Disentangling structural genomic and behavioural barriers in a sea of connectivity.

Genetic divergence among populations arises through natural selection or drift and is counteracted by connectivity and gene flow. In sympatric populations, isolating mechanisms are thus needed to limit the homogenizing effects of gene flow to allow for adaptation and speciation. Chromosomal inversions act as an important mechanism maintaining isolating barriers, yet their role in sympatric populations and divergence with gene flow is not entirely understood. Here, we revisit the question of whether inversions play a role in the divergence of connected populations of the marine fish Atlantic cod (Gadus morhua), by exploring a unique data set combining whole-genome sequencing data and behavioural data obtained with acoustic telemetry. Within a confined fjord environment, we find three genetically differentiated Atlantic cod types belonging to the oceanic North Sea population, the western Baltic population and a local fjord-type cod. Continuous behavioural tracking over 4 year revealed temporally stable sympatry of these types within the fjord. Despite overall weak genetic differentiation consistent with high levels of gene flow, we detected significant frequency shifts of three previously identified inversions, indicating an adaptive barrier to gene flow. In addition, behavioural data indicated that North Sea cod and individuals homozygous for the LG12 inversion had lower fitness in the fjord environment. However, North Sea and fjord-type cod also occupy different depths, possibly contributing to prezygotic reproductive isolation and representing a behavioural barrier to gene flow. Our results provide the first insights into a complex interplay of genomic and behavioural isolating barriers in Atlantic cod and establish a new model system towards an understanding of the role of genomic structural variants in adaptation and diversification.

Life on the edge: O2 binding in Atlantic cod red blood cells near their southern distribution limit is not sensitive to temperature or haemoglobin genotype.

Atlantic cod are a commercially important species believed to be threatened by warming seas near their southern, equatorward upper thermal edge of distribution. Limitations to circulatory O2 transport, in particular cardiac output, and the geographic distribution of functionally different haemoglobin (Hb) genotypes have separately been suggested to play a role in setting thermal tolerance in this species. The present study assessed the thermal sensitivity of O2 binding in Atlantic cod red blood cells with different Hb genotypes near their upper thermal distribution limit and modelled its consequences for the arterio-venous O2 saturation difference, Sa-vO2 , another major determinant of circulatory O2 supply rate. The results showed statistically indistinguishable red blood cell O2 binding between the three HbI genotypes in wild-caught Atlantic cod from the Irish Sea (53° N). Red blood cells had an unusually low O2 affinity, with reduced or even reversed thermal sensitivity between pH 7.4 and 7.9, and 5.0 and 20.0°C. This was paired with strongly pH-dependent affinity and cooperativity of red blood cell O2 binding (Bohr and Root effects). Modelling of Sa-vO2  at physiological pH, temperature and O2 partial pressures revealed a substantial capacity for increases in Sa-vO2  to meet rising tissue O2 demands at 5.0 and 12.5°C, but not at 20°C. Furthermore, there was no evidence for an increase of maximal Sa-vO2  with temperature. It is suggested that Atlantic cod at such high temperatures may solely depend on increases in cardiac output and blood O2 capacity, or thermal acclimatisation of metabolic rate, for matching circulatory O2 supply to tissue demand.

Climate change and fishing: a century of shifting distribution in North Sea cod.

Globally, spatial distributions of fish stocks are shifting but although the role of climate change in range shifts is increasingly appreciated, little remains known of the likely additional impact that high levels of fishing pressure might have on distribution. For North Sea cod, we show for the first time and in great spatial detail how the stock has shifted its distribution over the past 100 years. We digitized extensive historical fisheries data from paper charts in UK government archives and combined these with contemporary data to a time-series spanning 1913-2012 (excluding both World Wars). New analysis of old data revealed that the current distribution pattern of cod - mostly in the deeper, northern- and north-easternmost parts of the North Sea - is almost opposite to that during most of the Twentieth Century - mainly concentrated in the west, off England and Scotland. Statistical analysis revealed that the deepening, northward shift is likely attributable to warming; however, the eastward shift is best explained by fishing pressure, suggestive of significant depletion of the stock from its previous stronghold, off the coasts of England and Scotland. These spatial patterns were confirmed for the most recent 3 1/2 decades by data from fisheries-independent surveys, which go back to the 1970s. Our results demonstrate the fundamental importance of both climate change and fishing pressure for our understanding of changing distributions of commercially exploited fish.

