Early ontogeny of the lesser sandeel (Ammodytes marinus).

BACKGROUND: Lesser sandeel (Ammodytes marinus) is widely distributed in North Sea ecosystems. Sandeel acts as a critical trophic link between zooplankton and top predators (fish, mammals, sea birds). Because they live buried in the sand, sandeel may be directly affected by the rapid expansion of anthropogenic activities linked to their habitat on the sea bottom (e.g., hydrocarbon extraction, offshore renewable energy, and subsea mining). It is, therefore, important to understand the impact of cumulative environmental and anthropogenic stressors on this species. A detailed description of the ontogenetic timeline and developmental staging for this species is lacking limiting the possibilities for comparative developmental studies assessing, e.g., the impact of various environmental stressors. RESULTS: A detailed description of the morphological development of lesser sandeel and their developmental trajectory, obtained through visual observations and microscopic techniques, is presented. Methods for gamete stripping and intensive culture of the early life stages are also provided. CONCLUSION: This work provides a basis for future research to understand the effect of cumulative environmental and anthropogenic stressors on development in the early life stages of lesser sandeel.

Atlantic cod (Gadus morhua) larvae are attracted by low-frequency noise simulating that of operating offshore wind farms.

The number and size of offshore wind (OW) turbines is increasing rapidly. OW turbines produce continuous, low-frequency noise that could impact marine fish dispersing/migrating through the facilities. Any such impact would be relevant for larval stages, which have limited possibility to swim away from OW facilities. If directional movement of fish larvae at sea is impacted by low-frequency continuous sound is unknown. We observe the behavior of Atlantic cod larvae (N = 89) in response to low-frequency sound while they are drifting in a Norwegian fjord inside transparent drifting chambers. We transmit 100 Hz continuous sound in the fjord, in the intensity range of OW turbines' operational noise, and measure the sound pressure and 3-D particle motion. Half of the larvae (N = 45) are exposed to low-frequency (100 Hz) continuous sound, while the other half (N = 44) are observed under the same conditions but without the sound. Exposure does not affect the routine and maximum swimming speeds or the turning behavior of the larvae. Control larvae orient to the northwest. In contrast, exposed larvae orient towards the source of low-frequency sound and particle motion. This provides a basis to assess how OW might impact dispersal in this species.

Magnetic fields generated by submarine power cables have a negligible effect on the swimming behavior of Atlantic lumpfish (Cyclopterus lumpus) juveniles.

Submarine power cables carry electricity over long distances. Their geographic distribution, number, and areal coverage are increasing rapidly with the development of, for example, offshore wind facilities. The flow of current passing through these cables creates a magnetic field (MF) that can potentially affect marine organisms, particularly those that are magnetosensitive. The lumpfish (Cyclopterus lumpus) is a migratory species that is widely distributed in the North Atlantic Ocean and Barents Sea. It migrates between coastal spawning grounds and pelagic offshore feeding areas. We tested whether lumpfish respond to MFs of the same intensity as those emitted by high voltage direct current (HVDC) submarine power cables. Laboratory experiments were conducted by placing juvenile lumpfish in an artificial MF gradient generated by a Helmholtz coil system. The intensity of the artificial MF used (230 µT) corresponded to the field at 1 m from a high-power submarine cable. The fish were filmed for 30 min with the coil either on or off. Swimming speeds, and presence in the different parts of a raceway, were extracted from the videos and analyzed. Juvenile lumpfish activity, defined as the time that the fish spent swimming relative to stationary pauses (attached to the substrate), and the distance travelled, were unaffected by exposure to the artificial MF. The swimming speed of juvenile lumpfish was reduced (by 16%) when the coil was on indicating that the fish could either sense the MF or the induced electric field created by the movement of the fish through the magnetic field. However, it seems unlikely that a 16% decrease in swimming speed occurring within 1 m of HVDC cables would significantly affect Atlantic lumpfish migration or homing.

Co-exposure to UV radiation and crude oil increases acute embryotoxicity and sublethal malformations in the early life stages of Atlantic haddock (Melanogrammus aeglefinus).

