Marine molluscs and fish as biomarkers of pollution stress in littoral regions of the Red Sea, Mediterranean Sea and North Sea

The intensive development of industry and urban structures along the seashores of the world, as well as the immense increase in marine transportation and other activities, has resulted in the deposition of thousands of new chemicals and organic compounds, endangering the existence of organisms and ecosystems. The conventional single biomarker methods used in ecological assessment studies cannot provide an adequate base for environmental health assessment, management and sustainability planning. The present study uses a set of novel biochemical, physiological, cytogenetic and morphological methods to characterize the state of health of selected molluscs and fish along the shores of the German North Sea, as well as the Israeli Mediterranean and Red Sea. The methods include measurement of activity of multixenobiotic resistance-mediated transporter (MXRtr) and the system of active transport of organic anions (SATOA) as indicators of antixenobiotic defence; glutathione S-transferase (GST) activity as an indicator of biotransformation of xenobiotics; DNA unwinding as a marker of genotoxicity; micronucleus test for clastogenicity; levels of phagocytosis for immunotoxicity; cholinesterase (ChE) activity and level of catecholamines as indicators of neurotoxicity; permeability of external epithelia to anionic hydrophilic probe, intralysosomal accumulation of cationic amphiphilic probe and activity of non-specific esterases as indicators of cell/tissue viability. Complete histopathological examination was used for diagnostics of environmental pathology. The obtained data show that the activity of the defensive pumps, MXRtr and SATOA in the studied organisms was significantly higher in the surface epithelia of molluscs from a polluted site than that of the same species from control, unpolluted stations, providing clear evidence of response to stress. Enhanced frequency of DNA lesions (alkaline and acidic DNA unwinding) and micronucleus-containing cells was significantly higher in samples from polluted sites in comparison to those from the clean sites that exhibited genotoxic and clastogenic activity of the pollutants. In all the studied molluscs a negative correlation was found between the MXRtr levels of activity and the frequency of micronucleus-containing hemocytes. The expression of this was in accordance with the level of pollution. The complete histopathological examination demonstrates significantly higher frequencies of pathological alterations in organs of animals from polluted sites. A strong negative correlation was found between the frequency of these alterations and MXRtr activity in the same specimens. In addition to these parameters, a decrease in the viability was noted in molluscs from the polluted sites, but ChE activities remained similar at most sites. The methods applied in our study unmasked numerous early cryptic responses and negative alterations of health in populations of marine biota sampled from the polluted sites. This demonstrates that genotoxic, clastogenic and pathogenic xenobiotics are present and act in the studied sites and this knowledge can provide a reliable base for consideration for sustainable development. Received: 2 March 1999 / Received in revised form: 2 August 1999 / Accepted: 3 August 1999     

Species assemblages of pelagic fish embryos in the southern North Sea between 1984 and 2000

The occurrence and abundance of the pelagic eggs of southern North Sea spring-spawning fish were analysed between 1984 and 2000. Species number varied between six (1986) and 14 (1999) and was positively correlated with sea surface temperature. With one exception, dab eggs were always the most abundant and usually highly dominant. Ranking of species depended on temperature, but no significant differences in ranking between years was discernible. Although with the increase in temperature in the 1990s a change in species assemblage was evident [species belonging to the boreal-Mediterranean (Lusitanian) group became more apparent in the species assemblage] this did not lead to an increased species diversity (Shannon Index) or a change in other community parameters. It appears that the recent developments regarding spawning stock biomass of commercial North Sea fish is reflected in the declining egg abundance of the respective commercial and larger species (i.e. cod, flounder, plaice) and an increase in abundance of the eggs of small species (i.e. long rough dab, rockling) over the years. Received in revised form: 5 November 2001 Electronic Publication     

Evidence for density-dependent growth in North Sea gadoids

The classical view on density-dependent growth is that an increase in population density heightens intraspecific competition for food, leading to reduced food intake and depressed growth. This paper summarizes the analysis of English Groundfish Survey, International Young Fish Survey and ICES Roundfish Working Group data for evidence of density-dependent growth of I- and II-group cod, haddock and whiting in the North Sea.
Within Roundfish areas there was a negative relationship between growth and density in some instances, but it was small. However, there were persistent differences in both growth rate and density between Roundfish areas. In all cases, except for I-group cod, there appeared to be a tendency for fish in low-density areas to be larger than fish in high-density areas; this might be due to feeding competition but other explanations are possible. The results urge caution in interpreting commercial catch data for evidence of density-dependent growth, since changes in fishing effort in particular areas could significantly bias the conclusions.
There was evidence of enhanced survival of small fish in good year-classes; this would depress the mean size at age, thereby mimicking the effects of density-dependent growth.     

