Extreme ENSO conditions have contrasting effects on Antarctic euphausiid body condition during winter

doi:10.21203/rs.3.rs-2210989/v1

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Extreme ENSO conditions have contrasting effects on Antarctic euphausiid body condition during winter

https://doi.org/10.21203/rs.3.rs-2210989/v1

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published 06 Apr, 2023

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El Niño Southern Oscillation (ENSO) events are increasing in frequency and intensity, with profound global impacts on marine environments. These events may result in contrasting ocean conditions around the Antarctic Peninsula, with varying effects on euphausiids because of their diverse life histories, habitats, and feeding ecologies. We conducted surveys in August and September 2014 and 2016 around the northern Antarctic Peninsula and examined the dietary carbon sources, trophic position, and body condition of five euphausiids (Euphausia crystallorophias, E. frigida, E. superba post-larvae and larvae, E. triacantha, and Thysanoessa macrura) in relation to environmental conditions each year. Principal component analysis of environmental conditions showed that 2014 was associated with high chlorophyll-a, low salinity, and shallow upper mixed-layer depths, while 2016 was associated with low chlorophyll-a, high salinity, and deep upper mixed-layer depths. Carbon sources varied between years, with most species enriched in δ¹³C in 2016. Trophic position was consistent between years and among species except E. frigida, which was enriched in δ¹⁵N in 2016. E. triacantha was the only species with lower body condition in 2016. We considered these outcomes in the context of the neutral ENSO index of 2014 and the positive ENSO index of 2016, which had contrasting effects on the type, quality, and distribution of food resources each year. We conclude that ENSO conditions around the northern Antarctic Peninsula may result in a more favorable feeding environment for all euphausiids except E. triacantha, which may be the most negatively impacted by the predicted increase in El Niño conditions.

ENSO

Southern Ocean

euphausiid

climate change

Over the last several decades, the Antarctic Peninsula has undergone rapid environmental changes: increases in atmospheric (Jones et al. 2019) and seawater temperatures (Verona et al. 2018), decreases in the duration of annual sea-ice cover (Stammerjohn et al. 2012), and predicted increases in the frequency and/or intensity of extreme climate events (Cai et al. 2014; Morley et al. 2020), which may further modulate sea-ice dynamics in this region. Because changes to the physical environment heavily influence ecological and biological interactions in polar marine ecosystems, understanding how such change affects these ecosystems is critical for predicting how they may respond to future change.

As mostly primary or secondary consumers sensitive to fluctuations in environmental conditions, Antarctic zooplankton can be good indicators of environmental change (Johnston et al. 2022). Shifts in zooplankton distribution, abundance, prey consumption, growth, and reproduction have all been linked to environmental variability (e.g., Siegel and Loeb 1995; Quetin et al. 2007; Mackey et al. 2012; Constable et al. 2014; Driscoll et al. 2015; Richerson et al. 2018; Reiss et al. 2020). Of all species, Euphausia superba has been the most intensively studied (e.g., Atkinson et al. 2004, 2019; Meyer et al. 2010; Flores et al. 2012). However, understanding the effects of environmental variability on other euphausiids may provide valuable insight into how future environmental change may reshape the ecological landscape of the Antarctic Peninsula.

The five euphausiid species most common in the marine ecosystem around the northern Antarctic Peninsula include Euphausia crystallorophias, E. frigida, E. superba, E. triacantha, and Thysanoessa macrura. These species are distinct with respect to habitat and feeding ecology (Table 1), and therefore may be affected differently by environmental change. Ongoing environmental trends around the Antarctic Peninsula over the last several decades include strengthened westerly winds associated with the positive phase of the Southern Annular Mode (SAM), a poleward shift in the Antarctic Circumpolar Current (ACC), increased water temperatures, shoaled upper mixed layer (UML) depths, an increased presence of warm Circumpolar Deep Water (CDW) on the continental shelf, and decreased sea-ice extent and duration (sen Gupta et al. 2009; Constable et al. 2014). Increased warming is expected to lead to a decrease in the nutritional quality of phytoplankton (Deppeler and Davidson 2017). While these environmental changes are likely to persist and perhaps intensify in the future, they may be compounded by a projected increase in the positive trend of the SAM (Zhang et al. 2020) and an increase in the frequency and intensity of extreme El Niño Southern Oscillation (ENSO) events (Cai et al. 2014), which have pronounced impacts on sea ice variability along the Antarctic Peninsula (Yuan 2004) and may further disrupt ecological relationships in this region.