Crude oil causes severe abnormalities in developing fish. Photomodification of constituents in crude oil increases its toxicity several fold. We report on the effect of crude oil, in combination with ultraviolet (UV) radiation, on Atlantic haddock (Melanogrammus aeglefinus) embryos. Accumulation of crude oil on the eggshell makes haddock embryos particularly susceptible to exposure. At high latitudes, they can be exposed to UV radiation many hours a day. Haddock embryos were exposed to crude oil (5-300 µg oil/L nominal loading concentrations) for three days in the presence and absence of UV radiation (290-400 nm). UV radiation partly degraded the eggs' outer membrane resulting in less accumulation of oil droplets in the treatment with highest oil concentration (300 µg oil/L). The co-exposure treatments resulted in acute toxicity, manifested by massive tissue necrosis and subsequent mortality, reducing LC50 at hatching stage by 60 % to 0.24 µg totPAH/L compared to 0.62 µg totPAH/L in crude oil only. In the treatment with nominal low oil concentrations (5-30 µg oil/L), only co-exposure to UV led to sublethal morphological heart defects. Including phototoxicity as a parameter in risk assessments of accidental oil spills is recommended.

Blood-based gene expression as non-lethal tool for inferring salinity-habitat history of European eel (Anguilla anguilla).

The European eel is a facultative catadromous species, meaning that it can skip the freshwater phase or move between marine and freshwater habitats during its continental life stage. Otolith microchemistry, used to determine the habitat use of eel or its salinity history, requires the sacrifice of animals. In this context, blood-based gene expression may represent a non-lethal alternative. In this work, we tested the ability of blood transcriptional profiling to identify the different salinity-habitat histories of European eel. Eels collected from different locations in Norway were classified through otolith microchemistry as freshwater residents (FWR), seawater residents (SWR) or inter-habitat shifters (IHS). We detected 3451 differentially expressed genes from blood by comparing FWR and SWR groups, and then used that subset of genes in a machine learning approach (i.e., random forest) to the extended FWR, SWR, and IHS group. Random forest correctly classified 100% of FWR and SWR and 83% of the IHS using a minimum of 30 genes. The implementation of this non-lethal approach may replace otolith-based microchemistry analysis for the general assessment of life-history tactics in European eels. Overall, this approach is promising for the replacement or reduction of other lethal analyses in determining certain fish traits.

Increasing temperature and prey availability affect the growth and swimming kinematics of Atlantic herring (Clupea harengus) larvae.

Climate change will increase the magnitude and duration of warming events and the variability in the phenology and abundance of available prey to the early life stages of fish. These factors influence physiological, behavioral and ecological processes, impacting growth, development and survival. Using a fully factorial design with two prey-availability treatments (1200 prey items L-1 (high prey abundance) or 40 prey items L-1 (low prey abundance)) under three temperature regimes (8, 10 and 12°C), the swimming kinematics of 6-week old spring-spawning Atlantic herring larvae were examined using silhouette video photography. Higher temperatures combined with food limitation significantly decreased the growth and swimming kinematics of larval herring, with the most negative effect observed in larvae reared at 12°C and exposed to low food abundances. Specifically, larvae displayed reduced locomotory behaviors and reduced vertical movements. By contrast, larvae reared at high prey abundance and at 12°C displayed more active swimming and exploratory behavior, as evidenced by an increase in both locomotory behavior and vertical and horizontal turn angles, suggesting increased motivation to search for food. This research highlights the importance of determining to what degree fish larvae are sensitive to changes in temperature and how these changes might be further influenced by food availability.

Magnetic fields generated by the DC cables of offshore wind farms have no effect on spatial distribution or swimming behavior of lesser sandeel larvae (Ammodytes marinus).

In the North Sea, the number and size of offshore wind (OW) turbines, together with the associated network of High Voltage Direct Current (HVDC) subsea cables, will increase rapidly over the coming years. HVDC cables produce magnetic fields (MFs) that might have an impact on marine animals that encounter them. One of the fish species that is at risk of exposure to MF associated with OW is the lesser sandeel (Ammodytes marinus), a keystone species of the North Sea basin. Lesser sandeel could be exposed to MF as larvae, when they drift in proximity of OW turbines. Whether MFs impact the behavior of lesser sandeel larvae, with possible downstream effects on their dispersal and survival, is unknown. We tested the behavior of 56 lesser sandeel larvae, using a setup designed to simulate the scenario of larvae drifting past a DC cable. We exposed the larvae to a MF intensity gradient (150-50 µT) that is within the range of MFs produced by HVDC subsea cables. Exposure to the MF gradient did not affect the spatial distribution of lesser sandeel larvae in a raceway tank 50 cm long, 7 cm wide and 3.5 cm deep. Nor did the MF alter their swimming speed, acceleration or distance moved. These results show that static MF from DC cables would not impact behavior of lesser sandeel larvae during the larval period of their life although it does not exclude the possibility that later life stages could be affected.

