Stabilizing selection on Atlantic cod supergenes through a millennium of extensive exploitation.

Life on Earth has been characterized by recurring cycles of ecological stasis and disruption, relating biological eras to geological and climatic transitions through the history of our planet. Due to the increasing degree of ecological abruption caused by human influences many advocate that we now have entered the geological era of the Anthropocene, or "the age of man." Considering the ongoing mass extinction and ecosystem reshuffling observed worldwide, a better understanding of the drivers of ecological stasis will be a requisite for identifying routes of intervention and mitigation. Ecosystem stability may rely on one or a few keystone species, and the loss of such species could potentially have detrimental effects. The Atlantic cod (Gadus morhua) has historically been highly abundant and is considered a keystone species in ecosystems of the northern Atlantic Ocean. Collapses of cod stocks have been observed on both sides of the Atlantic and reported to have detrimental effects that include vast ecosystem reshuffling. By whole-genome resequencing we demonstrate that stabilizing selection maintains three extensive "supergenes" in Atlantic cod, linking these genes to species persistence and ecological stasis. Genomic inference of historic effective population sizes shows continued declines for cod in the North Sea-Skagerrak-Kattegat system through the past millennia, consistent with an early onset of the marine Anthropocene through industrialization and commercialization of fisheries throughout the medieval period.

Movement diversity and partial sympatry of coastal and Northeast Arctic cod ecotypes at high latitudes.

Movement diversity within species represent an important but often neglected, component of biodiversity that affects ecological and genetic interactions, as well as the productivity of exploited systems. By combining individual tracking data from acoustic telemetry with novel genetic analyses, we describe the movement diversity of two Atlantic cod Gadus morhua ecotypes in two high-latitude fjord systems: the highly migratory Northeast Arctic cod (NEA cod) that supports the largest cod fishery in the world, and the more sedentary Norwegian coastal cod, which is currently in a depleted state. As predicted, coastal cod displayed a higher level of fjord residency than NEA cod. Of the cod tagged during the spawning season, NEA cod left the fjords permanently to a greater extent and earlier compared to coastal cod, which to a greater extent remained resident and left the fjords temporarily. Despite this overall pattern, horizontal movements atypical for the ecotypes were common with some NEA cod remaining within the fjords year-round and some coastal cod displaying a low fjord fidelity. Fjord residency and exit timing also differed with spawning status and body size, with spawning cod and large individuals tagged during the feeding season more prone to leave the fjords and earlier than non-spawning and smaller individuals. While our results confirm a lower fjord dependency for NEA cod, they highlight a movement diversity within each ecotype and sympatric residency between ecotypes, previously undetected by population-level monitoring. This new knowledge is relevant for the management, which should base their fisheries advice for these interacting ecotypes on their habitat use and seasonal movements.

Protection from fishing improves body growth of an exploited species.

Hunting and fishing are often size-selective, which favours slow body growth. In addition, fast growth rate has been shown to be positively correlated with behavioural traits that increase encounter rates and catchability in passive fishing gears such as baited traps. This harvest-induced selection should be effectively eliminated in no-take marine-protected areas (MPAs) unless strong density dependence results in reduced growth rates. We compared body growth of European lobster (Homarus gammarus) between three MPAs and three fished areas. After 14 years of protection from intensive, size-selective lobster fisheries, the densities in MPAs have increased considerably, and we demonstrate that females moult more frequently and grow more during each moult in the MPAs. A similar, but weaker pattern was evident for males. This study suggests that MPAs can shield a wild population from slow-growth selection, which can explain the rapid recovery of size structure following implementation. If slow-growth selection is a widespread phenomenon in fisheries, the effectiveness of MPAs as a management tool can be higher than currently anticipated.

Sea temperature effects on depth use and habitat selection in a marine fish community.

