RRS Discovery DY021 Cruise Report, March 2015

The Shelf Sea Biogeochemistry research programme directly relates to the delivery of the NERC Earth system science theme and aims to provide evidence that supports a number of marine policy areas and statutory requirements, such as the Marine Strategy Framework Directive and Marine and Climate Acts. The shelf seas are highly productive compared to the open ocean, a productivity that underpins more than 90 per cent of global fisheries. Their importance to society extends beyond food production to include issues of biodiversity, carbon cycling and storage, waste disposal, nutrient cycling, recreation and renewable energy resources. The shelf seas have been estimated to be the most valuable biome on Earth, but they are under considerable stress, as a result of anthropogenic nutrient loading, overfishing, habitat disturbance, climate change and other impacts. However, even within the relatively well-studied European shelf seas, fundamental biogeochemical processes are poorly understood. For example: the role of shelf seas in carbon storage; in the global cycles of key nutrients (nitrogen, phosphorus, silicon and iron); and in determining primary and secondary production, and thereby underpinning the future delivery of many other ecosystem services. Improved knowledge of such factors is not only required by marine policymakers; it also has the potential to increase the quality and cost-effectiveness of management decisions at the local, national and international levels under conditions of climate change. The Shelf Sea Biogeochemistry research programme will take a holistic approach to the cycling of nutrients and carbon and the controls on primary and secondary production in UK and European shelf seas, to increase understanding of these processes and their role in wider biogeochemical cycles. It will thereby significantly improve predictive marine biogeochemical and ecosystem models over a range of scales. The scope of the programme includes exchanges with the open ocean (transport on and off the shelf to a depth of around 500m), together with cycling, storage and release processes on the shelf slope, and air-sea exchange of greenhouse gases (carbon dioxide and nitrous oxide). The DY021 cruise is the first of the 2015 Benthic SSB cruises to investigate the 4 main ‘representative’ sites in the Celtic Sea that will represent all the various sediment types found in the whole area, these being Mud, San, Sandy-Mud and Muddy-Sand. The cruise will also carry out complimentary sampling at the Pelagic SSB programme main site called CANDYFLOSS in the central Shelf area in order to better link the Benthic and Pelagic programmes.

Warmer, deeper and greener mixed layers in the north Atlantic subpolar gyre over the last 50 years.

Shifts in global climate resonate in plankton dynamics, biogeochemical cycles, and marine food webs. We studied these linkages in the North Atlantic subpolar gyre (NASG), which hosts extensive phytoplankton blooms. We show that phytoplankton abundance increased since the 1960s in parallel to a deepening of the mixed layer and a strengthening of winds and heat losses from the ocean, as driven by the low frequency of the North Atlantic Oscillation (NAO). In parallel to these bottom-up processes, the top-down control of phytoplankton by copepods decreased over the same time period in the western NASG, following sea surface temperature changes typical of the Atlantic Multi-decadal Oscillation (AMO). While previous studies have hypothesized that climate-driven warming would facilitate seasonal stratification of surface waters and long-term phytoplankton increase in subpolar regions, here we show that deeper mixed layers in the NASG can be warmer and host a higher phytoplankton biomass. These results emphasize that different modes of climate variability regulate bottom-up (NAO control) and top-down (AMO control) forcing on phytoplankton at decadal timescales. As a consequence, different relationships between phytoplankton, zooplankton, and their physical environment appear subject to the disparate temporal scale of the observations (seasonal, interannual, or decadal). The prediction of phytoplankton response to climate change should be built upon what is learnt from observations at the longest timescales.

Warmer, deeper and greener mixed layers in the north Atlantic subpolar gyre over the last 50 years.

