First measurements of field metabolic rate in wild juvenile fishes show strong thermal sensitivity but variations between sympatric ecotypes

The relationship between physiology and temperature has a large influence on population-level responses to climate change. In natural settings, direct thermal effects on metabolism may be exaggerated or offset by behavioural responses influencing individual energy balance. Drawing on a newly developed proxy, we provide the first estimates of the thermal performance curve of field metabolism in a wild fish. We investigate the thermal sensitivity of field metabolic rate in two sympatric, genetically distinct ecotypes of Atlantic cod from the Skagerrak coast of southern Norway. The combined ecotype median of field metabolic rate increased with increasing temperature until around 16°C, coincident with the thermal optimum for growth for juvenile Atlantic cod. Individual cod experienced temperatures in excess of the thermal optimum for field metabolic rate, indicating some degree of thermal limitation of field metabolism in a complex natural environment with the potential for thermal refugia. The two cod ecotypes showed different thermal performance curves for field metabolic rate, revealing that genetic components to temperature sensitivity persist beyond acclimation effects. The cold-adapted fjord ecotype maintained higher field metabolic rates at cooler temperatures than the warm-adapted North Sea ecotype, which showed clear preference for warmer waters around the thermal optimum. Field metabolic rates of the two ecotypes were strongly influenced by year and location of sampling, implying more complex behavioural responses to environmental conditions. We emphasise that the energy uses reflecting physiological conditions in the field should be considered in the evaluation of the effect of climatic variables on fish population dynamics and demonstrate that otolith isotopes provide an analytical framework to answer this question.     

Climate effects on size‐at‐age: growth in warming waters compensates for earlier maturity in an exploited marine fish

Over the past 3 decades, North Sea Atlantic cod (Gadus morhua) have exhibited variable length‐at‐age along with declines in spawning stock biomass and timing of maturity. Multiple factors affecting growth and development in fish acted on this economically important stock over the same period including warming waters and an intensive fishery. Here, we employ North Sea cod as a model population, exploring how a physiologically relevant temperature metric (the growing degree‐day, GDD; °C day) can be used to compare year‐classes on a physiologically relevant time‐scale, disentangling influences of climate (thermal history) on observed length‐at‐age trends. We conclude that the trends in North Sea cod length‐at‐age observed during the last three decades can be explained by a combination of temperature‐dependent growth increases and a trend toward earlier maturation, the latter likely induced by the intensive fishing pressure, and possibly evidence of fisheries‐induced evolution.     

Assessment of production of eggs of Eastern Baltic cod (Gadus morhua callarias L.) on the basis of long-term ichthyoplankton data

Proceeding from long-term data on the numbers of eggs of cod in ichthyoplankton, the total annual production of cod eggs at four main spawning grounds of the Baltic Sea was calculated. It was shown that the long-term fluctuations of cod egg production were positively related to the dynamics of the volume of waters coming to the Baltic Sea in years of the North Sea advections. It is suggested that this dependence was determined by a set of adaptations providing the extension of cod reproduction upon the improvement of the environment.     

Assessment of production of eggs of eastern Baltic cod (<Emphasis Type="Italic">Gadus morhua callarias</Emphasis> L.) on the basis of long-term ichthyoplankton data

Proceeding from long-term data on the numbers of eggs of cod in ichthyoplankton, the total annual production of cod eggs at four main spawning grounds of the Baltic Sea was calculated. It was shown that the long-term fluctuations of cod egg production were positively related to the dynamics of the volume of waters coming to the Baltic Sea in years of the North Sea advections. It is suggested that this dependence was determined by a set of adaptations providing the extension of cod reproduction upon the improvement of the environment.     

Diel temperature patterns of juvenile lemon sharks Negaprion brevirostris, in a shallow-water nursery

The relatively complex pattern of temperature selection exhibited by juvenile lemon sharks Negaprion brevirostris in the North Sound differed markedly from many previously described responses of fish preferenda. Thermal data demonstrated that juvenile N. brevirostris did not attempt to behaviourally maintain a constant eccritic temperature. Rather, juveniles selected progressively warmer temperatures throughout the day until reaching the highest temperatures available, and then moved to cooler temperatures during late evening and early morning hours. It is possible that by exploiting habitat thermal heterogeneity juvenile N. brevirostris prolong activities such as feeding or digestion well into the cooler parts of the evening. The complex pattern of temperature occupation by juvenile N. brevirostris within the thermally heterogeneous North Sound nursery is probably linked to key daily activities such as prey capture, predator avoidance and digestive efficiency.     