The extent to which these changes may affect the life cycles of Antarctic euphausiids is known to some degree for E. superba (Quetin et al. 2007; Loeb et al. 2009; Meyer et al. 2010; Flores et al. 2012) and to a lesser degree for T. macrura (Richerson et al. 2018), but not for other euphausiid species. Responses to environmental change will depend on the physiological tolerances and prey requirements of each species. For more stenothermic species, such as E. crystallorophias and E. superba (Mackey et al. 2012; Atkinson et al. 2019; Johnston et al. 2022), these changes may result in habitat constriction. For other species, habitat may expand or contract as their preferred prey are redistributed as a result of shifts in marine productivity concomitant with the warming and reduced ice cover observed along the peninsula (Moline et al. 2004; Quetin et al. 2007; Montes-Hugo et al. 2009).

Table 1

Habitats and diets of euphausiid species common around the northern Antarctic Peninsula
Species	Habitat	Diet	Source
Euphausia crystallorophias	Stenothermic. Considered a coastal species and is closely tied to ice-covered habitats, although it is not known to inhabit or feed in ice	Considered an omnivore, but may become more carnivorous or detritivorous during winter	Kattner and Hagen 1998; Pakhomov et al. 1998; Falk-Petersen et al. 1999; Nicol et al. 2004
Euphausia frigida	Found mostly between the southern boundary of the Southern Antarctic Circumpolar Current Front (SACCF) and the Antarctic Polar Front	Considered a surface-feeding omnivore	Phleger et al. 1998; Mackey et al. 2012
Euphausia superba post-larvae	Stenothermic. Abundant over continental shelves during autumn and winter and expands its distribution to the shelf break and oceanic regions to spawn during spring and summer	Primarily herbivorous during summer and may feed opportunistically on zooplankton or detritus during winter	Hagen et al. 2001; Siegel 2005; Atkinson et al. 2008; Meyer et al. 2010; Schmidt et al. 2011; Reiss et al. 2017
Euphausia superba larvae	Stenothermic. Abundant mostly in offshore regions around the northern Antarctic Peninsula	Primarily herbivorous until their first winter, and may switch to a heterotrophic and/or sea ice biota diet in autumn and winter	Daly 1990; Meyer et al. 2002; Siegel 2005; Atkinson et al. 2008; Siegel et al. 2013; Walsh et al. 2020
Euphausia triacantha	Northern-most distribution of common euphausiids. A warm-water species found predominantly within the Antarctic Circumpolar Current, between the SACCF and the Antarctic Polar Front	A deep vertical migrator relative to other euphausiids with a coarser mesh feeding basket, and may be mostly carnivorous	Phleger et al. 1998; Mackey et al. 2012; Tarling et al. 2012; Loeb and Santora 2015
Thysanoessa macrura	Considered eurythermic with a ubiquitous distribution across the peninsula shelf and may be found deeper than most euphausiids except E. triacantha	Considered omnivorous, but may feed heavily on zooplankton	Kattner et al. 1996; Donnelly et al. 2006; Driscoll et al. 2015; Loeb and Santora 2015; Richerson et al. 2018

As part of its decades-long ecosystem monitoring program around the northern Antarctic Peninsula, the U.S. Antarctic Marine Living Resources (AMLR) Program conducted five consecutive winter surveys from 2012–2016. We collected samples of the five common euphausiid species for analyses of sources of dietary carbon (carbon stable isotopes), trophic position (nitrogen stable isotopes), and body condition (lipid content) to compare their responses to winter environmental variability. Throughout the study period, we observed a trend of decreased lipid content in 2014 in all euphausiids, regardless of habitat or diet (Walsh et al. 2020; Walsh and Reiss 2020). Lipid content rebounded in all species in 2015 but then diverged among species in 2016, with the highest lipid content of all study years in E. crystallorophias, E. superba post-larvae, and T. macrura, and the lowest lipid content of all years in E. triacantha.

