Oogenesis and reproductive investment of Atlantic herring are functions of not only present but long-ago environmental influences as well.

Following general life history theory, immediate reproductive investment (egg mass × fecundity/body mass) in oviparous teleosts is a consequence of both present and past environmental influences. This clarification questions the frequent use of season-independent (general) fecundity formulas in marine fish recruitment studies based on body metrics only. Here we test the underlying assumption of no lag effect on gametogenesis in the planktivorous, determinate-fecundity Atlantic herring (Clupea harengus) displaying large plasticity in egg mass and fecundity, examining Norwegian summer-autumn spawning herring (NASH), North Sea autumn-spawning herring (NSAH), and Norwegian spring-spawning herring (NSSH). No prior reproductive information existed for NASH. Compared with the 1960s, recent reproductive investment had dropped markedly, especially for NSAH, likely reflecting long-term changes in zooplankton biography and productivity. As egg mass was characteristically small for autumn spawners, although large for spring spawners (cf. different larval feeding conditions), fecundity was the most dynamic factor within reproductive investment. For the data-rich NSSH, we showed evidence that transient, major declines in zooplankton abundance resulted in low fecundity over several subsequent seasons, even if Fulton's condition factor (K) turned high. Temporal trends in Kslope (K on total length) were, however, informative. These results clarify that fecundity is defined by (i) dynamics of primary (standing stock) oocytes and (ii) down-regulation of secondary oocytes, both processes intimately linked to environmental conditions but operating at different timescales. Thus, general fecundity formulas typically understate interannual variability in actual fecundity. We therefore argue for the use of segmented fecundity formulas linked to dedicated monitoring programs.

First thorough assessment of de novo oocyte recruitment in a teleost serial spawner, the Northeast Atlantic mackerel (Scomber scombrus) case.

The understanding of teleost fecundity type (determinate or indeterminate) is essential when deciding which egg production method should be applied to ultimately estimate spawning stock biomass. The fecundity type is, however, unknown or controversial for several commercial stocks, including the Northeast Atlantic mackerel (Scomber scombrus). Aiming at solving this problem, we applied state-of-the-art laboratory methods to document the mackerel fecundity type, including any de novo oocyte recruitment during spawning. Initially, active mackerel spawning females were precisely classified according to their spawning status. The number and size of all phasei-specific oocytes (12 phases), with a special attention to previtellogenic oocytes phases (PVO [PVO2 to PVO4a-c]), were also thoroughly investigated. Examinations of relative fecundity (RFi) clarified that the latest phase of PVOs (PVO4c) are de novo recruited to the cortical alveoli-vitellogenic pool during the spawning period, resulting in a dome-shaped seasonal pattern in RFi. Hence, we unequivocally classify mackerel as a true indeterminate spawner. As PVO4c oocytes were currently identified around 230 µm, mackerel fecundity counts should rather use this diameter as the lower threshold instead of historically 185 µm. Any use of a too low threshold value in this context will inevitably lead to an overestimation of RFi and thereby underestimated spawning stock biomass.

Genetic factors have a major effect on growth, number of vertebrae and otolith shape in Atlantic herring (Clupea harengus).

Atlantic herring, Clupea harengus, have complex population structures. Mixing of populations is known, but the extent of connectivity is still unclear. Phenotypic plasticity results in divergent phenotypes in response to environmental factors. A marked salinity gradient occurs from Atlantic Ocean (salinity 35) into the Baltic Sea (salinity range 2-12). Herring from both habitats display phenotypic and genetic variability. To explore how genetic factors and salinity influence phenotypic traits like growth, number of vertebrae and otolith shape an experimental population consisting of Atlantic purebreds and Atlantic/Baltic F1 hybrids were incubated and co-reared at two different salinities, 16 and 35, for three years. The F1-generation was repeatedly sampled to evaluate temporal variation. A von Bertalanffy growth model indicated that reared Atlantic purebreds had a higher maximum length (26.2 cm) than Atlantic/Baltic hybrids (24.8 cm) at salinity 35, but not at salinity 16 (25.0 and 24.8 cm, respectively). In contrast, Atlantic/Baltic hybrids achieved larger size-at-age than the wild caught Baltic parental group. Mean vertebral counts and otolith aspect ratios were higher for reared Atlantic purebreds than Atlantic/Baltic hybrids, consistent with the differences between parental groups. There were no significant differences in vertebral counts and otolith aspect ratios between herring with the same genotype but raised in different salinities. A Canonical Analysis of Principal Coordinates was applied to analyze the variation in wavelet coefficients that described otolith shape. The first discriminating axis identified the differences between Atlantic purebreds and Atlantic/Baltic hybrids, while the second axis represented salinity differences. Assigning otoliths based on genetic groups (Atlantic purebreds vs. Atlantic/Baltic hybrids) yielded higher classification success (~90%) than based on salinities (16 vs. 35; ~60%). Our results demonstrate that otolith shape and vertebral counts have a significant genetic component and are therefore useful for studies on population dynamics and connectivity.

Comparative biology and population mixing among local, coastal and offshore Atlantic herring (Clupea harengus) in the North Sea, Skagerrak, Kattegat and western Baltic.