Shifts in global climate resonate in plankton dynamics, biogeochemical cycles, and marine food webs. We studied these linkages in the North Atlantic subpolar gyre (NASG), which hosts extensive phytoplankton blooms. We show that phytoplankton abundance increased since the 1960s in parallel to a deepening of the mixed layer and a strengthening of winds and heat losses from the ocean, as driven by the low frequency of the North Atlantic Oscillation (NAO). In parallel to these bottom-up processes, the top-down control of phytoplankton by copepods decreased over the same time period in the western NASG, following sea surface temperature changes typical of the Atlantic Multi-decadal Oscillation (AMO). While previous studies have hypothesized that climate-driven warming would facilitate seasonal stratification of surface waters and long-term phytoplankton increase in subpolar regions, here we show that deeper mixed layers in the NASG can be warmer and host a higher phytoplankton biomass. These results emphasize that different modes of climate variability regulate bottom-up (NAO control) and top-down (AMO control) forcing on phytoplankton at decadal timescales. As a consequence, different relationships between phytoplankton, zooplankton, and their physical environment appear subject to the disparate temporal scale of the observations (seasonal, interannual, or decadal). The prediction of phytoplankton response to climate change should be built upon what is learnt from observations at the longest timescales.

Potential consequences of climate change for primary production and fish production in large marine ecosystems

Existing methods to predict the effects of climate change on the biomass and production of marine communities are predicated on modelling the interactions and dynamics of individual species, a very challenging approach when interactions and distributions are changing and little is known about the ecological mechanisms driving the responses of many species. An informative parallel approach is to develop size-based methods. These capture the properties of food webs that describe energy flux and production at a particular size, independent of species' ecology. We couple a physical-biogeochemical model with a dynamic, size-based food web model to predict the future effects of climate change on fish biomass and production in 11 large regional shelf seas, with and without fishing effects. Changes in potential fish production are shown to most strongly mirror changes in phytoplankton production. We project declines of 30-60% in potential fish production across some important areas of tropical shelf and upwelling seas, most notably in the eastern Indo-Pacific, the northern Humboldt and the North Canary Current. Conversely, in some areas of the high latitude shelf seas, the production of pelagic predators was projected to increase by 28-89%.

An innovative statistical approach to constructing a readily comprehensible food web for a demersal fish community

Many food webs are so complex that it is difficult to distinguish the relationships between predators and their prey. We have therefore developed an approach that produces a food web which clearly demonstrates the strengths of the relationships between the predator guilds of demersal fish and their prey guilds in a coastal ecosystem. Subjecting volumetric dietary data for 35 abundant predators along the lower western Australia coast to cluster analysis and the SIMPROF routine separated the various species x length class combinations into 14 discrete predator guilds. Following nMDS ordination, the sequence of points for these predator guilds represented a 'trophic' hierarchy. This demonstrated that, with increasing body size, several species progressed upwards through this hierarchy, reflecting a marked change in diet, whereas others remained within the same guild. A novel use of cluster analysis and SIMPROF then identified each group of prey that was ingested in a common pattern across the full suite of predator guilds. This produced 12 discrete groups of taxa (prey guilds) that each typically comprised similar ecological/functional prey, which were then also aligned in a hierarchy. The hierarchical arrangements of the predator and prey guilds were plotted against each other to show the percentage contribution of each prey guild to the diet of each predator guild. The resultant shade plot demonstrates quantitatively how food resources are spread among the fish species and revealed that two prey guilds, one containing cephalopods and teleosts and the other small benthic/epibenthic crustaceans and polychaetes, were consumed by all predator guilds.

Transregional linkages in the North-Eastern Atlantic - An ‘end-to-end ’ analysis of pelagic ecosystems

