Decades of dietary data demonstrate regional food web structures in the Southern Ocean

Understanding regional‐scale food web structure in the Southern Ocean is critical to informing fisheries management and assessments of climate change impacts on Southern Ocean ecosystems and ecosystem services. Historically, a large component of Southern Ocean ecosystem research has focused on Antarctic krill, which provide a short, highly efficient food chain, linking primary producers to higher trophic levels. Over the last 15 years, the presence of alternative energy pathways has been identified and hypotheses on their relative importance in different regions raised. Using the largest circumpolar dietary database ever compiled, we tested these hypotheses using an empirical circumpolar comparison of food webs across the four major regions/sectors of the Southern Ocean (defined as south of 40°S) within the austral summer period. We used network analyses and generalizations of taxonomic food web structure to confirm that while Antarctic krill are dominant as the mid‐trophic level for the Atlantic and East Pacific food webs (including the Scotia Arc and Western Antarctic Peninsula), mesopelagic fish and other krill species are dominant contributors to predator diets in the Indian and West Pacific regions (East Antarctica and the Ross Sea). We also highlight how tracking data and habitat modeling for mobile top predators in the Southern Ocean show that these species integrate food webs over large regional scales. Our study provides a quantitative assessment, based on field observations, of the degree of regional differentiation in Southern Ocean food webs and the relative importance of alternative energy pathways between regions.     

The role of notothenioid fish in the food web of the Ross Sea shelf waters: a review

The Ross Sea, a large, high-latitude (72–78°S) embayment of the Antarctic continental shelf, averages 500 m deep, with troughs to 1,200 m and the shelf break at 700 m. It is covered by pack ice for 9 months of the year. The fish fauna of about 80 species includes primarily 4 families and 53 species of the endemic perciform suborder Notothenioidei. This review focuses on the diet and role in the food web of notothenioids and top-level bird and mammal predators, and also includes new information on the diets of artedidraconids and bathydraconids. Although principally a benthic group, notothenioids have diversified to form an adaptive radiation that includes pelagic and semipelagic species. In the southern Ross Sea, notothenioids dominate the fish fauna at levels of abundance and biomass >90% and are, therefore, inordinately important in the food web. Antarctic krill (Euphausia superba) and mesopelagic fishes are virtually absent from the shelf waters of the Ross Sea. Of the four notothenioid families, nototheniids show the most ecological and dietary diversification, with pelagic, cryopelagic, epibenthic and benthic species. Neutrally buoyant Pleuragramma antarcticum constitutes >90% of both the abundance and biomass of the midwater fish fauna. Most benthic nototheniids are opportunistic and feed on seasonally or locally abundant zooplanktonic prey. Artedidraconids are benthic sit-and-wait predators. Larger bathydraconids are benthic predators on fish while smaller species feed mainly on benthic crustaceans. Channichthyids are less dependent on the bottom for food than other notothenioids. Some species combine benthic and pelagic life styles; others are predominantly pelagic and all consume euphausiids and/or fish. South polar skuas, Antarctic petrels, Adélie and emperor penguins, Weddell seals and minke and killer whales are the higher vertebrate components of the food web, and all prey on notothenioids to some extent. Based on the frequency of occurrence of prey items in the stomachs of fish, bird and mammal predators, P. antarcticum and ice krill E. crystallorophias are the key species in the food web of the Ross Sea. P. antarcticum is a component of the diet of at least 11 species of nototheniid, bathydraconid and channichthyid fish and, at frequencies of occurrence from 71 to 100%, is especially important for Dissostichus mawsoni, Gvozdarus svetovidovi and some channichthyids. At least 16 species of notothenioids serve as prey for bird and mammal predators, but P. antarcticum is the most important and is a major component of the diet of south polar skua, Adélie and emperor penguins and Weddell seals, at frequencies of occurrence from 26 to 100%. E. crystallorophias is consumed by some nototheniid and channichthyid fish and can be of importance in the diet of emperor and Adélie penguins, although in the latter case, this is dependent on location and time of year.Unlike the linear phytoplanktonE. superbaconsumers of the E. superba food chain hypothesized for much of the Southern Ocean, the food web of the Ross Sea shelf is non-linear, with complex prey-predator interactions. Notothenioid fish play a key role: as predators, they occupy most of the trophic niches available in the ecosystem, relying on benthic, zooplanktonic and nektonic organisms; as prey, they are important food resources for each other and for most top predators living and foraging on the shelf. They also constitute the major link between lower (invertebrates) and higher (birds and mammals) levels of the food web. This is especially true for P. antarcticum. Along with E. crystallorophias, its ecological role in the Ross Sea is equivalent to that of myctophids and E. superba elsewhere in the Southern Ocean.     

