Seeking the true time: Exploring otolith chemistry as an age-determination tool.

Fish otoliths' chronometric properties make them useful for age and growth rate estimation in fisheries management. For the Eastern Baltic Sea cod stock (Gadus morhua), unclear seasonal growth zones in otoliths have resulted in unreliable age and growth information. Here, a new age estimation method based on seasonal patterns in trace elemental otolith incorporation was tested for the first time and compared with the traditional method of visually counting growth zones, using otoliths from the Baltic and North seas. Various trace elemental ratios, linked to fish metabolic activity (higher in summer) or external environment (migration to colder, deeper habitats with higher salinity in winter), were tested for age estimation based on assessing their seasonal variations in concentration. Mg:Ca and P:Ca, both proxies for growth and metabolic activity, showed greatest seasonality and therefore have the best potential to be used as chemical clocks. Otolith image readability was significantly lower in the Baltic than in the North Sea. The chemical (novel) method had an overall greater precision and percentage agreement among readers (11.2%, 74.0%) than the visual (traditional) method (23.1%, 51.0%). Visual readers generally selected more highly contrasting zones as annuli whereas the chemical readers identified brighter regions within the first two annuli and darker zones thereafter. Visual estimates produced significantly higher, more variable ages than did the chemical ones. Based on the analyses in our study, we suggest that otolith microchemistry is a promising alternative ageing method for fish populations difficult to age, such as the Eastern Baltic cod.

Otolith chemistry indicates recent worsened Baltic cod condition is linked to hypoxia exposure.

Deoxygenation worldwide is increasing in aquatic systems with implications for organisms' biology, communities and ecosystems. Eastern Baltic cod has experienced a strong decline in mean body condition (i.e. weight at a specific length) over the past 20 years with effects on the fishery relying on this resource. The decrease in cod condition has been tentatively linked in the literature to increased hypoxic areas potentially affecting habitat range, but also to benthic prey and/or cod physiology directly. To date, no studies have been performed to test these mechanisms. Using otolith trace element microchemistry and hypoxia-responding metrics based on manganese (Mn) and magnesium (Mg), we investigated the relationship between fish body condition at capture and exposure to hypoxia. Cod individuals collected after 2000 with low body condition had a higher level of Mn/Mg in the last year of life, indicating higher exposure to hypoxic waters than cod with high body condition. Moreover, lifetime exposure to hypoxia was even more strongly correlated to body condition, suggesting that condition may reflect long-term hypoxia status. These results were irrespective of fish age or sex. This implies that as Baltic cod visit poor-oxygen waters, perhaps searching for benthic food, they compromise their own performance. This study specifically sheds light on the mechanisms leading to the low condition of cod and generally points to the impact of deoxygenation on ecosystems and fisheries.

Effects of freezing on length and mass measurements of Atlantic cod Gadus morhua in the Baltic Sea.

An aggregated sample of 925 Atlantic cod Gadus morhua collected by four countries in different regions of the Baltic Sea during different seasons were measured (total length, LT = 161-890 mm and weighed (mass, M = 45-6900 g) both before freezing and after defrosting. The cod were found to decrease significantly in both LT and M following death and frozen storage. There was an average (±SD) change in LT of -2.91% (±0.05%) following freezing, independent of starting LT . Total M changed by -2.65% (±0.14%), independent of starting mass. Shrinkage of LT and M did not differ significantly between 1 and 4 months frozen storage, though LT shrinkage was significantly greater after 1 or 4 months in the freezer compared with after 5 days. There was significant variation in LT and M shrinkage between regions of capture. A significant negative relationship between condition of cod and LT or M change was also observed. Equations to back-calculate fresh LT and M from thawed LT , M and standard length (LS ), gutted LT , gutted LS and gutted M are provided.

Metapopulation theory identifies biogeographical patterns among core and satellite marine bacteria scaling from tens to thousands of kilometers.

Metapopulation theory developed in terrestrial ecology provides applicable frameworks for interpreting the role of local and regional processes in shaping species distribution patterns. Yet, empirical testing of metapopulation models on microbial communities is essentially lacking. We determined regional bacterioplankton dynamics from monthly transect sampling in the Baltic Sea Proper using 16S rRNA gene sequencing. A strong positive trend was found between local relative abundance and occupancy of populations. Notably, the occupancy-frequency distributions were significantly bimodal with a satellite mode of rare endemic populations and a core mode of abundant cosmopolitan populations (e.g. Synechococcus, SAR11 and SAR86 clade members). Temporal changes in population distributions supported several theoretical frameworks. Still, bimodality was found among bacterioplankton communities across the entire Baltic Sea, and was also frequent in globally distributed datasets. Datasets spanning waters with widely different physicochemical characteristics or environmental gradients typically lacked significant bimodal patterns. When such datasets were divided into subsets with coherent environmental conditions, bimodal patterns emerged, highlighting the importance of positive feedbacks between local abundance and occupancy within specific biomes. Thus, metapopulation theory applied to microbial biogeography can provide novel insights into the mechanisms governing shifts in biodiversity resulting from natural or anthropogenically induced changes in the environment.