This review examines interregional linkages and gives an overview perspective on marine ecosystem functioning in the north-eastern Atlantic. It is based on three of the 'systems' considered by the European Network of Excellence for Ocean Ecosystems Analysis (EUR-OC EANS was established in 2004 under the European Framework VI funding programme to promote integration of marine ecological research within Europe), the Arctic and Nordic Seas, North Atlantic shelf seas and North Atlantic. The three systems share common open boundaries and the transport of water, heat, nutrients and particulates across these boundaries modifies local processes. Consistent with the EUR-OC EANS concept of 'end-to-end' analyses of marine food webs, the review takes an integrated approach linking ocean physics, lower trophic levels and working up the food web to top predators such as marine mammals. We begin with an overview of the regions focusing on the major physical patterns and their implications for the microbial community, phytoplankton, zooplankton, fish and top predators. Human-induced links between the regional systems are then considered and finally possible changes in the regional linkages over the next century are discussed. Because of the scale of potential impacts of climate change, this issue is considered in a separate section. The review demonstrates that the functioning of the ecosystems in each of the regions cannot be considered in isolation and the role of the atmosphere and ocean currents in linking the North Atlantic Ocean, North Atlantic shelf seas and the Arctic and Nordic Seas must be taken into account. Studying the North Atlantic and associated shelf seas as an integrated 'basin-scale' system will be a key challenge for the early twenty-first century. This requires a multinational approach that should lead to improved ecosystem-based approaches to conservation of natural resources, the maintenance of biodiversity, and a better understanding of the key role of the north-eastern Atlantic in the global carbon cycle.

DNA barcoding identifies a cosmopolitan diet in the ocean sunfish

The ocean sunfish (Mola mola) is the world’s heaviest bony fish reaching a body mass of up to 2.3 tonnes. However, the prey M. mola consumes to fuel this prodigious growth remains poorly known. Sunfish were thought to be obligate gelatinous plankton feeders, but recent studies suggest a more generalist diet. In this study, through molecular barcoding and for the first time, the diet of sunfish in the north-east Atlantic Ocean was characterised. Overall, DNA from the diet content of 57 individuals was successfully amplified, identifying 41 different prey items. Sunfish fed mainly on crustaceans and teleosts, with cnidarians comprising only 16% of the consumed prey. Although no adult fishes were sampled, we found evidence for an ontogenetic shift in the diet, with smaller individuals feeding mainly on small crustaceans and teleost fish, whereas the diet of larger fish included more cnidarian species. Our results confirm that smaller sunfish feed predominantly on benthic and on coastal pelagic species, whereas larger fish depend on pelagic prey. Therefore, sunfish is a generalist predator with a greater diversity of links in coastal food webs than previously realised. Its removal as fisheries’ bycatch may have wider reaching ecological consequences, potentially disrupting coastal trophic interactions.

DNA barcoding identifies a cosmopolitan diet in the ocean sunfish

The ocean sunfish (Mola mola) is the world’s heaviest bony fish reaching a body mass of up to 2.3 tonnes. However, the prey M. mola consumes to fuel this prodigious growth remains poorly known. Sunfish were thought to be obligate gelatinous plankton feeders, but recent studies suggest a more generalist diet. In this study, through molecular barcoding and for the first time, the diet of sunfish in the north-east Atlantic Ocean was characterised. Overall, DNA from the diet content of 57 individuals was successfully amplified, identifying 41 different prey items. Sunfish fed mainly on crustaceans and teleosts, with cnidarians comprising only 16% of the consumed prey. Although no adult fishes were sampled, we found evidence for an ontogenetic shift in the diet, with smaller individuals feeding mainly on small crustaceans and teleost fish, whereas the diet of larger fish included more cnidarian species. Our results confirm that smaller sunfish feed predominantly on benthic and on coastal pelagic species, whereas larger fish depend on pelagic prey. Therefore, sunfish is a generalist predator with a greater diversity of links in coastal food webs than previously realised. Its removal as fisheries’ bycatch may have wider reaching ecological consequences, potentially disrupting coastal trophic interactions.

