Environmental preferences and critical habitat for the velvet belly lanternshark (Etmopterus spinax) in Icelandic waters.

The velvet belly lanternshark (Etmopterus spinax) is a small, bioluminescent shark that is caught as bycatch in many deep-sea fisheries in the Atlantic Ocean. Using data from 10,597 seasonal research survey tows spanning 11 years, the distribution, relative abundance, life history, and environmental preferences of E. spinax in Icelandic waters was examined for the first time. E. spinax (n = 8774) were only captured in relatively deep offshore waters to the south and west of Iceland. Females grew to larger sizes than males and reached 50% sexual maturity at a total length of 50 cm. Females at a late stage of maturity and very small juveniles (<20 cm) were restricted to the central south Icelandic shelf, suggesting that this might be critical habitat for the reproduction of the species. Most of the sharks were captured at depths of 400-500 m, a relatively narrow depth range, and classified as a stenothermic warm-water species with habitat temperature restricted to about 6.3-8.0°C. Teleosts, crustaceans and cephalopods made up most of the diet. There was no indication of a decline in abundance over the time span of the survey. However, climate-induced warming of the deep ocean may shift the distribution of the species to more northerly waters within Iceland.

Species independence of eye lens dimensions in teleosts and elasmobranchs.

The vertebrate eye lens grows incrementally, adding layers of elongated, tightly packed lens fiber cells at the outer margin of the lens. With subsequent growth, previously-deposited fiber cells degrade, leaving a region of fully denucleated and organelle-free cells which are responsible for the high transparency and low light scattering characteristics of the lens. The objective of this study was to determine if the horizon separating the gelatinous outer cortex of the lens from its hardened interior occurred at a consistent location within the lens of several teleost and elasmobranch fish species, and could be linked to fiber cell morphology or function. A fixed ratio of 0.69±0.01 of hardened eye lens diameter (HD) to overall eye lens diameter (LD) was observed in a broad size range of Atlantic cod (Gadus morhua), haddock (Melanogrammus aeglefinus), thorny skate (Amblyraja radiata) and round ray (Rajella fyllae). The location of the hardened lens horizon was similar to that reported for optical plasticity and spherical aberration, but not that of fiber cell denucleation, suggesting that fiber cell dehydration continues after the loss of internal organelles. Our findings support a previous suggestion that the maintenance of optical quality during fish eye lens growth requires a precisely-fixed HD:LD ratio, while the ubiquity of a fixed ratio across fish taxa may suggest that many fish species possess a common refractive index profile. The linear relationship between HD and fish length should allow fish length to be backcalculated from the diameter of the isolated lens core, thus aiding research using isotope ratios of lens laminae or inner cores to reconstruct early life history events.

Growth portfolios buffer climate-linked environmental change in marine systems.

Large-scale, climate-induced synchrony in the productivity of fish populations is becoming more pronounced in the world's oceans. As synchrony increases, a population's "portfolio" of responses can be diminished, in turn reducing its resilience to strong perturbation. Here we argue that the costs and benefits of trait synchronization, such as the expression of growth rate, are context dependent. Contrary to prevailing views, synchrony among individuals could actually be beneficial for populations if growth synchrony increases during favorable conditions, and then declines under poor conditions when a broader portfolio of responses could be useful. Importantly, growth synchrony among individuals within populations has seldom been measured, despite well-documented evidence of synchrony across populations. Here, we used century-scale time series of annual otolith growth to test for changes in growth synchronization among individuals within multiple populations of a marine keystone species (Atlantic cod, Gadus morhua). On the basis of 74,662 annual growth increments recorded in 13,749 otoliths, we detected a rising conformity in long-term growth rates within five northeast Atlantic cod populations in response to both favorable growth conditions and a large-scale, multidecadal mode of climate variability similar to the East Atlantic Pattern. The within-population synchrony was distinct from the across-population synchrony commonly reported for large-scale environmental drivers. Climate-linked, among-individual growth synchrony was also identified in other Northeast Atlantic pelagic, deep-sea and bivalve species. We hypothesize that growth synchrony in good years and growth asynchrony in poorer years reflects adaptive trait optimization and bet hedging, respectively, that could confer an unexpected, but pervasive and stabilizing, impact on marine population productivity in response to large-scale environmental change.