Understanding the responses of aquatic animals to temperature variability is essential to predict impacts of future climate change and to inform conservation and management. Most ectotherms such as fish are expected to adjust their behaviour to avoid extreme temperatures and minimize acute changes in body temperature. In coastal Skagerrak, Norway, sea surface temperature (SST) ranges seasonally from 0 to over 20°C, representing a challenge to the fish community which includes cold-, cool- and warm-water affinity species. By acoustically tracking 111 individuals of Atlantic cod Gadus morhua, pollack Pollachius pollachius and ballan wrasse Labrus bergylta in 2015-2018, we examined how coexisting species within a fish community adjusted their behaviour (i.e. vertical distribution in the water column and habitat selection) to cope with the thermal variation. Mixed-effect models showed that thermal preference was a main driver of behaviour and habitat use of the fish community in a southern Norwegian fjord. Cod used colder waters, compared with pollack and ballan wrasse. Increases in SST during summer were associated with the use of deeper, colder waters by cod, especially by larger individuals, and conversely with the occupancy of shallower areas by pollack and ballan wrasse. During winter, when SST dropped and the thermal stratification reversed, pollack and ballan wrasse moved to deeper, relatively warmer areas, while cod selected shallower, colder habitats. Although habitat selection was affected by temperature, species-specific habitat selection was observed even when temperature was similar throughout habitats. This study shows how cohabiting fish species respond to thermal heterogeneity, suggesting that (a) temperature regulates the access to the different depths and habitats and (b) behavioural plasticity may be an important factor for coping with temperature variability and potentially for adaptation to climate change.

Fishing pressure impacts the abundance gradient of European lobsters across the borders of a newly established marine protected area.

Marine protected areas (MPAs) are considered viable fisheries management tools due to their potential benefits of adult spillover and recruitment subsidy to nearby fisheries. However, before-after control-impact studies that explore the biological and fishery effects of MPAs to surrounding fisheries are scarce. We present results from a fine-scale spatial gradient study conducted before and after the implementation of a 5 km2 lobster MPA in southern Norway. A significant nonlinear response in lobster abundance, estimated as catch-per-unit-effort (CPUE) from experimental fishing, was detected within 2 years of protection. After 4 years, CPUE values inside the MPA had increased by a magnitude of 2.6 compared to before-protection values. CPUE showed a significant nonlinear decline from the centre of the MPA, with a depression immediately outside the border and a plateau in fished areas. Overall fishing pressure almost doubled over the course of the study. The highest increase in fishing pressure (by a magnitude of 3) was recorded within 1 km of the MPA border, providing a plausible cause for the depression in CPUE. Taken together, these results demonstrate the need to regulate fishing pressure in surrounding areas when MPAs are implemented as fishery management tools.

The Pillars of Hercules as a bathymetric barrier to gene flow promoting isolation in a global deep-sea shark (Centroscymnus coelolepis).

Knowledge of the mechanisms limiting connectivity and gene flow in deep-sea ecosystems is scarce, especially for deep-sea sharks. The Portuguese dogfish (Centroscymnus coelolepis) is a globally distributed and near threatened deep-sea shark. C. coelolepis population structure was studied using 11 nuclear microsatellite markers and a 497-bp fragment from the mtDNA control region. High levels of genetic homogeneity across the Atlantic (Φ(ST) = -0.0091, F(ST) = 0.0024, P > 0.05) were found suggesting one large population unit at this basin. The low levels of genetic divergence between Atlantic and Australia (Φ(ST) = 0.0744, P < 0.01; F(ST) = 0.0015, P > 0.05) further suggested that this species may be able to maintain some degree of genetic connectivity even across ocean basins. In contrast, sharks from the Mediterranean Sea exhibited marked genetic differentiation from all other localities studied (Φ(ST) = 0.3808, F(ST) = 0.1149, P < 0.001). This finding suggests that the shallow depth of the Strait of Gibraltar acts as a barrier to dispersal and that isolation and genetic drift may have had an important role shaping the Mediterranean shark population over time. Analyses of life history traits allowed the direct comparison among regions providing a complete characterization of this shark's populations. Sharks from the Mediterranean had markedly smaller adult body size and size at maturity compared to Atlantic and Pacific individuals. Together, these results suggest the existence of an isolated and unique population of C. coelolepis inhabiting the Mediterranean that most likely became separated from the Atlantic in the late Pleistocene.

Continuous sound from a marine vibrator causes behavioural responses of free-ranging, spawning Atlantic cod (Gadus morhua).

