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.     

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.     

Pop‐up satellite archival tag effects on the diving behaviour,growth and survival of adult Atlantic salmon Salmo salar at sea

The effects of large, externally attached pop‐up satellite archival tags (PSATs) were compared with those of small implanted data storage tags (DSTs) on adult Atlantic salmon Salmo salar during their ocean migration in regards to depth utilization, diving depth, diving rate, diving speed and temperatures experienced. Additionally the return rate and growth of individuals tagged with PSATs was compared with those of small acoustic tags and DSTs. Overall, the depth distribution of individuals tagged with PSATs was similar to that of those tagged with DSTs, reflecting the pelagic nature of S. salar at sea. Individuals tagged with PSATs, however, dived less frequently and to shallower depths, and dived and surfaced at slower velocities. Sea surface temperatures experienced by individuals tagged with PSATs were similar to those experienced by those tagged with DSTs for the same time of year, suggesting that there were no large differences in the ocean migration. Return rates did not depend on whether individuals were tagged with PSATs or not, indicating that survival at sea was not impacted by PSATs in comparison to small internal tags. Individuals tagged with PSATs, however, had a smaller increase in body mass than those tagged with acoustic tags or DSTs. It was concluded that PSATs are suitable for use in researching large‐scale migratory behaviour of adult S. salar at sea, but that some effects on their behaviour from tagging must be expected. Effects of PSATs may be largest in the short term when S. salar are swimming in bursts at high speeds. Even though individuals tagged with PSATs performed deep and frequent dives, the results of this study suggest that untagged individuals would perform even deeper and more frequent dives than tagged individuals.     

A field and experimental evaluation of the effect of data storage tags on the growth of cod

The effect of electronic data storage tags (DSTs) on the growth of cod Gadus morhua was evaluated in laboratory and field experiments. In the first laboratory experiment, large DSTs (60 × 18 mm, 3 g in water ) attached externally for 3 months did not have any effect ( anova , P  > 0·05) on the growth of adult cod (mean ±  s . d . 65 ± 4·5 cm total length) relative to untagged adult cod. In a second experiment, small DSTs (34 × 11 mm, 1·5 g in water) implanted into young cod (48·1 ± 4·4 cm) for an 8 month period did not have any effect upon the growth relative to untagged controls ( anova , P  > 0·05). Length data returned from tagging experiments conducted on adult cod (57·3 ± 7·5 cm) in the North Sea showed that the growth of fish tagged either externally or internally with large DSTs was not different ( t ‐test, P  > 0·05). Attachment wounds, however, provided evidence that external attachment of DSTs should be avoided unless sensor configuration requires access to the external environment, and that internal implantation should be preferred whenever possible.     

Migration route and spawning area fidelity by North Sea plaice

Data from plaice, Pleuronectes platessa L., tagged with electronic data storage tags, were used to test whether these fishes exhibited migration route and spawning area fidelity in successive spawning seasons. Depth and temperature data were recorded for each fish over 365-512 days in the central North Sea and this information was used to reconstruct movements based on tidal locations. We discovered highly directed seasonal migrations from the winter spawning area south of a major topographical feature, Dogger Bank Tail End, to summer feeding grounds 250 km to the north in deep, cold, thermally stratified water. Our results show synchronous timing of migration, repeated pre- and post-spawning migration routes and 100% spawning area fidelity, including two individuals that returned to within 20 km of their previous season's spawning location. This is the first study to provide a complete reconstruction of annual migrations by individual fishes, showing strong homing behaviour along consistent migration routes.     

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.     

Diel vertical migration of European hake Merluccius merluccius and associated temperature histories: insights from a pilot data-storage tagging (DST) experiment

A pioneering experiment of archival tagging of European hake Merluccius merluccius provided evidence of a diel vertical migration pattern which was analysed using an automatic method, developed and validated through time-frequency analyses. Frequent vertical movements across the thermocline were observed and fish experienced rapid temperature changes >7° C. These tagging-recapture data also suggested a homing behaviour to feeding grounds.     

