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.     

Spatial and temporal variations in parasite prevalence and infracommunity structure in herring (Clupea harengus L.) caught to the west of the British Isles and in the North and Baltic Seas: implications for fisheries science

Herring Clupea harengus L. viscera were examined for endoparasitic infections as part of a multidisciplinary stock identification project (WESTHER, EU Contract no. Q5RS-2002-01 056) which applied a range of stock discrimination techniques to the same individual fishes to obtain comparable results for multivariate analysis. Spawning and non-spawning adults, and juvenile herring were caught, over 3 years, by commercial and research vessels from numerous locations to the west of the UK and Ireland, along with control samples of spawning fish from the eastern Baltic Sea, and juveniles from sites in the eastern and western North Sea, and the north of Norway. The metacercariae of two renicolid digeneans (Cercaria pythionike and Cercaria doricha), one larval nematode (Anisakis simplex s.s.) and one larval cestode (Lacistorhynchus tenuis) were selected as tag species. Results were compared with those from herring collected between 1973 and 1982, which suggested remarkable stability in the parasite fauna of herring in the study area. These species were used to compare the parasite infracommunities of spawning herring. A significant variation in infracommunity structure was observed between different spawning grounds. These results suggest that the parasite fauna of herring are spatially variable but remain temporally stable in both the short and long term. Significant differences in prevalence and abundance of infections and comparisons of parasite infracommunity enabled the separation of putative herring stocks west of the British Isles. Distinctive patterns of parasite infection in two different spawning groups off the north coast of Scotland suggest that this area is occupied by two spawning populations, one recruiting from the west of Scotland, the other from outside this area, and most likely from the eastern North Sea. The distribution patterns of L. tenuis, C. doricha and C. pythionike suggest the potential for fish that spawn in three distinct International Council for the Exploration of the Seas (ICES) management units to be present in mixed aggregations found over the Malin Shelf, with significant implications for management in this area.     

Outlier Loci Detect Intraspecific Biodiversity amongst Spring and Autumn Spawning Herring across Local Scales

Herring, Clupea harengus, is one of the ecologically and commercially most important species in European northern seas, where two distinct ecotypes have been described based on spawning time; spring and autumn. To date, it is unknown if these spring and autumn spawning herring constitute genetically distinct units. We assessed levels of genetic divergence between spring and autumn spawning herring in the Baltic Sea using two types of DNA markers, microsatellites and Single Nucleotide Polymorphisms, and compared the results with data for autumn spawning North Sea herring. Temporally replicated analyses reveal clear genetic differences between ecotypes and hence support reproductive isolation. Loci showing non-neutral behaviour, so-called outlier loci, show convergence between autumn spawning herring from demographically disjoint populations, potentially reflecting selective processes associated with autumn spawning ecotypes. The abundance and exploitation of the two ecotypes have varied strongly over space and time in the Baltic Sea, where autumn spawners have faced strong depression for decades. The results therefore have practical implications by highlighting the need for specific management of these co-occurring ecotypes to meet requirements for sustainable exploitation and ensure optimal livelihood for coastal communities.     

Oxygen and salinity characteristics of predator–prey distributional overlaps shown by predatory Baltic cod during spawning

In the distributional overlap volume of Baltic cod Gadus morhua and its prey, studied in the Bornholm Basin in the southern Baltic Sea, only a fraction of the sprat Sprattus sprattus population vertically overlapped with the Baltic cod population. Sprat occurred in the intermediate water, in the halocline and in the bottom water, while herring Clupea harengus and Baltic cod occurred exclusively in the halocline and in the bottom water. Only parts of the sprat population were hence accessible for Baltic cod, and only a fraction of the sprat had access to the Baltic cod eggs below the halocline. Baltic cod–clupeid overlap volumes appeared to be determined by salinity stratification and oxygenation of the bottom water. Hydrography time series were used to estimate average habitat volumes and overlap from July to September in 1958–1999. In the 1999 survey spawning Baltic cod had greater ratios of empty stomachs and lower average rations than non-spawning Baltic cod. The average ration for Baltic cod caught within 11· 4 m from the bottom (demersal) did not differ from the average ration of Baltic cod caught in shallower waters (pelagic), because spawning and non-spawning Baltic cod in both strata were caught at equal rates. The diet of the Baltic cod caught demersally contained more benthic invertebrates, especially Saduria entomon, but Baltic cod caught pelagically also had fresh benthic food in their stomachs, indicating vertical migration of individual fish.     

