Epigenetic patterns in Atlantic herring (Clupea harengus): Temperature and photoperiod as environmental stressors during larval development.

Understanding the molecular mechanisms underlying individual responses to environmental changes is crucial for species conservation and management. Pelagic fishes including Atlantic herring (Clupea harengus) are of particular interest because of their key ecological and economic roles and their susceptibility to a changing ocean from global warming. Temperature and photoperiod have been linked with spawning time and location in adult herring, but no study has thus far investigated the role of environmental factors on gene regulation during the vulnerable early developmental stages. Here, we examine DNA methylation patterns of larval herring bred under two temperatures (11°C and 13°C) and photoperiod (6 and 12 h) regimes in a 2 × 2 factorial design. We found consistently high levels of global methylation across all individuals and a decline in global methylation with increased developmental stage that was more pronounced at 13°C (p ≤ 0.007) than at 11°C (p ≥ 0.21). Most of the differentially methylated sites were in exon and promoter regions for genes linked to metabolism and development, some of which were hypermethylated at higher temperature. These results demonstrate the important role of DNA methylation during larval development and suggest that this molecular mechanism might be key in regulating early-stage responses to environmental stressors in Atlantic herring.

Early arrival of spring-spawning Atlantic herring Clupea harengus at their spawning ground in the Kiel Fjord, western Baltic, relates to increasing winter seawater temperature.

The disturbance of marine organism phenology due to climate change and the subsequent effects on recruitment success are still poorly understood, especially in migratory fish species, such as the Atlantic herring (Clupea harengus; Clupeidae). Here we used the commercial catch data from a local fisher over a 50-year period (1971-2020) to estimate western Baltic spring-spawning (WBSS) herring mean arrival time Q50 (i.e., the week when 50% of the total fish catches had been made) at their spawning ground within the Kiel Fjord, southwest Baltic Sea, and the duration of the spawning season for each year. The relationship between the seawater temperature in the Kiel Bight and other environmental parameters (such as water salinity, North Atlantic and Atlantic multidecadal oscillations) and Q50 was evaluated using a general linear model to test the hypothesis that fish arrived earlier after warm than cold winters. We also estimated the accumulated thermal time to Q50 during gonadal development to estimate the effects of seawater temperature on the variations of Q50. The results of this study revealed a dramatic decrease in herring catches within the Kiel Fjord since the mid-1990s, as documented for the whole southwestern Baltic Sea. Warmer winter seawater temperature was the only factor related to an earlier arrival (1 week for one January seawater temperature degree increase) of herring at their spawning ground. The relationship was found for the first time on week 52 of the year prior to spawning and was the strongest (50% of the variability explained) from the fourth week of January (8 weeks before the mean Q50 among the studied years). A thermal constant to Q50 (~316°C day) was found when temperatures were integrated from the 49th week of the year prior to spawning. These results indicate that seawater temperature enhanced the speed of gonadal maturation during the latest phases of gametogenesis, leading to an early fish arrival under warm conditions. The duration of the spawning season was elongated during warmer years, therefore potentially mitigating the effects of trophic mismatch when fish spawn early. The results of this study highlight the altering effects of climate change on the spawning activity of a migratory fish species in the Baltic Sea where fast global changes presage that in other coastal areas worldwide.

Identification of male heterogametic sex-determining regions on the Atlantic herring Clupea harengus genome.

The sex determination system of Atlantic herring Clupea harengus L., a commercially important fish, was investigated. Low coverage whole-genome sequencing of 48 females and 55 males and a genome-wide association study revealed two regions on chromosomes 8 and 21 associated with sex. The genotyping data of the single nucleotide polymorphisms associated with sex showed that 99.4% of the available female genotypes were homozygous, whereas 68.6% of the available male genotypes were heterozygous. This is close to the theoretical expectation of homo/heterozygous distribution at low sequencing coverage when the males are factually heterozygous. This suggested a male heterogametic sex determination system in C. harengus, consistent with other species within the Clupeiformes group. There were 76 protein coding genes on the sex regions but none of these genes were previously reported master sex regulation genes, or obviously related to sex determination. However, many of these genes are expressed in testis or ovary in other species, but the exact genes controlling sex determination in C. harengus could not be identified.