The food of some Aantarctic fish in the western Ross Sea in summer 1979

Summary The food of fish in the western area of the Ross Sea was studied. Four locations were sampled using a bottom trawl. Twenty-four species of fish belonging to six families were caught. Pleuragramma antarcticum was the most important species among them and Chionodraco myersi was also abundant. The food chain, starting from small crustaceans such as Parathemisto gaudichaudii, copepods and Euphausia crystallorophias and extending through P. antarcticum to channichthyids is considered the most important chain in the food web of the fish community of the western Ross Sea in summer. The significance of the ecological role of P. antarcticum in the food web of the fish community of this area where the krill, Euphausia superba, is scarce is discussed.     

Austral Summer Bloom of Loricate Choanoflagellates in the Central Ross Sea Polynya

A bloom of loricate choanoflagellates was recorded for the first time in the Ross Sea polynya during the austral summer 2017. Both individual cells and uncommon large‐size colonies (200 μm length) represent the 42–55% of the total plankton community (i.e. specimens from 5 to 150 μm length). Choanoflagellates serve as a link between low and mid trophic levels since they prey on bacteria and in turn are ingested by zooplankton. This twofold role and the unusual abundance recorded in the Antarctic ecosystem may have relevant but still unknown effects on food web structure and dynamics in that area.     

Spatially Extensive Standardized Surveys Reveal Widespread,Multi-Decadal Increase in East Antarctic Adélie Penguin Populations

Seabirds are considered to be useful and practical indicators of the state of marine ecosystems because they integrate across changes in the lower trophic levels and the physical environment. Signals from this key group of species can indicate broad scale impacts or response to environmental change. Recent studies of penguin populations, the most commonly abundant Antarctic seabirds in the west Antarctic Peninsula and western Ross Sea, have demonstrated that physical changes in Antarctic marine environments have profound effects on biota at high trophic levels. Large populations of the circumpolar-breeding Adélie penguin occur in East Antarctica, but direct, standardized population data across much of this vast coastline have been more limited than in other Antarctic regions. We combine extensive new population survey data, new population estimation methods, and re-interpreted historical survey data to assess decadal-scale change in East Antarctic Adélie penguin breeding populations. We show that, in contrast to the west Antarctic Peninsula and western Ross Sea where breeding populations have decreased or shown variable trends over the last 30 years, East Antarctic regional populations have almost doubled in abundance since the 1980’s and have been increasing since the earliest counts in the 1960’s. The population changes are associated with five-year lagged changes in the physical environment, suggesting that the changing environment impacts primarily on the pre-breeding age classes. East Antarctic marine ecosystems have been subject to a number of changes over the last 50 years which may have influenced Adélie penguin population growth, including decadal-scale climate variation, an inferred mid-20th century sea-ice contraction, and early-to-mid 20^th century exploitation of fish and whale populations.     

Genetic diversity and condition factor: a significant relationship in Flemish but not in German populations of the European bullhead (Cottus gobio L.)

