Multiple Trophic Markers Trace Dietary Carbon Sources in Barents Sea Zooplankton During Late Summer

Abstract

We investigated diets of 24 Barents Sea zooplankton taxa to understand pelagic food-web processes during late summer, including the importance of sea ice algae-produced carbon. This was achieved by combining insights derived from multiple and complementary trophic marker approaches to construct individual aspects of feeding. Specifically, we determined proportions of algal-produced fatty acids (FAs) to reflect the reliance on diatom- versus dinoflagellate-derived carbon, highly branched isoprenoid (HBI) lipids that distinguish between ice-associated and pelagic carbon sources, and sterols to indicate the degree of carnivory. Copepods had the strongest diatom signal based on FAs, while a lack of sea ice algae-associated HBIs (IP25, IPSO25) suggested that they fed on pelagic rather than ice-associated diatoms. The amphipod Themisto libellula and the ctenophores Beroë cucumis and Mertensia ovum had a higher contribution of dinoflagellate-produced FAs. There was a high degree of carnivory in this food web, as indicated by the FA carnivory index 18:1(n−9)/18:1(n−7) (mean value < 1 only in the pteropod Clione limacina), the presence of copepod-associated FAs in most of the taxa, and the absence of algal-produced HBIs in small copepod taxa, such as Oithona similis and Pseudocalanus spp. The coherence between concentrations of HBIs and phytosterols within individuals suggested that phytosterols provide a good additional indication for algal ingestion. Sea ice algae-associated HBIs were detected in six zooplankton species (occurring in krill, amphipods, pteropods, and appendicularians), indicating an overall low to moderate contribution of ice-associated carbon from late-summer sea ice to pelagic consumption. The unexpected occurrence of ice-derived HBIs in pteropods and appendicularians, however, suggests an importance of sedimenting ice-derived material at least for filter feeders within the water column at this time of year.

Winter Carnivory and Diapause Counteract the Reliance on Ice Algae by Barents Sea Zooplankton

“…However, productivity varies significantly depending on oceanographic conditions, nutrient concentrations and sea-ice cover (Sakshaug and Slagstad, 1992;Falk-Petersen et al, 2000b;Reigstad et al, 2002;Hop et al, 2019). Nevertheless, phytoplankton carbon is generally considered to be sufficient to meet the energetic requirements of the food web (Verity et al, 2002;Tamelander et al, 2006;Wassmann et al, 2006;Kohlbach et al, 2021). Additionally, sea ice-associated (sympagic) primary production can provide an alternative or supplemental source of carbon for some zooplankton taxa, early in the season (Søreide et al, 2008;Gradinger, 2009) and also during summer (Scott et al, 1999;Assmy et al, 2013;Kohlbach et al, 2016Kohlbach et al, , 2021Brown et al, 2017).…”

“…Nevertheless, phytoplankton carbon is generally considered to be sufficient to meet the energetic requirements of the food web (Verity et al, 2002;Tamelander et al, 2006;Wassmann et al, 2006;Kohlbach et al, 2021). Additionally, sea ice-associated (sympagic) primary production can provide an alternative or supplemental source of carbon for some zooplankton taxa, early in the season (Søreide et al, 2008;Gradinger, 2009) and also during summer (Scott et al, 1999;Assmy et al, 2013;Kohlbach et al, 2016Kohlbach et al, , 2021Brown et al, 2017). During winter, primary production levels in the water column (Kvernvik et al, 2018) and in sea ice are practically zero (Mikkelsen et al, 2008), and the ice algal biomass trapped in internal ice layers might be difficult to access for grazers (Van Leeuwe et al, 2018).…”

“…SIC data acquired from Bremen University (http://www.iup.uni-bremen.de:8084/amsr2/) (Spreen et al, 2008). More detailed information on sampling stations can be found in Kohlbach et al (2021).…”

“…The potential importance of sea-ice algae for copepods that do not perform diapause during winter is unclear (Cleary et al, 2017); thus far, information on their carbon source composition during the dark period is mostly restricted to late autumn (Scott et al, 2000) and the winterspring transition (Wold et al, 2011). Other species with a more omnivorous/carnivorous lifestyle, such as Themisto amphipods, are less impacted by the lower algal productivity and can thus remain active during winter (Hagen and Auel, 2001;Kraft et al, 2013); they have a pelagic lifestyle but are often encountered at the sea ice-water interface (David et al, 2015) and are capable of utilizing sympagic carbon (Wang et al, 2015;Kohlbach et al, 2016Kohlbach et al, , 2021.…”

“…Thus, the distribution of membrane and storage lipids in an animal's body can give information on their nutritional condition and overwintering strategies (Kattner et al, 1994). Highly branched isoprenoid (HBI) lipids and sterols can further complement food-web studies (e.g., Schmidt et al, 2018;Kohlbach et al, 2021). Different HBIs allow for the differentiation of sympagic (IP 25 and IPSO 25 ) and pelagic (HBIs III and IV) carbon (Belt et al, 2012;Brown and Belt, 2012;Belt, 2018), whereas phyto-and animal-derived sterols allow conclusions about the degree of carnivory of a species (Drazen et al, 2008;Ruess and Müller-Navarra, 2019).…”