Links between the three-dimensional movements of whale sharks (Rhincodon typus) and the bio-physical environment off a coral reef.

BACKGROUND: Measuring coastal-pelagic prey fields at scales relevant to the movements of marine predators is challenging due to the dynamic and ephemeral nature of these environments. Whale sharks (Rhincodon typus) are thought to aggregate in nearshore tropical waters due to seasonally enhanced foraging opportunities. This implies that the three-dimensional movements of these animals may be associated with bio-physical properties that enhance prey availability. To date, few studies have tested this hypothesis. METHODS: Here, we conducted ship-based acoustic surveys, net tows and water column profiling (salinity, temperature, chlorophyll fluorescence) to determine the volumetric density, distribution and community composition of mesozooplankton (predominantly euphausiids and copepods) and oceanographic properties of the water column in the vicinity of whale sharks that were tracked simultaneously using satellite-linked tags at Ningaloo Reef, Western Australia. Generalised linear mixed effect models were used to explore relationships between the 3-dimensional movement behaviours of tracked sharks and surrounding prey fields at a spatial scale of ~ 1 km. RESULTS: We identified prey density as a significant driver of horizontal space use, with sharks occupying areas along the reef edge where densities were highest. These areas were characterised by complex bathymetry such as reef gutters and pinnacles. Temperature and salinity profiles revealed a well-mixed water column above the height of the bathymetry (top 40 m of the water column). Regions of stronger stratification were associated with reef gutters and pinnacles that concentrated prey near the seabed, and entrained productivity at local scales (~ 1 km). We found no quantitative relationship between the depth use of sharks and vertical distributions of horizontally averaged prey density. Whale sharks repeatedly dove to depths where spatially averaged prey concentration was highest but did not extend the time spent at these depth layers. CONCLUSIONS: Our work reveals previously unrecognized complexity in interactions between whale sharks and their zooplankton prey.

Variability in prey field structure drives inter-annual differences in prey encounter by a marine predator, the little penguin.

Understanding how marine predators encounter prey across patchy landscapes remains challenging due to difficulties in measuring the three-dimensional structure of pelagic prey fields at scales relevant to animal movement. We measured at-sea behaviour of a central-place forager, the little penguin (Eudyptula minor), over 5 years (2015-2019) using GPS and dive loggers. We made contemporaneous measurements of the prey field within the penguins' foraging range via boat-based acoustic surveys. We developed a prey encounter index by comparing estimates of acoustic prey density encountered along actual penguin tracks to those encountered along simulated penguin tracks with the same characteristics as real tracks but that moved randomly through the prey field. In most years, penguin tracks encountered prey better than simulated random movements greater than 99% of the time, and penguin dive depths matched peaks in the vertical distribution of prey. However, when prey was unusually sparse and/or deep, penguins had worse than random prey encounter indices, exhibited dives that mismatched depth of maximum prey density, and females had abnormally low body mass (5.3% lower than average). Reductions in prey encounters owing to decreases in the density or accessibility of prey may ultimately lead to reduced fitness and population declines in central-place foraging marine predators.

Ecosystem approach to harvesting in the Arctic: Walking the tightrope between exploitation and conservation in the Barents Sea.

Projecting the consequences of warming and sea-ice loss for Arctic marine food web and fisheries is challenging due to the intricate relationships between biology and ice. We used StrathE2EPolar, an end-to-end (microbes-to-megafauna) food web model incorporating ice-dependencies to simulate climate-fisheries interactions in the Barents Sea. The model was driven by output from the NEMO-MEDUSA earth system model, assuming RCP 8.5 atmospheric forcing. The Barents Sea was projected to be > 95% ice-free all year-round by the 2040s compared to > 50% in the 2010s, and approximately 2 °C warmer. Fisheries management reference points (FMSY and BMSY) for demersal fish (cod, haddock) were projected to increase by around 6%, indicating higher productivity. However, planktivorous fish (capelin, herring) reference points were projected to decrease by 15%, and upper trophic levels (birds, mammals) were strongly sensitive to planktivorous fish harvesting. The results indicate difficult trade-offs ahead, between harvesting and conservation of ecosystem structure and function.

Krill and salp faecal pellets contribute equally to the carbon flux at the Antarctic Peninsula.