New data on the longevity of coastal cod Gadus morhua Linnaeus, 1758 in the White Sea

The cod, Gadus morhua, is a common and abundant demersal fish in the White Sea coastal zone. The published data on the maximum age of White Sea cod still requires additional documentation, because some authors have noted difficulties in age determination by otoliths of large specimens. To obtain accurate data on the longevity of this species in the White Sea, an image analysis of thin‐sections of otoliths was made for age estimation. Research surveys in the Chupa Inlet and adjacent waters of the Kandalaksha Bay were conducted in June to August from 2007 to 2013. The five largest specimens of a total of 3564 captured fish were selected for age determination. Age of these largest individuals ranged between 7 and 12 years, total length and weight varied from 60.2 to 77.0 cm and from 2.4 to 6.1 kg, respectively. According to the data, maximal White Sea cod longevity is greater than in previously published data, and demonstrates similar longevity to conspecifics from the Baltic and North seas, whereas its life cycle is much shorter than cod from the Northeast Arctic, Iceland, Greenland, Newfoundland and Labrador stocks.     

Recolonization history and large-scale dispersal in the open sea: the case study of the North Atlantic cod, Gadus morhua L.

Most studies of the genetic structure of Atlantic cod have focused on small geographical scales. In the present study, the genetic structure of cod sampled on spawning grounds in the North Atlantic was examined using eight microsatellite loci and the Pan I locus. A total of 954 cod was collected from nine different regions: the Baltic Sea, the North Sea, the Celtic Sea, the Irish Sea and Icelandic waters during spring 2002 and spring 2003, from Norwegian waters and the Faroe Islands (North and West spawning grounds) in spring 2003, and from Canadian waters in 1998. Temporal stability among spawning grounds was observed in Icelandic waters and the Celtic Sea, and no significant difference was observed between the samples from the Baltic Sea and between the samples from Faroese waters. F -statistics showed significant differences between most populations and a pattern of isolation-by-distance was described with microsatellite loci. The Pan I locus revealed the presence of two genetically distinguishable basins, the North-west Atlantic composed of the Icelandic and Canadian samples and the North-east Atlantic composed of all other samples. Permutation of allele sizes at each microsatellite locus among allelic states supported a mutational component to the genetic differentiation, indicating a historical origin of the observed variation. Estimation of the time of divergence was approximately 3000 generations, which places the origin of current genetic pattern of cod in the North Atlantic in the late Weichselian (Wisconsinian period), at last glacial maximum.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 94 , 315–329.     

Ecological and genetic impact of Atlantic cod larval drift in the Skagerrak

We evaluate the hypothesis that Atlantic cod larvae are passively transported by sea currents from off-shore spawning areas to settle in coastal waters, a hypothesis which has recently gained support from genetic analysis of cod in the North Sea-Skagerrak area. Such larval transport has been suggested to be an important mechanism behind the commonly observed low spatial genetic differentiation in many marine organisms. Here, we apply an ARMAX(2,2) model for juvenile abundance and use long-term monitoring data from the Skagerrak coast, constituting 54 continuous annual series from 1945 to 1997. Analysing the model, we find that the product of the size of the North Sea breeding stock and the strength of the net inflow of North Sea waters had a significant, positive effect on the abundance of coastal juvenile cod. The peak effect occurs during the month of March, just after spawning, when eggs and larvae remain pelagic and sensitive to currents. In contrast, we find no evidence of any direct effect of the North Sea spawning stock alone. Our analyses indicate that 15-20,000 0-group larvae from the North Sea reach each fjord per year, on average. This corresponds to about 1-10% of the total 0-group population in each fjord on average. These findings clearly demonstrate a direct link between larval drift and gene flow in the marine environment.     

The influence of feeding behaviour on growth of Atlantic cod (Gadus morhua,Linnaeus, 1758) in the North Sea

The objective of this study was to resolve key mechanisms driving individual growth patterns of Atlantic cod (Gadus morhua). Growth dynamics were analysed by linking growth patterns with stomach content composition and environmental temperature. Samples were collected in August/September of the years 2009, 2010 and 2011 in the north‐eastern part of the central North Sea. Prey selection was assessed by identification of individual prey items in the stomach content to species. Ten feeding groups were identified consisting of individuals with one prey type dominating their stomach contents (≥75% by mass), of which six were used for growth analyses: “Sandeel”, “Clupeids”, “Norway pout”, “Flatfishes”, “Crustaceans” and “Brittle stars”. For each group, growth patterns were estimated based on measures of otolith growth increments. The stomach contents showed that cod as a species are opportunistic in their prey selection, but at the same time indicated that the total, broad feeding niche width of the population is dominated by individual diet specialization and that many individuals temporally show a preference for a particular prey type. The contribution of invertebrates and particularly crustaceans decreased with increasing cod size, whereas that of fish and predominantly herring increased. Prey type had a significant effect on growth, while temperature had no effect. Slowest growth was observed in the cod group preying on sandeel, while cod preying on Norway pout showed the fastest growth. No significant difference was observed between groups preying on brittle stars, crustaceans, flatfishes and herring. Growth in the year before capture did however not differ between any of these groups. Across sampling years, growth chronology patterns were similar but not significantly influenced by temperature.     

