Modelling the effects of climate change on the distribution and production of marine fishes: accounting for trophic interactions in a dynamic bioclimate envelope model

Climate change has already altered the distribution of marine fishes. Future predictions of fish distributions and catches based on bioclimate envelope models are available, but to date they have not considered interspecific interactions. We address this by combining the species-based Dynamic Bioclimate Envelope Model (DBEM) with a size-based trophic model. The new approach provides spatially and temporally resolved predictions of changes in species' size, abundance and catch potential that account for the effects of ecological interactions. Predicted latitudinal shifts are, on average, reduced by 20% when species interactions are incorporated, compared to DBEM predictions, with pelagic species showing the greatest reductions. Goodness-of-fit of biomass data from fish stock assessments in the North Atlantic between 1991 and 2003 is improved slightly by including species interactions. The differences between predictions from the two models may be relatively modest because, at the North Atlantic basin scale, (i) predators and competitors may respond to climate change together; (ii) existing parameterization of the DBEM might implicitly incorporate trophic interactions; and/or (iii) trophic interactions might not be the main driver of responses to climate. Future analyses using ecologically explicit models and data will improve understanding of the effects of inter-specific interactions on responses to climate change, and better inform managers about plausible ecological and fishery consequences of a changing environment.

Mechanisms of long-term decline in size of lesser sandeels in the North Sea explored using a growth and phenology model

The lesser sandeel Ammodytes marinus is a key species in the North Sea ecosystem, transferring energy from planktonic producers to top predators. Previous studies have shown a long-term decline in the size of 0-group sandeels in the western North Sea, but they were unable to pinpoint the mechanism (later hatching, slower growth or changes in size-dependent mortality) or cause. To investigate the first 2 possibilities we combined 2 independent time series of sandeel size, namely data from chick-feeding Atlantic puffins Fratercula arctica and from the Continuous Plankton Recorder (CPR), in a novel statistical model implemented using Markov Chain Monte Carlo (MCMC). The model estimated annual mean length on 1 July, as well as hatching date and growth rate for sandeels from 1973 to 2006. Mean length-at-date declined by 22% over this period, corresponding to a 60% decrease in energy content, with a sharper decline since 2002. Up to the mid-1990s, the decline was associated with a trend towards later hatching. Subsequently, hatching became earlier again, and the continued trend towards smaller size appears to have been driven by lower growth rates, particularly in the most recent years, although we could not rule out changes in size-dependent mortality. Our findings point to major changes in key aspects of sandeel life history, which we consider are most likely due to direct and indirect temperature-related changes over a range of biotic factors, including the seasonal distribution of copepods and intra- and inter-specific competition with planktivorous fish. The results have implications both for the many predators of sandeels and for age and size of maturation in this aggregation of North Sea sandeels.

Spatial and inter-decadal variability in plankton abundance and composition in the Northwest Atlantic (1958-2006)

The results of Continuous Plankton Recorder sampling in the NW Atlantic between 1958 and 2006 are presented for 11 plankton taxa in eight shelf and deep ocean regions. For shelf regions, phytoplankton abundances increased in the early 1990s, mainly in winter, as the contribution of Arctic-derived freshwater to the Newfoundland (NLS) and Scotian shelves (SS) increased. Farther east, in the sub-polar gyre, phytoplankton levels increased with rising temperatures during the 1990s and 2000s. In both areas, the changes can be explained by increased stratification. The increased influx of arctic water to the NLS in the 1990s was also probably directly responsible for the increased abundances of two arctic Calanus species (C. glacialis and C. hyperboreus) and indirectly responsible for the decreased abundance of Calanus I–IV (mainly C. finmarchicus), perhaps via changes in food composition. On the SS the arctic Calanus species increased in abundance in the 2000s, likely as the result of increased transport from the Arctic via the Gulf of St Lawrence. In the deep ocean, plankton seasonal cycles changed little over the decades and increasing phytoplankton levels in the 2000s were accompanied by increases in zooplankton abundance, suggesting bottom-up control. In shelf regions, phytoplankton increases in the 1990s were in winter and Calanus I–IV appeared earlier in spring than in previous decades. Zooplankton levels generally did not change overall however, perhaps because the species examined were mainly inactive during winter.

Validation of the detection of Alexandrium species using specific RNA probes tested in a microarray format: Calibration of signal using variability of RNA content with environmental conditions.

