Temperature and pressure dependency of oxygen consumption during long-term sustained swimming of European eels.

Many aspects of the typically 5000-10,000 km spawning migration of the European eel (Anguilla anguilla) remain unknown. As part of this migration, eels undertake extensive diurnal vertical migrations to depths below 1000 m, being exposed to a wide range of temperatures and hydrostatic pressures. In this experimental study, we exposed eels to different combinations of temperature (12-20°C) and pressure (100--800 kPa) during long-term sustained swimming (32-47 days). Both temperature and pressure affected oxygen consumption rate, such that there was a significant increase of metabolic rate with temperature, whereas pressure reduced oxygen consumption, albeit only at higher temperatures. Average oxygen consumption rates ranged between 15 mg kg-1 h-1 (12°C, 100 kPa) and 30.2 mg kg-1 h-1 (20°C, 100 kPa), highlighting the remarkably high swimming efficiency of this species and, more importantly, indicating that past evaluations of the cost of transport are potentially overestimates as they are often based on experiments conducted at atmospheric pressure at higher temperatures.

Visual Gene Expression Reveals a cone-to-rod Developmental Progression in Deep-Sea Fishes.

Vertebrates use cone cells in the retina for color vision and rod cells to see in dim light. Many deep-sea fishes have adapted to their environment to have only rod cells in the retina, while both rod and cone genes are still preserved in their genomes. As deep-sea fish larvae start their lives in the shallow, and only later submerge to the depth, they have to cope with diverse environmental conditions during ontogeny. Using a comparative transcriptomic approach in 20 deep-sea fish species from eight teleost orders, we report on a developmental cone-to-rod switch. While adults mostly rely on rod opsin (RH1) for vision in dim light, larvae almost exclusively express middle-wavelength-sensitive ("green") cone opsins (RH2) in their retinas. The phototransduction cascade genes follow a similar ontogenetic pattern of cone-followed by rod-specific gene expression in most species, except for the pearleye and sabretooth (Aulopiformes), in which the cone cascade remains dominant throughout development, casting doubts on the photoreceptor cell identity. By inspecting the whole genomes of five deep-sea species (four of them sequenced within this study: Idiacanthus fasciola, Chauliodus sloani; Stomiiformes; Coccorella atlantica, and Scopelarchus michaelsarsi; Aulopiformes), we found that they possess one or two copies of the rod RH1 opsin gene, and up to seven copies of the cone RH2 opsin genes in their genomes, while other cone opsin classes have been mostly lost. Our findings hence provide molecular evidence for a limited opsin gene repertoire in deep-sea fishes and a conserved vertebrate pattern whereby cone photoreceptors develop first and rod photoreceptors are added only at later developmental stages.

Bone resorption and body reorganization during maturation induce maternal transfer of toxic metals in anguillid eels.

During their once-in-a-lifetime transoceanic spawning migration, anguillid eels do not feed, instead rely on energy stores to fuel the demands of locomotion and reproduction while they reorganize their bodies by depleting body reserves and building up gonadal tissue. Here we show how the European eel (Anguilla anguilla) breaks down its skeleton to redistribute phosphorus and calcium from hard to soft tissues during its sexual development. Using multiple analytical and imaging techniques, we characterize the spatial and temporal degradation of the skeletal framework from initial to final gonadal maturation and use elemental mass ratios in bone, muscle, liver, and gonadal tissue to determine the fluxes and fates of selected minerals and metals in the eels' bodies. We find that bone loss is more pronounced in females than in males and eventually may reach a point at which the mechanical stability of the skeleton is challenged. P and Ca are released and translocated from skeletal tissues to muscle and gonads, leaving both elements in constant proportion in remaining bone structures. The depletion of internal stores from hard and soft tissues during maturation-induced body reorganization is accompanied by the recirculation, translocation, and maternal transfer of potentially toxic metals from bone and muscle to the ovaries in gravid females, which may have direct deleterious effects on health and hinder the reproductive success of individuals of this critically endangered species.

A novel hyperbaric swimming respirometer allows the simulation of varying swimming depths in fish respirometry studies.

The understanding of swimming physiology and knowledge on the metabolic costs of swimming are important for assessing effects of environmental factors on migratory behavior. Swim tunnels are the most common experimental setups for measuring swimming performance and oxygen uptake rates in fishes; however, few can realistically simulate depth and the changes in hydrostatic pressure that many fishes experience, e.g. during diel vertical migrations. Here, we present a new hyperbaric swimming respirometer (HSR) that can simulate depths of up to 80 m. The system consists of three separate, identical swimming tunnels, each with a volume of 205 L, a control board and a storage tank with water treatment. The swimming chamber of each tunnel has a length of 1.40 m and a diameter of 20 cm. The HSR uses the principle of intermittent-flow respirometry and has here been tested with female European eels (Anguilla anguilla). Various pressure, temperature and flow velocity profiles can be programmed, and the effect on metabolic activity and oxygen consumption can be assessed. Thus, the HSR provides opportunities to study the physiology of fish during swimming in a simulated depth range that corresponds to many inland, coastal and shelf waters.

