Scaling up experimental ocean acidification and warming research: from individuals to the ecosystem

Understanding long-term, ecosystem-level impacts of climate change is challenging because experimental research frequently focuses on short-term, individual-level impacts in isolation. We address this shortcoming first through an inter-disciplinary ensemble of novel experimental techniques to investigate the impacts of 14-month exposure to ocean acidification and warming (OAW) on the physiology, activity, predatory behaviour and susceptibility to predation of an important marine gastropod (Nucella lapillus). We simultaneously estimated the potential impacts of these global drivers on N. lapillus population dynamics and dispersal parameters. We then used these data to parameterise a dynamic bioclimatic envelope model, to investigate the consequences of OAW on the distribution of the species in the wider NE Atlantic region by 2100. The model accounts also for changes in the distribution of resources, suitable habitat and environment simulated by finely resolved biogeochemical models, under three IPCC global emissions scenarios. The experiments showed that temperature had the greatest impact on individual level responses, while acidification has a similarly important role in the mediation of predatory behaviour and susceptibility to predators. Changes in Nucella predatory behaviour appeared to serve as a strategy to mitigate individual level impacts of acidification, but the development of this response may be limited in the presence of predators. The model projected significant large-scale changes in the distribution of Nucella by the year 2100 that were exacerbated by rising greenhouse gas emissions. These changes were spatially heterogeneous, as the degree of impact of OAW on the combination of responses considered by the model varied depending on local environmental conditions and resource availability. Such changes in macro-scale distributions cannot be predicted by investigating individual level impacts in isolation, or by considering climate stressors separately. Scaling up the results of experimental climate change research requires approaches that account for long-term, multi-scale responses to multiple stressors, in an ecosystem context.

Impacts of ocean acidification in a warming Mediterranean Sea: An overview

Mediterranean Sea fisheries supply significant local and international markets, based largely on small pelagic fish, artisanal fisheries and aquaculture of finfish (mainly seabass and seabream) and shellfish (mussels and oysters). Fisheries and aquaculture contribute to the economy of countries bordering this sea and provide food and employment to coastal communities employing ca 600,000 people. Increasing temperatures and heat wave frequency are causing stress and mortality in marine organisms and ocean acidification is expected to worsen these effects, especially for bivalves and coralligenous systems. Recruitment and seed production present possible bottlenecks for shellfish aquaculture in the future since early life stages are vulnerable to acidification and warming. Although adult finfish seem able to withstand the projected increases in seawater CO2, degradation of seabed habitats and increases in harmful blooms of algae and jellyfish might adversely affect fish stocks. Ocean acidification should therefore be factored into fisheries and aquaculture management plans. Rising CO2 levels are expected to reduce coastal biodiversity, altering ecosystem functioning and possibly impacting tourism being the Mediterranean the world’s most visited region. We recommend that ocean acidification is monitored in key areas of the Mediterranean Sea, with regular assessments of the likely socio-economic impacts to build adaptive strategies for the Mediterranean countries concerned.

Future fish distributions constrained by depth in warming seas

European continental shelf seas have experienced intense warming over the past 30 years1. In the North Sea, fish have been comprehensively monitored throughout this period and resulting data provide a unique record of changes in distribution and abundance in response to climate change2, 3. We use these data to demonstrate the remarkable power of generalized additive models (GAMs), trained on data earlier in the time series, to reliably predict trends in distribution and abundance in later years. Then, challenging process-based models that predict substantial and ongoing poleward shifts of cold-water species4, 5, we find that GAMs coupled with climate projections predict future distributions of demersal (bottom-dwelling) fish species over the next 50 years will be strongly constrained by availability of habitat of suitable depth. This will lead to pronounced changes in community structure, species interactions and commercial fisheries, unless individual acclimation or population-level evolutionary adaptations enable fish to tolerate warmer conditions or move to previously uninhabitable locations.

Future fish distributions constrained by depth in warming seas

European continental shelf seas have experienced intense warming over the past 30 years1. In the North Sea, fish have been comprehensively monitored throughout this period and resulting data provide a unique record of changes in distribution and abundance in response to climate change2, 3. We use these data to demonstrate the remarkable power of generalized additive models (GAMs), trained on data earlier in the time series, to reliably predict trends in distribution and abundance in later years. Then, challenging process-based models that predict substantial and ongoing poleward shifts of cold-water species4, 5, we find that GAMs coupled with climate projections predict future distributions of demersal (bottom-dwelling) fish species over the next 50 years will be strongly constrained by availability of habitat of suitable depth. This will lead to pronounced changes in community structure, species interactions and commercial fisheries, unless individual acclimation or population-level evolutionary adaptations enable fish to tolerate warmer conditions or move to previously uninhabitable locations.

