Linking cod (Gadus morhua) and climate: investigating variability in Irish Sea cod recruitment

How climatic variability and anthropogenic pressures interact to influence recruitment is a key factor in achieving sustainable resource management. However, the combined effects of these pressures can make it difficult to detect non‐stationary interactions or shifts in the relationships with recruitment. Here we examine the links between climate and Irish Sea cod recruitment during a period of declining spawning stock biomass (SSB). Specifically, we test for a shift in the relationship between recruitment, SSB and climate by comparing an additive (generalized additive model, GAM) and non‐additive threshold model (TGAM). The relationship between recruitment success, SSB and the climatic driver, sea surface temperature, was best described by the TGAM, with a threshold identified between recruitment and SSB at approximately 7900 t. The analysis suggests a threshold shift in the relationship between recruitment and SSB in Irish Sea cod, with cod recruitment being more sensitive to climatic variability during the recent low SSB regime.     

Temperature influences on growth of unfished juvenile Northern cod (Gadus morhua) during stock collapse

This study examined growth of unfished juvenile Northern cod (Gadus morhua) off Newfoundland concomitant with stock collapse in the cold early 1990s. Two unpublished data sets were examined, one from collapse‐period trapping sites along the northeast coast of Newfoundland and one from a post‐collapse inshore trawl survey. Cumulative surface and bottom temperatures were significant predictors of growth rates of the young fish with year‐classes born during collapse experiencing slower growth than those born during subsequent warming. Relationships between accrued temperature and growth were consistent across periods, with slow growth of collapse‐period fish reflecting slower accumulation of temperature‐at‐age. Temperature influences were spatially broad‐based with no significant differences in growth rates for fish captured along the entire northeast coast of Newfoundland. Predicted differences in growth rates for collapse versus recovery year‐classes were proportional to cumulative surface temperatures but not cumulative bottom temperatures. Although significant, temperature effects on growth were relatively unimportant at youngest ages. Overall, growth differences between periods were small but large differences occurred between slowest and fastest growing year‐classes. The results suggest initial responses to increasing temperatures were delayed following collapse. We conclude that although temperature was an important determinant of dampened productivity that it alone cannot account for the collapse and slow recovery of the stock. This is the first known study to directly quantitatively link temperature impacts to an unfished component of the Northern cod stock complex during collapse, removing need for implicit assumptions about whether or not cold conditions contributed to the collapse of this iconic fish stock.     

Changes in Atlantic cod (Gadus morhua L.) sperm quality during the spawning season

The biology of cod reproduction is well described in the scientific literature. However, sperm biology and spermatozoa management are poorly studied in this species. Because of its recent farming expansion, a better knowledge of cod gametes is becoming especially useful. This work aimed at establishing tools to study sperm biology in cod, and also investigated the existence of changes in cod sperm quality during the spawning period. We showed that sperm concentration could be assessed using spectrophotometry at 260 nm. Sperm motility significantly decreased after a 168‐h storage at 4 °C. A 1:9 dilution of sperm in a non‐activating medium (1/3 seawater and 2/3 freshwater, osmotic pressure: 360 mOsm kg^?1) improved sperm storage. Sperm concentration, sperm velocity and storage capacity at 4 °C peaked during the medium period of the spawning season and then decreased to values close to those observed at the beginning of the reproductive period. The measured values of osmotic pressure, pH, protein, Na⁺, Cl^? and Ca²⁺ concentrations of the seminal fluid were modified along the spawning period. Cell damage was noted at the end of the spawning period: local blebs were observed on the flagellum but also loops at its distal part. On the other hand, spermatocrit did not vary with the sampling date. In conclusion, cod sperm quality is modified during the spawning period, the highest‐quality samples being collected during the medium part of this season.     