Spawning by the European eel across 2000 km of the Sargasso Sea.

It has been known for about a century that European eels have a unique life history that includes offshore spawning in the Sargasso Sea about 5000-7000 km away from their juvenile and adult habitats in Europe and northern Africa. Recently hatched eel larvae were historically collected during Danish, German and American surveys in specific areas in the southern Sargasso Sea. During a 31 day period of March and April 2014, Danish and German research ships sampled for European eel larvae along 15 alternating transects of stations across the Sargasso Sea. The collection of recently hatched eel larvae (≤12 mm) from 70° W and eastward to 50° W showed that the European eel had been spawning across a 2000 km wide region of the North Atlantic Ocean. Historical collections made from 1921 to 2007 showed that small larvae had also previously been collected in this wide longitudinal zone, showing that the spatial extent of spawning has not diminished in recent decades, irrespective of the dramatic decline in recruitment. The use of such a wide spawning area may be related to variations in the onset of the silver eel spawning migration, individual differences in their long-term swimming ability, or aspects of larval drift.

Evidence for High Concentrations and Maternal Transfer of Substituted Diphenylamines in European Eels Analyzed by Two-Dimensional Gas Chromatography-Time-of-Flight Mass Spectrometry and Gas Chromatography-Fourier Transform Ion Cyclotron Resonance Mass Spectrometry.

Chemical pollution is hypothesized to be one of the factors driving the strong decline of the critically endangered European eel population. Specifically, the impact of contaminants on the quality of spawning eels and subsequent embryo survival and development has been discussed as crucial investigation point. However, so far, only very limited information on potential negative effects of contaminants on the reproduction of eels is available. Through the combination of nontargeted ultrahigh-resolution mass spectrometry and multidimensional gas chromatography, combined with more-conventional targeted analytical approaches and multimedia mass-balance modeling, compounds of particular relevance, and their maternal transfer in artificially matured European eels from the German river Ems have been identified. Substituted diphenylamines were, unexpectedly, found to be the primary organic contaminants in the eel samples, with concentrations in the µg g-1 wet weight range. Furthermore, it could be shown that these contaminants, as well as polychlorinated biphenyls (PCBs), organochlorine pesticides, and polyaromatic hydrocarbons (PAHs), are not merely stored in lipid rich tissue of eels but maternally transferred into gonads and eggs. The results of this study provide unique information on both the fate and behavior of substituted diphenylamines in the environment as well as their relevance as contaminants in European eels.

A question of origin: dioxin-like PCBs and their relevance in stock management of European eels.

The stock of European Eel (Anguilla anguilla L.) has reached an all-time low in 2011. Spawner quality of mature eels in terms of health status and fitness is considered one of the key elements for successful migration and reproduction. Dioxin-like Polychlorinated Biphenyls (dl-PCBs) are known persistent organic pollutants potentially affecting the reproductive capability and health status of eels throughout their entire lifetime. In this study, muscle tissue samples of 192 European eels of all continental life stages from 6 different water bodies and 13 sampling sites were analyzed for contamination with lipophilic dl-PCBs to investigate the potential relevance of the respective habitat in light of eel stock management. Results of this study reveal habitat-dependent and life history stage-related accumulation of targeted PCBs. Sum concentrations of targeted PCBs differed significantly between life stages and inter-habitat variability in dl-PCB levels and -profiles was observed. Among all investigated life stages, migrant silver eels were found to be the most suitable life history stage to represent their particular water system due to habitat dwell-time and their terminal contamination status. With reference to a possible negative impact of dl-PCBs on health and the reproductive capability of eels, it was hypothesized that those growing up in less polluted habitats have a better chance to produce healthy offspring than those growing up in highly polluted habitats. We suggest that the contamination status of water systems is fundamental for the life cycle of eels and needs to be considered in stock management and restocking programs.

Maternal transfer of dioxin-like compounds in artificially matured European eels.

