Twenty-five emerging questions when detecting, understanding, and predicting future fish distributions in a changing climate.

The 2023 Annual Symposium of the Fisheries Society of the British Isles hosted opportunities for researchers, scientists, and policy makers to reflect on the state of art of predicting fish distributions and consider the implications to the marine and aquatic environments of a changing climate. The outcome of one special interest group at the Symposium was a collection of questions, organized under five themes, which begin to capture the state of the field and identify priorities for research and management over the coming years. The five themes were Physiology, Mechanisms, Detect and Measure, Manage, and Wider Ecosystems. The questions, 25 of them, addressed concepts which remain poorly understood, are data deficient, and/or are likely to be impacted in measurable or profound ways by climate change. Moving from the first to the last theme, the questions expanded in the scope of their considerations, from specific processes within the individual to ecosystem-wide impacts, but no one question is bigger than any other: each is important in detecting, understanding, and predicting fish distributions, and each will be impacted by an aspect of climate change. In this way, our questions, particularly those concerning unknown mechanisms and data deficiencies, aimed to offer a guide to other researchers, managers, and policy makers in the prioritization of future work as a changing climate is expected to have complex and disperse impacts on fish populations and distributions that will require a coordinated effort to address.

Lemon sole Microstomus kitt in the northern North Sea: a multidisciplinary approach to the early life-history dynamics.

Lemon sole Microstomus kitt is a commercially valuable flatfish species that occurs in shelf waters around the northeast Atlantic. Only the most basic life-history information is available for the North Sea. Spawning is generally assumed to occur between early May and October, with a peak between May and August. Lemon sole larvae have been found in the water column in the northern North Sea in winter during standard surveys. Larvae captured in November/December 2016 and January/February 2017 using the International Council for the Exploration of the Seas standard 2 m Midwater Ring trawls (MIK) were analysed to gain a better understanding of the pelagic early life-history stages of lemon sole, especially in relation to the timing of spawning and the dispersal of overwintering larvae. Larval age was estimated from sagittal otolith primary increment counts. The larvae caught in November/December ranged in nominal age from 4 to 45 days post-hatching which suggests that spawning continues into late October and November. Most, but not all, of the larvae caught in January/February were post metamorphosis, and the difference in age between the two sampling dates was consistent with the elapsed time between samplings. The estimated hatching dates confirm that lemon sole spawning extends into late autumn in the northern North Sea, with overwintering larvae in all developmental stages. Drift modelling of eggs and larvae released at historically documented spawning grounds in the northern North Sea suggests that these grounds are also the source for all of the larvae sampled during the 2016-2017 surveys.

Quantitative molecular detection of larval Atlantic herring (Clupea harengus) in stomach contents of Atlantic mackerel (Scomber scombrus) marks regions of predation pressure.

Mortality rates in the early life-history stages of fishes are generally high yet identifying the causes remain unclear. Faltering recruitment rates of Atlantic herring (Clupea harengus) in the Norwegian Sea indicate a need to identify which mortality factors influence larval herring survival. Previous research suggests that increased predation pressure by Atlantic mackerel (Scomber scombrus) may contribute to the disconnect between spawning stock biomass and recruitment. To quantify the contribution of predation pressure by Atlantic mackerel to herring larval mortality, two research cruises were conducted within a probable "hot spot" (67-72° N) for intensified mackerel predation based on particle drift simulations. Mackerel stomach contents were analysed for herring larvae content using droplet digital polymerase chain reaction (ddPCR) with a quantitative molecular detection assay specific for herring. The ddPCR results demonstrate clear predation by mackerel on herring larvae and also suggest that the alternative use of visual examination may give misleading results. Our results show that mackerel should be considered a potentially important predator on herring larvae. The quantitative molecular assay presented here shows great promise as an efficient and specific tool to correctly identify and quantify predation pressure on early life-history stages of fishes.

Genetic response to human-induced habitat changes in the marine environment: A century of evolution of European sprat in Landvikvannet, Norway.

