On the roles of cell size and trophic strategy in North Atlantic diatom and dinoflagellate communities

We have examined the inter- and intra-group seasonal succession of 113 diatom and dinoflagellate taxa, as surveyed by the Continuous Plankton Recorder (CPR) in the North Atlantic, by grouping taxa according to two key functional traits: cell size (mg C cell21) and trophic strategy (photoautotrophy, mixotrophy, or heterotrophy). Mixotrophic dinoflagellates follow photoautotrophic diatoms but precede their obligate heterotrophic counterparts in the succession because of the relative advantages afforded by photosynthesizing when light and nutrients are available in spring. The mean cell size of the sampled diatoms is smallest in the summer, likely because of the higher specific nutrient affinity of smaller relative to larger cells. Contrastingly, we hypothesize that mixotrophy diminishes the size selection based on nutrient limitation and accounts for the lack of a seasonal size shift among surveyed dinoflagellates. Relatively small, heterotrophic dinoflagellates (mg C cell21 , 1023) peak after other, larger dinoflagellates, in part because of the increased abundance of their small prey during nutrientdeplete summer months. The largest surveyed diatoms (mg C cell21 . 1022) bloom later than others, and we hypothesize that this may be because of their relatively slow maximum potential growth rates and high internal nutrient storage, as well as to the slower predation of these larger cells. The new trait database and analysis presented here helps translate the taxonomic information of the CPR survey into metrics that can be directly compared with trait-based models.

Latitudinal phytoplankton distribution and the neutral theory of biodiversity

Aim Recent studies have suggested that global diatom distributions are not limited by dispersal, in the case of both extant species and fossil species, but rather that environmental filtering explains their spatial patterns. Hubbell's neutral theory of biodiversity provides a framework in which to test these alternatives. Our aim is to test whether the structure of marine phytoplankton (diatoms, dinoflagellates and coccolithophores) assemblages across the Atlantic agrees with neutral theory predictions. We asked: (1) whether intersite variance in phytoplankton diversity is explained predominantly by dispersal limitation or by environmental conditions; and (2) whether species abundance distributions are consistent with those expected by the neutral model. Location Meridional transect of the Atlantic (50 degrees N50 degrees S). Methods We estimated the relative contributions of environmental factors and geographic distance to phytoplankton composition using similarity matrices, Mantel tests and variation partitioning of the species composition based upon canonical ordination methods. We compared the species abundance distribution of phytoplankton with the neutral model using Etienne's maximum-likelihood inference method. Results Phytoplankton communities are slightly more determined by niche segregation (24%), than by dispersal limitation and ecological drift (17%). In 60% of communities, the assumption of neutrality in species' abundance distributions could not be rejected. In tropical zones, where oceanic gyres enclose large stable water masses, most communities showed low species immigration rates; in contrast, we infer that communities in temperate areas, out of oligotrophic gyres, have higher rates of species immigration. Conclusions Phytoplankton community structure is consistent with partial niche assembly and partial dispersal and drift assembly (neutral processes). The role of dispersal limitation is almost as important as habitat filtering, a fact that has been largely overlooked in previous studies. Furthermore, the polewards increase in immigration rates of species that we have discovered is probably caused by water mixing conditions and productivity.

Temporal changes in plankton of the North Sea: community shifts and environmental drivers

This paper analyses long-term and seasonal changes in the North Sea plankton community during the period 1970 to 2008. Based on Continuous Plankton Recorder (CPR) data covering 38 yr, major changes in both phytoplankton and zooplankton abundance and community structure were identified. Regime changes were detected around 1978, 1989 and 1998. The first 2 changes have been discussed in the literature and are defined as a cold episodic event (1978) and a regime shift towards a warm dynamic regime (1989). The effect of these 2 regime changes on plankton indicators was assessed and checked against previous studies. The 1998 change represents a shift in the abundance and seasonal patterns of dinoflagellates and the dominant zooplankton group, the neritic copepods. Furthermore, environmental factors such as air temperature, wind speed and the North Atlantic water inflow were identified as potential drivers of change in seasonal patterns, and the most-likely environmental causes for detected changes were assessed. We suggest that a change in the balance of dissolved nutrients driven by these environmental factors was the cause of the latest change in plankton community structure, which in turn could have affected the North Sea fish community.