The dinoflagellate genus Alexandrium contains several toxin producing species and strains, which can cause major economic losses to the shell fish industry. It is therefore important to be able to detect these toxin producers and also distinguish toxic strains from some of the morphologically identical non-toxic strains. To facilitate this DNA probes to be used in a microarray format were designed in silico or developed from existing published probes. These probes targeted either the 18S or 28S ribosomal ribonucleic acid (rRNA) gene in Alexandrium tamarense Group I, Group III and Group IV, Alexandrium ostenfeldii and Alexandrium minutum. Three strains of A. tamarense Group I, A. tamarense Group III, A. minutum and two strains of A. ostenfeldii were grown at optimal conditions and transferred into new environmental conditions changing either the light intensity, salinity, temperature or nutrient concentrations, to check if any of these environmental conditions induced changes in the cellular ribonucleic acid (RNA) concentration or growth rate. The aim of this experiment was the calibration of several species-specific probes for the quantification of the toxic Alexandrium strains. Growth rates were highly variable but only elevated or lowered salinity significantly lowered growth rate for A. tamarense Group I and Group III; differences in RNA content were not significant for the majority of the treatments. Only light intensity seemed to affect significantly the RNA content in A. tamarense Group I and Group III, but this was still within the same range as for the other treatments meaning that a back calibration from RNA to cell numbers was possible. The designed probes allow the production of quantitative information for Alexandrium species for the microarray chip.

Validation of the detection of Pseudo-nitzschia spp. using specific RNA probes tested in a microarray format: Calibration of signal based on variability of RNA content with environmental conditions.

Harmful algal blooms (HAB) occur worldwide and cause health problems and economic damage to fisheries and tourism. Monitoring for toxic algae is therefore essential but is based primarily on light microscopy, which is time consuming and can be limited by insufficient morphological characters such that more time is needed to examine critical features with electron microscopy. Monitoring with molecular tools is done in only a few places world-wide. EU FP7 MIDTAL (Microarray Detection of Toxic Algae) used SSU and LSU rRNA genes as targets on microarrays to identify toxic species. In order to comply with current monitoring requirements to report cell numbers as the relevant threshold measurement to trigger closure of fisheries, it was necessary to calibrate our microarray to convert the hybridisation signal obtained to cell numbers. Calibration curves for two species of Pseudo-nitzschia for use with the MIDTAL microarray are presented to obtain cell numbers following hybridisation. It complements work presented by Barra et al. (2012b. Environ. Sci. Pollut. Res. doi: 10.1007/s11356-012-1330-1v) for two other Pseudo-nitzschia spp., Dittami and Edvardsen (2012a. J. Phycol. 48, 1050) for Pseudochatonella, Blanco et al. (2013. Harmful Algae 24, 80) for Heterosigma, McCoy et al. (2013. FEMS. doi: 10.1111/1574-6941.12277) for Prymnesium spp., Karlodinium veneficum, and cf. Chatonella spp. and Taylor et al. (2014. Harmful Algae, in press) for Alexandrium.

The response of phytoplankton to climate variability associated with the North Atlantic Oscillation

Inter-annual variability in the timing of phytoplankton spring bloom and phytoplankton community structure in the central North Atlantic Ocean was quantified using ocean color data and continuous plankton recorder (CPR) data. This variability was related to the North Atlantic Oscillation using correlation analysis and multivariate auto-regression models. The initiation of the spring bloom derived from CPR phytoplankton color index data is similar to that derived from satellite chlorophyll, and exhibits a nominal correlation with the sea surface temperature (SST) and the North Atlantic Oscillation (NAO). The extrapolated spring bloom timing suggested later initiation of blooms in the mid-1980s and earlier initiation of blooms in the 1990s. The climatological phytoplankton community structure in the central North Atlantic is dominated by diatoms, except for a shift in community composition favoring dinoflagellates in August. The ratio of diatoms to total phytoplankton abundance and the ratio of dinoflagellates to total phytoplankton abundance are both closely correlated with the NAO and SST. The extended time series of phytoplankton community structure between 1985 and 2009, deduced from the time series of SST and NAO over the same interval, showed a decadal shift away from diatoms towards dinoflagellates. The linkages between the NAO, and changes in stratification and phytoplankton processes occur over a larger scale than previously observed.

