Drivers and effects of Karenia mikimotoi blooms in the western English Channel

Naturally occurring red tides and harmful algal blooms (HABs) are of increasing importance in the coastal environment and can have dramatic effects on coastal benthic and epipelagic communities worldwide. Such blooms are often unpredictable, irregular or of short duration, and thus determining the underlying driving factors is problematic. The dinoflagellate Karenia mikimotoi is an HAB, commonly found in the western English Channel and thought to be responsible for occasional mass finfish and benthic mortalities. We analysed a 19-year coastal time series of phytoplankton biomass to examine the seasonality and interannual variability of K. mikimotoi in the western English Channel and determine both the primary environmental drivers of these blooms as well as the effects on phytoplankton productivity and oxygen conditions. We observed high variability in timing and magnitude of K. mikimotoi blooms, with abundances reaching >1000 cells mL�1 at 10 m depth, inducing up to a 12-fold increase in the phytoplankton carbon content of the water column. No long-term trends in the timing or magnitude of K. mikimotoi abundance were evident from the data. Key driving factors were identified as persistent summertime rainfall and the resultant input of low-salinity high-nutrient river water. The largest bloom in 2009 was associated with highest annual primary production and led to considerable oxygen depletion at depth, most likely as a result of enhanced biological breakdown of bloom material; however, this oxygen depletion may not affect zooplankton. Our data suggests that K. mikimotoi blooms are not only a key and consistent feature of western English Channel productivity, but importantly can potentially be predicted from knowledge of rainfall or river discharge.

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.

Investigation of benthic community change over a century-wide scale in the western English Channel

Since the early part of the 20th Century the impact of a range of anthropogenic activities in our coastal seas has steadily increased. The effect of such activities is a major cause for concern but in the benthic environment few studies exist that date back more than a few decades. Hence understanding long term changes is a challenge. Within this study we utilized a historic benthic dataset and resurveyed an area west of Eddystone reef in the English Channel previously investigated 112 years ago. The aim of the present work was to describe the current benthic community structure and investigate potential differences between 1895 and 2007. For each of the four major phyla investigated (Polychaeta, Crustacea, Mollusca and Echinodermata), multivariate community analysis showed significant differences between the historic and contemporary surveys. Echinoderm diversity showed a clear reduction between 1895 and 2007. The sea urchins Echinus esculentus, Spatangus purpureus, and Psammechinus miliaris and large star-fish Marthasterias glacialis showed reductions in abundance, in some cases being entirely absent from the survey area in 2007. Polychaetes showed a shift from tubiculous species to small errant and predatory species such as Glycera, Nephtys, and Lumbrineris spp. Within the group Mollusca large species such as Pecten maximus and Laevicardium crassum decreased in abundance while small species increased. Crustaceans in 1895 were dominated by crab species which were present in similar abundances in 2007, but, the order Amphipoda appeared to show a significant increase. While some of the differences observed could stem from differences in methodologies between the surveys, in particular increases of small cryptic species, the loss of large conspicuous species was judged to be genuine. The study area is an important beam trawling and scallop dredging ground; the differences observed are concomitant with changes generally associated with disturbance from demersal fishing activities such as these.

Long-term variability of the siphonophores Muggiaea atlantica and M. kochi in the Western English Channel

We investigated long-term variability of the calycophoran siphonophores Muggiaea atlantica and Muggiaea kochi in the Western English Channel (WEC) between 1930 and 2011. Our aims were to describe long-term changes in abundance and temporal distribution in relation to local environmental dynamics. In order to better understand mechanisms that regulate the species’ populations, we identified periods that were characteristic of in situ population growth and the environmental optima associated with these events. Our results show that between 1930 and the 1960s both M. atlantica and M. kochi were transient components of the WEC ecosystem. In the late 1960s M. atlantica, successfully established a resident population in the WEC, while the occurrence of M. kochi became increasingly sporadic. Once established as a resident species, the seasonal abundance and distribution of M. atlantica increased. Analysis of environmental conditions associated with in situ population growth revealed that temperature and prey were key determinants of the seasonal distribution and abundance of M. atlantica. Salinity was shown to have an indirect effect, likely representing a proxy for water circulation in the WEC. Anomalies in the seasonal cycle of salinity, indicating deviation from the usual circulation pattern in the WEC, were negatively associated with in situ growth, suggesting dispersal of the locally developing M. atlantica population. However, our findings identified complexity in the relationship between characteristics of the environment and M. atlantica variability. The transition from a period of transiency (1930–1968) to residency (1969–2011) was tentatively attributed to structural changes in the WEC ecosystem that occurred under the forcing of wider-scale hydroclimatic changes.

