Covariance among North Sea ecosystem state indicators during the past 50 years - contrasts between coastal and open waters

Regime shift and principal component analysis of a spatially disaggregated database capturing time-series of climatic, nutrient and plankton variables in the North Sea revealed considerable covariance between groups of ecosystem indicators. Plankton and climate time-series span the period 1958–2003, those of nutrients start in 1980. In both regions, the period from 1989 to 2001 identified in principal component 1 had warmer surface waters, higher Atlantic inflow and stronger winds, than the periods before or after. However, it was preceded by a regime shift in both open (PC2) and coastal (PC3) waters during 1977 towards more hours of sunlight and higher water temperature, which lasted until 1997. The relative influence of nutrient availability and climatic forcing differed between open and coastal North Sea regions. Inter-annual variability in phytoplankton dynamics of the open North Sea was primarily regulated by climatic forcing, specifically by sea surface temperature, Atlantic inflow and co-varying wind stress and NAO. Coastal phytoplankton variability, however, was regulated by insolation and sea surface temperature, as well as Si availability, but not by N or P. Regime shifts in principal components of hydrographic and climatic variables (explaining 55 and 61% of the variance in coastal and open water variables) were detected using Rodionov's sequential t-test. These shifts in hydroclimatic variables which occurred around 1977, 1989, 1997 and 2001, were synchronized in open and coastal waters, and were tracked by open water chlorophyll and copepods, but not by coastal plankton. North–central–south or open-coastal spatial breakdowns of the North Sea explained similar amounts of variability in most ecosystem indicators with the exception of diatom abundance and chlorophyll concentration, which were clearly better explained using the open-coastal configuration.

Plankton indicators and ocean observing systems: support to the marine ecosystem state assessment

Ecological indicators are used extensively as tools to manage environmental resources. In the oceans, indicators of plankton can be measured using a variety of observing systems including: mooring stations, ships, autonomous floats and ocean colour remote sensing. Given the broad range of temporal and spatial sampling resolutions of these different observing systems, as well as discrepancies in measurements obtained from different sensors, the estimation and interpretation of plankton indicators can present significant challenges. To provide support to the assessment of the state of the marine ecosystem, we propose a suite of plankton indicators and subsequently classify them in an ecological framework that characterizes key attributes of the ecosystem. We present two case studies dealing with plankton indicators of biomass, size structure and phenology, estimated using the most spatially extensive and longest in situ and remote-sensing observations. Discussion of these studies illustrates how some of the challenges in estimating and interpreting plankton indicators may be addressed by using for example relative measurement thresholds, interpolation procedures and delineation of biogeochemical provinces. We demonstrate that one of the benefits attained, when analyzing a suite of plankton indicators classified in an ecological framework, is the elucidation of non-trivial changes in composition, structure and functioning of the marine ecosystem.

Region-wide changes in marine ecosystem dynamics: state-space models to distinguish trends from step changes

Regime shifts are sudden changes in ecosystem structure that can be detected across several ecosystem components. The concept that regime shifts are common in marine ecosystems has gained popularity in recent years. Many studies have searched for the step-like changes in ecosystem state expected under a simple interpretation of this idea. However, other kinds of change, such as pervasive trends, have often been ignored. We assembled over 300 ecological time series from seven UK marine regions, covering two to three decades. We developed state-space models for the first principal component of the time series in each region, a common measure of ecosystem state. Our models allowed both trends and step changes, possibly in combination. We found trends in three of seven regions and step changes in two of seven regions. Gradual and sudden changes are therefore important trajectories to consider in marine ecosystems.

How well do ecosystem indicators communicate the effects of anthropogenic eutrophication?