Greenland cod (Gadus morhua): modeling recruitment variation during the second half of the 20th century

Two approaches were used to qualify observed variability in Greenland cod (Gadus morhua) recruitment. In the first analysis, we used the linear trend of the Greenland cod recruitment time series and climatic variables, such as air temperatures from the Denmark Strait and wind conditions off East Greenland and Southwest Greenland, to explain the interannual variation in cod recruitment off Greenland. The model resulting from this ‘trend/environmental approach’, explained 79% of the interannual variation in cod recruitment off Greenland. In the second, analytical approach, the ‘regime approach’, multiple linear regression models were used, with the input data being the time series of cod recruitment and spawning stock biomass (SSB) from Iceland and Greenland, sea surface and air temperatures around Greenland, and zonal wind components between Iceland and Greenland. Model results indicated that, during the decades between 1950 and 1990, there were three different cause–effect regimes which significantly influenced the variability of cod recruitment. The three regimes included: (a) the 1950s and 1960s, a regime with favorable sea surface temperatures and a self‐sustaining cod stock off Greenland with high SSB that produced a series of above‐average, strong year classes; (b) the 1970s and 1980s, a regime of declining SSB and recruitment, with recruitment dependent on advection from Iceland; and (c) the 1990s, when the advective potential for recruitment from the Icelandic cod stock was the only available source for replenishment of the Greenland cod stocks, because cod recruitment in Greenland waters was negligible. The three models explained 76–77% of the observed interannual variation in cod recruitment off Greenland. Both approaches suggested that advective factors were the dominant influences for cod recruitment in the ‘Iceland–Greenland System’.     

Seasonal spawning and wind‐regulated retention‐dispersal of early life stage Atlantic cod (Gadus morhua) in a Newfoundland fjord

Sequential ichthyoplankton surveys were used to determine the spatial and temporal distribution of eggs and larvae over coastal spawning grounds of Atlantic cod (Gadus morhua) in Smith Sound, Trinity Bay, Newfoundland, during the spring and summer of 2006 and 2007. Egg densities showed similar patterns for both years with two peaks in abundance in spring (March–April) and late summer (late July). A clear progression of development stages (1–4) was observed in spring and summer in 2006 and summer in 2007, suggesting retention of eggs within the Sound during these periods. Modelled predictions of vertical egg distributions indicated eggs were broadly distributed near the surface during spring (March–April), but were concentrated below the pycnocline (>10 m) within the inner portions of the Sound during the summer months (July–August). Back‐calculated peaks in spawning based on water temperatures were estimated at 11 and 4 April for 2006 and 2007, respectfully, with late season peaks centred on 21–24 July for both years. Environmental data indicated cooler water temperatures and periods of high wind stress in spring, and warmer, calmer periods late summer, consistent with higher retention and faster development times on the spawning grounds later in the season. We conclude that spring and summer spawning events result in different distributions of early life stages and may lead to different distributions of juvenile and adult fish.     

Length-based Beverton and Holt spawning stock biomass per-recruit-models, with application to the Lates stappersii (Boulenger) stock in Lake Tanganyika

Two kinds of length-based Beverton and Holt spawning stock biomass per-recruit ( SSB/R )-models are presented. The first allows the computation of the absolute value of SSB/R . The second estimates the index of SSB/R , also called 'relative SSB/R '. Both models are extensions of the original age-based Beverton and Holt SSB/R -models. The SSB/R and its index can be assessed with reference to variations in the exploitation characteristics. These models were applied to the Lates stappersii (Boulenger) stock in Lake Tanganyika using fishing mortality as the independent variable. They produce an absolute value of SSB/R of 12.95 g, representing 22.4% of that of the 'virgin' stock for the 1993–1994 equilibrium-fishing regime. This level is indicative of an unsafe state of the stock in question. Moreover, the SSB for L. stappersii seems to be fragile under increased fishing pressure as, for example, doubling or tripling the current fishing regime would reduce the current SSB/R by 57.3 and 77.4%, respectively. In general, the use of length-based Beverton and Holt SSB/R -models is handicapped by underlying hypotheses and sub-models which are restrictive.     