Krill and salps are important for carbon flux in the Southern Ocean, but the extent of their contribution and the consequences of shifts in dominance from krill to salps remain unclear. We present a direct comparison of the contribution of krill and salp faecal pellets (FP) to vertical carbon flux at the Antarctic Peninsula using a combination of sediment traps, FP production, carbon content, microbial degradation, and krill and salp abundances. Salps produce 4-fold more FP carbon than krill, but the FP from both species contribute equally to the carbon flux at 300 m, accounting for 75% of total carbon. Krill FP are exported to 72% to 300 m, while 80% of salp FP are retained in the mixed layer due to fragmentation. Thus, declining krill abundances could lead to decreased carbon flux, indicating that the Antarctic Peninsula could become a less efficient carbon sink for anthropogenic CO2 in future.

Gill Transcriptomic Responses to Toxin-producing Alga Prymnesium parvum in Rainbow Trout.

The gill of teleost fish is a multifunctional organ involved in many physiological processes, including protection of the mucosal gill surface against pathogens and other environmental antigens by the gill-associated lymphoid tissue (GIALT). Climate change associated phenomena, such as increasing frequency and magnitude of harmful algal blooms (HABs) put extra strain on gill function, contributing to enhanced fish mortality and fish kills. However, the molecular basis of the HAB-induced gill injury remains largely unknown due to the lack of high-throughput transcriptomic studies performed on teleost fish in laboratory conditions. We used juvenile rainbow trout (Oncorhynchus mykiss) to investigate the transcriptomic responses of the gill tissue to two (high and low) sublethal densities of the toxin-producing alga Prymnesium parvum, in relation to non-exposed control fish. The exposure time to P. parvum (4-5 h) was sufficient to identify three different phenotypic responses among the exposed fish, enabling us to focus on the common gill transcriptomic responses to P. parvum that were independent of dose and phenotype. The inspection of common differentially expressed genes (DEGs), canonical pathways, upstream regulators and downstream effects pointed towards P. parvum-induced inflammatory response and gill inflammation driven by alterations of Acute Phase Response Signalling, IL-6 Signalling, IL-10 Signalling, Role of PKR in Interferon Induction and Antiviral Response, IL-8 Signalling and IL-17 Signalling pathways. While we could not determine if the inferred gill inflammation was progressing or resolving, our study clearly suggests that P. parvum blooms may contribute to the serious gill disorders in fish. By providing insights into the gill transcriptomic responses to toxin-producing P. parvum in teleost fish, our research opens new avenues for investigating how to monitor and mitigate toxicity of HABs before they become lethal.

Sampling the fish gill microbiome: a comparison of tissue biopsies and swabs.

BACKGROUND: Understanding the influence of methodology on results is an essential consideration in experimental design. In the expanding field of fish microbiology, many best practices and targeted techniques remain to be refined. This study aimed to compare microbial assemblages obtained from Atlantic salmon (Salmo salar) gills by swabbing versus biopsy excision. Results demonstrate the variation introduced by altered sampling strategies and enhance the available knowledge of the fish gill microbiome. RESULTS: The microbiome was sampled using swabs and biopsies from fish gills, with identical treatment of samples for 16S next generation Illumina sequencing. Results show a clear divergence in microbial communities obtained through the different sampling strategies, with swabbing consistently isolating a more diverse microbial consortia, and suffering less from the technical issue of host DNA contamination associated with biopsy use. Sequencing results from biopsy-derived extractions, however, hint at the potential for more cryptic localisation of some community members. CONCLUSIONS: Overall, results demonstrate a divergence in the obtained microbial community when different sampling methodology is used. Swabbing appears a superior method for sampling the microbiota of mucosal surfaces for broad ecological research in fish, whilst biopsies might be best applied in exploration of communities beyond the reach of swabs, such as sub-surface and intracellular microbes, as well as in pathogen diagnosis. Most studies on the external microbial communities of aquatic organisms utilise swabbing for sample collection, likely due to convenience. Much of the ultrastructure of gill tissue in live fish is, however, potentially inaccessible to swabbing, meaning swabbing might fail to capture the full diversity of gill microbiota. This work therefore also provides valuable insight into partitioning of the gill microbiota, informing varied applications of different sampling methods in experimental design for future research.

The Simrad EK60 echosounder dataset from the Malaspina circumnavigation.