Year-to-year variation in larval fish assemblages of the Southern North Sea

In order to test the temporal stability within and the reproducibility of larval fish assemblages between years, the larval fish assemblage at Helgoland Roads, North Sea (NE Atlantic) was quantitatively sampled almost daily from January 2003 to December 2005. The survey resulted in a total of 462 samples containing 50,632 larval fish of at least 42 taxa. In winter the larval fish assemblage was mainly dominated by larvae emerging from demersal eggs. This changed gradually to larvae hatching from pelagic eggs. Larvae from pelagic eggs dominated the ichthyoplankton assemblage in summer. A remarkably stable seasonality in terms of dominance patterns with recurring, season-specific fish assemblages was observed over the 3 years, despite substantial variation in environmental conditions such as a temperature difference of almost 20°C between summer and winter. The lesser sandeel (Ammodytes marinus), was the only species which showed significant fluctuations in abundance between the years. After removal of this species from the analysis, the dominance patterns of the remaining fish species were almost identical between years.     

Long-term changes in growth and age at maturity of mackerel, Scomber scombrus L., from the North Sea

Mean length and mean weight at age of Atlantic mackerel in the North Sea increased significantly between 1960 and 1979, then, decreased markedly during the 1980s. In contrast, median age at maturity decreased (c. 1-1.5 years) from 1960. Median length at maturity remained stable until the 1980s, when it declined sharply. The significance of these changes is discussed in relation to variation in sea temperature, food availability and stock size. It is speculated that the changes during the 1980s resulted from immigration of western stock mackerel.     

Effects of the severe winter 1995/96 on the benthic macrofauna of the Wadden Sea and the coastal North Sea near the island of Sylt

The development of benthic macrofauna in the Wadden Sea and in the coastal North Sea after the severe winter of 1995/96 is compared with the preceding years with mild to moderate winters. In the intertidal of the Wadden Sea, ice-drift and low temperature caused the expected changes in species composition by increasing winter mortality in sensitive species, and by exceptionally high recruitment of some species during the succeeding summer. In the shallow subtidal (10–20 m depth), similar winter effects were observed. However, recovery of many subtidal populations was still incomplete until the summer of 1997. It is suggested that this was due to hydrographic conditions that carried many larvae or drifting juveniles into more distant offshore areas. This may have limited larval supply and may have delayed recovery at the onshore sites. Since in the eastern North Sea severe winters are accompanied by frequent easterly winds, it is not clear whether decreasing winter abundances in some species were due to increased mortality, or to a seaward dislocation of organisms. Received in revised form: 7 May 2001 Electronic Publication     

Candidatus Abditibacter,a novel genus within the Cryomorphaceae,thriving in the North Sea

Coastal phytoplankton blooms are frequently followed by successive blooms of heterotrophic bacterial clades. The class Flavobacteriia within the Bacteroidetes has been shown to play an important role in the degradation of high molecular weight substrates that become available in the later stages of such blooms. One of the flavobacterial clades repeatedly observed over the course of several years during phytoplankton blooms off the coast of Helgoland, North Sea, is Vis6. This genus-level clade belongs to the family Cryomorphaceae and has been resistant to cultivation to date. Based on metagenome assembled genomes, comparative 16S rRNA gene sequence analyses and fluorescence in situ hybridization, we here propose a novel candidate genus Abditibacter, comprising three novel species Candidatus Abditibacter vernus, Candidatus Abditibacter forsetii and Candidatus Abditibacter autumni. While the small genomes of the three novel photoheterotrophic species encode highly similar gene repertoires, including genes for degradation of proteins and algal storage polysaccharides such as laminarin, two of them – Ca. A. vernus and Ca. A. forsetii – seem to have a preference for spring blooms, while Ca. A. autumni almost exclusively occurs in late summer and autumn.     

Occurrence of pelagic stingray Pteroplatytrygon violacea (Bonaparte, 1832) in the North Sea

A mature male pelagic stingray Pteroplatytrygon violacea (99 cm total length, 33·5 cm disc length and 42 cm disc width; 2·5 kg) was caught by commercial Nephrops trawl in the North Sea (at c . 54º49' N; 0º57' W) on 14 November 2005. Records of P. violacea in the north-east Atlantic are reviewed, with only two vagrant specimens known from the North Sea, representing the most northerly records of this species in the Atlantic Ocean.     