Variability of DNA microsatellite loci in populations of Pacific cod <Emphasis Type="Italic">Gadus macrocephalus</Emphasis> Tilesius (Gadidae)

Despite almost a hundred years of studies on the Pacific cod’s biological and ecological peculiarities, many of them and especially population structure remain poorly understood. The variability of DNA microsatellite loci Gmo3, Gmo34, Gmo35, Pgmo32, and Gmo 19 was analyzed for the cod sampled in different areas of the North Pacific. The cod sampled nearby the Southern Kurils, differed significantly by Gmo3 and Pgmo32 compared to the populations inhabiting the Bering Sea, the Sea of Okhotsk and the coastal waters off Canada. Further, Pacific cod of the three latter populations demonstrated high similarity (I = 0.996) in spite of considerable geographic remoteness of these areas from one another.     

Temperature-dependent development rates of plaice (Pleuronectes platessa L.) eggs from the Irish Sea

Experimentally derived temperature-dependent development ratesfor planktonic fish eggs are required for developing IndividualBased Models (IBMs) of early life history stages and for estimatingdaily egg production in ichthyoplankton surveys. Developmentrates of Irish Sea plaice eggs were experimentally determinedfor temperatures between 4.5 and 12° C. Differences in developmentrates were apparent when these results were compared with literaturedata for eggs from North Sea parents. On average, plaice eggsfrom the Irish Sea developed more rapidly and hatched up to2 days earlier compared with North Sea eggs incubated at thesame temperature. In terms of parental effects, larger femalestended to produce larger eggs but egg size decreased over successivebatches from the same female within a year. Temperature-dependentegg development rates were influenced by egg size in a non-linearmanner for eggs incubated at 6° C, but egg size had no effectat higher temperatures. Since most plaice eggs sampled fromthe Irish Sea during ichthyoplankton surveys in 1995 and 2000were found in waters cooler than 8° C, such effects maymodify egg development rates in the wild.     

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.     

Cod in hot water: observations of behaviour in relation to temperature

Fish behaviour varies considerably in response to changes in environmental and biological conditions. Cod ( Gadus morhua ) is not a homeothermic species and recent research has suggested that the recruitment and distribution of cod stocks may be influenced by temperature. Concerns have therefore been raised about the potential effect of climate change on stocks that are already at the southern limits of their range. We used data storage tags (DSTs) to observe the behaviour of cod in relation to temperature between 1999 and 2002. Over 3500 days of data were collected from 17 individuals tagged in the North and Irish Seas. We describe how the patterns in the temperature experience of cod are related to behavioural mechanisms, such as horizontal and vertical migration, that match habitat choice to physiological preferences. The results are discussed in the context of this behavioural response to short‐ and long‐term shifts in thermal regime and the potential consequences on the overall behaviour and distribution of cod stocks.     

Oxygen limitation of thermal tolerance in cod, Gadus morhua L., studied by magnetic resonance imaging and on-line venous oxygen monitoring

The hypothesis of an oxygen-limited thermal tolerance due to restrictions in cardiovascular performance at extreme temperatures was tested in Atlantic cod, Gadus morhua (North Sea). Heart rate, changes in arterial and venous blood flow, and venous oxygen tensions were determined during an acute temperature change to define pejus ("getting worse") temperatures that border the thermal optimum range. An exponential increase in heart rate occurred between 2 and 16 degrees C (Q(10) = 2.38 +/- 0.35). Thermal sensitivity was reduced beyond 16 degrees C when cardiac arrhythmia became visible. Flow-weighted magnetic resonance imaging (MRI) measurements of temperature-dependent blood flow revealed no exponential but a hyperbolic increase of blood flow with a moderate linear increase at temperatures >4 degrees C. Therefore, temperature-dependent heart rate increments are not mirrored by similar increments in blood flow. Venous Po(2) (Pv(O(2))), which reflects the quality of oxygen supply to the heart of cod (no coronary circulation present), followed an inverse U-shaped curve with highest Pv(O(2)) levels at 5.0 +/- 0.2 degrees C. Thermal limitation of circulatory performance in cod set in below 2 degrees C and beyond 7 degrees C, respectively, characterized by decreased Pv(O(2)). Further warming led to a sharp drop in Pv(O(2)) beyond 16.1 +/- 1.2 degrees C in accordance with the onset of cardiac arrhythmia and, likely, the critical temperature. In conclusion, progressive cooling or warming brings cod from a temperature range of optimum cardiac performance into a pejus range, when aerobic scope falls before critical temperatures are reached. These patterns might cause a shift in the geographical distribution of cod with global warming.     