Apparently contradictory routes in the expansion of two fish species in the Eastern Atlantic.

One specimen of the boreal Clupea harengus (Clupeidae) was caught southerly, in the Gulf of Cádiz (southern Spain), whereas a specimen of the subtropical Epinephelus aeneus (Serranidae) was caught northerly, in Galician waters (north-west of Spain). These catches represent a new southernmost record in the eastern Atlantic for C. harengus and the second northernmost for E. aeneus. The co-occurrence of warm and cold affinity fishes in temperate latitudes is unusual, but the existence of anomalies in the temperature of the Atlantic waters could be behind these findings.

Variation in egg mass within two Atlantic herring Clupea harengus stocks.

The main objective of this study was to investigate if egg size (mass) at spawning is invariant for Scotia-Fundy summer and autumn (SFSH) and Icelandic summer (ISSH) spawning herring Clupea harengus. Oocyte dry mass measurements for SFSH females collected in 2001 and ISSH females collected in 1999 and 2000 showed a large variation. Difference in egg dry mass among fish was found to vary by as much as twofold in each stock. For ISSH, variation in egg mass was also apparent from oocyte volume measurements made jointly with a histological examination of the ovaries. Approximately 20% of the variation in egg mass could be explained by maternal whole-body mass or total length, indicating that length or age composition in the stocks can potentially influence the recruitment success. This implies that fisheries management strategies should aim to maintain a broad range in age composition.

Detection of Allee effects in marine fishes: analytical biases generated by data availability and model selection.

The demographic Allee effect, or depensation, implies positive association between per capita population growth rate and population size at low abundances, thereby lowering growth ability of sparse populations. This can have far-reaching consequences on population recovery ability and colonization success. In the context of marine fishes, there is a widespread perception that Allee effects are rare or non-existent. However, studies that have failed to detect Allee effects in marine fishes have suffered from several fundamental methodological and data limitations. In the present study, we challenge the prevailing perception about the rarity of Allee effects by analysing nine populations of Atlantic herring (Clupea harengus), using Bayesian statistical methods. We find that populations of the same species can show either strong evidence for Allee effects or compensation. We explicitly demonstrate how the evidence for Allee effects is strongly provisional on observations made at low population abundances. We contrast our statistical approach with previous attempts to detect Allee effects and illustrate methodological issues that can lead to erroneous conclusions about the nature of population dynamics at low abundance. The present study demonstrates that there is no substantive scientific basis to support the perception that Allee effects are rare or non-existent in marine fishes.

Population genomic evidence for adaptive differentiation in the Baltic Sea herring.

Detecting and estimating the degree of genetic differentiation among populations of highly mobile marine fish having pelagic larval stages is challenging because their effective population sizes can be large, and thus, little genetic drift and differentiation is expected in neutral genomic sites. However, genomic sites subject to directional selection stemming from variation in local environmental conditions can still show substantial genetic differentiation, yet these signatures can be hard to detect with low-throughput approaches. Using a pooled RAD-seq approach, we investigated genomewide patterns of genetic variability and differentiation within and among 20 populations of Atlantic herring in the Baltic Sea (and adjacent Atlantic sites), where previous low-throughput studies and/or studies based on few populations have found limited evidence for genetic differentiation. Stringent quality control was applied in the filtering of 1 791 254 SNPs, resulting in a final data set of 68 182 polymorphic loci. Clear differentiation was identified between Atlantic and Baltic populations in many genomic sites, while differentiation within the Baltic Sea area was weaker and geographically less structured. However, outlier analyses - whether including all populations or only those within the Baltic Sea - uncovered hundreds of directionally selected loci in which variability was associated with either salinity, temperature or both. Hence, our results support the view that although the degree of genetic differentiation among Baltic Sea herring populations is low, there are many genomic regions showing elevated divergence, apparently as a response to temperature- and salinity-related natural selection. As such, the results add to the increasing evidence of local adaptation in highly mobile marine organisms, and those in the young Baltic Sea in particular.