Dynamics of air–sea CO2 fluxes in the northwestern European shelf based on voluntary observing ship and satellite observations

From January 2011 to December 2013, we constructed a comprehensive pCO2 data set based on voluntary observing ship (VOS) measurements in the western English Channel (WEC). We subsequently estimated surface pCO2 and air–sea CO2 fluxes in northwestern European continental shelf waters using multiple linear regressions (MLRs) from remotely sensed sea surface temperature (SST), chlorophyll a concentration (Chl a), wind speed (WND), photosynthetically active radiation (PAR) and modeled mixed layer depth (MLD). We developed specific MLRs for the seasonally stratified northern WEC (nWEC) and the permanently well-mixed southern WEC (sWEC) and calculated surface pCO2 with uncertainties of 17 and 16 μatm, respectively. We extrapolated the relationships obtained for the WEC based on the 2011–2013 data set (1) temporally over a decade and (2) spatially in the adjacent Celtic and Irish seas (CS and IS), two regions which exhibit hydrographical and biogeochemical characteristics similar to those of WEC waters. We validated these extrapolations with pCO2 data from the SOCAT and LDEO databases and obtained good agreement between modeled and observed data. On an annual scale, seasonally stratified systems acted as a sink of CO2 from the atmosphere of −0.6 ± 0.3, −0.9 ± 0.3 and −0.5 ± 0.3 mol C m−2 yr−1 in the northern Celtic Sea, southern Celtic sea and nWEC, respectively, whereas permanently well-mixed systems acted as source of CO2 to the atmosphere of 0.2 ± 0.2 and 0.3 ± 0.2 mol C m−2 yr−1 in the sWEC and IS, respectively. Air–sea CO2 fluxes showed important inter-annual variability resulting in significant differences in the intensity and/or direction of annual fluxes. We scaled the mean annual fluxes over these provinces for the last decade and obtained the first annual average uptake of −1.11 ± 0.32 Tg C yr−1 for this part of the northwestern European continental shelf. Our study showed that combining VOS data with satellite observations can be a powerful tool to estimate and extrapolate air–sea CO2 fluxes in sparsely sampled area.

The combined effects of seasonal community succession and adaptive algal physiology on lipid profiles of coastal phytoplankton in the western English channel

Lipids are key constituents of marine phytoplankton, and some fatty acids (key constituents of lipids) are essential dietary components for secondary producers. However, in natural marine ecosystems the interactions of factors affecting seasonal phytoplankton lipid composition are still poorly understood. The aim of this study was to assess the roles of seasonal succession in phytoplankton community composition and nutrient concentrations, on the lipid composition of the phytoplankton community. Fatty acid and polar lipid composition in seston was measured in surface waters at the time series station L4, an inshore station in the Western English Channel, from January to December 2013. Redundancy analyses (RDA) were used to identify factors (abiotic and biotic) that explained the seasonal variability in phytoplankton lipids. RDA demonstrated that nutrients (namely nitrogen) explained the majority of variation in phytoplankton lipid composition, as well as a smaller explanatory contribution from changes in phytoplankton community composition. The physiological adaptations of the phytoplankton community to nutrient deplete conditions during the summer season when the water column was stratified, was further supported by changes in the polar lipid to phytoplankton biomass ratios (also modelled with RDA) and increases in the lipid to chlorophyll a ratios, which are both indicative of nutrient stress. However, the association of key fatty acid markers with phytoplankton groups e.g. 22:6 n-3 and dinoflagellate biomass (predominant in summer), meant there were no clear seasonal differences in the overall degree of fatty acid saturation, as might have been expected from typical nutrient stress on phytoplankton. Based on the use of polyunsaturated fatty acids (PUFA) as markers of ‘food quality’ for grazers, our results suggest that in this environment high food quality is maintained throughout summer, due to seasonal succession towards flagellated phytoplankton species able to maintain PUFA synthesis under surface layer nutrient depletion.

