Acoustic monitoring of artificial reefs reveals Atlantic cod and weakfish spawning and presence of individual bottlenose dolphins.

The artificial reefs in New York's waters provide structure in areas that are typically flat and sandy, creating habitat for a multitude of species as an area to spawn, forage, and reside. Passive acoustic data collected on the Fire Island and Shinnecock artificial reefs between 2018 and 2022 detected spawning-associated calls of weakfish (Cynoscion regalis) and Atlantic cod (Gadus morhua), as well as the presence of individual bottlenose dolphins (Tursiops truncatus) through their signature whistles. Weakfish and Atlantic cod were more vocally active on the Fire Island reef, where Atlantic cod grunts peaked during a new moon phase in December, and weakfish spawning experienced variable peaks between mid-July and mid-August on both reefs. Fifty-seven individual bottlenose dolphins were identified, with whistle repeats ranging from seconds to years apart. Passive acoustic monitoring allows for simultaneous collection of information on multiple species at different trophic levels as well as behavioral information that helps managers understand how these animals utilize these habitats, which can lead to improved conservation measures.

Physiological responses of Atlantic cod to climate change indicate that coastal ecotypes may be better adapted to tolerate ocean stressors.

Healthy ecosystems and species have some degree of resilience to changing conditions, however as the frequency and severity of environmental changes increase, resilience may be diminished or lost. In Sweden, one example of a species with reduced resilience is the Atlantic cod (Gadus morhua). This species has been subjected to overfishing, and with additional pressures such as habitat degradation and changing environmental conditions there has been little to no recovery, despite more than a decade of management actions. Given the historical ecological, economical, and cultural significance of cod, it is important to understand how Atlantic cod respond to global climate change to recover and sustainably manage this species in the future. A multi-stressor experiment was conducted to evaluate physiological responses of juvenile cod exposed to warming, ocean acidification, and freshening, changes expected to occur in their nursery habitat. The response to single drivers showed variable effects related to fish biometrics and increased levels of oxidative stress dependent parameters. Importantly, two separate responses were seen within a single treatment for the multi-stressor and freshening groups. These within-treatment differences were correlated to genotype, with the offshore ecotype having a heightened stress response compared to the coastal ecotype, which may be better adapted to tolerate future changes. These results demonstrate that, while Atlantic cod have some tolerance for future changes, ecotypes respond differently, and cumulative effects of multiple stressors may lead to deleterious effects for this important species.

Spawning fish maintains trophic synchrony across time and space beyond thermal drivers.

Increasing ocean temperature will speed up physiological rates of ectotherms. In fish, this is suggested to cause earlier spawning due to faster oocyte growth rates. Over time, this could cause spawning time to become decoupled from the timing of offspring food resources, a phenomenon referred to as trophic asynchrony. We used biological data, including body length, age, and gonad developmental stages collected from >125,000 individual Northeast Arctic cod (Gadus morhua) sampled between 59 and 73° N in 1980-2019. Combined with experimental data on oocyte growth rates, our analyses show that cod spawned progressively earlier by about a week per decade, partly due to ocean warming. It also appears that spawning time varied by more than 40 days, depending on year and spawning location. The significant plasticity in spawning time seems to be fine-tuned to the local phytoplankton spring bloom phenology. This ability to partly overcome thermal drivers and thus modulate spawning time could allow individuals to maximize fitness by closely tracking local environmental conditions important for offspring survival. Our finding highlights a new dimension for trophic match-mismatch and should be an important consideration in models used to predict phenology dynamics in a warmer climate.

Land use change and coastal water darkening drive synchronous dynamics in phytoplankton and fish phenology on centennial timescales.

At high latitudes, the suitable window for timing reproductive events is particularly narrow, promoting tight synchrony between trophic levels. Climate change may disrupt this synchrony due to diverging responses to temperature between, for example, the early life stages of higher trophic levels and their food resources. Evidence for this is equivocal, and the role of compensatory mechanisms is poorly understood. Here, we show how a combination of ocean warming and coastal water darkening drive long-term changes in phytoplankton spring bloom timing in Lofoten Norway, and how spawning time of Northeast Arctic cod responds in synchrony. Spring bloom timing was derived from hydrographical observations dating back to 1936, while cod spawning time was estimated from weekly fisheries catch and roe landing data since 1877. Our results suggest that land use change and freshwater run-off causing coastal water darkening has gradually delayed the spring bloom up to the late 1980s after which ocean warming has caused it to advance. The cod appear to track phytoplankton dynamics by timing gonadal development and spawning to maximize overlap between offspring hatch date and predicted resource availability. This finding emphasises the importance of land-ocean coupling for coastal ecosystem functioning, and the potential for fish to adapt through phenotypic plasticity.