The population structure of Atlantic herring (Clupea harengus) from 13 local, coastal and offshore areas of the North Sea, Skagerrak, Kattegat and western Baltic (northeast Atlantic) was studied using biological and environmental data from 1970-2015. The objective was to identify distinct populations by comparing variability in the temporal and spatial phenotypic characteristics and evaluate the potential for mixing of populations in time and space. The populations varied in biological characteristics such as mean vertebral counts (VS), growth and maturity ogives. Generalized additive models indicated temporally stable VS in the North Sea and western Baltic, whereas intra-annual temporal variation of VS occurred in other areas. High variability of VS within a population was not affected by environmental factors such as temperature and salinity. Consequently, seasonal VS variability can be explained by the presence or absence of herring populations as they migrate between areas. The three main populations identified in this paper correspond to the three managed stocks in this area: Norwegian spring spawners (NSS), western Baltic spring spawners (WBSS) and North Sea autumn spawners (NSAS). In addition, several local populations were identified in fjords or lakes along the coast, but our analyses could not detect direct mixing of local populations with the three main populations. Our results highlight the importance of recognizing herring dynamics and understanding the mixing of populations as a challenge for management of herring.

Feeding Ecology of Northeast Atlantic Mackerel, Norwegian Spring-Spawning Herring and Blue Whiting in the Norwegian Sea.

The Norwegian spring-spawning (NSS) herring (Clupea harengus), blue whiting (Micromesistius poutassou) and Northeast Atlantic (NEA) mackerel (Scomber scombrus) are extremely abundant pelagic planktivores that feed in the Norwegian Sea (NS) during spring and summer. This study investigated the feeding ecology and diet composition of these commercially important fish stocks on the basis of biological data, including an extensive set of stomach samples in combination with hydrographical data, zooplankton samples and acoustic abundance data from 12 stock monitoring surveys carried out in 2005-2010. Mackerel were absent during the spring, but had generally high feeding overlap with herring in the summer, with a diet mainly based on calanoid copepods, especially Calanus finmarchicus, as well as a similar diet width. Stomach fullness in herring diminished from spring to summer and feeding incidence was lower than that of mackerel in summer. However, stomach fullness did not differ between the two species, indicating that herring maintain an equally efficient pattern of feeding as mackerel in summer, but on a diet that is less dominated by copepods and is more reliant on larger prey. Blue whiting tended to have a low dietary overlap with mackerel and herring, with larger prey such as euphausiids and amphipods dominating, and stomach fullness and feeding incidence increasing with length. For all the species, feeding incidence increased with decreasing temperature, and for mackerel so did stomach fullness, indicating that feeding activity is highest in areas associated with colder water masses. Significant annual effects on diet composition and feeding-related variables suggested that the three species are able to adapt to different food and environmental conditions. These annual effects are likely to have an important impact on the predation pressure on different plankton groups and the carrying capacity of individual systems, and emphasise the importance of regular monitoring of pelagic fish diets.

Characteristics of the Norwegian Coastal Current during Years with High Recruitment of Norwegian Spring Spawning Herring (Clupea harengus L.).

Norwegian Spring Spawning herring (NSSH) Clupea harengus L. spawn on coastal banks along the west coast of Norway. The larvae are generally transported northward in the Norwegian Coastal Current (NCC) with many individuals utilizing nursery grounds in the Barents Sea. The recruitment to this stock is highly variable with a few years having exceptionally good recruitment. The principal causes of recruitment variability of this herring population have been elusive. Here we undertake an event analysis using data between 1948 and 2010 to gain insight into the physical conditions in the NCC that coincide with years of high recruitment. In contrast to a typical year when northerly upwelling winds are prominent during spring, the years with high recruitment coincide with predominantly southwesterly winds and weak upwelling in spring and summer, which lead to an enhanced northward coastal current during the larval drift period. Also in most peak recruitment years, low-salinity anomalies are observed to propagate northward during the spring and summer. It is suggested that consistent southwesterly (downwelling) winds and propagating low-salinity anomalies, both leading to an enhanced northward transport of larvae, are important factors for elevated recruitment. At the same time, these conditions stabilize the coastal waters, possibly leading to enhanced production and improved feeding potential along the drift route to Barents Sea. Further studies on the drivers of early life history mortality can now be undertaken with a better understanding of the physical conditions that prevail during years when elevated recruitment occurs in this herring stock.

Latitudinal Gradient in Otolith Shape among Local Populations of Atlantic Herring (Clupea harengus L.) in Norway.

Otolith shape analysis of Atlantic herring (Clupea harengus) in Norwegian waters shows significant differentiation among fjords and a latitudinal gradient along the coast where neighbouring populations are more similar to each other than to those sampled at larger distances. The otolith shape was obtained using quantitative shape analysis, the outlines were transformed with Wavelet and analysed with multivariate methods. The observed morphological differences are likely to reflect environmental differences but indicate low dispersal among the local herring populations. Otolith shape variation suggests also limited exchange between the local populations and their oceanic counterparts, which could be due to differences in spawning behaviour. Herring from the most northerly location (69°N) in Balsfjord, which is genetically more similar to Pacific herring (Clupea pallasii), differed in otolith shape from all the other populations. Our results suggest that the semi-enclosed systems, where the local populations live and breed, are efficient barriers for dispersal. Otolith shape can thus serve as a marker to identify the origin of herring along the coast of Norway.