Climate and fishing steer ecosystem regeneration to uncertain economic futures.

Overfishing of large predatory fish populations has resulted in lasting restructurings of entire marine food webs worldwide, with serious socio-economic consequences. Fortunately, some degraded ecosystems show signs of recovery. A key challenge for ecosystem management is to anticipate the degree to which recovery is possible. By applying a statistical food-web model, using the Baltic Sea as a case study, we show that under current temperature and salinity conditions, complete recovery of this heavily altered ecosystem will be impossible. Instead, the ecosystem regenerates towards a new ecological baseline. This new baseline is characterized by lower and more variable biomass of cod, the commercially most important fish stock in the Baltic Sea, even under very low exploitation pressure. Furthermore, a socio-economic assessment shows that this signal is amplified at the level of societal costs, owing to increased uncertainty in biomass and reduced consumer surplus. Specifically, the combined economic losses amount to approximately 120 million € per year, which equals half of today's maximum economic yield for the Baltic cod fishery. Our analyses suggest that shifts in ecological and economic baselines can lead to higher economic uncertainty and costs for exploited ecosystems, in particular, under climate change.

Predator transitory spillover induces trophic cascades in ecological sinks.

Understanding the effects of cross-system fluxes is fundamental in ecosystem ecology and biological conservation. Source-sink dynamics and spillover processes may link adjacent ecosystems by movement of organisms across system boundaries. However, effects of temporal variability in these cross-system fluxes on a whole marine ecosystem structure have not yet been presented. Here we show, using 35 y of multitrophic data series from the Baltic Sea, that transitory spillover of the top-predator cod from its main distribution area produces cascading effects in the whole food web of an adjacent and semi-isolated ecosystem. At varying population size, cod expand/contract their distribution range and invade/retreat from the neighboring Gulf of Riga, thereby affecting the local prey population of herring and, indirectly, zooplankton and phytoplankton via top-down control. The Gulf of Riga can be considered for cod a "true sink" habitat, where in the absence of immigration from the source areas of the central Baltic Sea the cod population goes extinct due to the absence of suitable spawning grounds. Our results add a metaecosystem perspective to the ongoing intense scientific debate on the key role of top predators in structuring natural systems. The integration of regional and local processes is central to predict species and ecosystem responses to future climate changes and ongoing anthropogenic disturbances.

A metacommunity perspective on source­sink dynamics and management: the Baltic Sea as a case study.

The degree to which metapopulation processes influence fish stock dynamics is a largely unresolved issue in marine science and management, especially for highly mobile species such as Atlantic cod (Gadus morhua) and herring (Clupea harengus). The Baltic Sea comprises a heterogeneous oceanographic environment that structures the spatial and temporal distribution of the dominant species cod, herring, and sprat (Sprattus sprattus). Despite local differences, the stocks are traditionally managed as homogeneous units. Here, we present a metacommunity-perspective on source­sink dynamics of Baltic Sea fish stocks by using a spatially disaggregated statistical food web model. The model is fitted to area-specific time series of multiple abiotic and biotic variables using state-space methods. Our analysis reveals pronounced net fluxes between areas, indicative of source­sink dynamics, as well as area-specific differences in species interactions (i.e., density dependence, competition, and predator­prey) and the degree of fishing and climate impact on survival and recruitment. Furthermore, model simulations show that decreasing exploitation pressure in the source area for cod (without reallocating fishing effort) produces an increase in neighboring sink habitats, but a decline of prey species in response to increased predation. Our approach provides valuable insight concerning metacommunity-structuring of marine fish and may serve as an important tool for implementing sustainable management strategies under the ecosystem approach to marine and fisheries management.

Cod otoliths document accelerating climate impacts in the Baltic Sea.

