Divergent responses of pelagic and benthic fish body-size structure to remoteness and protection from humans.

Animal body-size variation influences multiple processes in marine ecosystems, but habitat heterogeneity has prevented a comprehensive assessment of size across pelagic (midwater) and benthic (seabed) systems along anthropic gradients. In this work, we derive fish size indicators from 17,411 stereo baited-video deployments to test for differences between pelagic and benthic responses to remoteness from human pressures and effectiveness of marine protected areas (MPAs). From records of 823,849 individual fish, we report divergent responses between systems, with pelagic size structure more profoundly eroded near human markets than benthic size structure, signifying greater vulnerability of pelagic systems to human pressure. Effective protection of benthic size structure can be achieved through MPAs placed near markets, thereby contributing to benthic habitat restoration and the recovery of associated fishes. By contrast, recovery of the world's largest and most endangered fishes in pelagic systems requires the creation of highly protected areas in remote locations, including on the High Seas, where protection efforts lag.

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.

Atlantic cod individual spatial behaviour and stable isotope associations in a no-take marine reserve.

Foraging is a behavioural process and, therefore, individual behaviour and diet are theorized to covary. However, few comparisons of individual behaviour type and diet exist in the wild. We tested whether behaviour type and diet covary in a protected population of Atlantic cod, Gadus morhua. Working in a no-take marine reserve, we could collect data on natural behavioural variation and diet choice with minimal anthropogenic disturbance. We inferred behaviour using acoustic telemetry and diet from stable isotope compositions (expressed as δ13 C and δ15 N values). We further investigated whether behaviour and diet could have survival costs. We found cod with shorter diel vertical migration distances fed at higher trophic levels. Cod δ13 C and δ15 N values scaled positively with body size. Neither behaviour nor diet predicted survival, indicating phenotypic diversity is maintained without survival costs for cod in a protected ecosystem. The links between diet and diel vertical migration highlight that future work is needed to understand whether the shifts in this behaviour during environmental change (e.g. fishing or climate), could lead to trophic cascades.

Eco-evolutionary dynamics of Atlantic cod spatial behavior maintained after the implementation of a marine reserve.

The effects of marine reserves on the life history and demography of the protected populations are well-established, typically increasing population density and body size. However, little is known about how marine reserves may alter the behavior of the populations that are the target of protection. In theory, marine reserves can relax selection on spatial behavioral phenotypes that were previously targeted by the fishery and also drive selection in favor of less mobile individuals. In this study, we used acoustic telemetry to monitor the individual spatial behavior of 566 Atlantic cod (Gadus morhua Linnaeus, 1758) moving within a marine reserve and a control site in southern Norway, starting 1 year before the implementation of the marine reserve and lasting up to 9 years after. Following a before-after-control-impact approach, we investigated changes in (1) survival, (2) selection acting on behavioral traits, and (3) mean behavioral phenotypes, after the implementation of the marine reserve. We focused on three behavioral traits commonly used to describe the mobility of aquatic animals: home range size, depth position, and diel vertical migration range. Survival increased after reserve implementation, but contrary to our expectations, it subsequently decreased to preprotection levels after just 3 years. Further, we found no significance in selection patterns acting on any of the three behavioral traits after reserve implementation. Although some changes related to water column use (the tendency to occupy deeper waters) were observed in the marine reserve after 9 years, they cannot unequivocally be attributed to protection. Our results show that survival and behavioral responses to marine reserves in some cases may be more complex than previously anticipated and highlight the need for appropriately scaled management experiments and more integrated approaches to understand the effects of marine protected areas on harvested aquatic species.

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.

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.

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.

Depletion of coastal predatory fish sub-stocks coincided with the largest sea urchin grazing event observed in the NE Atlantic.

