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.

Long-term declining trend of zooplankton biomass in the Tropical Atlantic

We report evidences that the zooplankton biomass in the tropical Atlantic has declined with an almost 10-fold drop from the 1950s to 2000. The results of the multiple regression analysis showed that the decline in zooplankton biomass was positively related to the NAO-index and to phosphate concentration. We also found that the depth of the thermocline has decreased over the period of our investigation. Thus, the decline we report in zooplankton biomass may be related to the combined effect of two phenomena driven by global temperature increase: (1) the widening of the distributional range of tropical species due to the expansion of the ‘tropical belt’ and (2) a decrease in primary production resulting from the thinning of the thermocline. The decline of zooplankton biomass we report suggests that global warming of the ocean may be altering tropical food webs, and through them, it may also indirectly impact tropical oceans biogeochemical cycles.

Have climate induced changes in zooplankton communities led to poor conditions for larval fish growth? A test on cod larvae on the UK shelf

Climate effects have been shown to be at least partly responsible for the reorganisation in the plankton ecosystem on the shelf seas of NW Europe over the last 50 years. Most fish larvae feed primarily on zooplankton, so changes in zooplankton quantity, quality and seasonal timing have been hypothesized to be a key factor affecting their survival. To investigate this we have implemented a 1-dimensional trophodynamic growth model of cod larvae for the waters around the UK covering the period 1960 to 2003. Larval growth is modelled as the difference between the amount of food absorbed by the larva and its various metabolic costs. Prey availability is based upon the biomass and size of available preys (i.e. adults and nauplii copepods and cladocerans) taken from the Continuous Plankton Recorder dataset. Temperature and wind forcing are also taken into account. Results suggest that observed changes in plankton community structure may have had less impact than previously suggested. This is because changes in prey availability may be compensated for by increased temperatures resulting in little overall impact on potential larval growth. Stock recovery, at least in the short term is likely to be more dependent upon conserving the year classes recruited to allow spawning stock biomass to rebuild. If as our model suggests, the larvae are still able to survive in the changing environment, reduction in fishing on the adults is needed to allow the stock to recover.

The importance of zooplankton in reducing levels of atmospheric CO sub(2) via the biological pump

Zooplankton play a key role in climate change through the transfer of large quantities of CO sub(2) to the deep ocean by a process known as the biological pump. Plankton composition is crucial as associated mineral material facilitates sinking of carbon rich debris and some taxa package faecal and detrital material. Ocean acidification may impact calcareous groups. Zooplankton have also been shown to be highly sensitive indicators of environmental change. Results will be presented to show that ocean temperature, circulation and planktonic ecosystems (using data from the Continuous Plankton Recorder, CPR survey) in the North Atlantic are changing rapidly in concert and that there is evidence to suggest that the changes are an ocean wide response to global warming with potential feedback effects. Given the importance of the oceans to the carbon cycle, even a minor change in the flux of carbon to the deep ocean would have a big impact increasing growth of atmospheric CO sub(2). We have virtually no understanding of the spatial and temporal variability in the efficiency of the biological pump for most of the world's ocean. Establishing new plankton monitoring programmes backed up by appropriate research to help understand processes is needed to address this gap in knowledge. There is little doubt within a global change context and the future of mankind that a potential acceleration in the growth of atmospheric carbon due to a reduction in the efficiency of the biological pump is a key issue for future research in zooplankton ecology.

In hot water: zooplankton and climate change

An overview is provided of the observed and potential future responses of zooplankton communities to global warming. I begin by describing the importance of zooplankton in ocean ecosystems and the attributes that make them sensitive beacons of climate change. Global warming may have even greater repercussions for marine ecosystems than for terrestrial ecosystems, because temperature influences water column stability, nutrient enrichment, and the degree of new production, and thus the abundance, size composition, diversity, and trophic efficiency of zooplankton. Pertinent descriptions of physical changes in the ocean in response to climate change are given as a prelude to a detailed discussion of observed impacts of global warming on zooplankton. These manifest as changes in the distribution of individual species and assemblages, in the timing of important life-cycle events, and in abundance and community structure. The most illustrative case studies, where climate has had an obvious, tangible impact on zooplankton and substantial ecosystem consequences, are presented. Changes in the distribution and phenology of zooplankton are faster and greater than those observed for terrestrial groups. Relevant projected changes in ocean conditions are then presented, followed by an exploration of potential future changes in zooplankton communities from the perspective of different modelling approaches. Researchers have used a range of modelling approaches on individual species and functional groups forced by output from climate models under future greenhouse gas emission scenarios. I conclude by suggesting some potential future directions in climate change research for zooplankton, viz. the use of richer zooplankton functional groups in ecosystem models; greater research effort in tropical systems; investigating climate change in conjunction with other human impacts; and a global zooplankton observing system.

