate metabolite for this response is Tiliacorine, a plant-derived alkaloid with confirmed cytotoxic activity.

Effects of microplastics on bivalves: Are experimental settings reflecting conditions in the field?

Bivalves are the focus of experimental research as they can filtrate a broad size range of microplastics (MPs) with negative consequences for their physiology. Studies use a range of MP shapes, materials, sizes and concentrations raising the question on whether these reflect environmental observations. We review experimental studies on the effects of MPs on marine bivalves and contrast the MP characteristics used with corresponding data from the environment. Mussels were the most common bivalve across experiments which reflect their high abundance and broad distribution in the field. Although fibres are the dominant shape of MPs in coastal systems, most studies focus on spherules and beads, and MP concentrations are often orders of magnitude higher than environmental levels. For higher relevance of experimental findings we recommend that maximum experimental concentrations of MPs are in the range of 100-1000 particles/L, that there is more focus on microfibers and that concentration is reported in particles/volume.

Effects of long-term exposure to microfibers on ecosystem services provided by coastal mussels.

The biofiltration capacity of bivalve populations is known to alleviate the effects of coastal eutrophication. However, this important ecosystem service could potentially be impaired by the increasing microplastic abundance in near shore environments. It is known that relatively large microplastics (∼500 µm) impair the filtration capacity of bivalves. However, the effect of smaller microplastics, and specifically microfibers, is not known even though they are more common in many natural systems and similar in size to phytoplankton, the main food source of mussels. Here, we investigated the effects of long-term exposure to microfibers (MFs), which are smaller than 100 µm, on the biofiltration capacity of the blue mussel, Mytilus edulis. Our findings show that long-term exposure (here 39 days) to microfibers significantly reduced (21%) the clearance of phytoplankton (Tetraselmis sp). While previous studies have shown that larger microplastics can decrease the filtration capacity of mussels after short-term exposure, our findings suggest that, for smaller MFs, mussel's clearance capacity is significantly affected after long-term exposure (39 days in this study). This may be due to the accumulation of MFs in the digestive system. In addition, the most efficient phytoplankton consumers were more susceptible to MF accumulation in the digestive system. This suggests that prolonged exposure to MF of coastal mussels could negatively impact the biofiltration of more potent individuals, thus decreasing the ecosystem service potential of the population as a whole.

Nitrogen as the main driver of benthic diatom composition and diversity in oligotrophic coastal systems.

Phytoplankton is the main indicator group for eutrophication in coastal ecosystems, however its high dispersal potential does not enable the assessment of localized effects of coastal nutrient enrichment. Benthic diatoms are sessile microalgae associated with sandy substrates and have the potential to reflect more localized pollution impacts. Although benthic diatoms are widely used bioindicators in freshwater systems, they have rarely been used for assessing the eutrophication status of oligotrophic environments such as the eastern Mediterranean Sea. In the present study, we assess the efficiency of benthic diatoms as bioindicators of nutrient enrichment in oligotrophic coastal systems, by investigating the effect of different physicochemical conditions and nutrient concentrations on the assemblage composition, diversity and individual species populations. To do this, we sampled along a eutrophication gradient formed by anthropogenic nutrient inputs from a metropolitan area. The main driver of assemblage composition, diversity and biomass of diatoms was nitrogen concentration and its temporal and spatial changes. Nitrogen loadings were positively correlated with increased biomass of Cocconeis spp. and negatively correlated with Mastogloia spp. Our findings suggest that in coastal ecosystems of oligotrophic marine ecoregions, benthic diatom assemblage structure and specific taxonomic groups can be reliable predictors of coastal eutrophication offering higher spatial resolution compared to phytoplankton.

Temporal phosphate gradients reveal diverse acclimation responses in phytoplankton phosphate uptake.

Phytoplankton face environmental nutrient variations that occur in the dynamic upper layers of the ocean. Phytoplankton cells are able to rapidly acclimate to nutrient fluctuations by adjusting their nutrient-uptake system and metabolism. Disentangling these acclimation responses is a critical step in bridging the gap between phytoplankton cellular physiology and community ecology. Here, we analyzed the dynamics of phosphate (P) uptake acclimation responses along different P temporal gradients by using batch cultures of the diatom Phaeodactylum tricornutum. We employed a multidisciplinary approach that combined nutrient-uptake bioassays, transcriptomic analysis, and mathematical models. Our results indicated that cells increase their maximum nutrient-uptake rate (Vmax) both in response to P pulses and strong phosphorus limitation. The upregulation of three genes coding for different P transporters in cells experiencing low intracellular phosphorus levels supported some of the observed Vmax variations. In addition, our mathematical model reproduced the empirical Vmax patterns by including two types of P transporters upregulated at medium-high environmental and low intracellular phosphorus levels, respectively. Our results highlight the existence of a sequence of acclimation stages along the phosphate continuum that can be understood as a succession of acclimation responses. We provide a novel conceptual framework that can contribute to integrating and understanding the dynamics and wide diversity of acclimation responses developed by phytoplankton.