The population genetics of the Antarctic neritic krill species Euphausia crystallorophias was examined by nucleotide sequence variation in its mitochondrial DNA. A 616 base pair region of the cytochrome c oxidase subunit I (COI) gene was screened for mutations by single-strand conformational polymorphism (SSCP) combined with restriction digestion. E. crystallorophias caught in three different regions of the Antarctic coastline were used--two samples from the Mertz Glacier Polynya and one sample each from the western side of the Antarctic Peninsula and from the Davis Sea. Significant genetic differences between krill samples were identified. However, the extent of these differences did not correlate with the degree of geographic separation between the sampling sites. This suggests that the genetic structuring may be the result of small-scale differentiation rather than differentiation between resident populations in separate parts of the Southern Ocean. The possibility that genetic differences between samples within a region are as important as differences between regions has implications for other studies of krill population genetics.     

A trophic mass balance model of the eastern Chukchi Sea with comparisons to other high-latitude systems

The Chukchi Sea is a seasonally ice-covered, marginal Arctic-shelf sea that possesses both large petroleum reserves and abundant biological communities, including migratory mammals and seabirds. We developed a mass balance food web model for the eastern Chukchi Sea to evaluate the trophic structure of this ecosystem and to compare food web properties of the Chukchi Sea to those of other high-latitude marine ecosystems. We compiled data on biomass levels, diet composition, demographic rates (production, consumption), and fishery removals, and used these data to construct an Ecopath trophic mass balance model. The majority of biomass was concentrated in benthic invertebrates and most of the mass flow above trophic level 2.0 was through these groups. We found that density estimates of most fish groups derived from trawl survey data using area-swept methods were insufficient to match the consumptive demands of predators, and that densities needed to be several-fold greater to meet modeled demand. We also used a set of system metrics derived from a common modeling framework to highlight differences in ecosystem structure between the eastern Chukchi Sea and other high-latitude systems. The extent of benthic dominance observed in the eastern Chukchi Sea was unique among the systems examined, both in terms of food web structure and associated mass flows between benthic and pelagic components. In relation to total biomass density, the eastern Chukchi Sea had low production when compared with the other systems, and this lower turnover rate suggests that recovery from disturbance might be slow.     

Intra-seasonal variation in foraging behavior among Ad��lie penguins (Pygocelis adeliae) breeding at Cape Hallett, Ross Sea, Antarctica

We investigated intra-seasonal variation in foraging behavior of chick-rearing Adélie penguins, Pygoscelis adeliae, during two consecutive summers at Cape Hallett, northwestern Ross Sea. Although foraging behavior of this species has been extensively studied throughout the broad continental shelf region of the Ross Sea, this is the first study to report foraging behaviors and habitat affiliations among birds occupying continental slope waters. Continental slope habitat supports the greatest abundances of this species throughout its range, but we lack information about how intra-specific competition for prey might affect foraging and at-sea distribution and how these attributes compare with previous Ross Sea studies. Foraging trips increased in both distance and duration as breeding advanced from guard to crèche stage, but foraging dive depth, dive rates, and vertical dive distances travelled per hour decreased. Consistent with previous studies within slope habitats elsewhere in Antarctic waters, Antarctic krill (Euphausia superba) dominated chick meal composition, but fish increased four-fold from guard to crèche stages. Foraging-, focal-, and core areas all doubled during the crèche stage as individuals shifted distribution in a southeasterly direction away from the coast while simultaneously becoming more widely dispersed (i.e., less spatial overlap among individuals). Intra-specific competition for prey among Adélie penguins appears to influence foraging behavior of this species, even in food webs dominated by Antarctic krill.     