Summer feeding ecology of harp seals (Phoca groenlandica) in relation to arctic cod (Boreogadus saida) in the Canadian high arctic

Summary The diet and feeding behaviour of harp seals, Phoca groenlandica, was examined in two high arctic locations. Fish otoliths were used to evaluate dietary composition and aspects of the population dynamics of the major prey species, arctic cod, Boreogadus saida. Harp seals, primarily adults, arrive in the high arctic in mid to late June and depart by early October. Their migration is undertaken specifically for feeding. Harp seals feed intensively on arctic cod, often occurring in dense multispecies aggregations in late summer. The average weight of harp seal stomach contents was high; glutted individuals contained as much as 6% of their body weight in food. Although arctic cod declined in abundance between years, size of cod ingested was similar between areas and years, and overlapped completely with cod taken by other marine mammals. Age/size segregation of arctic cod may account for poor representation of fish <3 years old in the seal diet. Widespread reproductive failure of arctic cod could have a profound influence on the energy balance of adult harp seals since there does not appear to be an alternate food source of equivalent energy value and abundance in arctic waters. Increasing harp seal populations will likely result in increased competition with a host of arctic cod predators, particularly ringed seals.     

Summer and fall movement of cownose ray, <Emphasis Type="Italic">Rhinoptera bonasus</Emphasis>, along the east coast of United States observed with pop-up satellite tags

Cownose ray, Rhinoptera bonasus, is a common elasmobranch species along the southeast United States coast that recently has received negative attention. These rays can consume considerable amounts of commercial shellfish raising concerns regarding their control and need for effective management. However, limited information is known regarding their population abundance and migration patterns. We addressed the latter by reviewing 25 tagged cownose rays in Chesapeake Bay with pop-up satellite archival tags (PSATs) to study their movement patterns during summer and fall and identify wintering grounds. Eleven tags provided useful data on temperature, depth, light level and/or end locations. The migration tracks were deciphered through geolocation based on light levels, sea surface temperatures and depth constraints. PSAT end locations indicated southern wintering grounds in the coastal waters of central Florida. Female rays migrated out of Chesapeake Bay at the end of September to early October and continued their southerly migration to Florida. Male rays exited the bay in July and migrated northward based on their estimated movement tracks. The male rays appeared to have a second summer feeding ground off the coast of southern New England. In the fall, males migrated south from New England to the same wintering grounds as the females. No diel differences in habitat use were detected; however, males tended to occupy a wider depth and temperature range compared to females. Information on the movement patterns and habitat use for cownose rays will assist in determining more effective recreational and commercial management plans.     

Ticket to spawn: Combining economic and genetic data to evaluate the effect of climate and demographic structure on spawning distribution in Atlantic cod

Climate warming and harvesting affect the dynamics of species across the globe through a multitude of mechanisms, including distribution changes. In fish, migrations to and distribution on spawning grounds are likely influenced by both climate warming and harvesting. The Northeast Arctic (NEA) cod (Gadus morhua) performs seasonal migrations from its feeding grounds in the Barents Sea to spawning grounds along the Norwegian coast. The distribution of cod between the spawning grounds has historically changed at decadal scales, mainly due to variable use of the northern and southern margins of the spawning area. Based on historical landing records, two major hypotheses have been put forward to explain these changes: climate and harvesting. Climate could affect the distribution through, for example, spatial habitat shifts. Harvesting could affect the distribution through impacting the demographic structure. If demographic structure is important, theory predicts increasing spawner size with migration distance. Here, we evaluate these hypotheses with modern data from a period (2000–2016) of increasing temperature and recovering stock structure. We first analyze economic data from the Norwegian fisheries to investigate geographical differences in size of spawning fish among spawning grounds, as well as interannual differences in mean latitude of spawning in relation to changes in temperature and demographic parameters. Second, we analyze genetically determined fish sampled at the spawning grounds to unambiguously separate between migratory NEA cod and potentially smaller sized coastal cod of local origin. Our results indicate smaller spawners farther away from the feeding grounds, hence not supporting the hypothesis that harvesting is a main driver for the contemporary spawning ground distribution. We find a positive correlation between annual mean spawning latitude and temperature. In conclusion, based on contemporary data, there is more support for climate compared to harvesting in shaping spawning ground distribution in this major fish stock in the North Atlantic Ocean.     