Feeding of Calanus finmarchicus and Oithona similis on the microplankton assemblage in the Irminger Sea, North Atlantic

The present investigation reviews published data on the feeding rates and prey selection of Oithona similis females, Calanus finmarchicus nauplii and females in the Irminger Sea in April/May and July/August 2002. Our aim was to examine how the feeding rates and prey selection of these three copepod stages respond to concomitant changes in microplankton community composition and prey abundance. Copepods typically ingested prey overall according to its ambient concentration although significant species and stage-specific differences in prey-type ingestion and selection were apparent. Despite being of comparable weight, the ingestion rates of C. finmarchicus nauplii were always higher than those of the O. similis females. Moreover, C. finmarchicus nauplii and O. similis females fed preferentially on diatoms and ciliates respectively, whereas adult female C. finmarchicus showed limited prey selectivity. Copepod grazing impact on total and on ciliates/dinoflagellates standing stock was <0.5 and <2%, respectively. We attribute this result to a combination of low grazing rates, low copepod abundance and low microplankton biomass, all of which are indicative of the non-bloom conditions under which these experiments were conducted. The differences in copepod feeding rates and prey selection we report reflect species and stage-specific eco-physiological adaptations, which may act as important driving forces for marine ecosystem structuring and functioning.

Changes in marine dinoflagellate and diatom abundance under climate change

Marine diatoms and dinoflagellates play a variety of key ecosystem roles as important primary producers (diatoms and some dinoflagellates) and grazers (some dinoflagellates). Additionally some are harmful algal bloom (HAB) species and there is widespread concern that HAB species may be increasing accompanied by major negative socio-economic impacts, including threats to human health and marine harvesting1, 2. Using 92,263 samples from the Continuous Plankton Recorder survey, we generated a 50-year (1960–2009) time series of diatom and dinoflagellate occurrence in the northeast Atlantic and North Sea. Dinoflagellates, including both HAB taxa (for example, Prorocentrum spp.) and non-HAB taxa (for example, Ceratium furca), have declined in abundance, particularly since 2006. In contrast, diatom abundance has not shown this decline with some common diatoms, including both HAB (for example, Pseudo-nitzschia spp.) and non-HAB (for example, Thalassiosira spp.) taxa, increasing in abundance. Overall these changes have led to a marked increase in the relative abundance of diatoms versus dinoflagellates. Our analyses, including Granger tests to identify criteria of causality, indicate that this switch is driven by an interaction effect of both increasing sea surface temperatures combined with increasingly windy conditions in summer.

Spatial variability of the plankton trophic interaction in the North Sea: a new feature after the early 1970s

Traditionally, marine ecosystem structure was thought to be bottom-up controlled. In recent years, a number of studies have highlighted the importance of top-down regulation. Evidence is accumulating that the type of trophic forcing varies temporally and spatially, and an integrated view – considering the interplay of both types of control – is emerging. Correlations between time series spanning several decades of the abundances of adjacent trophic levels are conventionally used to assess the type of control: bottom-up if positive or top-down if this is negative. This approach implies averaging periods which might show time-varying dynamics and therefore can hide part of this temporal variability. Using spatially referenced plankton information extracted from the Continuous Plankton Recorder, this study addresses the potential dynamic character of the trophic structure at the planktonic level in the North Sea by assessing its variation over both temporal and spatial scales. Our results show that until the early-1970s a bottom-up control characterized the base of the food web across the whole North Sea, with diatoms having a positive and homogeneous effect on zooplankton filter-feeders. Afterwards, different regional trophic dynamics were observed, in particular a negative relationship between total phytoplankton and zooplankton was detected off the west coast of Norway and the Skagerrak as opposed to a positive one in the southern reaches. Our results suggest that after the early 1970s diatoms remained the main food source for zooplankton filter-feeders east of Orkney–Shetland and off Scotland, while in the east, from the Norwegian Trench to the German Bight, filter-feeders were mainly sustained by dinoflagellates.