Anthropogenic eutrophication affects the Mediterranean, Black, North and Baltic Seas to various extents. Responses to nutrient loading and methods of monitoring relevant indicators vary regionally, hindering interpretation of ecosystem state changes and preventing a straightforward pan-European assessment of eutrophication symptoms. Here we summarize responses to nutrient enrichment in Europe's seas, comparing existing time-series of selected pelagic (phytoplankton biomass and community composition, turbidity, N:P ratio) and benthic (macro flora and faunal communities, bottom oxygen condition) indicators based on their effectiveness in assessing eutrophication effects. Our results suggest that the Black Sea and Northern Adriatic appear to be recovering from eutrophication due to economic reorganization in the Black Sea catchment and nutrient abatement measures in the case of the Northern Adriatic. The Baltic is most strongly impacted by eutrophication due to its limited exchange and the prevalence of nutrient recycling. Eutrophication in the North Sea is primarily a coastal problem, but may be exacerbated by climatic changes. Indicator interpretation is strongly dependent on sea-specific knowledge of ecosystem characteristics, and no single indicator can be employed to adequately compare eutrophication state between European seas. Communicating eutrophication-related information to policy-makers could be facilitated through the use of consistent indicator selection and monitoring methodologies across European seas. This work is discussed in the context of the European Commission's recently published Marine Strategy Directive.

The assessment of a global marine ecosystem model on the basis of emergent properties and ecosystem function: a case study with ERSEM

Ecosystem models are often assessed using quantitative metrics of absolute ecosystem state, but these model-data comparisons are disproportionately vulnerable to discrepancies in the location of important circulation features. An alternative method is to demonstrate the models capacity to represent ecosystem function; the emergence of a coherent natural relationship in a simulation indicates that the model may have an appropriate representation of the ecosystem functions that lead to the emergent relationship. Furthermore, as emergent properties are large-scale properties of the system, model validation with emergent properties is possible even when there is very little or no appropriate data for the region under study, or when the hydrodynamic component of the model differs significantly from that observed in nature at the same location and time. A selection of published meta-analyses are used to establish the validity of a complex marine ecosystem model and to demonstrate the power of validation with emergent properties. These relationships include the phytoplankton community structure, the ratio of carbon to chlorophyll in phytoplankton and particulate organic matter, the ratio of particulate organic carbon to particulate organic nitrogen and the stoichiometric balance of the ecosystem. These metrics can also inform aspects of the marine ecosystem model not available from traditional quantitative and qualitative methods. For instance, these emergent properties can be used to validate the design decisions of the model, such as the range of phytoplankton functional types and their behaviour, the stoichiometric flexibility with regards to each nutrient, and the choice of fixed or variable carbon to nitrogen ratios.

Abrupt shifts in the Gironde fish community: an indicator of ecological changes in an estuarine ecosystem

For decades, global climate change has directly and indirectly affected the structure and function of ecosystems. Abrupt changes in biodiversity have been observed in response to linear or sudden modifications to the environment. These abrupt shifts can cause long-term reorganizations within ecosystems, with communities exhibiting new functional responses to environmental factors. Over the last 3 decades, the Gironde estuary in southwest France has experienced 2 abrupt shifts in both the physical and chemical environments and the pelagic community. Rather than describing these shifts and their origins, we focused on the 3 inter-shift periods, describing the structure of the fish community and its relationship with the environment during these periods. We described fish biodiversity using a limited set of descriptors, taking into account both species composition and relative species abundances. Inter-shift ecosystem states were defined based on the relationship between this description and the hydro-physico-chemical variables and climatic indices defining the main features of the environment. This relationship was described using generalized linear mixed models on the entire time series and for each inter-shift period. Our results indicate that (1) the fish community structure has been significantly modified, (2) environmental drivers influencing fish diversity have changed during these 3 periods, and (3) the fish-environment relationships have been modified over time. From this, we conclude a regime shift has occurred in the Gironde estuary. We also highlight that anthropogenic influences have increased, which re-emphasizes the importance of local management in maintaining fish diversity and associated goods and services within the context of climate change.

