The effect of progressive hypoxia on swimming activity and schooling in Atlantic herring

Schools of herring exposed to progressive hypoxia show a peak in velocity during severe hypoxia, at 15–34% oxygen saturation, followed by a decrease in swimming speed until school disruption occurred. The observed increase in swimming speed during severe hypoxia reveals a graded response, since the lower the fish's swimming speed prior to severe hypoxia ( U ₉₅₋₅₀, the speed at oxygen saturations between 95 and 50%), the greater the relative increase in swimming speed. The oxygen saturations at which both peak velocity and school disruption occurred were lower for fish with lowest U ₉₅₋₅₀, suggesting that the fish with the slowest speed U ₉₅₋₅₀ reach their critical P_O2 (at which there is respiratory distress) last, i.e. at lower oxygen saturation. At a functional level, it is suggested that herring encountering hypoxia increase their speed in order to find more favourable conditions, and the magnitude of this increase is modulated by their respiratory distress. It is also hypothesised that the observed increase in speed may be related to an increase in the rate of position shifting within the school. Since the oxygen saturation at which the response to hypoxia occurs and the magnitude of the response are related to the fish's preferred speed prior to severe hypoxia, it is suggested that such a preferred speed should be measured in experiments testing the effect of hypoxia on fish behaviour.     

The development of schooling behaviour in Atlantic herring Clupea harengus

The timing of the development of schooling behaviour in Atlantic herring Clupea harengus and the quantitative and qualitative evolution of such behaviour in the larval and post-metamorphic stages were investigated with a simulation model and experimental observations of laboratory-reared fish. Herring larvae started to develop schooling behaviour between the lengths of 35 and 40 mm. This coincided with the beginning of metamorphosis, characterized by ontogenetic changes which require a switch to a different antipredator strategy from that employed by early larvae, while providing the sensory and anatomical mechanisms necessary for the formation of schools. Schooling behaviour was established at the end of metamorphosis (50–55 mm) and its characteristics continued to evolve throughout the early juvenile stage. A critical period in terms of vulnerability to predation is expected between the end of the larval and beginning of the juvenile stages, before schooling behaviour is fully developed. The implications of some of the results for the methodology of future studies are also discussed.     

Development of microsatellite loci in Pacific herring (Clupea pallasi)

Fifteen polymorphic di‐, tri‐ and tetranucleotide microsatellite markers were developed in Pacific herring (Clupea pallasi) to aid in the delineation of population structure of herring in British Columbia. Twelve of the microsatellite loci were analysed in over 4000 wild herring. Expected heterozygosities ranged 0.73–0.95, and only two loci significantly deviated from Hardy–Weinberg equilibrium.     

Larval distribution, abundance, and stock structure of British Columbia herring

Pacific herring Clupea pallasi spawn in shallow and intertidal areas. Larval distributions and abundance of three major and several minor stocks were examined to determine if larvae mix among different spawning locations. The surveys were short, intensive, and occurred mainly within the first 30 days of larval life. Each major stock had a discrete larval distribution with continuous larval distributions within stock boundaries. Some overlap of distributions occurred among smaller stocks. Most larvae were found in inshore waters but there were no obvious oceanographic factors, such as fronts or eddies, to explain all the distributions. Estuarine circulation in inlets could promote larval retention in some areas. The results support the present geographic definitions for local herring stocks. The results are generally consistent with the concept of discrete larval distribution, including retention areas, as the basis for herring Stock Structure.     

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.     

Duration of synchronous cleavage cycles and rate of development at different temperatures in the Baltic herring

The duration of one synchronous cleavage cycle (τ₀) in Clupea harengus membras at different temperatures ( T ) was given by: (logτ₀)= 2.4349–0–0684T for T= 0.9–13°C, and (logτ₀)= 1.61010–oooit for t= 13–18–7°C.     

Modelling changes in migration pattern of herring: collective behaviour and numerical domination

According to the adopted-migrant hypothesis, first time spawning herring Clupea harengus learn their migration pattern from schooling with older individuals. Changes in migration pattern of Norwegian spring-spawning herring co-occur with the recruitment of abundant year classes to the spawning stock. It is argued that this is due to the abundant year classes being unable to learn from the older ones since most of the recruiting year class only experience their own naïve class-mates. An individual-based school simulation study is presented to explore the hypothesis. Behaviour is simulated using individual rules that take into account the movements of nearby individuals. After establishing a schooling pattern, a small proportion of the individuals is directed to move towards a given position while the remaining individuals keep using their behaviour rules. When <4% of the individuals are so directed there is no response seen in the remaining school. But when ≥7% of the total school is directed to a specific location, the remaining individuals always respond and follow the directed individuals. The simulations thus show that determined individuals can have a substantial influence on the collective behaviour of schools. Furthermore, the knife-edge response in school behaviour suggests that the relative abundance of determined individuals in a school plays an important part in the collective behaviour. This mechanism can explain the observed changes in migration pattern of Norwegian spring-spawning herring associated with the recruitment of abundant year classes to the adult Stock.     