Partitioning, bioavailability and effects of oestrogens and xeno-oestrogens in the aquatic environment

This review provides insights into the distribution and impact of oestrogens and xeno-oestrogens in the aquatic environment and highlights some significant knowledge gaps in our understanding of endocrine disrupting chemicals. Key areas of uncertainty in the assessment of risk include the role of estuarine sediments in mediating the fate and bioavailability of environmental (xeno)oestrogens (notably their transfer to benthic organisms and estuarine food chains), together with evidence for endocrine disruption in invertebrate populations. Emphasis is placed on using published information to interpret the behaviour and effects of a small number of model compounds thought to contribute to oestrogenic effects in nature; namely, the natural steroid 17 beta -oestradiol (E2) and the synthetic hormone 17 alpha -ethinyloestradiol (EE2), together with the alkyl-phenols octyl- and nonyl-phenol (OP, NP) as oestrogen mimics. Individual sections of the review are devoted to sources and concentrations of (xeno)oestrogens in waterways, sediment partitioning and persistence, bioaccumulation rates and routes, assays and biomarkers of oestrogenicity, and, finally, a synopsis of reproductive and ecological effects in aquatic species.

Long-Term Oceanographic and Ecological Research in the Western English Channel

Long-term research in the western English Channel, undertaken by the marine laboratories in Plymouth, is described and details of survey methods, sites, and time series given in this chapter. Major findings are summarized and their limitations outlined. Current research, with recent reestablishment and expansion of many sampling programmes, is presented, and possible future approaches are indicated. These unique long-term data sets provide an environmental baseline for predicting complex ecological responses to local, regional, and global environmental change. Between 1888 and the present, investigations have been carried out into the physical, chemical, and biological components (ranging from plankton and fish to benthic and intertidal assemblages) of the western English Channel ecosystem. The Marine Biological Association of the United Kingdom has performed the main body of these observations. More recent contributions come from the Continuous Plankton Recorder Survey, now the Sir Alister Hardy Foundation for Ocean Science, dating from 1957; the Institute for Marine Environmental Research, from 1974 to 1987; and the Plymouth Marine Laboratory, which was formed by amalgamation of the Institute for Marine Environmental Research and part of the Marine Biological Association, from 1988. Together, these contributions constitute a unique data series; one of the longest and most comprehensive samplings of environmental and marine biological variables in the world. Since the termination of many of these time series in 1987-1988 during a reorganisation of UK marine research, there has been a resurgence of interest in long-term environmental change. Many programmes have been restarted and expanded with support from several agencies. The observations span significant periods of warming (1921-1961; 1985-present) and cooling (1962-1980). During these periods of change, the abundance of key species underwent dramatic shifts. The first period of warming saw changes in zooplankton, pelagic fish, and larval fish, including the collapse of an important herring fishery. During later periods of change, shifts in species abundances have been reflected in other assemblages, such as the intertidal zone and the benthic fauna. Many of these changes appear to be related to climate, manifested as temperature changes, acting directly or indirectly. The hypothesis that climate is a forcing factor is widely supported today and has been reinforced by recent studies that show responses of marine organisms to climatic attributes such as the strength of the North Atlantic Oscillation. The long-term data also yield important insights into the effects of anthropogenic disturbances such as fisheries exploitation and pollution. Comparison of demersal fish hauls over time highlights fisheries effects not only on commercially important species but also on the entire demersal community. The effects of acute ("Torrey Canyon" oil spill) and chronic (tributyltin [TBT] antifoulants) pollution are clearly seen in the intertidal records. Significant advances in diverse scientific disciplines have been generated from research undertaken alongside the long-term data series.

Temporal and spatial variability of Oithona spp. abundance and phenology in the North Atlantic, North Pacific and Southern Ocean using the CPR data

The genus Oithona is considered the most ubiquitous and abundant copepod group in the world oceans. Although they generally make-up a lower proportion of the total copepod biomass, because of their high numerical abundance, preferential feeding for microzooplankton and motile preys, Oithona spp. plays an important role in microbial food webs and can provide a food source for other planktonic organisms. Thus, changes in Oithona spp. overall abundance and the timing of their annual maximum (i.e. phenology) can have important consequences for both energy flow within marine food webs and secondary production. Using the long term data (1954-2005) collected by the Continuous Plankton Recorder (CPR), the present study, investigates whether global climate warming my have affected the long term trends in Oithona spp. population abundance and phenology in relation to biotic and abiotic variables and over a wide latitudinal range and diverse oceanographic regions in the Atlantic, Pacific and Southern Ocean.