Magnetic fields produced by subsea high-voltage direct current cables reduce swimming activity of haddock larvae (Melanogrammus aeglefinus).

High-voltage direct current (HVDC) subsea cables are used to transport power between locations and from/to nearshore and offshore facilities. HVDC cables produce magnetic fields (B-fields) that could impact marine fish. Atlantic haddock (Melanogrammus aeglefinus) is a demersal fish that is at risk of exposure to anthropogenic B-fields. Their larvae drift over the continental shelf, and use the Earth's magnetic field for orientation during dispersal. Therefore, anthropogenic magnetic fields from HVDC cables could alter their behavior. We tested the behavior of 92 haddock larvae using a setup designed to simulate the scenario of larvae drifting past a B-field in the intensity range of that produced by a DC subsea cable. We exposed the larvae to a B-field intensity ranging from 50 to 150 µT in a raceway tank. Exposure to the B-field did not affect the spatial distribution of haddock larvae in the raceway. Larvae were categorized by differences in their exploratory behavior in the raceway. The majority (78%) of larvae were nonexploratory, and exposure to the artificial B-field reduced their median swimming speed by 60% and decreased their median acceleration by 38%. There was no effect on swimming of the smaller proportion (22%) of exploratory larvae. These observations support the conclusion that the swimming performance of nonexploratory haddock larvae would be reduced following exposure to B-field from HVDC cables. The selective impact on nonexploratory individuals, and the lack of impact on exploratory individuals, could have population-scale implications for haddock in the wild.

Joint temporal trends in river thermal and hydrological conditions can threaten the downstream migration of the critically endangered European eel.

Climate change is modifying the hydrological and thermal regimes of rivers worldwide, threatening the triggering of organisms' key life-cycle processes. European eel (Anguilla anguilla) is a critically endangered fish species that migrates over several thousand kilometres between its rearing habitats in continental waters of Europe and North Africa and its spawning area in the Sargasso Sea. Downstream migration of adult eels occurs during periods of decreasing river water temperature associated with high discharge but changes in these environmental cues may affected eel migratory conditions. An innovative multivariate method was developed to analyse long-term datasets of daily water temperature, discharge and eel passage in two European rivers. Over the past 50 years, water temperature and discharge increased in both rivers during the downstream migration period from August to November. Silver eels preferentially migrated at temperatures between 10 and 20 °C combined with high discharge. Environmental changes have resulted in the migration of silver eels under warmer water temperatures. This example illustrates how the changes in environmental cues have led to a growing mismatch between the migratory conditions preferentially selected and those actually used, which may threaten the completion of the eel's life cycle and ultimately the persistence of this already critically endangered species.

Feeding habitat and silvering stage affect lipid content and fatty acid composition of European eel Anguilla anguilla tissues.

Lipids, particularly fatty acids (FAs), are major sources of energy and nutrients in aquatic ecosystems and play key roles during vertebrate development. The European eel Anguilla anguilla goes through major biochemical and physiological changes throughout its lifecycle as it inhabits sea- (SW), and/or brackish- (BW) and/or freshwater (FW) habitats. With the ultimate goal being to understand the reasons for eels adopting a certain life history strategy (FW or SW residency vs. 'habitat shifting'), we explored differences in lipid content and FA composition of muscle, liver and eyes from eels collected across Norwegian SW, BW and FW habitats, and at different lifecycle stages (yellow to silver). FW and SW eels had a higher lipid content overall compared to BW eels, reflecting differences in food availability and life history strategies. SW eels had higher proportions of certain monounsaturated FAs (MUFAs; 18:1n-9, 20:1n-9), and of the essential polyunsaturated FAs 20:5n-3 (eicosapentaenoic acid, EPA) and 22:6n-3 (docosahexaenoic acid) than FW eels, reflecting a marine-based diet. In contrast, the muscle of FW eels had higher proportions of 18:3n-3, 18:2n-6 and 20:4n-6 (arachidonic acid), as is typical of FW organisms. MUFA proportions increased in later stage eels, consistent with the hypothesis that the eels accumulate energy stores prior to migration. In addition, the decrease of EPA with advancing stage may be associated with the critical role that this FA plays in eel sexual development. Lipid and FA information provided further understanding of the habitat use and overall ecology of this critically endangered species.