Macrofaunal crustaceans in the benthic boundary layer from the shelf break to abyssal depths in the Ross Sea (Antarctica)

The New Zealand International Polar Year–Census of Antarctic Marine Life (NZ IPY-CAML) project added to previous benthic studies in the Ross Sea by extending sampling north from the continental shelf to previously unsampled areas of the shelf break, slope, abyssal plain and seamounts in the region. The aim of the current study is to give first insights into the deep-sea community structure of the Ross Sea focussing on a component of the benthic boundary layer that is macrofaunal crustaceans collected one metre above the seafloor. We assess changes in Ross Sea crustacean community composition from the shelf break (474 m) to the abyss (3,490 m) and compare the Ross Sea crustacean fauna to areas elsewhere in the Southern Ocean. Analyses reveal high relative abundances, suggesting an important role in the food web. Among the peracarid crustaceans, there was a decline in the proportion of amphipods with increasing depth. Three of 15 isopod families (Acanthaspidiidae, Nannoniscidae and Desmosomatidae) were identified to species level and about 72 % of the species were new to science. Isopod diversity in the Ross Sea abyss appears to be comparable to that in the highly speciose Weddell deep sea. Standardised sampling of these crustacean communities allows setting the biodiversity of the Ross Sea into a global context.     

Insights into spatial distribution patterns of early stages of the Antarctic silverfish,Pleuragramma antarctica,in the platelet ice of Terra Nova Bay,Antarctica

Polar Biology - The Antarctic silverfish, Pleuragramma antarctica, is ecologically important for connecting lower and upper trophic levels within the coastal marine Antarctic food web. In recent...     

Decrease in stomach contents in the Antarctic minke whale (Balaenoptera bonaerensis) in the Southern Ocean

The Antarctic minke whale (Balaenoptera bonaerensis) is one of the major krill predators in Antarctic waters. A reported decline in energy storage over almost two decades indicates that food availability for the whales may also have declined recently. To test this hypothesis, catch data from 20 survey years in the Japanese Whale Research Program in the Antarctic (JARPA) and its second phase (JARPA II) (1990/91–2009/10), which covered the longitudinal sector between 35°E and 145°W south of 58°S, were used to investigate whether there was any annual trend in the stomach contents weight of Antarctic minke whales. A linear mixed-effects analysis showed a 31 % (95 % CI 12.6–45.3 %) decrease in the weight of stomach contents over the 20 years since 1990/1991. A similar pattern of decrease was found in both males and females, except in the case of females sampled at higher latitude in the Ross Sea. These results suggest a decrease in the availability of krill for Antarctic minke whales in the lower latitudinal range of the research area. The results are consistent with the decline in energy storage reported previously. The decrease in krill availability could be due to environmental changes or to an increase in the abundance of other krill-feeding predators. The latter appears somewhat more likely, given the recent rapid recovery of humpback whale. Furthermore, humpback whales are not found in the Ross Sea, where both Antarctic krill and ice krill (Euphausia crystallorophias) are available, and where no change in prey availability for Antarctic minke whales is indicated.     

Complexity and structural properties of food webs in the Barents Sea

A food web topology describes the diversity of species and their trophic interactions, i.e. who eats whom, and structural analysis of food web topologies can provide insight into ecosystem structure and function. It appears simple, at first sight, to list all species and their trophic interactions. However, the very large number of species at low trophic levels and the impossibility to monitor all trophic interactions in the ocean makes it impossible to construct complete food web topologies. In practice, food web topologies are simplified by aggregating species into groups termed trophospecies. It is not clear though, how much simplified versions of food webs retain the structural properties of more detailed networks. Using the most comprehensive Barents Sea food web to date, we investigate the performance of methods to construct simplified food webs using three approaches: taxonomic, structural and regular clustering. We then evaluate how topological properties vary with the level of network simplification. Results show that alteration of food web structural properties due to aggregation are highly sensitive to the methodology used for grouping species and trophic links. In the specific case of the Barents Sea, we show that it is possible to preserve key structural properties of the original complex food web in simplified versions when using taxonomic or structural clustering combined with intermediate 25% linkage for trophic aggregation.     

