Regional and annual variation in black-legged kittiwake breeding productivity is related to sea surface temperature

Spatiotemporal variation in seabird demographic parameters is often pronounced and may be an important source of information on the state of marine ecosystems. Black-legged kittiwakes Rissa tridactyla in Britain and Ireland show strong regional structure in breeding productivity, and both temporal and spatial variation are probably related to abundance of the principal prey of breeding kittiwakes, the lesser sandeel Ammodytes marinus. Annual regional estimates of sandeel abundance do not exist, prohibiting direct tests of this hypothesis. We examined relationships between kittiwake breeding productivity and 2 potential proxies of sandeel abundance, winter sea surface temperature (SST) and abundance of Calanus copepods, within and among 6 regions in Britain and Ireland from 1986 to 2004. Means and trends in winter SST differed among regions, with higher means and less pronounced increasing trends in western (Atlantic) regions than in eastern (North Sea) regions. A negative relationship between breeding productivity and winter SST in the previous year was found within 2 regions (East Scotland and Orkney), as well as in a cross-regional analysis. Results were inconclusive for Calanus abundance, with a positive relationship in East Scotland and negative in Orkney. These results demonstrate that although a single environmental driver (SST) is related to both within- and between-region variation in a key demographic parameter, regional heterogeneity in SST trends as well as the importance of other factors may lead to highly variable responses. Understanding this heterogeneity is critical for predicting long-term effects of climate change or other anthropogenic drivers on marine ecosystems.

A new procedure to optimize the selection of groups in a classification tree

Agglomerative cluster analyses encompass many techniques, which have been widely used in various fields of science. In biology, and specifically ecology, datasets are generally highly variable and may contain outliers, which increase the difficulty to identify the number of clusters. Here we present a new criterion to determine statistically the optimal level of partition in a classification tree. The criterion robustness is tested against perturbated data (outliers) using an observation or variable with values randomly generated. The technique, called Random Simulation Test (RST), is tested on (1) the well-known Iris dataset [Fisher, R.A., 1936. The use of multiple measurements in taxonomic problems. Ann. Eugenic. 7, 179–188], (2) simulated data with predetermined numbers of clusters following Milligan and Cooper [Milligan, G.W., Cooper, M.C., 1985. An examination of procedures for determining the number of clusters in a data set. Psychometrika 50, 159–179] and finally (3) is applied on real copepod communities data previously analyzed in Beaugrand et al. [Beaugrand, G., Ibanez, F., Lindley, J.A., Reid, P.C., 2002. Diversity of calanoid copepods in the North Atlantic and adjacent seas: species associations and biogeography. Mar. Ecol. Prog. Ser. 232, 179–195]. The technique is compared to several standard techniques. RST performed generally better than existing algorithms on simulated data and proved to be especially efficient with highly variable datasets.

Macrophysiology of Calanus finmarchicus in the North Atlantic Ocean

Copepods represent the major part of the dry weight of the mesozooplankton in pelagic ecosystems and therefore have a central role in the secondary production of the North Atlantic Ocean. The calanoid copepod species Calanus finmarchicus is the main large copepod in subarctic waters of the North Atlantic, dominating the dry weight of the mesozooplankton in regions such as the northern North Sea and the Norwegian Sea. The objective of this work was to investigate the relationships between both the fundamental and realised niches of C. finmarchicus in order to better understand the future influence of global climate change on the abundance, the spatial distribution and the phenology of this key-structural species. Based on standardised Principal Component Analyses (PCAs), a macroecological approach was applied to determine factors affecting the spatial distribution of C. finmarchicus and to characterise its realised niche. Second, an ecophysiological model was used to calculate the Potential Egg Production Rate (PEPR) of C. finmarchicus and the centre of its fundamental niche. Relationships between the two niches were then investigated by correlation analysis. We found a close relationship between the fundamental and realised niches of C. finmarchicus at spatial, monthly and decadal scales. While the species is at the centre of its niche in the subarctic gyre, our joint macroecological and macrophysiological analyses show that it is at the edge of its niche in the North Sea, making the species in this region more vulnerable to temperature changes.

