Impact of climate change on marine pelagic phenology and trophic mismatch

Phenology, the study of annually recurring life cycle events such as the timing of migrations and flowering, can provide particularly sensitive indicators of climate change. Changes in phenology may be important to ecosystem function because the level of response to climate change may vary across functional groups and multiple trophic levels. The decoupling of phenological relationships will have important ramifications for trophic interactions, altering food-web structures and leading to eventual ecosystem-level changes. Temperate marine environments may be particularly vulnerable to these changes because the recruitment success of higher trophic levels is highly dependent on synchronization with pulsed planktonic production. Using long-term data of 66 plankton taxa during the period from 1958 to 2002, we investigated whether climate warming signals are emergent across all trophic levels and functional groups within an ecological community. Here we show that not only is the marine pelagic community responding to climate changes, but also that the level of response differs throughout the community and the seasonal cycle, leading to a mismatch between trophic levels and functional groups.

Is observed variability in the long-term results of the Continuous Plankton Recorder survey a response to climate change?

In the more than 50 years that the Continuous Plankton Recorder (CPR) survey has operated on a regular monthly basis in the north-east Atlantic and North Sea, large changes have been witnessed in the planktonic ecosystem. These changes have taken the form of long-term trends in abundance for certain species or stepwise changes for others, and in many cases are correlated with a mode of climatic variability in the North Atlantic, either: (1) the North Atlantic Oscillation (NAO), a basin-scale atmospheric alteration of the pressure field between the Azores high pressure cell and the Icelandic Low; or (2) the Gulf Stream Index (GSI), which measures the latitudinal position of the north wall of the Gulf Stream. Recent work has shown that the changes in the GSI are coupled with the NAO and Pacific Southern Oscillation with a 2 year lag. The plankton variability is also possibly linked to changes observed in the distribution and flux of water masses in the surface, intermediate and deep waters of the North Atlantic. For example, in the last two decades, the extent and location of the formation of North Atlantic Deep Water, Labrador Sea Intermediate Water and Norwegian Sea intermediate and upper-layer water has altered considerably. This paper discusses the extent to which observed changes in plankton abundance and distribution may be linked to this basin-scale variability in hydrodynamics. The results are also placed within the context of global climate warming and the possible effects of the observed melting of Arctic permafrost and sea ice on the subpolar North Atlantic.

DISCOVERY 2010: Spatial and temporal variability in a dynamic polar ecosystem

The Scotia Sea has been a focus of biological- and physical oceanographic study since the Discovery expeditions in the early 1900s. It is a physically energetic region with some of the highest levels of productivity in the Southern Ocean. It is also a region within which there have been greater than average levels of change in upper water column temperature. We describe the results of three cruises transecting the central Scotia Sea from south to north in consecutive years and covering spring, summer and autumn periods. We also report on some community level syntheses using both current-day and historical data from this region. A wide range of parameters were measured during the field campaigns, covering the physical oceanography of the region, air–sea CO2 fluxes, macro- and micronutrient concentrations, the composition and biomass of the nano-, micro- and mesoplankton communities, and the distribution and biomass of Antarctic krill and mesopelagic fish. Process studies examined the effect of iron-stress on the physiology of primary producers, reproduction and egestion in Antarctic krill and the transfer of stable isotopes between trophic layers, from primary consumers up to birds and seals. Community level syntheses included an examination of the biomass-spectra, food-web modelling, spatial analysis of multiple trophic layers and historical species distributions. The spatial analyses in particular identified two distinct community types: a northern warmer water community and a southern cold community, their boundary being broadly consistent with the position of the Southern Antarctic Circumpolar Current Front (SACCF). Temperature and ice cover appeared to be the dominant, over-riding factors in driving this pattern. Extensive phytoplankton blooms were a major feature of the surveys, and were persistent in areas such as South Georgia. In situ and bioassay measurements emphasised the important role of iron inputs as facilitators of these blooms. Based on seasonal DIC deficits, the South Georgia bloom was found to contain the strongest seasonal carbon uptake in the ice-free zone of the Southern Ocean. The surveys also encountered low-production, iron-limited regions, a situation more typical of the wider Southern Ocean. The response of primary and secondary consumers to spatial and temporal heterogeneity in production was complex. Many of the life-cycles of small pelagic organisms showed a close coupling to the seasonal cycle of food availability. For instance, Antarctic krill showed a dependence on early, non-ice-associated blooms to facilitate early reproduction. Strategies to buffer against environmental variability were also examined, such as the prevalence of multiyear life-cycles and variability in energy storage levels. Such traits were seen to influence the way in which Scotia Sea communities were structured, with biomass levels in the larger size classes being higher than in other ocean regions. Seasonal development also altered trophic function, with the trophic level of higher predators increasing through the course of the year as additional predator-prey interactions emerged in the lower trophic levels. Finally, our studies re-emphasised the role that the simple phytoplankton-krill-higher predator food chain plays in this Southern Ocean region, particularly south of the SACCF. To the north, alternative food chains, such as those involving copepods, macrozooplankton and mesopelagic fish, were increasingly important. Continued ocean warming in this region is likely to increase the prevalence of such alternative such food chains with Antarctic krill predicted to move southwards.