Identifying four phytoplankton functional types from space: An ecological approach

Deriving maps of phytoplankton taxa based on remote sensing data using bio-optical properties of phytoplankton alone is challenging. A more holistic approach was developed using artificial neural networks, incorporating ecological and geographical knowledge together with ocean color, bio-optical characteristics, and remotely sensed physical parameters. Results show that the combined remote sensing approach could discriminate four major phytoplankton functional types (diatoms, dinoflagellates, coccolithophores, and silicoflagellates) with an accuracy of more than 70%. Models indicate that the most important information for phytoplankton functional type discrimination is spatio-temporal information and sea surface temperature. This approach can supply data for large-scale maps of predicted phytoplankton functional types, and an example is shown.

Variability in phytoplankton community structure in response to the North Atlantic Oscillation and implications for organic carbon flux

The North Atlantic Oscillation (NAO) is a major mode of variability in the North Atlantic, dominating atmospheric and oceanic conditions. Here, we examine the phytoplankton community-structure response to the NAO using the Continuous Plankton Recorder data set. In the Northeast Atlantic, in the transition region between the gyres, variability in the relative influence of subpolar or subtropical-like conditions is reflected in the physical environment. During positive NAO periods, the region experiences subpolar-like conditions, with strong wind stress and deep mixed layers. In contrast, during negative NAO periods, the region shifts toward more subtropical-like conditions. Diatoms dominate the phytoplankton community in positive NAO periods, whereas in negative NAO periods, dinoflagellates outcompete diatoms. The implications for interannual variability in deep ocean carbon flux are examined using data from the Porcupine Abyssal Plain time-series station. Contrary to expectations, carbon flux to 3000 m is enhanced when diatoms are outcompeted by other phytoplankton functional types. Additionally, highest carbon fluxes were not associated with an increase in biomineral content, which implies that ballasting is not playing a dominant role in controlling the flux of material to the deep ocean in this region. In transition zones between gyre systems, phytoplankton populations can change in response to forcing induced by opposing NAO phases.

Evaluating The Ribosomal Internal Transcribed Spacer (ITS) as a Candidate Dinoflagellate Barcode Marker

DNA barcoding offers an efficient way to determine species identification and to measure biodiversity. For dinoflagellates, an ancient alveolate group of about 2000 described extant species, DNA barcoding studies have revealed large amounts of unrecognized species diversity, most of which is not represented in culture collections. To date, two mitochondrial gene markers, Cytochrome Oxidase I (COI) and Cytochrome b oxidase (COB), have been used to assess DNA barcoding in dinoflagellates, and both failed to amplify all taxa and suffered from low resolution. Nevertheless, both genes yielded many examples of morphospecies showing cryptic speciation and morphologically distinct named species being genetically similar, highlighting the need for a common marker. For example, a large number of cultured Symbiodinium strains have neither taxonomic identification, nor a common measure of diversity that can be used to compare this genus to other dinoflagellates.

Ecological Investigations with the Continuous Plankton Recorder: The Phytoplankton in the Southern North Sea. 1932-37.