We provide the raw acoustic data collected from the R/V Hesperides during the global Malaspina 2010 Spanish Circumnavigation Expedition (14th December 2010, Cádiz-14th July 2011, Cartagena) using a Simrad EK60 scientific echosounder operating at 38 and 120 kHz. The cruise was divided into seven legs: leg 1 (14th December 2010, Cádiz-13th January 2011, Rio de Janeiro), leg 2 (17th January 2011, Rio de Janeiro-6th February 2011, Cape Town), leg 3 (11th February 2011, Cape Town-13th March 2011, Perth), leg 4 (17th March 2011, Perth-30th March 2011, Sydney), leg 5 (16th April 2011, Auckland-8th May 2011, Honolulu), leg 6 (13th May 2011, Honolulu-10th June 2011, Cartagena de Indias) and leg 7 (19th June 2011, Cartagena de Indias-14th July 2011, Cartagena). The echosounder was calibrated at the start of the expedition and calibration parameters were updated in the data acquisition software (ER60) i.e., the logged raw data are calibrated. We also provide a data summary of the acoustic data in the form of post-processed products.

Oxidative stress, metabolic activity and mercury concentrations in Antarctic krill Euphausia superba and myctophid fish of the Southern Ocean.

Indicators of oxidative stress and metabolic capacity are key factors in understanding the fitness of wild populations. In the present study, these factors were evaluated in the pelagic Southern Ocean taxa Antarctic krill (Euphausia superba) and myctophid fish (Electrona antarctica, Gymnoscopelus braueri and G. nicholsi) to establish a baseline record for future studies. Mercury (Hg) concentrations were also analysed to evaluate its potential impacts on species biochemical performance. E. superba had higher metabolic activity than most of the myctophid species, which may explain the comparatively lower energy reserves found in the former. The activity of antioxidant enzymes showed, generally, a lower level in E. superba than in the myctophid species. The lack of any relationship between Hg concentrations and organisms' antioxidant and biotransformation defence mechanisms indicate that levels of Hg accumulated in the studied species were not high enough to affect their biochemical processes adversely.

Mercury biomagnification in a Southern Ocean food web.

Biomagnification of mercury (Hg) in the Scotia Sea food web of the Southern Ocean was examined using the stable isotope ratios of nitrogen (δ15N) and carbon (δ13C) as proxies for trophic level and feeding habitat, respectively. Total Hg and stable isotopes were measured in samples of particulate organic matter (POM), zooplankton, squid, myctophid fish, notothenioid fish and seabird tissues collected in two years (austral summers 2007/08 and 2016/17). Overall, there was extensive overlap in δ13C values across taxonomic groups suggesting similarities in habitats, with the exception of the seabirds, which showed some differences, possibly due to the type of tissue analysed (feathers instead of muscle). δ15N showed increasing enrichment across groups in the order POM to zooplankton to squid to myctophid fish to notothenioid fish to seabirds. There were significant differences in δ15N and δ13C values among species within taxonomic groups, reflecting inter-specific variation in diet. Hg concentrations increased with trophic level, with the lowest values in POM (0.0005 ± 0.0002 µg g-1 dw) and highest values in seabirds (3.88 ± 2.41 µg g-1 in chicks of brown skuas Stercorarius antarcticus). Hg concentrations tended to be lower in 2016/17 than in 2007/08 for mid-trophic level species (squid and fish), but the opposite was found for top predators (i.e. seabirds), which had higher levels in the 2016/17 samples. This may reflect an interannual shift in the Scotia Sea marine food web, caused by the reduced availability of a key prey species, Antarctic krill Euphausia superba. In 2016/17, seabirds would have been forced to feed on higher trophic-level prey, such as myctophids, that have higher Hg burdens. These results suggest that changes in the food web are likely to affect the pathway of mercury to Southern Ocean top predators.

Bayesian Network Analysis reveals resilience of the jellyfish Aurelia aurita to an Irish Sea regime shift.