Habitat changes represent one of the five most pervasive threats to biodiversity. However, anthropogenic activities also have the capacity to create novel niche spaces to which species respond differently. In 1880, one such habitat alterations occurred in Landvikvannet, a freshwater lake on the Norwegian coast of Skagerrak, which became brackish after being artificially connected to the sea. This lake is now home to the European sprat, a pelagic marine fish that managed to develop a self-recruiting population in barely few decades. Landvikvannet sprat proved to be genetically isolated from the three main populations described for this species; that is, Norwegian fjords, Baltic Sea, and the combination of North Sea, Kattegat, and Skagerrak. This distinctness was depicted by an accuracy self-assignment of 89% and a highly significant F ST between the lake sprat and each of the remaining samples (average of ≈0.105). The correlation between genetic and environmental variation indicated that salinity could be an important environmental driver of selection (3.3% of the 91 SNPs showed strong associations). Likewise, Isolation by Environment was detected for salinity, although not for temperature, in samples not adhering to an Isolation by Distance pattern. Neighbor-joining tree analysis suggested that the source of the lake sprat is in the Norwegian fjords, rather than in the Baltic Sea despite a similar salinity profile. Strongly drifted allele frequencies and lower genetic diversity in Landvikvannet compared with the Norwegian fjords concur with a founder effect potentially associated with local adaptation to low salinity. Genetic differentiation (F ST) between marine and brackish sprat is larger in the comparison Norway-Landvikvannet than in Norway-Baltic, which suggests that the observed divergence was achieved in Landvikvannet in some 65 generations, that is, 132 years, rather than gradually over thousands of years (the age of the Baltic Sea), thus highlighting the pace at which human-driven evolution can happen.

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.

Genetic analysis redraws the management boundaries for the European sprat.

Sustainable fisheries management requires detailed knowledge of population genetic structure. The European sprat is an important commercial fish distributed from Morocco to the Arctic circle, Baltic, Mediterranean, and Black seas. Prior to 2018, annual catch advice on sprat from the International Council for the Exploration of the Sea (ICES) was based on five putative stocks: (a) North Sea, (b) Kattegat-Skagerrak and Norwegian fjords, (c) Baltic Sea, (d) West of Scotland-southern Celtic Seas, and (e) English Channel. However, there were concerns that the sprat advice on stock size estimates management plan inadequately reflected the underlying biological units. Here, we used ddRAD sequencing to develop 91 SNPs that were thereafter used to genotype approximately 2,500 fish from 40 locations. Three highly distinct and relatively homogenous genetic groups were identified: (a) Norwegian fjords; (b) Northeast Atlantic including the North Sea, Kattegat-Skagerrak, Celtic Sea, and Bay of Biscay; and (c) Baltic Sea. Evidence of genetic admixture and possibly physical mixing was detected in samples collected from the transition zone between the North and Baltic seas, but not between any of the other groups. These results have already been implemented by ICES with the decision to merge the North Sea and the Kattegat-Skagerrak sprat to be assessed as a single unit, thus demonstrating that genetic data can be rapidly absorbed to align harvest regimes and biological units.

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.

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.

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.

Synergies between climate and management for Atlantic cod fisheries at high latitudes.

The widespread depletion of commercially exploited marine living resources is often seen as a general failure of management and results in criticism of contemporary management procedures. When populations show dramatic and positive changes in population size, this invariably leads to questions about whether favorable climatic conditions or good management (or both) were responsible. The Barents Sea cod (Gadus morhua) stock has recently increased markedly and the spawning stock biomass is now at an unprecedented high. We identify the crucial social and environmental factors that made this unique growth possible. The relationship between vital rates of Barents Sea cod stock productivity (recruitment, growth, and mortality) and environment is investigated, followed by simulations of population size under different management scenarios. We show that the recent sustained reduction in fishing mortality, facilitated by the implementation of a "harvest control rule," was essential to the increase in population size. Simulations show that a drastic reduction in fishing mortality has resulted in a doubling of the total population biomass compared with that expected under the former management regime. However, management alone was not solely responsible. We document that prevailing climate, operating through several mechanistic links, positively reinforced management actions. Heightened temperature resulted in an increase in the extent of the suitable feeding area for Barents Sea cod, likely offering a release from density-dependent effects (for example, food competition and cannibalism) through prolonged overlap with prey and improved adult stock productivity. Management and climate may thus interact to give a positive outlook for exploited high-latitude marine resources.

Frequent skipped spawning in the world's largest cod population.

Life-history theory suggests that animals may skip reproductive events after initial maturation to maximize lifetime fitness. In iteroparous teleosts, verifying past spawning history is particularly difficult; the degree of skipped spawning at the population level therefore remains unknown. We unequivocally show frequent skipped spawning in Northeast Arctic cod (NEAC) in a massive field and laboratory effort from 2006 to 2008. This was verified by postovulatory follicles in temporarily arrested ovaries close to the putative spawning period. At the population level, "skippers" were estimated to be approximately equally abundant as spawning females in 2008, constituting ∼24% of the females 60-100 cm. These females never truly started vitellogenesis and principally remained on the feeding grounds when spawners migrated southward, avoiding any migration costs. The proximate cause of skipping seems to be insufficient energy to initiate oocyte development, indicating that skipped spawning may partly be a density-dependent response important in population regulation. Our data also indicate more skipping among smaller females and potential tradeoffs between current and future reproductive effort. We propose that skipped spawning is an integral life-history component for NEAC, likely varying annually, and it could therefore be an underlying factor causing some of the currently unexplained large NEAC recruitment variation. The same may hold for other teleosts.