Effects of Exposure to Low Concentrations of Oil on the Expression of Cytochrome P4501a and Routine Swimming Speed of Atlantic Haddock (Melanogrammus aeglefinus) Larvae In Situ.

Exposure to environmentally relevant concentrations of oil could impact survival of fish larvae in situ through subtle effects on larval behavior. During the larval period, Atlantic haddock (Melanogrammus aeglefinus) are transported toward nursery grounds by ocean currents and active swimming, which can modify their drift route. Haddock larvae are sensitive to dispersed oil; however, whether exposure to oil during development impacts the ability of haddock larvae to swim in situ is unknown. Here, we exposed Atlantic haddock embryos to 10 and 80 µg oil/L (0.1 and 0.8 µg ∑PAH/L) of crude oil for 8 days and used a novel approach to measure its effect on the larval swimming behavior in situ. We assessed the swimming behavior of 138 haddock larvae in situ, in the North Sea, using a transparent drifting chamber. Expression of cytochrome P4501a (cyp1a) was also measured. Exposure to 10 and 80 µg oil/L significantly reduced the average in situ routine swimming speed by 30-40% compared to the controls. Expression of cyp1a was significantly higher in both exposed groups. This study reports key information for improving oil spill risk assessment models and presents a novel approach to study sublethal effects of pollutants on fish larvae in situ.

Age of European silver eels during a period of declining abundance in Norway.

The European eel (Anguilla anguilla) is critically endangered throughout its range. Knowledge about age distribution of future spawners (silver eels) is essential to monitor the status and contribute to the recovery of this species. Determination of age in anguillid eels is challenging, especially in eels from the northern part of the distribution area where growth is slow and age at maturation can be up to 30 years or more. Eels from the river Imsa in Norway have been monitored since 1975, and this reference time series has been used to assess the stock at the European level. Population dynamics in this catchment were analyzed during the late 1980s by estimating ages on whole cleared otoliths. However, techniques for revealing annual increments on otoliths have evolved over the years sometimes yielding significant differences in age estimates. In this study, the historical otolith data were reanalyzed using a grinding and polishing method rather than reading the whole otolith. The new age estimates were considerably higher than the previous ones, sometimes by up to 29 years. Since the 1980s, mean age of silver eels only slightly increased (from 19 to 21 years in the 2010s). This was mainly due to the disappearance of younger silver eels (<15 years) in the 2010s. The new age estimates agreed with the steep decline in recruitment which occurred in the late 1980s in the Imsa catchment. Mean growth (30 mm/year, min-max: 16-64 mm/year) has not changed since the 1980s, although density in the catchment has decreased. Revealing and reading age of slow-growing eels remain a challenge but adding a measure of otolith reading uncertainty may improve age data collection and contribute to recovery measures for this species.

Impact of magnetic fields generated by AC/DC submarine power cables on the behavior of juvenile European lobster (Homarus gammarus).

The number of submarine power cables using either direct or alternating current is expected to increase drastically in coming decades. Data concerning the impact of magnetic fields generated by these cables on marine invertebrates are scarce. In this context, the aim of this study was to explore the potential impact of anthropogenic static and time-varying magnetic fields on the behavior of recently settled juvenile European lobsters (Homarus gammarus) using two different behavioral assays. Day-light conditions were used to stimulate the sheltering behavior and facilitate the video tracking. We showed that juvenile lobsters did not exhibit any change of behavior when submitted to an artificial magnetic field gradient (maximum intensity of 200 µT) compared to non-exposed lobsters in the ambient magnetic field. Additionally, no influence was noted on either the lobsters' ability to find shelter or modified their exploratory behavior after one week of exposure to anthropogenic magnetic fields (225 ±â€¯5 µT) which remained similar to those observed in control individuals. It appears that static and time-varying anthropogenic magnetic fields, at these intensities, do not significantly impact the behavior of juvenile European lobsters in daylight conditions. Nevertheless, to form a complete picture for this biological model, further studies are needed on the other life stages as they may respond differently.

