Climate-induced effects on the meroplankton and the benthic-pelagic ecology of the North Sea

Analyses of long-term time series of North Sea plankton and sea surface temperature (SST) data reveal that the annual planktonic larval abundance of three benthic phyla, Echinodermata, Arthropoda, and Mollusca, responds positively and immediately to SST. Long-term outcomes for the planktonic abundance of these three phyla are different, however. The planktonic larvae of echinoderms and decapod crustaceans have increased in abundance from 1958 to 2005, and especially since the mid-1980s, as North Sea SST has increased. In contrast, the abundance of bivalve mollusc larvae has declined, despite the positive year-to-year relationship between temperature and bivalve larval abundance continuing to hold. We argue that the changes in meroplankton abundance, coincident with increased phytoplankton and declining holoplankton, reflect the synchronous effect of rising SST and related changes in the pelagic community on the reproduction and recruitment of many benthic marine invertebrates. Under this scenario, the long-term decline in bivalve mollusc larvae will reflect increased predation on the settled larvae and adults by benthic decapods. These alterations in the zooplankton may therefore describe an ecosystem-wide restructuring of North Sea trophic interactions.

Long-term changes in the meroplankton of the North Sea

Data from the continuous plankton recorder (CPR) survey collected in the late-1940s to early-1960s indicated that the abundance of decapod larvae was low and the seasonal peak of abundance was late following cold winters. The phenological effect of temperature was shown to be consistent with relationships between both geographical and interannual patterns of variation. Analyses of CPR data collected from the 1940s to the present day reveal large-scale long-term changes in the abundance and phenology of the North Sea meroplankton. Echinoderm larvae, whose peak abundance has advanced by 47 days, show the greatest shift in timing. Echinoderm larvae have also increased in abundance to become the most abundant taxon in North Sea CPR samples. Genetic and morphological analyses of CPR samples show that the variations in echinoderm larvae are mainly attributable to an increasing abundance and earlier occurrence of the larvae of a resident species, Echinocardium cordatum, rather than a change in species composition. The remarkable scale of the changes in abundance and phenology of the meroplankton, which are greater than those seen in the holoplankton, has stimulated the development of further research into the causes and effects of these changes.

Climate effects and benthic-pelagic coupling in the North Sea

The North Sea is one of the most biologically productive ecosystems in the world and supports important fisheries. Climate-induced changes occurred in the pelagic ecosystems of the North Sea during the 1980s. These changes, which have been observed from phytoplankton to fish and among permanent (holoplankton) and temporary (meroplankton) plankton species, have resulted in alterations in plankton community composition and seasonality. Until now, the effects of climate-driven changes on biological linkages between pelagic and benthic ecosystems have not been examined. The present study indicates that changes in benthic organisms could have a profound effect on the trophodynamics of the pelagos. We demonstrate this by analyses of a long-term time series of North Sea plankton and sea surface temperature data. We discover that pronounced changes in the North Sea meroplankton, mainly related to an increased abundance and spatial distribution of the larvae of a benthic echinoderm, Echinocardium cordatum, result primarily from a stepwise increase in sea temperature after 1987 that has caused warmer conditions to occur earlier in the year than previously. Key stages of reproduction in E. cordatum, gametogenesis and spawning, appear to be influenced by winter and spring sea temperature and their larval development is affected by the quantity and quality of their phytoplankton food. Our analyses suggest that a new thermal regime in the North Sea in winter and spring may have benefited reproduction and survival in this benthic species. As a result, E. cordatum may be altering the trophodynamics of the summer pelagic ecosystem through competition between its larvae and holozooplankton taxa.

Genetic analysis of Continuous Plankton Recorder (CPR) samples

Genetic analysis of Continuous Plankton Recorder (CPR) samples is enabling greater taxonomic resolution and the study of plankton population structure. Here, we present some results from the genetic analysis of CPR samples collected in the North Sea and north-eastern Atlantic that reveal the impacts of climate on benthic-pelagic coupling and the food web. We show that pronounced changes in the North Sea meroplankton are related to an increased abundance and spatial distribution of the larvae of the benthic echinoderm, Echinocardium cordatum. Key stages of reproduction in E. cordatum, gametogenesis and spawning, are influenced by winter and spring sea temperature (January-May). A stepwise increase in sea temperature after 1987, which has created warmer conditions earlier in the year, together with increased summer phytoplankton, may benefit the reproduction and survival of this benthic species. Competition between the larvae of E. cordatum and other holozooplanlcton taxa may now be altering the trophodynamics of the summer pelagic ecosystem. In the north-eastern Atlantic the genetic analysis of fish larvae sampled by the CPR has revealed an unprecedented increase in the abundance of juvenile snake pipefish, Entelurus aequoreiis since 2002. We argue that increased sea surface temperatures in winter and spring when the eggs of E. aqueoreus, which are brooded by the male, are developing and the young larvae are growing in the plankton are a likely cause. The increased abundance of this species in Atlantic and adjacent European seas already appears to be influencing the marine food web.