Thermal impacts on the growth, development and ontogeny of critical swimming speed in Atlantic herring larvae.

Increases in swimming ability have a profound influence on larval fish growth and survival by increasing foraging success, predator avoidance and the ability to favorably influence transport. Understanding how development and environmental factors combine to influence swimming performance in aquatic organisms is particularly important during the transition from viscous to inertial environments. We measured the growth, development and ontogenetic changes in critical swimming speed (Ucrit) in Atlantic herring (Clupea harengus) larvae reared at three temperatures (7, 11, 15°C). Temperature had a significant effect on growth rates (from 0.21 at 7°C to 0.34mm·d(-1) at 15°C), and larval morphology-at-length (increased dry weight (DW), body height and developmental rate at warmer temperatures). Temperature-dependent differences in morphology influenced swimming performance (e.g. the exponential increase in Ucrit with increasing body size was faster at warmer temperatures). Larvae entered the transition to an inertial environment (Reynolds numbers ≥300) at body lengths between 15 (15°C) and 17mm (7°C). Inter-individual differences in Ucrit were not related to nutritional condition (RNA·DNA(-1) or DNA·DW(-1)), but were negatively correlated to length-at-age, suggesting a trade-off between growth rate and locomotor activity. The Ucrit data from this and previously published studies suggest that Atlantic herring pass through four activity phases: 1) yolk-sac (<0.6cm·s(-1)), 2) pre-flexion (0.6-3.0cm·s(-1), temperature effect changes with body size), 3) post-flexion (up to 6-8cm·s(-1), Q10~1.8-2.0), 4) juvenile-adult period (20-170cm·s(-1)).

Investigating the effects of pelagic trawling on the welfare of Atlantic herring (Clupea harengus).

The effects of pelagic trawling on the health and welfare of Atlantic herring (Clupea harengus L.) were investigated on a refrigerated seawater vessel operating in the North Sea. A total of 495 Atlantic herring (Clupea harengus L.) were sampled during five hauls from two fishing trips in September 2021 and 2022. For assessments of consciousness and mortality, a Reflex Action Mortality Predictor test (i.e. RAMP-test) was used on herring collected following trawling and pumping. Inspections for external and internal damage or wounds were performed via morphological welfare indicators and analyses of photos and radiographs. In addition, blood samples were taken and analysed for haematological indicators of stress. Following trawling and pumping, only 5% of the investigated herring showed signs of external wounds associated with the morphological indicators of welfare, and no internal damage was observed in the radiographic inspections. However, 96% of the assessed herring scored 0 on all three reflexes included in the RAMP-test and were therefore judged dead. On average, herring lost 95% of their scales, while 95% of herring had a very high degree of ruptured red blood cells (i.e. haemolysis). Extensive scale loss results in a deterioration of the skin's protective barrier function, which in turn impairs the osmoregulatory capacity of the herring. This was evident by elevated levels of plasma osmolality and circulating chloride concentrations, which could also likely explain the high occurrence of haemolysis in captured herring. Extended trawling time and larger catch size proved to be two important factors to consider, as the former led to increased plasma levels of osmolality, whereas the latter was associated with elevated plasma levels of lactate and cortisol. In conclusion, the high mortality appears to be influenced by a combination of factors such as severe stress, loss of osmoregulatory ability, crowding density within the trawl, and extended trawling times. This study provides important information on the welfare of wild Atlantic herring caught using pelagic trawls and highlights areas where improvements can be made to safeguard the welfare of fish captured in pelagic fisheries in the future.

Five cuts from herring (Clupea harengus): Comparison of nutritional and chemical composition between co-product fractions and fillets.

Weight distribution, proximate composition, fatty acids, amino acids, minerals and vitamins were investigated in five sorted cuts (head, backbone, viscera + belly flap, tail, fillet) emerging during filleting of spring and fall herring (Clupea harengus). The herring co-product cuts constituted âˆ¼ 60 % of the whole herring weight, with backbone and head dominating. Substantial amounts of lipids (5.8-17.6 % wet weight, ww) and proteins (12.8-19.2 % ww) were identified in the co-products, the former being higher in fall than in spring samples. Co-product cuts contained up to 43.1 % long-chain n-3 polyunsaturated fatty acids (LC n-3 PUFA) of total FA, absolute levels peaking in viscera + belly flap. All cuts contained high levels of essential amino acids (up to 43.3 %), nutritional minerals (e.g., iodine, selenium, calcium, and iron/heme-iron), and vitamins E, D, and B12. Co-products were, in many cases, more nutrient-rich than the fillet and could be excellent sources for both (functional) food and nutraceuticals.