The planktonic stages of the salmon louse (Lepeophtheirus salmonis) are tolerant of end-of-century pCO2 concentrations.

The copepod Lepeophtheirus salmonis is an obligate ectoparasite of salmonids. Salmon lice are major pests in salmon aquaculture and due to its economic impact Lepeophtheirus salmonis is one of the most well studied species of marine parasite. However, there is limited understanding of how increased concentration of pCO2 associated with ocean acidification will impact host-parasite relationships. We investigated the effects of increased pCO2 on growth and metabolic rates in the planktonic stages, rearing L. salmonis from eggs to 12 days post hatch copepodids under three treatment levels: Control (416 µatm), Mid (747 µatm), and High (942 µatm). The pCO2 treatment had a significant effect on oxygen consumption rate with the High treatment animals exhibiting the greatest respiration. The treatments did not have a significant effect on the other biological endpoints measured (carbon, nitrogen, lipid volume, and fatty acid content). The results indicate that L. salmonis have mechanisms to compensate for increased concentration of pCO2and that populations will be tolerant of projected future ocean acidification scenarios. The work reported here also describes catabolism during the lecithotrophic development of L. salmonis, information that is not currently available to parameterize models of dispersal and viability of the planktonic free-living stages.

Exposure to teflubenzuron negatively impacts exploratory behavior, learning and activity of juvenile European lobster (Homarus gammarus).

Infestations with salmon lice, a parasitic copepod, is a major problem in the salmon farming industry. Teflubenzuron is an in-feed pharmaceutical applied to control lice outbreaks; the standard medication is 10 mg per kg fish per day for seven days. Surveys reveal that teflubenzuron accumulates and persists in the sediment around fish farms and causes deformities and mortality in juvenile European lobster (Homarus gammarus), a species commonly found in the vicinity of salmon farms in Norway. To date, there is no information on sub-lethal effects of teflubenzuron on, for example, behavior. We conducted an experiment to assess possible difference in the shelter seeking behavior of teflubenzuron-exposed (N = 19) vs. not exposed (N = 19) H. gammarus juveniles. The teflubenzuron-exposed juveniles had been given very low concentrations, 1.7 µg per pellet twice per week for 113 days prior to this experiment. The concentration of teflubenzuron was estimated to be less than 1 ng/g lobster when they were tested in the behavior experiment. Animals were placed in a lane with a shelter at one end. Once a lobster had found and entered the shelter, they were repeatedly displaced back to the opposite end of the lane, for a total of 3 repeated runs per animal. Three of the exposed juveniles failed to settle in the shelter, and the remaining teflubenzuron-exposed animals took significantly more time to explore the environment and to find and recognize shelter. Furthermore, exposed lobsters also exhibited slower walking speed compared to the controls. These results demonstrate that teflubenzuron significantly reduces exploratory behavior, learning and activity of juvenile H. gammarus. Thus, exposure to teflubenzuron could increase predation mortality of juvenile lobsters in the wild.

Whether European eel leptocephali use the Earth's magnetic field to guide their migration remains an open question.

European eels (Anguilla anguilla) migrate between the southwestern Sargasso Sea and the European and Mediterranean coasts. In a recent paper in Current Biology, Naisbett-Jones et al.[1] claim to "provide the first evidence that they [eels] derive positional information from the Earth's magnetic field" and that this information guides their migration. The evidence reported by Naisbett-Jones et al.[1] in support of this conclusion was derived from eels collected in the Severn River (UK), approximately 50 km upstream of the estuary (i.e. not "in the Severn Estuary" as stated by the authors). Eels collected this far into rivers are benthic and fully adapted to freshwater; that is, they are late-stage glass eels (∼ 2 years old), not the pelagic leptocephalus (larval) life stage that actually undertakes the trans-Atlantic migration. The entire interpretive framework for the Naisbett-Jones et al.[1] study rests on the assumption that the behaviour of these late-stage freshwater glass eels, and their responses to magnetic fields, can be used as a proxy for the responses of eel leptocephali. The authors present no evidence in support of this key assumption.

Glass eels (Anguilla anguilla) have a magnetic compass linked to the tidal cycle.