Scaling laws of marine predator search behaviour.

Many free-ranging predators have to make foraging decisions with little, if any, knowledge of present resource distribution and availability. The optimal search strategy they should use to maximize encounter rates with prey in heterogeneous natural environments remains a largely unresolved issue in ecology. Lévy walks are specialized random walks giving rise to fractal movement trajectories that may represent an optimal solution for searching complex landscapes. However, the adaptive significance of this putative strategy in response to natural prey distributions remains untested. Here we analyse over a million movement displacements recorded from animal-attached electronic tags to show that diverse marine predators-sharks, bony fishes, sea turtles and penguins-exhibit Lévy-walk-like behaviour close to a theoretical optimum. Prey density distributions also display Lévy-like fractal patterns, suggesting response movements by predators to prey distributions. Simulations show that predators have higher encounter rates when adopting Lévy-type foraging in natural-like prey fields compared with purely random landscapes. This is consistent with the hypothesis that observed search patterns are adapted to observed statistical patterns of the landscape. This may explain why Lévy-like behaviour seems to be widespread among diverse organisms, from microbes to humans, as a 'rule' that evolved in response to patchy resource distributions.

Seasonal migrations of the European sea bass (Dicentrarchus labrax L.) in UK and surrounding waters.

The movements and behaviour of mature European sea bass (Dicentrarchus labrax L.) in UK waters have not been studied extensively since a series of mark-recapture experiments during the 1970s, 80s and 90s. To better understand the timing and extent of seasonal migrations, 171 mature sea bass > 42 cm were internally tagged with floated electronic tags programmed to record temperature and depth, and released in the English Channel, in the southern North Sea and in the Irish Sea. Among the 48 tags returned to date, sea bass were at liberty for 370 ± 337 days and were recovered 172 ± 200 km from their respective release locations. Most tags were recovered from beaches (54%), or via the fishery (44%). A comparison of the reconstructed tracks from returned electronic tags with the recapture locations of 237 mark-recapture returns (6.5%) from 3615 sea bass released between 1970 and 2020 showed strong overlap. Seasonal movements between shallow areas (Q2-Q3) and deeper spawning areas (Q4-Q1) were accompanied by elevated vertical swimming speeds and average water temperatures of 8.5 °C in the English Channel and Irish Sea, but lower temperatures in the North Sea. Movements between the Celtic Sea/Irish Sea and the North Sea and vice versa demonstrate high levels of connectivity in UK waters. We demonstrate that a proportion of sea bass remained resident within the North Sea throughout the year, with a strong suggestion that spawning might be occurring. These data have significant implications for the future sustainable management of sea bass stocks in UK and surrounding waters.

Tidal and circadian patterns of European eel during their spawning migration in the North Sea and the English Channel.

Technological advances in tracking methods enable the mapping of anguillid eel migration routes from continental habitats to their spawning sites in the ocean. However, the behaviour and orientation abilities of anguillids are still poorly understood, and have only rarely been studied on the continental shelf. Here we present the results of a study into the vertical and horizontal movement behaviour of 42 European eels (Anguilla anguilla L.) tagged with electronic tags that migrated through the North Sea and English Channel towards and into the Atlantic Ocean during their spawning migration. We used actograms, periodograms and linear mixed effects models to determine the periodicity and significance of the timing and pattern of vertical movement and activity. Overall, eels had a complex behavioural repertoire that included classical diel vertical migration (DVM), reverse DVM and vertical movement behaviours that synchronized with tidal patterns. All of the eels that were tracked showed one or more of these behaviours during their time at liberty, and many exhibited all of them. We also observed that the eels had a higher horizontal migration speed when the current in the favourable direction was stronger. This, together with the vertical movement synchronized with the tides, suggests the eels adopt selective tidal stream transport. Finally, tracked eels had a higher vertical movement range at night compared to daytime. We hypothesize that these behaviours are driven by bio-energetic efficient movement, navigation and predator avoidance.