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.     

Decreased Temperature Facilitates Short-Term Sea Star Wasting Disease Survival in the Keystone Intertidal Sea Star Pisaster ochraceus

An extensive 2013 mass mortality event along the West Coast of North America due to Sea Star Wasting Disease (SSWD) has affected at least 20 species of sea stars. Among environmental factors potentially contributing to the timing of the current outbreak, increased coastal water temperatures are hypothesized to have contributed to previous and current outbreaks of SSWD. With a laboratory experiment, we tested whether cooler temperatures, similar to average winter temperatures, compared to average summer temperatures could slow the progression of morbidity or prevent SSWD mortality entirely in Pisaster ochraceus. Sea stars housed in cooler water progressed through SSWD states more slowly than sea stars housed at summer temperatures. However, the cooler temperature did not prevent SSWD mortality, and all stars died of the disease. Our data are consistent with experimental studies and field observations during previous and current outbreaks, and support the hypothesis that changes in coastal water temperatures have influenced one of the largest disease related mass mortality events in our oceans.     

Francisella noatunensis subsp. noatunensis is the aetiological agent of visceral granulomatosis in wild Atlantic cod Gadus morhua

During the 1980s and 1990s wild-caught cod displaying visceral granulomatosis were sporadically identified from the southern North Sea. Presumptive diagnoses at the time included mycobacterial infection, although mycobacteria were never cultivated or observed histologically from these fish. Farmed cod in Norway displaying gross pathology similar to that identified previously in cod from the southern North Sea were recently discovered to be infected with the bacterium Francisella noatunensis subsp, noatunensis. Archived formalin-fixed paraffin-embedded tissues from the original North Sea cases were investigated for the presence of Mycobacterium spp. and Francisella spp. using real-time polymerase chain reaction, DNA sequencing and immunohistochemistry. Whilst no evidence of mycobacterial infection was found, F. noatunensis subsp. noatunensis was identified in association with pathological changes consistent with Francisella infections described from farmed cod in recent years. This study shows that francisellosis occurred in wild-caught cod in the southern North Sea in the 1980s and 1990s and demonstrates that this disease predates intensive aquaculture of cod.     

Histology of pseudobranchial tumours in Atlantic cod(Gadus morhua) from the North Sea and the Baltic Sea

Atlantic cod bearing pseudobranchial tumours were investigated from both North Sea and Baltic Sea areas. Light and electron microscopic studies revealed a tumorous structure previously described in cod from Atlantic and Pacific waters. Additionally, cysts, multinucleated cells and early stages of mitosis are described. These findings support the hypothesis that pseudobranchial tumours are instigated by a protozoan infection causing xenotumours associated with the pseudobranch organ. The cells contained in these lesions showed similarities to amoebae.     

North Sea cod and climate change – modelling the effects of temperature on population dynamics

In order to examine the likely impacts of climate change on fish stocks, it is necessary to couple the output from large‐scale climate models to fisheries population simulations. Using projections of future North Sea surface temperatures for the period 2000–2050 from the Hadley General Circulation Model, we estimate the likely effects of climate change on the North Sea cod population. Output from the model suggests that increasing temperatures will lead to an increased rate of decline in the North Sea cod population compared with simulations that ignore environmental change. Although the simulation developed here is relatively simplistic, we demonstrate that inclusion of environmental factors in population models can markedly alter one's perception of how the population will behave. The development of simulations incorporating environment effects will become increasingly important as the impacts of climate change on the marine ecosystem become more pronounced.     

Multi-torsking: simultaneous measurements of cod behaviour show differences between North Sea and Irish Sea stocks*

Fish behaviour can vary considerably in response to environmental and biological conditions. We used electronic Data Storage Tags (DSTs) to investigate the behaviour of cod in different environments; 74 North Sea cod and 20 Irish Sea cod were tagged and released in late-March 1999. So far, 32 tags (>2000 days of data) have been returned from the North Sea and four (>700 days) from the Irish Sea. The maximum recorded depth of a North Sea cod was 84 m, while Irish Sea cod utilised a depth range of 154 m. Active depth changes were of greater magnitude and rate in Irish Sea cod than North Sea cod. In addition, Irish Sea cod were continually active and made proportionally more active depth changes than North Sea cod, which were very active during migration (March–June) but exhibited little vertical movement during the summer months. To our knowledge, this is the first time that the behaviour patterns of cod from different stocks have been measured simultaneously over extended periods at such a fine temporal scale. In addition to describing considerable inter-stock differences in behaviour, our results suggest that while cod in the Irish Sea remain active and highly mobile throughout the year, North Sea cod reduce their movements during the summer feeding period. Our findings will contribute to the development of more biologically realistic management models used for evaluating the efficacy of fisheries technical measures, such as closed areas.