Distribution of transparent exopolymer particles (TEP) in distinct regions of the Southern Ocean

Highlights

• Transparent exopolymer particles (TEP) were measured in the Southern Ocean during summer.

• Phytoplankton were the main drivers of both horizontal and vertical TEP distribution.

• Light stress and sea ice melt and retreat further tuned TEP distribution.

• TEP enrichment generally occurred near the upper surface (0.1 vs 4 m).

• Upper-surface enrichment was likely enhanced by wind-provoked turbulence and bubbles.

Abstract

Transparent exopolymer particles (TEP) are an abundant class of suspended organic particles, mainly formed by polysaccharides, which play important roles in biogeochemical and ecological processes in the ocean. In this study we investigated horizontal and vertical TEP distributions (within the euphotic layer, including the upper surface) and their short-term variability along with a suite of environmental and biological variables in four distinct regions of the Southern Ocean. TEP concentrations in the surface (4 m) averaged 102.3 ± 40.4 μg XG eq. L⁻¹ and typically decreased with depth. Chlorophyll a (Chl a) concentration was a better predictor of TEP variability across the horizontal (R² = 0.66, p < 0.001) and vertical (R² = 0.74, p < 0.001) scales than prokaryotic heterotrophic abundance and production. Incubation experiments further confirmed the main role of phytoplankton as TEP producers. The highest surface TEP concentrations were found north of the South Orkney Islands (144.4 ± 21.7 μg XG eq. L⁻¹), where the phytoplankton was dominated by cryptophytes and haptophytes; however, the highest TEP:Chl a ratios were found south of these islands (153.4 ± 29.8 μg XG eq (μg Chl a)⁻¹, compared to a mean of 79.3 ± 54.9 μg XG eq (μg Chl a)⁻¹ in the whole cruise, in association with haptophyte dominance, proximity of sea ice and high exposure to solar radiation. TEP were generally enriched in the upper surface (10 cm) respect to 4 m, despite a lack of biomass enrichment, suggesting either upward transport by positive buoyancy or bubble scavenging, or higher production at the upper surface by light stress or aggregation. TEP concentrations did not present any significant cyclic diel pattern. Altogether, our results suggest that photobiological stress, sea ice melt and turbulence add to phytoplankton productivity in driving TEP distribution across the Antarctic Peninsula area and Atlantic sector of the Southern Ocean.

Introduction

Transparent exopolymer particles (TEP) are gel-like organic particles stainable with Alcian Blue, a specific dye for acidic polysaccharides (Alldredge et al., 1993), that have deserved attention due to their influence in biogeochemical and ecological processes (Passow, 2002b). TEP are partly formed by the abiotic self-assembly from dissolved precursors (Chin et al., 1998; Orellana and Verdugo, 2003), thus connecting the dissolved to particulate organic matter continuum (Engel et al., 2004). In addition, TEP affect the biological carbon pump, not only because TEP by themselves may comprise a mean of 5–10% of primary production synthates (Mari et al., 2017) that can sink into the deep ocean, but also because they promote particle aggregation (Engel et al., 2004), thus favoring the sinking of marine snow to the deep ocean (Burd and Jackson, 2009). TEP also influence air-sea gas exchanges like that of carbon dioxide (CO₂) (Wurl et al., 2016; Jenkinson et al., 2018), since they tend to accumulate at the surface microlayer (SML, the uppermost water layer, Cunliffe et al. (2013)), either after ascending through the water column (Azetsu-Scott and Passow, 2004) or upon direct production in this layer (Wurl et al., 2011b).

Phytoplankton are believed to be the main source of TEP and their precursors (Alldredge et al., 1993; Passow, 2002b; Van Oostende et al., 2012; Engel et al., 2015), being diatoms (Passow et al., 1994; Mari and Burd, 1998; Passow et al., 2001; Passow, 2002a) and haptophytes, like Phaeocystis (Hong et al., 1997), the groups that seem to release larger amounts. Prokaryotic heterotrophs (Stoderegger and Herndl, 1999; Ortega-Retuerta et al., 2010) and other organisms, such as suspension feeders (Heinonen et al., 2007), zooplankton (Prieto et al., 2001) and seagrass (Iuculano et al., 2017a), can also produce TEP.

Sinks of TEP comprise photolysis by UV radiation (Ortega-Retuerta et al., 2009a), sinking to the deep ocean, entrance to the atmosphere (Kuznetsova et al., 2005), and degradation and consumption by microorganisms (Ling and Alldredge, 2003). Many variables influence either sources, sinks or both, hindering the prediction of TEP distribution in the ocean. For example, high solar radiation has a dual effect; it stimulates TEP release by microbes (Iuculano et al., 2017b) but also causes TEP photolysis (Ortega-Retuerta et al., 2009a) or affect positively (Shammi et al., 2017) or negatively (Orellana and Verdugo, 2003) the abiotic self-assembly of dissolved exopolymers into TEP. Other variables such as temperature (Nicolaus et al., 1999; Claquin et al., 2008), CO₂ concentration (Engel, 2002), nutrient availability (Mari et al., 2005) and viral infections (Nissimov et al., 2018) can also influence TEP cycling. Moreover, the TEP production per phytoplankton biomass increases along the bloom stages (Pedrotti et al., 2010), thus adding complexity to the TEP dynamics.

The Southern Ocean (SO) is characterized by the presence of the Antarctic Circumpolar Current, which connects the waters of the Pacific, Indian and Atlantic Oceans, and by having strong upwellings that enrich surface waters with macronutrients (Sarmiento et al., 2004). Productivity is generally limited by the lack of iron in combination with deep surface mixing and low light and temperature (Moore et al., 2013; Hoppe et al., 2017), although some regions are locally supplied with iron, particularly in the vicinity of islands (Morris and Sanders, 2011).

The study of TEP distributions in the SO is of particular importance in light of these ocean's peculiarities. The SO is considered the largest region for anthropogenic CO₂ sequestration in the world (Frölicher et al., 2015), especially around the island systems (Pollard et al., 2009), through higher CO₂ solubility in cold waters and a relatively high particulate organic carbon (POC) surface export flux in comparison to lower latitudes (Boyd and Trull, 2007; Marinov et al., 2008). Indeed, C export fluxes have been reported to attain 30–50% of net primary production (Buesseler, 2001). Since TEP may account for an important fraction of POC mass (Engel, 2004; Zamanillo et al., 2019) and export flux (Passow, 2002b; Wurl et al., 2011a), their study in the SO is important to better predict the magnitude of the biological carbon pump and the future dynamics of atmospheric CO₂.

In this study we describe the horizontal and vertical (within the euphotic layer) distributions, and short-term (diel) variability of TEP, along with relevant physical, chemical and biological variables, in four distinct regions of the SO. The four regions were characterized by distinct phytoplankton communities, bloom stages and environmental and ecological properties. Our objectives were: (a) to identify the main drivers of TEP distribution across contrasting environmental conditions, both horizontally and vertically, and (b) to examine the short-term temporal variability of TEP and biological variables, over diel cycles. Data co-variation analyses and experimental incubations were conducted to ascertain the role of microorganisms (phytoplankton vs. heterotrophic prokaryotes) in TEP production.