Electrophoretic identification of Anisakis sp. larvae (Ascaridida: Anisakidae) from Clupea harengus L. in Baltic Sea

On the basis of electrophoretic studies carried out on 15 gene-enzyme systems, 80 Anisakis sp. larvae from the herring Clupea harengus, fished in South Baltic Sea and Gdanisk Bay, were identified as Anisakis simplex B. This is the first record of Anisakis simplex B in the Baltic Sea. The spawning migration of the herrings from the North Sea to the Baltic Sea and the distribution of A. simplex B are briefly discussed.     

On the distribution of larvae and localization of spawning stocks of White Sea herring <Emphasis Type="Italic">Clupea pallasii marisalbi</Emphasis>

On the basis of ichthyoplankton surveys made in June 2004–2005 and 2007, June–July 2010, and July 2011 in these bays and beyond them (in open waters of the White Sea Basin and adjacent areas of the Gorlo) larvae of White Sea herring were absent. Principal aggregations of larvae are found in the Kandalaksha Bay in June 2004–2005 and 2007. In the Onega Bay and in the Dvina Bay surveyed in June 2007 abundance of larvae was ratter low and in June–July 2010 and July 2011 in these bays and beyond them (in open waters of the White Sea Basin and adjacent areas of the Gorlo) larvae of White Sea herring were absent. Within the Kandalasksha Bay, from year to year, there were two disconnected aggregations of larvae. The space between them was situated in the open part of the bay along the transect of the Chupa Estuary and the Umba Estuary. One of the aggregations of larvae occupied the tail of the bay, and the second aggregation occupied the ante-mouth and mouth areas of the Chupa Estuary. It is supposed that these aggregations result from spawning of two independent spawning groups of the White Sea herring spawning in isolated regions of the Kandalaksha Bay. Presence of the bulk of larvae of the White Sea herring within the limits of the Kandakaksha Bay and their almost complete absence at the boundary of the bay with the White Sea Basin and at the boundaries between the Onega Bay and the Dvina Bay and the Basin support the hypothesis on the absence of an exchange with larvae between stocks of the White Sea herring spawning in large bays of the White Sea. The larvae are retained within shallow waters of the Kandalaksha Bay by the system of two-layer water circulation in the areas of spawning of herring in bays and gulfs of the estuarine type. Their drift outside of the Onega Bay and the Dvina Bay may be delimited by frontal divides at their boundaries with the Basin.     

Marine landscapes and population genetic structure of herring (Clupea harengus L.) in the Baltic Sea

Numerically small but statistically significant genetic differentiation has been found in many marine fish species despite very large census population sizes and absence of obvious barriers to migrating individuals. Analyses of morphological traits have previously identified local spawning groups of herring (Clupea harengus L.) in the environmentally heterogeneous Baltic Sea, whereas allozyme markers have not revealed differentiation. We analysed variation at nine microsatellite loci in 24 samples of spring-spawning herring collected at 11 spawning locations throughout the Baltic Sea. Significant temporal differentiation was observed at two locations, which we ascribe to sympatrically spawning but genetically divergent 'spawning waves'. Significant differentiation was also present on a geographical scale, though pairwise F(ST) values were generally low, not exceeding 0.027. Partial Mantel tests showed no isolation by geographical distance, but significant associations were observed between genetic differentiation and environmental parameters (salinity and surface temperature) (0.001 < P < or = 0.099), though these outcomes were driven mainly by populations in the southwestern Baltic Sea, which also exhibits the steepest environmental gradients. Application of a novel method for detecting barriers to gene flow by combining geographical coordinates and genetic differentiation allowed us to identify two zones of lowered gene flow. These zones were concordant with the separation of the Baltic Sea into major basins, with environmental gradients and with differences in migration behaviour. We suggest that similar use of landscape genetics approaches may increase the understanding of the biological significance of genetic differentiation in other marine fishes.     