Robust time-series of direct observations of jellyfish abundance are not available for many ecosystems, leaving it difficult to determine changes in jellyfish abundance, the possible causes (e.g. climate change) or the consequences (e.g. trophic cascades). We sought an indirect ecological route to reconstruct jellyfish abundance in the Irish Sea: since zooplankton are jellyfish prey, historic variability in zooplankton communities may provide proxies for jellyfish abundance. We determined the Bayesian ecological network of jellyfish-zooplankton dependencies using jellyfish- and zooplankton-abundance data obtained using nets during a 2-week cruise to the Irish Sea in 2008. This network revealed that Aurelia aurita abundance was dependent on zooplankton groups Warm Temperate and Temperate Oceanic as defined by previous zooplankton ecology work. We then determined historic zooplankton networks across the Irish Sea from abundance data from Continuous Plankton Recorder surveys conducted between 1970 and 2000. Transposing the 2008 spatial dependencies onto the historic networks revealed that Aurelia abundance was more strongly dependent over time on sea surface temperature than on the zooplankton community. The generalist predatory abilities of Aurelia may have insulated this jellyfish over the 1985 regime shift when zooplankton composition in the Irish Sea changed abruptly, and also help explain its globally widespread distribution.

Improved bathymetry leads to >4000 new seamount predictions in the global ocean - but beware of phantom seamounts!

Seamounts are important marine habitats that are hotspots of species diversity. Relatively shallow peaks, increased productivity and offshore locations make seamounts vulnerable to human impact and difficult to protect. Present estimates of seamount numbers vary from anywhere between 10,000 to more than 60,000. Seamount locations can be estimated by extracting large, cone-like features from bathymetry grids (based on criteria of size and shape). These predicted seamounts are a useful reference for marine researchers and can help direct exploratory surveys. However, these predictions are dependent on the quality of the surveys underpinning the bathymetry. Historically, quality has been patchy, but is improving as mapping efforts step up towards the target of complete seabed coverage by 2030. This study presents an update of seamount predictions based on SRTM30 PLUS global bathymetry version 11 and examines a potential source of error in these predictions. This update was prompted by a seamount survey in the British Indian Ocean Territory in 2016, where locations of two putative seamounts were visited. These 'seamounts' were targeted based on previous predictions, but these features were not detected during echosounder surveys. An examination of UK hydrographic office navigational (Admiralty) charts for the area showed that the summits of these putative features had soundings reporting 'no bottom detected at this depth' where 'this depth' was similar to the seabed reported from the bathymetry grids: we suspect that these features likely resulted from an initial misreading of the charts. We show that 15 'phantom seamount' features, derived from a misinterpretation of no bottom sounding data, persist in current global bathymetry grids and updated seamount predictions. Overall, we predict 37,889 seamounts, an increase of 4437 from the previous predictions derived from an older global bathymetry grid (SRTM30 PLUS v6). This increase is due to greater detail in newer bathymetry grids as acoustic mapping of the seabed expands. The new seamount predictions are available at https://doi.pangaea.de/10.1594/PANGAEA.921688.

Main drivers of mercury levels in Southern Ocean lantern fish Myctophidae.

Myctophids are the most abundant fish group in the Southern Ocean pelagic ecosystem and are an important link in the Antarctic marine food web. Due to their major ecological role, evaluating the level of mercury (Hg) contamination in myctophids is important as a step towards understanding the trophic pathway of this contaminant. The concentrations of total Hg were determined in muscle, gill, heart and liver tissue of 9 myctophid species to quantify tissue partitioning variability between species. Organic Hg concentration and proportion in muscle was also determined. Hg concentrations were higher in the liver and heart than in muscle and gills, but the proportion of organic Hg was almost 100% in muscle, indicating that the main uptake route for Hg is through the diet. Most of the species analysed have similar vertical and horizontal distributions, and similar feeding modes and prey. Geographical and temporal variability of Hg concentrations was examined using samples from 3 different sampling cruise (2007/08, 2015/16 and 2016/17) and 2 locations (South Georgia and South Orkneys Islands). Our results appear to indicate a decreasing trend in Hg contamination over the last decade, particularly gill tissue, which is in agreement with a previous study on squid from the same region. There was no significant variability in Hg concentration between the different sampling locations. Hg levels were consistent with values reported previously for myctophids around the world, indicating low global-scale geographic variability. A positive relationship between fish size and Hg concentration was found for most species, with the exception of Electrona antarctica females, which may be explained through Hg elimination by egg laying. We estimate that myctophids collectively comprise a Southern Ocean mercury 'reserve' of ≈1.82 metric tonnes.