The evaluation of time series: their scientific value and contribution to policy needs. Occasional Publication of the Marine Biological Association 22

In 2000 a Review of Current Marine Observations in relation to present and future needs was undertaken by the Inter-Agency Committee for Marine Science and Technology (IACMST). The Marine Environmental Change Network (MECN) was initiated in 2002 as a direct response to the recommendations of the report. A key part of the current phase of the MECN is to ensure that information from the network is provided to policy makers and other end-users to enable them to produce more accurate assessments of ecosystem state and gain a clearer understanding of factors influencing change in marine ecosystems. The MECN holds workshops on an annual basis, bringing together partners maintaining time-series and long-term datasets as well as end-users interested in outputs from the network. It was decided that the first workshop of the MECN continuation phase should consist of an evaluation of the time series and data sets maintained by partners in the MECN with regard to their ‘fit for purpose’ for answering key science questions and informing policy development. This report is based on the outcomes of the workshop. Section one of the report contains a brief introduction to monitoring, time series and long-term datasets. The various terms are defined and the need for MECN type data to complement compliance monitoring programmes is discussed. Outlines are also given of initiatives such as the United Kingdom Marine Monitoring and Assessment Strategy (UKMMAS) and Oceans 2025. Section two contains detailed information for each of the MECN time series / long-term datasets including information on scientific outputs and current objectives. This information is mainly based on the presentations given at the workshop and therefore follows a format whereby the following headings are addressed: Origin of time series including original objectives; current objectives; policy relevance; products (advice, publications, science and society). Section three consists of comments made by the review panel concerning all the time series and the network. Needs or issues highlighted by the panel with regard to the future of long-term datasets and time-series in the UK are shown along with advice and potential solutions where offered. The recommendations are divided into 4 categories; ‘The MECN and end-user requirements’; ‘Procedures & protocols’; ‘Securing data series’ and ‘Future developments’. Ever since marine environmental protection issues really came to the fore in the 1960s, it has been recognised that there is a requirement for a suitable evidence base on environmental change in order to support policy and management for UK waters. Section four gives a brief summary of the development of marine policy in the UK along with comments on the availability and necessity of long-term marine observations for the implementation of this policy. Policy relating to three main areas is discussed; Marine Conservation (protecting biodiversity and marine ecosystems); Marine Pollution and Fisheries. The conclusion of this section is that there has always been a specific requirement for information on long-term change in marine ecosystems around the UK in order to address concerns over pollution, fishing and general conservation. It is now imperative that this need is addressed in order for the UK to be able to fulfil its policy commitments and manage marine ecosystems in the light of climate change and other factors.

Unanticipated biological changes and global warming

Evidence of global warming is now unequivocal, and studies suggest that it has started to influence natural systems of the planet, including the oceans. However, in the marine environment, it is well-known that species and ecosystems can also be influenced by natural sources of large-scale hydro-climatological variability. The North Atlantic Oscillation (NAO) was negatively correlated with the mean abundance of one of the subarctic key species Calanus finmarchicus in the North Sea. This correlation was thought to have broken down in 1996, however, the timing has never been tested statistically. The present study revisits this unanticipated change and reveals that the correlation did not break down in 1996 as originally proposed but earlier, at the time of an abrupt ecosystem shift in the North Sea in the 1980s. Furthermore, the analyses demonstrate that the correlation between the NAO and C. finmarchicus abundance is modulated by the thermal regime of the North Sea, which in turn covaries positively with global temperature anomalies. This study thereby provides evidence that global climate change is likely to alter some empirical relationships found in the past between species abundance or the ecosystem state and large-scale natural sources of hydro-climatological variability. A theory is proposed to explain how this might happen. These unanticipated changes, also called ‘surprises’ in climatic research, are a direct consequence of the complexity of both climatic and biological systems. In this period of rapid climate change, it is therefore hazardous to integrate meteo-oceanic indices such as the NAO in models used in the management of living resources, as it has been sometimes attempted in the past.

Climate, plankton and cod

While a few North Atlantic cod stocks are stable, none have increased and many have declined in recent years. Although overfishing is the main cause of most observed declines, this study shows that in some regions, climate by its influence on plankton may exert a strong control on cod stocks, complicating the management of this species that often assumes a constant carrying capacity. First, we investigate the likely drivers of changes in the cod stock in the North Sea by evaluating the potential relationships between climate, plankton and cod. We do this by deriving a Plankton Index that reflects the quality and quantity of plankton food available for larval cod. We show that this Plankton Index explains 46.24% of the total variance in cod recruitment and 68.89% of the variance in total cod biomass. Because the effects of climate act predominantly through plankton during the larval stage of cod development, our results indicate a pronounced sensitivity of cod stocks to climate at the warmer, southern edge of their distribution, for example in the North Sea. Our analyses also reveal for the first time, that at a large basin scale, the abundance of Calanus finmarchicus is associated with a high probability of cod occurrence, whereas the genus Pseudocalanus appears less important. Ecosystem-based fisheries management (EBFM) generally considers the effect of fishing on the ecosystem and not the effect of climate-induced changes in the ecosystem state for the living resources. These results suggest that EBFM must consider the position of a stock within its ecological niche, the direct effects of climate and the influence of climate on the trophodynamics of the ecosystem.

