Increasing picocyanobacteria success in shelf waters contributes to long-term food web degradation.

Continental margins are disproportionally important for global primary production, fisheries and CO2 uptake. However, across the Northeast Atlantic shelves, there has been an ongoing summertime decline of key biota-large diatoms, dinoflagellates and copepods-that traditionally fuel higher tropic levels such as fish, sea birds and marine mammals. Here, we combine multiple time series with in situ process studies to link these declines to summer nutrient stress and increasing proportions of picophytoplankton that can comprise up to 90% of the combined pico- and nanophytoplankton biomass in coastal areas. Among the pico-fraction, it is the cyanobacterium Synechococcus that flourishes when iron and nitrogen resupply to surface waters are diminished. Our field data show how traits beyond small size give Synechococcus a competitive edge over pico- and nanoeukaryotes. Key is their ability to grow at low irradiances near the nutricline, which is aided by their superior light-harvesting system and high affinity to iron. However, minute size and lack of essential biomolecules (e.g. omega-3 polyunsaturated fatty acids and sterols) render Synechococcus poor primary producers to sustain shelf sea food webs efficiently. The combination of earlier spring blooms and lower summer food quantity and quality creates an increasing period of suboptimal feeding conditions for zooplankton at a time of year when their metabolic demand is highest. We suggest that this nutrition-related mismatch has contributed to the widespread, ~50% decline in summer copepod abundance we observe over the last 60 years. With Synechococcus clades being prominent from the tropics to the Arctic and their abundances increasing worldwide, our study informs projections of future food web dynamics in coastal and shelf areas where droughts and stratification lead to increasing nutrient starvation of surface waters.

Relationships of temperature and biodiversity with stability of natural aquatic food webs.

Temperature and biodiversity changes occur in concert, but their joint effects on ecological stability of natural food webs are unknown. Here, we assess these relationships in 19 planktonic food webs. We estimate stability as structural stability (using the volume contraction rate) and temporal stability (using the temporal variation of species abundances). Warmer temperatures were associated with lower structural and temporal stability, while biodiversity had no consistent effects on either stability property. While species richness was associated with lower structural stability and higher temporal stability, Simpson diversity was associated with higher temporal stability. The responses of structural stability were linked to disproportionate contributions from two trophic groups (predators and consumers), while the responses of temporal stability were linked both to synchrony of all species within the food web and distinctive contributions from three trophic groups (predators, consumers, and producers). Our results suggest that, in natural ecosystems, warmer temperatures can erode ecosystem stability, while biodiversity changes may not have consistent effects.

Causal networks of phytoplankton diversity and biomass are modulated by environmental context.

Untangling causal links and feedbacks among biodiversity, ecosystem functioning, and environmental factors is challenging due to their complex and context-dependent interactions (e.g., a nutrient-dependent relationship between diversity and biomass). Consequently, studies that only consider separable, unidirectional effects can produce divergent conclusions and equivocal ecological implications. To address this complexity, we use empirical dynamic modeling to assemble causal networks for 19 natural aquatic ecosystems (N24◦~N58◦) and quantified strengths of feedbacks among phytoplankton diversity, phytoplankton biomass, and environmental factors. Through a cross-system comparison, we identify macroecological patterns; in more diverse, oligotrophic ecosystems, biodiversity effects are more important than environmental effects (nutrients and temperature) as drivers of biomass. Furthermore, feedback strengths vary with productivity. In warm, productive systems, strong nitrate-mediated feedbacks usually prevail, whereas there are strong, phosphate-mediated feedbacks in cold, less productive systems. Our findings, based on recovered feedbacks, highlight the importance of a network view in future ecosystem management.

Intraseasonal predictability of natural phytoplankton population dynamics.

It is difficult to make skillful predictions about the future dynamics of marine phytoplankton populations. Here, we use a 22-year time series of monthly average abundances for 198 phytoplankton taxa from Station L4 in the Western English Channel (1992-2014) to test whether and how aggregating phytoplankton into multi-species assemblages can improve predictability of their temporal dynamics. Using a non-parametric framework to assess predictability, we demonstrate that the prediction skill is significantly affected by how species data are grouped into assemblages, the presence of noise, and stochastic behavior within species. Overall, we find that predictability one month into the future increases when species are aggregated together into assemblages with more species, compared with the predictability of individual taxa. However, predictability within dinoflagellates and larger phytoplankton (>12 µm cell radius) is low overall and does not increase by aggregating similar species together. High variability in the data, due to observational error (noise) or stochasticity in population growth rates, reduces the predictability of individual species more than the predictability of assemblages. These findings show that there is greater potential for univariate prediction of species assemblages or whole-community metrics, such as total chlorophyll or biomass, than for the individual dynamics of phytoplankton species.

Effects of elevated CO2 on phytoplankton community biomass and species composition during a spring Phaeocystis spp. bloom in the western English Channel.