The European eel (Anguilla anguilla) has one of the longest migrations in the animal kingdom. It crosses the Atlantic Ocean twice during its life history, migrating between the spawning area in the Sargasso Sea and Europe, where it is widely distributed. The leptocephalus larvae drift with the Gulf Stream and other currents for more than a year and metamorphose into glass eels when they arrive on the continental shelf and move toward coastal areas. The mechanisms underlying glass eel orientation toward the coast and into freshwater systems are poorly known. However, anguillid eels, including the glass eel life stage, have a geomagnetic sense, suggesting the possibility that they use Earth's magnetic field to orient toward the coast. To test this hypothesis, we used a unique combination of laboratory tests and in situ behavioral observations conducted in a drifting circular arena. Most (98%) of the glass eels tested in the sea exhibited a preferred orientation that was related to the tidal cycle. Seventy-one percent of the same eels showed the same orientation during ebb tide when tested in the laboratory under a manipulated simulated magnetic field in the absence of any other cue. These results demonstrate that glass eels use a magnetic compass for orientation and suggest that this magnetic orientation system is linked to a circatidal rhythm.

Magnetic compass orientation in the European eel.

European eel migrate from freshwater or coastal habitats throughout Europe to their spawning grounds in the Sargasso Sea. However, their route (~ 6000 km) and orientation mechanisms are unknown. Several attempts have been made to prove the existence of magnetoreception in Anguilla sp., but none of these studies have demonstrated magnetic compass orientation in earth-strength magnetic field intensities. We tested eels in four altered magnetic field conditions where magnetic North was set at geographic North, South, East, or West. Eels oriented in a manner that was related to the tank in which they were housed before the test. At lower temperature (under 12°C), their orientation relative to magnetic North corresponded to the direction of their displacement from the holding tank. At higher temperatures (12-17°C), eels showed bimodal orientation along an axis perpendicular to the axis of their displacement. These temperature-related shifts in orientation may be linked to the changes in behavior that occur between the warm season (during which eels are foraging) and the colder fall and winter (during which eels undertake their migrations). These observations support the conclusion that 1. eels have a magnetic compass, and 2. they use this sense to orient in a direction that they have registered moments before they are displaced. The adaptive advantage of having a magnetic compass and learning the direction in which they have been displaced becomes clear when set in the context of the eel's seaward migration. For example, if their migration is halted or blocked, as it is the case when environmental conditions become unfavorable or when they encounter a barrier, eels would be able to resume their movements along their old bearing when conditions become favorable again or when they pass by the barrier.

Effect of sub-lethal exposure to ultraviolet radiation on the escape performance of Atlantic cod larvae (Gadus morhua).

UNLABELLED: The amount of ultraviolet (UV) radiation reaching the earth's surface has increased due to depletion of the ozone layer. Several studies have reported that UV radiation reduces survival of fish larvae. However, indirect and sub-lethal impacts of UV radiation on fish behavior have been given little consideration. We observed the escape performance of larval cod (24 dph, SL: 7.6±0.2 mm; 29 dph, SL: 8.2±0.3 mm) that had been exposed to sub-lethal levels of UV radiation vs. unexposed controls. Two predators were used (in separate experiments): two-spotted goby (Gobiusculus flavescens; a suction predator) and lion's mane jellyfish (Cyanea capillata; a "passive" ambush predator). Ten cod larvae were observed in the presence of a predator for 20 minutes using a digital video camera. Trials were replicated 4 times for goby and 5 times for jellyfish. Escape rate (total number of escapes/total number of attacks ×100), escape distance and the number of larvae remaining at the end of the experiment were measured. In the experiment with gobies, in the UV-treated larvae, both escape rate and escape distance (36%, 38±7.5 mm respectively) were significantly lower than those of control larvae (75%, 69±4.7 mm respectively). There was a significant difference in survival as well (UV: 35%, CONTROL: 63%). No apparent escape response was observed, and survival rate was not significantly different, between treatments (UV: 66%, CONTROL: 74%) in the experiment with jellyfish. We conclude that the effect and impact of exposure to sub-lethal levels of UV radiation on the escape performance of cod larvae depends on the type of predator. Our results also suggest that prediction of UV impacts on fish larvae based only on direct effects are underestimations.