Feeding rates and prey selectivity of planktonic decapod larvae in the Western English Channel

Meroplankton are seasonally important contributors to the zooplankton, particularly at inshore sites, yet their feeding ecology is poorly known relative to holoplankton. While several studies have measured feeding in decapod larvae, few studies have examined the feeding rates of decapod larvae on natural prey assemblages throughout the reproductive season. We conducted 8 feeding experiments with Necora puber, Liocarcinus spp. and Upogebia spp. zoea larvae collected from the L4 monitoring site off Plymouth (50°15.00′N, 4°13.02′W) during spring–summer 2009 and 2010. This period spanned moderate-to-high food availability (0.5–1.6 µg chl-a L−1), but a great range in food composition with small cells <20 µm dominating in 2010. Daily rations averaged 17, 60 and 22 % of body C for the 3 respective decapod species. Clearance rates differed according to prey type, and all 3 decapod genera showed evidence of selection of dinoflagellates. Importantly, small cells including nano- and pico-plankton were ingested, this being demonstrated independently by flow cytometric analysis of the feeding experiments and molecular analysis. PCR-based analysis of the haptophyte portion of the diet revealed ingestion of Isochrysis galbana by decapod larvae in the bottle incubations and Isochrysis galbana and Phaeocystis globosa by decapod larvae collected directly from the field. This study has shown that pico- and nano-sized plankton form an important supplement to the diverse and variable diet of decapod larvae.

Feeding selectivity of bivalve larvae on natural plankton assemblages in the Western English Channel

Meroplankton, including bivalve larvae, are an important and yet understudied component of coastal marine food webs. Understanding the baseline of meroplankton ecology is imperative to establish and predict their sensitivity to local and global marine stressors. Over an annual cycle (October 2009–September 2010), bivalve larvae were collected from the Western Channel Observatory time series station L4 (50°15.00′N, 4°13.02′W). The morphologically similar larvae were identified by analysis of the 18S nuclear small subunit ribosomal RNA gene, and a series of incubation experiments were conducted to determine larval ingestion rates on natural plankton assemblages. Complementary gut content analysis was performed using a PCR-based method for detecting prey DNA both from field-collected larvae and those from the feeding experiments. Molecular identification of bivalve larvae showed the community composition to change over the course of the sampling period with domination by Phaxas in winter and higher diversity in autumn. The larvae selected for nanoeukaryotes (2–20 µm) including coccolithophores (<20 µm) which together comprised >75 % of the bivalve larvae diet. Additionally, a small percentage of carbon ingested originated from heterotrophic ciliates (<30 µm). The molecular analysis of bivalve larvae gut content provided increased resolution of identification of prey consumed and demonstrated that the composition of prey consumed established through bottle incubations conferred with that established from in situ larvae. Despite changes in bivalve larvae community structure, clearance rates of each prey type did not change significantly over the course of the experiment, suggesting different bivalve larvae species may consume similar prey.

How does Calanus helgolandicus maintain its population in a variable environment? Analysis of a 25-year time series from the English Channel