Investigation of the temporal effects of spawning season and maternal and paternal differences on egg quality in Atlantic cod Gadus morhua L. broodstock

A better understanding of the parameters affecting egg quality and larval survival is of importance for continued development of cod broodstock and efficient husbandry practices. Decision tree analysis (DTA) was applied to analyse 3 years of egg quality data in an effort to extract the most important variables (i.e. predictors) in explaining differences in egg quality. The effect of three predictors (spawning time, maternal and paternal differences) has been studied on early cleavage pattern parameters, egg diameters, fertilization and hatching rates and has shown that females are the dominant variable and that time has a limited and inconsistent impact on the data. When using maternal, paternal differences and batch number (instead of spawning time) as predictors, the results confirm that no particular relationship is found between batch order (i.e. order in time) and egg quality. Moreover, batches with a higher egg quality show a consistency in the parameters assessed (i.e. batches with higher rates of normality in any parameter tend to be normal for other parameters). This is confirmed by the significant correlations found between cleavage parameters. Our results highlight that spawning time is of less importance than female parent contribution in ensuring high rates of fertilization and larval hatch, and maximizing general egg quality.     

Long-term variability in spawning stock age structure influences climate–recruitment link for Barents Sea cod

Fish populations may spawn a vast number of offspring, while only a small and highly variable fraction of a new cohort survives long enough to enter into the fisheries as recruits. It is intuitive that the size and state of the spawning stock, the adult part of the fish population, is important for recruitment. Additionally, environmental conditions can greatly influence survival through vulnerable early life stages until recruitment. To understand what regulates recruitment, an essential part of fish population dynamics, it is thus necessary to explain the impact of fluctuations in both spawning stock and environment, including interactions. Here, we examine if the connection between the environment and recruitment is affected by the state of the spawning stock, including biomass, mean age and age diversity. Specifically, we re-evaluate the hypothesis stating that recruitment from a spawning stock dominated by young fish and few age classes is more vulnerable to environmental fluctuations. We expand upon earlier work on the Barents Sea stock of Atlantic cod, now with data series extended in time both backwards and forwards to cover the period 1922–2019. While our findings are correlative and cannot prove a specific cause and effect mechanism, they support earlier work and strengthen the evidence for the hypothesis above. Furthermore, this study supports that advice to fisheries management should include considerations of environmental status.     

Oceanographic influences on the distribution of Baltic cod, Gadus morhua, during spawning in the Bornholm Basin of the Baltic Sea

The Baltic Sea is a stratified, semienclosed sea typified by a low-salinity surface layer and a deep saline layer of varying volume, salinity, temperature and oxygen concentration. The relationships between these oceanographic factors and the distribution of Baltic cod are presented, utilizing results from a survey carried out during the 1995 spawning period in the Bornholm Basin, at present the main spawning area of this stock. Cod distribution, abundance and population structure were estimated from hydroacoustic and trawl data and related to hydrographic parameters as well as to bottom depth. In the central basin, cod were aggregated in an intermediate layer about 15 m thick. This area of peak abundance was defined at its upper limit by the halocline and at the lower limit by oxygen content. The majority of individuals caught in the basin centre were in spawning or pre-spawning condition with a high proportion of males to females. On the basin slopes, aggregations of cod were found near the bottom. These individuals were mainly immature and maturing stages with an increasing proportion of females to males with size. Salinity and oxygen conditions were found to be the major factors influencing the vertical and horizontal distribution of adult cod. Abundance of immature cod was also positively related to decreasing bottom depths. The effect of temperature was minor. The observed size- and sex-dependent spawning aggregation patterns, in association with habitat volume and stock size, may influence cod catchability and thereby the assessment and exploitation patterns of this stock.     

Territorial and agonistic interactions between farmed and wild cod (Gadus morhua)

Studies of contest competition between wild and farmed fish have mostly focused on fish with strongly territorial behaviour. Little is known about species with more plastic social behaviour, such as Atlantic cod (Gadus morhua L.), a species that can either aggressively defend territories or shoal. There is also concern that cod that escape from farms will compete with wild populations. We examined dyadic contest competition between wild and farmed juvenile cod using an intruder–resident experimental set‐up in the laboratory. No prior residency advantage was observed, but the differences between farmed and wild cod were clear. Farmed cod were more submissive than wild cod and fled earlier during contests, which suggests that wild fish often out‐compete farmed intruders. Both fish types initiated aggression earlier against fish of the same background. A multivariate analysis of 11 different behavioural traits indicated that a group of 59% of farmed fish were behaviourally very similar to the 55% most submissive wild fish. These results suggest that wild juvenile cod may be quite robust towards competition for food and shelter from juvenile farmed cod, but further research is needed to verify this pattern.     