Tendencies in the Herring Population Development of the Baltic Sea

During the 1960's a change in population structure of Baltic herring started which resulted in the dominance of spring spawners in the entire Baltic since the beginning 1970's. Autumn spawning herring is very rare in the yields of fisheries since. This development has been accompanied by a likely increase of the total stock biomass of herring in the area. Yields of herring fisheries increased remarkable up to 1984, partly as a result of increased fishing effort. Recent developments of stock biomasses point to dependencies on fluctuations of growth rates. Growth is influenced by several environmental factors but is very likely especially dependent on abundance of food and on temperature. Eutrophication of the Baltic Sea increased perhaps the abundance of food for the planktonfeeding herring but it may have been contributing to the depletion of autumn spawning herring via the declining oxygen content of bottom water layers during the past 20 years.     

Discontinuous distributions of the fish acanthocephalans Pomphorhynchm laevis and Acanthocephalus anguillae in Britain and Ireland: an hypothesis

The current distributions of the freshwater fish acanthocephalans Pomphorhynchus laevis and Acanthocephalus anguillae are described and shown to be discontinuous and mutually exclusive, both regionally and locally, in the British Isles. An hypothesis is erected to account for this pattern. It is suggested that as the continental freshwater cyprinids colonized post-glacial mainland Britain via the eastward-flowing rivers and the Thames-Rhine link, they brought with them both species of acanthocephalan. The present, more extensive distribution of P. laevis in the British Isles and Ireland is explained by (1) early formation of a marine strain that colonized the Baltic and North Sea and estuaries of North Sea rivers, (2) later transfers of infected barbel to other English rivers from the R. Thames by man, and (3) transfers to Ireland of infected cyprinids from England by man. Different and restricted availability of preferred definitive and intermediate hosts subsequently resulted in the formation of distinct strains in England and Ireland. The distribution of A. anguillae can be explained by similar anthropogenic influences, but since its definitive and intermediate hosts are more widely available, strain formation has not yet been detected. Competitive interactions between the two parasites in the intestine of the definitive hosts are thought to be responsible for their mutual exclusiveness.     

Larval growth and drift pattern and the separation of herring spawning groups in the North Sea*

Data from two internationally co-ordinated survey programmes are used in an attempt to display the events in the early life that took place during the ‘recovery period’ of the North Sea herring Stock, 1979–1986. During the period, an increasing importance of the spawning grounds off Buchan and off Yorkshire is evident from distributions of newly hatched herring larvae. The dramatic changes in relative importance of spawning grounds are traced in the data on both late larvae (6 months old) and juveniles (18 months old). The onset of extended spawning off Buchan and off Yorkshire was followed by increase in distinct groups of late larvae of large mean length, and by enlargement of a group of medium-sized juveniles. It is hypothesized that the identified groups are interconnected. Thus, larvae spawned off Buchan and off Yorkshire are found to have growth rates superior to those attained by larvae from west of Scotland and around the Orkney/Shetland Isles, whereas the relationship is reversed in the juveniles. In the investigated period, larval drift routes exhibited the same trends from year to year, the drift of the northerly spawned larvae being the most variable. Thus, changes in the relative contributions from spawning grounds apparently influence the overall spatial distribution as well as size composition of larval and juvenile North Sea herring. The findings indicate that groups of larvae retain, to a large extent, separate distributions until metamorphosis, and point to larval drift pattern as a determinant of spawning group distinctness.     

Differential utilization of energy during wintering and spawning migration in Norwegian spring-spawning herring

The energy utilization in non-feeding Norwegian spring-spawning herring Clupea harengus was examined during periods of wintering in a fjord system in northern Norway and southward spawning migration (800 km distance) to the main spawning area off western Norway. At the onset of wintering the gonadosomatic index (IG) was higher and the amount of mesenteric fat was lower in male than in female herring, whereas the subsequent increase in IG and decrease in mesenteric fat occurred at a higher rate in females than in males. However, no differences were recorded between sexes in fat content (%) of whole fish at any time of the year. The absolute energy loss increased, whereas the relative energy loss decreased, with fish length. Furthermore, the absolute and relative length specific energy losses were two to three and three to four times higher, respectively, during spawning migration than during wintering. The distinct energy loss was attributed mainly to fat metabolism, whereas the storage protein only was transferred from the soma to the gonads and remained relatively constant in whole herring throughout the wintering and spawning migration. © 1999 The Fisheries Society of the British Isles     

