Behavioural differences in starving herring Clupea harengus L. larvae correlate with body levels of essential fatty acids

Twenty days after hatching, a single stock of Atlantic herring ( Clupea harengus L.) larvae, cultured in the presence of rotifers and Artemia nauplii but showing little or no active feeding behaviour, displayed clear signs of starvation. Three groups of fish were distinguished: group I was generally pinhead-shaped, tended to swim with a spinning motion and floated vertically; group 2 lay moribund on the bottom of the tank; group 3 showed normal, active swimming behaviour. Fatty acids of total lipid extracted from groups 1 and 2 differed from group 3 in having markedly reduced percentages of 20:5n-3, 22:6n-3, 20:1 and 22:1. We conclude that individuals within a single stock of cultured herring larvae respond differently to starvation and that this generates well defined behavioural differences which correlate with levels of n-3 polyunsaturated fatty acids (PUFA) in body lipid. The implications of these observations are discussed.     

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.     

Glycoconjugates in the otolithic membrane of herring larvae: a possible framework for encoding the life history recorder in fishes

Glycoconjugates in the inner ear of herring Clupea harengus larvae, investigated by laser confocal and electron microscopy, were located mainly in the gelatinous layer of the otolithic membranes, forming a collar around the proximal surfaces of the otoliths. The site of secretion was located on the surface of the sensory macula, from which a colonnade of glycoconjugate streamers projected through the subcupular region to connect with the gelatinous layer of each otolith. An electron dense component of the outer gelatinous layers, shown by TEM to be closely associated with the sensory kinocilia, suggested that they provided a basis for the streamers and offered a potential role in directing the path of secretion. It is hypothesized that this highly structured glycoconjugate framework could provide a mechanism for localizing and containing ionic and protein gradients previously detected in this vicinity and which are considered to have a key role in driving the differential growth and mineralization of the otoliths.     

Effects of two Avtemia diets with different contents of polyunsaturated fatty acids on the lipid composition of larvae of Atlantic herring (Clupea harengus

Atlantic herring larvae ( Clupea harengus ) were fed two enriched Artemia diets with different contents of (n-3) highly unsaturated fatty acids (HUFA), one containing low levels of 20: 5(n-3) and no 22: 6(n-3), the other containing substantial levels of both 20: 5(n-3) and 22: 6(n-3). After 30 days of culture, fatty acid compositions of lipid classes in the heads, bodies and eyes of the larvae were analysed. Fish fed Artemia with the low (n-3) HUFA diet lacking 22: 6(n-3) had lower amounts of total (n-3)HUFA and, in particular, of 22:6(n-3) in individual phospholipids and total neutral lipids of heads, bodies and eyes as compared to fish fed Artemia with high levels of (n-3)HUFA. The amount of 22: 6(n-3) in the fatty acids of phosphatidyl-ethanolamine of eyes was particularly susceptible to dietary depletion. The implications of these findings are discussed, particularly in relation to dietary requirements for 22: 6(n-3) during development of neural tissue in predatory fish iarvae.     

State-dependent spawning migration in Norwegian spring-spawning herring

Norwegian spring-spawning herring Clupea harengus winter in fjords of northern Norway, whereas the subsequent spawning occurs at various locations along the coast with a main bulk off the south-western coast. The distance of the southward spawning migration tends to increase with the length and condition of the fish. The costs and benefits of the southward migration were modelled in terms of fitness (number of surviving offspring). The model assumes that larvae have increasing growth and survival rates further south as they pass through warmer water during the northward drift in the coastal current. In agreement with the observed spawning distribution, optimal spawning grounds were predicted off the southwestern coast and farther south with increasing fish length and condition. The present study suggests that homing is not a successful strategy for these herring, and instead the selection of spawning grounds depends on individual internal state (length, condition), the cost of migration and the probability of larval survival.     

Vulnerability of late larval and early juvenile Atlantic herring, Clupea harengus, to predation by whiting,Merlangius merlangus

Laboratory experiments investigated changes in the vulnerability of herring to predation by whiting during growth from <34 to >80mm in length, Premetamorphic herring (<50mm) failed to react to c . 50% of attacks by the predator, but this was reduced to c . 20% in postmetamorphic fish. Premetamorphic herring failing to react had c. 30% probability of survival due to unforced errors by the predator (unsuccessful attacks that did not elicit a reaction by the prey), but these errors did not occur after herring metamorphosis. The loss of the advantage of lower conspicuousness following metamorphosis was counterbalanced by increased reactivity. Antipredator benefits should increase with schooling behaviour (first evident in experiments at c . 50 mm), so predation mortality should decrease in postmetamorphic herring in the sea. Metamorphosis itself would be associated with high predation risk since conspicuousness is enhanced but reactivity and schooling behaviour are still not fully developed.     