Estimation of digestion rates for herring Clupea harengus L. feeding on fish larvae

Two methods for estimating digestion rate were evaluated and the digestion rate to disappearance was estimated to be 0·30 h⁻¹ for herring Clupea harengus feeding on capelin Mallotus villosus larvae. Due to high individual variability in feeding rates in schooling fish species, groups should be fed in separate tanks and stomach contents collected from each group at a predetermined time.     

Variation in body condition, fat content and growth rate of Icelandic summer-spawning herring Clupea harengus L.

Interannual variation in Fulton's condition factor ( K ), total body-fat content and growth rate were investigated for the Icelandic summer-spawning herring Clupea harengus over the period from 1963 to 1999. The results show a close relationship between K and the body-fat content in the autumn, both of which correlated to the growth rate in the same calendar year. A relationship was also found between K during the prespawning season (February to June) and K in the autumn (September to December) in the same year. The different measures of body condition were not found to be related to sea temperature or zooplankton indices, while the spawning stock biomass had negative effects on the fish condition. The results imply that the body condition in the autumn is representative of the feeding success over the whole foregoing year and is therefore related to the growth rate that year. The growth rate appears to be relatively uniform throughout the year.     

Mechanical understanding of hunting waves generated by killer whales

The wave wash hunting employed by Orcinus orca, also known as killer whales, is unique in that the prey is hunted outside of the water by generating waves. To quantitatively analyze the specific mechanism of the wave wash, data were obtained using computational fluid dynamics (CFD), and wave theory was introduced as the theoretical background to clarify the mechanism. The relationships between the swimming characteristics and wave parameters are defined in this paper. The results obtained by numerical investigation revealed that the wavelength increased with the swimming speed. Additionally, the wave height increased as the swimming speed increased and the swimming depth became shallower, and subsequently converged to a maximum of 2.42 m. The success of hunting is determined by two wave parameters, which indicate the intensity of the wave wash: the wave height and force exerted on the prey. The metabolic rate and the drag force are considered to evaluate the efficiency of the locomotion, which varied according to the swimming speed (V) and swimming depth (d) of the whales. To generate hunting waves efficiently, the optimal ranges of V and d were estimated to be 3 ~ 5 m/s and 0.5 m ~ 1.1 m respectively.     

Thiaminase activity of gastrointestinal contents of salmon and herring from the Baltic Sea

Potential thiaminase activity of Baltic herring Clupea harengus ranged from 0 to c. 55 nmol g-1 min-1 while potential thiaminase activity in Baltic salmon Salmo salar gastrointestinal (GI) contents ranged from 7 to c. 60 nmol g-1 min-1. About 30% of the Baltic herring analysed had a potential thiaminase activity equivalent to Baltic salmon GI contents. The results are consistent with the hypothesis that thiaminase in the forage fish of Baltic salmon may be an important link in the aetiology of the thiamine deficiency syndrome, M74, in Baltic salmon and indicate that Baltic salmon might feed selectively on Baltic herring with high thiaminase activity.     

Differences in temperature conditions and somatic growth rate of larval and early juvenile spring-spawned herring from the Vistula Lagoon, Baltic Sea manifested in the otolith to fish size relationship

Larval and juvenile herring Clupea harengus collected in the Polish part of the Vistula Lagoon in May-July 1997 had hatched between 17 April and 9 June and originated from three cohorts. The spawning season began on 1 March at 3·8° C and was completed on 3 June at 12·7° C. Mortality among larvae was high in the first 2 weeks of April, probably associated with significant temperature decrease at the beginning of the spawning season. The growth of 10–48 mm L _S herring was linear, highest for larvae and juveniles from the first cohort (0·58 mm mm^-1 day^-1), slower for the second cohort (0·55 mm mm^-1 day^-1) and the slowest for the third cohort (0·45 mm mm day^-1). Temperature effects on the growth were inconclusive and potentially unfavourable feeding conditions in June might have been responsible for the relatively slow growth of third cohort larvae and juveniles.
Relationships between otolith size (perimeter, length, width, area, and weight) and fish size ( L _S) differed among the three cohorts, related mostly to the positive temperature effect on otolith growth, individuals growing in warmer water had larger otoliths. Although a negative growth rate effect was observed as well, it was less significant.     

