Phenological trends and trophic mismatch across multiple levels of a North Sea pelagic food web

Differential phenological responses to climate among species are predicted to disrupt trophic interactions, but datasets to evaluate this are scarce. We compared phenological trends for species from 4 levels of a North Sea food web over 24 yr when sea surface temperature (SST) increased significantly. We found little consistency in phenological trends between adjacent trophic levels, no significant relationships with SST, and no significant pairwise correlations between predator and prey phenologies, suggesting that trophic mismatching is occurring. Finer resolution data on timing of peak energy demand (mid-chick-rearing) for 5 seabird species at a major North Sea colony were compared to modelled daily changes in length of 0-group (young of the year) lesser sandeels Ammodytes marinus. The date at which sandeels reached a given threshold length became significantly later during the study. Although the phenology of all the species except shags also became later, these changes were insufficient to keep pace with sandeel length, and thus mean length (and energy value) of 0-group sandeels at mid-chick-rearing showed net declines. The magnitude of declines in energy value varied among the seabirds, being more marked in species showing no phenological response (shag, 4.80 kJ) and in later breeding species feeding on larger sandeels (kittiwake, 2.46 kJ) where, due to the relationship between sandeel length and energy value being non-linear, small reductions in length result in relatively large reductions in energy. However, despite the decline in energy value of 0-group sandeels during chick-rearing, there was no evidence of any adverse effect on breeding success for any of the seabird species. Trophic mismatch appears to be prevalent within the North Sea pelagic food web, suggesting that ecosystem functioning may be disrupted.

Temporal changes in plankton of the North Sea: community shifts and environmental drivers

This paper analyses long-term and seasonal changes in the North Sea plankton community during the period 1970 to 2008. Based on Continuous Plankton Recorder (CPR) data covering 38 yr, major changes in both phytoplankton and zooplankton abundance and community structure were identified. Regime changes were detected around 1978, 1989 and 1998. The first 2 changes have been discussed in the literature and are defined as a cold episodic event (1978) and a regime shift towards a warm dynamic regime (1989). The effect of these 2 regime changes on plankton indicators was assessed and checked against previous studies. The 1998 change represents a shift in the abundance and seasonal patterns of dinoflagellates and the dominant zooplankton group, the neritic copepods. Furthermore, environmental factors such as air temperature, wind speed and the North Atlantic water inflow were identified as potential drivers of change in seasonal patterns, and the most-likely environmental causes for detected changes were assessed. We suggest that a change in the balance of dissolved nutrients driven by these environmental factors was the cause of the latest change in plankton community structure, which in turn could have affected the North Sea fish community.

Biodiversity and ecosystems: Change at the community level

Some commercial fish species of the northeast Atlantic Ocean have relocated in response to warming. The impact of warming on marine assemblages in the region may already be much greater than appreciated, however, with over 70% of common demersal fish species responding through changes in abundance, rather than range. The northeast Atlantic Ocean is one of the most productive marine ecoregions in the world with a substantial commercial fishery. It is also a region that has undergone particularly rapid warming over the past 50 years, up to four times faster than the global average1. Compared with other marine regions worldwide, the biological response in the northeast Atlantic Ocean has been particularly dramatic, reflecting this rapid warming. Studies have documented biogeographical movements in marine plankton of over 1,000 km northwards2 and advances in the onset of key life-history events by six to eight weeks3. In addition, there has been limited evidence of distributional shifts in some fish species along latitudinal and depth gradients in response to warming4, 5. Writing in Current Biology, Stephen Simpson and colleagues6 present the most comprehensive analysis so far of the impact of warming on commercially important European continental-shelf fish species in the region, and in doing so show that there has been a profound reorganization of local communities.

Synchronous response of marine plankton ecosystems to climate in the Northeast Atlantic and the North Sea

Over the last few decades, global warming has accelerated both the rate and magnitude of changes observed in many functional units of the Earth System. In this context, plankton are sentinel organisms because they are sensitive to subtle levels of changes in temperature and might help in identifying the current effects of climate change on pelagic ecosystems. In this paper, we performed a comparative approach in two regions of the North Atlantic (i.e. the Northeast Atlantic and the North Sea) to explore the relationships between changes in marine plankton, the regional physico-chemical environment and large-scale hydro-climatic forcing using four key indices: the North Atlantic Oscillation (NAO), the Atlantic Multidecadal Oscillation (AMO), the East Atlantic (EA) pattern and Northern Hemisphere Temperature (NHT) anomalies. Our analyses suggest that long-term changes in the states of the two ecosystems were synchronous and correlated to the same large-scale hydro-climatic variables: NHT anomalies, the AMO and to a lesser extent the EA pattern. No significant correlation was found between long-term ecosystem modifications and the state of the NAO. Our results suggest that the effect of climate on these ecosystems has mainly occurred in both regions through the modulation of the thermal regime.