Microbial spatial variability: An example from the Celtic Sea

In July 2004, dominant populations of microbial ultraplankton (<5 μm), in the surface of the Celtic Sea (between UK and Eire), were repeatedly mapped using flow cytometry, at 1.5 km resolution over a region of diameter 100 km. The numerically dominant representatives of all basic functional types were enumerated including one group of phototrophic bacteria (Syn), two groups of phytoplankton (PP, NP), three groups of heterotrophic bacterioplankton (HB) and the regionally dominant group of heterotrophic protists (HP). The distributions of all organisms showed strong spatial variability with little relation to variability in physical fields such as salinity and temperature. Furthermore, there was little agreement between distributions of different organisms. The only linear correlation consistently explaining more than 50% of the variance between any pairing of the organism groups enumerated is between two different groups of HB. Specifically, no linear, or non-linear, relationship is found between any pairings of SYB, PP or HB groups with their protist predators HP. Looking for multiple dependencies, factor analysis reveals three groupings: Syn, PP and low nucleic acid content HB (LNA); high nucleic acid content HB (HNA); HP and NP. Even the manner in which the spatial variability of Syn, PP and HB abundance varies as a function of lengthscale (represented by a semivariogram) differs significantly from that for HP. In summary, although all microbial planktonic groups enumerated are present and numerically dominant throughout the region studied, at face value the relationships between them seem weak. Nevertheless, the behaviour of a simple, illustrative ecological model, with strongly interacting phototrophs and heterotrophs, with stochastic forcing, is shown to be consistent with the observed poor correlations and differences in how spatial variability varies with lengthscale. Thus, our study suggests that a comparison of microbial abundances alone may not discern strong underlying trophic interactions. Specific knowledge of these processes, in particular grazing, will be required to explain the causes of the observed microbial spatial variability and its resulting consequences for the functioning of the ecosystem.

DIESE Final Report

The DIESE program (Determination of relevant Indicators for Environmental monitoring: A Strategy for Europe) brought together seven French and British research teams, a private company and the agencies responsible for the management of water bodies of the two countries (ONEMA and the Environmental Agency) in a joint effort to document the ecotoxicological effects related to the presence of chemicals in the environment. To contribute to a better understanding and management of the environment, the program has expanded its efforts to (1) use existing knowledge, or new information acquired during the research program, to identify important biological problems affecting wildlife, (2) increase our understanding of toxicological mechanisms involved and thus be able to identify the causes of the identified dysfunctions and (3) to hone our expertise and vigilance systems in order to better monitor changes in the environment and make appropriate diagnoses. The first part of the program identified clear biological effects, and using biological tests representative of the mechanisms of action of compounds, identified the responsible compounds present in the environment. In connection with the feminization observed in many fish species in European streams, a search for estrogenic and anti-androgenic compounds was conducted. A new test identifying estrogenic compounds has been developed in roach and the ER-Calux test for anti-androgenic effects has been implemented. The results showed that, in addition to biocides such as triclosan and chlorophène, many aromatic hydrocarbon compounds are likely to disturb the physiology of living organisms by interacting with the androgen receptor. Six of these were identified in sediment extracts: benzanthrone, fluoranthene, 1,2- benzodiphenylene sulfide, benzo[a]pyrene, benz[a] anthracene, and 9-phenylcarbazole. The second part of the program aimed at documenting and understanding the mechanisms of action of chemicals leading to physiological changes. This work represents a particular challenge when dealing with molluscs, as knowledge about their physiology and endocrinology is still fragmentary. Thus, new technologies including metabolomic and transcriptomic analyses have been implemented in order to obtain a comprehensive picture of the effects on molluscs. Metabolomic research demonstrated that estrogenic compounds are able to alter the metabolism of eicosanoids and amines, while transcriptomic strategies identified genes whose expression is altered in intersex clams. Because these genes mainly appear as “male” genes, the results suggest that these profound physiological changes result from demasculinisation of male clams. Proteomic studies have also been carried out to elucidate the mechanisms of action of pollutants on fish physiology. These studies generally included a set of molecular marker measurements in an integrative and ecological perspective. The results showed that not only male fish physiology is altered but also female reproductive status is impaired. Moreover, it appeared that other alterations of the fish endocrine system, such as androgenic effects, are at work and that the immune system is also subject to chemical pressure including effects from environmental estrogens. Notably, the immune system, like the endocrine system, seems to show periods of particular sensitivity during development. Measurements on growth and on the general metabolism emphasize the importance of environmental conditions in the physiology of aquatic organisms and in particular the inter-site variability due to temperature,hypoxic conditions, and fish development strategies. They thus provide a unique perspective that allow us to better understand the context and consequences of natural conditions on the population. In a third part of the program, the research conducted had the objective of developing and testing a biomarker strategy to support the environmental management methodologies. Two lanes of specific studies have been followed. The first was to implement, over all or part of the study area, robust biomarkers to establish maps that highlight the water bodies at risk and provide information on sources of compounds and associated disturbances. The second part of the work aimed at exploring methodologies to take advantage of biomarker measurements and to integrate them in a very simple and clear index. Partial or comprehensive maps of the Channel area were produced to report the presence of mutagenic or anti-androgenic compounds in the sediments, intersex fish and clams, and imposex. These maps may remain to be completed and work will be necessary to confront this information in order to learn relevant lessons for management of the environment, a goal that the DIESE program has contributed to by providing some necessary and original information.