Anthropogenic deoxygenation of the Baltic Sea caused major declines in demersal and benthic habitat quality with consequent impacts on biodiversity and ecosystem services. Using Baltic cod otolith chemical proxies of hypoxia, salinity, and fish metabolic status and growth, we tracked changes from baseline conditions in the late Neolithic (4500 BP) and early twentieth century to the present, in order to understand how recent, accelerating climate change has affected this key species. Otolith hypoxia proxies (Mn:Mg) increased with expanding anoxic water volumes, but decreased with increasing salinity indexed by otolith Sr:Ca. Metabolic status proxied by otolith Mg:Ca and reconstructed growth were positively related to dissolved oxygen percent saturation, with particularly severe declines since 2010. This long-term record of otolith indicators provides further evidence of a profound state change in oxygen for the worse, in one of the world's largest inland seas. Spreading hypoxia due to climate warming will likely impair fish populations globally and evidence can be tracked with otolith chemical biomarkers.

Spatio-temporal patterns of whiting (Merlangius merlangus) in the Adriatic Sea under environmental forcing.

Understanding how environmental factors affect species distribution is crucial for the conservation and management of marine organisms, especially in the face of global changes. Whiting (Merlangius merlangus) is a demersal cold-temperate fish, considered a 'relict species' in the Adriatic Sea. Despite its significance to commercial fisheries in the region, the specific drivers behind its spatial and temporal patterns have not been thoroughly examined. Here, we fitted a set of Generalized Linear Mixed Effects Models to data collected in the Northern and Central Adriatic from 1999 to 2019 during the Mediterranean International Trawl Survey to investigate the potential influence of depth, seafloor temperature and seafloor dissolved oxygen on the annual biomass density and spatial distribution of whiting in the spring-summer season. Our results showed that depth, and to a lesser degree temperature and oxygen, are important predictors of whiting distribution in this period, with preferences for depths of ~ 45 m, temperature of ~ 15.4°C and dissolved oxygen > 5.5 ml L-1. We predicted a persistent core area of distribution in front of the Po River Delta, in the Northern Adriatic Sea, while the density progressively declined towards the Central and Southern Adriatic Sea along the Italian coast. Additionally, the temporal trend exhibited high fluctuations over the years, occurring in cycles of 3 to 4 years. Finally, by comparing the biomass density estimates obtained under optimal conditions with those derived from the actual values for each variable, our analysis revealed that temperature had a pronounced and general impact on biomass density in the northern survey area (predictions revealed a density reduction of approximately two-thirds), while oxygen displayed a minor and more localized influence. This work deepens the current knowledge about the ecology of whiting in the Adriatic Sea and provides support for the conservation and management of this species.

Cohort dynamics give rise to alternative stable community states.

Many ecological systems can exhibit alternative stable states (ASS), which implies that ecological communities may diverge depending on their initial state, despite identical environmental conditions. Here we present a new mechanism that can cause ASS in competition systems. Using a physiologically structured model of competing populations, representing Baltic Sea sprat and herring and their resources, we show how cohort-driven population cycles may result in priority effects leading to ASS. Similar mechanisms could, depending on mortality level, also result in a "resident strikes back" phenomenon. We argue that the prerequisites for the occurrence of ASS in our model system, that is, communities with competing populations exhibiting cohort cycles and variation in size at maturation, may be common in ecological systems.

Predators with multiple ontogenetic niche shifts have limited potential for population growth and top-down control of their prey.

Catastrophic collapses of top predators have revealed trophic cascades and community structuring by top-down control. When populations fail to recover after a collapse, this may indicate alternative stable states in the system. Overfishing has caused several of the most compelling cases of these dynamics, and in particular Atlantic cod stocks exemplify such lack of recovery. Often, competition between prey species and juvenile predators is hypothesized to explain the lack of recovery of predator populations. The predator is then considered to compete with its prey for one resource when small and to subsequently shift to piscivory. Yet predator life history is often more complex than that, including multiple ontogenetic diet shifts. Here we show that no alternative stable states occur when predators in an intermediate life stage feed on an additional resource (exclusive to the predator) before switching to piscivory, because predation and competition between prey and predator do not simultaneously structure community dynamics. We find top-down control by the predator only when there is no feedback from predator foraging on the additional resource. Otherwise, the predator population dynamics are governed by a bottleneck in individual growth occurring in the intermediate life stage. Therefore, additional resources for predators may be beneficial or detrimental for predator population growth and strongly influence the potential for top-down community control.

Influence of ecological traits on spatio-temporal dynamics of an elasmobranch community in a heavily exploited basin.