Establishment of trophic continuum in the food web of the Yellow Sea and East China Sea ecosystem: Insight from carbon and nitrogen stable isotopes

The determination of trophic level for the biology in a marine ecosystem is very important as alteration of its structure and function may be reflected in the tro-phic level of component species. A change in trophic level indicates variation in an organism’s feeding bi-ology or in the pathway of energy flow from primary producers to the consumer. The gut content analysis is a traditional method for studying trophodynamics of food web in marine ecosystems. Species composition and amounts in al…     

Trophic plasticity of Antarctic echinoids under contrasted environmental conditions

Echinoids are common members of Antarctic zoobenthos, and different groups can show important trophic diversity. As part of the ANT-XXIX/3 cruise of RV Polarstern, trophic plasticity of sea urchins was studied in three neighbouring regions (Drake Passage, Bransfield Strait and Weddell Sea) featuring several depth-related habitats offering different trophic environments to benthic consumers. Three families with contrasting feeding habits (Cidaridae, Echinidae and Schizasteridae) were studied. Gut content examination and stable isotopes ratios of C and N suggest that each of the studied families showed a different response to variation in environmental and food conditions. Schizasteridae trophic plasticity was low, and these sea urchins were bulk sediment feeders relying on sediment-associated organic matter in all regions and/or depth-related habitats. Cidaridae consumed the most animal-derived material. Their diet varied according to the considered area, as sea urchins from Bransfield Strait relied mostly on living and/or dead animal material, while specimens from Weddell Sea fed on a mixture of dead animal material and other detritus. Echinidae also showed important trophic plasticity. They fed on various detrital items in Bransfield Strait, and selectivity of ingested material varied across depth-related habitats. In Weddell Sea, stable isotopes revealed that they mostly relied on highly ¹³C-enriched food items, presumably microbially reworked benthic detritus. The differences in adaptive strategies could lead to family-specific responses of Antarctic echinoids to environmental and food-related changes.     

Establishment of trophic continuum in the food web of the Yellow Sea and East China Sea ecosystem: Insight from carbon and nitrogen stable isotopes

Stable carbon and nitrogen isotope ratios (δ¹³C and δ¹⁵N) are used to study the trophic structure of food web in the Yellow Sea and East China Sea ecosystem. The trophic continuum of pelagic food web from phytoplankton to top preyer was elementarily established, and a trophic structure diagram in the Yellow Sea and East China Sea was outlined in combination with carbon isotopic data of benthic organisms, which is basically consistent with and makes some improvements on the simplified Yellow Sea food web and the trophic structure diagram drawn based on the biomass of main resource population during 1985–1986. This result indicates that the stable isotope method is a potential useful means for further studying the complete marine food web trophic continuum from viruses to top predators and food web stability.     

Temporal and spatial changes in benthic invertebrate trophic networks along a taxonomic richness gradient

Species interactions underlie most ecosystem functions and are important for understanding ecosystem changes. Representing one type of species interaction, trophic networks were constructed from biodiversity monitoring data and known trophic links to assess how ecosystems have changed over time. The Baltic Sea is subject to many anthropogenic pressures, and low species diversity makes it an ideal candidate for determining how pressures change food webs. In this study, we used benthic monitoring data for 20 years (1980–1989 and 2010–2019) from the Swedish coast of the Baltic Sea and Skagerrak to investigate changes in benthic invertebrate trophic interactions. We constructed food webs and calculated fundamental food web metrics evaluating network horizontal and vertical diversity, as well as stability that were compared over space and time. Our results show that the west coast of Sweden (Skagerrak) suffered a reduction in benthic invertebrate biodiversity by 32% between the 1980s and 2010s, and that the number of links, generality of predators, and vulnerability of prey have been significantly reduced. The other basins (Bothnian Sea, Baltic Proper, and Bornholm Basin) do not show any significant changes in species richness or consistent significant trends in any food web metrics investigated, demonstrating resilience at a lower species diversity. The decreased complexity of the Skagerrak food webs indicates vulnerability to further perturbations and pressures should be limited as much as possible to ensure continued ecosystem functions.     

Molecular evidence for genetic subdivision of Antarctic krill (Euphausia superba Dana) populations.