Marine vibrators are a new technology being developed for seismic surveys. These devices can transmit continuous instead of impulsive sound and operate over a narrower frequency band and at lower peak pressure than airguns, which is assumed to reduce their environmental impacts. We exposed spawning Atlantic cod (Gadus morhua) to sound produced by a prototype, but full-scale, marine vibrator, and monitored behavioural responses of tagged cod using acoustic telemetry. Fish were exposed to 10 × 3 h continuous sound treatments over a 4-day period using a randomised-block design. Sound exposure levels were comparable to airgun exposure experiments conducted previously with the same set-up ranging from ∼115 to 145 dB re 1 µPa2s during exposure. Telemetry data were used to assess 1) whether marine vibrator exposure displaced cod from the spawning ground, through estimation of residence and survival probabilities, and 2) fine-scale behavioural responses within the test site, namely swimming depth, activity levels, displacement, and home ranges. Forty-two spawning cod were tagged prior to the exposure, with 22 present during the exposure. All 22 tags were equipped with pressure sensors and ten of these additionally with accelerometers. While no premature departure from the spawning site was observed, cod reacted to the exposure by decreasing their activity levels (by up to 50%, SE = 7%) and increasing their swimming depth (by up to 2.5 m, SE = 1.0 m) within the test site during the exposure period. These behavioural responses varied by sex and time of day. Cod reactions to a marine vibrator may be more pronounced than reactions to airguns, possibly because continuous sound is more disturbing to fish than intermittent sound at the same exposure levels. However, given sample size limitations of the present study, further studies with continuous sound are necessary to fully understand its impact and biological significance.

Lobster and cod benefit from small-scale northern marine protected areas: inference from an empirical before-after control-impact study.

Marine protected areas (MPAs) are increasingly implemented as tools to conserve and manage fisheries and target species. Because there are opportunity costs to conservation, there is a need for science-based assessment of MPAs. Here, we present one of the northernmost documentations of MPA effects to date, demonstrated by a replicated before-after control-impact (BACI) approach. In 2006, MPAs were implemented along the Norwegian Skagerrak coast offering complete protection to shellfish and partial protection to fish. By 2010, European lobster (Homarus gammarus) catch-per-unit-effort (CPUE) had increased by 245 per cent in MPAs, whereas CPUE in control areas had increased by 87 per cent. Mean size of lobsters increased by 13 per cent in MPAs, whereas increase in control areas was negligible. Furthermore, MPA-responses and population development in control areas varied significantly among regions. This illustrates the importance of a replicated BACI design for reaching robust conclusions and management decisions. Partial protection of Atlantic cod (Gadus morhua) was followed by an increase in population density and body size compared with control areas. By 2010, MPA cod were on average 5 cm longer than in any of the control areas. MPAs can be useful management tools in rebuilding and conserving portions of depleted lobster populations in northern temperate waters, and even for a mobile temperate fish species such as the Atlantic cod.

Large females connect Atlantic cod spawning sites.

The Earth's ecosystems are increasingly deprived of large animals. Global simulations suggest that this downsizing of nature has serious consequences for biosphere functioning. However, the historical loss of large animals means that it is now often impossible to secure empirical data revealing their true ecological importance. We tracked 465 mature Atlantic cod (Gadus morhua) during their winter spawning season and show that large females (up to 114 centimeters in length), which are still found in mid-Norway, were characterized by more complex movement networks compared with smaller females. Large males were sparse but displayed similar movement patterns. Our finding implies that management programs promoting large fish will have positive impacts on population resilience by facilitating the continued use of a diversity of spawning habitats and the connectivity between them.

Contrasting management regimes indicative of mesopredator release in temperate coastal fish assemblages.