In this contribution, we propose fishery driven predator release as the cause for the largest grazing event ever observed in the NE Atlantic. Based on the evolving appreciation of limits to population connectivity, published and previously unpublished data, we discuss whether overfishing caused a grazer bloom of the sea urchin (Strongylocentrotus droebachiensis) resulting in overgrazing of more than 2000 km2 kelp (Laminaria hyperborea) forest along Norwegian and Russian coasts during the 1970 s. We show that coastal fisheries likely depleted predatory coastal fish stocks through modernization of fishing methods and fleet. These fish were important predators on urchins and the reduction coincided with the urchin bloom. From this circumstantial evidence, we hypothesize that coastal predatory fish were important in regulating sea urchins, and that a local population dynamics perspective is necessary in management of coastal ecosystems.

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.

Protected areas buffer against harvest selection and rebuild phenotypic complexity.

Harvest mortality typically truncates the harvested species' size structure, thereby reducing phenotypic complexity, which can lead to reduced population productivity, increased population variability, and selection on an array of life history traits that can further alter these demographic processes. Marine protected areas (MPAs) are a potential tool to protect older, larger individuals and therefore mitigate such ecological and evolutionary effects of harvest, depending on the degree of connectivity among areas. Such MPA protection relies on a shift in size-dependent mortality, the measurement of which can therefore serve as an early indicator of whether MPAs might achieve the desired longer-term ecological and evolutionary responses. We directly measured MPA effects on size-selective mortality and associated size structure using mark-recapture data on European lobster (Homarus gammarus) collected at three MPA-control area pairs in southern Norway during one decade (n = 5,943). Mark-recapture modeling, accounting for variation in recapture probabilities, revealed (1) that annual mean survival was higher inside MPAs (0.592) vs. control areas (0.298) and (2) that significant negative relationships between survival and body size occurred at the control areas but not in the MPAs, where the effect of body size was predominantly positive. Additionally, we found (3) that mean and maximum body size increased over time inside MPAs but not in control areas. Overall, our results suggest that MPAs can rebuild phenotypic complexity (i.e., size structure) and provide protection from harvest selection.

Harvest selection on multiple traits in the wild revealed by aquatic animal telemetry.

Harvesting can have profound impacts on the ecology and evolution of marine populations. However, little is known about the strength and direction of fisheries-induced selection acting on multiple traits in the wild. Here, we used acoustic telemetry to directly monitor individual behavior and fate in an intensively harvested species, the European lobster (Homarus gammarus, n = 100), in southern Norway. Overall, 24% of the tracked lobsters survived the two-month harvest season within the study area. Our results indicated that local survival was not random with respect to phenotype. We found no clear support for fisheries-induced selection acting directly on body size. However, lobsters with large crusher claws relative to their body size, typical of socially dominant individuals, appeared at higher risk of being captured in the conventional trap fishery. We also detected a fine-scale spatial gradient in survival. After accounting for this gradient, individuals displaying larger home ranges were more likely to survive the harvest season. Finally, we found significant repeatabilities for lobster behavior on a monthly timescale, indicating that individual behavioral attributes tended to persist and may reflect personality. Our study therefore provides empirical support for the need to consider an evolutionary enlightened approach to fisheries management that considers the influence of harvest on multiple traits of target species.

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.

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.

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.

Harvesting changes mating behaviour in European lobster.

Removing individuals from a wild population can affect the availability of prospective mates and the outcome of competitive interactions, with subsequent effects on mating patterns and sexual selection. Consequently, the rate of harvest-induced evolution is predicted to be strongly dependent on the strength and dynamics of sexual selection, yet there is limited empirical knowledge on the interplay between selective harvesting and the mating systems of exploited species. In this study, we used genetic parentage assignment to compare mating patterns of the highly valued and overexploited European lobster (Homarus gammarus) in a designated lobster reserve and nearby fished area in southern Norway. In the area open to fishing, the fishery is regulated by a closed season, a minimum legal size and a ban on the harvest of egg-bearing females. Due to the differences in size and sex-specific fishing mortality between the two areas, males and females are of approximately equal average size in the fished area, whereas males tend to be larger in the reserve. Our results show that females would mate with males larger than their own body size, but the relative size difference was significantly larger in the reserve. Sexual selection acted positively on both body size and claw size in males in the reserve, while it was nonsignificant in fished areas. This strongly suggests that size truncation of males by fishing reduces the variability of traits that sexual selection acts upon. If fisheries continue to target large individuals (particularly males) with higher relative reproductive success, the weakening of sexual selection will likely accelerate fisheries-induced evolution towards smaller body size.