Biologging, Remotely-Sensed Oceanography and the Continuous Plankton Recorder Reveal the Environmental Determinants of a Seabird Wintering Hotspot

Marine environments are greatly affected by climate change, and understanding how this perturbation affects marine vertebrates is a major issue. In this context, it is essential to identify the environmental drivers of animal distribution. Here, we focused on the little auk (Alle alle), one of the world’s most numerous seabirds and a major component in Arctic food webs. Using a multidisciplinary approach, we show how little auks adopt specific migratory strategies and balance environmental constraints to optimize their energy budgets. Miniature electronic loggers indicate that after breeding, birds from East Greenland migrate .2000 km to overwinter in a restricted area off Newfoundland. Synoptic data available from the Continuous Plankton Recorder (CPR) indicate that this region harbours some of the highest densities of the copepod Calanus finmarchicus found in the North Atlantic during winter. Examination of large-scale climatic and oceanographic data suggests that little auks favour patches of high copepod abundance in areas where air temperature ranges from 0uC to 5uC. These results greatly advance our understanding of animal responses to extreme environmental constraints, and highlight that information on habitat preference is key to identifying critical areas for marine conservation.

Transient dynamics of an altered large marine ecosystem

Overfishing of large-bodied benthic fishes and their subsequent population collapses on the Scotian Shelf of Canada’s east coast1, 2 and elsewhere3, 4 resulted in restructuring of entire food webs now dominated by planktivorous, forage fish species and macroinvertebrates. Despite the imposition of strict management measures in force since the early 1990s, the Scotian Shelf ecosystem has not reverted back to its former structure. Here we provide evidence of the transient nature of this ecosystem and its current return path towards benthic fish species domination. The prolonged duration of the altered food web, and its current recovery, was and is being governed by the oscillatory, runaway consumption dynamics of the forage fish complex. These erupting forage species, which reached biomass levels 900% greater than those prevalent during the pre-collapse years of large benthic predators, are now in decline, having outstripped their zooplankton food supply. This dampening, and the associated reduction in the intensity of predation, was accompanied by lagged increases in species abundances at both lower and higher trophic levels, first witnessed in zooplankton and then in large-bodied predators, all consistent with a return towards the earlier ecosystem structure. We conclude that the reversibility of perturbed ecosystems can occur and that this bodes well for other collapsed fisheries.

Long-term changes in abundance and distribution of microzooplankton in the NE Atlantic and North Sea

Long-term changes in mesozooplankton and phytoplankton populations have been well documented in the North Atlantic region, whereas data for microzooplankton are scarce. This neglected component of the plankton is a vital link in marine food-webs, grazing on smaller flagellates and cyanobacteria and in turn providing food for the larger mesozooplankton. We use the latest tintinnid (Ciliophora, Protista) data from the Continuous Plankton Recorder (CPR) survey in the NE Atlantic and North Sea to examine the phenology, distribution and abundance of this important group of ciliates. Presence/absence data came from 167 122 CPR samples collected between 1960 and 2009 and abundance data from 49 662 samples collected between 1996 and 2009. In the North Atlantic the genus Dictyocysta spp. dominated and Parafavella gigantea showed an increase in abundance around Iceland and Greenland. In the North Sea higher densities of Tintinnopsis spp., Favella serrata and Ptychocylis spp. were found. The presence of tintinnids in CPR samples collected in the North Atlantic has increased over the last 50 years and the seasonal window of high abundance has lengthened. Conversely in the North Sea there has been an overall reduction in abundance. We discuss possible drivers for these long-term changes and point the way forward to more holistic studies that examine how ecosystems, rather than just selected taxa, are responding to climate change.

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.