Discrimination of Baltic herring populations with respect to Anisakis simplex larvae infection

Samples of herring Clupea harengus in the Baltic were collected during the spawning season in western, middle and eastern waters off the Polish coast. Two samples were taken per area, several morphometric characters were measured and some meristic characters (vertebrae and gill rakers) were counted. Infection with Anisakis simplex larvae, total length, age and maturity stage were recorded. Univariate and multivariate statistical tests were used to compare the samples, discriminant analysis was applied to separate herring populations and the fraction of herring populations in each area was estimated. The results obtained indicated that infected fish represented a mixed group of western and central Baltic herring. In the first samples collected from each area, the share of the western population decreased from 40% in the western to 18% in the middle and 13% in the eastern coasts. The share of western herring was higher in the second samples collected in the same area and decreased from 91% in the western coast to 14 and 32% in the middle and eastern ones, respectively.     

Temperature-driven changes in early life-history stages influence the Gulf of Riga spring spawning herring (<Emphasis Type="Italic">Clupea harengus m</Emphasis>.) recruitment abundance

Processes occurring during early life-history stages influence the year-class abundance of marine fish. We found that the abundance of 1-year-old spring spawning herring is statistically significantly determined by the number of post-flexion herring larvae in the Gulf of Riga (Baltic Sea). The abundance of consecutive developmental stages of larvae: yolk-sac, pre-flexion, flexion and post-flexion strongly correlated with each other, indicating that factors which already influence the yolk-sac stage are important in determining the abundance of post-flexion herring larvae. Winter air temperature before spawning determined the timing of maximum abundance of pre-flexion herring larvae, but not their main prey: copepod nauplii, implying that different mechanisms governing major preconditions for the formation of year-class strength. The abundance of post-flexion larvae displayed a potential dome-shaped relationship with sea surface temperature experienced after hatching. We suggest that increased summer temperatures, which exceed the physiological optimum negatively, affect the survival of post-flexion herring larvae. Overall, future climate warming poses an additional risk to larval herring survival and this may lead to a reduction in those herring stock which rely on recruitment from shallow coastal areas.     

Phylogeographical structure, distribution and genetic variation of the green algae Ulva intestinalis and U. compressa (Chlorophyta) in the Baltic Sea area

The marine algae Ulva intestinalis and U. compressa are morphologically plastic with many overlapping characters and are therefore difficult to distinguish from each other. The present distribution of U. intestinalis and U. compressa is investigated along the salinity gradient in the Baltic Sea area through analyses of internal transcribed spacer (ITS) sequence data. Also, the amount and distribution of intraspecific genetic polymorphism in the ITS region is studied allowing inferences on the phylogeographical pattern and postglacial recolonization of the Baltic Sea area. The data show that of the two species only U. intestinalis occurs in the Baltic Sea. The distribution of U. compressa is more restricted than previously reported, and it was not found in salinities lower than 15 ppt. All of Scandinavia and the Baltic Sea were covered with ice during the last ice age and the organisms in the Baltic Sea must have colonized the area after the ice had started to melt. The genetic diversity of U. intestinalis and U. compressa in the Baltic Sea and the neighbouring area was found to be reduced compared to that in the British Isles. This reduction may be the result of either a historical reduction of diversity or an adaptation of specific clones to the northern environmental conditions.     

Temporal stability of the population genetic structure of the White Sea herring <Emphasis Type="Italic">Сlupea pallasii marisalbi</Emphasis>

The length–age distributions and genetic variation of ten microsatellite loci were examined in samples of herring from the Chupa Inlet of the Kandalaksha Gulf of the White Sea. The samples were collected on the same spawning grounds over a period of 13 years and during the same spawning season. The obtained data demonstrate stability of the length structure and genetic characteristics (allele and genotype frequencies, allelic richness, and heterozygosity). The degree of temporal genetic differentiation was not statistically significant, θ = 0.0038 (CI,–0.0006 to 0.006). Spatial differentiation of the White Sea herring far outweighs the level of temporal variability, which makes it possible to suggest the important role of reproductive isolation in the formation of the population genetic structure of herring.     