Evidence of hybridization between genetically distinct Baltic cod stocks during peak population abundance(s).

Range expansions can lead to increased contact of divergent populations, thus increasing the potential of hybridization events. Whether viable hybrids are produced will most likely depend on the level of genomic divergence and associated genomic incompatibilities between the different entities as well as environmental conditions. By taking advantage of historical Baltic cod (Gadus morhua) otolith samples combined with genotyping and whole genome sequencing, we here investigate the genetic impact of the increased spawning stock biomass of the eastern Baltic cod stock in the mid 1980s. The eastern Baltic cod is genetically highly differentiated from the adjacent western Baltic cod and locally adapted to the brackish environmental conditions in the deeper Eastern basins of the Baltic Sea unsuitable for its marine counterparts. Our genotyping results show an increased proportion of eastern Baltic cod in western Baltic areas (Mecklenburg Bay and Arkona Basin)-indicative of a range expansion westwards-during the peak population abundance in the 1980s. Additionally, we detect high frequencies of potential hybrids (including F1, F2 and backcrosses), verified by whole genome sequencing data for a subset of individuals. Analysis of mitochondrial genomes further indicates directional gene flow from eastern Baltic cod males to western Baltic cod females. Our findings unravel that increased overlap in distribution can promote hybridization between highly divergent populations and that the hybrids can be viable and survive under specific and favourable environmental conditions. However, the observed hybridization had seemingly no long-lasting impact on the continuous separation and genetic differentiation between the unique Baltic cod stocks.

Mapping silver eel migration routes in the North Sea.

Recent developments in tracking technology resulted in the mapping of various marine spawning migration routes of the European eel (Anguilla anguilla). However, migration routes in the North Sea have rarely been studied, despite many large European rivers and hence potential eel growing habitat discharge into the North Sea. In this study, we present the most comprehensive map to date with migration routes by silver European eels in the North Sea and document for the first time successful eel migration through the English Channel. Migration tracks were reconstructed for 42 eels tagged in Belgium and 12 in Germany. Additionally, some eels moved up north to exit the North Sea over the British Isles, confirming the existence of two different routes, even for eels exiting from a single river catchment. Furthermore, we observed a wide range in migration speeds (6.8-45.2 km day-1). We hypothesize that these are likely attributed to water currents, with eels migrating through the English Channel being significantly faster than eels migrating northward.

First direct evidence of adult European eels migrating to their breeding place in the Sargasso Sea.

The European eel (Anguilla anguilla) is critically endangered (according to the most recent IUCN assessment) and has suffered a 95% decline in recruitment since the 1980s, attributed in part to factors occurring during the marine phases of its life-cycle. As an adult, the European eel undertakes the longest spawning migration of all anguillid eels, a distance of 5000 to 10,000 km across the Atlantic Ocean to the Sargasso Sea. However, despite the passage of almost 100 years since Johannes Schmidt proposed the Sargasso Sea as the breeding place of European eels on the basis of larval surveys, no eggs or spawning adults have ever been sampled there to confirm this. Fundamental questions therefore remain about the oceanic migration of adult eels, including navigation mechanisms, the routes taken, timings of arrival, swimming speed and spawning locations. We attached satellite tags to 26 eels from rivers in the Azores archipelago and tracked them for periods between 40 and 366 days at speeds between 3 and 12 km day-1, and provide the first direct evidence of adult European eels reaching their presumed breeding place in the Sargasso Sea.

First tracking of the oceanic spawning migrations of Australasian short-finned eels (Anguilla australis).