Phytoplankton phenology indices in coral reef ecosystems: Application to ocean-color observations in the Red Sea

Phytoplankton, at the base of the marine food web, represent a fundamental food source in coral reef ecosystems. The timing (phenology) and magnitude of the phytoplankton biomass are major determinants of trophic interactions. The Red Sea is one of the warmest and most saline basins in the world, characterized by an arid tropical climate regulated by the monsoon. These extreme conditions are particularly challenging for marine life. Phytoplankton phenological indices provide objective and quantitative metrics to characterize phytoplank- ton seasonality. The indices i.e. timings of initiation, peak, termination and duration are estimated here using 15 years (1997–2012) of remote sensing ocean-color data from the European Space Agency (ESA) Climate Change Initiative project (OC-CCI) in the entire Red Sea basin. The OC-CCI product, comprising merged and bias-corrected observations from three independent ocean-color sensors (SeaWiFS, MODIS and MERIS), and processed using the POLYMER algorithm (MERIS period), shows a significant increase in chlorophyll data cover- age, especially in the southern Red Sea during the months of summer NW monsoon. In open and reef-bound coastal waters, the performance of OC-CCI chlorophyll data is shown to be comparable with the performance of other standard chlorophyll products for the global oceans. These features have permitted us to investigate phytoplankton phenology in the entire Red Sea basin, and during both winter SE monsoon and summer NW monsoon periods. The phenological indices are estimated in the four open water provinces of the basin, and further examined at six coral reef complexes of particular socio-economic importance in the Red Sea, including Siyal Islands, Sharm El Sheikh, Al Wajh bank, Thuwal reefs, Al Lith reefs and Farasan Islands. Most of the open and deeper waters of the basin show an apparent higher chlorophyll concentration and longer duration of phyto- plankton growth during the winter period (relative to the summer phytoplankton growth period). In contrast, most of the reef-bound coastal waters display equal or higher peak chlorophyll concentrations and equal or lon- ger duration of phytoplankton growth during the summer period (relative to the winter phytoplankton growth period). The ecological and biological significance of the phytoplankton seasonal characteristics are discussed in context of ecosystem state assessment, and particularly to support further understanding of the structure and functioning of coral reef ecosystems in the Red Sea.

4 ◦C and beyond: what did this mean for biodiversity in the past?

How do the predicted climatic changes (IPCC, 2007) for the next century compare in magnitude and rate to those that Earth has previously encountered? Are there comparable intervals of rapid rates of temperature change, sea-level rise and levels of atmospheric CO2 that can be used as analogues to assess possible biotic responses to future change? Or are we stepping into the great unknown? This perspective article focuses on intervals in time in the fossil record when atmospheric CO2 concentrations increased up to 1200 ppmv, temperatures in mid- to high-latitudes increased by greater than 4 ?C within 60 years, and sea levels rose by up to 3 m higher than present. For these intervals in time, case studies of past biotic responses are presented to demonstrate the scale and impact of the magnitude and rate of such climate changes on biodiversity. We argue that although the underlying mechanisms responsible for these past changes in climate were very different (i.e. natural processes rather than anthropogenic), the rates and magnitude of climate change are similar to those predicted for the future and therefore potentially relevant to understanding future biotic response. What emerges from these past records is evidence for rapid community turnover, migrations, development of novel ecosystems and thresholds from one stable ecosystem state to another, but there is very little evidence for broad-scale extinctions due to a warming world. Based on this evidence from the fossil record, we make four recommendations for future climate-change integrated conservation strategies.