Several eel species of the genus Anguilla are considered endangered due to a severe decline in recruitment. Up to now, the reasons for this threatening development are not fully understood. The eel's highly specialized biology can lead to explicitly high accumulation of globally distributed organic lipophilic contaminants during its continental life. Because of this and due the particular toxicological sensitivity of early life stages of oviparous organisms towards dioxin-like compounds, it is crucial to improve our understanding concerning toxicokinetics and maternal transfer of organic contaminants in eels. This study presents analytical data on maternal transfer of dioxin-like (dl) compounds in relevant tissue samples taken from artificially matured and non-matured European silver eels (Anguilla anguilla) from German inland waters using gas chromatography coupled with mass spectrometry (GC/MS) and high-resolution mass spectrometry (GC/HRMS). Detected concentrations revealed a lipid-driven transfer of targeted compounds from muscle-fat-reserves to gonads and eggs respectively, with no distinct preferences concerning the chlorination degree of targeted compounds. Dl-PCBs were shown to contribute the major share of toxicity equivalents found in analysed eel tissues. Maternal muscle tissue to egg concentration ratios in wet weight-based samples had a mean of 6.95 ± 1.49 in accordance with the differences in total lipid content in the respective body matrices. Dioxins and furans in analysed samples were (from a toxicological point of view) of less relevance. Furthermore it was shown that muscle concentrations in silver eels could be used in future assessments to make conservative predictions for expected egg concentrations in female eels.

A physiologically based toxicokinetic (PBTK) model for moderately hydrophobic organic chemicals in the European eel (Anguilla anguilla).

The European eel (Anguilla anguilla) is a facultatively catadromous fish species with a complex life cycle. Its current population status is alarming: recruitment has decreased drastically since the 1980s and its stock is still considered to be outside safe biological limits. Although there is no consensus on the reasons for this situation, it is currently thought to have resulted from a combination of different stressors, including anthropogenic contaminants. To deepen our understanding of the processes leading to the accumulation of lipophilic organic contaminants in yellow eels (i.e. the feeding, continental growth stage), we developed a physiologically based toxicokinetic model using our own data and values from the literature. Such models can predict the uptake and distribution of water-borne organic chemicals in the whole fish and in different tissues at any time during exposure. The predictive power of the model was tested against experimental data for six chemicals with n-octanol-water partitioning coefficient (log Kow) values ranging from 2.13-4.29. Model performance was excellent, with a root mean squared error of 0.28 log units. This model has the potential to help identify suitable habitats for restocking under eel management plans.

Maternal transfer of emerging brominated and chlorinated flame retardants in European eels.

The European eel (Anguilla anguilla) is regarded as a critically endangered species. Scientists are in agreement that the "quality of spawners" is a vital factor for the survival of the species. This quality can be impaired by parasites, disease and pollution. Especially endocrine disrupting organic chemicals pose a potential threat to reproduction and development of offspring. To our knowledge, the findings in this publication for the first time describe maternal transfer of contaminants in eels. We analysed the concentrations of in total 53 polybrominated diphenyl ethers (PBDEs) and their halogenated substitutes in muscle, gonads and eggs of artificially matured European eels and in muscle and gonads of untreated European eels that were used for comparison. We found evidence that persistent organic pollutants such as PBDEs, as well as their brominated and chlorinated substitutes are redistributed from muscle tissue to gonads and eggs. Concentrations ranged from 0.001 ng g(-1)ww for sum Dechlorane metabolites (DPMA, aCL10DP, aCl11DP) to 2.1 ng g(-1)ww for TBA in eggs, 0.001 ng g(-1)ww for Dechlorane metabolites to 9.4 ng g(-1)ww for TBA in gonads and 0.002 ng g(-1)ww for Dechlorane metabolites to 54 ng g(-1)ww for TBA in muscle tissue. Average egg muscle ratios (EMRs) for compounds detectable in artificially matured eels from both Schlei Fjord and Ems River ranged from 0.01 for Dechlorane 602 (DDC-DBF) to 10.4 for PBEB. Strong correlations were found between flame retardant concentrations and lipid content in the analysed tissue types, as well as transfer rates and octanol-water partitioning coefficient, indicating that these parameters were the driving factors for the observed maternal transfer. Furthermore, indications were found, that TBP-DBPE, TBP-AE, BATE and TBA have a significant uptake from the surrounding water, rather than just food and might additionally be formed by metabolism or biotransformation processes. Dechloranes seem to be of increasing relevance as contaminants in eels and are transferred to eggs. A change of the isomer pattern in comparison to the technical product of Dechlorane Plus (DP) was observed indicating a redistribution of DP from muscle tissue to gonads during silvering with a preference of the syn-isomer. The highly bioaccumulative DDC-DBF was the most abundant Dechlorane in all fish of the comparison group even though it is not produced or imported in the EU. The aldrin related "experimental flame retardant" dibromoaldrin (DBALD) was detected for the first time in the environment in similar or higher concentrations than DP.

PAH metabolites, GST and EROD in European eel (Anguilla anguilla) as possible indicators for eel habitat quality in German rivers.

