On the processes linking climate to ecosystem changes

While documentation of climate effects on marine ecosystems has a long history, the underlying processes have often been elusive. In this paper we review some of the ecosystem responses to climate variability and discuss the possible mechanisms through which climate acts. Effects of climatological and oceanographic variables, such as temperature, sea ice, turbulence, and advection, on marine organisms are discussed in terms of their influence on growth, distribution, reproduction, activity rates, recruitment and mortality. Organisms tend to be limited to specific thermal ranges with experimental findings showing that sufficient oxygen supply by ventilation and circulation only occurs within these ranges. Indirect effects of climate forcing through effects on the food web are also discussed. Research and data needs required to improve our knowledge of the processes linking climate to ecosystem changes are presented along with our assessment of our ability to predict ecosystem responses to future climate change scenarios. (C) 2009 Elsevier B.V. All rights reserved.

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.

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.

Can the Continuous Plankton Recorder (CPR) be used to infer sardine diet?

Knowledge on the impact of climate variability in the diet of planktivorous fish is limited by the laborious work involved in stomach content analysis, impractical for large scale studies. Routine measurements of plankton such as the Continuous Plankton Recorder (CPR) survey provide valuable information of the temporal variation of phyto- and zooplankton prey availability for higher trophic levels. Sardines are a world-wide distributed and commercially important planktivorous fish, at the basis of the pelagic marine food web. Being predominantly non-selective filter-feeders, their diets closely correspond to the water plankton species and a significant relationship was recently found between Sardina pilchardus feeding intensity and remotely sensed chlorophyll alpha . Data of sardine stomach prey composition and CPR were obtained during 2003 for the same location off the west coast of Portugal, an area characterised by strong seasonality of plankton abundance and composition, mainly governed by upwelling events. Phyto- and zooplankton prey in sardine stomachs were identified to the lowest possible taxa and their numerical and volumetric abundance was registered, as well as their contribution to the prey carbon content. The seasonal variation of the abundance and composition of sardine diet was then compared to the abundance and composition of the water plankton obtained with the CPR at the same time and for the same area where the fish were collected, in order to evaluate if CPR data can be used to proxy sardine prey availability and diet composition at large temporal scales.

The meso-scale response of subarctic North Pacific seabird community structure to lower trophic level abundance and diversity

Understanding the mechanisms that structure communities and influence biodiversity are fundamental goals of ecology. To test the hypothesis that the abundance and diversity of upper-trophic level predators (seabirds) is related to the underlying abundance and diversity of their prey (zooplankton) and ecosystem-wide energy availability (primary production), we initiated a monitoring program in 2002 that jointly and repeatedly surveys seabird and zooplankton populations across a 7,500 km British Columbia-Bering Sea-Japan transect. Seabird distributions were recorded by a single observer (MH) using a strip-width technique, mesozooplankton samples were collected with a Continuous Plankton Recorder, and primary production levels were derived using the appropriate satellite parameters and the Vertically Generalized Production Model (Behrenfeld and Falkowski 1997). Each trophic level showed clear spatio-temporal patterns over the course of the study. The strongest relationship between seabird abundance and diversity and the lower trophic levels was observed in March/April ('spring') and significant relationships were also found through June/July ('summer'). No discernable relationships were observed during the September/October ('fall') months. Overall, mesozooplankton abundance and biomass explained the dominant portion of seabird abundance and diversity indices (richness, Simpson's Index, and evenness), while primary production was only related to seabird richness. These findings underscore the notion that perturbations of ocean productivity and lower trophic level ecosystem constituents influenced by climate change, such as shifts in timing (phenology) and synchronicity (match-mismatch), could impart far-reaching consequences throughout the marine food web.

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.