Anguillid eel populations have declined dramatically over the last 50 years in many regions of the world, and numerous species are now under threat. A critical life-history phase is migration from freshwater to distant oceans, culminating in a single life-time spawning event. For many anguillids, especially those in the southern hemisphere, mystery still shrouds their oceanic spawning migrations. We investigated the oceanic spawning migrations of the Australasian short-finned eel (Anguilla australis) using pop-up satellite archival tags. Eels were collected from river estuaries (38° S, 142° E) in south-eastern temperate Australia. In 2019, 16 eels were tracked for up to about 5 months, ~ 2620 km from release, and as far north as the tropical Coral Sea (22° S, 155° E) off the north-east coast of Australia. Eels from southern Australia appeared to access deep water off the Australian coast via two main routes: (i) directly east via Bass Strait, or (ii) south-east around Tasmania, which is the shortest route to deep water. Tagged eels exhibited strong diel vertical migrations, alternating between the warm euphotic zone (~ 100-300 m, 15-20 °C) at night and the mesopelagic zone (~ 700-900 m, 6-8 °C) during the day. Marine predators, probably lamnid sharks, tuna, or marine mammals, ended many eel migrations (at least ~ 30%), largely before the eels had left the Australian continental shelf. The long and risky marine migrations of Australasian eels highlight the need for better information on the processes contributing to eel mortality throughout the life cycle, including the impacts of future changes to oceanic currents, predator abundance and direct anthropogenic disturbances.

Redefining the oceanic distribution of Atlantic salmon.

Determining the mechanisms driving range-wide reductions in Atlantic salmon marine survival is hindered by an insufficient understanding of their oceanic ecology and distribution. We attached 204 pop-up satellite archival tags to post-spawned salmon when they migrated to the ocean from seven European areas and maiden North American salmon captured at sea at West Greenland. Individuals migrated further north and east than previously reported and displayed increased diving activity near oceanographic fronts, emphasizing the importance of these regions as feeding areas. The oceanic distribution differed among individuals and populations, but overlapped more between geographically proximate than distant populations. Dissimilarities in distribution likely contribute to variation in growth and survival within and among populations due to spatio-temporal differences in environmental conditions. Climate-induced changes in oceanographic conditions will alter the location of frontal areas and may have stock-specific effects on Atlantic salmon population dynamics, likely having the largest impacts on southern populations.

Horizontal and vertical movements of starry smooth-hound Mustelus asterias in the northeast Atlantic.

Commercial landings of starry smooth-hound Mustelus asterias in northern European seas are increasing, whilst our knowledge of their ecology, behaviour and population structure remains limited. M. asterias is a widely distributed demersal shark, occupying the waters of the southern North Sea and Irish Sea in the north, to at least the southern Bay of Biscay in the south, and is seasonally abundant in UK waters. There are no species-specific management measures for the northeast Atlantic stock, and the complexity of its population structure is not yet fully understood. To address this issue, we deployed both mark-recapture and electronic tags on M. asterias to gain novel insights into its horizontal and vertical movements. Our data suggest that the habitat use of M. asterias changes on a seasonal basis, with associated changes in geographical distribution, depth utilisation and experienced temperature. We report the first direct evidence of philopatry for this species, and also provide initial evidence of sex-biased dispersal and potential metapopulation-like stock structuring either side of the UK continental shelf. Investigations of finer-scale vertical movements revealed clear diel variation in vertical activity. The illustrated patterns of seasonal space-use and behaviour will provide important information to support the stock assessment process and will help inform any future management options.

Assessment of the quality of European silver eels and tentative approach to trace the origin of contaminants - A European overview.