The effect of growth rate on otolith-based discrimination of cod (Gadus morhua) ecotypes.

Otolith shape has previously been used to identify ecotypes within the Icelandic cod (Gadus morhua) stock, using DST profiles to validate the results. Fish otolith shape variation has repeatedly been found to be largely determined by growth rate. To examine the effect of growth rate on the relationship between otolith shape and cod ecotypes (using the Pan I genotype as a proxy for ecotype), 826 archived sagittal otoliths collected over a 58 year sampling period were retrieved, the individual growth rate calculated, and otolith shape described using both Normalized Elliptic Fourier transform and Discrete Wavelet transform. Discriminant functions of otolith shape successfully classified ecotype, whether using Fourier or Wavelet descriptors, but only when excluding a heterozygous genotype from the analysis. The otolith shape variability of this genotype lowered the classification success, while otolith shape, in turn, was significantly affected by growth rate and cohort. Growth rate differences previously reported for the ecotypes were present, but were less marked than expected and indeed, growth rate variance attributable to ecotype identity was dwarfed by cohort- and location-related variance in growth. Such a strong effect of growth rate suggests that cod ecotype discrimination based on otolith shape is sensitive to both temporal and spatial variations in growth, which can mask the effect of ecotype-related growth rate differences on otolith shape.

Differences in metabolic rate between two Atlantic cod (Gadus morhua) populations estimated with carbon isotopic composition in otoliths.

The isotopic composition of inorganic carbon in otoliths (δ13Coto) can be a useful tracer of metabolic rates and a method to study ecophysiology in wild fish. We evaluated environmental and physiological sources of δ13Coto variation in Icelandic and Northeast Arctic (NEA) cod (Gadus morhua) over the years 1914-2013. Individual annual growth increments of otoliths formed at age 3 and 8 were micromilled and measured by isotope-ratio mass spectrometry. Simultaneously, all annual increment widths of the otoliths were measured providing a proxy of fish somatic growth. We hypothesized that changes in the physiological state of the organism, reflected by the isotopic composition of otoliths, can affect the growth rate. Using univariate and multivariate mixed-effects models we estimated conditional correlations between carbon isotopic composition and growth of fish at different levels (within individuals, between individuals, and between years), controlling for intrinsic and extrinsic effects on both otolith measurements. δ13Coto was correlated with growth within individuals and between years, which was attributed to the intrinsic effects (fish age or total length). There was no significant correlation between δ13Coto and growth between individuals, which suggests that caution is needed when interpreting δ13Coto signals. We found a significant decrease in δ13Coto through the century which was explained by the oceanic Suess effect-admixture of isotopically light carbon from fossil fuel. We calculated the proportion of the respired carbon in otolith carbonate (Cresp) using carbon isotopic composition in diet and dissolved inorganic carbon of the seawater. This approach allowed us to correct the values for each stock in relation to these two environmental baselines. Cresp was on average 0.275 and 0.295 in Icelandic and NEA stock, respectively. Our results provide an insight into the physiological basis for differences in growth characteristics between these two cod stocks, and how that may vary over time.

Shifting fish distributions in warming sub-Arctic oceans.

The distributional response of marine fishes to climate warming would be expected to be very different than that of homeothermic birds and mammals, due both to more direct thermal effects on poikilothermic fish physiology and on reduced habitat fragmentation. In this study, we use a combination of linear models and graphical tools to quantify three-dimensional distribution shifts in 82 fish species caught in 5390 standardized groundfish survey tows over a 22-year time frame in the highly-productive sub-Arctic waters around Iceland. Over a 1 °C range, temperature significantly modified the distributional centroids of 72% of all fish species, but had relatively little effect on diversity. Most of the geographic shifts were to the northwest, and there was no overall tendency to move to deeper waters. A doubling of species abundance significantly influenced the distribution of 62% of species, but lacked the poleward orientation observed with temperature increases. Stenothermal species, those near their upper or lower thermal limits, and those with restricted spatial ranges were most likely to shift their distribution in response to climate warming, while deepwater species were not. A 2-3 °C warming of marine waters seems likely to produce large-scale changes in the location of many sub-Arctic fisheries.

Century-long cod otolith biochronology reveals individual growth plasticity in response to temperature.