Microplastic study reveals the presence of natural and synthetic fibres in the diet of King Penguins (Aptenodytes patagonicus) foraging from South Georgia.

Marine ecosystems are experiencing substantial disturbances due to climate change and overfishing, and plastic pollution is an additional growing threat. Microfibres are among the most pervasive pollutants in the marine environment, including in the Southern Ocean. However, evidence for microfibre contamination in the diet of top predators in the Southern Ocean is rare. King Penguins (Aptenodytes patagonicus) feed on mesopelagic fish, which undergo diel vertical migrations towards the surface at night. Microfibres are concentrated in surface waters and sediments but can also be concentrated in fish, therefore acting as contamination vectors for diving predators feeding at depth. In this study, we investigate microfibre contamination of King Penguin faecal samples collected in February and March 2017 at South Georgia across three groups: incubating, chick-rearing and non-breeding birds. After a KOH digestion to dissolve the organic matter and a density separation step using a NaCl solution, the samples were filtered to collect microfibres. A total of 77% of the penguin faecal samples (36 of 47) contained microfibres. Fibres were measured and characterized using Fourier-Transform Infrared spectroscopy to determine their polymeric identity. Most fibres (88%) were made of natural cellulosic materials (e.g. cotton, linen), with only 12% synthetic (e.g. polyester, nylon) or semi-synthetic (e.g. rayon). An average of 21.9 ±â€¯5.8 microfibres g-1 of faeces (lab dried mass) was found, with concentrations more than twice as high in incubating penguins than in penguins rearing chicks. Incubating birds forage further north at the Antarctic Polar Front and travel longer distances from South Georgia than chick-rearing birds. This suggests that long-distance travelling penguins are probably more exposed to the risk of ingesting microfibres when feeding north of the Antarctic Polar Front, which might act as a semi-permeable barrier for microfibres. Microfibres could therefore provide a signature for foraging location in King Penguins.

Mercury levels in Southern Ocean squid: Variability over the last decade.

The concentrations of total and proportions of organic mercury were measured in tissues of 355 individuals of 8 species of Southern Ocean squid (Alluroteuthis antarcticus, Bathyteuthis abyssicola, Filippovia knipovitchi, Galiteuthis glacialis, Gonatus antarcticus, Kondakovia longimana, Psychroteuthis glacialis and Slosarczykovia circumantarctica). Squid were caught around South Georgia (Scotia Sea) during 5 cruises, between the austral summers of 2006/07 to 2016/17 to evaluate temporal changes in bioaccumulation and tissue partitioning. Total mercury concentrations varied between 4 ng g-1 and 804 ng g-1 among all tissues. Net accumulation of mercury in muscle with size was observed in A. antarcticus, B. abyssicola and P. glacialis, but no relationship was found for S. circumantarctica and lower concentrations were observed in larger individuals of G. glacialis. Muscle tissues had the highest mercury concentrations in the majority of species, except for F. knipovitchi for which the digestive gland contained highest concentrations. In terms of the percentage of organic mercury in the tissues, muscle always contained the highest values (67%-97%), followed by the digestive gland (22%-38%). Lowest organic mercury percentages were found consistently in the gills (9%-19%), suggesting only low levels of incorporation through the dissolved pathway and/or a limited redistribution of dietary organic mercury towards this tissue. Overall, results are indicative of a decreasing trend of mercury concentrations in the majority of analysed species over the last decade. As cephalopods are an important Southern Ocean trophic link between primary consumers and top predators, these changes suggest decreasing mercury levels in lower trophic levels and an alleviation of the mercury burden on higher predators that consume squid.

Spatial variability in total and organic mercury levels in Antarctic krill Euphausia superba across the Scotia Sea.

