Non-linearities, regime shifts and recovery: The recent influence of climate on Black Sea chlorophyll

The Black Sea ecosystem experienced severe eutrophication-related degradation during the 1970s and 1980s. However, in recent years the Black Sea has shown some signs of recovery which are often attributed to a reduction in nutrient loading. Here, SeaWiFS chlorophyll a (chl a), a proxy for phytoplankton biomass, is used to investigate spatio-temporal patterns in Black Sea phytoplankton dynamics and to explore the potential role of climate in the Black Sea's recovery. Maps of chl a anomalies, calculated relative to the 8 year mean, emphasize spatial and temporal variability of phytoplankton biomass in the Black Sea, particularly between the riverine-influenced Northwest Shelf and the open Black Sea. Evolution of phytoplankton biomass has shown significant spatial variability of persistence of optimal bloom conditions between three major regions of the Black Sea. With the exception of 2001, chl a has generally decreased during our 8 year time-series. However, the winter of 2000–2001 was anomalously warm with low wind stress, resulting in reduced vertical mixing of the water column and retention of nutrients in the photic zone. These conditions were associated with anomalously high levels of chl a throughout much of the open Black Sea during the following spring and summer. The unusual climatic conditions occurring in 2001 may have triggered a shift in the Black Sea's chl a regime. The long-term significance of this recent shift is still uncertain but illustrates a non-linear response to climate forcing that makes future ecosystem changes in the pelagic Black Sea ecosystem difficult to predict.

A long-term chlorophyll dataset reveals regime shift in North Sea phytoplankton biomass unconnected to nutrient levels

During the 1980s, a rapid increase in the Phytoplankton Colour Index (PCI), a semiquantitative visual estimate of algal biomass, was observed in the North Sea as part of a regionwide regime shift. Two new data sets created from the relationship between the PCI and SeaWiFS chlorophyll a (Chl a) quantify differences in the previous and current regimes for both the anthropogenically affected coastal North Sea and the comparatively unaffected open North Sea. The new regime maintains a 13% higher Chl a concentration in the open North Sea and a 21% higher concentration in coastal North Sea waters. However, the current regime has lower total nitrogen and total phosphorus concentrations than the previous regime, although the molar N: P ratio in coastal waters is now well above the Redfield ratio and continually increasing. Besides becoming warmer, North Sea waters are also becoming clearer (i.e., less turbid), thereby allowing the normally light-limited coastal phytoplankton to more effectively utilize lower concentrations of nutrients. Linear regression analyses indicate that winter Secchi depth and sea surface temperature are the most important predictors of coastal Chl a, while Atlantic inflow is the best predictor of open Chl a; nutrient concentrations are not a significant predictor in either model. Thus, despite decreasing nutrient concentrations, Chl a continues to increase, suggesting that climatic variability and water transparency may be more important than nutrient concentrations to phytoplankton production at the scale of this study.

Spatio-Temporal Variability of the North Sea Cod Recruitment in Relation to Temperature and Zooplankton

The North Sea cod (Gadus morhua, L.) stock has continuously declined over the past four decades linked with overfishing and climate change. Changes in stock structure due to overfishing have made the stock largely dependent on its recruitment success, which greatly relies on environmental conditions. Here we focus on the spatio-temporal variability of cod recruitment in an effort to detect changes during the critical early life stages. Using International Bottom Trawl Survey (IBTS) data from 1974 to 2011, a major spatio-temporal change in the distribution of cod recruits was identified in the late 1990s, characterized by a pronounced decrease in the central and southeastern North Sea stock. Other minor spatial changes were also recorded in the mid-1980s and early 1990s. We tested whether the observed changes in recruits distribution could be related with direct (i.e. temperature) and/or indirect (i.e. changes in the quantity and quality of zooplankton prey) effects of climate variability. The analyses were based on spatially-resolved time series, i.e. sea surface temperature (SST) from the Hadley Center and zooplankton records from the Continuous Plankton Recorder Survey. We showed that spring SST increase was the main driver for the most recent decrease in cod recruitment. The late 1990s were also characterized by relatively low total zooplankton biomass, particularly of energy-rich zooplankton such as the copepod Calanus finmarchicus, which have further contributed to the decline of North Sea cod recruitment. Long-term spatially-resolved observations were used to produce regional distribution models that could further be used to predict the abundance of North Sea cod recruits based on temperature and zooplankton food availability.