The absence of functional top predators has been proposed as a mechanism acting to shape fish assemblages in temperate marine ecosystems, with cascading effects on lower trophic levels. We explore this scenario by comparing the trophic and functional status of fish assemblages in Norwegian marine national parks, open to fishing, to a nearby coastal seascape that harbors a system of marine protected areas (MPAs) including a no-take zone. Demersal fish assemblages were sampled using fyke nets over three consecutive seasons. Atlantic cod (Gadus morhua) is potentially a dominant top predator in this ecosystem, and historically, this and other gadids have been targeted by the full range of former and present fisheries. In the present study, we find that average body size of the Atlantic cod was significantly larger in the zoned seascape compared to the unprotected areas (mean ± SD: 36.6 cm ± 14.38 vs. 23.4 ± 7.50; p < .001) and that the unprotected seascape was characterized by a higher abundance of mesopredator fish species. These observations are consistent with the hypothesis that the protection of top predators within MPAs aids to control the mesopredator populations and provides empirical support to the notion that the present state of many coastal fish assemblages is driven by mesopredator release linked to functional depletion of large top predators.

Technological creep masks continued decline in a lobster (Homarus gammarus) fishery over a century.

Fishery-dependent data are frequently used to inform management decisions. However, inferences about stock development based on commercial data such as Catch-Per-Unit-Effort (CPUE) can be severely biased due to a phenomenon known as technological creep, where fishing technology improves over time. Here we show how trap improvement over nine decades has driven technological creep in a European lobster (Homarus gammarus) fishery. We combined fishing data, experimental fishing with contemporary and older trap types, and information on depletion effects during fishing seasons. The resulting standardized CPUE time series indicates a 92% decline in lobster abundance between 1928 and 2019 compared to 70% if technological creep is not corrected for. Differences are most pronounced within the last 40 years when the most substantial shift in gear technology occurred: an uncorrected CPUE index suggests an 8% increase in lobster abundance during this period, while the corrected CPUE index declined by 57%. We conclude that technological creep has masked a continuous stock decline, particularly in recent decades and largely driven by the shift from one- to two-chambered traps, as well as the ability of newer trap designs to capture larger lobsters. Our study confirms the importance of adequate standardization, including technological development, when using fishery dependent CPUE for monitoring and management of data-limited fisheries.

Spawning stock and recruitment in North Sea cod shaped by food and climate.

In order to provide better fisheries management and conservation decisions, there is a need to discern the underlying relationship between the spawning stock and recruitment of marine fishes, a relationship which is influenced by the environmental conditions. Here, we demonstrate how the environmental conditions (temperature and the food availability for fish larvae) influence the stock-recruitment relationship and indeed what kind of stock-recruitment relationship we might see under different environmental conditions. Using unique zooplankton data from the Continuous Plankton Recorder, we find that food availability (i.e. zooplankton) in essence determines which model applies for the once large North Sea cod (Gadus morhua) stock. Further, we show that recruitment is strengthened during cold years and weakened during warm years. Our combined model explained 45 per cent of the total variance in cod recruitment, while the traditional Ricker and Beverton-Holt models only explained about 10 per cent. Specifically, our approach predicts that a full recovery of the North Sea cod stock might not be expected until the environment becomes more favourable.

Pathogen-induced rapid evolution in a vertebrate life-history trait.

Anthropogenic factors, including climate warming, are increasing the incidence and prevalence of infectious diseases worldwide. Infectious diseases caused by pathogenic parasites can have severe impacts on host survival, thereby altering the selection regime and inducing evolutionary responses in their hosts. Knowledge about such evolutionary consequences in natural populations is critical to mitigate potential ecological and economic effects. However, studies on pathogen-induced trait changes are scarce and the pace of evolutionary change is largely unknown, particularly in vertebrates. Here, we use a time series from long-term monitoring of perch to estimate temporal trends in the maturation schedule before and after a severe pathogen outbreak. We show that the disease induced a phenotypic change from a previously increasing to a decreasing size at maturation, the most important life-history transition in animals. Evolutionary rates imposed by the pathogen were high and comparable to those reported for populations exposed to intense human harvesting. Pathogens thus represent highly potent drivers of adaptive phenotypic evolution in vertebrates.

Selection on fish personality differs between a no-take marine reserve and fished areas.