Calanus helgolandicus is a key copepod of the NE Atlantic and fringing shelves, with a distribution that is expanding northwards with oceanic warming. The Plymouth L4 site has warmed over the past 25-years, and experiences large variations in the timing and availability of food for C. helgolandicus. Here we examine the degree to which these changes translate into variation in reproductive output and subsequently C. helgolandicus population size. Egg production rates (eggs female−1 day−1) were maximal in the spring to early-summer period of diatom blooms and high ciliate abundance, rather than during the equally large autumn blooms of autotrophic dinoflagellates. Egg hatch success was lower in spring however, with a greater proportion of naupliar deformities then also. Both the timing and the mean summer abundance of C. helgolandicus (CI–CVI) reflected those of spring total reproductive output. However this relationship was driven by inter-annual variability in female abundance and not that of egg production per female, which ranged only two-fold. Winter abundance of C. helgolandicus at L4 was much more variable than abundance in other seasons, and reflected conditions from the previous growing season. However, these low winter abundances had no clear carry-over signal to the following season’s population size. Overall, the C. helgolandicus population appears to be surprisingly resilient at this dynamic, inshore site, showing no long-term phenology shift and only a four-fold variation in mean abundance between years. This dampening effect may reflect a series of mortality sources, associated with the timing of stratification in the early part of the season, likely affecting egg sinking and loss, plus intense, density-dependent mortality of early stages in mid-summer likely through predation.

Abundance of a chlorophyll a precursor and the oxidation product hydroxychlorophyll a during seasonal phytoplankton community progression in the Western English Channel

This study presents the first in-situ measurements of the chlorophyll a oxidation product, hydroxychlorophyll a as well as the chlorophyll a precursor, chlorophyll aP276 conducted over an annual cycle. Chlorophyll a oxidation products, such as hydroxychlorophyll a may be associated with the decline of algal populations and can act as an initial step in the degradation of chlorophyll a into products which can be found in the geochemical record, important for studying past climate change events. Here, hydroxychlorophyll a and chlorophyll aP276 were measured at the long-term monitoring station L4, Western Channel Observatory (UK, www.westernchannelobservatory.org) over an annual cycle (2012). Weekly measurements of phytoplankton species composition and abundance enabled detailed analysis of possible sources of hydroxychlorophyll a. Dinoflagellates, 2 diatom species, the prymnesiophyte Phaeocystis spp. and the coccolithophorid Emiliania huxleyi were all associated with hydroxychlorophyll a occurrence. However, during alternate peaks in abundance of the diatoms, no association with hydroxychlorophyll a occurred, indicating that the oxidation of chlorophyll a was dependant not only on species but also on additional factors such as the mode of mortality, growth limiting factor (i.e. nutrient concentration) or phenotypic plasticity. Surface sediment samples contained 10 times more hydroxychlorophyll a (relative to chlorophyll a) than pelagic particulate samples, indicating that more chlorophyll a oxidation occurred during sedimentation or at the sediment–water interface, than in the pelagic environment. In addition, chlorophyll aP276 correlated with chl-a concentration, thus supporting its assignment as a chl-a precursor.

Dynamic responses of the benthic bacterial community at the Western English Channel observatory site L4 are driven by deposition of fresh phytodetritus

The impact of the seasonal deposition of phytoplankton and phytodetritus on surface sediment bacterial abundance and community composition was investigated at the Western English Channel site L4. Sediment and water samples were collected from January to September in 2012, increasing in frequency during periods of high water column phytoplankton abundance. Compared to the past two decades, the spring bloom in 2012 was both unusually long in duration and contained higher than average biomass. Within spring months, the phytoplankton bloom was well mixed through the water column and showed accumulations near the sea bed, as evidenced by flow cytometry measurements of nanoeukaryotes, water column chlorophyll a and the appearance of pelagic phytoplankton at the sediment. Measurements of chlorophyll and chlorophyll degradation products indicated phytoplankton material was heavily degraded after it reached the sediment surface: the nature of the chlorophyll degradation products (predominantly pheophorbide, pyropheophorbide and hydroxychlorophyllone) was indicative of grazing activity. The abundance of bacterial 16S rRNA genes g−1 sediment (used as a proxy for bacterial biomass) increased markedly with the onset of the phytoplankton bloom, and correlated with measurements of chlorophyll at the surface sediment. Together, this suggests that bacteria may have responded to nutrients released via grazing activity. In depth sequencing of the 16S rRNA genes indicated that the composition of the bacterial community shifted rapidly through-out the prolonged spring bloom period. This was primarily due to an increase in the relative sequence abundance of Flavobacteria.