The dynamics of a metapopulation: changes in life-history traits in resident herring that co-occur with oceanic herring during spawning.

Different populations of Atlantic herring are regarded as forming a metapopulation, but we know little about the dynamics of the connectivity and degree of interbreeding between the populations. Based on data from three periods between 1962 and 2011, we identified the presence of two components of herring in a small semi-enclosed coastal marine ecosystem based on different somatic growth patterns and mean vertebrae sum (VS). The two components were interpreted as belonging to a resident herring population and the migratory, oceanic Norwegian spring spawning (NSS) herring population, and they co-occurred during spawning. In the 1960s, resident herring characterized by slow growth and low VS co-occurred with rapid growth, high VS oceanic NSS herring. Similar slow-growing resident and rapid-growing NSS herring were found in the 1970-80s, but both populations now had low VS suggesting similar origins. Finally, in the 2000s both populations showed rapid growth. The changes coincided with the NSS herring going from a state of high abundance and oceanic distribution to a collapse in the late 1960s that resulted in a coastal distribution closer to resident herring populations, before full recovery and resumption of the migratory, oceanic pattern in the 1990s. During all three periods, NSS herring were only present in the local system up to an age of about five years, but the synchronous spawning of the populations supports mixed spawning and interbreeding. During the investigation period both longevity, length at age (growth) and length-at-first maturity increased markedly for the resident herring, which then became more similar to the NSS herring. Genetic and/or cultural factors are believed to be the main causes of the observed changes in life history traits, although some effect of changes in environmental factors cannot be excluded. Our study suggests that relationships among populations in a metapopulation can be highly dynamic.

Seasonal dynamics of Atlantic herring (Clupea harengus L.) populations spawning in the vicinity of marginal habitats.

Gillnet sampling and analyses of otolith shape, vertebral count and growth indicated the presence of three putative Atlantic herring (Clupea harengus L.) populations mixing together over the spawning season February-June inside and outside an inland brackish water lake (Landvikvannet) in southern Norway. Peak spawning of oceanic Norwegian spring spawners and coastal Skagerrak spring spawners occurred in March-April with small proportions of spawners entering the lake. In comparison, spawning of Landvik herring peaked in May-June with high proportions found inside the lake, which could be explained by local adaptations to the environmental conditions and seasonal changes of this marginal habitat. The 1.85 km(2) lake was characterized by oxygen depletion occurring between 2.5 and 5 m depth between March and June. This was followed by changes in salinity from 1-7‰ in the 0-1 m surface layer to levels of 20-25‰ deeper than 10 m. In comparison, outside the 3 km long narrow channel connecting the lake with the neighboring fjord, no anoxic conditions were found. Here salinity in the surface layer increased over the season from 10 to 25‰, whereas deeper than 5 m it was stable at around 35‰. Temperature at 0-5 m depth increased significantly over the season in both habitats, from 7 to 14 °C outside and 5 to 17 °C inside the lake. Despite differences in peak spawning and utilization of the lake habitat between the three putative populations, there was an apparent temporal and spatial overlap in spawning stages suggesting potential interbreeding in accordance with the metapopulation concept.

Meta-ecosystems and biological energy transport from ocean to coast: the ecological importance of herring migration.

Ecosystems are not closed, but receive resource subsidies from other ecosystems. Energy, material and organisms are moved between systems by physical vectors, but migrating animals also transport resources between systems. We report on large scale energy transport from ocean to coast by a migrating fish population, the Norwegian spring-spawning (NSS) herring Clupea harengus. We observe a rapid body mass increase during parts of the annual, oceanic feeding migration and we use a bioenergetics model to quantify energy consumption. The model predicts strong seasonal variation in food consumption with a marked peak in late May to July. The copepod Calanus finmarchicus is the most important prey and 23 x 10(6) tones (wet weight) of C. finmarchicus is consumed annually. The annual consumption-biomass ratio is 5.2. During the feeding migration 17% of consumed energy is converted to body mass. The biomass transported to the coast and left as reproductive output is estimated from gonad weight and is about 1.3 x 10(6) tones for the current population. This transport is to our knowledge the world's largest flux of energy caused by a single population. We demonstrate marked temporal variation in transport during the last century and discuss the effects of NSS herring in the ocean, as a major consumer, and at the coast, where eggs and larvae are important for coastal predators. In particular, we suggest that the rapid decline of lobster Homarus gammarus landings in Western Norway during the 1960s was related to the collapse of NSS herring. We also discuss spatial variation in energy transport caused by changed migration patterns. Both climate and fisheries probably triggered historical changes in the migration patterns of NSS herring. New migration routes emerge at the level of individuals, which in turn determines where resources are gathered and delivered, and therefore, how meta-ecosystems function.