Marine reserves can protect fish populations by increasing abundance and body size, but less is known about the effect of protection on fish behaviour. We looked for individual consistency in movement behaviours of sea trout in the marine habitat using acoustic telemetry to investigate whether they represent personality traits and if so, do they affect survival in relation to protection offered by a marine reserve. Home range size had a repeatability of 0.21, suggesting that it represents a personality trait, while mean swimming depth, activity and diurnal vertical migration were not repeatable movement behaviours. The effect of home range size on survival differed depending on the proportion of time fish spent in the reserve, where individuals spending more time in the reserve experienced a decrease in survival with larger home ranges while individuals spending little time in the reserve experienced an increase in survival with larger home ranges. We suggest that the diversity of fish home range sizes could be preserved by establishing networks of marine reserves encompassing different habitat types, ensuring both a heterogeneity in environmental conditions and fishing pressure.

Disparate movement behavior and feeding ecology in sympatric ecotypes of Atlantic cod.

Coexistence of ecotypes, genetically divergent population units, is a widespread phenomenon, potentially affecting ecosystem functioning and local food web stability. In coastal Skagerrak, Atlantic cod (Gadus morhua) occur as two such coexisting ecotypes. We applied a combination of acoustic telemetry, genotyping, and stable isotope analysis to 72 individuals to investigate movement ecology and food niche of putative local "Fjord" and putative oceanic "North Sea" ecotypes-thus named based on previous molecular studies. Genotyping and individual origin assignment suggested 41 individuals were Fjord and 31 were North Sea ecotypes. Both ecotypes were found throughout the fjord. Seven percent of Fjord ecotype individuals left the study system during the study while 42% of North Sea individuals left, potentially homing to natal spawning grounds. Home range sizes were similar for the two ecotypes but highly variable among individuals. Fjord ecotype cod had significantly higher δ13C and δ15N stable isotope values than North Sea ecotype cod, suggesting they exploited different food niches. The results suggest coexisting ecotypes may possess innate differences in feeding and movement ecologies and may thus fill different functional roles in marine ecosystems. This highlights the importance of conserving interconnected populations to ensure stable ecosystem functioning and food web structures.

Marine protected areas rescue a sexually selected trait in European lobster.

Marine protected areas (MPAs) are increasingly implemented worldwide to maintain and restore depleted populations. However, despite our knowledge on the myriad of positive responses to protection, there are few empirical studies on the ability to conserve species' mating patterns and secondary sexual traits. In male European lobsters (Homarus gammarus), the size of claws relative to body size correlates positively with male mating success and is presumably under sexual selection. At the same time, an intensive trap fishery exerts selection against large claws in males. MPAs could therefore be expected to resolve these conflicting selective pressures and preserve males with large claws. We explored this hypothesis by contrasting claw size of males and females in three pairs of MPAs and nearby fished areas in southern Norway. By finding that male lobsters have up to 8% larger claws inside MPAs compared to similarly sized males in fished areas, our study provides evidence that MPAs rescue a secondary sexual trait. Recovery from harvest selection acting on claws is the most likely explanation; however, the higher abundance of lobster inside MPAs does not rule out a plastic response on claw size due to increased competition. Regardless of the underlying cause, our study demonstrates (a) the value of protected areas as a management tool for mitigating fisheries-induced evolution and (b) that MPAs help maintaining the scope for sexual selection in populations with vulnerable life histories and complex mating system.

Nine decades of decreasing phenotypic variability in Atlantic cod.

Changes in phenotypic variability in natural populations have received little attention in comparison with changes in mean trait values. This is unfortunate because trait diversity may influence adaptive evolutionary change and population stability. We combine two unique data sets to illuminate complex trait changes in Atlantic cod along the Norwegian Skagerrak coast: (i) an annual beach seine survey starting in 1919, monitoring juvenile body size and abundance and (ii) capture-mark-recapture data from which we estimated selection on juvenile body size and growth. We demonstrate that the variability of juvenile size has been steadily decreasing across nine decades, with no evidence for a similar trend in mean size. We also report that small, slow-growing fish as well as large, fast-growing fish are selected against. Together, these results suggest long-term stabilizing selection acting on Atlantic cod, and emphasize the need for further studies evaluating the full complexity of trait changes in wild populations.

Migratory passage structures at hydropower plants as potential physiological and behavioural selective agents.