Influence of larval transport and temperature on recruitment dynamics of North Sea cod (Gadus morhua) across spatial scales of observation

The survival of fish eggs and larvae, and therefore recruitment success, can be critically affected by transport in ocean currents. Combining a model of early‐life stage dispersal with statistical stock–recruitment models, we investigated the role of larval transport for recruitment variability across spatial scales for the population complex of North Sea cod (Gadus morhua). By using a coupled physical–biological model, we estimated the egg and larval transport over a 44‐year period. The oceanographic component of the model, capable of capturing the interannual variability of temperature and ocean current patterns, was coupled to the biological component, an individual‐based model (IBM) that simulated the cod eggs and larvae development and mortality. This study proposes a novel method to account for larval transport and success in stock–recruitment models: weighting the spawning stock biomass by retention rate and, in the case of multiple populations, their connectivity. Our method provides an estimate of the stock biomass contributing to recruitment and the effect of larval transport on recruitment variability. Our results indicate an effect, albeit small, in some populations at the local level. Including transport anomaly as an environmental covariate in traditional stock–recruitment models in turn captures recruitment variability at larger scales. Our study aims to quantify the role of larval transport for recruitment across spatial scales, and disentangle the roles of temperature and larval transport on effective connectivity between populations, thus informing about the potential impacts of climate change on the cod population structure in the North Sea.     

Patterns in the spawning of cod (Gadus morhua L.), sole (Solea solea L.) and plaice (Pleuronectes platessa L.) in the Irish Sea as determined by generalized additive modelling

Eleven ichthyoplankton cruises were undertaken covering most of the Irish Sea during the period February to June, 1995. To identify spawning localities and investigate temporal trends in egg production, the data on stage 1 A egg distributions of cod ( Gadus morhua ), plaice ( Pleuronectes platessa ) and sole ( Solea solea ) have been modelled using generalized additive models (GAMs). A two-stage approach was adopted where presence/absence was firstly modelled as a binary process and a GAM surface subsequently fitted to egg production (conditional on presence). We demonstrate that this approach can be used to model egg production both in space and in time. The spawning sites for cod, plaice and sole in the Irish Sea were defined in terms of the probability of egg occurrence. For cod, we demonstrate that by integrating under predicted egg production surfaces, a cumulative production curve can be generated and used to define percentiles of production and thus delimit the extent of the spawning season. However, for plaice and sole, the surveys did not fully cover the spawning season and the limitations that this imposes on GAM modelling of these data are discussed. Comparison of the spawning sites in 1995 with historical data suggests that the locations of cod, plaice and sole egg production in the Irish Sea have probably remained relatively constant over the last 30 years.     

Seasonal shift in spawning of Atlantic cod (Gadus morhua L.) by photoperiod manipulation: egg quality in relation to temperature and intensive larval rearing

Commercial intensive fry production of Atlantic cod will be dependent on production of viable eggs independent of season. This can only be done by manipulation of maturation by photoperiod, but little is known about potential effects on egg characteristics and larval viability. In two cod broodstocks, maturation was successfully advanced or delayed 6 months compared with normal spawning season (March–April) by manipulation of photoperiod. The advanced broodstock spawned both in spring and autumn the same year. In two of the spawning tanks during autumn, ambient temperature was reduced after reaching 13.7°C during the first half of the spawning period. Egg quality and viability were monitored, and several egg batches were incubated, hatched and start‐fed for examination of growth and survival. Temperatures above 9.6°C resulted in significant reductions in fertilization and normal egg development. Concurrently, fractions of dead and unfertilized eggs increased with elevated temperature. Actual relative fecundity was not affected by temperature. Egg characteristics improved when temperature was controlled and lowered below 9.6°C. Occurrence of irregular spawners suggests that handling of broodstock fish should be avoided during maturation and spawning. Cod larvae originating from eggs of the advanced or delayed broodstocks were successfully reared beyond metamorphosis. Survival was 9.0–46.6% and 29.3% in green and clear water respectively. Survival correlated with both initial and average feeding conditions, but growth rate did not correlate with either of survival and feeding conditions. Specific growth rates (8.3–13.6% day⁻¹) is comparable with other intensive rearing trials with cod, but were lower than reported from nature‐like systems.     