Antarctic krill (Euphausia superba Dana) is a key species in the Antarctic food web and occurs on a circumcontinental scale. Population genetic structure of this species was investigated by sequence analysis of the ND1 mitochondrial gene in four population samples collected at different geographical localities around the Antarctic continent. Results indicate the existence of significant genetic differences between samples, and we suggest that oceanographic barriers could be sufficiently strong and temporally stable to restrict gene flow between distinct areas. Moreover, our data indicate that Antarctic krill is not at mutation-drift equilibrium and that the species possibly has a low effective population size as compared to the census size.     

Concentrations of Thirteen Trace Metals in Scales of Three Nototheniid Fishes from Antarctica (James Ross Island,Antarctic Peninsula)

In this study, we assessed concentrations of 13 trace metals in the scales of Notothenia coriiceps, Trematomus bernacchii and Gobionotothen gibberifrons caught off the coast of James Ross Island (Antarctic Peninsula). Overall, our results for scales broadly match those of previous studies using different fish and different organs, with most metals found at trace levels and manganese, aluminium, iron and zinc occurring at high levels in all species. This suggests that scales can serve as a useful, non-invasive bioindicator of long-term contamination in Antarctic fishes. High accumulation of manganese, aluminium, iron and zinc is largely due to high levels in sediments associated with nearby active volcanic sites. Manganese, vanadium and aluminium showed significant positive bioaccumulation in T. bernacchii (along with non-significant positive accumulation of iron, zinc, cobalt and chromium), most likely due to greater dietary specialisation on sediment feeding benthic prey and higher trophic species. Levels of significance in bioaccumulation regressions were strongly affected by large-scale variation in the data, driven largely by individual differences in diet and/or changes in habitat use and sex differences associated with life stage and reproductive status. Increased levels of both airborne deposition and precipitation and meltwater runoff associated with climate change may be further adding to the already high levels of manganese, aluminium, iron and zinc in Antarctic Peninsula sediments. Further long-term studies are encouraged to elucidate mechanisms of uptake (especially for aluminium and iron) and possible intra- and interspecific impacts of climate change on the delicate Antarctic food web.

     

Genetic homogeneity of krill (Euphausia superba Dana) in the Southern Ocean

Summary Development of a comprehensive picture of the genetic population structure of the Antarctic krill (Euphausia superba) has been hampered by a lack of genetic data from two major areas of the species' distribution, the Bellingshausen Sea and the Ross Sea. Evidence from earlier studies of a discrete Bellingshausen Sea population was based on anomalous allele frequencies in two sample sets that were collected near the west coast of the Antarctic Peninsula rather than in the Bellingshausen Sea proper. In this paper we describe the first biochemical genetic data obtained on krill from the central Bellingshausen Sea and from the Ross Sea. Analyses of eight polymorphic loci in samples from these two areas have failed to provide any evidence of population structuring within the Pacific sector of the Southern Ocean, and have indicated that Pacific sector krill cannot be genetically discriminated from Atlantic sector krill or Indian Ocean sector krill. These findings further support the hypothesis of a single circumpolar breeding population of Antarctic krill.     

Energy flow and network analysis of Terminos Lagoon, SW Gulf of Mexico

The food web in Terminos Lagoon, south-western Gulf of Mexico was dominated by the detrital pathway, with benthic invertebrates playing a significant role in transferring energy from detritus to higher trophic levels. The fish yield per unit of net primary production was only 0.04%. Fractional trophic levels ranged from 1.0 to 3.31, with fish occupying the highest trophic levels. Using network analysis, the system network was mapped into a linear food chain and five discrete trophic levels were found with a mean trophic transfer efficiency of 7%. Analysis of mixed trophic impacts showed that fish had very little impact on the other compartments, due to their relatively low biomass and consumption, with exception of the Engraulidae. Detritus and lower trophic levels had significant positive impacts on other groups in the system, suggesting 'bottom-up' control of the food web. A high detritivory: herbivory ratio (4.6: 1) indicated that most of the primary production was recycled through the detritus-based food web. A Finn cycling index of 7% and average path length of 10 were obtained.