Temporal patterns of iron limitation in the Ross Sea as determined from chlorophyll fluorescence

Highlights

• The degree of fluorescence quenching is a powerful tool to understand phytoplankton physiology.

• Iron stress follows the different bloom phases of accumulation.

• Levels of iron limitation linked to succession of community structure.

Abstract

The Ross Sea is one of the most productive regions in the Southern Ocean, with a significant role in carbon cycling as well as the massive abundance of higher trophic levels. The seasonal cycle is well established with an early summer Phaeocystis antarctica bloom that declines followed by a diatom bloom in late summer. This seasonal progression of the phytoplankton has been linked to the availability of iron in the mixed layer. Investigating the temporal progression of iron limitation is often limited by both the decreased sampling resolution from traditional platforms, such as ships, and the lack of regular deployments of specific sensors that can measure phytoplankton physiology. Through the use of a novel technique that uses the degree of quenching (NPQ_Glider), determined from a standard fluorometer deployed on a buoyancy glider, a proxy for iron limitation, α_NPQ, was calculated for a glider time series in the Ross Sea from December 2011 to February 2012. Surface chlorophyll concentrations indicated that there were four stages: the first being a pre-bloom phase, the second in which phytoplankton growth was rapid, resulting in the accumulation of biomass; the third in which biomass in the surface layer decreased, and the fourth in which chlorophyll concentrations remained low but the POC:Chl ratio increased. The levels of NPQ_Glider in this region were much higher compared to other Southern Ocean regions, with the highest levels in the third phase. Similarly, α_NPQ remained low throughout most of the time series except for the transition from the second to third phase when the surface biomass decreases. The increase in POC:Chl ratios in the final phase combined with the low values of α_NPQ suggest the switch from a Phaeocystis antarctica bloom to a potentially non-iron limited diatom bloom. These results confirm that the application of novel methodologies to proven and reliable sensors will provide a greater understanding of biogeochemical cycles and their controls throughout the ocean.

Introduction

The Ross Sea is one of the most productive regions in the Southern Ocean (SO) (Arrigo and van Dijken, 2004; Smith et al., 2014a), with an annual productivity that can exceed 200 g C m⁻² (Smith and Kaufman, 2018). This carbon fixation has been estimated to account for roughly a quarter of the total Southern Ocean biological carbon uptake (Arrigo et al., 2008; Arrigo et al., 1998). It is also one of the most well studied regions in the Southern Ocean, and these investigations have demonstrated the importance of the intense seasonal productivity and massive phytoplankton standing stocks to the ecology of its upper trophic levels (Smith et al., 2014a). The high phytoplankton biomass displays a high degree of both spatial (Arrigo et al., 1999; Arrigo and McClain, 1994; Smith et al., 2013) and temporal variability (Smith et al., 2011; Smith et al., 2000); however, the dominant scale of variability appears to be temporal (Jones and Smith, 2017). These variations are driven by both physical and biological controls of seasonal progression, with bloom initiation beginning in late October with decreased ice coverage, increased irradiance, lengthening photoperiods and shoaling mixed layer depths (Smith et al., 2000; Smith and Gordon, 1997). The phytoplankton biomass peaks in mid- to late December, after which further growth is limited by the availability of iron (Ryan-Keogh et al., 2017; Sedwick et al., 2011). Increasing our observations in this region is vitally important to gain a clearer understanding of these physical and biological controls of primary production, given the potential future changes in water column stratification (Boyd et al., 2008; Smith et al., 2014b) and nutrient inputs to this region (Mahowald and Luo, 2003; Tagliabue et al., 2008).

The Ross Sea continental shelf is characterized by a persistent polynya, an area of open water surrounded by sea ice, that greatly increases in size in the austral spring and summer (Arrigo and van Dijken, 2003; Reddy et al., 2007). The phytoplankton assemblage is dominated in spring by the haptophyte Phaeocystis antarctica (Arrigo et al., 1999; Smith and Gordon, 1997). This species reaches very high biomass levels in terms of contribution to total chlorophyll-a, and these begin to decline in late December; after this, diatoms increase in abundance in mid- to late summer (Arrigo and van Dijken, 2004; DiTullio and Smith, 1996; Goffart et al., 2000; Smith et al., 2013; Smith et al., 2000), and can reach similar levels of magnitude as the P. antarctica bloom (Smith et al., 2011). It is postulated that this shift in composition results from decreased iron availability as the water column stratifies and the flux of dissolved Fe from below is decreased, which has significant effects upon the intracellular requirements of both Phaeocystis antarctica and SO diatoms. Culture studies have demonstrated that Southern Ocean diatoms have significantly lower Fe:C ratios when compared to other species (Coale et al., 2003; Kustka et al., 2015; Sedwick et al., 2007; Strzepek et al., 2012; Strzepek et al., 2011) as a result of these species increasing the size of their photosynthetic units rather than the number (Strzepek et al., 2012, Strzepek et al., 2011). Thus, the iron requirements for photosynthesis may be lowered due to this acclimation. Indeed, iron concentrations on the Ross Sea continental shelf have been well documented (McGillicuddy et al., 2015; Sedwick et al., 2011), with pre-bloom and deep-water concentrations of ~1 nM, but spring phytoplankton growth reduces them to an average of 0.06 nM, levels that would be expected to limit growth (Timmermans et al., 2004). These low concentrations continue for much of the growing season, although some localized inputs from dust and deeper mixing can occur (de Jong et al., 2013). Overall, the Ross Sea experiences iron limitation over much of the continental shelf in summer.

Iron limitation of phytoplankton in the ocean is predominantly measured using active chlorophyll fluorescence and the determination of their photochemical efficiency (F_v/F_m) (Kolber et al., 1998), due to the high iron requirements of photosynthetic pigments (Behrenfeld et al., 1996). Whilst these measurements can be routinely made on samples collected from ships, very few systems are included for deployments on autonomous platforms such as gliders (Carvalho et al., 2020), largely due to the large power demand of present instruments. Instead, recent studies have shown that you can obtain similar degrees of information on phytoplankton physiology (Ryan-Keogh and Thomalla, 2020; Schallenberg et al., 2020) from standard fluorometers that are regularly deployed to measure ambient chlorophyll-a concentrations as a proxy for phytoplankton biomass (Roesler et al., 2017). The studies utilize concurrent measurements of F_v/F_m and non-photochemical quenching (NPQ), a decrease in the ratio of photons emitted as fluorescence to those absorbed by photosynthetic pigments (Cullen, 1982; Falkowski and Kolber, 1995; Kiefer, 1973), to confirm mechanistic relationships under cases of iron limitation (Alderkamp et al., 2012; Schallenberg et al., 2020; Schallenberg et al., 2008; Schuback et al., 2015; Schuback and Tortell, 2019), before developing proxies of NPQ from standard fluorometers. This study builds upon these results to investigate the development of iron limitation across the summer growing season on the Ross Sea continental shelf, utilising the degree of quenching from standard fluorescence sensors mounted on profiling buoyancy gliders. Gliders provide unprecedented scales of measurements in both space and time, helping to fill the space-time gaps in radically under-sampled oceans. We examine whether physical forcing mechanisms result in changes in the degree of quenching and iron limitation in a restricted region of the Ross Sea.