High Lipid Content of Prey Fish and n-3 PUFA Peroxidation Impair the Thiamine Status of Feeding-Migrating Atlantic Salmon (Salmo salar) and Is Reflected in Hepatic Biochemical Indices.

Signs of impaired thiamine (vitamin B1) status in feeding-migrating Atlantic salmon (Salmo salar) were studied in three Baltic Sea areas, which differ in the proportion and nutritional composition of prey fish sprat (Sprattus sprattus) and herring (Clupea harengus). The concentration of n-3 polyunsaturated fatty acids (n-3 PUFAs) increased in salmon with dietary lipids and n-3 PUFAs, and the hepatic peroxidation product malondialdehyde (MDA) concentration increased exponentially with increasing n-3 PUFA and docosahexaenoic acid (DHA, 22:6n-3) concentration, whereas hepatic total thiamine concentration, a sensitive indicator of thiamine status, decreased with the increase in both body lipid and n-3 PUFA or DHA concentration. The hepatic glucose 6-phosphate dehydrogenase activity was suppressed by high dietary lipids. In salmon muscle and in prey fish, the proportion of thiamine pyrophosphate increased, and that of free thiamine decreased, with increasing body lipid content or PUFAs, or merely DHA. The thiamine status of salmon was impaired mainly due to the peroxidation of n-3 PUFAs, whereas lipids as a source of metabolic energy had less effect. Organochlorines or general oxidative stress did not affect the thiamine status. The amount of lipids, and, specifically, their long-chain n-3 PUFAs, are thus responsible for generating thiamine deficiency, and not a prey fish species per se.

Assessing microplastic as a vector for chemical entry into fish larvae using a novel tube-feeding approach.

A tube-feeding model for administering microplastic (MP, Ø = 30 µm) spheres to fish larvae was employed to quantify the uptake of hydrophobic organic contaminants (HOCs) into the larval body through a single administration of MP. Polychlorinated biphenyl-153 (PCB-153) was used as a representative HOC that can be sorbed to MP in the sea. Atlantic herring (Clupea harengus) larvae (34-51 days post-hatching) were selected as the animal model. The herring larvae were tube-fed a single load of up to 200 polystyrene or polyethylene MP spheres spiked with 14C-labelled PCB-153, and the control larvae were tube-fed an isotonic solution without MP. At the time of sampling (24 h post feeding), some larvae had evacuated all MP spheres from the gut, while others still had MP remaining in the gut. In larvae with a significant number of MP spheres still present in the gut, whole-body scintillation counting (including the MP in the gut lumen) showed elevated levels of the tracer compared to those in the control fish larvae. For larvae in which all or almost all MP had been evacuated by the time of sampling, the tracer levels of the whole body were not significantly different compared to those for the control fish larvae. These data indicate that there was no significant transfer of PCB-153 from contaminated MP into fish larvae within a gut-transit time of <24 h. This study suggests that the vector role of MP in HOC uptake and absorption may be minor compared to that of other HOC uptake pathways.

Nutritional and Sensory Properties of Protein Hydrolysates Based on Salmon (Salmo salar), Mackerel (Scomber scombrus), and Herring (Clupea harengus) Heads and Backbones.

Protein hydrolysates based on salmon, mackerel, and herring heads and backbones were produced, and the sensory properties of the hydrolysates were evaluated by a highly trained sensory panel. The nutritional content of the products was evaluated, and the hydrolysates contained all the amino acids inherent to the raw material, including considerable levels of connective tissue amino acids glycine, proline, and hydroxyproline. Hydrolysates based on herring were the most flavor intense, whereas hydrolysates based on salmon were deemed more palatable. In this work, choice of fraction (heads vs. backbones) and enzyme had minor effects on sensory and nutritional properties, indicating that choice of raw material species was the major factor for flavor development in the produced protein hydrolysates. There were large variations in protein content and amino acid composition in the raw material fractions, but as expected, only minor variations were found in the final products.