Resilience assessment in complex natural systems.

Ecological resilience is the capability of an ecosystem to maintain the same structure and function and avoid crossing catastrophic tipping points (i.e. undergoing irreversible regime shifts). While fundamental for management, concrete ways to estimate and interpret resilience in real ecosystems are still lacking. Here, we develop an empirical approach to estimate resilience based on the stochastic cusp model derived from catastrophe theory. The cusp model models tipping points derived from a cusp bifurcation. We extend cusp in order to identify the presence of stable and unstable states in complex natural systems. Our Cusp Resilience Assessment (CUSPRA) has three characteristics: (i) it provides estimates on how likely a system is to cross a tipping point (in the form of a cusp bifurcation) characterized by hysteresis, (ii) it assesses resilience in relation to multiple external drivers and (iii) it produces straightforward results for ecosystem-based management. We validate our approach using simulated data and demonstrate its application using empirical time series of an Atlantic cod population and marine ecosystems in the North Sea and the Mediterranean Sea. We show that Cusp Resilience Assessment is a powerful method to empirically estimate resilience in support of a sustainable management of our constantly adapting ecosystems under global climate change.

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.

Effects of weathered polyethylene microplastic ingestion on sexual maturation, fecundity and egg quality in maturing broodstock Atlantic cod Gadus morhua.

Microplastics (MPs) have become a global issue as they are omnipresent in the ocean. Fish ingesting MPs through feed could be affected in their physiological function, e.g., disrupted enzyme production and function, reduction of feeding and reproductive failure. This study assessed the effects of feed containing naturally weathered MPs from the Oslofjord (Norway) on the reproductive physiology of Atlantic cod (Gadus morhua). Farmed cod broodstock were fed either control (C-diet) or feeds containing 1% microplastic (MP-diet) starting nine months prior to spawning, from June until May. No major differences were found between diet groups in overall biometrics or gonad histology. Sex steroid levels (testosterone, 11-ketotestosterone and 17ß-estradiol) resulted in expected profiles increasing over time without any significant differences between treatments. Gene expression levels of the steroidogenic enzyme 20ß-hydroxysteroid dehydrogenase (20ß-hsd) and vitellogenin1 (vtg1) showed significant differences between dietary treatments with lower expression in the control group. This can be a direct effect of MPs, but endocrine disrupting effects of potentially leachable plastic additives cannot be completely ruled out. Thus, these enzymes could be indicators of exposure to contaminants that disrupt sexual maturation by affecting the production of primarily maturation-inducing steroid. Although the concentration of MPs employed in this study may not be high enough to elicit any observable short-term biological effects, the observed gene expression suggests that long-term consequences should be considered caused by an expected increase of MPs in marine environments.

Age structure affects population productivity in an exploited fish species.

Long-term changes in the age and size structure of animal populations are well documented, yet their impacts on population productivity are poorly understood. Fishery exploitation can be a major driver of changes in population age-size structure because fisheries significantly increase mortality and often selectively remove larger and older fish. Climate change is another potential driver of shifts in the demographic structure of fish populations. Northeast Arctic (NEA) cod is the largest population of Atlantic cod (Gadus morhua) and one of the world's most important commercial fish stocks. This population has experienced considerable changes in population age-size structure over the past century, largely in response to fishing. In this study, we investigate whether changes in spawner age structure have affected population productivity in NEA cod, measured as recruits per spawning stock biomass, over the past 75 years. We find evidence that shifts in age structure toward younger spawners negatively affect population productivity, implying higher recruitment success when the spawning stock is composed of older individuals. The positive effect of an older spawning stock is likely linked to maternal effects and higher reproductive output of larger females. Our results indicate a threefold difference in productivity between the youngest and oldest spawning stock that has been observed since the 1950s. Further, our results suggest a positive effect of environmental temperature and a negative effect of intraspecific cannibalism by older juveniles on population productivity, which partly masked the effect of spawner age structure unless accounted for in the model. Collectively, these findings emphasize the importance of population age structure for the productivity of fish populations and suggest that harvest-induced demographic changes can have negative feedbacks for fisheries that lead to a younger spawning stock. Incorporating demographic data into harvest strategies could thus facilitate sustainable fishery management.