Recruitment in a changing environment: the 2000s North Sea herring recruitment failure

Environmentally induced change appears to be impacting the recruitment of North Sea herring (Clupea harengus). Despite simultaneously having a large adult population, historically low exploitation, and Marine Stewardship Council accreditation (implying sustainability), there have been an unprecedented 6 sequential years of poor juvenile production (recruitment). Analysis suggests that the poor recruitment arises during the larval overwintering phase, with recent survival rates greatly reduced. Contemporary warming of the North Sea has caused significant changes in the plankton community, and a recently identified regime shift around 2000 shows close temporal agreement with the reduced larval survival. It is, therefore, possible that we are observing the first consequences of this planktonic change for higher trophic levels. There is no indication of a recovery in recruitment in the short term. Fishing mortality is currently outside the agreed management plan, and forecasts show a high risk of the stock moving outside safe biological limits soon, potentially precipitating another collapse of the stock. However, bringing the realized fishing mortality back in line with the management plan would likely alleviate the problem. This illustrates again that recruitment is influenced by more than just spawning-stock biomass, and that changes in other factors can be of equal, or even greater, importance. In such dynamically changing environments, recent management success does not necessarily guarantee future sustainability.

The emergence of automated high-frequency flow cytometry: revealing temporal and spatial phytoplankton variability

Phytoplankton observation is the product of a number of trade-offs related to sampling processes, required level of diversity and size spectrum analysis capabilities of the techniques involved. Instruments combining the morphological and high-frequency analysis for phytoplankton cells are now available. This paper presents an application of the automated high-resolution flow cytometer Cytosub as a tool for analysing phytoplanktonic cells in their natural environment. High resolution data from a temporal study in the Bay of Marseille (analysis every 30 min over 1 month) and a spatial study in the Southern Indian Ocean (analysis every 5 min at 10 knots over 5 days) are presented to illustrate the capabilities and limitations of the instrument. Automated high-frequency flow cytometry revealed the spatial and temporal variability of phytoplankton in the size range 1−∼50 μm that could not be resolved otherwise. Due to some limitations (instrumental memory, volume analysed per sample), recorded counts could be statistically too low. By combining high-frequency consecutive samples, it is possible to decrease the counting error, following Poisson’s law, and to retain the main features of phytoplankton variability. With this technique, the analysis of phytoplankton variability combines adequate sampling frequency and effective monitoring of community changes.

Temporal and spatial variation in the Nazaré Canyon (Western Iberian margin): Inter-annual and canyon heterogeneity effects on meiofauna biomass and diversity

The Nazaré Canyon on the Portuguese Margin (NE Atlantic) was sampled during spring-summer for three consecutive years (2005–2007), permitting the first inter-annual study of the meiofaunal communities at the Iberian Margin at two abyssal depths (~3500 m and ~4400 m). Using new and already published data, the meiofauna standing stocks (abundance and biomass) and nematode structural and functional diversity were investigated in relation to the sediment biogeochemistry (e.g. organic carbon, nitrogen, chlorophyll a, phaeopigments) and grain size. A conspicuous increase in sand content from 2005 to 2006 and decrease of phytodetritus at both sites, suggested the occurrence of one or more physical disturbance events. Nematode standing stocks and trophic diversity decreased after these events, seemingly followed by a recovery/recolonisation period in 2007, which was strongly correlated with an increase in the quantity and bioavailability of phytodetrital organic matter supplied. Changes in meiofauna assemblages, however, also differed between stations, likely because of the contrasting hydrodynamic and food supply conditions. Higher meiofauna and nematode abundances, biomass and trophic complexity were found at the shallowest canyon station, where the quantity, quality and bioavailability of food material were higher than at the deeper site. The present results suggest that even though inter-annual variations in the sedimentary environment can regulate the meiofauna in the abyssal Nazaré Canyon, heterogeneity between sampling locations in the canyon were more pronounced.