A comparison of two zooplankton time series data collected in the Gulf of Maine

Interannual and seasonal trends of zooplankton abundance and species composition were compared between the Bongo net and Continuous Plankton Recorder (CPR) time series in the Gulf of Maine. Data from 5799 Bongo and 3118 CPR samples were compared from the years 1978–2006. The two programs use different sampling methods, with the Bongo time series composed of bimonthly vertically integrated samples from locations throughout the region, while the CPR was towed monthly at 10 m depth on a transect that bisects the region. It was found that there was a significant correlation between the interannual (r = 0.67, P < 0.01) and seasonal (r = 0.95, P < 0.01) variability of total zooplankton counts. Abundance rankings of individual taxa were highly correlated and temporal trends of dominant copepods were similar between samplers. Multivariate analysis also showed that both time series equally detected major shifts in community structure through time. However, absolute abundance levels were higher in the Bongo and temporal patterns for many of the less abundant taxa groups were not similar between the two devices. The different mesh sizes of the samplers probably caused some of the discrepancies; but diel migration patterns, damage to soft bodied animals and avoidance of the small CPR aperture by some taxa likely contributed to the catch differences between the two devices. Nonetheless, Bongo data presented here confirm the previously published patterns found in the CPR data set, and both show that the abundance increase of the 1990s has been followed by average to below average levels from 2002 to 06.

Distribution and multi-annual abundance trends of the copepod Temora longicornis in the US Northeast shelf ecosystem

The average spatial distribution and annual abundance cycle are described for the copepod Temora longicornis from samples collected on broadscale surveys (1977-2006) and along continuous plankton recorder transects (1961-2006) of the US Northeast continental shelf ecosystem. After its annual low in winter, T. longicornis abundance begins to increase in coastal waters with the northern progression of spring conditions. Annual maximum shelf concentrations were found in the more southern inshore waters of the region during the summer months. Abundance throughout most of the ecosystem increased sharply in the early 1990s and remained high through 2001. During this period, the copepod became more numerous and widespread in offshore shelf waters. Abundance declined to approximately average levels in 2002 for the remainder of the time series, but its extended offshore range remained intact. Correlation analysis found that the copepods interannual abundance variability had a significant negative relationship with surface salinity anomalies throughout the ecosystem, with higher correlations found in the northernmost subareas. Temora longicornis abundance in the ecosystem's southernmost subarea (Middle Atlantic Bight) did not increase in the 1990s and was found to be negatively correlated to surface temperature, indicating that continued global warming could adversely impact the copepods annual abundance cycle in this region.

Long-term changes in North Atlantic zooplankton biomass

New measures of zooplankton biomass have been derived from CPR samples in the North Atlantic from 1958 to 2005. The final aim was to investigate how the zooplankton standing stock had varied throughout the last decades, knowing that in different areas of the North Atlantic significant changes in the distribution of the dominant zooplankton species as well as the plankton assemblage have been observed. During the forty-five years of monitoring the contribution of the different groups (e.g. copepods, euphausiids, meroplankton larvae) to the total zooplankton biomass has been evaluated. The changes in the phenology of the biomass were also considered. The relationship between quantity, quality and seasonal timing of plankton and the poor fish recruitment seen in recent years in the North Sea are also discussed.

Basin scale distribution of zooplankton in the Ligurian Sea (north-western Mediterranean) in late autumn

Mesozooplankton biomass and abundance were evaluated in epipelagic waters at 59 stations covering the Italian sector of the Ligurian Sea (north-western Mediterranean) in December 1990. This region is characterised by a cyclonic circulation which encloses a central divergence zone and is associated with a main thermohaline front offshore the western Ligurian coast. At the end of autumn, mesozooplankton biomass (range: 0.80–4.24 mg DW m−3) and the abundance (range: 83.8–932 ind. m−3) were lower in the divergence zone. On the contrary, in the Ligurian frontal zone at the periphery of the divergence and on the eastern continental shelf the greatest values of biomass and abundance were recorded. Copepods and appendicularians dominated the mesozooplankton community, the main taxa being the copepods Clausocalanus spp. (46% of total zooplankton) and Oithona spp. (15%) and the appendicularian Fritillaria spp. (12%). Three hydrological sub-regions, i.e. the divergence, the eastern continental shelf and the periphery of the divergence, were characterised by different zooplankton communities and characteristic species. Environmental differences between the three zones were mainly related to changes in bottom topography, sea surface temperatures and quantity of particulate organic matter. Vertical mesozooplankton abundance and taxa distribution from the surface to 1,900 m depth were also examined in one station. The results showed that the bulk of the community was concentrated in the upper 200 m, small copepods being dominant particularly in the upper 50 m. The copepod community was more diversified in sub-superficial waters, with a maximum observed in the 200–400 m layer. The distributions of main zooplankton taxa described in epipelagic waters in the eastern Ligurian Sea in autumn were compared with their distribution at surface in the north-western Mediterranean obtained by sampling performed with the Continuous Plankton Recorder in 1997–1999. The analysis of the zooplankton community in CPR samples confirms the dominance of small copepods (Paracalanus spp., Clausocalanus spp., Oithona spp.) and appendicularians in the north-western Mediterranean in late autumn-winter and shows that their distribution is mainly related to the main mesoscale hydrographic features characterising this basin.

