The West Antarctic Peninsula (WAP) exhibits strong spatial and temporal oceanographic variability, resulting in highly heterogeneous biological productivity. Calcifying organisms that live in the waters off the WAP respond to temporal and spatial variations in ocean temperature and chemistry. These marine calcifiers are potentially threatened by regional climate change with waters already naturally close to carbonate undersaturation. Future projections of carbonate production in the Southern Ocean are challenging due to the lack of historical data collection and complex, decadal climate variability. Here we present a 6-year-long record of the shell fluxes, morphology and stable isotope variability of the polar planktic foraminifera
The West Antarctic Peninsula (WAP; Fig. 1) is a highly climatically sensitive region, characterised by strong seasonal and interannual variability in atmospheric, cryospheric and oceanographic conditions
A map of the study area with the Palmer Long-Term Ecological Research programme (Palmer LTER) sediment trap location marked with the triangle. Grey regions show ice shelf regions. Main map is enlarged view of blue box and was made using etopo1 bathymetry.
Understanding the impact of a changing climate on planktic foraminifera – when superimposed on the high environmental variability of the WAP – is challenging and requires the study of long-term (decadal-scale) observations. This challenge is complicated by the fact that for a long time two genotypes of the morphospecies have been considered as one species (
To this end, we investigate the controls on
The shelf adjacent to Anvers Island, WAP, is one of the key localities of the Palmer Long-Term Ecological Research programme (Palmer LTER; Fig.
Between 2006 and 2012, SST and water temperature at 100 m depth showed pronounced seasonal and inter-annual variability (SST shown in Fig.
Environmental parameters plotted with foraminiferal and organic matter time series flux record from Palmer LTER sediment trap.
Sediment trap samples were stored at 5
Morphological analysis of the Nps specimens was carried out both manually and using an automated microscopy technique. The automated high-throughput method was used to determine the morphological character of the entire Nps population at the site. The manual method was conducted on a smaller number of individuals (maximum 50) as an independent validation of automated measurements.
Automated analysis of bulk samples used an automated microscope and image analysis system
Approximately 50 specimens per sample were fixed onto glass slides and imaged using an Olympus SZX7 transmitted light microscope equipped with a QImaging FAST 1394 camera and QCapture software. Image backgrounds were changed to black in Adobe Photoshop CC 2015. A smoothing factor of 5 was also applied to the outline of each specimen to ensure that angular lines from pixels were rounded without altering the shape of the specimens. Morphological parameters were measured using Image-Pro Plus 6.2, including area, major axis, minor axis, maximum diameter, minimum diameter, mean diameter, perimeter, roundness, length and width, as well as derived parameters such as circularity ratio, elongation ratio, box ratio and compactness coefficient.
Single-specimen isotope analysis captures the full range of growth conditions experienced during the lifetime of the foraminifera
Prior to analysis, specimens were weighed individually on a Mettler Toledo XPR2U high-precision microbalance (
Equilibrium calcite
Nps flux displays a double peak in some years
To assess the comparability of the automated and manually derived morphometric datasets, we compared the normalised maximum diameter (MD) of specimens
MD, sphericity and mean grey value, measured using automated microscopy, illustrate intra- and inter-annual variability in Nps size and calcification (Fig.
Time series record of the foraminiferal morphological parameters collected by the automated analysis.
Statistical analysis was only carried out on morphometric data collected using the manual method (Fig.
Boxplot of
A total of 14 of the 32 samples display a non-normal distribution of size-invariant parameters. Principal component analysis (PCA) of the distributions of the four size-invariant morphological parameters that relate to shape (circularity ratio, box ratio, elongation ratio and compactness coefficient) reveals two statistically defined clusters (Fig.
Scanning electron microscope images of
A range of approximately 1 ‰ is observed in the single-specimen analyses of Nps
Multi-specimen and single-specimen adult
Single-specimen
Boxplot of single-specimen
The range of both
Assuming no vital effect, the predicted
A qualitative view of our flux data reveals that, whilst there are generally fewer foraminifera in winter than summer, there is also pronounced interannual variability, indicating that there are complex controls on foraminiferal flux in addition to seasonal climatologies of water column conditions. Spearman's rank analysis indicates that there are significant correlations for Nps flux only with organic carbon and organic nitrogen flux (Table S8, Fig. S10), with the highest fluxes between November and February associated with phytoplankton blooms. Both organic carbon and nitrogen fluxes correlate with other environmental parameters, such as SST, Chl
PCA revealed that seasonality alone cannot explain all of the observed morphological variability (Supplement). Redundancy analysis (RDA) of the means shows a single dominant trend in the joint space of the manually collected size-normalised, size-dependent, size-invariant morphological data (see Supplement for definitions) and the environmental parameters (Fig.