Allee effects and the Allee-effect zone in northwest Atlantic cod.

According to the theory of compensatory dynamics, depleted populations should recover when the threat responsible for their decline is removed because per capita population growth is assumed to be highest when populations are at their smallest viable sizes. Yet, many seriously depleted fish populations have failed to recover despite threat mitigation. Atlantic cod (Gadus morhua) stocks off Newfoundland, despite 30 years of dramatically reduced fishing mortality and numerous fishery closures, have not recovered, suggesting that drivers other than fishing can regulate the growth of collapsed fish populations, inhibiting or preventing their recovery. Here, using Bayesian inference, we show strong evidence of Allee effects in a south Newfoundland cod population, based on data on recruitment and spawning stock biomass. We infer the Allee-effect threshold, below which recovery is impaired. We demonstrate the necessity of data at low population sizes to make inferences about the nature of low-abundance dynamics. Our work indicates that Allee effects are not negligible in commercially exploited fish populations, as commonly projected, and that they represent an inhibitory force that can effectively prevent recovery from overfishing. Our findings contrast with prevailing fisheries management practices that assume compensatory dynamics at low abundances with potential to seriously overestimate the recovery potential of collapsed populations.

Tradeoffs of managing cod as a sustainable resource in fluctuating environments.

Sustainable human exploitation of living marine resources stems from a delicate balance between yield stability and population persistence to achieve socioeconomic and conservation goals. But our imperfect knowledge of how oceanic oscillations regulate temporal variation in an exploited species can obscure the risk of missing management targets. We illustrate how applying a management policy to suppress fluctuations in fishery yield in variable environments (prey density and regional climate) can present unintended outcomes in harvested predators and the sustainability of harvesting. Using Atlantic cod (Gadus morhua, an apex predatory fish) in the Barents Sea as a case study we simulate age-structured population and harvest dynamics through time-varying, density-dependent and density-independent processes with a stochastic, process-based model informed by 27-year monitoring data. In this model, capelin (Mallotus villosus, a pelagic forage fish), a primary prey of cod, fluctuations modulate the strength of density-dependent regulation primarily through cannibalistic pressure on juvenile cod survival; sea temperature fluctuations modulate thermal regulation of cod feeding, growth, maturation, and reproduction. We first explore how capelin and temperature fluctuations filtered through cod intrinsic dynamics modify catch stability and then evaluate how management to suppress short-term variability in catch targets alters overharvest risk. Analyses revealed that suppressing year-to-year catch variability impedes management responses to adjust fishing pressure, which becomes progressively out of sync with variations in cod abundance. This asynchrony becomes amplified in fluctuating environments, magnifying the amplitudes of both fishing pressure and cod abundance and then intensifying the density-dependent regulation of juvenile survival through cannibalism. Although these transient dynamics theoretically give higher average catches, emergent, quasicyclic behaviors of the population would increase long-term yield variability and elevate overharvest risk. Management strategies that overlook the interplay of extrinsic (fishing and environment) and intrinsic (life history and demography) fluctuations thus can inadvertently destabilize fish stocks, thereby jeopardizing the sustainability of harvesting. These policy implications underscore the value of ecosystem approaches to designing management measures to sustainably harvest ecologically connected resources while achieving socioeconomic security.

Otolith "spawning zones" across multiple Atlantic cod populations: Do they accurately record maturity and spawning?

Specific changes identified in the otolith macrostructure of Northeast Arctic cod as "spawning zones" are presumed to represent spawning events, but recent experimental studies have challenged this relationship. Because these zones are not routinely recorded outside of Norway, otoliths from multiple Atlantic cod populations with different life history and environmental traits were first examined to see if spawning zones could be identified as a general characteristic of cod. Then, a large archival collection of cod otoliths was used to investigate temporal changes in the occurrence of spawning zones and test for correlations between maturity at age derived from otolith spawning zones and gonad maturity stages. This study shows that spawning zones likely are a universal trait of Atlantic cod and not limited to certain environments or migratory behaviors as previously proposed. Maturity at age derived from spawning zone data showed trends consistent with those from gonad examinations. However, spawning zones appear to form with a one- or two-year lag with sexual maturity, which is suspected to reflect a stabilizing of energy partitioning after the first spawning events. Our results illustrate the potential for use of spawning zones, for example in species or populations with limited available maturity data, and highlights the need for addressing the physiological processes behind their formation.