Environmental DNA: A New Low-Cost Monitoring Tool for Pathogens in Salmonid Aquaculture.

Environmental DNA (eDNA) metabarcoding is a relatively new monitoring tool featuring in an increasing number of applications such as the facilitation of the accurate and cost effective detection of species in environmental samples. eDNA monitoring is likely to have a major impact on the ability of salmonid aquaculture industry producers and their regulators to detect the presence and abundance of pathogens and other biological threats in the surrounding environment. However, for eDNA metabarcoding to develop into a useful bio-monitoring tool it is necessary to (a) validate that sequence datasets derived from amplification of metabarcoding markers reflect the true species' identity, (b) test the sensitivity under different abundance levels and environmental noise and (c) establish a low-cost sequencing method to enable the bulk processing of field samples. In this study, we employed an elaborate experimental design whereby different combinations of five biological agents were crossed at three abundance levels and exposed to sterile pre-filtered and unfiltered seawater, prior to coarse filtering and then eDNA ultrafiltration of the resultant material. We then benchmarked the low-cost, scalable, Ion Torrent sequencing method against the current gold-standard Illumina platform for eDNA surveys in aquaculture. Based on amplicon-seq of the 18S SSU rDNA v9 region, we were able to identify two parasites (Lepeophtheirus salmonis and Paramoeba perurans) to species level, whereas the microalgae species Prymnesium parvum, Pseudo-nitzschia seriata, and P. delicatissima could be assigned correctly only to the genus level. Illumina and Ion Torrent provided near identical results in terms of community composition in our samples, whereas Ion Torrent was more sensitive in detecting species richness when the medium was unfiltered seawater. Both methods were able to reflect the difference in relative abundance between treatments in 4 out of 5 species when samples were exposed to the unfiltered seawater, despite the significant amount of background noise from both bacteria and eukaryotes. Our findings indicate that eDNA metabarcoding offers significant potential in the monitoring of species harmful to aquaculture and for this purpose, the low-cost Ion Torrent sequencing is as accurate as Illumina in determining differences in their relative abundance between samples.

Changes in Microbial (Bacteria and Archaea) Plankton Community Structure after Artificial Dispersal in Grazer-Free Microcosms.

Microbes are considered to have a global distribution due to their high dispersal capabilities. However, our knowledge of the way geographically distant microbial communities assemble after dispersal in a new environment is limited. In this study, we examined whether communities would converge because similar taxa would be selected under the same environmental conditions, or would diverge because of initial community composition, after artificial dispersal. To this aim, a microcosm experiment was performed, in which the temporal changes in the composition and diversity of different prokaryoplankton assemblages from three distant geographic coastal areas (Banyuls-sur-Mer in northwest Mediterranean Sea, Pagasitikos Gulf in northeast Mediterranean and Woods Hole, MA, USA in the northwest Atlantic), were studied. Diversity was investigated using amplicon pyrosequencing of the V1-V3 hypervariable regions of the 16S rRNA. The three assemblages were grown separately in particle free and autoclaved Banyuls-sur-mer seawater at 18 °C in the dark. We found that the variability of prokaryoplankton community diversity (expressed as richness, evenness and dominance) as well as the composition were driven by patterns observed in Bacteria. Regarding community composition, similarities were found between treatments at family level. However, at the OTU level microbial communities from the three different original locations diverge rather than converge during incubation. It is suggested that slight differences in the composition of the initial prokaryoplankton communities, resulted in separate clusters the following days even when growth took place under identical abiotic conditions.

Phytoplankton succession in recurrently fluctuating environments.