Comparison of Zooplankton Sampling Performance of Longhurst-Hardy Plankton Recorder and Bongo Nets

Data on the abundance and biomass of zooplankton off the northwestern Portuguese coast, separately estimated with a Longhurst-Hardy Plankton Recorder (LHPR) and a Bongo net, were analysed to assess the comparative performance of the samplers. Zooplankton was collected along four transects perpendicular to the coast, deployments alternating between samplers. Total zooplankton biomass measured using the LHPR was significantly higher than that using the Bongo net. Apart from Appendicularia and Cladocera, abundances of other taxa (Copepoda, Mysidacea, Euphausiacea, Decapoda larvae, Amphipoda, Siphonophora, Hydromedusae, Chaetognatha and Fish eggs) were also consistently higher in the LHPR. Some of these differences were probably due to avoidance by the zooplankton of the Bongo net. This was supported by a comparative analysis of prosome length of the copepod Calanus helgolandicus sampled by the two nets that showed that Calanus in the LHPR samples were on average significantly larger, particularly in day samples. A ratio estimator was used to produce a factor to convert Bongo net biomass and abundance estimates to equate them with those taken with the LHPR. This method demonstrates how results from complementary zooplankton sampling strategies can be made more equivalent.

Bridging the gap between marine biogeochemical and fisheries sciences; configuring the zooplankton link

Exploring climate and anthropogenic impacts on marine ecosystems requires an understanding of how trophic components interact. However, integrative end-to-end ecosystem studies (experimental and/or modelling) are rare. Experimental investigations often concentrate on a particular group or individual species within a trophic level, while tropho-dynamic field studies typically employ either a bottom-up approach concentrating on the phytoplankton community or a top-down approach concentrating on the fish community. Likewise the emphasis within modelling studies is usually placed upon phytoplankton-dominated biogeochemistry or on aspects of fisheries regulation. In consequence the roles of zooplankton communities (protists and metazoans) linking phytoplankton and fish communities are typically under-represented if not (especially in fisheries models) ignored. Where represented in ecosystem models, zooplankton are usually incorporated in an extremely simplistic fashion, using empirical descriptions merging various interacting physiological functions governing zooplankton growth and development, and thence ignoring physiological feedback mechanisms. Here we demonstrate, within a modelled plankton food-web system, how trophic dynamics are sensitive to small changes in parameter values describing zooplankton vital rates and thus the importance of using appropriate zooplankton descriptors. Through a comprehensive review, we reveal the mismatch between empirical understanding and modelling activities identifying important issues that warrant further experimental and modelling investigation. These include: food selectivity, kinetics of prey consumption and interactions with assimilation and growth, form of voided material, mortality rates at different age-stages relative to prior nutrient history. In particular there is a need for dynamic data series in which predator and prey of known nutrient history are studied interacting under varied pH and temperature regimes.

Have we been underestimating the effects of ocean acidification in zooplankton?

Understanding how copepods may respond to ocean acidification (OA) is critical for risk assessments of ocean ecology and biogeochemistry. The perception that copepods are insensitive to OA is largely based on experiments with adult females. Their apparent resilience to increased carbon dioxide (pCO2 ) concentrations has supported the view that copepods are 'winners' under OA. Here, we show that this conclusion is not robust, that sensitivity across different life stages is significantly misrepresented by studies solely using adult females. Stage-specific responses to pCO2 (385-6000 μatm) were studied across different life stages of a calanoid copepod, monitoring for lethal and sublethal responses. Mortality rates varied significantly across the different life stages, with nauplii showing the highest lethal effects; nauplii mortality rates increased threefold when pCO2 concentrations reached 1000 μatm (year 2100 scenario) with LC50 at 1084 μatm pCO2 . In comparison, eggs, early copepodite stages, and adult males and females were not affected lethally until pCO2 concentrations ≥3000 μatm. Adverse effects on reproduction were found, with >35% decline in nauplii recruitment at 1000 μatm pCO2 . This suppression of reproductive scope, coupled with the decreased survival of early stage progeny at this pCO2 concentration, has clear potential to damage population growth dynamics in this species. The disparity in responses seen across the different developmental stages emphasizes the need for a holistic life-cycle approach to make species-level projections to climate change. Significant misrepresentation and error propagation can develop from studies which attempt to project outcomes to future OA conditions solely based on single life history stage exposures.

Ecological Investigations with the Continuous Plankton Recorder: The Zooplankton (other than Copepoda and Young Fish) in the Southern North Sea, 1932-37.