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.

Monitoring marine plankton ecosystems: Identification of the most relevant indicators of the state of an ecosystem

The number of variables involved in the monitoring of an ecosystem can be high and often one of the first stages in the analysis is to reduce the number of variables. We describe a method developed for geological purposes, using the information theory, that enables selection of the most relevant variables. This technique also allows the examination of the asymmetrical relationships between variables. Applied to a set of physical and biological variables (plankton assemblages in four areas of the North Sea), the method shows that biological variables are more informative than physical variables although the controlling factors are mainly physical (sea surface temperature in winter and spring). Among biological variables, diversity measures and warm-water species assemblages are informative for the state of the North Sea pelagic ecosystems while among physical variables sea surface temperature in late winter and early spring are highly informative. Although often used in bioclimatology, the utilisation of the North Atlantic Oscillation (NAO) index does not seem to provide a lot of information. The method reveals that only the extreme states of this index has an influence on North Sea pelagic ecosystems. The substantial and persistent changes that were detected in the dynamic regime of the North Sea ecosystems and called regime shift are detected by the method and corresponds to the timing of other shifts described in the literature for some European Systems such as the Baltic and the Mediterranean Sea when both physical and biological variables are considered.

Marine plankton phenology and life history in a changing climate: current research and future directions

Increasing availability and extent of biological ocean time series (from both in situ and satellite data) have helped reveal significant phenological variability of marine plankton. The extent to which the range of this variability is modified as a result of climate change is of obvious importance. Here we summarize recent research results on phenology of both phytoplankton and zooplankton. We suggest directions to better quantify and monitor future plankton phenology shifts, including (i) examining the main mode of expected future changes (ecological shifts in timing and spatial distribution to accommodate fixed environmental niches vs. evolutionary adaptation of timing controls to maintain fixed biogeography and seasonality), (ii) broader understanding of phenology at the species and community level (e.g. for zooplankton beyond Calanus and for phytoplankton beyond chlorophyll), (iii) improving and diversifying statistical metrics for indexing timing and trophic synchrony and (iv) improved consideration of spatio-temporal scales and the Lagrangian nature of plankton assemblages to separate time from space changes.

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.

Challenges for implementing the Marine Strategy Framework Directive in a climate of macroecological change

Unprecedented basin-scale ecological changes are occurring in our seas. As temperature and carbon dioxide concentrations increase, the extent of sea ice is decreasing, stratification and nutrient regimes are changing and pH is decreasing. These unparalleled changes present new challenges for managing our seas, as we are only just beginning to understand the ecological manifestations of these climate alterations. The Marine Strategy Framework Directive requires all European Member States to achieve good environmental status (GES) in their seas by 2020; this means management towards GES will take place against a background of climate-driven macroecological change. Each Member State must set environmental targets to achieve GES; however, in order to do so, an understanding of large-scale ecological change in the marine ecosystem is necessary. Much of our knowledge of macroecological change in the North Atlantic is a result of research using data gathered by the Continuous Plankton Recorder (CPR) survey, a near-surface plankton monitoring programme that has been sampling in the North Atlantic since 1931. CPR data indicate that North Atlantic and North Sea plankton dynamics are responding to both climate and human-induced changes, presenting challenges to the development of pelagic targets for achievement of GES in European Seas. Thus, the continuation of long-term ecological time series such as the CPR survey is crucial for informing and supporting the sustainable management of European seas through policy mechanisms.

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.

