Cascading trophic impacts of reduced biomass in the Ross Sea, Antarctica: just the tip of the iceberg?

Abstract

BRAD A. SEIBEL* AND HEIDI M. DIERSSEN†Monterey Bay Aquarium Research Institute, Moss Landing, California 95039A significant reduction in phytoplankton biomass in theRoss Sea was reported in the austral summer of 2000–2001,a possible consequence of a disruption in sea-ice retreatdue to the presence of an immense iceberg, B15 (1) (Fig. 1).Our observations in McMurdo Sound suggest temporallyand trophically cascading impacts of that depression inproductivity. Reduced phytoplankton stocks clearly affectedthe pteropod Limacina helicina (Phipps, 1774) (Gastro-poda: Mollusca), an abundant primary consumer in theregion (2, 3), as indicated by depressed metabolic rates in2000–2001. The following season, for the first time onrecord, L. helicina was absent from McMurdo Sound. Manyimportant predators, including whales and fishes, relyheavily on L. helicina for food (3, 4). However, most obvi-ously impacted by its absence was Clione antarctica (Smith,1902), an abundant pteropod mollusc (Gastropoda) thatfeeds exclusively on L. helicina (5). Metabolic rates of C.antarctica were depressed by 50% in 2001–2002. BothL.helicina and C. antarctica are important components ofpolar ecosystems and may be good indicators of overallecosystem “health” in McMurdo Sound and perhaps in theRoss Sea. In this last austral summer, 2002–2003, sea-iceextent was much higher and phytoplankton stocks weredramatically lower than any reported previously, effectspossibly associated with El Nin˜o conditions, and we hypoth-esize that pteropods and their consumers may be furtherimpacted.In the Southern Ocean, phytoplankton production islinked strongly to the seasonal oscillations in the extent ofthe sea ice (6, 7) and survival of higher trophic levels isdependent on reproductive cycles that are synchronous withphytoplankton blooms. This is especially true of the directfood link between L. helicina and C. antarctica. L. helicinalives and feeds in the water column by extending a web ofmucus that traps phytoplankton and, to a lesser extent, smallzooplankton (3). L. helicina is the exclusive food source ofC. antarctica throughout the life cycle, and the two specieshave parallel life histories. They grow in concert, with thepreferred prey size increasing with predator size (3). Suchspecificity within the context of a highly seasonal environ-ment requires precise timing to ensure that predator andprey coexist. The coevolved predator-prey relationship be-tween L. helicina and C. antarctica provides a uniqueopportunity to study the ecological and trophic conse-quences of a depression in primary productivity in the RossSea.A 50% to 75% reduction in phytoplankton biomass, es-timated as chlorophyll a (Chl) concentrations, and highsea-ice cover was observed in December 2000–2001 rela-tive to previous years (Table 1; Fig. 2; 8). A limited bloomdid form by February, but annual primary production wasstill only 60% of the previous year (1). We believe that thereduced phytoplankton stocks in 2000–2001 had pro-nounced impacts on the condition of primary consumers inthe region, causing cascading effects through higher trophiclevels in the following year. This assertion is supported hereby a series of metabolic measurements made on L. helicinaand C. antarctica between 1999 and 2002.Nutritional state is known to be among the primary de-terminants of metabolism in all organisms, including ptero-pods (3), and is especially important in the highly seasonalAntarctic environment (9, 10). Food availability will influ-ence, among other things, the rates of protein synthesis,oxygen consumption, growth, and reproduction (9–11). Wecollected L. helicina and C. antarctica at four samplingstations along Ross Island (Fig. 1) and measured the oxygen