Influence of climate change and trophic coupling across four trophic levels in the Celtic Sea

Climate change has had profound effects upon marine ecosystems, impacting across all trophic levels from plankton to apex predators. Determining the impacts of climate change on marine ecosystems requires understanding the direct effects on all trophic levels as well as indirect effects mediated by trophic coupling. The aim of this study was to investigate the effects of climate change on the pelagic food web in the Celtic Sea, a productive shelf region in the Northeast Atlantic. Using long-term data, we examined possible direct and indirect ‘bottom-up’ climate effects across four trophic levels: phytoplankton, zooplankton, mid-trophic level fish and seabirds. During the period 1986–2007, although there was no temporal trend in the North Atlantic Oscillation index (NAO), the decadal mean Sea Surface Temperature (SST) in the Celtic Sea increased by 0.66±0.02°C. Despite this, there was only a weak signal of climate change in the Celtic Sea food web. Changes in plankton community structure were found, however this was not related to SST or NAO. A negative relationship occurred between herring abundance (0- and 1-group) and spring SST (0-group: p = 0.02, slope = −0.305±0.125; 1-group: p = 0.04, slope = −0.410±0.193). Seabird demographics showed complex species–specific responses. There was evidence of direct effects of spring NAO (on black-legged kittiwake population growth rate: p = 0.03, slope = 0.0314±0.014) as well as indirect bottom-up effects of lagged spring SST (on razorbill breeding success: p = 0.01, slope = −0.144±0.05). Negative relationships between breeding success and population growth rate of razorbills and common guillemots may be explained by interactions between mid-trophic level fish. Our findings show that the impacts of climate change on the Celtic Sea ecosystem is not as marked as in nearby regions (e.g. the North Sea), emphasizing the need for more research at regional scales.

Climate-induced changes in the North Sea Decapoda over the last 60 years

In the mid-1980s the North Sea ecosystem experienced a climate-induced regime shift that has favoured decapods and detritivores in the benthos and jellyfish in the plankton over commercial fisheries. Here, we investigate changes among the Decapoda in the North Sea plankton over the last 60 yr. Decapods are important predators in the plankton and the benthos where they can influence productivity and structure communities. In the North Sea it has been suggested that a climate-driven increase in decapod abundance has been important in propagating the climate signal through the North Sea food web. We show that climate-induced changes in the Decapoda in the central and southern North Sea include the presence of new warm-water taxa, changes in the abundance and proportions of commercial species of shrimp, and an earlier occurrence of decapod larvae in the plankton compared with the period 1981–1983. Notable amongst the warm-water taxa appearing in the North Sea is the predatory swimming crab Polybius henslowii that can swarm in large numbers when conditions are favourable and that is known to exhibit range shifts in response to fluctuations in hydroclimatic forcing. We suggest that climate-induced changes among North Sea decapods have played an important role in the trophic amplification of a climate signal and the development of the new North Sea dynamic regime. Understanding these changes is likely to be imperative for a successful ecosystem-based approach to the future management of North Sea fisheries at a time of climate change.

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.

North Sea ecosystem change from swimming crabs to seagulls

A recent increase in sea temperature has established a new ecosystem dynamic regime in the North Sea. Climate-induced changes in decapods have played an important role. Here, we reveal a coincident increase in the abundance of swimming crabs and lesser black-backed gull colonies in the North Sea, both in time and in space. Swimming crabs are an important food source for lesser black-backed gulls during the breeding season. Inhabiting the land, but feeding mainly at sea, lesser black-backed gulls provide a link between marine and terrestrial ecosystems, since the bottom-up influence of allochthonous nutrient input from seabirds to coastal soils can structure the terrestrial food web. We, therefore, suggest that climate-driven changes in trophic interactions in the marine food web may also have ensuing ramifications for the coastal ecology of the North Sea.

Comparisons of zooplankton time series

Evidence for climate-correlated low frequency variability of various components of marine ecosystems has accumulated rapidly over the past 2 decades. There has also been a growing recognition that society needs to learn how the fluctuations of these various components are linked, and to predict the likely amplitude and steepness of future changes. Demographic characteristics of marine zooplankton make them especially suitable for examining variability of marine ecosystems at interannual to decadal time scales. Their life cycle duration is short enough that there is little carryover of population membership from year to year, but long enough that variability can be tracked with monthly-to-seasonal sampling. Because zooplankton are rarely fished, comparative analysis of changes in their abundance can greatly enhance our ability to evaluate the importance of and interaction between physical environment, food web, and fishery harvest as causal mechanisms driving ecosystem level changes. A number of valuable within-region analyses of zooplankton time series have been published in the past decade, covering a variety of modes of variability including changes in total biomass, changes in size structure and species composition, changes in spatial distribution, and changes in seasonal timing. But because most zooplankton time series are relatively short compared to the time scales of interest, the statistical power of local analyses is often low, and between-region and between-variable comparisons are also needed. In this paper, we review the results of recent within- and between-region analyses, and suggest some priorities for future work.