Herbivore and nutrient impact on primary producer assemblages in a tropical marine environment

Globally, human populations are increasing and coastal ecosystems are becoming increasingly impacted by anthropogenic stressors. As eutrophication and exploitation of coastal resources increases, primary producer response to these drivers becomes a key indicator of ecosystem stability. Despite the importance of monitoring primary producers such as seagrasses and macroalgae, detailed studies on the response of these benthic habitat components to drivers remain relatively sparse. Utilizing a multi-faceted examination of turtle-seagrass and sea urchin-macroalgae consumer and nutrient dynamics, I elucidate the impact of these drivers in Akumal, Quintana Roo, Mexico. In Yal Ku Lagoon, macroalgae bioindicators signified high nutrient availability, which is important for further studies, but did not consistently follow published trends reflecting decreased δ 15N content with distance from suspected source. In Akumal Bay, eutrophication and grazing by turtles and fishes combine to structure patches within the seagrass beds. Grazed seagrass patches had higher structural complexity and productivity than patches continually grazed by turtles and fishes. Results from this study indicate that patch abandonment may follow giving-up density theory, the first to be recorded in the marine environment. As Diadema antillarum populations recover after their massive mortality thirty years ago, the role these echinoids will have in reducing macroalgae cover and altering ecosystem state remains to be clear. Although Diadema antillarum densities within the coral reef ecosystem were comparable to other regions within the Caribbean, the echinoid population in Akumal Bay was an insufficient driver to prevent dominance of a turf-algal-sediment (TAS) state. After a four year study, declining coral cover coupled with increased algal cover suggests that the TAS-dominated state is likely to persist over time despite echinoid recovery. Studies on macroalgal diversity and nutrients within this same region of echinoids indicated diversity and nutrient content of macroalgae increased, which may further increase the persistence of the algal-dominated state. This study provides valuable insight into the variable effects of herbivores and nutrients on primary producers within a tropical coastal ecosystem. Results from this work challenge many of the currently accepted theories on primary producer response to nutrients and herbivory while providing a framework for further studies into these dynamics.

Environmental controls on bioturbation processes in marine benthic habits

Through bioturbation, the macrofauna mediate chemical, physical and biological processes in marine benthic ecosystems. Because of the importance of bioturbation as ecosystem mediator, various studies have been conducted on bioturbation intensity and depth, and the relation of bioturbation processes to environmental condition and ecosystem state. This thesis builds on those previous studies, using a standard field and analytical protocol and by expanding the geographical scale to three climatic regions along Canada’s East Coast and Arctic margins, the Arctic Archipelago, the coastal Subarctic (Labrador Fjords), and the temperate continental climate zone (Gulf of Maine and adjacent Scotian shelf/slope). This Ph.D. study provides a comprehensive assessment of environmental influences on bioturbation along gradients in latitude and ocean depth. Bioturbation intensity, mixing depth, and bioturbation structures were studied in relation to the quantity and quality of potential food sources (organic matter) and substrate characteristics to gain an understanding of the environmental controls on bioturbation in these regions. The three main research chapters of this thesis are divided based on the contrasting climatic and geographical regions studied. The analytical approach included seabed sampling with a boxcorer, describing the sedimentary fabric and bioturbation structures by X-radiography, estimating bioturbation intensity and depth applying a biodiffusion model to particle tracer profiles of ²¹⁰Pbₓs, ²²⁸Thₓs, ²³⁴Thₓs, and chlorophyll-a, and analyzing benthic organic matter and substrate characteristics. Strong regional and cross-climatic relations of bioturbation processes with combinations of environmental factors were observed. In particular, bioturbation depth and the vertical extent of bioturbation structures responded to the environmental patterns observed and, therefore, represented potentially applicable predictors of environmental conditions and ecosystem state. The results of this Ph.D. study may be further extended to other geographical regions with similar environmental characteristics to predict the effects of benthic habitat alterations through environmental stresses on a global scale. Integrated with biological data produced by fellow CHONe scientists the presented data may provide valuable information about functional roles of macrofaunal species and community traits in marine benthic ecosystems along Canada’s extensive East Coast and Arctic margins.