North Sea cod and climate change – modelling the effects of temperature on population dynamics

In order to examine the likely impacts of climate change on fish stocks, it is necessary to couple the output from large‐scale climate models to fisheries population simulations. Using projections of future North Sea surface temperatures for the period 2000–2050 from the Hadley General Circulation Model, we estimate the likely effects of climate change on the North Sea cod population. Output from the model suggests that increasing temperatures will lead to an increased rate of decline in the North Sea cod population compared with simulations that ignore environmental change. Although the simulation developed here is relatively simplistic, we demonstrate that inclusion of environmental factors in population models can markedly alter one's perception of how the population will behave. The development of simulations incorporating environment effects will become increasingly important as the impacts of climate change on the marine ecosystem become more pronounced.     

Sexual dimorphism in the energetics of reproduction and growth of North Sea plaice, Pleuronectes platessa L.

The chemical composition and energy content of North Sea plaice during the spawning period were examined in mature males and females and in immature fish, to study differences in the allocation of energy over reproduction and somatic growth between the sexes. At the beginning of the spawning period mature males and females had equal dry weights of lipid that were 70% higher than in immatures. Protein content in mature males was equal to that in immatures but was 23 % higher in mature females. Immature males and females did not differ in chemical composition. At the end of the spawning period, spent and immature fish had equal lipid contents, but protein content in spent females was 10% lower than in spent males, and 17% lower than in immatures. Gross energy content of the body decreased by 44% (65·2 to 36·3 J cm^-3) in mature females, 27% (55·0 to 40·OJ cm^-3) in mature males, and 9% (48·7 to 44·2J cm^-3) in immatures. Energy content of plaice eggs was estimated at 6·60 kJ per 1000 eggs. Reproductive investment was estimated from the energy loss during the spawning period and included the energy of sex products and spawning metabolism. Somatic growth comprised the annual increase in energy content of fish. The pattern of energy allocation over reproduction and somatic growth differed between males and females. Males started their reproduction at a smaller length and a younger age and allocated a higher proportion of the available energy into reproduction than females. Available energy resources for somatic growth and reproduction (surplus production) were equal between the sexes up to a length of about 30 cm. Beyond this length male surplus production levelled off whereas female surplus production continued to increase. The differences in surplus production and the allocation patterns are discussed. For female plaice the energy allocated into egg production was estimated as between 48 and 64% of the total amount of energy lost during spawning. The remaining energy is used for metabolism during the spawning period, yielding an estimate of the metabolic rate of mature females of between 6·4 and 9·1 kJ day^-1. A maximum estimate of the metabolic rate of mature males was 7·4 kJ day^-1.     

The diet and growth of O-group flounder,Platichthys flesus (L.), in the River Dee,North Wales

Many O-group flounder, Platichthys flesus, live in the lower reaches of rivers in North West Europe; while there is extensive information on the niche that they occupy in estuarine and marine environments, little is known of their life in freshwater. The diet of O-group flounder in the Lower Welsh River Dee was studied by stomach contents analysis of diel and seasonal samples. The dominant prey were chironomid larvae and pupae, tubificid oligochaetes and cyclopoid copepods. There was little quantitative variation in diet temporally, although a weak crepuscular pattern of stomach fullness was shown. There was wide variation in length and weight in all months, but the mean values at age I were 60 mm and 2.9 g respectively.     

Copepod feeding behaviour and egg production during a dinoflagellate bloom in the North Sea

Feeding strategies of copepods were studied during a dinoflagellate-dominated bloom in the North Sea in August 2001. The aim of this study was to evaluate the importance of mesozooplankton grazing as a biological loss factor of harmful algal blooms under natural conditions. Therefore, ingestion, egestion and egg production experiments were performed with the most abundant copepod species Calanus helgolandicus, Temora longicornis and Acartia sp. feeding on the natural phytoplankton community. Dinophysis norvegica and Ceratium furca were the most abundant dinoflagellate species at the time of the experiments. Grazing experiments as well as examination of fecal pellet content revealed C. helgolandicus fed efficiently on D. norvegica. Ingestion rates up to 47 cells female⁻¹ h⁻¹ were measured and a large proportion of the C. helgolandicus fecal pellets contained intact D. norvegica cells. Dinophysis cells were rarely seen in fecal pellets produced by T. longicornis, and never observed in pellets produced by Acartia sp. The ingestion rate of C. furca, which was the dominating Ceratium species, mimicked that of D. norvegica. C. helgolandicus grazed significantly on C. furca (16 cells female⁻¹ h⁻¹), while the ingestion rate of T. longicornis was low and Acartia sp. was not able to graze on C. furca. Egg production experiments revealed that 92% of the C. helgolandicus females produced eggs. The specific egg production rate and the proportion of females producing eggs among T. longicornis were low. This field experiment clearly shows that some copepod species feed efficiently on D. norvegica and C. furca under natural conditions, which may affect the bloom development of these dinoflagellates.     