Environmental correlates of population differentiation in Atlantic herring

The marine environment is characterized by few physical barriers, and pelagic fishes commonly show high migratory potential and low, albeit in some cases statistically significant, levels of genetic divergence in neutral genetic marker analyses. However, it is not clear whether low levels of differentiation reflect spatially separated populations experiencing gene flow or shallow population histories coupled with limited random genetic drift in large, demographically isolated populations undergoing independent evolutionary processes. Using information for nine microsatellite loci in a total of 1951 fish, we analyzed genetic differentiation among Atlantic herring from eleven spawning locations distributed along a longitudinal gradient from the North Sea to the Western Baltic. Overall genetic differentiation was low (theta = 0.008) but statistically significant. The area is characterized by a dramatic shift in hydrography from the highly saline and temperature stable North Sea to the brackish Baltic Sea, where temperatures show high annual variation. We used two different methods, a novel computational geometric approach and partial Mantel correlation analysis coupled with detailed environmental information from spawning locations to show that patterns of reproductive isolation covaried with salinity differences among spawning locations, independent of their geographical distance. We show that reproductive isolation can be maintained in marine fish populations exhibiting substantial mixing during larval and adult life stages. Analyses incorporating genetic, spatial, and environmental parameters indicated that isolating mechanisms are associated with the specific salinity conditions on spawning locations.     

Influence of temperature on evasive responses of Atlantic herring larvae attacked by yearling herring, Clupea harengus L.

Predation encounters were staged in the laboratory between yearling herring, Clupea harengus L., 66 to 104 mm t.l. , and herring larvae, 8 to 30 mm t.l. ., at 8,11 and 14 o C. Video records were used to quantify prey behaviour. Prey responsiveness, reactive distance, response latency, and apparent looming threshold were not affected by temperature. Response speeds increased with temperature. Predator error rate and capture success showed no consistent thermal effects. Although the experiments could not fully evaluate the influence of temperature on the predators, results suggest that the predator's performance largely governs the outcome of an attack on a larva and that higher temperatures favour the predator by increasing the frequency of its encounter with prey.     

A deep dive into fat: Investigating blubber lipidomic fingerprint of killer whales and humpback whales in northern Norway

In cetaceans, blubber is the primary and largest lipid body reservoir. Our current understanding about lipid stores and uses in cetaceans is still limited, and most studies only focused on a single narrow snapshot of the lipidome. We documented an extended lipidomic fingerprint in two cetacean species present in northern Norway during wintertime. We were able to detect 817 molecular lipid species in blubber of killer whales (Orcinus orca) and humpback whales (Megaptera novaeangliae). The profiles were largely dominated by triradylglycerols in both species and, to a lesser extent, by other constituents including glycerophosphocholines, phosphosphingolipids, glycerophosphoethanolamines, and diradylglycerols. Through a unique combination of traditional statistical approaches, together with a novel bioinformatic tool (LION/web), we showed contrasting fingerprint composition between species. The higher content of triradylglycerols in humpback whales is necessary to fuel their upcoming half a year fasting and energy‐demanding migration between feeding and breeding grounds. In adipocytes, we assume that the intense feeding rate of humpback whales prior to migration translates into an important accumulation of triacylglycerol content in lipid droplets. Upstream, the endoplasmic reticulum is operating at full capacity to supply acute lipid storage, consistent with the reported enrichment of glycerophosphocholines in humpback whales, major components of the endoplasmic reticulum. There was also an enrichment of membrane components, which translates into higher sphingolipid content in the lipidome of killer whales, potentially as a structural adaptation for their higher hydrodynamic performance. Finally, the presence of both lipid‐enriched and lipid‐depleted individuals within the killer whale population in Norway suggests dietary specialization, consistent with significant differences in δ¹⁵N and δ¹³C isotopic ratios in skin between the two groups, with higher values and a wider niche for the lipid‐enriched individuals. Results suggest the lipid‐depleted killer whales were herring specialists, while the lipid‐enriched individuals might feed on both herrings and seals.     