A 21-year time series of phytoplankton community structure was analysed in relation to Phaeocystis spp. to elucidate its contribution to the annual carbon budget at station L4 in the western English Channel (WEC). Between 1993-2014 Phaeocystis spp. contributed ∼4.6% of the annual phytoplankton carbon and during the March - May spring bloom, the mean Phaeocystis spp. biomass constituted 17% with a maximal contribution of 47% in 2001. Upper maximal weekly values above the time series mean ranged from 63 to 82% of the total phytoplankton carbon (∼42-137mg carbon (C)m-3) with significant inter-annual variability in Phaeocystis spp. Maximal biomass usually occurred by the end of April, although in some cases as early as mid-April (2007) and as late as late May (2013). The effects of elevated pCO2 on the Phaeocystis spp. spring bloom were investigated during a fifteen-day semi-continuous microcosm experiment. The phytoplankton community biomass was estimated at ∼160mgCm-3 and was dominated by nanophytoplankton (40%, excluding Phaeocystis spp.), Phaeocystis spp. (30%) and cryptophytes (12%). The smaller fraction of the community biomass comprised picophytoplankton (9%), coccolithophores (3%), Synechococcus (3%), dinoflagellates (1.5%), ciliates (1%) and diatoms (0.5%). Over the experimental period, total biomass increased significantly by 90% to ∼305mgCm-3 in the high CO2 treatment while the ambient pCO2 control showed no net gains. Phaeocystis spp. exhibited the greatest response to the high CO2 treatment, increasing by 330%, from ∼50mgCm-3 to over 200mgCm-3 and contributing ∼70% of the total biomass. Taken together, the results of our microcosm experiment and analysis of the time series suggest that a future high CO2 scenario may favour dominance of Phaeocystis spp. during the spring bloom. This has significant implications for the formation of hypoxic zones and the alteration of food web structure including inhibitory feeding effects and lowered fecundity in many copepod species.

Long-term dynamics in a soft-bottom amphipod community and the influence of the pelagic environment.

The processes and patterns seen in coastal benthic communities can be strongly influenced by the overlying pelagic environmental conditions. Integrating long-term biological and environmental data (both benthic and pelagic) can give insight into the specific relationships between key benthic functional groups and natural temporal changes in the marine environment. The identity and abundance of amphipod species found at Station L4 (Western English Channel) were tracked for 7 years (2008-2014), whilst simultaneously, annual changes in phytoplankton biomass, water temperature, salinity and chlorophyll a concentration were also characterized. The main species were persistent and showed little variability along the study period. Overall, however, there were significant changes in the structure of the whole community between sampling times, highlighting the importance of less numerically-dominant species in driving temporal variability. Surprisingly, the current study did not detect a significant influence of the phytoplankton biomass on benthic amphipod dynamics. On the other hand, there was a clear and constant correlation between bottom water temperatures and amphipod abundance. This pattern is different from that observed in other detritivorous species at L4, highlighting the complexity of benthic-pelagic coupling and the high variability of the response to pelagic conditions among different groups. As a result of the biogeographic position of the Western English Channel, the key role of amphipods in benthic communities, the influence of the temperature in their populations dynamics, as well as the solid baseline provided here and in previous studies, the monitoring of long-term amphipod dynamics in the English Channel could be a valuable tool to evaluate the biological effect of climate change over marine benthic communities.

Metabolically active, non-nitrogen fixing, Trichodesmium in UK coastal waters during winter.

Trichodesmium, a colonial cyanobacterium typically associated with tropical waters, was observed between January and April 2014 in the western English Channel. Sequencing of the heterocyst differentiation (hetR) and 16S rRNA genes placed this community within the Clade IV Trichodesmium, an understudied clade previously found only in low numbers in warmer waters. Nitrogen fixation was not detected although measurable rates of nitrate uptake and carbon fixation were observed. Trichodesmium RuBisCO transcript abundance relative to gene abundance suggests the potential for viable and potentially active Trichodesmium carbon fixation. Observations of Trichodesmium when coupled with a numerical advection model indicate that Trichodesmium communities can remain viable for >3.5 months at temperatures lower than previously expected. The results suggest that Clade IV Trichodesmium occupies a different niche to other Trichodesmium species, and is a cold- or low-light-adapted variant.

The influence of balanced and imbalanced resource supply on biodiversity-functioning relationship across ecosystems.

Numerous studies show that increasing species richness leads to higher ecosystem productivity. This effect is often attributed to more efficient portioning of multiple resources in communities with higher numbers of competing species, indicating the role of resource supply and stoichiometry for biodiversity-ecosystem functioning relationships. Here, we merged theory on ecological stoichiometry with a framework of biodiversity-ecosystem functioning to understand how resource use transfers into primary production. We applied a structural equation model to define patterns of diversity-productivity relationships with respect to available resources. Meta-analysis was used to summarize the findings across ecosystem types ranging from aquatic ecosystems to grasslands and forests. As hypothesized, resource supply increased realized productivity and richness, but we found significant differences between ecosystems and study types. Increased richness was associated with increased productivity, although this effect was not seen in experiments. More even communities had lower productivity, indicating that biomass production is often maintained by a few dominant species, and reduced dominance generally reduced ecosystem productivity. This synthesis, which integrates observational and experimental studies in a variety of ecosystems and geographical regions, exposes common patterns and differences in biodiversity-functioning relationships, and increases the mechanistic understanding of changes in ecosystems productivity.

Ocean net heat flux influences seasonal to interannual patterns of plankton abundance.

Changes in the net heat flux (NHF) into the ocean have profound impacts on global climate. We analyse a long-term plankton time-series and show that the NHF is a critical indicator of ecosystem dynamics. We show that phytoplankton abundance and diversity patterns are tightly bounded by the switches between negative and positive NHF over an annual cycle. Zooplankton increase before the transition to positive NHF in the spring but are constrained by the negative NHF switch in autumn. By contrast bacterial diversity is decoupled from either NHF switch, but is inversely correlated (r = -0.920) with the magnitude of the NHF. We show that the NHF is a robust mechanistic tool for predicting climate change indicators such as spring phytoplankton bloom timing and length of the growing season.