Is the marginal otolith increment width a reliable recent growth index for larval and juvenile herring?

Marginal otolith increment width analysis was performed on field‐collected larval and juvenile spring‐spawned herring Clupea harengus that experienced variable feeding conditions and high temperatures that were above the optimum for growth. Although drastic zooplankton biomass reduction had a significant effect on increment width, a delay of a few days in the otolith response was observed. More importantly, a very clear, positive temperature effect on marginal increment width was demonstrated in fish characterized by temperature independent somatic growth. These results indicate that under natural conditions it may be impossible to distinguish increment width changes related to variation in feeding conditions from changes caused by temperature fluctuations. Therefore, it was concluded that marginal otolith increment width analysis could not be used as a recent growth index ( I _G) for herring larvae and juveniles exposed to drastic temperature fluctuations. The implication of these results is significant not only for the use of marginal increments as a recent growth index, but also if growth rate backcalculation is to be used as a research method.     

Effects of alternative prey on predation intensity from herring Clupea harengus and sandeel Ammodytes marinus on capelin Mallotus villosus larvae in the Barents Sea

Stomach contents from lesser sandeel Ammodytes marinus and herring Clupea harengus caught at one and three stations, respectively, were analysed to investigate predation intensity on capelin Mallotus villosus larvae. Most capelin larvae were found in the anterior sections of the stomachs close to the oesophagus, indicating that rapid digestion rates of larvae reduced the abundance in the posterior sections. The anterior sections of the stomachs had alternating layers of either copepods or capelin larvae and krill. This shows that the individual predators switched between feeding on either copepods or on krill and capelin larvae. A total of 549 capelin larvae was found in 440 fish stomachs. Capelin larvae were found in 20% of the sandeel stomachs, and 24, 34 and 62% of the stomachs from the three herring stations, respectively. Many of the predator stomachs contained more than five larvae, and up to 28 larvae were found in one herring stomach. The herring appeared to prey selectively on the largest capelin larvae, and the number of larvae per stomach was much higher in stomachs where krill had recently been eaten than where copepods were dominant. The predation intensity measured in this study is much higher than reported in earlier studies, and it is suggested that the predators were feeding using a searching image, and that the concentrations of alternative prey (copepods and krill) varied around a switching threshold.     

A study of the assimilation of fluorescent pigments of microalgae Isochrysis galbana by the early larval stages of turbot and herring

The appearance of large supranuclear vacuoles in the enterocytes of 1- and 4-days post-hatch larvae of turbot and herring, respectively, revealed by the pinocytotic uptake of a fluorescent marker (FITCdextran), indicates a potential for the absorption of dissolved nutrients by the endotrophic stages of marine fish larvae. Ingestion of algal cells by turbot larvae was observed soon after hatching, but low level pinocytotic absorption of algal material was first seen during the second day. More extensive lysis of algal cells and pinocytotic absorption occurred 24 h later. Although lysis of I. galbana was shown to occur at low external osmolarities, it is unlikely that sufficiently low osmolarities present in the hind gut of turbot larvae explained the observed rupture of algae. Other mechanisms for digestion are discussed. In newly hatched herring larvae, algal cells were unable to pass beyond the constriction in the mid-gut caused by the yolk sac. When algal cells were eventually seen to pass into the hind gut, there was no evidence of algal digestion or absorption throughout the remaining endotrophic and early exotrophic stages of herring larvae, although pinocytosis was observed to occur mid-way through the endotrophic stage.     

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.     

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.     

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.     