Trophodynamics and stability of regional scale ecosystems in the Northeast Atlantic

This study addresses the long-term stability of three trophic groupings in the Northeast Atlantic at regional scales. The most abundant taxa representing phytoplankton, herbivorous copepods, and carnivorous zooplankton were examined from the Continuous Plankton Recorder database. Multivariate control charts using a Bray–Curtis similarity metric were used to assess whether fluctuations within trophic groupings were within or beyond the expected variability. Two evaluation periods were examined: annual changes between 1960 and 1999 (2000–2009 baseline) and recent changes between 2000 and 2009 (1960–1999 baseline). The trends over time in abundance/biomass of trophic levels were region-specific, especially in carnivorous copepods, where abundance did not mirror trends in the overall study area. The stability of phytoplankton was within the expected limits, although not in 2008 and 2009. Higher trophic levels were less stable, perhaps reflecting the added complexity of interactions governing their abundance. In addition, some regions were consistently less stable than others. Correlations in stability between adjacent trophic levels were positive at large marine ecosystem scale but generally non-significant at regional scales. The study suggests that certain regions may be particularly vulnerable to periods of instability in community structure. The benefits of using the control chart method rather than other multivariate measures of plankton dynamics are discussed.

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.

Pattern and scale of variability among Northwest Atlantic Shelf plankton communities

Continuous plankton recorders (CPRs) have been used in the Northwest Atlantic for almost 50 years. While data collected by these surveys have provided valuable information on long-term variability in plankton populations, all previous analyses have been limited to only a portion of the geographic range of the available data. Here we present an analysis of the CPR data from the Mid Atlantic Bight to the Labrador Sea. Across this wide geographic range, we found many common associations among the taxa. In particular, the changes in most regions were strongly size structured, with small and medium copepods varying together and often positively related to indicators of phytoplankton abundance. The time series from nearby regions were strongly correlated; however, after 1990, the spatial pattern became more complex. During this period, several of the copepod taxa, noticeably Calanus finmarchicus and Centropages typicus, experienced a series of anomalies that appeared to propagate from northeast to southwest. Although the direction of propagation was consistent with the shelf circulation, the anomalies propagated at a rate much slower than typical current speeds. The timing of the copepod anomalies and their phase speed were similar in character to observed changes in salinity and the position of the Shelf Slope Front. The correspondence between the changes in the plankton community and changes in the physical environmental suggests that physical conditions are a strong driver of interannual variability in Northwest Atlantic Shelf ecosystems.

Have climate induced changes in zooplankton communities led to poor conditions for larval fish growth? A test on cod larvae on the UK shelf

Climate effects have been shown to be at least partly responsible for the reorganisation in the plankton ecosystem on the shelf seas of NW Europe over the last 50 years. Most fish larvae feed primarily on zooplankton, so changes in zooplankton quantity, quality and seasonal timing have been hypothesized to be a key factor affecting their survival. To investigate this we have implemented a 1-dimensional trophodynamic growth model of cod larvae for the waters around the UK covering the period 1960 to 2003. Larval growth is modelled as the difference between the amount of food absorbed by the larva and its various metabolic costs. Prey availability is based upon the biomass and size of available preys (i.e. adults and nauplii copepods and cladocerans) taken from the Continuous Plankton Recorder dataset. Temperature and wind forcing are also taken into account. Results suggest that observed changes in plankton community structure may have had less impact than previously suggested. This is because changes in prey availability may be compensated for by increased temperatures resulting in little overall impact on potential larval growth. Stock recovery, at least in the short term is likely to be more dependent upon conserving the year classes recruited to allow spawning stock biomass to rebuild. If as our model suggests, the larvae are still able to survive in the changing environment, reduction in fishing on the adults is needed to allow the stock to recover.