1. The changes in the composition and distribution of the plankton of the southern North Sea have been investigated month by month, from June 1932 to December 1937; the present report deals with the phytoplankton. The survey was carried out by the Continuous Plankton Recorder, towed at a standard depth of 10 metres, by ships on regular steamship lines across the North Sea from Hull towards the Skagerrak, to Bremen and to Rotterdam, and later between London and Esbjerg. 2. The material and methods are described, together with a discussion on the validity of this type of survey and some comparison of its results with those obtained by other methods (pp. 76-86). 3. Particular attention has been paid to Rhizosolenia styliformis (pp. 92- 107), Biddulphia sinensis (pp. 108-115), Phaeocystis (pp. 149-153), and the Dinoflagellates (pp. 134-149); of these the first three are known to be of particular importance in relation to the herring fisheries. More generalised data are available for the principal diatoms other than R. styliformis and B. sinensis (pp. 116-134). 4. The main part of the work is an ecological study of the phytoplankton changes in time and space over the 5½ years. Each year is marked by some distinct variations in the abundance and the times of increase, maximum numbers and decline as recorded in the different forms. These variations in the annual cycles are compared on the different lines by a series of graphs arranged against a time scale of months, a set for each year being placed side by side (Plates I-XXI). More detailed studies by more frequent records were made in the autumns of 1934, 1935, 1936 and 1937 (cf. Figs. 3 and 4). The changes in spatial distribution are shown by a series of monthly maps arranged in a similar manner for each year (Plates XXII-LXIV). These intensive studies of the changes in time and space are also intended to form the basis for correlations with other features in the general ecology of the area (e. g. the zooplankton, hydrology, meteorology and fisheries) to be made in later publications. 5. Whilst each form has shown its own peculiar features, a trend towards a general increase in the phytoplankton as a whole has been observed during the period, although the years 1934 and 1936 have in some respects shown deviations and regressive features, and not all organisms have revealed the same trend. The possible relation of this gradual trend to other events observed in recent years in these and neighbouring waters is discussed (pp. 162-167). 6. The application of these results to the study of patchiness (pp. 154-158), inter-relationships in the plankton (pp. 159-160) and to water movements (pp. 160-162) is briefly discussed.

Effects of increases in temperature and nutrients on phytoplankton community structure and photosynthesis in the Western English Channel

Anthropogenic climate change is exerting pressures on coastal ecosystems through increases in temperature, precipitation and ocean acidification. Phytoplankton community structure and photo-physiology are therefore adapting to these conditions. Changes in phytoplankton biomass and photosynthesis in relation to temperature and nutrient concentrations were assessed using a 14 year dataset from a coastal station in the Western English Channel (WEC). Dinoflagellate and coccolithophorid biomass exhibited a positive correlation with temperature, reaching the highest biomass at between 15 and 17°C. Diatoms showed a negative correlation with temperature, with highest biomass at 10°C. Chlorophyll a (chl a) normalised light-saturated photosynthetic rates (PBm) exhibited a hyperbolic response to increasing temperature, with an initial linear increase from 8 to 11°C, and reaching a plateau from 12°C. There was however no significant positive correlation between nutrients and phytoplankton biomass or PBm, which reflects the lag time between nutrient input and phytoplankton growth at this coastal site. The major phytoplankton groups that occurred at this site occupied distinct thermal niches, which in turn modified PBm. Increasing temperature, and higher water column stratification, was major factors in the initiation of dinoflagellates blooms at this site. Dinoflagellates blooms during summer also co-varied with silicate concentration, and acted as a tracer of dissolved inorganic nitrogen and phosphate from river run-off, which were subsequently reduced during these blooms. The data implies that increasing temperature and high river runoff during summer, will promote dinoflaglellates blooms in the WEC.

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.

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.

Ecological equivalence of species within phytoplankton functional groups

1.There are tens of thousands of species of phytoplankton found throughout the tree of life. Despite this diversity, phytoplankton are often aggregated into a few functional groups according to metabolic traits or biogeochemical role. We investigate the extent to which phytoplankton species dynamics are neutral within functional groups. 2.Seasonal dynamics in many regions of the ocean are known to affect phytoplankton at the functional group level leading to largely predictable patterns of seasonal succession. It is much more difficult to make general statements about the dynamics of individual species. 3.We use a 7 year time-series at station L4 in the Western English Channel with 57 diatom and 17 dinoflagellate species enumerated weekly to test if the abundance of diatom and dinoflagellate species vary randomly within their functional group envelope or if each species is driven uniquely by external factors. 4.We show that the total biomass of the diatom and dinoflagellate functional groups is well predicted by irradiance and temperature and quantify trait values governing the growth rate of both functional groups. The biomass dynamics of the functional groups are not neutral and each has their own distinct responses to environmental forcing. Compared to dinoflagellates, diatoms have faster growth rates, and grow faster under lower irradiance, cooler temperatures, and higher nutrient conditions. 5.The biomass of most species vary randomly within their functional group biomass envelope, most of the time. As a consequence, modelers will find it difficult to predict the biomass of most individual species. Our analysis supports the approach of using a single set of traits for a functional group and suggests that it should be possible to determine these traits from natural communities.