Development stage distribution as a proxy for feeding success and growth for first feeding Norwegian spring spawning herring larvae

The estimation of growth rates in young herring larvae (Clupea harengus) in the field can be difficult because the primary increments in the otoliths may not be discernible or formed at a daily level. Likewise, the estimation of mortality rates of fish larvae in the field is very difficult to achieve, especially in a rigorous quantitative manner. In this study, the authors suggest the use of a stage-based proxy of feeding success, growth and potential survival or mortality risk of field-caught larvae. The stage-based proxy is derived based on observations from previous laboratory studies where larvae successfully completing start-feeding on external food sources will advance through the early development stages, whereas those that do not (unsuccessful larvae) remain and accumulate in the development stage preceding first feeding. The relative occurrence of larvae in the early development stages is therefore expected to reflect feeding conditions of the larvae, with higher ratios of unsuccessful larvae indicative of poor feeding success and higher mortality risk. Using field data on Norwegian spring spawning herring, the authors document that the relative occurrence of larvae in the late non-feeding stage is significantly higher at lower average zooplankton concentrations, in line with the predictions of the authors that this novel approach of using a stage-based proxy could be a useful indication of feeding success, growth and mortality in the field. Further, there was a significant interaction effect with ambient temperature, with the ratio being higher at low zooplankton concentrations at higher temperatures. This study also suggests that these findings are not population specific as the same accumulation of non-feeding larvae in the late non-feeding stage was observed in laboratory-reared larvae of both autumn and spring spawning herring populations.     

Morphometric variations among larval Anisakis simplex (Nematoda: Ascaridoidea) from fishes of the North Atlantic and their use as biological indicators of host stocks

Synopsis Analysis of variance on mean dimensions of samples of larval Anisakis simplex from Atlantic salmon (Salmo salar) and Atlantic herring (Clupea harengus harengus) indicated that highly significant morphometric differences existed. Subsequent analyses were simplified by using only the total body length of the larvae which was easily measured. Also the multiple range tests indicated that length showed the highest degree of heterogeneity. No difference (P > 0.2) was detected in the lengths of larvae from male and female salmon and most analyses suggested there was no change in length of the larvae with an increase in age of the host. There was, however, significant heterogeneity in the length of larvae in salmon which had spent more than one winter at sea and this heterogeneity was related in some way to the geographic localities in which the samples were taken. Possible reasons for these differences and the use of morphometric variants of Anisakis as a biological indicator are discussed.     

Herring as cannibals

Egg cannibalism near the sea bottom was observed in herring Clupea harengus at the end of the spawning season. About 10% of the individuals had consumed eggs and egg feeders were predominantly spent males.     

Interannual and regional variations in body length, weight and energy content of age-0 Pacific herring from Prince William Sound, Alaska

Age-0 Pacific herring were surveyed in October of 4 years in a large northern Gulf of Alaska estuary, to determine the range of variations in length, weight and whole body energy content (WBEC). These parameters reflect their preparedness for surviving their first winter's fast. During the surveys there were distinct regional and interannual variations in all three parameters for individual groups of herring in Prince William Sound. Likewise, with each collection there was typically a large range of size and WBEC values. The average standard length was (±S.D.) 80±13 mm (range=40–118), the mean whole body wet weight was 5·7±3·0 g (range=0·7–29·2) and the average WBEC of all age-0 herring captured, regardless of year or site (n=1471), was 5·4± 1·0 kJ g⁻¹ wet weight (range=2·4–9·4). The large range of WBEC and size indicates that age-0 herring at different capture sites were not all equally prepared for surviving their first winter.     

Population structure of Atlantic herring, Clupea harengus L.

During the last decade, genetic studies have been carried out on samples of Atlantic herring, CIupea harengus L., from the Baltic, North Sea, British Isles, Norwegian sea-waters and in the western part of the North Atlantic Ocean. Based on direct comparisons of samples drawn from several areas, the available information on allozyme variation was compiled into a comparable data set and analysed for population structure and genetic distance. The results are discussed in relation to the present stock model for herring.     

Characterization of 14 tetranucleotide microsatellite loci derived from Pacific herring

Spawning aggregations of Pacific herring (Clupea pallasi) often exhibit significant interannual variation in allele frequencies of neutral gene markers. We isolated 14 tetranucleotide microsatellites to examine hypothetical processes that may produce this unique genetic signal. We developed and tested primer pairs for each locus and then estimated locus variability in samples (n = 60) from two populations. The number of alleles per locus ranged from five to 49. The expected heterozygosity across loci and populations ranged from 0.20 to 0.96. These microsatellites will be useful for estimating genetic variation in herring on a fine geographical scale.