Otolith biochronologies combine growth records from individual fish to produce long-term growth sequences, which can help to disentangle individual from population-level responses to environmental variability. This study assessed individual thermal plasticity of Atlantic cod (Gadus morhua) growth in Icelandic waters based on measurements of otolith increments. We applied linear mixed-effects models and developed a century-long growth biochronology (1908-2014). We demonstrated interannual and cohort-specific changes in the growth of Icelandic cod over the last century which were mainly driven by temperature variation. Temperature had contrasting relationships with growth-positive for the fish during the youngest ages and negative during the oldest ages. We decomposed the effects of temperature on growth observed at the population level into within-individual effects and among-individual effects and detected significant individual variation in the thermal plasticity of growth. Variance in the individual plasticity differed across cohorts and may be related to the mean environmental conditions experienced by the group. Our results underscore the complexity of the relationships between climatic conditions and the growth of fish at both the population and individual level, and highlight the need to distinguish between average population responses and growth plasticity of the individuals for accurate growth predictions.

A century of fish growth in relation to climate change, population dynamics and exploitation.

Marine ecosystems, particularly in high-latitude regions such as the Arctic, have been significantly affected by human activities and contributions to climate change. Evaluating how fish populations responded to past changes in their environment is helpful for evaluating their future patterns, but is often hindered by the lack of long-term biological data available. Using otolith increments of Northeast Arctic cod (Gadus morhua) as a proxy for individual growth, we developed a century-scale biochronology (1924-2014) based on the measurements of 3,894 fish, which revealed significant variations in cod growth over the last 91 years. We combined mixed-effect modeling and path analysis to relate these growth variations to selected climate, population and fishing-related factors. Cod growth was negatively related to cod population size and positively related to capelin population size, one of the most important prey items. This suggests that density-dependent effects are the main source of growth variability due to competition for resources and cannibalism. Growth was also positively correlated with warming sea temperatures but negatively correlated with the Atlantic Multidecadal Oscillation, suggesting contrasting effects of climate warming at different spatial scales. Fishing pressure had a significant but weak negative direct impact on growth. Additionally, path analysis revealed that the selected growth factors were interrelated. Capelin biomass was positively related to sea temperature and negatively influenced by herring biomass, while cod biomass was mainly driven by fishing mortality. Together, these results give a better understanding of how multiple interacting factors have shaped cod growth throughout a century, both directly and indirectly.

Global spatial risk assessment of sharks under the footprint of fisheries.

Effective ocean management and the conservation of highly migratory species depend on resolving the overlap between animal movements and distributions, and fishing effort. However, this information is lacking at a global scale. Here we show, using a big-data approach that combines satellite-tracked movements of pelagic sharks and global fishing fleets, that 24% of the mean monthly space used by sharks falls under the footprint of pelagic longline fisheries. Space-use hotspots of commercially valuable sharks and of internationally protected species had the highest overlap with longlines (up to 76% and 64%, respectively), and were also associated with significant increases in fishing effort. We conclude that pelagic sharks have limited spatial refuge from current levels of fishing effort in marine areas beyond national jurisdictions (the high seas). Our results demonstrate an urgent need for conservation and management measures at high-seas hotspots of shark space use, and highlight the potential of simultaneous satellite surveillance of megafauna and fishers as a tool for near-real-time, dynamic management.

Ocean predation and mortality of adult Atlantic salmon.

Predation and mortality are often difficult to estimate in the ocean, which hampers the management and conservation of marine fishes. We used data from pop-up satellite archival tags to investigate the ocean predation and mortality of adult Atlantic salmon (Salmo salar) released from 12 rivers flowing into the North Atlantic Ocean. Data from 156 tagged fish revealed 22 definite predation events (14%) and 38 undetermined mortalities (24%). Endothermic fish were the most common predators (n = 13), with most of these predation events occurring in the Gulf of St. Lawrence and from the Bay of Biscay to the Irish Shelf. Predation by marine mammals, most likely large deep-diving toothed whales (n = 5), and large ectothermic fish (n = 4) were less frequent. Both the estimated predation rates (ZP) and total mortality rates (ZM) where higher for Atlantic salmon from Canada, Ireland, and Spain (ZP = 0.60-1.32 y-1, ZM = 1.73-3.08 y-1) than from Denmark and Norway (ZP = 0-0.13 y-1, ZM = 0.19-1.03 y-1). This geographical variation in ocean mortality correlates with ongoing population declines, which are more profound for southern populations, indicating that low ocean survival of adults may act as an additional stressor to already vulnerable populations.