Temporal variability in total, micro- and nano-phytoplankton primary production at a coastal site in the Western English Channel

Primary productivity and subsequent carbon cycling in the coastal zone have a significant impact on the global carbon budget. It is currently unclear how anthropogenic activity could alter these budgets but long term coastal time series of hydrological, biogeochemical and biological measurements represent a key means to better understand past drivers, and hence to predicting future seasonal and inter-annual variability in carbon fixation in coastal ecosystems. An 8-year time series of primary production from 2003 to 2010, estimated using a recently developed absorption-based algorithm, was used to determine the nature and extent of change in primary production at a coastal station (L4) in the Western English Channel (WEC). Analysis of the seasonal and inter-annual variability in production demonstrated that on average, nano- and pico-phytoplankton account for 48% of the total carbon fixation and micro-phytoplankton for 52%. A recent decline in the primary production of nano- and pico-phytoplankton from 2005 to 2010 was observed, corresponding with a decrease in winter nutrient concentrations and a decrease in the biomass of Phaeocystis sp. Micro-phytoplankton primary production (PPM) remained relatively constant over the time series and was enhanced in summer during periods of high precipitation. Increases in sea surface temperature, and decreases in wind speeds and salinity were associated with later spring maxima in PPM. Together these trends indicate that predicted increases in temperature and decrease in wind speeds in future would drive later spring production whilst predicted increases in precipitation would also continue these blooms throughout the summer at this site.

Dynamics of air–sea CO2 fluxes in the northwestern European shelf based on voluntary observing ship and satellite observations

From January 2011 to December 2013, we constructed a comprehensive pCO2 data set based on voluntary observing ship (VOS) measurements in the western English Channel (WEC). We subsequently estimated surface pCO2 and air–sea CO2 fluxes in northwestern European continental shelf waters using multiple linear regressions (MLRs) from remotely sensed sea surface temperature (SST), chlorophyll a concentration (Chl a), wind speed (WND), photosynthetically active radiation (PAR) and modeled mixed layer depth (MLD). We developed specific MLRs for the seasonally stratified northern WEC (nWEC) and the permanently well-mixed southern WEC (sWEC) and calculated surface pCO2 with uncertainties of 17 and 16 μatm, respectively. We extrapolated the relationships obtained for the WEC based on the 2011–2013 data set (1) temporally over a decade and (2) spatially in the adjacent Celtic and Irish seas (CS and IS), two regions which exhibit hydrographical and biogeochemical characteristics similar to those of WEC waters. We validated these extrapolations with pCO2 data from the SOCAT and LDEO databases and obtained good agreement between modeled and observed data. On an annual scale, seasonally stratified systems acted as a sink of CO2 from the atmosphere of −0.6 ± 0.3, −0.9 ± 0.3 and −0.5 ± 0.3 mol C m−2 yr−1 in the northern Celtic Sea, southern Celtic sea and nWEC, respectively, whereas permanently well-mixed systems acted as source of CO2 to the atmosphere of 0.2 ± 0.2 and 0.3 ± 0.2 mol C m−2 yr−1 in the sWEC and IS, respectively. Air–sea CO2 fluxes showed important inter-annual variability resulting in significant differences in the intensity and/or direction of annual fluxes. We scaled the mean annual fluxes over these provinces for the last decade and obtained the first annual average uptake of −1.11 ± 0.32 Tg C yr−1 for this part of the northwestern European continental shelf. Our study showed that combining VOS data with satellite observations can be a powerful tool to estimate and extrapolate air–sea CO2 fluxes in sparsely sampled area.