Central European Greylag Geese Anser anser show a shortening of migration distance and earlier spring arrival over 60 years

Global climate change can cause pronounced changes in species? migratory behaviour. Numerous recent studies have demonstrated climate‐driven changes in migration distance and spring arrival date in waterbirds, but detailed studies based on long‐term records of individual recapture or re‐sighting events are scarce. Using re‐sighting data from 430 marked individuals spanning a 60‐year period (winters 1956/1957 to 2015/2016), we assessed patterns in migration distance and spring arrival date, wintering‐site fidelity and survival in the increasing central European breeding population of Greylag Geese Anser anser. We demonstrate a long‐term decrease in migration distance, changes in the wintering range caused by winter partial short‐stopping, and the earlier arrival of geese on their breeding grounds. Greylag Geese marked on central Europe moulting grounds have not been recorded wintering in Spain since 1986 or in Tunisia and Algeria since 2004. The migration distance and spring arrival of geese indicated an effect of temperature at the breeding site and values of the NAO index. Greylag Geese migrate shorter distances and arrive earlier in milder winters. We suggest that shifts in the migratory behaviour of Central European Greylag Geese are individual temperature‐dependent decisions to take advantage of wintering grounds becoming more favourable closer to their breeding grounds, allowing birds to acquire breeding territories earlier.     

Migration pathways, behavioural thermoregulation and overwintering grounds of blue sharks in the Northwest Atlantic

The blue shark Prionace glauca is the most abundant large pelagic shark in the Atlantic Ocean. Although recaptures of tagged sharks have shown that the species is highly migratory, migration pathways towards the overwintering grounds remain poorly understood. We used archival satellite pop-up tags to track 23 blue sharks over a mean period of 88 days as they departed the coastal waters of North America in the autumn. Within 1-2 days of entering the Gulf Stream (median date of 21 Oct), all sharks initiated a striking diel vertical migration, taking them from a mean nighttime depth of 74 m to a mean depth of 412 m during the day as they appeared to pursue vertically migrating squid and fish prey. Although functionally blind at depth, calculations suggest that there would be a ~2.5-fold thermoregulatory advantage to swimming and feeding in the markedly cooler deep waters, even if there was any reduced foraging success associated with the extreme depth. Noting that the Gulf Stream current speeds are reduced at depth, we used a detailed circulation model of the North Atlantic to examine the influence of the diving behaviour on the advection experienced by the sharks. However, there was no indication that the shark diving resulted in a significant modification of their net migratory pathway. The relative abundance of deep-diving sharks, swordfish, and sperm whales in the Gulf Stream and adjacent waters suggests that it may serve as a key winter feeding ground for large pelagic predators in the North Atlantic.     

Long-term satellite telemetry of the movements and habitat utilisation by green turtles in the Mediterranean

There is a relative paucity of data regarding the at-sea distribution and behaviour of marine turtles. This is especially true for the critically endangered green turtle Chelonia mydas population in the Mediterranean. Six adult female green turtles were equipped with satellite transmitters and tracked for periods of between 28 and 293 d following their final nesting of the season in northern Cyprus. Data elucidated hitherto unknown migratory pathways and highlighted the importance of North African coastal waters as feeding habitat for adults of this species. For three individuals, instruments transmitted detailed information on dive depth, dive duration and water temperature which afforded novel insights into behaviour during different stages of migration, feeding in the foraging grounds and most remarkably, during a period of midwinter diapause when water temperatures were generally below 25°C. Turtles showed fidelity to specific shallow inshore feeding areas and moved offshore to deeper wintering sites.     

Electronic tags reveal behaviour of captured and discarded fish

Internally implanted data storage tags (DST) recording hydrostatic pressure (depth) and temperature in Atlantic cod Gadus morhua were used to track the behaviour of nine individuals during fishing operations. Gadus morhua showed identifiable and characteristic behavioural responses to different capture processes. In a unique observation, one fish survived being discarded and upon return to the seabed exhibited a cessation of activity comparable to observations on stressed fish under laboratory conditions.     

Evidence of Segregated Spawning in a Single Marine Fish Stock: Sympatric Divergence of Ecotypes in Icelandic Cod?

There is increasing recognition of intraspecific diversity and population structure within marine fish species, yet there is little direct evidence of the isolating mechanisms that maintain it or documentation of its ecological extent. We analyzed depth and temperature histories collected by electronic data storage tags retrieved from 104 Atlantic cod at liberty ≥1 year to evaluate a possible isolating mechanisms maintaining population structure within the Icelandic cod stock. This stock consists of two distinct behavioral types, resident coastal cod and migratory frontal cod, each occurring within two geographically distinct populations. Despite being captured together on the same spawning grounds, we show the behavioral types seem reproductively isolated by fine-scale differences in spawning habitat selection, primarily depth. Additionally, the different groups occupied distinct seasonal thermal and bathymetric niches that generally demonstrated low levels of overlap throughout the year. Our results indicate that isolating mechanisms, such as differential habitat selection during spawning, might contribute to maintaining diversity and fine-scale population structure in broadcast-spawning marine fishes.     