Neuroendocrine regulation of reproduction in Atlantic cod (Gadus morhua): Evidence of Eya3 as an integrator of photoperiodic cues and nutritional regulation to initiate sexual maturation.

Evidence from mammals and aves alludes to a possibly conserved seasonal photoperiod induced neuroendocrine cascade which stimulates subsequent sexual maturation however our understanding of this mechanism in teleosts is lacking. Unlike all teleosts studied to date, the Atlantic cod (Gadus morhua) is a short day breeder with the reduction in day-length from the summer solstice stimulating gametogenesis. Cod specific orthologues of eya3, tshß and dio2 were identified and their expression was monitored in the brain and pituitary of cod held under either stimulated or inhibited photoperiod conditions. While no differential expression was apparent in brain dio2 & tshß and pituitary tshß, there was significant temporal variation in expression of pituitary eya3 under the SNP treatment, with expression level elevating in association with active gametogenesis. Under the LL treatment, sexual maturation was inhibited and there was a corresponding suppression of eya3 expression. In a second study the impact of size/energetic status on the initiation of sexual maturation was investigated. In the feed restricted population maturation was significantly suppressed (5% sexually mature) compared to the ab libitum fed stock (95% sexually mature) with there being a concomitant significant suppression in pituitary eya3 expression. Overall, these results suggest that pituitary eya3 has the potential to act as an integrator of both environmental and energetic regulation of sexual maturation of cod. Being the first account of eya3 induction in a short day breeding teleost, the conserved association with stimulation of reproduction and not seasonal state indicates that the upstream drivers which initiate the pathway differ among vertebrates according to their breeding strategies, but the pathway itself and its role in the reproductive cascade appears to be conserved across the vertebrate clade.

Genomic stability through time despite decades of exploitation in cod on both sides of the Atlantic.

The mode and extent of rapid evolution and genomic change in response to human harvesting are key conservation issues. Although experiments and models have shown a high potential for both genetic and phenotypic change in response to fishing, empirical examples of genetic responses in wild populations are rare. Here, we compare whole-genome sequence data of Atlantic cod (Gadus morhua) that were collected before (early 20th century) and after (early 21st century) periods of intensive exploitation and rapid decline in the age of maturation from two geographically distinct populations in Newfoundland, Canada, and the northeast Arctic, Norway. Our temporal, genome-wide analyses of 346,290 loci show no substantial loss of genetic diversity and high effective population sizes. Moreover, we do not find distinct signals of strong selective sweeps anywhere in the genome, although we cannot rule out the possibility of highly polygenic evolution. Our observations suggest that phenotypic change in these populations is not constrained by irreversible loss of genomic variation and thus imply that former traits could be reestablished with demographic recovery.

Some recent data on sperm morphology and motility kinetics in Atlantic cod (Gadus morhua L.).

Studying biology of sperm provides valuable information to optimize artificial reproduction and is crucial for sustainable aquaculture. Here, we investigated morphology of spermatozoon in Atlantic cod (Gadus morhua) using transmission and scanning electron microscopy. Furthermore, spermatozoa motility kinetics at different osmolalities were studied using computer-assisted sperm analysis software. The spermatozoon lacked an acrosome and consisted of a head, midpiece, and flagellum. The head of spermatozoa was round, oval, and rather elongated in shape, showing high variations in dimensions. There were up to 6 mitochondria that encircled the proximal part of the flagellum. The proximal and distal centrioles were located within the nuclear notch and arranged orthogonal to each other. The axoneme had a typical 9 + 2 microtubule structure. The flagellar length of spermatozoon was 66.94 ± 0.46 µm. Spermatozoa were immotile in the seminal plasma. Dilution of sperm with natural seawater (1100 mOsmol/kg) resulted in initiation of motility for 91.0 ± 3.4% of spermatozoa with average velocity of 86.2 ± 2.3 µm/s and beating frequency of 52 Hz. The duration of spermatozoa motility was > 6 min; however, the percentage of motile spermatozoa decreased at 60 s post-activation. When osmolality of natural seawater was modified using distilled water or NaCl, spermatozoa motility was not initiated at ≤ 400 and ≥ 2500 mOsmol/kg, and the highest percentage of motility was observed at 730-1580 mOsmol/kg. In a sucrose solution, spermatozoa motility was initiated and suppressed at 600 and 1500 mOsmol/kg, respectively, and highest percentage of motility was observed at 800-1100 mOsmol/kg. Spermatozoon morphology comparisons within Gadiformes showed differences in dimensions of head and mitochondria, flagellar length, and number of mitochondria. The present study provides valuable data that can be used for phylogenetic implications based on spermatozoon morphology and for development of artificial fertilization and sperm cryopreservation protocols based on sperm motility.