Phaeocystis colony distribution in the North Atlantic Ocean since 1948, and interpretation of long-term changes in the Phaeocystis hotspot in the North Sea

Monitoring of Phaeocystis since 1948 during the Continuous Plankton Recorder survey indicates that over the last 5.5 decades the distribution of its colonies in the North Atlantic Ocean was not restricted to neritic waters: occurrence was also recorded in the open Atlantic regions sampled, most frequently in the spring. Apparently, environmental conditions in open ocean waters, also those far offshore, are suitable for complete lifecycle development of colonies (the only stage recorded in the survey). In the North Sea the frequency of occurrence was also highest in spring. Its southeastern part was the Phaeocystis abundance hotspot of the whole area covered by the survey. Frequency was especially high before the 1960s and after the 1980s, i.e., in the periods when anthropogenic nutrient enrichment was relatively low. Changes in eutrophication have obviously not been a major cause of long-term Phaeocystis variation in the southeastern North Sea, where total phytoplankton biomass was related significantly to river discharge. Evidence is presented for the suggestion that Phaeocystis abundance in the southern North Sea is to a large extent determined by the amount of Atlantic Ocean water flushed in through the Dover Strait. Since Phaeocystis plays a key role in element fluxes relevant to climate the results presented here have implications for biogeochemical models of cycling of carbon and sulphur. Sea-to-air exchange of CO₂ and dimethyl sulphide (DMS) has been calculated on the basis of measurements during single-year cruises. The considerable annual variation in phytoplankton and in its Phaeocystis component reported here does not warrant extrapolation of such figures.     

Unchanging diet in a stable colony: contemporary and past diet composition of black-legged kittiwakes <Emphasis Type="Italic">Rissa tridactyla</Emphasis> at Helgoland,south-eastern North Sea

In contrast to the situation at the west coast of the North Sea, the breeding colony of black-legged kittiwakes Rissa tridactyla at Helgoland in the south-eastern North Sea did not exhibit severe declines since 1990 but instead numbers increased and only lately stabilised. Declines at the west coast of the North Sea were attributed to a lower abundance and lower quality of the key prey, sandeels. We hypothesised that kittiwakes at Helgoland do not rely as heavily on sandeels as their conspecifics. We analysed stomach contents of nestlings and adults of 2001, 2002, 2004 and 2006. In concordance with earlier studies of the 1980s and 1990s, young whiting Merlangius merlangus was the most important prey species in 2001, 2002 and 2004. Clupeids and sandeels were consumed in lower proportions. While earlier studies suggested whiting to originate from fisheries discards, evidence now supports that kittiwakes prey upon whiting in areas of hydrographic fronts. No whiting was recovered in samples of 2006 and the proportion of fish prey was low. Main prey items were polychaete worms (Nereidae), which were presumably consumed as swarming Heteronereis stages. An observed strong rise in water temperature in summer 2006 might have influenced food availability of kittiwakes by inducing swarming of Nereidae. Overall, kittiwakes breeding on Helgoland showed a positive population trend for several decades while mainly feeding on whiting.     

Chemical industry effluent impacts on reproduction and biochemistry in a North Sea population of viviparous blenny (Zoarces viviparus)

The reproduction biology and some biochemicalbiomarkers of viviparous blenny (Zoarcesviviparus L.) were studied in a Swedish fjord on theNorth Sea coast which receives chemical industrywaste-water. Data for comparison purposes wereobtained from a reference area used in the nationalmonitoring programme. The viviparous blenny has agestation period of 4–5 months. By analysing larvalsurvival and growth, reproductive performance wasshown to be significantly reduced in female blennyexposed to petrochemical effluents. Larval growth wassignificantly lowered, and the proportion of femalescarrying dead juveniles was higher than at thereference site. Also, the mean number of deadjuveniles per female was significantly higher in theeffluent area. Among sampling sites, responses were negatively correlated with the distance from theeffluent outlets. The narrow age distribution ofadults in exposed areas, and the difference in catchper unit effort, indicated increased adult mortality.No significant improvements in reproductiveperformance were seen when results were compared withprevious studies from 1988–1989. Significantdifferences in a set of enzymes associated with thedetoxification of xenobiotics, or the antioxidantdefence against organo- and oxyradicals, confirmed theexposure of the studied population to organic pollutants.     