Introducing a method for extracting horizontal migration patterns from data storage tags

While data storage tags typically provide information about depth and temperature, the horizontal position of fish is difficult to obtain. The objective of this study is therefore to introduce a method for reconstructing horizontal migration patterns of fish tagged with DSTs. The method works by: establishing a database on bathymetry and environmental information about the target area, moving a large number of virtual fish between the release and recapture positions using a biased random walk procedure, and then terminate trajectories where the information at position is in disagreement with the tag information. For example a trajectory is terminated if the tag depth is greater than the bottom depth. The method is exemplified with two tag recordings from Northeast Arctic cod (Gadus morhua L.) in the Barents Sea. The results show that termination of impossible trajectories limits the number of potential trajectories between release and recapture positions, and in particular the usage of multiple termination criteria (depth and temperature) proved to be effective in reducing the number of possible trajectories. The method is general, simple to use, and can also be used in combination with geolocation methods.     

Harvest selection on Atlantic cod behavioral traits: implications for spatial management

Harvesting wild populations may contrast or reinforce natural agents of selection and potentially cause evolutionary changes in life-history traits such as growth and maturation. Harvest selection may also act on behavioral traits, although this field of research has so far received less attention. We used acoustic tags and a network of receivers to monitor the behavior and fate of individual Atlantic cod (Gadus morhua, N = 60) in their natural habitat on the Norwegian Skagerrak coast. Fish with a strong diel vertical migration, alternating between shallow- and deep-water habitats, had a higher risk of being captured in the fishery (traps, gillnet, hand line) as compared to fish that stayed in deeper water. There was also a significant negative correlation between fish size (30-66 cm) and the magnitude of diel vertical migration. Natural selection on behavior was less clear, but tended to favor fish with a large activity space. On a monthly time scale we found significant repeatabilities for cod behavior, meaning that individual characteristics tended to persist and therefore may be termed personality traits. We argue that an evolutionary approach to fisheries management should consider fish behavior. This would be of particular relevance for spatial management actions such as marine reserve design.     

Genetic differentiation among Atlantic cod in south and south-east Icelandic waters: synaptophysin (Syp I) and haemoglobin (HbI) variation

Significant differences were found at the synaptophysin ( Syp I) locus between two groups of Icelandic cod Gadus morhua ; Loftstaõahraun (spawning ground), Reykjanesgrunn and Eyrabakkabugur (feeding grounds) on the one hand and Kantur (spawning ground) and Austfjarõadjúp (feeding ground) on the other. There was also a considerable genetic heterogeneity within the former group. The results indicate that the cod in south and south-east Icelandic waters do not belong to one panmictic population.     

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.     

Individual variation in migratory movements and winter behaviour of Iberian Lesser Kestrels Falco naumanni revealed by geolocators

The population decline of the Lesser Kestrel Falco naumanni has been the subject of studies across its Western Palaearctic breeding range, but little is known about its use of pre‐migratory areas or African wintering quarters. We used geolocators to describe the temporal and spatial patterns of Portuguese Lesser Kestrel migration and wintering behaviour. Data on the complete migration were obtained from four individuals and another three provided further information. Prior to southward migration, Lesser Kestrels showed two different behaviours: northward‐orientated movements to Spain and movements in the proximity of the breeding area. Autumn migration took place mostly in late September; spring departures occurred mainly in the first half of February. Wintering grounds included Senegal, Mauritania and Mali, with individuals overlapping considerably in Senegal. Movements registered within the wintering grounds suggest itinerant behaviour in relation to local flushes of prey. During spring migration, birds crossed the Sahara Desert through Mauritania, Western Sahara and Morocco before passing over the Mediterranean to reach Portugal. Autumn migration lasted 4.8 ± 1.1 days, and spring migration lasted 4.1 ± 0.3 days. The mean daily flight range varied between approximately 300 and 850 km for an entire journey of around 2500 km. Effective protection of roosting sites in both pre‐migratory and wintering areas and maintaining grasshopper populations in Sahelian wintering quarters appear crucial in preserving this threatened migratory raptor across its African–Eurasian flyway. There was no evidence of any deleterious effects of fitting birds with loggers.