I. The report describes the main monthly changes in the distribution and abundance of the zooplankton, other than Copepoda and young fish (dealt with in separate reports), over the southern part of the North Sea from 1932 to 1937. The work is part of the survey carried out by Continuous Plankton Recorders towed at a depth of 10 metres on regular steamship lines between England and the Continent. 2. The limitations to the sampling method are discussed, and it is shown to be unsuitable for recording Mysidacea and Euphausiacea on account of their marked diurnal variation due presumably to vertical migration; they are omitted from the report. 3. The changing distribution of Sagitta, Limacina, Clione, Lamellibranch larvae, Cladocera, Caprellid Amphipoda, Decapod larvae, Echinoderm larvae and Oikopleura are shown in a series of monthly charts while their seasonal fluctuations are compared in time-chart histograms. 4. The Alima larvae of Squilla are recorded on a few occasions in the regions where the Channel opens into the North Sea. 5. The distributional characteristics of the different forms, i.e. their tendencies to even or " patchy " production, are compared.

Impact of zooplankton food selectivity on plankton dynamics and nutrient cycling

Within models, zooplankton grazing is typically defined as being dependent on total prey concentration, with feeding selectivity expressed only as a function of prey size. This behavior ignores taxonomic preferences shown by the preda- tors and the capacity of some zooplankton to actively select or reject individual prey items from mixtures. We carried out two model experiments comparing impacts of zooplankton displaying passive and active selection, which resulted in contrasting dynamics for the pelagic system. Passive selection by the grazer resulted in a top down control on the prey with a fast turn-over of nutrients. Active selection, on the other hand led to a bottom-up control, with slower nutrient turnover constraining primary production by changing the system toward export of particulate matter. Our results suggest that selective feeding behavior is an important trait, and should be considered alongside size and taxonomy when studying the role of zooplankton impact in the ecosystem.

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.

Contrasting transcriptome response to thermal stress in two key zooplankton species, Calanus finmarchicus and C. glacialis

Climate change has already led to the range expansion of warm-water plankton assemblages in the northeast Atlantic and the corresponding range contraction of colder-water species. The temperate copepod Calanus finmarchicus is predicted to shift farther northward into polar waters traditionally dominated by the arctic copepod C. glacialis. To identify temperaturemediated changes in gene expression that may be critical for the thermal acclimation and resilience of the 2 Calanus spp., we conducted a whole transcriptome profiling using RNA-seq on an Ion Torrent platform. Transcriptome responses of C. finmarchicus and C. glacialis from Disko Bay, west Greenland, were investigated under realistic thermal stresses (at + 5, +10 and +15°C) for 4 h and 6 d. C. finmarchicus showed a strong response to temperature and duration of stress, involving up-regulation of genes related to protein folding, transcription, translation and metabolism. In sharp contrast, C. glacialis displayed only low-magnitude changes in gene expression in response to temperature and duration of stress. Differences in the thermal responses of the 2 species, particularly the lack of thermal stress response in C. glacialis, are in line with laboratory and field observations and suggest a vulnerability of C. glacialis to climate change.

Island-coastal and oceanic epipelagic zooplankton biodiversity in the southwestern Indian Ocean

The oceanic Indian Ocean zooplankton species and their distributions have been well described, but the zooplankton of coastal regions, particularly around the oceanic islands, has not been well researched, either taxonomically or experimentally. The environment of the Mascarene region in the southwestern Indian Ocean and zooplankton research that has been carried out there is detailed, along with gaps in our knowledge. Suggestions are given for future research, particularly on the zooplankton species adapted to live in the fluctuating environment of inshore waters, including studies on taxonomy and biodiversity, life cycles, dispersion and genetics. Problems of carrying out taxonomic research are highlighted.

Role of zooplankton dynamics for Southern Ocean phytoplankton biomass and global biogeochemical cycles

Global ocean biogeochemistry models currently employed in climate change projections use highly simplified representations of pelagic food webs. These food webs do not necessarily include critical pathways by which ecosystems interact with ocean biogeochemistry and climate. Here we present a global biogeochemical model which incorporates ecosystem dynamics based on the representation of ten plankton functional types (PFTs); six types of phytoplankton, three types of zooplankton, and heterotrophic bacteria. We improved the representation of zooplankton dynamics in our model through (a) the explicit inclusion of large, slow-growing zooplankton, and (b) the introduction of trophic cascades among the three zooplankton types. We use the model to quantitatively assess the relative roles of iron vs. grazing in determining phytoplankton biomass in the Southern Ocean High Nutrient Low Chlorophyll (HNLC) region during summer. When model simulations do not represent crustacean macrozooplankton grazing, they systematically overestimate Southern Ocean chlorophyll biomass during the summer, even when there was no iron deposition from dust. When model simulations included the developments of the zooplankton component, the simulation of phytoplankton biomass improved and the high chlorophyll summer bias in the Southern Ocean HNLC region largely disappeared. Our model results suggest that the observed low phytoplankton biomass in the Southern Ocean during summer is primarily explained by the dynamics of the Southern Ocean zooplankton community rather than iron limitation. This result has implications for the representation of global biogeochemical cycles in models as zooplankton faecal pellets sink rapidly and partly control the carbon export to the intermediate and deep ocean.