Penguins as ecosystem proxies? Identifying millennial-scale shifts in carbon sources and phytoplankton regimes in the Antarctic marine ecosystem

The Southern Ocean is undergoing recent rapid physical and biological change. A rise in sea-surface temperature and significant losses in sea ice extent affect phytoplankton community composition, food web dynamics, and biogeochemical cycling. For example, recent anthropogenic climate change in the Antarctic Peninsula is related to decreases in large-celled diatoms in favor of small-celled phytoplankton, which has significant implications for CO₂ drawdown and carbon transfer to higher trophic organisms. Pygoscelis penguins serve as a sensitive indicator for ecosystem change. Prior studies of bulk tissue stable carbon isotope values in preserved eggshell (δ¹³C_bulk) from Adélie penguin (P. adeliae) colonies around Antarctica show an abrupt shift from higher to lower values within the last 200 years. This has been hypothesized as indicative of increased consumption of krill over fish. However, dietary, environmental, and physiological processes alter δ¹³C_bulk values and their relative influences are difficult to disentangle. Here, we use compound-specific stable isotope analysis (CSIA) of essential amino acids (EAAs) in a Holocene time series of Adélie penguin eggshells to re-interpret prior δ¹³C_bulk studies and trace carbon flow and relative importance of basal carbon sources in the Antarctic food web over time. EAA δ¹³C values provide unique isotopic fingerprints of primary producers that are transferred through a food web unmodified, preserving a record of the baseline plankton source in the tissues of higher trophic consumers. Using a fingerprinting approach with Adélie penguin eggshells, we determined the contribution of key primary producers to the Antarctic food web throughout much of the Holocene to identify changes in plankton regimes and carbon sources linked to climate regimes. This novel approach improves past environmental reconstructions and may provide mechanisms driving ecosystem change to facilitate future predictions of Antarctic ecosystem health.