Molecular analysis of Continuous Plankton Recorder samples, an examination of echinoderm larvae in the North Sea

Analysis of the biological time series of plankton samples collected by the Continuous Plankton Recorder (CPR) in the North Atlantic and North Sea has shown a regime shift in the plankton in this region. Both the distributions of planktonic organisms and their timing of occurrence in the seasonal cycle have changed and these changes appear to ref lect global warming. In the North Sea the planktonic larvae of echinoderms have shown a recent dramatic increase in both relative and absolute abundance and their seasonal peak of occurrence has advanced by 47 days. The identity of the echinoderm larvae involved in this change has, however, remained equivocal. The small size of many organisms like echinoderm larvae combined with incomplete taxonomic keys hinders their visual identification and their fragility often means that useful morphological features are damaged during sampling by the CPR. Here, using new molecular methods applied to CPR samples, we show that planktonic larvae of the benthic Echinocardium cordatum dominate the North Sea plankton. We argue that since this species benefits from mild winters and warmer waters their numerical increase in the plankton is consistent with recent climatic changes that appear to be affecting the wider ecology of this region.

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.

An overview of Calanus helgolandicus ecology in European waters

We review current knowledge and understanding of the biology and ecology of the calanoid copepod Calanus helgolandicus in European waters, as well as provide a collaborative synthesis of data from 18 laboratories and 26 sampling stations in areas distributed from the northern North Sea to the Aegean and Levantine Seas. This network of zooplankton time-series stations has enabled us to collect and synthesise seasonal and multi-annual data on abundance, body size, fecundity, hatching success and vertical distribution of C. helgolandicus. An aim was to enable comparison with its congener Calanus finmarchicus, which has been studied intensively as a key component of European and north east Atlantic marine ecosystems. C. finmarchicus is known to over-winter at depth, whereas the life-cycle of C. helgolandicus is less well understood. Overwintering populations of C. helgolandicus have been observed off the Atlantic coast between 400 and 800 m, while in the Mediterranean there is evidence of significant deep-water populations at depths as great as 4200 m. The biogeographical distribution of C. helgolandicus in European coastal waters covers a wide range of habitats, from open ocean to coastal environments, and its contribution to mesozooplankton biomass ranges from 6% to 93%. Highest abundances were recorded in the Adriatic and off the west coast of Spain. C. helgolandicus is generally found in 9-20 C water, with maximum abundances from 13-17 C. In contrast, C. finmarchicus is found in cooler water between 0 and 15 C, with peak abundances from 0 to 9 C. As water has warmed in the North Atlantic over recent decades, the range of C. helgolandicus and its abundance on the fringes of its expanding range have increased. This review will facilitate development of population models of C. helgolandicus. This will not only help answer remaining questions but will improve our ability to forecast future changes, in response to a warming climate, in the abundance and distribution of this important 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.

Marine biodiversity and climate change: assessing and predicting the influence of climatic change using intertidal rocky shore biota. Occasional Publication of the Marine Biological Association 20

In the last 60 years climate change has altered the distribution and abundance of many seashore species. Below is a summary of the findings of this project. The MarClim project was a four year multi-partner funded project created to investigate the effects of climatic warming on marine biodiversity. In particular the project aimed to use intertidal species, whose abundances had been shown to fluctuate with changes in climatic conditions, as indicator species of likely responses of species not only on rocky shores, but also those found offshore. The project used historic time series data, from in some cases the 1950s onwards, and contemporary data collected as part of the MarClim project (2001-2005), to provide evidence of changes in the abundance, range and population structure of intertidal species and relate these changes to recent rapid climatic warming. In particular quantitative counts of barnacles, limpets and trochids were made as well as semi-quantitative surveys of up to 56 intertidal taxa.Historic and contemporary data informed experiments to understand the mechanisms behind these changes and models to predict future species ranges and abundances.

