The winter pack-ice zone provides a sheltered but food-poor habitat for larval Antarctic krill

Abstract

A ntarctic krill Euphausia superba, a key species in Southern Ocean food webs 1 , plays a central role in ecosystem processes and community dynamics of apex predators, and is the target of a commercial fishery 2 . Krill spawn in late spring and their larvae develop during summer, autumn and under the ice in winter to emerge as juveniles in the following spring. The newly spawned eggs sink from the surface to up to 1,000 m depth where they hatch and the developing larvae actively swim upwards to feed in the upper water column 1 . Larval Antarctic krill have low lipid reserves, which are insufficient to support long periods of starvation. Therefore, winter, when primary production is minimal, is assumed to be a critical bottleneck for larval krill development and hence recruitment to the adult population 3,4 . Present hypotheses suggest that high algal biomass in winter sea ice enhances larval krill winter-feeding conditions and growth [5][6][7][8] . This implies that larvae have access to this high algal biomass within the sea ice. However, recent observations 9,10 indicate that the linkage between sea ice and krill recruitment success is not as direct as has been suggested. The timing of ice-edge advance and annual ice-season duration is highly variable, and does not necessarily show a clear link to krill recruitment in the following year ( Supplementary Figs. 1 and 2). Along the Antarctic Peninsula, adult krill have a five to six year population cycle with oscillations in biomass exceeding an order of magnitude 9 . According to bioenergetics models, part of the variability is due to interannual variation in reproductive output 11 as well as autumn blooms that may govern the possible overwinter survival rate of larvae 11,12 . In the Bransfield Strait, three krill winter surveys have shown that krill abundance is an order of magnitude higher than in summer, regardless of concurrent sea-ice conditions 10 A dominant Antarctic ecological paradigm suggests that winter sea ice is generally the main feeding ground for krill larvae. Observations from our winter cruise to the southwest Atlantic sector of the Southern Ocean contradict this view and present the first evidence that the pack-ice zone is a food-poor habitat for larval development. In contrast, the more open marginal ice zone provides a more favourable food environment for high larval krill growth rates. We found that complex under-ice habitats are, however, vital for larval krill when water column productivity is limited by light, by providing structures that offer protection from predators and to collect organic material released from the ice. The larvae feed on this sparse ice-associated food during the day. After sunset, they migrate into the water below the ice (upper 20 m) and drift away from the ice areas where they have previously fed. Model analyses indicate that this behaviour increases both food uptake in a patchy food environment and the likelihood of overwinter transport to areas where feeding conditions are more favourable in spring.

Aerial surveys for Antarctic minke whales (Balaenoptera bonaerensis) reveal sea ice dependent distribution patterns

“…These were covered by our surveys only to a limited extent, owing to an even survey coverage across the area. With sea ice providing habitat for the overwintering of phytoplankton and krill, seasons of high winter ice extension typically support greater primary production than seasons with less ice-covered habitat in winter (Loeb et al, 1997;Meyer et al, 2017;Nicol et al, 2008). In all our survey years, very low ice concentrations were encountered in stratum WAP.…”

The Weddell Gyre, Southern Ocean: Present Knowledge and Future Challenges

“…The importance of sea‐ice microbial community as food source for WG zooplankton is thought to increase during winter, although this pattern has been challenged by recent data. While some studies suggest that ice algae can provide up to 67% of the zooplankton carbon (Kohlbach et al, ), others conclude that pelagic production is more important as a food source and that sea ice mainly provides shelter (Meyer et al, ).…”

Dependency of Antarctic zooplankton species on ice algae‐produced carbon suggests a sea ice‐driven pelagic ecosystem during winter

“…Assuming typical densities of krill larvae in over‐rafted under‐ice habitats (mean 853 ind. m −2 , Meyer et al, ), this value would locally reach up to 13.6 mg C m −2 day −1 . The true feeding rates of krill larvae during our study may have been even lower, as suggested by Meyer et al (), albeit neglecting the large contribution of heterotrophic prey to the krill diet (Schaafsma et al, ).…”

“…In our study region, water column Chlorophyll a and pigment concentrations are typically below 0.1 mg/m 3 between April and August (Comiso, McClain, Sullivan, Ryan, & Leonard, ; David et al, ), regardless of the presence of sea ice. Only in marginal ice‐zone blooms, Chlorophyll a concentrations reached 0.4–0.9 mg/m 3 (Meyer et al, ). Conversely, Antarctic bottom ice algal Chlorophyll a concentrations are higher by about one order of magnitude.…”

“…To overcome insufficient primary production in the water column during winter, some species, such as the euphausiid Thysanoessa macrura , accumulate large lipid reserves in the form of wax esters and/or triacylglycerols (Hagen, Kattner, & Graeve, ; Kattner, Graeve, & Hagen, ; Lee, Hagen, & Kattner, ). Of particular interest are young Antarctic krill Euphausia superba (“krill”), which occur in large abundances at the sea ice–water interface, and can rely heavily on sea ice‐associated carbon sources during winter (Kohlbach, Lange, et al, ; Schaafsma et al, ), although this dependence can vary by sea ice type (Meyer et al, ). Various copepod species are known to undergo diapause, migrating into deeper water layers during winter (Voronina, ), after accumulating lipids from the summer phytoplankton blooms (Lee, Hirota, & Barnett, ).…”