Juvenile cod (Gadus morhua) mortality and the importance of bottom sediment type to recruitment on Georges Bank

The demersal settlement of pelagic juvenile fish has been considered a critical period in which the final adjustment is made to the size of a year class. Distribution patterns of pelagic and recently settled juvenile cod (Gadus morhua) were examined from nine surveys on Georges Bank during the summer over 5 years, 1984–1989, to relate juvenile survival to the sedimentary environment. Pelagic juveniles were widespread across Georges Bank in June, and by mid‐July they occurred on all bottom types from sand to gravel on eastern Georges Bank. However, by late July‐early August they were mostly abundant on the northeastern edge gravel deposit, which with its complex relief, provides abundant prey and refuge from predators. A bank‐wide estimate of pelagic juvenile abundance in 1986 and 1987 was used to assess mortality of the recently settled juveniles and to evaluate the relative importance of survivors from the northeastern edge gravel area to recruitment of the Georges Bank population. Settlement mortality rates over 1–2 months on the northeastern gravel area ranged from 3 to 8% day^?1, which compared reasonably with other studies. The seasonal abundance of the pelagic juveniles was almost an order of magnitude higher in 1987 than 1986; however, recruitment at age 1 was similar, indicating that a high mortality of the demersal juveniles occurred in 1987. The limited northeastern gravel area on Georges Bank may represent a survival bottleneck depending on the variability in the distribution and abundance of juvenile cod settlement in relation to that of their predators.     

Digestive capacity and compensatory growth in Atlantic cod (Gadus morhua)

The objective of this study was to examine whether digestive capacity correlates with growth rate in Atlantic cod (Gadus morhua). Ninety fish (1035±240 g; 478±36 mm) were assigned to one of three treatments: deprived of food for 5 weeks and then re-fed for 24 days, deprived for 10 weeks and then re-fed for 24 days, or fed for 24 days without deprivation (controls). Three times a week during feeding, the fish were provided with meals of capelin (Mallotus villosus) in excess. Within each treatment, ten fish were sacrificed before and twenty after the feeding period. The relative masses of the pyloric caeca, intestine, and white muscle were determined. Cytochrome c oxidase (CCO), citrate synthase (CS), and nucleoside diphosphate kinase (NDPK) activities were assayed in the pyloric caeca, intestine, and muscle as was trypsin activity in the pyloric caeca. During the re-feeding period, fish that had been deprived of food for 10 weeks showed compensatory growth, growing 1.9 times faster than the controls (0.94±0.26 versus 0.50±0.31% body mass ⋅ day⁻¹). Fish that displayed compensatory growth had a lower relative white muscle mass than controls (66.5±4.1% vs. 69.6±7.4%) while the relative masses of the pyloric caeca (2.21±0.49% vs. 1.78±0.31%) and intestine (0.95±0.20% vs. 0.77±0.15%) were greater than the controls, suggesting that the sizes of these digestive tissues might correlate with compensatory growth capacity. Citrate synthase in the pyloric caeca was the only enzyme that showed higher activity during compensatory growth (8.57±0.94 U ⋅ g tissue⁻¹ compared to 7.13±1.03 U ⋅ g tissue⁻¹ in the control group). This suggests that aerobic catabolic capacity of pyloric caeca could be related to growth capacity during recovery, possibly via the energetic cost of digestive enzyme synthesis. This revised version was published online in July 2006 with corrections to the Cover Date.     