Environmental variability during 2014 and 2016 largely was the result of a “failed” ENSO event in 2014 and an extreme ENSO event in 2015/16. During austral summer and fall of 2014, the formation of an anomalous warm water volume in the tropical Pacific Ocean and multiple westerly wind bursts signaled the development of a strong ENSO event (Levine and McPhaden 2016). However, during austral winter 2014, a large easterly wind burst halted the development, but the remaining warm water volume set the stage for the development of an extreme ENSO event during the first half of 2015 that persisted into 2016 (McPhaden 2015).

In this paper, we review contrasting oceanographic conditions in the study site between a neutral ENSO in 2014 and a strong ENSO in 2016 and examine how those conditions affected sources of dietary carbon, trophic level, and body condition of five important euphausiid species with different overwintering life history strategies. We discuss how the environmental conditions each year may have affected food availability and quality for each of the five species across the northern Antarctic Peninsula, and the potential effects of predicted ENSO extremes in the future.

Survey methods for the U.S. AMLR Program Antarctic winter studies have been published previously (Reiss et al. 2015, 2017; Walsh et al. 2020; Walsh and Reiss 2020).

Survey area and general survey design

The U.S. AMLR Program conducted winter surveys (August and September 2014, August 2016) around the northern Antarctic Peninsula aboard the National Science Foundation’s research vessel/ice breaker (RVIB) Nathaniel B. Palmer (Fig. 1). We sampled a historical grid of 110 fixed stations that were categorized into four sampling areas: the Elephant Island Area (EI; 43,865 km²), the Joinville Island Area (JI; 18,151 km²), the South Area (SA, or Bransfield Strait; 24,479 km²), and the West Area (WA, or area immediately north of Livingston and King George Islands; 38,524 km²). In 2016, we also sampled the Gerlache Strait (GS). Descriptions of the bathymetry and circulation in these areas is provided in Reiss et al. (2015). Logistical constraints (e.g., time, inclement weather, thick ice) prevented us from sampling all stations each year, but all areas were sampled each year.

At-sea sampling

At each station, we deployed a Conductivity, Temperature, Depth (CTD) rosette equipped with 24 Niskin bottles (10 l) to 750 m or to within 10 m of the bottom (SBE911; Sea-Bird Scientific). The bottles collected seawater on the upcast at 750, 200, 100, 75, 50, 40, 30, 20, 15, and 5 m. We determined the upper mixed layer (UML; m) depth at each station from CTD profiles by calculating the depth at which the water density changed by 0.05 kg m^− 3 relative to the average density of the upper 10 m of the water column (Mitchell and Holm-Hansen 1991). UML temperature and salinities were defined to be means over the depth range of the UML.

To examine differences in hydrographic structure between 2014 and 2016, we identified a transect extending from 60^oS in the EI sampling area directly south to 62.75^oS in the JI sampling area (hereafter “the EI transect”) (grey shaded area on Fig. 1). Along the EI transect, we determined the position of the intersection of the 27.6 kg m^− 3 (σ_t) isopycnal with the surface each year as an indicator of the presence and extent of CDW from the Drake Passage in the survey area (Reiss et al. 2009), and the amount of cold, high-salinity water in the Bransfield Strait. We also compared depth profiles of temperature and salinity at two locations in the SA sampling area (the Bransfield Current and the Bransfield Basin) to further examine hydrographic variability in relation to the presence of CDW in the Bransfield Strait between these two years (blue and yellow stars on Fig. 1).