The forgotten feeding ground: patterns in seasonal and depth-specific food intake of adult cod Gadus morhua in the western Baltic Sea.

This study presents the diet composition of western Baltic cod Gadus morhua based on 3150 stomachs sampled year-round between 2016 and 2017 using angling, gillnetting and bottom trawling, which enhanced the spatio-temporal coverage of cod habitats. Cod diet composition in shallow areas (<20 m depth) was dominated by benthic invertebrate species, mainly the common shore crab Carcinus maneas. Compared to historic diet data from the 1960s and 1980s (limited to depth >20 m), the contribution of herring Clupea harengus decreased and round goby Neogobius melanostomus occurred as a new prey species. Statistical modelling revealed significant relationships between diet composition, catch depth, fish length and season. Generalized additive modelling identified a negative relationship between catch depth and stomach content weight, suggesting reduced food intake in winter when cod use deeper areas for spawning and during peak summer when cod tend to avoid high water temperatures. The results of this study highlight the importance of shallow coastal areas as major feeding habitats of adult cod in the western Baltic Sea, which were previously unknown because samples were restricted to deeper trawlable areas. The results strongly suggest that historic stomach analyses overestimated the role of forage fish and underestimated the role of invertebrate prey. Eventually, this study shows the importance of a comprehensive habitat coverage for unbiased stomach sampling programmes to provide a more reliable estimation of top predator diet, a key information for food web analyses and multispecies models.

Intra-annual variation in feeding of Atlantic cod Gadus morhua: the importance of ephemeral prey bursts.

Seasonal prey bursts are important for the life cycles and energy budgets of many predators. This study documents the diet and, especially, the importance of the ephemeral occurrence of capelin as prey for Atlantic cod (Gadus morhua) in Godthaabsfjord, west Greenland, over an annual cycle. The cod showed clear differences in diet composition on the 11 sampling dates resulting in a spring-summer, late summer-autumn and winter cluster. Moreover, a single sampling date, 12 May, was defined by cod gorge feeding on spawning capelin, which led to average stomach contents 4.3 times higher than the average for the remaining sampling dates. Changes in nitrogen stable isotope values from 22 April to 7 July in cod liver and muscle tissue were used to calculate the consumption of capelin. Based on this, the consumption of capelin varied between 538 and 658 g wet weight for a 1.3 kg cod. Using published consumption/biomass estimates and observed growth rates, the capelin intake corresponds to 10.1%-33.3% of the annual food consumption and accounts for 28.1%-34.5% of the annual growth of the cod. The present study documents the omnivorous feeding mode of Atlantic cod but highlights the utilization and importance of ephemeral prey bursts for the annual energy budget of the cod. It is hypothesized that access to capelin is critical for the postspawning recovery of Godthaabsfjord cod.

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.

Population-level effects of acoustic disturbance in Atlantic cod: a size-structured analysis based on energy budgets.

Anthropogenic underwater noise may negatively affect marine animals. Yet, while fishes are highly sensitive to sounds, effects of acoustic disturbances on fishes have not been extensively studied at the population level. In this study, we use a size-structured model based on energy budgets to analyse potential population-level effects of anthropogenic noise on Atlantic cod (Gadus morhua). Using the model framework, we assess the impact of four possible effect pathways of disturbance on the cod population growth rate. Through increased stress, changes in foraging and movement behaviour, and effects on the auditory system, anthropogenic noise can lead to (i) increased energy expenditure, (ii) reduced food intake, (iii) increased mortality, and (iv) reduced reproductive output. Our results show that population growth rates are particularly sensitive to changes in energy expenditure and food intake because they indirectly affect the age of maturation, survival and fecundity. Sub-lethal effects of sound exposure may thus affect populations of cod and fishes with similar life histories more than lethal effects of sound exposure. Moreover, anthropogenic noise may negatively affect populations when causing persistent increases of energy expenditure or decreases of food intake. Effects of specific acoustic pollutants on energy acquisition and expenditure should therefore be further investigated.