The stock of the European eel (Anguilla anguilla L.) continues to decline and has reached a new minimum in 2011. Poor health status of the spawners due to organic contaminants is one of the possible causes for this dramatic situation. Polycyclic aromatic hydrocarbons (PAHs) are ubiquitous contaminants, which are rapidly metabolized in vertebrates. EROD (ethoxyresorufin-O-deethylase) and GST (glutathione-S-transferase) are two enzymes involved in PAH detoxification in fish. In this study, PAH metabolites as well as EROD and GST activity in a large, comprising dataset of more than 260 migratory and pre-migratory eels from five large German river basin districts were used to describe PAH exposure and its metabolism as possible indicators for the habitat quality for eels. Eel from the river Elbe appear to be moderately contaminated with PAH. Highest mean values of PAH metabolites were analysed in fish from the river Rhine. However, the results suggest that contaminants such as PAH are metabolized in the fish and may have contributed to EROD activity in eels caught from the Elbe estuary to 600 km upstream. Since the eel's onset of cessation of feeding is closely linked to maturation and migration, we propose bile pigments as new indicators contributing to identify the proportion of migratory eel, which is crucial information for eel management plans. We showed that PAH metabolites normalized to bile pigments as well as EROD could be used to describe the habitat quality and might be suitable parameters in search for suitable stocking habitats.

Brominated flame retardants and Dechloranes in European and American eels from glass to silver life stages.

The populations of American (Anguilla rostrata) and European eels (Anguilla anguilla) have been declining rapidly in the last decades. Organic contaminants are suspected to be one of the possible causes for the decline; however, so far there have been few investigations of the uptake of specific compounds by different life cycle stages (e.g. freshwater or marine stage) and how the contamination patterns develop throughout the eel's life cycle. In the present study we measured concentrations of polybrominated diphenylethers (PBDEs), alternate brominated flame retardants (alternate BFRs) and Dechloranes (Decs) in different life stages of European and American eels to compare the contamination patterns and their development throughout the eel's life cycle. In general, concentrations of flame retardants (FRs) were similar to or higher in American than in European eels, and a greater number of FRs were detected. PBDE congeners that are characteristic of the Penta-PBDE formulation were the most abundant FRs in all adult eels as well as American glass eels. In European glass eels the alternate BFR 2,3-dibromopropyl-2,4,6-tribromophenylether (DPTE) and Dechlorane Plus were the dominating FRs, with average concentrations of 1.1±0.31 ng g(-1) ww and up to 0.32 ng g(-1) ww respectively. Of the PBDEs BDE-183 was the most abundant congener in European glass eels. Low concentrations (less than 10% of the total contamination) of Tetra and Penta-PBDEs in juvenile European eels indicated that bans of technical Penta-PBDE in the European Union are effective. Enrichment of PBDEs was observed over the life stages of both European and American eels. However, a greater relative contribution of PBDEs to the sum FR contamination in American eels indicated an on-going exposure to these substances. High contributions of alternate BFRs in juvenile eels indicated an increased use of these substances in recent years. Concentrations seemed to be driven primarily by location, rather than life stage or age.

Brominated flame retardants and dechloranes in eels from German Rivers.

The levels of PBDEs, alternate BFRs and dechloranes in European Eel (Anguilla anguilla) samples (elvers, yellow and silver eels) were investigated to compare the contamination of eels from the rivers Elbe and Rhine and to estimate the BFR contamination throughout the eel's life cycle. PBDEs were the dominating flame retardants (FRs) in muscle tissues of yellow and silver eels, while the alternate BFR 2,3-dibromopropyl-2,4,6-tribromophenyl ether (DPTE) and the Dechlorane 602 were the dominating FRs in elvers (juvenile eels). Concentrations of FRs in silver eels from river Rhine were generally higher than concentrations in other eels analysed with up to 46 ng g(-1) wet weight (ww) ∑PBDEs. The concentrations in yellow and silver eels from river Elbe were similar with an average of 9.0±5.1 ng g(-1)ww and 8.1±3.7 ng g(-1)ww respectively. PBDE concentrations in elvers were comparably low (0.02 (BDE-100) to 0.1 (BDE-183) ng g(-1)ww), which lead to the conclusion that these contaminants were mostly ingested within the rivers. Among the alternate BFRs and dechloranes, DPTE as well as the Dechlorane 602 and Dechlorane Plus (DP) were found in all life cycle stages and rivers with concentrations between 0.01 ng g(-1)ww and 0.7 ng g(-1)ww. Dechlorane 603 could only be detected in silver eels from river Rhine. Pentabromoethylbenzene (PBEB) was only found in yellow and silver eels and bis(2-ethylhexyl)tetrabromophthalate (BEHTBP) could only be detected in elvers. These are the first reports of Dec-602 and 603 in aquatic organisms from Europe. The results of this study show the lasting relevance of PBDEs as contaminants in rivers and river-dwelling species but also the growing relevance of emerging contaminants such as alternate BFRs and dechloranes.