Ocean structure and climate (Eastern North Atlantic): in situ measurement and remote sensing

Structure and climate of the east North Atlantic are appraised within a framework of in situ measurement and altimeter remote sensing from 0 degree - 60 degree N. Long zonal expendable bathythermograph /conductivity-temperature-depth probe sections show repeating internal structure in the North Atlantic Ocean. Drogued buoys and subsurface floats give westward speeds for eddies and wavelike structure. Records from longterm current meter deployments give the periodicity of the repeating structure. Eddy and wave characteristics of period, size or wavelength, westward propagation speed, and mean currents are derived at 20 degree N, 26 degree N, 32.5 degree N, 36 degree N and 48 degree N from in situ measurements in the Atlantic Ocean. It is shown that ocean wave and eddy-like features measured in situ correlate with altimeter structure. Interior ocean wave crests or cold dome-like temperature structures are cyclonic and have negative surface altimeter anomalies; mesoscale internal wave troughs or warm structures are anticyclonic and have positive surface height anomalies. Along the Eastern Boundary, flows and temperature climate are examined in terms of sla and North Atlantic Oscillation (NAO) Index. Longterm changes in ocean climate and circulation are derived from sla data. It is shown that longterm changes from 1992 to 2002 in the North Atlantic Current and the Subtropical Gyre transport determined from sla data correlate with winter NAO Index such that maximum flow conditions occurred in 1995 and 2000. Minimum circulation conditions occurred between 1996-1998. Years of extreme negative winter NAO Index result in enhanced poleward flow along the Eastern Boundary and anomalous winter warming along the West European Continental Slope as was measured in 1990, 1996, 1998 and 2001.

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.

Depth gradients of benthic standing stock and diversity on the continental margin at a high-latitude ice-free site (off Spitsbergen 79 degrees N)

High-latitude seas are mostly covered by multi-year ice, which impacts processes of primary production and sedimentation of organic matter. Because of the warming effect of West Spitsbergen Current (WSC), the waters off West Spitsbergen have only winter ice cover. That is uncommon for such a high latitude and enables to separate effects of multiyear-ice cover from the latitudinal patterns. Macrofauna was sampled off Kongsfjord (79°N) along the depth gradient from 300 to 3000 m. The density, biomass and diversity at shallow sites situated in a canyon were very variable. Biomass was negatively correlated with depth (R=-0.86R=-0.86, p<0.001), and ranged from 61 g ww m−2 (212 m) to 1 g ww m−2 (2025 m). The biomasses were much higher than in the multiyear-ice covered High Arctic at similar depths, while resembling those from temperate and tropical localities. Species richness (expressed by number of species per sample and species–area accumulation curves) decreased with depth. There was no clear depth-related pattern in diversity measures: Hurbert rarefaction, Shannon–Wiener or Pielou. The classic increase of species richness and diversity with depth was not observed. Species richness and diversity of deep-sea macrofauna were much lower in our study than in comparable studies of temperate North Atlantic localities. That is related to geographic isolation of Greenland–Icelandic–Norwegian (GIN) seas from the Atlantic pool of species.

Predicted levels of future ocean acidification and temperature rise could alter community structure and biodiversity in marine benthic communities

A mesocosm experiment was conducted to quantify the effects of reduced pH and elevated temperature on an intact marine invertebrate community. Standardised faunal communities, collected from the extreme low intertidal zone using artificial substrate units, were exposed to one of eight nominal treatments (four pH levels: 8.0, 7.7, 7.3 and 6.7, crossed with two temperature levels: 12 and 16°C). After 60 days exposure communities showed significant changes in structure and lower diversity in response to reduced pH. The response to temperature was more complex. At higher pH levels (8.0 and 7.7) elevated temperature treatments contained higher species abundances and diversity than the lower temperature treatments. In contrast, at lower pH levels (7.3 and 6.7), elevated temperature treatments had lower species abundances and diversity than lower temperature treatments. The species losses responsible for these changes in community structure and diversity were not randomly distributed across the different phyla examined. Molluscs showed the greatest reduction in abundance and diversity in response to low pH and elevated temperature, whilst annelid abundance and diversity was mostly unaffected by low pH and was higher at the elevated temperature. The arthropod response was between these two extremes with moderately reduced abundance and diversity at low pH and elevated temperature. Nematode abundance increased in response to low pH and elevated temperature, probably due to the reduction of ecological constraints, such as predation and competition, caused by a decrease in macrofaunal abundance. This community-based mesocosm study supports previous suggestions, based on observations of direct physiological impacts, that ocean acidification induced changes in marine biodiversity will be driven by differential vulnerability within and between different taxonomical groups. This study also illustrates the importance of considering indirect effects that occur within multispecies assemblages when attempting to predict the consequences of ocean acidification and global warming on marine communities.

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.