We determined chlorophyll-a (chl a) from water samples collected between 5 and 200 m (Holm-Hansen et al. 1965; Holm-Hansen and Riemann 1978). We filtered samples (285 ml) through glass fiber filters (25.4 mm; Whatman, Inc.), and we extracted chl a in methanol over 24 hrs and determined chl a concentration using a calibrated Trilogy fluorometer (Turner Designs). We calculated integrated chl a (to 100 m, mg chl a m^− 2) using concentrations at the discrete depths of each sample from 5 m to 100 m and averaging between depths to calculate the intermediate depth concentrations.

At each station, we towed an Isaacs-Kidd Midwater Trawl (IKMT) net with 505 µm mesh to 170 m or to within 10 m of the bottom. We determined the volume of seawater filtered using a calibrated flow meter mounted on the net’s frame (Model 2030 R, General Oceanics, Inc.). We identified large zooplankton, including euphausiids, using a microscope when more detailed identification was required.

Stable isotope analysis

Stable isotopes provide a record of diet over several weeks to months (Frazer et al. 1997). Higher ratios of heavy to light nitrogen isotopes (¹⁵N/¹⁴N, denoted as δ¹⁵N) reflect higher trophic position, with consumer tissue enriched in δ¹⁵N by 3–4‰ relative to prey (Post 2002). Ratios of heavy to light carbon isotopes (¹³C/¹²C, denoted as δ¹³C) reflect different sources of dietary carbon.

We used the same samples for stable isotope analysis that we used for lipid analysis (Fig. 2). We extracted lipid first, then freeze-dried vials of lipid-free zooplankton for 14–16 hrs. We then pulverized dried samples using a mortar and pestle, and weighed aliquots (0.8–1.2 mg) into tin capsules (5 x 9 mm, Costech Analytical Technologies). Samples were analyzed for δ¹³C and δ¹⁵N at the University of California Davis Stable Isotope Facility (UCD SIF) using a PDZ Europa ANCA-GSL elemental analyzer interfaced to a PDZ Europa 20–20 isotope ratio mass spectrometer (Sercon). We report ratios in parts per thousand (‰) compared to standards (PeeDee limestone for δ¹³C and atmospheric N₂ for δ¹⁵N).

We did not acid-treat euphausiid samples prior to stable isotope analysis because zooplankton contain few, if any, calcified structures, and acidification may skew δ¹⁵N values (Schlacher and Connolly 2014). We did remove lipid from samples prior to stable isotope analysis because it is depleted in ¹³C relative to other tissues and may result in biased values of δ¹³C. However, lipid removal can also skew δ¹⁵N values (Post et al. 2007). When lipid is extracted using the technique we used (Folch et al. 1957), mean fractionation of δ¹⁵N is only 0.25‰, which is close to typical analytical error (Post et al. 2007).

Lipid analysis

Compared to stable isotopes, fluctuations in lipid content are more rapid and may reflect changes in diet over days to weeks (Meyer et al. 2002). We froze individuals of each species collected from the same station and year at ˗20°C until lipid analysis, usually no later than 48 hours after collection (Fig. 2). For one E. crystallorophias sample in 2016, we pooled 17 individuals across two stations in the South Area to provide a suitable mass for lipid analysis. We extracted lipid from aliquots of 0.5–1.5 g of homogenized animals in a 2:1 chloroform:methanol solution with 0.01% butylated hydroxytoluene as a preservative (Folch et al. 1957; Budge et al. 2006). We filtered lipid dissolved in the chloroform fraction through anhydrous sodium sulfate into pre-weighed glass tubes to remove all traces of methanol and water, and then evaporated the chloroform solvent under nitrogen to dryness. We then re-weighed the tubes to the nearest 0.001 g on the same calibrated analytical balance (Model PA214, S/N: 8331270072, Ohaus) to determine percent lipid in each sample. We determined dry mass of samples by freeze-drying all 2016 lipid-extracted samples for 16 hrs (VirTis Benchtop K Lyophilizer, SP Scientific) and adding back the mass of the removed lipid. We calculated the mean percent mass loss for each species and applied that to the wet mass of each sample to determine dry mass.

Data analysis

We compared environmental variables (water temperature, salinity, UML, and chl a) between years using the Mann-Whitney U test for non-normal data (Shapiro-Wilk normality test).