The European eel is critically endangered. Although the quality of silver eels is essential for their reproduction, little is known about the effects of multiple contaminants on the spawning migration and the European eel management plan does not take this into account. To address this knowledge gap, we sampled 482 silver eels from 12 catchments across Europe and developed methods to assess three aspects of eel quality: muscular lipid content (N = 169 eels), infection with Anguillicola crassus (N = 482), and contamination by persistent organic pollutants (POPs, N = 169) and trace elements (TEs, N = 75). We developed a standardized eel quality risks index (EQR) using these aspects for the subsample of 75 female eels. Among 169 eels, 33% seem to have enough muscular lipids content to reach the Sargasso Sea to reproduce. Among 482 silver eels, 93% were infected by A. crassus at least once during their lifetime. All contaminants were above the limit of quantification, except the 1,2-bis(2,4,6-tribromophenoxy)ethane (BTBPE), Ag and V. The contamination by POPs was heterogeneous between catchments while TEs were relatively homogeneous, suggesting a multi-scale adaptation of management plans. The EQR revealed that eels from Warwickshire were most impacted by brominated flame-retardants and agricultural contaminants, those from Scheldt were most impacted by agricultural and construction activities, PCBs, coal burning, and land use, while Frémur eels were best characterized by lower lipid contents and high parasitic and BTBPE levels. There was a positive correlation between EQR and a human footprint index highlighting the capacity of silver eels for biomonitoring human activities and the potential impact on the suitability of the aquatic environment for eel population health. EQR therefore represents a step forward in the standardization and mapping of eel quality risks, which will help identify priorities and strategies for restocking freshwater ecosystems.

Ocean predation and mortality of adult Atlantic salmon.

Predation and mortality are often difficult to estimate in the ocean, which hampers the management and conservation of marine fishes. We used data from pop-up satellite archival tags to investigate the ocean predation and mortality of adult Atlantic salmon (Salmo salar) released from 12 rivers flowing into the North Atlantic Ocean. Data from 156 tagged fish revealed 22 definite predation events (14%) and 38 undetermined mortalities (24%). Endothermic fish were the most common predators (n = 13), with most of these predation events occurring in the Gulf of St. Lawrence and from the Bay of Biscay to the Irish Shelf. Predation by marine mammals, most likely large deep-diving toothed whales (n = 5), and large ectothermic fish (n = 4) were less frequent. Both the estimated predation rates (ZP) and total mortality rates (ZM) where higher for Atlantic salmon from Canada, Ireland, and Spain (ZP = 0.60-1.32 y-1, ZM = 1.73-3.08 y-1) than from Denmark and Norway (ZP = 0-0.13 y-1, ZM = 0.19-1.03 y-1). This geographical variation in ocean mortality correlates with ongoing population declines, which are more profound for southern populations, indicating that low ocean survival of adults may act as an additional stressor to already vulnerable populations.

Translating Marine Animal Tracking Data into Conservation Policy and Management.

There have been efforts around the globe to track individuals of many marine species and assess their movements and distribution, with the putative goal of supporting their conservation and management. Determining whether, and how, tracking data have been successfully applied to address real-world conservation issues is, however, difficult. Here, we compile a broad range of case studies from diverse marine taxa to show how tracking data have helped inform conservation policy and management, including reductions in fisheries bycatch and vessel strikes, and the design and administration of marine protected areas and important habitats. Using these examples, we highlight pathways through which the past and future investment in collecting animal tracking data might be better used to achieve tangible conservation benefits.

Scaling marine fish movement behavior from individuals to populations.