Comparative analysis European wide marine ecosystem shifts - a large scale approach for developing the basis for ecosystem-based management

Abrupt and rapid ecosystem shifts (where major reorganizations of food-web and community structures occur), commonly termed regime shifts, are changes between contrasting and persisting states of ecosystem structure and function. These shifts have been increasingly reported for exploited marine ecosystems around the world from the North Pacific to the North Atlantic. Understanding the drivers and mechanisms leading to marine ecosystem shifts is crucial in developing adaptive management strategies to achieve sustainable exploitation of marine ecosystems. An international workshop on a comparative approach to analysing these marine ecosystem shifts was held at Hamburg University, Institute for Hydrobiology and Fisheries Science, Germany on 1-3 November 2010. Twenty-seven scientists from 14 countries attended the meeting, representing specialists from seven marine regions, including the Baltic Sea, the North Sea, the Barents Sea, the Black Sea, the Mediterranean Sea, the Bay of Biscay and the Scotian Shelf off the Canadian East coast. The goal of the workshop was to conduct the first large-scale comparison of marine ecosystem regime shifts across multiple regional areas, in order to support the development of ecosystem-based management strategies.

Biomass changes and trophic amplification of plankton in a warmer ocean

Ocean warming can modify the ecophysiology and distribution of marine organisms, and relationships between species, with nonlinear interactions between ecosystem components potentially resulting in trophic amplification. Trophic amplification (or attenuation) describe the propagation of a hydroclimatic signal up the food web, causing magnification (or depression) of biomass values along one or more trophic pathways. We have employed 3-D coupled physical-biogeochemical models to explore ecosystem responses to climate change with a focus on trophic amplification. The response of phytoplankton and zooplankton to global climate-change projections, carried out with the IPSL Earth System Model by the end of the century, is analysed at global and regional basis, including European seas (NE Atlantic, Barents Sea, Baltic Sea, Black Sea, Bay of Biscay, Adriatic Sea, Aegean Sea) and the Eastern Boundary Upwelling System (Benguela). Results indicate that globally and in Atlantic Margin and North Sea, increased ocean stratification causes primary production and zooplankton biomass to decrease in response to a warming climate, whilst in the Barents, Baltic and Black Seas, primary production and zooplankton biomass increase. Projected warming characterized by an increase in sea surface temperature of 2.29 ± 0.05 °C leads to a reduction in zooplankton and phytoplankton biomasses of 11% and 6%, respectively. This suggests negative amplification of climate driven modifications of trophic level biomass through bottom-up control, leading to a reduced capacity of oceans to regulate climate through the biological carbon pump. Simulations suggest negative amplification is the dominant response across 47% of the ocean surface and prevails in the tropical oceans; whilst positive trophic amplification prevails in the Arctic and Antarctic oceans. Trophic attenuation is projected in temperate seas. Uncertainties in ocean plankton projections, associated to the use of single global and regional models, imply the need for caution when extending these considerations into higher trophic levels.

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.

Flexible C : N ratio enhances metabolism of large phytoplankton when resource supply is intermittent

Phytoplankton cell size influences particle sinking rate, food web interactions and biogeographical distributions. We present a model in which the uptake, storage and assimilation of nitrogen and carbon are explicitly resolved in different-sized phytoplankton cells. In the model, metabolism and cellular C :N ratio are influenced by the accumulation of carbon polymers such as carbohydrate and lipid, which is greatest when cells are nutrient starved, or exposed to high light. Allometric relations and empirical data sets are used to constrain the range of possible C : N, and indicate that larger cells can accumulate significantly more carbon storage compounds than smaller cells. When forced with extended periods of darkness combined with brief exposure to saturating irradiance, the model predicts organisms large enough to accumulate significant carbon reserves may on average synthesize protein and other functional apparatus up to five times faster than smaller organisms. The advantage of storage in terms of average daily protein synthesis rate is greatest when modeled organisms were previously nutrient starved, and carbon storage reservoirs saturated. Small organisms may therefore be at a disadvantage in terms of average daily growth rate in environments that involve prolonged periods of darkness and intermittent nutrient limitation. We suggest this mechanism is a significant constraint on phytoplankton C :N variability and cell size distribution in different oceanic regimes.