We used the Bivariate ENSO index (BEST, Smith and Sardeshmukh 2000) for each sampling month in each year to represent the prevailing environmental conditions. We also examined values from three and six months prior to sampling each year to account for temporal lags between shifts in the BEST index and when environmental conditions in Antarctica reflected those shifts. We then performed a principal component analysis (PCA) to characterize environmental conditions at each sampling station using chl a, water temperature, salinity, and UML depth. The first and second principal components (PC1 and PC2, respectively) were compared between years using the Mann-Whitney U test for non-normal data (Shapiro-Wilk normality test).

To identify differences in body condition within species between years, we arcsine-square-root transformed percent lipid data to approximate normal distributions. We compared species-specific differences in body condition between years using the Student’s t-test. To identify differences in δ¹³C and δ¹⁵N within species between years, we used the Student’s t-test when the variable was normally distributed, and the Mann-Whitney U test when the variable failed the Shapiro-Wilk normality test. We performed all statistical tests in R, version 4.1.2 (R Core Team 2021) and created all graphics using QGIS (v 3.4.7-Madeira) and the R package “ggplot2” (Wickham 2016).

Environmental differences between years

Environmental conditions varied between years (Table 2). Chl a was higher in 2014 (Mann-Whitney U = 7371, p < 0.001). Salinity was higher in 2016 (Mann-Whitney U = 3678.5, p < 0.001). Although UML depth among stations between years was highly variable and the difference between years was not significant, UML depth was deeper in 2016 (Mann-Whitney U = 4398, p = 0.07). Temperature likely did not differ between years (Mann-Whitney U = 4917, p = 0.55).

The first principal component (PC1) explained 41% of the variance in environmental conditions at sampling stations. PC1 scores differed between years (Mann-Whitney U = 3096, p < 0.001), with 2014 associated with negative scores (-0.404 ± 1.199 (SD)) and 2016 associated with positive scores (0.455 ± 1.22 (SD)). Salinity and UML depth were positively correlated with PC1 in both years and trended in the opposite direction as chl a, which was negatively correlated with PC1 in both years. Water temperature was not correlated with PC1 in either year.

The second principal component (PC2) explained 25% of the variance in environmental conditions at sampling stations. PC2 scores were not different between years (Mann-Whitney U = 4669, p = 0.39). Out of all environmental variables, only water temperature was correlated with PC2 and increased as PC2 scores increased in both years.

Table 2

Water column properties (mean ± SD) for all sampling areas and years. The Gerlache Strait was not sampled in 2014. Data for each station can be found in Walsh et al. (2020)
AMLR area	Year	Number stations sampled	Integrated chl a (100 m)	Water temp. (^oC)	Salinity	Upper mixed-layer depth (m)
Elephant Island (EI)	2014	43	17.24 ± 8.09	-1.71 ± 0.14	33.92 ± 0.20	62.70 ± 36.45
	2016	29	15.38 ± 5.08	-1.66 ± 0.21	34.09 ± 0.22	93.59 ± 100.05
Joinville Island (JI)	2014	23	9.89 ± 5.62	-1.75 ± 0.10	34.35 ± 0.17	75.35 ± 90.44
	2016	2	8.69 ± 0.73	-1.74 ± 0.07	34.36 ± 0.04	179.5 ± 75.66
South Area (SA)	2014	17	9.45 ± 2.97	-1.77 ± 0.07	34.27 ± 0.14	82.00 ± 82.57
	2016	29	5.80 ± 1.27	-1.72 ± 0.16	34.39 ± 0.10	142.03 ± 143.12
West Area (WA)	2014	21	17.39 ± 4.28	-1.81 ± 0.05	33.95 ± 0.15	79.91 ± 64.80
	2016	20	10.32 ± 2.72	-1.79 ± 0.06	34.11 ± 0.21	64.57 ± 110.78
Gerlache Strait (GS)	2014	0	NA	NA	NA	NA
	2016	9	1.91 ± 0.87	-1.65 ± 0.11	34.27 ± 0.04	58.78 ± 63.24