Stabilization of herring (Clupea harengus) by-products against lipid oxidation by rinsing and incubation with antioxidant solutions.

To allow value adding into foods, stabilizing strategies for fish by-products are needed based on their high susceptibility to hemoglobin (Hb)-mediated lipid oxidation. Here, three strategies for preventing lipid oxidation in herring (Clupea harengus) by-products during ice-storage were studied: (i) rinsing away Hb with water or 0.9% NaCl with/without antioxidants (Duralox-MANC, erythorbate and ethylenediamine-tetraacetic acid (EDTA)), (ii) incubation in water/0.9% NaCl with/without antioxidants, (iii) mincing with subsequent addition of the mentioned antioxidants. Only 10-18% Hb was rinsed away in (i), and the effect of this rinsing on peroxide value (PV) or TBA-reactive substances (TBARS) development was limited. Rinsing or incubating by-products in antioxidant solutions however significantly (p ≤ 0.05) increased shelf life from <1 day to >12 days; Duralox-MANC was particularly efficient. The presented strategies could hereby facilitate more diversified end-use of herring by-products from being 100% feed, to include also high-quality minces, protein isolates or oils for the food industry.

Sources of polychlorinated dibenzo-p-dioxins and dibenzofurans to Baltic Sea herring.

Levels of polychlorinated dibenzo-p-dioxins and dibenzofurans (PCDD/Fs) in herring (Clupea harengus) remain high in several parts of the Baltic Sea, despite declines in PCDD/F emissions since the 1980s. The reasons behind this are not well understood. This study applied a statistical modeling approach where sources of PCDD/Fs that contaminate Baltic biota were quantitatively assessed by analyzing existing datasets. PCDD/F patterns were extracted from a herring dataset using positive matrix factorization (PMF). The extracted biota patterns were transformed into sediment patterns using fish-to-sediment transformation factors, and the resulting patterns were compared with known source PCDD/F patterns. The model distinguished three model patterns, which explained 85% of the data. These patterns were matched to tetra-chlorophenol (TCP), penta-chlorophenol/atmospheric background (PCP/AB), and thermal source patterns, respectively. The thermal source was the largest contributor to toxic equivalents (TEQ) in herring, but the level decreased from 42 ±â€¯9.0 pg TEQ g-1 lipid weight (lw) before year 2000 (pre-2000) to 15 ±â€¯2.4 pg TEQ g-1 lw post-2000, i.e., a decline of around one-third in the original TEQ concentration. The contribution of TCP more than doubled, from 2.1 ±â€¯0.62 pg TEQ g-1 lw to 5.6 ±â€¯1.1 pg TEQ g-1 lw, and the relative contribution of PCP/AB also increased. These increasing trends suggest that, as primary air emissions of PCDD/Fs are managed and levels decline, the impact of TCP and PCP/AB sources on Baltic Sea biota will become more important over time and that PCDD/F-contaminated sites in coastal areas and marine environments require more attention.

Making the most of survey data: Incorporating age uncertainty when fitting growth parameters.

Individual growth is an important parameter and is linked to a number of other biological processes. It is commonly modeled using the von Bertalanffy growth function (VBGF), which is regularly fitted to age data where the ages of the animals are not known exactly but are binned into yearly age groups, such as fish survey data. Current methods of fitting the VBGF to these data treat all the binned ages as the actual ages. We present a new VBGF model that combines data from multiple surveys and allows the actual age of an animal to be inferred. By fitting to survey data for Atlantic herring (Clupea harengus) and Atlantic cod (Gadus morhua), we compare our model with two other ways of combining data from multiple surveys but where the ages are as reported in the survey data. We use the fitted parameters as inputs into a yield-per-recruit model to see what would happen to advice given to management. We found that each of the ways of combining the data leads to different parameter estimates for the VBGF and advice for policymakers. Our model fitted to the data better than either of the other models and also reduced the uncertainty in the parameter estimates and models used to inform management. Our model is a robust way of fitting the VBGF and can be used to combine data from multiple sources. The model is general enough to fit other growth curves for any taxon when the age of individuals is binned into groups.