Origins of the Greenland shark (Somniosus microcephalus): Impacts of ice-olation and introgression.

Herein, we use genetic data from 277 sleeper sharks to perform coalescent-based modeling to test the hypothesis of early Quaternary emergence of the Greenland shark (Somniosus microcephalus) from ancestral sleeper sharks in the Canadian Arctic-Subarctic region. Our results show that morphologically cryptic somniosids S. microcephalus and Somniosus pacificus can be genetically distinguished using combined mitochondrial and nuclear DNA markers. Our data confirm the presence of genetically admixed individuals in the Canadian Arctic and sub-Arctic, and temperate Eastern Atlantic regions, suggesting introgressive hybridization upon secondary contact following the initial species divergence. Conservative substitution rates fitted to an Isolation with Migration (IM) model indicate a likely species divergence time of 2.34 Ma, using the mitochondrial sequence DNA, which in conjunction with the geographic distribution of admixtures and Pacific signatures likely indicates speciation associated with processes other than the closing of the Isthmus of Panama. This time span coincides with further planetary cooling in the early Quaternary period followed by the onset of oscillating glacial-interglacial cycles. We propose that the initial S. microcephalus-S. pacificus split, and subsequent hybridization events, were likely associated with the onset of Pleistocene glacial oscillations, whereby fluctuating sea levels constrained connectivity among Arctic oceanic basins, Arctic marginal seas, and the North Atlantic Ocean. Our data demonstrates support for the evolutionary consequences of oscillatory vicariance via transient oceanic isolation with subsequent secondary contact associated with fluctuating sea levels throughout the Quaternary period-which may serve as a model for the origins of Arctic marine fauna on a broad taxonomic scale.

Listening in on the past: what can otolith δ18O values really tell us about the environmental history of fishes?

Oxygen isotope ratios from fish otoliths are used to discriminate marine stocks and reconstruct past climate, assuming that variations in otolith δ18O values closely reflect differences in temperature history of fish when accounting for salinity induced variability in water δ18O. To investigate this, we exploited the environmental and migratory data gathered from a decade using archival tags to study the behaviour of adult plaice (Pleuronectes platessa L.) in the North Sea. Based on the tag-derived monthly distributions of the fish and corresponding temperature and salinity estimates modelled across three consecutive years, we first predicted annual otolith δ18O values for three geographically discrete offshore sub-stocks, using three alternative plausible scenarios for otolith growth. Comparison of predicted vs. measured annual δ18O values demonstrated >96% correct prediction of sub-stock membership, irrespective of the otolith growth scenario. Pronounced inter-stock differences in δ18O values, notably in summer, provide a robust marker for reconstructing broad-scale plaice distribution in the North Sea. However, although largely congruent, measured and predicted annual δ18O values did not fully match [ corrected]. Small, but consistent, offsets were also observed between individual high-resolution otolith δ18O values measured during tag recording time and corresponding δ18O predictions using concomitant tag-recorded temperatures and location-specific salinity estimates. The nature of the shifts differed among sub-stocks, suggesting specific vital effects linked to variation in physiological response to temperature. Therefore, although otolith δ18O in free-ranging fish largely reflects environmental temperature and salinity, we counsel prudence when interpreting otolith δ18O data for stock discrimination or temperature reconstruction until the mechanisms underpinning otolith δ18O signature acquisition, and associated variation, are clarified.

Shark predation on migrating adult American eels (Anguilla rostrata) in the Gulf of St. Lawrence.