Lagrangian evolution of DMS during the Southern Ocean gas exchange experiment: The effects of vertical mixing and biological community shift

Concentrations of dimethylsulfide (DMS) and its precursor dimethylsulfoniopropionate (DMSP) are highly variable in time and space. What is driving the variability in DMS(P), and can those variability be explained by physical processes and changes in the biological community? During the Southern Ocean Gas Exchange Experiment (SO GasEx) in the austral fall of 2008, two 3He/SF6 labeled patches were created in the surface water. SF6 and DMS were surveyed continuously in a Lagrangian framework, while direct measurements of air-sea exchange further constrained the gas budgets. Turbulent diffusivity at the base of the mixed layer was estimated from SF6 profiles and used to calculate the vertical fluxes of DMS and nutrients. Increasing mixed layer nutrient concentrations due to mixing were associated with a shift in the phytoplankton community structure, which in turned likely affected the sulfur dynamics on timescales of days. DMS concentration as well as air-sea DMS flux appeared to be decoupled from the DMSP concentration, possibly due to grazing and bacterial DMS production. Contrary to expectations, in an environment with high winds and modest productivity, physical processes (air-sea exchange, photochemistry, vertical mixing) only accounted for a small fraction of DMS loss from the surface water. Among the DMS sinks, inferred biological consumption most likely dominated during SO GasEx.

Impacts of bioturbation on temporal variation in bacterial and archaeal nitrogen-cycling gene abundance in coastal sediments

In marine environments, macrofauna living in or on the sediment surface may alter the structure, diversity and function of benthic microbial communities. In particular, microbial nitrogen (N)-cycling processes may be enhanced by the activity of large bioturbating organisms. Here, we study the effect of the burrowing mud shrimp Upogebia deltaura upon temporal variation in the abundance of genes representing key N-cycling functional guilds. The abundance of bacterial genes representing different N-cycling guilds displayed different temporal patterns in burrow sediments in comparison with surface sediments, suggesting that the burrow provides a unique environment where bacterial gene abundances are influenced directly by macrofaunal activity. In contrast, the abundances of archaeal ammonia oxidizers varied temporally but were not affected by bioturbation, indicating differential responses between bacterial and archaeal ammonia oxidizers to environmental physicochemical controls. This study highlights the importance of bioturbation as a control over the temporal variation in nitrogen-cycling microbial community dynamics within coastal sediments.

On the temporal consistency of chlorophyll products derived from three ocean-colour sensors

Satellite ocean-colour sensors have life spans lasting typically five-to-ten years. Detection of long-term trends in chlorophyll-a concentration (Chl-a) using satellite ocean colour thus requires the combination of different ocean-colour missions with sufficient overlap to allow for cross-calibration. A further requirement is that the different sensors perform at a sufficient standard to capture seasonal and inter-annual fluctuations in ocean colour. For over eight years, the SeaWiFS, MODIS-Aqua and MERIS ocean-colour sensors operated in parallel. In this paper, we evaluate the temporal consistency in the monthly Chl-a time-series and in monthly inter-annual variations in Chl-a among these three sensors over the 2002–2010 time period. By subsampling the monthly Chl-a data from the three sensors consistently, we found that the Chl-a time-series and Chl-a anomalies among sensors were significantly correlated for >90% of the global ocean. These correlations were also relatively insensitive to the choice of three Chl-a algorithms and two atmospheric-correction algorithms. Furthermore, on the subsampled time-series, correlations between Chl-a and time, and correlations between Chl-a and physical variables (sea-surface temperature and sea-surface height) were not significantly different for >92% of the global ocean. The correlations in Chl-a and physical variables observed for all three sensors also reflect previous theories on coupling between physical processes and phytoplankton biomass. The results support the combining of Chl-a data from SeaWiFS, MODIS-Aqua and MERIS sensors, for use in long-term Chl-a trend analysis, and highlight the importance of accounting for differences in spatial sampling among sensors when combining ocean-colour observations.

