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.

Regional climate change and harmful algal blooms in the northeast Atlantic

We investigated long-term spatial variability in a number of Harmful Algal Blooms (HABs) in the northeast Atlantic and North Sea using data from the Continuous Plankton Recorder. Over the last four decades, some dinoflagellate taxa showed pronounced variation in the south and east of the North Sea, with the most significant increases being restricted to the adjacent waters off Norway. There was also a general decrease along the eastern coast of the United Kingdom. The most prominent feature in the interannual bloom frequencies over the last four decades was the anomalously high values recorded in the late 1980s in the northern and central North Sea areas. The only mesoscale area in the northeast Atlantic to show a significant increase in bloom formation over the last decade was the Norwegian coastal region. The changing spatial patterns of HAB taxa and the frequency of bloom formation are discussed in relation to regional climate change, in particular, changes in temperature, salinity, and the North Atlantic Oscillation (NAO). Areas highly vulnerable to the effects of regional climate change on HABs are Norwegian coastal waters and the Skagerrak. Other vulnerable areas include Danish coastal waters, and to a lesser extent, the German and Dutch Bight and the northern Irish Sea. Quite apart from eutrophication, our results give a preview of what might happen to certain HAB genera under changing climatic conditions in temperate environments and their responses to variability of climate oscillations such as the NAO.

Encounter success of free-ranging marine predator movements across a dynamic prey landscape

Movements of wide-ranging top predators can now be studied effectively using satellite and archival telemetry. However, the motivations underlying movements remain difficult to determine because trajectories are seldom related to key biological gradients, such as changing prey distributions. Here, we use a dynamic prey landscape of zooplankton biomass in the north-east Atlantic Ocean to examine active habitat selection in the plankton-feeding basking shark Cetorhinus maximus. The relative success of shark searches across this landscape was examined by comparing prey biomass encountered by sharks with encounters by random-walk simulations of ‘model’ sharks. Movements of transmitter-tagged sharks monitored for 964 days (16754km estimated minimum distance) were concentrated on the European continental shelf in areas characterized by high seasonal productivity and complex prey distributions. We show movements by adult and sub-adult sharks yielded consistently higher prey encounter rates than 90% of random-walk simulations. Behavioural patterns were consistent with basking sharks using search tactics structured across multiple scales to exploit the richest prey areas available in preferred habitats. Simple behavioural rules based on learned responses to previously encountered prey distributions may explain the high performances. This study highlights how dynamic prey landscapes enable active habitat selection in large predators to be investigated from a trophic perspective, an approach that may inform conservation by identifying critical habitat of vulnerable species.

How well does the Continuous Plankton Recorder (CPR) sample zooplankton? A comparison with the Longhurst Hardy Plankton Recorder (LHPR) in the northeast Atlantic

The Continuous Plankton Recorder (CPR) survey has collected data on basin- scale zooplankton abundance in the North Atlantic since the 1930s. These data have been used in many studies to elucidate seasonal patterns and long-term change in plankton populations, as well as more recently to validate ecosystem models. There has, however, been relatively little comparison of the data from the CPR with that from other samplers. In this study we compare zooplankton abundance estimated from the CPR in the northeast Atlantic with near-surface samples collected by a Longhurst-Hardy Plankton Recorder (LHPR) at Ocean Weather Station India (59 degree N, 19 degree W) between 1971 and 1975. Comparisons were made for six common copepods in the region: Acartia clausi, Calanus finmarchicus, Euchaeta norvegica, Metridia lucens, Oithona sp. and Pleuromamma robusta. Seasonal cycles based on CPR data were similar to those recorded by the LHPR. Differences in absolute abundances were apparent, however, with the CPR underestimating abundances by a factor of between 5 and 40, with the exception of A. clausi. Active avoidance by zooplankton is thought to be responsible. This avoidance is species specific, so that care must be taken describing communities, as the CPR emphasises those species that are preferentially caught, a problem common to many plankton samplers.

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.