Understanding how, where, and when animals move is a central problem in marine ecology and conservation. Key to improving our knowledge about what drives animal movement is the rising deployment of telemetry devices on a range of free-roaming species. An increasingly popular way of gaining meaningful inference from an animal's recorded movements is the application of hidden Markov models (HMMs), which allow for the identification of latent behavioral states in the movement paths of individuals. However, the use of HMMs to explore the population-level consequences of movement is often limited by model complexity and insufficient sample sizes. Here, we introduce an alternative approach to current practices and provide evidence of how the inclusion of prior information in model structure can simplify the application of HMMs to multiple animal movement paths with two clear benefits: (a) consistent state allocation and (b) increases in effective sample size. To demonstrate the utility of our approach, we apply HMMs and adapted HMMs to over 100 multivariate movement paths consisting of conditionally dependent daily horizontal and vertical movements in two species of demersal fish: Atlantic cod (Gadus morhua; n = 46) and European plaice (Pleuronectes platessa; n = 61). We identify latent states corresponding to two main underlying behaviors: resident and migrating. As our analysis considers a relatively large sample size and states are allocated consistently, we use collective model output to investigate state-dependent spatiotemporal trends at the individual and population levels. In particular, we show how both species shift their movement behaviors on a seasonal basis and demonstrate population space use patterns that are consistent with previous individual-level studies. Tagging studies are increasingly being used to inform stock assessment models, spatial management strategies, and monitoring of marine fish populations. Our approach provides a promising way of adding value to tagging studies because inferences about movement behavior can be gained from a larger proportion of datasets, making tagging studies more relevant to management and more cost-effective.

Warm water occupancy by North Sea cod.

The North Sea has warmed in recent years and there is an ongoing debate into how this is affecting the distribution of fishes and other marine organisms. Of particular interest is the commercially important Atlantic cod (Gadus morhua L.), which has declined sharply in abundance in the North Sea over the past 20 years. Observations of the temperature experienced by 129 individual cod throughout the North Sea were made during a large-scale electronic tagging programme conducted between 1999 and 2005. We asked whether individual cod fully occupied the thermal habitat available to them. To this end, we compared the temperature experience of cod with independently measured contemporaneous sea-bottom temperature data. The majority of cod experienced a warmer fraction of the sea than was potentially available to them. By summer, most of the individuals in the south experienced temperatures considered superoptimal for growth. Cooler waters were within the reach of the cod and a small number of individuals migrated to areas that allowed them to experience lower temperatures, indicating that the cod had the capacity to find cooler water. Most did not, however, suggesting that the changing thermal regime of the North Sea is not yet causing adult cod to move to cooler waters.

Flexible foraging movements of leatherback turtles across the North Atlantic Ocean.

Some marine species have been shown to target foraging at particular hotspots of high prey abundance. However, we show here that in the year after a nesting season, female leatherback turtles (Dermochelys coriacea) in the Atlantic generally spend relatively little time in fixed hotspots, especially those with a surface signature revealed in satellite imagery, but rather tend to have a pattern of near continuous traveling. Associated with this traveling, distinct changes in dive behavior indicate that turtles constantly fine tune their foraging behavior and diel activity patterns in association with local conditions. Switches between nocturnal vs. diurnal activity are rare in the animal kingdom but may be essential for survival on a diet of gelatinous zooplankton where patches of high prey availability are rare. These results indicate that in their first year after nesting, leatherback turtles do not fit the general model of migration where responses to resources are suppressed during transit. However, their behavior may be different in their sabbatical years away from nesting beaches. Our results highlight the importance of whole-ocean fishing gear regulations to minimize turtle bycatch.

First evidence of European eels exiting the Mediterranean Sea during their spawning migration.

The migration route and the spawning site of the European eel Anguilla anguilla are still uncertain. It has been suggested that the Mediterranean eel stock does not contribute to spawning because there is no evidence of eels leaving the Mediterranean Sea. To test this hypothesis, we equipped eight female silver eels from the south of France with pop-up satellite tags during escapement from coastal waters. Once in deeper water, the eels quickly established diel vertical migration (DVM) between the upper and lower mesopelagic zone. Five tagged eels were taken by predators within the Mediterranean, but two eels reached the Atlantic Ocean after six months and at distances greater than 2000 km from release. These eels ceased their DVM while they negotiated the Gibraltar Strait, and remained in deep water until they reached the Atlantic Ocean, when they recommenced DVM. Our results are the first to show that eels from Mediterranean can cross the Strait of Gibraltar and continue their migration into the Atlantic Ocean. This finding suggests that Mediterranean countries, as for other EU states, have an important role to play in contributing to conservation efforts for the recovery of the European eel stock.