Total and organic mercury concentrations were determined for males, females and juveniles of Euphausia superba collected at three discrete locations in the Scotia Sea (South Orkney Islands, South Georgia and Antarctic Polar Front) to assess spatial mercury variability in Antarctic krill. There was clear geographic differentiation in mercury concentrations, with specimens from the South Orkney Islands having total mercury concentrations 5 to 7 times higher than Antarctic krill from South Georgia and the Antarctic Polar Front. Mercury did not appear to accumulate with life-stage since juveniles had higher concentrations of total mercury (0.071 µg g-1 from South Orkney Islands; 0.014 µg g-1 from South Georgia) than adults (0.054 µg g-1 in females and 0.048 µg g-1 in males from South Orkney Islands; 0.006 µg g-1 in females and 0.007 µg g-1 in males from South Georgia). Results suggest that females may use egg laying as a mechanism to excrete mercury, with eggs having higher concentrations than the corresponding somatic tissue. Organic mercury makes up a minor percentage of total mercury (15-37%) with the percentage being greater in adults than in juveniles. When compared to euphausiids from other parts of the world, the concentration of mercury in Antarctic krill is within the same range, or higher, highlighting the global distribution of this contaminant. Given the high potential for biomagnification of mercury through food webs, concentrations in Antarctic krill may have deleterious effects on long-lived Antarctic krill predators.

Plankton.

Plankton comprises unicellular plants - phytoplankton - and generally small (millimetres or less) animals - zooplankton - that are adrift on the currents. Phytoplankton are responsible for about 45% of global annual primary production and are grazed by zooplankton, which in turn are suitably sized food items for predators including commercially important fish and great whales. Plankton are vital components of marine and freshwater water-column ecosystems. They also make major contributions to global biogeochemical cycling, and ameliorate atmospheric accumulation of carbon dioxide by 'pumping' carbon to the deep sea. The integrity of these roles is under threat from climate-related physiological impacts on individual organisms and on the wide-scale distribution of plankton communities.

Biogeography of the Global Ocean's Mesopelagic Zone.

The global ocean's near surface can be partitioned into distinct provinces on the basis of regional primary productivity and oceanography [1]. This ecological geography provides a valuable framework for understanding spatial variability in ecosystem function but has relevance only partway into the epipelagic zone (the top 200 m). The mesopelagic (200-1,000 m) makes up approximately 20% of the global ocean volume, plays important roles in biogeochemical cycling [2], and holds potentially huge fish resources [3-5]. It is, however, hidden from satellite observation, and a lack of globally consistent data has prevented development of a global-scale understanding. Acoustic deep scattering layers (DSLs) are prominent features of the mesopelagic. These vertically narrow (tens to hundreds of m) but horizontally extensive (continuous for tens to thousands of km) layers comprise fish and zooplankton and are readily detectable using echosounders. We have compiled a database of DSL characteristics globally. We show that DSL depth and acoustic backscattering intensity (a measure of biomass) can be modeled accurately using just surface primary productivity, temperature, and wind stress. Spatial variability in these environmental factors leads to a natural partition of the mesopelagic into ten distinct classes. These classes demark a more complex biogeography than the latitudinally banded schemes proposed before [6, 7]. Knowledge of how environmental factors influence the mesopelagic enables future change to be explored: we predict that by 2100 there will be widespread homogenization of mesopelagic communities and that mesopelagic biomass could increase by approximately 17%. The biomass increase requires increased trophic efficiency, which could arise because of ocean warming and DSL shallowing.

Moonlight Drives Ocean-Scale Mass Vertical Migration of Zooplankton during the Arctic Winter.

In extreme high-latitude marine environments that are without solar illumination in winter, light-mediated patterns of biological migration have historically been considered non-existent [1]. However, diel vertical migration (DVM) of zooplankton has been shown to occur even during the darkest part of the polar night, when illumination levels are exceptionally low [2, 3]. This paradox is, as yet, unexplained. Here, we present evidence of an unexpected uniform behavior across the entire Arctic, in fjord, shelf, slope and open sea, where vertical migrations of zooplankton are driven by lunar illumination. A shift from solar-day (24-hr period) to lunar-day (24.8-hr period) vertical migration takes place in winter when the moon rises above the horizon. Further, mass sinking of zooplankton from the surface waters and accumulation at a depth of ∼50 m occurs every 29.5 days in winter, coincident with the periods of full moon. Moonlight may enable predation of zooplankton by carnivorous zooplankters, fish, and birds now known to feed during the polar night [4]. Although primary production is almost nil at this time, lunar vertical migration (LVM) may facilitate monthly pulses of carbon remineralization, as they occur continuously in illuminated mesopelagic systems [5], due to community respiration of carnivorous and detritivorous zooplankton. The extent of LVM during the winter suggests that the behavior is highly conserved and adaptive and therefore needs to be considered as "baseline" zooplankton activity in a changing Arctic ocean [6-9]. VIDEO ABSTRACT.