Coastal marine systems are affected by seasonal variations in biogeochemical and physical processes, sometimes leading to alternating periods of reproductive growth limitation within an annual cycle. Transitions between these periods can be sudden or gradual. Human activities, such as reservoir construction and interbasin water transfers, influence these processes and can affect the type of transition between resource loading conditions. How such human activities might influence phytoplankton succession is largely unknown. Here, we employ a multispecies, multi-nutrient model to explore how nutrient loading switching mode might affect phytoplankton succession. The model is based on the Monod-relationship, predicting an instantaneous reproductive growth rate from ambient inorganic nutrient concentrations whereas the limiting nutrient at any given time was determined by Liebig's Law of the Minimum. When these relationships are combined with population loss factors, such as hydraulic displacement of cells associated with inflows, a characterization of a species' niche can be achieved through application of the R* conceptual model, thus enabling an ecological interpretation of modeling results. We found that the mode of reversal in resource supply concentrations had a profound effect. When resource supply reversals were sudden, as expected in systems influenced by pulsed inflows or wind-driven mixing events, phytoplankton were characterized by alternating succession dynamics, a phenomenon documented in inland water bodies of temperate latitudes. When resource supply reversals were gradual, as expected in systems influenced by seasonally developing wet and dry seasons, or annually occurring periods of upwelling, phytoplankton dynamics were characterized by mirror-image succession patterns. This phenomenon has not been reported previously in plankton systems but has been observed in some terrestrial plant systems. These findings suggest that a transition from alternating to "mirror-image" succession patterns might arise with continued coastal zone development, with crucial implications for ecosystems dependent on time-sensitive processes, e.g., spawning events and migration patterns.

Phytoplankton assemblage characteristics in recurrently fluctuating environments.

Annual variations in biogeochemical and physical processes can lead to nutrient variability and seasonal patterns in phytoplankton productivity and assemblage structure. In many coastal systems river inflow and water exchange with the ocean varies seasonally, and alternating periods can arise where the nutrient most limiting to phytoplankton growth switches. Transitions between these alternating periods can be sudden or gradual and this depends on human activities, such as reservoir construction and interbasin water transfers. How such activities might influence phytoplankton assemblages is largely unknown. Here, we employed a multispecies, multi-nutrient model to explore how nutrient loading switching mode might affect characteristics of phytoplankton assemblages. The model is based on the Monod-relationship, predicting an instantaneous growth rate from ambient inorganic nutrient concentrations whereas the limiting nutrient at any given time was determined by Liebig's Law of the Minimum. Our simulated phytoplankton assemblages self-organized from species rich pools over a 15-year period, and only the surviving species were considered as assemblage members. Using the model, we explored the interactive effects of complementarity level in trait trade-offs within phytoplankton assemblages and the amount of noise in the resource supply concentrations. We found that the effect of shift from a sudden resource supply transition to a gradual one, as observed in systems impacted by watershed development, was dependent on the level of complementarity. In the extremes, phytoplankton species richness and relative overyielding increased when complementarity was lowest, and phytoplankton biomass increased greatly when complementarity was highest. For low-complementarity simulations, the persistence of poorer-performing phytoplankton species of intermediate R*s led to higher richness and relative overyielding. For high-complementarity simulations, the formation of phytoplankton species clusters and niche compression enabled higher biomass accumulation. Our findings suggest that an understanding of factors influencing the emergence of life history traits important to complementarity is necessary to predict the impact of watershed development on phytoplankton productivity and assemblage structure.

A niche-based modeling approach to phytoplankton community assembly rules.

Six niche-based models proposed by Tokeshi, based on different assumptions of resource allocation by species, were fitted on phytoplankton relative abundance distributions, and potential environmental and biotic factors supporting the applicability of the fitted models were discussed. Overall 16 assemblages corresponding to different sampling times, various environmental conditions, and resource regimes within a year were fitted to the models. Phytoplankton biovolume was used as a measure of abundance, and a randomization test was applied to compare the model fit to the field data. The majority of the phytoplankton assemblages (11 of 16) were successfully described by the Random Fraction model, which is based on the theoretical assumption that resource is apportioned by the species in a random way. Only a few assemblages (three of 16), characterized by extremes in resource availability or disturbance, were not fitted by any of the models. The Random Fraction model in particular was rejected due to a steep slope during the first ranks, while the rest of the distribution remained relatively even, providing further evidence of resilience in phytoplankton communities. Although larger cells seem to have the potential to develop higher biomass, it seems that other factors, including the surface-to-volume ratio, counterbalance this advantage, resulting in a random-like behaviour in resource acquisition by phytoplankton, irrespective of cell size or species identity.