Selection by higher-order effects of salinity and bacteria on early life-stages of Western Baltic spring-spawning herring.

Habitat stratification by abiotic and biotic factors initiates divergence of populations and leads to ecological speciation. In contrast to fully marine waters, the Baltic Sea is stratified by a salinity gradient that strongly affects fish physiology, distribution, diversity and virulence of important marine pathogens. Animals thus face the challenge to simultaneously adapt to the concurrent salinity and cope with the selection imposed by the changing pathogenic virulence. Western Baltic spring-spawning herring (Clupea harengus) migrate to spawning grounds characterized by different salinities to which herring are supposedly adapted. We hypothesized that herring populations do not only have to cope with different salinity levels but that they are simultaneously exposed to higher-order effects that accompany the shifts in salinity, that is induced pathogenicity of Vibrio bacteria in lower saline waters. To experimentally evaluate this, adults of two populations were caught in their spawning grounds and fully reciprocally crossed within and between populations. Larvae were reared at three salinity levels, representing the spawning ground salinity of each of the two populations, or Atlantic salinity conditions resembling the phylogenetic origin of Clupea harengus. In addition, larvae were exposed to a Vibrio spp. infection. Life-history traits and gene expression analysis served as response variables. Herring seem adapted to Baltic Sea conditions and cope better with low saline waters. However, upon a bacterial infection, herring larvae suffer more when kept at lower salinities implying reduced resistance against Vibrio or higher Vibrio virulence. In the context of recent climate change with less saline marine waters in the Baltic Sea, such interactions may constitute key future stressors.

Projected habitat loss for Atlantic herring in the Baltic Sea.

Projected, climate-driven changes in rainfall patterns are expected to alter the salinity (S) of estuaries and larger brackish water bodies, such as the Baltic Sea. Some marine fish larvae are potentially more sensitive to low salinity than older stages, hence we compared the low salinity tolerance of Atlantic herring (Clupea harengus) larvae at the individual and population levels including four populations in the North and Baltic Seas. Acute low salinity tolerance was similar (S = 1.9-2.7) across populations and increased with increasing body size. Based on this physiological threshold and a regionally down-scaled climate model, spawning habitats in the northern and eastern Baltic Sea are projected to be largely unsuitable for herring by 2100. Although adaptive mechanisms may attenuate the effect in some species, the limited physiological tolerance of fish larvae will remain an important bottleneck for the persistence of marine fish populations in brackish waters undergoing climate-driven freshening.

Marine ecosystem connectivity mediated by migrant-resident interactions and the concomitant cross-system flux of lipids.

Accumulating research argues that migrants influence the functioning and productivity of local habitats and ecosystems along migration routes and potentially drive cross-system energy fluxes of considerable magnitude, yet empirical documentation of local ecological effects and descriptions of the underlying mechanisms are surprisingly rare. In this study, we discovered migrant-resident interactions and substantial cross-system lipid transportation in the transition zone between the Baltic Sea and the North Sea where a resident cod population (predators) was found to interact with a herring population (prey) on a seasonal basis. We traced the lipids, using fatty acid trophic markers (FATM), from the herring feeding grounds in the North Sea to the cod livers in the Western Baltic Sea. Time series analysis of population dynamics indicated that population-level production of cod is positively affected by the herring subsidies. However, the underlying mechanisms were more complicated than anticipated. During the herring season, large cod received most of its dietary lipids from the herring, whereas smaller cod were prevented from accessing the lipid pool due to a mismatch in predator-prey size ratio. Furthermore, while the herring were extremely rich in bulk energy, they were surprisingly poor in a specific functional fatty acid. Hence, our study was the first to illustrate how the magnitude cross-system fluxes of subsidies in migrant-resident systems are potentially constrained by the size structure of the resident predator population and the nutritional quality of the migrants.