Basin-scale phenology and effects of climate variability on global timing of initial seaward migration of Atlantic salmon (Salmo salar)

Migrations between different habitats are key events in the lives of many organisms. Such movements involve annually recurring travel over long distances usually triggered by seasonal changes in the environment. Often, the migration is associated with travel to or from reproduction areas to regions of growth. Young anadromous Atlantic salmon (Salmo salar) emigrate from freshwater nursery areas during spring and early summer to feed and grow in the North Atlantic Ocean. The transition from the freshwater (parr') stage to the migratory stage where they descend streams and enter salt water (smolt') is characterized by morphological, physiological and behavioural changes where the timing of this parr-smolt transition is cued by photoperiod and water temperature. Environmental conditions in the freshwater habitat control the downstream migration and contribute to within- and among-river variation in migratory timing. Moreover, the timing of the freshwater emigration has likely evolved to meet environmental conditions in the ocean as these affect growth and survival of the post-smolts. Using generalized additive mixed-effects modelling, we analysed spatio-temporal variations in the dates of downstream smolt migration in 67 rivers throughout the North Atlantic during the last five decades and found that migrations were earlier in populations in the east than the west. After accounting for this spatial effect, the initiation of the downstream migration among rivers was positively associated with freshwater temperatures, up to about 10 degrees C and levelling off at higher values, and with sea-surface temperatures. Earlier migration occurred when river discharge levels were low but increasing. On average, the initiation of the smolt seaward migration has occurred 2.5days earlier per decade throughout the basin of the North Atlantic. This shift in phenology matches changes in air, river, and ocean temperatures, suggesting that Atlantic salmon emigration is responding to the current global climate changes.

Spatio-temporal variability in ammonia oxidation and ammonia oxidising bacteria and archaea in coastal sediments of the Western English Channel

The abundance of ammonia-oxidising bacterial (AOB) and ammonia-oxidising archaeal (AOA) (amoA) genes and ammonia oxidation rates were compared bimonthly from July 2008 to May 2011 in 4 contrasting coastal sediments in the western English Channel. Despite a higher abundance of AOA amoA genes within all sediments and at all time-points, rates of ammonia oxidation correlated with AOB and not AOA amoA gene abundance. Sediment type was a major factor in determining both AOB amoA gene abundance and AOB community structure, possibly due to deeper oxygen penetration into the sandier sediments, increasing the area available for ammonia oxidation. Decreases in AOB amoA gene abundance were evident during summer and autumn, with maximum abundance and ammonia oxidation rates occurring in winter and early spring. PCR-DGGE of AOB amoA genes indicated that no seasonal changes to community composition occurred; however, a gradual movement in community composition occurred at 3 of the sites studied. The lack of correlation between AOA amoA gene abundance and ammonium oxidation rates, or any other environmental variable measured, may be related to the higher spatial variation amongst measurements, obscuring temporal trends, or the bimonthly sampling, which may have been too infrequent to capture temporal variability in the deposition of fresh organic matter. Alternatively, AOA may respond to changing substrate concentrations by an increase or decrease in transcript rather than gene abundance.

Temporal changes in total and size-fractioned chlorophyll-a in surface waters of three provinces in the Atlantic Ocean (September to November) between 2003 and 2010

Phytoplankton total chlorophyll concentration (TCHLa) and phytoplankton size structure are two important ecological indicators in biological oceanography. Using high performance liquid chromatography (HPLC) pigment data, collected from surface waters along the Atlantic Meridional Transect (AMT), we examine temporal changes in TCHLa and phytoplankton size class (PSC: micro-, nano- and pico-phytoplankton) between 2003 and 2010 (September to November cruises only), in three ecological provinces of the Atlantic Ocean. The HPLC data indicate no significant change in TCHLa in northern and equatorial provinces, and an increase in the southern province. These changes were not significantly different to changes in TCHLa derived using satellite ocean-colour data over the same study period. Despite no change in AMT TCHLa in northern and equatorial provinces, significant differences in PSC were observed, related to changes in key diagnostic pigments (fucoxanthin, peridinin, 19′-hexanoyloxyfucoxanthin and zeaxanthin), with an increase in small cells (nano- and pico-phytoplankton) and a decrease in larger cells (micro-phytoplankton). When fitting a three-component model of phytoplankton size structure — designed to quantify the relationship between PSC and TCHLa to each AMT cruise, model parameters varied over the study period. Changes in the relationship between PSC and TCHLa have wide implications in ecology and marine biogeochemistry, and provide key information for the development and use of empirical ocean-colour algorithms. Results illustrate the importance of maintaining a time-series of in-situ observations in remote regions of the ocean, such as that acquired in the AMT programme.