A genetic marker to separate Emiliania huxleyi (Prymnesiophyceae) morphotypes

Emiliania huxleyi (Lohm.) Hay and Mohler is a ubiquitous unicellular marine alga surrounded by an elaborate covering of calcite platelets called coccoliths. It is an important primary producer involved in oceanic biogeochemistry and climate regulation. Currently, E. huxleyi is separated into five morphotypes based on morphometric, physiological, biochemical, and immunological differences. However, a genetic marker has yet to be found to characterize these morphotypes. With the use of sequence analysis and denaturing gradient gel electrophoresis, we discovered a genetic marker that correlates significantly with the separation of the most widely recognized A and B morphotypes. Furthermore, we reveal that the A morphotype is composed of a number of distinct genotypes. This marker lies within the 3' untranslated region of a coccolith associated protein mRNA, which is implicated in regulating coccolith calcification. Consequently, we tentatively termed this marker the coccolith morphology motif.

Relating sardine recruitment in the Northern Benguela to satellite-derived sea surface height using a neural network pattern recognition approach

Processes of enrichment, concentration and retention are thought to be important for the successful recruitment of small pelagic fish in upwelling areas, but are difficult to measure. In this study, a novel approach is used to examine the role of spatio-temporal oceanographic variability on recruitment success of the Northern Benguela sardine Sardinops sagax. This approach applies a neural network pattern recognition technique, called a self-organising map (SOM), to a seven-year time series of satellite-derived sea level data. The Northern Benguela is characterised by quasi-perennial upwelling of cold, nutrient-rich water and is influenced by intrusions of warm, nutrient-poor Angola Current water from the north. In this paper, these processes are categorised in terms of their influence on recruitment success through the key ocean triad mechanisms of enrichment, concentration and retention. Moderate upwelling is seen as favourable for recruitment, whereas strong upwelling, weak upwelling and Angola Current intrusion appear detrimental to recruitment success. The SOM was used to identify characteristic patterns from sea level difference data and these were interpreted with the aid of sea surface temperature data. We found that the major oceanographic processes of upwelling and Angola Current intrusion dominated these patterns, allowing them to be partitioned into those representing recruitment favourable conditions and those representing adverse conditions for recruitment. A marginally significant relationship was found between the index of sardine recruitment and the frequency of recruitment favourable conditions (r super(2) = 0.61, p = 0.068, n = 6). Because larvae are vulnerable to environmental influences for a period of at least 50 days after spawning, the SOM was then used to identify windows of persistent favourable conditions lasting longer than 50 days, termed recruitment favourable periods (RFPs). The occurrence of RFPs was compared with back-calculated spawning dates for each cohort. Finally, a comparison of RFPs with the time of spawning and the index of recruitment showed that in years where there were 50 or more days of favourable conditions following spawning, good recruitment followed (Mann-Whitney U-test: p = 0.064, n = 6). These results show the value of the SOM technique for describing spatio-temporal variability in oceanographic processes. Variability in these processes appears to be an important factor influencing recruitment in the Northern Benguela sardine, although the available data time series is currently too short to be conclusive. Nonetheless, the analysis of satellite data, using a neural network pattern-recognition approach, provides a useful framework for investigating fisheries recruitment problems.

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.

Increased blooms of a dinoflagellate in the NW Atlantic

Sampling by the Continuous Plankton Recorder (CPR) over the NW Atlantic from 1960 to 2000 has enabled long-term studies of the larger components of the phytoplankton community, highlighting various changes, particularly during the 1990s. Analysis of an index of phytoplankton biomass, the Phytoplankton Colour Index (PCI) has revealed an increase over the past decade, most marked during the winter (December to February) months. Examination of the structure of the community using multiple linear-regression models indicates that the winter phytoplankton community composition has changed markedly in the 1990s compared to the 1960s. One phytoplankter, the dinoflagellate Ceratium arcticum (Cleve), has undergone dramatic changes in abundance during this period, with pronounced large winter blooms and decreased autumnal levels, and its contribution to the Phytoplankton Colour index values has increased significantly. Other dominant species in the phytoplankton community, both diatoms and dinoflagellates, did not show the same variations over the examined time period. It is suggested that the response of C. arcticum is probably a result of previously reported changes in stratification in the NW Atlantic, due to dynamic hydro-climatic (freshening and cooling) events.