Macroscale factors affecting diatom abundance: a synergistic use of Continuous Plankton Recorder and satellite remote sensing data

Diatoms exist in almost every aquatic regime; they are responsible for 20% of global carbon fixation and 25% of global primary production, and are regarded as a key food for copepods, which are subsequently consumed by larger predators such as fish and marine mammals. A decreasing abundance and a vulnerability to climatic change in the North Atlantic Ocean have been reported in the literature. In the present work, a data matrix composed of concurrent satellite remote sensing and Continuous Plankton Recorder (CPR) in situ measurements was collated for the same spatial and temporal coverage in the Northeast Atlantic. Artificial neural networks (ANNs) were applied to recognize and learn the complex non-monotonic and non-linear relationships between diatom abundance and spatiotemporal environmental factors. Because of their ability to mimic non-linear systems, ANNs proved far more effective in modelling the diatom distribution in the marine ecosystem. The results of this study reveal that diatoms have a regular seasonal cycle, with their abundance most strongly influenced by sea surface temperature (SST) and light intensity. The models indicate that extreme positive SSTs decrease diatom abundances regardless of other climatic conditions. These results provide information on the ecology of diatoms that may advance our understanding of the potential response of diatoms to climatic change.

Global latitudinal variations in marine copepod diversity and environmental factors

Latitudinal gradients in diversity are among the most striking features in ecology. For terrestrial species, climate (i.e. temperature and precipitation) is believed to exert a strong influence on the geographical distributions of diversity through its effects on energy availability. Here, we provide the first global description of geographical variation in the diversity of marine copepods, a key trophic link between phytoplankton and fish, in relation to environmental variables. We found a polar-tropical difference in copepod diversity in the Northern Hemisphere where diversity peaked at subtropical latitudes. In the Southern Hemisphere, diversity showed a tropical plateau into the temperate regions. This asymmetry around the Equator may be explained by climatic conditions, in particular the influence of the Inter-Tropical Convergence Zone, prevailing mainly in the northern tropical region. Ocean temperature was the most important explanatory factor among all environmental variables tested, accounting for 54 per cent of the variation in diversity. Given the strong positive correlation between diversity and temperature, local copepod diversity, especially in extra-tropical regions, is likely to increase with climate change as their large-scale distributions respond to climate warming.

Genome- and transcriptome-assisted development of nuclear insertion/deletion markers for Calanus species (Copepoda: Calanoida) identification

Copepods of the genus Calanus are key zooplankton species in temperate to arctic marine ecosystems. Despite their ecological importance, species identification remains challenging. Furthermore, the recent report of hybrids among Calanus species highlights the need for diagnostic nuclear markers to efficiently identify parental species and hybrids. Using next-generation sequencing analysis of both the genome and transcriptome from two sibling species, Calanus finmarchicus and Calanus glacialis, we developed a panel of 12 nuclear insertion/deletion markers. All the markers showed species-specific amplicon length. Furthermore, most of the markers were successfully amplified in other Calanus species, allowing the molecular identification of Calanus helgolandicus, Calanus hyperboreus and Calanus marshallae.

Have we been underestimating the effects of ocean acidification in zooplankton?

Understanding how copepods may respond to ocean acidification (OA) is critical for risk assessments of ocean ecology and biogeochemistry. The perception that copepods are insensitive to OA is largely based on experiments with adult females. Their apparent resilience to increased carbon dioxide (pCO2 ) concentrations has supported the view that copepods are 'winners' under OA. Here, we show that this conclusion is not robust, that sensitivity across different life stages is significantly misrepresented by studies solely using adult females. Stage-specific responses to pCO2 (385-6000 μatm) were studied across different life stages of a calanoid copepod, monitoring for lethal and sublethal responses. Mortality rates varied significantly across the different life stages, with nauplii showing the highest lethal effects; nauplii mortality rates increased threefold when pCO2 concentrations reached 1000 μatm (year 2100 scenario) with LC50 at 1084 μatm pCO2 . In comparison, eggs, early copepodite stages, and adult males and females were not affected lethally until pCO2 concentrations ≥3000 μatm. Adverse effects on reproduction were found, with >35% decline in nauplii recruitment at 1000 μatm pCO2 . This suppression of reproductive scope, coupled with the decreased survival of early stage progeny at this pCO2 concentration, has clear potential to damage population growth dynamics in this species. The disparity in responses seen across the different developmental stages emphasizes the need for a holistic life-cycle approach to make species-level projections to climate change. Significant misrepresentation and error propagation can develop from studies which attempt to project outcomes to future OA conditions solely based on single life history stage exposures.