Fundamental shift in vitamin B12 eco-physiology of a model alga demonstrated by experimental evolution.

A widespread and complex distribution of vitamin requirements exists over the entire tree of life, with many species having evolved vitamin dependence, both within and between different lineages. Vitamin availability has been proposed to drive selection for vitamin dependence, in a process that links an organism's metabolism to the environment, but this has never been demonstrated directly. Moreover, understanding the physiological processes and evolutionary dynamics that influence metabolic demand for these important micronutrients has significant implications in terms of nutrient acquisition and, in microbial organisms, can affect community composition and metabolic exchange between coexisting species. Here we investigate the origins of vitamin dependence, using an experimental evolution approach with the vitamin B(12)-independent model green alga Chlamydomonas reinhardtii. In fewer than 500 generations of growth in the presence of vitamin B(12), we observe the evolution of a B(12)-dependent clone that rapidly displaces its ancestor. Genetic characterization of this line reveals a type-II Gulliver-related transposable element integrated into the B(12)-independent methionine synthase gene (METE), knocking out gene function and fundamentally altering the physiology of the alga.

Temporal variability in total, micro- and nano-phytoplankton primary production at a coastal site in the Western English Channel

Primary productivity and subsequent carbon cycling in the coastal zone have a significant impact on the global carbon budget. It is currently unclear how anthropogenic activity could alter these budgets but long term coastal time series of hydrological, biogeochemical and biological measurements represent a key means to better understand past drivers, and hence to predicting future seasonal and inter-annual variability in carbon fixation in coastal ecosystems. An 8-year time series of primary production from 2003 to 2010, estimated using a recently developed absorption-based algorithm, was used to determine the nature and extent of change in primary production at a coastal station (L4) in the Western English Channel (WEC). Analysis of the seasonal and inter-annual variability in production demonstrated that on average, nano- and pico-phytoplankton account for 48% of the total carbon fixation and micro-phytoplankton for 52%. A recent decline in the primary production of nano- and pico-phytoplankton from 2005 to 2010 was observed, corresponding with a decrease in winter nutrient concentrations and a decrease in the biomass of Phaeocystis sp. Micro-phytoplankton primary production (PPM) remained relatively constant over the time series and was enhanced in summer during periods of high precipitation. Increases in sea surface temperature, and decreases in wind speeds and salinity were associated with later spring maxima in PPM. Together these trends indicate that predicted increases in temperature and decrease in wind speeds in future would drive later spring production whilst predicted increases in precipitation would also continue these blooms throughout the summer at this site.

Spatio-temporal Bayesian network models with latent variables for revealing trophic dynamics and functional networks in fisheries ecology

Ecosystems consist of complex dynamic interactions among species and the environment, the understanding of which has implications for predicting the environmental response to changes in climate and biodiversity. However, with the recent adoption of more explorative tools, like Bayesian networks, in predictive ecology, few assumptions can be made about the data and complex, spatially varying interactions can be recovered from collected field data. In this study, we compare Bayesian network modelling approaches accounting for latent effects to reveal species dynamics for 7 geographically and temporally varied areas within the North Sea. We also apply structure learning techniques to identify functional relationships such as prey–predator between trophic groups of species that vary across space and time. We examine if the use of a general hidden variable can reflect overall changes in the trophic dynamics of each spatial system and whether the inclusion of a specific hidden variable can model unmeasured group of species. The general hidden variable appears to capture changes in the variance of different groups of species biomass. Models that include both general and specific hidden variables resulted in identifying similarity with the underlying food web dynamics and modelling spatial unmeasured effect. We predict the biomass of the trophic groups and find that predictive accuracy varies with the models' features and across the different spatial areas thus proposing a model that allows for spatial autocorrelation and two hidden variables. Our proposed model was able to produce novel insights on this ecosystem's dynamics and ecological interactions mainly because we account for the heterogeneous nature of the driving factors within each area and their changes over time. Our findings demonstrate that accounting for additional sources of variation, by combining structure learning from data and experts' knowledge in the model architecture, has the potential for gaining deeper insights into the structure and stability of ecosystems. Finally, we were able to discover meaningful functional networks that were spatially and temporally differentiated with the particular mechanisms varying from trophic associations through interactions with climate and commercial fisheries.