Impact of climate change on Antarctic krill

Antarctic krill Euphausia superba (hereafter ‘krill’) occur in regions undergoing rapid environmental change, particularly loss of winter sea ice. During recent years, harvesting of krill has increased, possibly enhancing stress on krill and Antarctic ecosystems. Here we review the overall impact of climate change on krill and Antarctic ecosystems, discuss implications for an ecosystem-based fisheries management approach and identify critical knowledge gaps. Sea ice decline, ocean warming and other environmental stressors act in concert to modify the abundance, distribution and life cycle of krill. Although some of these changes can have positive effects on krill, their cumulative impact is most likely negative. Recruitment, driven largely by the winter survival of larval krill, is probably the population parameter most susceptible to climate change. Predicting changes to krill populations is urgent, because they will seriously impact Antarctic ecosystems. Such predictions, however, are complicated by an intense inter-annual variability in recruitment success and krill abundance. To improve the responsiveness of the ecosystem-based management approach adopted by the Commission for the Conservation of Antarctic Marine Living Resources (CCAMLR), critical knowledge gaps need to be filled. In addition to a better understanding of the factors influencing recruitment, management will require a better understanding of the resilience and the genetic plasticity of krill life stages, and a quantitative understanding of under-ice and benthic habitat use. Current precautionary management measures of CCAMLR should be maintained until a better understanding of these processes has been achieved.

Potential Climate Change Effects on the Habitat of Antarctic Krill in the Weddell Quadrant of the Southern Ocean

Antarctic krill is a cold water species, an increasingly important fishery resource and a major prey item for many fish, birds and mammals in the Southern Ocean. The fishery and the summer foraging sites of many of these predators are concentrated between 0 degrees and 90 degrees W. Parts of this quadrant have experienced recent localised sea surface warming of up to 0.2 degrees C per decade, and projections suggest that further widespread warming of 0.27 degrees to 1.08 degrees C will occur by the late 21st century. We assessed the potential influence of this projected warming on Antarctic krill habitat with a statistical model that links growth to temperature and chlorophyll concentration. The results divide the quadrant into two zones: a band around the Antarctic Circumpolar Current in which habitat quality is particularly vulnerable to warming, and a southern area which is relatively insensitive. Our analysis suggests that the direct effects of warming could reduce the area of growth habitat by up to 20%. The reduction in growth habitat within the range of predators, such as Antarctic fur seals, that forage from breeding sites on South Georgia could be up to 55%, and the habitat's ability to support Antarctic krill biomass production within this range could be reduced by up to 68%. Sensitivity analysis suggests that the effects of a 50% change in summer chlorophyll concentration could be more significant than the direct effects of warming. A reduction in primary production could lead to further habitat degradation but, even if chlorophyll increased by 50%, projected warming would still cause some degradation of the habitat accessible to predators. While there is considerable uncertainty in these projections, they suggest that future climate change could have a significant negative effect on Antarctic krill growth habitat and, consequently, on Southern Ocean biodiversity and ecosystem services.

Projected impacts of climate change on marine fish and fisheries

This paper reviews current literature on the projected effects of climate change on marine fish and shellfish, their fisheries, and fishery-dependent communities throughout the northern hemisphere. The review addresses the following issues: (i) expected impacts on ecosystem productivity and habitat quantity and quality; (ii) impacts of changes in production and habitat on marine fish and shellfish species including effects on the community species composition, spatial distributions, interactions, and vital rates of fish and shellfish; (iii) impacts on fisheries and their associatedcommunities; (iv) implications for food security and associated changes; and (v) uncertainty andmodelling skill assessment. Climate change will impact fish and shellfish, their fisheries, and fishery-dependent communities through a complex suite of linked processes. Integrated interdisciplinary research teams are forming in many regions to project these complex responses. National and international marine research organizations serve a key role in the coordination and integration of research to accelerate the production of projections of the effects of climate change on marine ecosystems and to move towards a future where relative impacts by region could be compared on a hemispheric or global level. Eight research foci were identified that will improve the projections of climate impacts on fish, fisheries, and fishery-dependent communities.

Causes and prediction of abrupt climate-driven ecosystem shifts in the North Atlantic

Warming of the global climate is now unequivocal and its impact on Earth’ functional units has become more apparent. Here, we show that marine ecosystems are not equally sensitive to climate change and reveal a critical thermal boundary where a small increase in temperature triggers abrupt ecosystem shifts seen across multiple trophic levels. This large-scale boundary is located in regions where abrupt ecosystem shifts have been reported in the North Atlantic sector and thereby allows us to link these shifts by a global common phenomenon. We show that these changes alter the biodiversity and carrying capacity of ecosystems and may, combined with fishing, precipitate the reduction of some stocks of Atlantic cod already severely impacted by exploitation. These findings offer a way to anticipate major ecosystem changes and to propose adaptive strategies for marine exploited resources such as cod in order to minimize social and economic consequences.