ENSO indices between years

Because ENSO indices are reported as single values by month and this study’s sampling windows each year spanned two months in 2014 (mid-August through mid-September) and one month in 2016 (August), statistical tests to explore relationships between ENSO indices and environmental variables were not feasible. Visual inspection of ENSO indices the months of sampling, as well as three and six months prior to sampling, showed little variation in 2014 (Fig. 3a). The ENSO index six months prior to sampling in 2016 reflected the strong ENSO signal that developed in late 2015. Although the signal declined over the next three months and was negative by the month of sampling, PC1 scores in 2016 reflected a temporal lag between the shift in the ENSO signal and when environmental conditions reflected the shift, and remained elevated over 2014 scores (Fig. 3b).

Water column properties along the EI transect and the Bransfield Strait

In 2014, the water column along the EI transect was more stratified than in 2016. The 27.6 σ_t isopycnal intersected the surface approximately 250 km from the northernmost stations, within the SA sampling area (Fig. 4c). In 2016, the 27.6 σ_t isopycnal intersected the surface approximately 100 km farther north compared to 2014, suggesting that colder, saltier water from the Weddell Sea was present in greater proportions over the study area in 2016 (Fig. 4f).

Depth profiles of temperature and salinity show that the extent of CDW intrusion into the SA sampling area varied between 2014 and 2016 (Fig. 5). Depth profiles of temperature at the Bransfield Current station show that in 2014, warm CDW was a strong feature between 200 and 400 m, suggesting that CDW flowed into the SA sampling area from the southwest (Fig. 5a). CDW was also present at the Bransfield Basin station in 2014, although the range of temperatures among years at this station was smaller (Fig. 5c). CDW was not a strong feature in the SA sampling area in 2016; water at both stations was colder and saltier, indicating that Weddell Sea Shelf Water (WSSW) was more prevalent in the region during 2016.

Stable isotopes

Isotopic turnover rates vary among species and are linked to temperature (Frazer et al. 1997), with poikilotherms in cold environments having slower turnover rates than homeotherms with higher metabolic rates (Ventura and Catalan 2008). Turnover rates have also been linked to size, with faster turnover rates for larger organisms (Post 2002). Data on turnover rates in Antarctic euphausiids is limited; however, Frazer et al. (1997) determined that turnover in E. superba larvae during winter may be negligible, while turnover rates during spring and summer may be higher. For this study, we assume that turnover rates among euphausiid species of similar sizes are comparable and that isotopic signatures largely reflect diets consumed weeks to months prior to sampling.

Dietary carbon sources (δ¹³C)

E. crystallorophias did not differ in δ¹³C between years (t_5.59 = 0.709, p = 0.51) (Fig. 6) and was enriched in δ¹³C relative to all other species. Although the difference was not significant, E. crystallorophias was the only species with higher δ¹³C values in 2014. E. superba larvae also formed a distinct group with respect to δ¹³C, between E. crystallorophias and the other euphausiids. E. superba larvae had higher values of δ¹³C in 2016 (t_13.7 = ˗4.35, p < 0.001). The rest of the euphausiid species demonstrated considerable overlap in δ¹³C. E. frigida, E. superba post-larvae, and T. macrura were all significantly enriched in δ¹³C in 2016 (E. frigida: t_9.39 = ˗5.15, p < 0.001; E. superba post-larvae: t_42.55 = ˗2.17, p = 0.036; T. macrura: Mann-Whitney U = 7, p < 0.001). E. triacantha showed little difference in δ¹³C between years (t_5.97 = ˗1.05, p = 0.34).

Trophic position (δ¹⁵N)

Of all species, only E. frigida showed a significant difference in δ¹⁵N between years, with higher values in 2016 (t_9.89 = -7.63, p < 0.001). Although the differences were not significant, E. crystallorophias, E. superba post-larvae, and T. macrura were all enriched in δ¹⁵N in 2016 (E. crystallorophias: Mann-Whitney U = 8, p = 1; E. superba post-larvae: Mann-Whitney U = 175, p = 0.08; T. macrura: Mann-Whitney U = 32, p = 0.07). E. superba larvae and E. triacantha showed little difference in δ¹⁵N values between years (E. superba larvae: Mann-Whitney U = 87, p = 0.78; E. triacantha: t_3.44 = 0.15, p = 0.89).