Elasmobranchs, which include sharks and batoids, play critical roles in maintaining the integrity and stability of marine food webs. However, these cartilaginous fish are among the most threatened vertebrate lineages due to their widespread depletion. Consequently, understanding dynamics and predicting changes of elasmobranch communities are major research topics in conservation ecology. Here, we leverage long-term catch data from a standardized bottom trawl survey conducted from 1996 to 2019, to evaluate the spatio-temporal dynamics of the elasmobranch community in the heavily exploited Adriatic Sea, where these fish have historically been depleted. We use joint species distribution modeling to quantify the responses of the species to environmental variation while also including important traits such as species age at first maturity, reproductive mode, trophic level, and phylogenetic information. We present spatio-temporal changes in the species community and associated modification of the trait composition, highlighting strong spatial and depth-mediated patterning. We observed an overall increase in the abundance of the dominant elasmobranch species, except for spurdog, which has shown a continued decline. However, our results showed that the present community displays lower age at first maturity and a smaller fraction of viviparous species compared to the earlier observed community due to changes in species' relative abundance. The selected traits contributed considerably to explaining community patterns, suggesting that the integration of trait-based approaches in elasmobranch community analyses can aid efforts to conserve this important lineage of fish.

Trophic cascades promote threshold-like shifts in pelagic marine ecosystems.

Fisheries can have a large impact on marine ecosystems, because the effects of removing large predatory fish may cascade down the food web. The implications of these cascading processes on system functioning and resilience remain a source of intense scientific debate. By using field data covering a 30-year period, we show for the Baltic Sea that the underlying mechanisms of trophic cascades produced a shift in ecosystem functioning after the collapse of the top predator cod. We identified an ecological threshold, corresponding to a planktivore abundance of approximately 17 x 10(10) individuals, that separates 2 ecosystem configurations in which zooplankton dynamics are driven by either hydroclimatic forces or predation pressure. Abundances of the planktivore sprat above the threshold decouple zooplankton dynamics from hydrological circumstances. The current strong regulation by sprat of the feeding resources for larval cod may hinder cod recovery and the return of the ecosystem to a prior state. This calls for the inclusion of a food web perspective in management decisions.

First tagging data on large Atlantic bluefin tuna returning to Nordic waters suggest repeated behaviour and skipped spawning.

Atlantic bluefin tuna (Thunnus thynnus; ABFT) is one of the most iconic fish species in the world. Recently, after being very rare for more than half a century, large bluefin tunas have returned to Nordic waters in late summer and autumn, marking the return of the largest predatory fish in Nordic waters. By tagging 18 bluefin tunas with electronic tags (pop-up satellite archival tags), we show that bluefin tuna observed in Nordic waters undertake different migration routes, with individuals migrating into the western Atlantic Ocean, while others stay exclusively in the eastern Atlantic and enter the Mediterranean Sea to spawn. We additionally present evidence of possible skipped spawning inferred from behavioural analyses. In Nordic waters, ABFT are primarily using the upper water column, likely reflecting feeding activity. The results support the hypothesis that ABFT migrating to Nordic waters return to the same general feeding area within the region on an annual basis. These observations may have important implications for management because (1) tunas that come into Nordic waters might represent only a few year classes (as evidenced by a narrow size range), and thus may be particularly vulnerable to area-specific exploitation, and (2) challenge the assumption of consecutive spawning in adult Atlantic bluefin tuna, as used in current stock assessment models. Without careful management and limited exploitation of this part of the ABFT population, the species' return to Nordic waters could be short-lived.

Effects of altered offshore food webs on coastal ecosystems emphasize the need for cross-ecosystem management.

By mainly targeting larger predatory fish, commercial fisheries have indirectly promoted rapid increases in densities of their prey; smaller predatory fish like sprat, stickleback and gobies. This process, known as mesopredator release, has effectively transformed many marine offshore basins into mesopredator-dominated ecosystems. In this article, we discuss recent indications of trophic cascades on the Atlantic and Baltic coasts of Sweden, where increased abundances of mesopredatory fish are linked to increased nearshore production and biomass of ephemeral algae. Based on synthesis of monitoring data, we suggest that offshore exploitation of larger predatory fish has contributed to the increase in mesopredator fish also along the coasts, with indirect negative effects on important benthic habitats and coastal water quality. The results emphasize the need to rebuild offshore and coastal populations of larger predatory fish to levels where they regain their control over lower trophic levels and important links between offshore and coastal systems are restored.

Linking consumer physiological status to food-web structure and prey food value in the Baltic Sea.

Declining physiological status in marine top consumers has been observed worldwide. We investigate changes in the physiological status and population/community traits of six consumer species/groups in the Baltic Sea (1993-2014), spanning four trophic levels and using metrics currently operational or proposed as indicators of food-web status. We ask whether the physiological status of consumers can be explained by food-web structure and prey food value. This was tested using partial least square regressions with status metrics for gray seal, cod, herring, sprat and the benthic predatory isopod Saduria as response variables, and abundance and food value of their prey, abundance of competitors and predators as predictors. We find evidence that the physiological status of cod, herring and sprat is influenced by competition, predation, and prey availability; herring and sprat status also by prey size. Our study highlights the need for management approaches that account for species interactions across multiple trophic levels.