Long-term changes in North Atlantic zooplankton biomass

New measures of zooplankton biomass have been derived from CPR samples in the North Atlantic from 1958 to 2005. The final aim was to investigate how the zooplankton standing stock had varied throughout the last decades, knowing that in different areas of the North Atlantic significant changes in the distribution of the dominant zooplankton species as well as the plankton assemblage have been observed. During the forty-five years of monitoring the contribution of the different groups (e.g. copepods, euphausiids, meroplankton larvae) to the total zooplankton biomass has been evaluated. The changes in the phenology of the biomass were also considered. The relationship between quantity, quality and seasonal timing of plankton and the poor fish recruitment seen in recent years in the North Sea are also discussed.

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.

Next Generation Sequencing Reveals the Hidden Diversity of Zooplankton Assemblages

Zooplankton play an important role in our oceans, in biogeochemical cycling and providing a food source for commercially important fish larvae. However, difficulties in correctly identifying zooplankton hinder our understanding of their roles in marine ecosystem functioning, and can prevent detection of long term changes in their community structure. The advent of massively parallel next generation sequencing technology allows DNA sequence data to be recovered directly from whole community samples. Here we assess the ability of such sequencing to quantify richness and diversity of a mixed zooplankton assemblage from a productive time series site in the Western English Channel. Methodology/Principle Findings Plankton net hauls (200 µm) were taken at the Western Channel Observatory station L4 in September 2010 and January 2011. These samples were analysed by microscopy and metagenetic analysis of the 18S nuclear small subunit ribosomal RNA gene using the 454 pyrosequencing platform. Following quality control a total of 419,041 sequences were obtained for all samples. The sequences clustered into 205 operational taxonomic units using a 97% similarity cut-off. Allocation of taxonomy by comparison with the National Centre for Biotechnology Information database identified 135 OTUs to species level, 11 to genus level and 1 to order, <2.5% of sequences were classified as unknowns. By comparison a skilled microscopic analyst was able to routinely enumerate only 58 taxonomic groups. Conclusions Metagenetics reveals a previously hidden taxonomic richness, especially for Copepoda and hard-to-identify meroplankton such as Bivalvia, Gastropoda and Polychaeta. It also reveals rare species and parasites. We conclude that Next Generation Sequencing of 18S amplicons is a powerful tool for elucidating the true diversity and species richness of zooplankton communities. While this approach allows for broad diversity assessments of plankton it may become increasingly attractive in future if sequence reference libraries of accurately identified individuals are better populated.

Questioning the role of phenology shifts and trophic mismatching in a planktonic food web

In a warming climate, differential shifts in the seasonal timing of predators and prey have been suggested to lead to trophic ‘‘mismatches’’ that decouple primary, secondary and tertiary production. We tested this hypothesis using a 25-year time-series of weekly sampling at the Plymouth L4 site, comparing 57 plankton taxa spanning 4 trophic levels. During warm years, there was a weak tendency for earlier timings of spring taxa and later timings of autumn taxa. While this is in line with many previous findings, numerous exceptions existed and only a few taxa (e.g. Gyrodinium spp., Pseudocalanus elongatus, and Acartia clausi) showed consistent, strong evidence for temperature-related timing shifts, revealed by all 4 of the timing indices that we used. Also, the calculated offsets in timing i.e. ‘‘mismatches’’) between predator and prey were no greater in extreme warm or cold years than during more average years. Further, the magnitude of these offsets had no effect on the ‘‘success’’ of the predator, in terms of their annual mean abundance or egg production rates. Instead numerous other factors override, including: inter-annual variability in food quantity, high food baseline levels, turnover rates and prolonged seasonal availability, allowing extended periods of production. Furthermore many taxa, notably meroplankton, increased well before the spring bloom. While theoretically a chronic mismatch, this likely reflects trade-offs for example in predation avoidance. Various gelatinous taxa (Phaeocystis, Noctiluca, ctenophores, appendicularians, medusae) may have reduced these predation constraints, with variable, explosive population outbursts likely responding to improved conditions. The match–mismatch hypothesis may apply for highly seasonal, pulsed systems or specialist feeders, but we suggest that the concept is being over-extended to other marine systems where multiple factors compensate.