Marine biodiversity, ecosystem functioning and carbon cycles

Although recent studies suggest that climate change may substantially accelerate the rate of species loss in the biosphere, only a few studies have focused on the potential consequences of a spatial reorganization of biodiversity with global warming. Here, we show a pronounced latitudinal increase in phytoplanktonic and zooplanktonic biodiversity in the extratropical North Atlantic Ocean in recent decades. We also show that this rise in biodiversity paralleled a decrease in the mean size of zooplanktonic copepods and that the reorganization of the planktonic ecosystem toward dominance by smaller organisms may influence the networks in which carbon flows, with negative effects on the downward biological carbon pump and demersal Atlantic cod (Gadus morhua). Our study suggests that, contrary to the usual interpretation of increasing biodiversity being a positive emergent property promoting the stability/resilience of ecosystems, the parallel decrease in sizes of planktonic organisms could be viewed in the North Atlantic as reducing some of the services provided by marine ecosystems to humans.

Long-term responses of North Atlantic calcifying plankton to climate change

The global increase in atmospheric carbon dioxide concentration is potentially threatening marine biodiversity in two ways. First, carbon dioxide and other greenhouse gases accumulating in the atmosphere are causing global warming1. Second, carbon dioxide is altering sea water chemistry, making the ocean more acidic2. Although temperature has a cardinal influence on all biological processes from the molecular to the ecosystem level3, acidification might impair the process of calcification or exacerbate dissolution of calcifying organisms4. Here, we show however that North Atlantic calcifying plankton primarily responded to climate-induced changes in temperatures during the period 1960–2009, overriding the signal from the effects of ocean acidification. We provide evidence that foraminifers, coccolithophores, both pteropod and nonpteropod molluscs and echinoderms exhibited an abrupt shift circa 1996 at a time of a substantial increase in temperature5 and that some taxa exhibited a poleward movement in agreement with expected biogeographical changes under sea temperature warming6,7. Although acidification may become a serious threat to marine calcifying organisms, our results suggest that over the study period the primary driver of North Atlantic calcifying planktonwas oceanic temperature.

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.

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.

Synergistic effects of climate and fishing in a marine ecosystem

Current climate change and overfishing are affecting the productivity and structure of marine ecosystems. This situation is unprecedented for the marine biosphere and it is essential to understand the mechanisms and pathways by which ecosystems respond. We report that climate change and overfishing are likely to be responsible for a rapid restructuring of a highly productive marine ecosystem with effects throughout the pelagos and the benthos. In the mid-1980s, climate change, consequent modifications in the North Sea plankton, and fishing, all reduced North Sea cod recruitment. In this region, production of many benthic species respond positively and immediately to temperature. Analysis of a long-term, spatially extensive biological (plankton and cod) and physical (sea surface temperature) dataset suggests that synchronous changes in cod numbers and sea temperature have established an extensive trophic cascade favoring lower trophic level groups over economic fisheries. A proliferation of jellyfish that we detect may signal the climax of these changes. This modified North Sea ecology may provide a clear indication of the synergistic consequences of coincident climate change and overfishing. The extent of the ecosystem restructuring that has occurred in the North Sea suggests we are unlikely to reverse current climate and human-induced effects through ecosystem resource management in the short term. Rather, we should understand and adapt to new ecological regimes. This implies that fisheries management policies will have to be fully integrated with the ecological consequences of climate change to prevent a similar collapse in an exploited marine ecosystem elsewhere.

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.

Variation among northeast Atlantic regions in the responses of zooplankton to climate change: Not all areas follow the same path

Broad scale climate forcing can interact with local environmental processes to affect the observed ecological phenomena. This causes potential problems of over-extrapolation for results from a limited number of sites or the averaging out of region-specific responses if data from too wide an area are combined. In this study, an area similar in extent to the Celtic Biscay Large Marine Ecosystem, but including off-shelf areas, was partitioned using clustering of satellite chlorophyll (chl-a) measurements. The resulting clusters were used to define areas over which to combine copepod data from the Continuous Plankton Recorder. Following filtering due to data limitations, nine regions were defined with sufficient records for analysis. These regions were consistent with known oceanographic structure in the study area. Off-shelf regions showed a progressively later timing in the seasonal peak of chl-a measurements moving northwards. Generalised additive models were used to estimate seasonal and multiannual signals in the adult and juvenile stages of Calanus finmarchicus, C. helgolandicus and the Paracalanus–Pseudocalanus group. Associations between variables (sea surface temperature (SST), phenology and annual abundance) differed among taxonomic groups, but even within taxonomic groups, relationships were not consistent across regions. For example, in the deep waters off Spain and Portugal the annual abundance of Calanus finmarchicus has a weak positive association with SST, in contrast to the pattern in most other regions. The regions defined in this study provide an objective basis for investigations into the long term dynamics of plankton populations and suggest suitable sub regions for deriving pelagic system indicators.