Anthropogenic activities affect fish populations worldwide. River dams have profound impacts on ecosystems by changing habitats and hindering migration. In an effort to counteract such effects, a range of mitigation measures have been installed at hydroelectric power plants. However, not all individuals in a population use these measures, potentially creating strong selection processes at hydroelectric power plants. This may be especially true during migration; fish can get heavily delayed or pass through a hydropower turbine, thus facing increased mortality compared with those using a safe bypass route. In this study, we quantify migration route choices of descending wild passive integrated transponder (PIT)-tagged Atlantic salmon smolts released upstream from a hydroelectric plant. We demonstrate how only a few metres' displacement of bypass canals can have a large impact on the fish guidance efficiency (FGE). The proportion of fish using the bypasses increased from 1% to 34% when water was released in surface gates closer to the turbine intake. During a period of low FGE, we observed two different smolt migratory strategies. While some individuals spent little time in the forebay before migrating through the turbine tunnel, others remained there. We suggest that these groups represent different behavioural types, and that suboptimal mitigation measures at hydropower intakes may, therefore, induce strong selection on salmon behavioural traits. The ultimate outcome of these selection mechanisms is discussed in light of potential trade-offs between turbine migration mortality coast and optimal sea entrance timing survival benefits.

Potential of a no-take marine reserve to protect home ranges of anadromous brown trout (Salmo trutta).

The extent to which no-take marine reserves can benefit anadromous species requires examination. Here, we used acoustic telemetry to investigate the spatial behavior of anadromous brown trout (sea trout, Salmo trutta) in relation to a small marine reserve (~1.5 km2) located inside a fjord on the Norwegian Skagerrak coast. On average, sea trout spent 42.3 % (±5.0% SE) of their time in the fjord within the reserve, a proportion similar to the area of the reserve relative to that of the fjord. On average, sea trout tagged inside the reserve received the most protection, although the level of protection decreased marginally with increasing home range size. Furthermore, individuals tagged outside the reserve received more protection with increasing home range size, potentially opposing selection toward smaller home range sizes inflicted on fish residing within reserves, or through selective fishing methods like angling. Monthly sea trout home ranges in the marine environment were on average smaller than the reserve, with a mean of 0.430 (±0.0265 SE) km2. Hence, the reserve is large enough to protect the full home range of some individuals residing in the reserve. Synthesis and applications: In general, the reserve protects sea trout to a varying degree depending on their individual behavior. These findings highlight evolutionary implications of spatial protection and can guide managers in the design of marine reserves and networks that preserve variation in target species' home range size and movement behavior.

Harvest Pressure on Coastal Atlantic Cod (Gadus morhua) from Recreational Fishing Relative to Commercial Fishing Assessed from Tag-Recovery Data.

Marine recreational fishing is a popular outdoor activity. However, knowledge about the magnitude of recreational catches relative to commercial catches in coastal fisheries is generally sparse. Coastal Atlantic cod (Gadus morhua) is a target species for recreational fishers in the North Atlantic. In Norway, recreational fishers are allowed to use a variety of traps and nets as well as long-line and rod and line when fishing for cod. From 2005 to 2013, 9729 cod (mean size: 40 cm, range: 15-93 cm) were tagged and released in coastal Skagerrak, southeast Norway. Both high-reward (NOK 500) and low-reward tags (NOK 50) were used in this study. Because some harvested fish (even those posting high-reward tags) may go unreported by fishers, reporting rates were estimated from mark-recovery models that incorporate detection parameters in their structure, in addition to survival and mortality estimates. During 2005 to 2013, a total of 1707 tagged cod were recovered and reported by fishers. We estimate the overall annual survival to be 33% (SE 1.5). Recreational rod and line fishing were responsible for 33.7% (SE 2.4) of total mortality, followed by commercial fisheries (15.1% SE 0.8) and recreational fixed gear (6.8% SE 0.4). Natural mortality was 44.4% (SE 2.5) of total mortality. Our findings suggest that recreational fishing-rod and line fishing in particular-is responsible for a substantial part of fishing mortality exerted on coastal cod in southern Norway.