In an attempt to document the migratory pathways and the environmental conditions encountered by American eels during their oceanic migration to the Sargasso Sea, we tagged eight silver eels with miniature satellite pop-up tags during their migration from the St. Lawrence River in Québec, Canada. Surprisingly, of the seven tags that successfully transmitted archived data, six were ingested by warm-gutted predators, as observed by a sudden increase in water temperature. Gut temperatures were in the range of 20 to 25°C-too cold for marine mammals but within the range of endothermic fish. In order to identify the eel predators, we compared their vertical migratory behavior with those of satellite-tagged porbeagle shark and bluefin tuna, the only endothermic fishes occurring non-marginally in the Gulf of St. Lawrence. We accurately distinguished between tuna and shark by using the behavioral criteria generated by comparing the diving behavior of these two species with those of our unknown predators. Depth profile characteristics of most eel predators more closely resembled those of sharks than those of tuna. During the first days following tagging, all eels remained in surface waters and did not exhibit diel vertical migrations. Three eels were eaten at this time. Two eels exhibited inverse diel vertical migrations (at surface during the day) during several days prior to predation. Four eels were eaten during daytime, whereas the two night-predation events occurred at full moon. Although tagging itself may contribute to increasing the eel's susceptibility to predation, we discuss evidence suggesting that predation of silver-stage American eels by porbeagle sharks may represent a significant source of mortality inside the Gulf of St. Lawrence and raises the possibility that eels may represent a reliable, predictable food resource for porbeagle sharks.

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.

Stable oxygen isotope reconstruction of ambient temperature during the collapse of a cod (Gadus morhua) fishery.

Changing environmental conditions set against a backdrop of high exploitation can result in severe consequences for commercially harvested stocks. The collapse of the Eastern Scotian Shelf cod (Gadus morhua L.) off eastern Canada was primarily due to overexploitation but may have been exacerbated by a widespread temperature decline. Recent studies have called for accurate determination of ambient temperature (the actual temperature exposure history of the fish) before discarding environmental conditions as a factor in the collapse. We used the stable oxygen isotope composition of otoliths (delta18O(oto)) to reconstruct the ambient temperature history of Eastern Scotian Shelf cod from 1970 to 2000 in order to determine whether the stock experienced the temperature decline or shifted their distribution to avoid it. To correct delta18O(oto) for seawater isotope content (deltaO(w)), we generated a new meta-equation for the relationship between delta18O(w) (per mil) and salinity (S, in psu) on the Eastern Scotian Shelf: delta18O(w) = 0.539 x S - 18.790. The ambient temperature series revealed that the large-scale geographic distribution of mature cod remained constant through the cooling period, although their ambient temperature was cooler than expected in warmer periods and warmer than expected in cooler periods, indicating small-scale thermoregulatory movement. Although the mean hydrographic temperature was 4 degrees C, mature cod usually inhabited the coldest available waters (mean ambient temperature = 3 degrees C), while the juveniles usually inhabited warmer waters (mean ambient temperature = 5.5 degrees C). Length-at-age was significantly related to ambient temperature, especially in the early years of growth, and therefore declining ambient temperatures were at least partially responsible for declines in asymptotic length (up to age 8 yr). The most active thermoregulatory movement occurred during a moderate warming period; therefore extreme warming events (such as those predicted under climate change) may force large-scale northward latitudinal shifts in this historically sedentary stock. Retroactive stable isotope chronologies can be an important tool in sustainable management strategies under the shifting climate conditions predicted for years to come.

Global patterns in marine dispersal estimates: the influence of geography, taxonomic category and life history.

We examine estimates of dispersal in a broad range of marine species through an analysis of published values, and evaluate how well these values represent global patterns through a comparison with correlates of dispersal. Our analysis indicates a historical focus in dispersal studies on low-dispersal/low-latitude species, and we hypothesize that these studies are not generally applicable and representative of global patterns. Large-scale patterns in dispersal were examined using a database of correlates of dispersal such as planktonic larval duration (PLD, 318 species) and genetic differentiation (FST, 246 species). We observed significant differences in FST (p<0.001) and PLD (p<0.001) between taxonomic groups (e.g. fishes, cnidarians, etc.). Within marine fishes (more than 50% of datasets), the prevalence of demersal eggs was negatively associated with PLD (R2=0.80, p<0.001) and positively associated with genetic structure (R2=0.74, p<0.001). Furthermore, dispersal within marine fishes (i.e. PLD and FST) increased with latitude, adult body size and water depth. Of these variables, multiple regression identified latitude and body size as persistent predictors across taxonomic levels. These global patterns of dispersal represent a first step towards understanding and predicting species-level and regional differences in dispersal, and will be improved as more comprehensive data become available.