Short-term variations in the fluxes and composition of seston in near-bottom traps in the southern North Sea

In this study we attempted to measure the potential food availability for macrobenthic interface feeders using a new device (sediment recorder) which traps bed load particles at a height of 10 cm above the sea floor. The recorder is positioned flat on the seabed and alternately exposes a shallow collector mounted in a smooth surface mimicking the sediment surface. The samples were analyzed for their content of chlorophyll a (Chl) and dry weight (DM). We compared the sediment recorder data with the results obtained with a sediment trap suspended 3.2 m above the sea floor. Measurements were carried out in spring and fall at two stations in the southern North Sea with different sediment type, maximum current velocities and biomass (sand, station B vs silty sand, station F). The recorder deployments in November yielded higher Chl fluxes and a higher quality of particles (Chl:DM ratio) than the trap at both stations. Unlike the trap samples, in which Chl and DM were always positively and strongly correlated, maximum Chl and DM fluxes in the recorder samples were out of phase, particularly at station B, pointing to a highly variable quality during the tidal cycle. Unexpectedly, Chl fluxes and Chl:DM ratios in the recorder samples at station B were higher than at station F in both seasons, although the benthic biomass at the latter station was five times higher. The highest Chl fluxes and particle quality (Chl:DM) at station B were measured during slack tides when interface feeding would be least hampered by drag forces. Station B is nevertheless characterized by a low macrobenthic biomass and a scarcity of interface feeders, specifically of suspension-feeding bivalves. Possible reasons for this apparent discrepancy are discussed. Electronic Publication     

Seasonal variability of inorganic and organic nitrogen in the North Sea

This study considers the cycling of nitrogen in the waters of the North Sea, particularly focussing on organic nitrogen. Dissolved inorganic nitrogen (DIN), dissolved organic nitrogen (DON) and particulate organic nitrogen (PON) were measured in the North Sea over a one-year period (autumn 2004–summer 2005). The surface water concentrations of nitrate, ammonium, DON and PON during the present study ranged from <0.1–7.2 μM, <0.1–2.0 μM, 1.9–11.2 μM and 0.3–5.6 μM, respectively, with DON the dominant fraction of total nitrogen at all times. These nutrients concentrations were significantly lower compared to previous studies in the southern North Sea. The seasonal variations showed high mean surface concentrations of nitrate (4.7 ± 0.6 μM) and DON (8.9 ± 0.9 μM), low ammonium (<0.1 μM) and PON (0.8 ± 0.1 μM) in winter, shifting to low nitrate (0.3 ± 0.3 μM) and DON (4.2 ± 1.2 μM) in summer, with high ammonium (0.8 ± 0.4 μM) in autumn and PON (2.5 ± 1.2 μM) in spring. Highest mean surface DON concentration was measured in winter and may be due to resuspension of the organic matter from the bottom sediments. For autumn and spring, phytoplankton DON release was likely to be the most significant source of DON as shown by high concentrations of low molecular weight (LMW) DON and its positive correlation to chlorophyll a. Low total and LMW DON concentrations during summer were likely to be due to the uptake of the LMW DON fraction by phytoplankton and bacteria and the stratification of the water column. DON is therefore shown to be a potentially important source of nitrogen in shelf seas especially after the spring bloom has depleted nitrate to limiting concentrations. Handling editor: L. Naselli-Flores     

Temperature experienced during vitellogenesis influences ovarian maturation and the timing of ovulation in common wolffish

Temperature treatment of common wolffish Anarhichas lupus during vitellogenesis affected the time of final maturation; ovulation in fish held at 8 and 12° C from mid-April to October was about four and five weeks delayed, compared with a 4° C group. Fish in the 8° C group had significantly larger eggs than those in the 4° C and the 12° C groups, and a significantly higher egg production than fish in the 12° C group. Temperature treatment did not affect either fertilization rate or relative fecundity, but absolute fecundity was significantly lower in the 12° C group than the other groups due to poor growth of the fish at high temperature. This did not affect the numbers of spawning individuals. There was a trend towards lower egg survival to the eyed stage in the 12° C group compared to the 4 and 8° C groups, although the effect was not statistically significant. The results indicate that both the timing of final maturation and investment in ovarian growth in common wolffish are affected by temperature experienced during vitellogenesis.