Differences in growth and chemical composition between male and female farmed cod (Gadus morhua) throughout a maturation cycle

The growth of farmed cod fed to satiation under natural conditions in the sea in North Norway (67°N) was followed over 1 year. At the start of the experiment in September 2003, the average weight was 1300 g. After 1 year, in September 2004, the average weight was 2800 g. From the end of November to June, the fish matured and spawned and there was little or no weight gain in the fish during this time. The male cod developed gonads earlier than the females. In February, the male gonad index was 19% and decreased to 7% by the end of April, whereas the female gonad index increased from 14% in February to 25% in April. The male liver index decreased by 2% in February and by another 3% in April, when it only decreased by 1% in the female cod. The muscle protein in the female cod was reduced by more than 20 g kg^?1 in April, and the difference between the muscle protein in the male and the female cod was still significant in September. No differences were found in the post‐rigour muscle pH due to the sex of the fish.     

A synthesis of large-scale patterns in the planktonic prey of larval and juvenile cod (Gadus morhua)

Data from 40 published studies of the diet composition of larval and juvenile cod (Gadus morhua) from around the northern North Atlantic were summarized to assess generic patterns in ontogenetic and regional variability in the key prey. The results showed that larvae at the northern edge of the latitudinal range of cod depend primarily on development stages of the copepod Calanus finmarchicus, whilst those at the southern edge depend on Para‐ and Pseudocalanus species. Juvenile cod preyed on a wider range of taxa than larvae, but euphausiids were the main target prey. Analysis of regional variations in the relative abundances of C. finmarchicus and Para/Pseudocalanus spp. in the plankton, as estimated by the continuous plankton recorder (CPR) surveys, showed a similar geographical pattern to the larval cod stomach contents. Comparison of CPR data from the 1960s and 70s with data from the 1990s showed that the boundary between C. finmarchicus and Para/Pseudocalanus spp. dominance has shifted northwards on both sides of the Atlantic, whilst the abundance of euphausiids in the southern cod stock regions has declined. The results are discussed in relation to regional differences in the response of cod stocks to climate variability.     

Optimum temperature and food-limited growth of larval Atlantic cod (Gadus morhua) and haddock (Melanogrammus aeglefinus) on Georges Bank

We estimated recent growth of Atlantic cod (Gadus morhua) and haddock (Melanogrammus aeglefinus) larvae collected on the southern flank of Georges Bank in May 1992–94 from the ratio of RNA to DNA (R/D) and water temperature. Growth of both species increased with water temperature to about 7°C and then decreased. The highest growth rates were observed in May 1993 at water temperatures around 7°C. These data confirm an earlier observation of comparable temperature optima for growth of Atlantic cod and haddock larvae in the north‐west Atlantic. Comparisons of field growth rates and temperature optima with data for larvae cultured at high temperatures and prey densities in the laboratory suggest that growth may have been food‐limited at higher temperatures on Georges Bank. Given that 7°C is the long‐term mean water temperature on the southern flank in May and that climate models predict a possible 2–4°C rise in water temperatures for the western North Atlantic, our findings point to a possible adverse effect of global warming on Atlantic cod and haddock.     

Incorporating an environmental stock–recruitment relationship in the assessment of Pacific cod (Gadus macrocephalus)

The robustness of a previously described environmentally mediated stock–recruitment relationship for Pacific cod in Hecate Strait, BC, Canada was tested with 10 yr of additional data. The original analysis tested several alternative hypotheses and concluded that water transport through Hecate Strait, as indicated by sea level height, coupled with cod spawning biomass formed the best model. The present analysis indicates the relationship held through the 1990s. The implications of variation in sea level on stock production were investigated with a delay‐difference stock production model that included an environmentally mediated stock–recruitment relationship. The model predicted that the maximum fishery yield would vary between 1750 and 3670 t yr^?1 over the observed range of sea level height, and the estimated unsustainable fishing mortality during periods of low productivity would be only 0.5 times that in periods of high productivity.