Characterization of a major histocompatibility class II A gene (Clha-DAA) with an embedded microsatellite marker in Atlantic herring (Clupea harengus L.)

An Atlantic herring major histocompatibility class II A ( Clha-DAA ) cDNA sequence has been characterized and was shown to encode a leader peptide, alpha-1 domain, alpha-2 domain, connecting peptide, transmembrane and cytoplasmic region. The Clha-DAA protein sequence has all the characteristics of a teleost class II A protein with conserved cysteines in both the alpha-1 and the alpha-2 domains and two potential N-linked glycosylation sites. Exon 2 sequences encoding the polymorphic alpha-1 domain from different individuals were analysed and revealed the presence of at least two loci. The Clha-DAA gene consists of four exons and three short introns. Four unique intron 3 sequences from multiple individuals were obtained and were shown to contain a (TG)_n microsatellite sequence. Primers were optimized such that only a single microsatellite locus designated Clha-DAA-INTR3 was amplified. Four herring populations from the North Sea and the Baltic Sea were genotyped for Clha-DAA-INTR3 . In total, 16 Clha-DAA-INTR3 alleles were detected; the distribution of the alleles showed no deviation from Hardy–Weinberg expectation. Levels of genetic differentiation among samples were of similar magnitude as have been reported earlier for neutral microsatellite loci between northern North Sea and Baltic Sea herring populations.     

Seasonal maturity development of Baltic cod in different spawning areas: importance of the Arkona Sea for the summer spawning stock

We investigated the seasonal maturity development of cod in four areas of the Baltic Sea. Two different spawning peaks were identified and found to be consistent over the period 1992–2005. In the Kiel Bight and Mecklenburg Bight (ICES SD 22) a spawning peak was observed from March to April (spring spawning). In the areas of the Arkona Sea (ICES SD 24) and Bornholm Sea (ICES SD 25) the spawning peak occurred during summer. In the Bornholm Sea, the main spawning activities began in June and ended in September, with a spawning peak in June–August (summer spawning). In the Arkona Sea, which is a transition area between the Mecklenburg Bight and the central Baltic Sea, spawning began in March and lasted until July, with a spawning peak in June–July (summer spawning). Seasonal maturity development and proportions of spawning cod in June in the Arkona Sea were similar to that of the Bornholm Sea. In addition, the proportion of spawning cod in the Arkona Sea was positively correlated with the size of the spawning stock in the Bornholm Sea. Our results provide evidence of a spatial expansion of spawning activities of the summer spawning stock from the eastern Baltic Sea into the Arkona Sea. Therefore, the Arkona Sea should be considered as one of the spawning habitats of the summer spawning stock of Baltic cod.     

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.     

Genetic biodiversity in the Baltic Sea: species-specific patterns challenge management

Information on spatial and temporal patterns of genetic diversity is a prerequisite to understanding the demography of populations, and is fundamental to successful management and conservation of species. In the sea, it has been observed that oceanographic and other physical forces can constitute barriers to gene flow that may result in similar population genetic structures in different species. Such similarities among species would greatly simplify management of genetic biodiversity. Here, we tested for shared genetic patterns in a complex marine area, the Baltic Sea. We assessed spatial patterns of intraspecific genetic diversity and differentiation in seven ecologically important species of the Baltic ecosystem—Atlantic herring (Clupea harengus), northern pike (Esox lucius), European whitefish (Coregonus lavaretus), three-spined stickleback (Gasterosteus aculeatus), nine-spined stickleback (Pungitius pungitius), blue mussel (Mytilus spp.), and bladderwrack (Fucus vesiculosus). We used nuclear genetic data of putatively neutral microsatellite and SNP loci from samples collected from seven regions throughout the Baltic Sea, and reference samples from North Atlantic areas. Overall, patterns of genetic diversity and differentiation among sampling regions were unique for each species, although all six species with Atlantic samples indicated strong resistence to Atlantic-Baltic gene-flow. Major genetic barriers were not shared among species within the Baltic Sea; most species show genetic heterogeneity, but significant isolation by distance was only detected in pike and whitefish. These species-specific patterns of genetic structure preclude generalizations and emphasize the need to undertake genetic surveys for species separately, and to design management plans taking into consideration the specific structures of each species.