Susceptibility of Atlantic herring and plaice larvae to predation by juvenile cod and herring at two constant temperatures

Predation encounters were staged in the laboratory to compare prey responsiveness, predator error rate, and predator capture success for juvenile cod Gadus morhua (a suction feeder) and herring Clupea harengus (a biting predator) preying on herring and plaice Pleuronectes platessa larvae. Trials were conducted at near natural temperature extremes for the larvae (8 and 13°C) to assess the importance of water temperature to the interaction. Herring larvae were significantly more responsive to attacks by herring than were plaice larvae (5·7 vs 0'0%). The two prey species were equally responsive to attacks by cod (2–6 vs 10%). Cod caught 91% of herring larvae attacked and juvenile herring caught 87%. Cod were successful in 96% of attacks on plaice, but juvenile herring caught significantly fewer (83%) plaice larvae. For each predator species, capture success did not vary significantly with prey species. Overall capture success for herring was significantly lower than that for cod. Responsiveness of herring larvae to attacks by juvenile herring increased with temperature, but predator error rate and capture success were not altered by water temperature.     

Vertebrate exploitation of pulsed marine prey: a review and the example of spawning herring

Short-term bursts of prey availability occur in many ecosystems and have potential important consequences for both predator biology and ecosystem function. Examples of prey ‘pulses’ in marine ecosystems include spawning runs of several anadromous and marine fishes, horseshoe crab spawning, and salmonid juvenile outmigrations, which are exploited by numerous species of vertebrate predators. In a few cases, the fitness or demographic consequences of such predator–prey interactions are known or inferred, but too often that information remains unknown. We explored the extent of temporal and spatial variation in one example of a pulsed marine resource: the spawning of Pacific herring (Clupea pallasii). Spawning herring provide a rich, aggregated resource to which dozens of species of vertebrate predators often exhibit strong numerical responses. However, the spawning events are often variable in both time (annual differences of several to many weeks) and space (both regional and more local differences in size and timing of events). Such variability must affect more mobile predators less than area-restricted predators, and thus its effect would vary not only among species but also within species, depending on constraints of the predator life history. Unpredictability of the prey concentrations, whatever their proximate causes, may contribute to maintenance of metapopulations of prey such as herring, if unpredictability lessens the impact of predation.     

Feeding, Ichthyophonus sp. infection, distribution and growth history of Norwegian spring-spawning herring in summer

After its collapse in the late 1960s, 1991 was the first year of systematic herring investigations after the Norwegian Sea stock returned to the traditional summer-feeding areas. Of 11 prey groups three dominated the diet; Calanus finmarchicus, Parathemisto spp. and Sebastes spp. There was a high prevalence of Ichthyophonus sp. at stations in the central and western parts of the Norwegian Sea where the cpue was low. This suggests that infected individuals were unable to return from the feeding to the wintering area of the Norwegian fjords. Highest cpue were recorded between 68–73° N and 5–15° E. Age groups 2, 3 and 8 were most frequently caught and age group 8 (the 1983 year class) dominated the samples. Herring occurred in dense concentrations where C. finmarchicus dominated diet. 0-group fish dominated diet at stations along the coast from 66–73° N and out to c . 300 km off the coast. Mature herring overlapped in distribution with 0-group fish and Sebastes spp. contributed largely to herring diet in this area. The first rich year-class after the collapse, the 1983 year class, had a faster growth than rich year classes from past herring periods, but slower than poor ones.     

The effects of thin layers on the vertical distribution of larval Pacific herring, Clupea pallasi

Temporal and spatial heterogeneity of resources is likely to have dramatic effects on the behaviors of zooplankton and ichthyoplankton, which in turn are likely to have strong effects on ecological dynamics such as predation, growth, and mating. The objective of this study was to determine whether vertically thin layers of extreme prey concentration affect the vertical distribution of larval Pacific herring (Clupea pallasi). We employed 2-m tall experimental tanks equipped with video cameras that scanned the vertical extent of the tanks to investigate the effects of thin layers on the vertical distribution of 5- and 10-day-old herring larvae. Three treatments were established: (1) a thin layer of prey (rotifers, Brachionus plicatilis) through density (salinity) stratification, (2) homogeneous vertical distribution of both prey and density, and (3) density (salinity) stratification, but with a homogeneous distribution of prey. We found that in all treatments the majority of larval herring were at the surface, near the light, despite the absence of a peak in rotifer abundance at this depth in some instances. However, there were also clear effects of the thin layers—secondary subsurface peaks in herring abundance occurred at the mid-depths in the stratified tanks, in and around the thin layers. In addition, our results provide some evidence that thin layers specifically, rather than prey patches generally, influence the vertical distribution of larval herring, i.e., larvae may use the physical properties of thin layers to locate and distribute themselves, instead of reacting solely to the prey patches. Thus thin layers can affect directly the vertical distribution of larval herring, and perhaps indirectly their horizontal distribution, as herring larvae live in environments (e.g., estuaries) where advective transport is also often vertically heterogeneous.