What determines the likelihood of species discovery in marine holozooplankton: is size, range or depth important?

The relationship between date of first description and size, geographic range and depth of occurrence is investigated for 18 orders of marine holozooplankton (comprising over 4000 species). Results of multiple regression analyses suggest that all attributes are linked, which reflects the complex interplay between them. Partial correlation coefficients suggest that geographic range is the most important predictor of description date, and shows an inverse relationship. By contrast, size is generally a poor indicator of description date, which probably mirrors the size-independent way in which specimens are collected, though there is clearly a positive relationship between both size and depth (for metabolic/trophic reasons), and size and geographic range. There is also a positive relationship between geographic range and depth that probably reflects the near constant nature of the deep-water environment and the wide-ranging currents to be found there. Although we did not explicitly incorporate either abundance or location into models predicting the date of first description, neither should be ignored.

Seasonal movements and behaviour of basking sharks from archival tagging: No evidence of winter hibernation

Habitat selection processes in highly migratory animals such as sharks and whales are important to understand because they influence patterns of distribution, availability and therefore catch rates. However, spatial strategies remain poorly understood over seasonal scales in most species, including, most notably, the plankton-feeding basking shark Cetorhinus maximus. It was proposed nearly 50 yr ago that this globally distributed species migrates from coastal summer-feeding areas of the northeast Atlantic to hibernate during winter in deep water on the bottom of continental-shelf slopes. This view has perpetuated in the literature even though the 'hibernation theory' has not been tested directly. We have now tracked basking sharks for the first time over seasonal scales (1.7 to 6.5 mo) using 'pop-up' satellite archival transmitters. We show that they do not hibernate during winter but instead undertake extensive horizontal (up to 3400 km) and vertical (> 750 m depth) movements to utilise productive continental-shelf and shelf-edge habitats during summer, autumn and winter. They travel long distances (390 to 460 km) to locate temporally discrete productivity 'hotspots' at shelf-break fronts, but at no time were prolonged movements into open-ocean regions away from shelf waters observed. Basking sharks have a very broad vertical diving range and can dive beyond the known range of planktivorous whales. Our study suggests this species can exploit shelf and slope-associated zooplankton communities in mesopelagic (200 to 1000 m) as well as epipelagic habitat (0 to 200 m).

Using continuous plankton recorder data

The continuous plankton recorder (CPR) survey is the largest multi-decadal plankton monitoring programme in the world. It was initiated in 1931 and by the end of 2004 had counted 207,619 samples and identified 437 phyto- and zooplankton taxa throughout the North Atlantic. CPR data are used extensively by the research community and in recent years have been used increasingly to underpin marine management. Here, we take a critical look at how best to use CPR data. We first describe the CPR itself, CPR sampling, and plankton counting procedures. We discuss the spatial and temporal biases in the Survey, summarise environmental data that have not previously been available, and describe the new data access policy. We supply information essential to using CPR data, including descriptions of each CPR taxonomic entity, the idiosyncrasies associated with counting many of the taxa, the logic behind taxonomic changes in the Survey, the semi-quantitative nature of CPR sampling, and recommendations on choosing the spatial and temporal scale of study. This forms the basis for a broader discussion on how to use CPR data for deriving ecologically meaningful indices based on size, functional groups and biomass that can be used to support research and management. This contribution should be useful for plankton ecologists, modellers and policy makers that actively use CPR data.

Climate change and marine plankton

Understanding how climate change will affect the planet is a key issue worldwide. Questions concerning the pace and impacts of climate change are thus central to many ecological and biogeochemical studies, and addressing the consequences of climate change is now high on the list of priorities for funding agencies. Here, we review the interactions between climate change and plankton communities, focusing on systematic changes in plankton community structure, abundance, distribution and phenology over recent decades. We examine the potential socioeconomic impacts of these plankton changes, such as the effects of bottom-up forcing on commercially exploited fish stocks (i.e. plankton as food for fish). We also consider the crucial roles that plankton might have in dictating the future pace of climate change via feedback mechanisms responding to elevated atmospheric CO sub(2) levels. An important message emerges from this review: ongoing plankton monitoring programmes worldwide will act as sentinels to identify future changes in marine ecosystems.