To summarise the ecological drivers on Nps flux, size and morphology, we describe a composite year (Figs. S1, S2) divided into six distinct phases (Fig.
Redundancy analysis biplot of the means of the normalised size-dependent and size-invariant morphological data (black diamond) and the environmental parameters (red circle).
During the Antarctic winter, Nps dwell at shallow depths, just below or within the sea ice
Spring sea ice break-up and melt results in decreased surface salinity. The onset of shallow stratification of the water column and release of nutrients from sea ice and glacial melt provides an ideal setting for diatom blooms. As a result, Chl
Highest Nps fluxes at the sediment trap site are associated with the warmest time of the year and the complete disappearance of sea ice by the end of November. Between late November and mid-January, SSTs continue to increase, and surface waters freshen, resulting in stronger surface stratification than during sea ice break-up (Phase 2). The melting sea ice and the development of shallow stratification lead to increased food availability, which is reflected in the Chl
Summary schematic of a typical year at the Palmer sediment trap site. Colours illustrate the six phases of the annual cycle described in the main text.
During the late summer phase, Nps flux decreases despite surface warming and increasing organic carbon flux, which peaks by mid-February. By this time, surface water stratification reaches its maximum and salinities their minimum due to input of glacial meltwater from the coastal region. Chl
By the end of summer, the Nps depth range contracts with foraminifera living closer to the sea surface. In the autumn Nps flux increases again while carbon flux and SST decrease. In response to cooling away from optimum temperatures, test sizes decline and fewer specimens reach reproductive maturity. During the second half of February, surface stratification decreases and subsurface water freshens and warms due to mixing with surface waters. The early part of this phase is characterised by a second peak in Chl
Nps fluxes are very low during early winter in response to decreasing organic carbon flux close to zero by May and sea water temperature cooling to freezing. The cooling leads to the erosion of surface water stratification and to deepening of the mixed layer. A decline in food availability results in smaller foraminiferal sizes, together with enhanced mortality rates during periods of sea ice formation
Anomalously large numbers of Nps (approximately 9500 individuals per day, compared to an overall mean flux of 300 individuals per day) sank into the sediment trap during October and November 2010 (Fig.
Nps flux, morphology and stable isotope composition are all closely linked to sea ice extent and food availability. Our records show that differences in the timing and amplitude of peak Nps flux between 2006 and 2012 are driven by the timing of the onset of sea ice melt. Additionally, during periods of extensive sea ice cover, smaller specimens are more abundant. In contrast, periods of high food availability (spring–summer period and/or lower sea ice concentration) and reproductive success result in higher
Sea ice has a complex but important relationship with the El Niño–Southern Oscillation (ENSO) and the Southern Annular Mode (SAM)
In comparison to 2010, 2012 was characterised by El Niño-like conditions over the Pacific Ocean, and SAM switched to a negative mode after September 2012
As anthropogenic forcings persist, it is expected that northerly winds will become more persistent and stronger in the future in response to a dominant positive SAM
At the Palmer LTER sediment trap site, Nps flux displays a large peak during the late-spring–early-summer period once the sea ice has completely retreated and Chl
Based on our improved understanding of Nps ecology we suggest that non-encrusted Nps specimens should not be combined with encrusted specimens for geochemical proxy analysis as the two different morphologies record different depth habitats and seasons. Nps proxy records that only utilise encrusted specimens will likely only reconstruct austral spring and summer conditions and may be biased towards heavier
Morphometric and stable isotope data presented in this study are available at
The supplement related to this article is available online at:
AM carried out the stable isotope and morphometric analyses. KRH and JP devised the study. DNS, KME and CLCJ assisted with the morphometric analyses and interpretation. FP and MJL assisted with the stable isotope analyses and interpretation. VP, MPM, SS and HD provided samples and ancillary data. All authors contributed to the preparation of the paper.
The authors declare that they have no conflict of interest.
The authors would like to thank all the officers and crews of the US ARSV Laurence M. Gould and all those who have been involved in recovering and deploying the Palmer LTER sediment trap throughout the years. The stable isotope analysis was carried out with the assistance of Susan Verdegaal-Warmerdam.
Anna Mikis was supported by a Cardiff University President's Scholarship, and the stable isotope analysis was funded by an Antarctic Science Ltd. International Bursary awarded to Anna Mikis. The sediment trap time series has been funded by a series of awards from the US NSF Office of Polar Programs, including award PLR-1440435 to Hugh Ducklow. Katharine R. Hendry is funded by a Royal Society University Research Fellowship (grant no. UF120084), and Daniela N. Schmidt is supported by a Royal Society Wolfson Merit Award. Kirsty M. Edgar was supported by a Leverhulme Trust Early Career Fellowship.
This paper was edited by Aldo Shemesh and reviewed by Gerald M. Ganssen and Sepulcre Sophie.