Personalities influence spatial responses to environmental fluctuations in wild fish.

Although growing evidence supports the idea that animal personality can explain plasticity in response to changes in the social environment, it remains to be tested whether it can explain spatial responses of individuals in the face of natural environmental fluctuations. This is a major challenge in ecology and evolution as spatial dynamics link individual- and population-level processes. In this study, we investigated the potential of individual personalities to predict differences in fish behaviour in the wild. Specifically, our goal was to answer if individual differences in plasticity of space use to sea surface temperature could be explained by differences in personality along the reactive-proactive axis. To address this question, we first conducted repeated standard laboratory assays (i.e., open-field test, novel object test and mirror stimulation test) to assess the personality type of 76 wild-caught Atlantic cod (Gadus morhua). Next, we released the fish back into the sea and monitored their spatial behaviour over large temporal (16 months) and spatial (a whole fjord) scales, using high-resolution acoustic tracking. We demonstrate that (a) cod personality traits are structured into a proactive-reactive syndrome (proactive fish being more bold, exploratory and aggressive), (b) mean depth use of individuals is mainly driven by sea temperature and (c) personality is a significant predictor of home range changes in the wild, where reactive, but not proactive, individuals reduced their home range as sea temperature increased. These findings expand our understanding of the ecological consequences of animal personality and the mechanisms shaping spatial dynamics of animals in nature.

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

[This corrects the article DOI: 10.1371/journal.pone.0149595.].

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.

Temperature-associated habitat selection in a cold-water marine fish.

Habitat selection is a complex process, which involves behavioural decisions guided by the multiple needs and constraints faced by individuals. Climate-induced changes in environmental conditions may alter those trade-offs and resulting habitat use patterns. In this study, we investigated the effect of sea temperature on habitat selection and habitat use of acoustically tagged Atlantic cod (Gadus morhua) at the Norwegian Skagerrak coast. Significant relationships between ocean temperature and habitat selection and use were found. Under favourable sea temperature thresholds (<16 °C), cod selected vegetated habitats, such as eelgrass and macroalgae beds, available in shallow areas. Selection for those habitats was especially high at night, when cod tended to ascend to shallower areas, presumably to feed. Selection and use of those habitats decreased significantly as temperature rose. Under increased sea surface temperature conditions, cod were absent from vegetated shallow habitats, both during the day and night, and selected instead non-vegetated rocky bottoms and sand habitats, available in deeper, colder areas. This study shows the dynamic nature of habitat selection and strongly suggests that cod in this region have to trade off food availability against favourable temperature conditions. Future increases in ocean temperature are expected to further influence the spatial behaviour of marine fish, potentially affecting individual fitness and population dynamics.

Behavioral responses of Atlantic cod to sea temperature changes.

Understanding responses of marine species to temperature variability is essential to predict impacts of future climate change in the oceans. Most ectotherms are expected to adjust their behavior to avoid extreme temperatures and minimize acute changes in body temperature. However, measuring such behavioral plasticity in the wild is challenging. Combining 4 years of telemetry-derived behavioral data on juvenile and adult (30-80 cm) Atlantic cod (Gadus morhua), and in situ ocean temperature measurements, we found a significant effect of sea temperature on cod depth use and activity level in coastal Skagerrak. During summer, cod were found in deeper waters when sea surface temperature increased. Further, this effect of temperature was stronger on larger cod. Diel vertical migration, which consists in a nighttime rise to shallow feeding habitats, was stronger among smaller cod. As surface temperature increased beyond ∼15°C, their vertical migration was limited to deeper waters. In addition to larger diel vertical migrations, smaller cod were more active and travelled larger distances compared to larger specimens. Cold temperatures during winter tended, however, to reduce the magnitude of diel vertical migrations, as well as the activity level and distance moved by those smaller individuals. Our findings suggest that future and ongoing rises in sea surface temperature may increasingly deprive cod in this region from shallow feeding areas during summer, which may be detrimental for local populations of the species.