Mediterranean marine copepods: basin-scale trends of the calanoid Centropages typicus

The Mediterranean Sea is located in a crossroad of mid-latitude and subtropical climatic modes that enhance contrasting environmental conditions over both latitudinal and longitudinal ranges. Here, we show that the large-scale environmental forcing is reflected in the basin scale trends of the adult population of the calanoid copepod Centropages typicus. The species is distributed over the whole Mediterranean basin, and maximal abundances were found in the north-western basin associated to oceanic fronts, and in the Adriatic Sea associated to shallow and semi enclosed waters. The peak of main abundances of C. typicus correlates with the latitudinal temperature gradient and the highest seasonal abundances occurred in spring within the 14–18°C temperature window. Such thermal cline may define the latitudinal geographic region where C. typicus seasonally dominates the >200 μm-sized spring copepod community in the Mediterranean Sea. The approach used here is generally applicable to investigate the large-scale spatial patterns of other planktonic organisms and to identify favourable environmental windows for population development.

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.

Biodiversity as a dynamic variable in the Gulf of Maine continuous plankton recorder transect

Studies relating biodiversity to ecosystem processes typically do not take into account changes in biodiversity through time. Marine systems are highly dynamic, with biodiversity changing at diel, seasonal and inter-decadal timescales. We examined the dynamics of biodiversity in the Gulf of Maine pelagic zooplankton community. Taxonomic data came from the Gulf of Maine continuous plankton recorder (CPR) transect, spanning the years 1961–2006. The CPR transect also contains coincident information on temperature and phytoplankton biomass (measured by the phytoplankton color index). Taxonomic richness varied at all timescales considered. The relationships between temperature and richness, and between phytoplankton and richness, also depended on temporal scale. The temperature–richness relationship was monotonic at the multi-decadal scale, and tended to be hump-shaped at finer scales; the productivity–richness relationship was hump-shaped at the multi-decadal scale, and tended to be monotonic at finer scales. Seasonal biodiversity dynamics were linked to temperature; inter-decadal biodiversity dynamics were linked to phytoplankton.

Long-term effects of ocean warming on the prokaryotic community: evidence from the vibrios

The long-term effects of ocean warming on prokaryotic communities are unknown because of lack of historical data. We overcame this gap by applying a retrospective molecular analysis to the bacterial community on formalin-fixed samples from the historical Continuous Plankton Recorder archive, which is one of the longest and most geographically extensive collections of marine biological samples in the world. We showed that during the last half century, ubiquitous marine bacteria of the Vibrio genus, including Vibrio cholerae, increased in dominance within the plankton-associated bacterial community of the North Sea, where an unprecedented increase in bathing infections related to these bacteria was recently reported. Among environmental variables, increased sea surface temperature explained 45% of the variance in Vibrio data, supporting the view that ocean warming is favouring the spread of vibrios and may be the cause of the globally increasing trend in their associated diseases.

Can we trust simple marine DMS parameterisations within complex climate models?

Dimethylsulphide (DMS) is a globally important aerosol precurser. In 1987 Charlson and others proposed that an increase in DMS production by certain phytoplankton species in response to a warming climate could stimulate increased aerosol formation, increasing the lower-atmosphere's albedo, and promoting cooling. Despite two decades of research, the global significance of this negative climate feedback remains contentious. It is therefore imperative that schemes are developed and tested, which allow for the realistic incorporation of phytoplankton DMS production into Earth System models. Using these models we can investigate the DMS-climate feedback and reduce uncertainty surrounding projections of future climate. Here we examine two empirical DMS parameterisations within the context of an Earth System model and find them to perform marginally better than the standard DMS climatology at predicting observations from an independent global dataset. We then question whether parameterisations based on our present understanding of DMS production by phytoplankton, and simple enough to incorporate into global climate models, can be shown to enhance the future predictive capacity of those models. This is an important question to ask now, as results from increasingly complex Earth System models lead us into the 5th assessment of climate science by the Intergovernmental Panel on Climate Change. Comparing observed and predicted inter-annual variability, we suggest that future climate projections may underestimate the magnitude of surface ocean DMS change. Unfortunately this conclusion relies on a relatively small dataset, in which observed inter-annual variability may be exaggerated by biases in sample collection. We therefore encourage the observational community to make repeat measurements of sea-surface DMS concentrations an important focus, and highlight areas of apparent high inter-annual variability where sampling might be carried out. Finally, we assess future projections from two similarly valid empirical DMS schemes, and demonstrate contrasting results. We therefore conclude that the use of empirical DMS parameterisations within simulations of future climate should be undertaken only with careful appreciation of the caveats discussed.