Ecological adaptation in Atlantic herring is associated with large shifts in allele frequencies at hundreds of loci.

Atlantic herring is widespread in North Atlantic and adjacent waters and is one of the most abundant vertebrates on earth. This species is well suited to explore genetic adaptation due to minute genetic differentiation at selectively neutral loci. Here, we report hundreds of loci underlying ecological adaptation to different geographic areas and spawning conditions. Four of these represent megabase inversions confirmed by long read sequencing. The genetic architecture underlying ecological adaptation in herring deviates from expectation under a classical infinitesimal model for complex traits because of large shifts in allele frequencies at hundreds of loci under selection.

Deficiency syndromes in top predators associated with large-scale changes in the Baltic Sea ecosystem.

Vitamin B1 (thiamin) deficiency is an issue periodically affecting a wide range of taxa worldwide. In aquatic pelagic systems, thiamin is mainly produced by bacteria and phytoplankton and is transferred to fish and birds via zooplankton, but there is no general consensus on when or why this transfer is disrupted. We focus on the occurrence in salmon (Salmo salar) of a thiamin deficiency syndrome (M74), the incidence of which is highly correlated among populations derived from different spawning rivers. Here, we show that M74 in salmon is associated with certain large-scale abiotic changes in the main common feeding area of salmon in the southern Baltic Sea. Years with high M74 incidence were characterized by stagnant periods with relatively low salinity and phosphate and silicate concentrations but high total nitrogen. Consequently, there were major changes in phytoplankton and zooplankton, with, e.g., increased abundances of Cryptophyceae, Dinophyceae, Diatomophyceae and Euglenophyceae and Acartia spp. during high M74 incidence years. The prey fish communities also had increased stocks of both herring and sprat in these years. Overall, this suggests important changes in the entire food web structure and nutritional pathways in the common feeding period during high M74 incidence years. Previous research has emphasized the importance of the abundance of planktivorous fish for the occurrence of M74. By using this 27-year time series, we expand this analysis to the entire ecosystem and discuss potential mechanisms inducing thiamin deficiency in salmon.

Multi-level trophic cascades in a heavily exploited open marine ecosystem.

Anthropogenic disturbances intertwined with climatic changes can have a large impact on the upper trophic levels of marine ecosystems, which may cascade down the food web. So far it has been difficult to demonstrate multi-level trophic cascades in pelagic marine environments. Using field data collected during a 33-year period, we show for the first time a four-level community-wide trophic cascade in the open Baltic Sea. The dramatic reduction of the cod (Gadus morhua) population directly affected its main prey, the zooplanktivorous sprat (Sprattus sprattus), and indirectly the summer biomass of zooplankton and phytoplankton (top-down processes). Bottom-up processes and climate-hydrological forces had a weaker influence on sprat and zooplankton, whereas phytoplankton variation was explained solely by top-down mechanisms. Our results suggest that in order to dampen the occasionally harmful algal blooms of the Baltic, effort should be addressed not only to control anthropogenic nutrient inputs but also to preserve structure and functioning of higher trophic levels.

The Baltic Sea as a time machine for the future coastal ocean.

Coastal global oceans are expected to undergo drastic changes driven by climate change and increasing anthropogenic pressures in coming decades. Predicting specific future conditions and assessing the best management strategies to maintain ecosystem integrity and sustainable resource use are difficult, because of multiple interacting pressures, uncertain projections, and a lack of test cases for management. We argue that the Baltic Sea can serve as a time machine to study consequences and mitigation of future coastal perturbations, due to its unique combination of an early history of multistressor disturbance and ecosystem deterioration and early implementation of cross-border environmental management to address these problems. The Baltic Sea also stands out in providing a strong scientific foundation and accessibility to long-term data series that provide a unique opportunity to assess the efficacy of management actions to address the breakdown of ecosystem functions. Trend reversals such as the return of top predators, recovering fish stocks, and reduced input of nutrient and harmful substances could be achieved only by implementing an international, cooperative governance structure transcending its complex multistate policy setting, with integrated management of watershed and sea. The Baltic Sea also demonstrates how rapidly progressing global pressures, particularly warming of Baltic waters and the surrounding catchment area, can offset the efficacy of current management approaches. This situation calls for management that is (i) conservative to provide a buffer against regionally unmanageable global perturbations, (ii) adaptive to react to new management challenges, and, ultimately, (iii) multisectorial and integrative to address conflicts associated with economic trade-offs.