Body condition (lipid content)

Limited data are available on the overwinter lipid utilization strategies of most Antarctic euphausiids except for E. superba. Most studies on E. superba (e.g., Meyer 2012) cite reduced feeding and metabolic rates in combination with increased mobilization of stored lipid to survive winter months when food availability is low. Studies on E. crystallorophias (Kattner and Hagen 1998)d macrura (Hagen and Kattner 1998) also cite increased mobilization of stored lipid during winter. However, since these early studies, feeding activity during winter has been shown to be regional, with E. superba in the Bransfield Strait showing more evidence of overwinter feeding than E. superba in other regions of Antarctica (Schmidt et al. 2014). Data on lipid content collected during U.S. AMLR Program summer surveys show that lipid content in E. superba and T. macrura is higher in winter than in summer (U.S. AMLR Program, unpubl.), suggesting that euphausiids continue to feed to some extent in the survey area during winter, and that euphausiid lipid content in this study reflected the feeding environment at the time samples were collected.

Although differences in lipid content in E. crystallorophias, E. frigida, and E. triacantha did not precisely meet the p = 0.05 threshold, these species were likely different between years (E. crystallorophias: t_5.29 = ˗2.52, p = 0.051; E. frigida: t_8.74 = ˗2.15, p = 0.061; E. triacantha: t_5.78 = 2.47, p = 0.0501) (Fig. 7). Both E. crystallorophias and E. frigida had higher lipid content in 2016, while E. triacantha had lower lipid content in 2016. E. superba post-larvae, E. superba larvae, and T. macrura all had significantly higher lipid content in 2016 (E. superba post-larvae: t_42.88 = ˗5.30, p < 0.001; E. superba larvae: t_10.53 = ˗2.66, p = 0.023; T. macrura: t_15.91 = ˗3.69, p = 0.002).

The Antarctic Peninsula ecosystem has been disproportionately affected by regional warming trends over the last several decades (Jones et al. 2019), with cascading effects for organisms that depend on a suite of ideal conditions for optimal feeding, growth, and reproduction (Quetin et al. 2007). We observed inter-annual changes in body condition in five species of Antarctic euphausiids that cannot be fully explained by changes in trophic position or sources of dietary carbon. While differences in annual lipid content were not significant for all species between years (likely due to small sample sizes for some species), we observed a general pattern of low lipid content in 2014 for all euphausiids. We also observed higher lipid content in 2016 for all species except E. triacantha. Because the SAM phase was variable and mostly positive in the six months leading up to the survey period each year (https://legacy.bas.ac.uk/met/gjma/sam.html accessed 11 August 2021) and sea ice cover was relatively low and similar in spatial coverage in both 2014 and 2016 (Walsh et al. 2020), we propose that environmental conditions generated by the neutral 2014 ENSO event and the extreme 2016 ENSO event were responsible for the observed trends in euphausiid lipid content between these years. Below we discuss how these events shaped the pelagic environment each year, how the prevailing environmental conditions may have affected prey quality and availability for each euphausiid species, and how Antarctic euphausiids may be affected in the future by projected increases in the frequency of extreme climate events.

Annual differences in environmental conditions and the biological community

We observed shallow UML depths, highly stratified surface layers with low salinity, and high levels of primary production in 2014. These conditions are consistent with the prevalence of warm CDW in the survey area that likely resulted from the strong easterly wind burst during austral winter that stopped the anticipated ENSO event from developing (McPhaden 2015). Wind stress anomalies around Antarctica may result in differences in sea surface height that shoal the boundary between cold surface water and warmer water below, causing bottom Ekman flow of CDW onto the continental shelf (Spence et al. 2017; Webb et al. 2019).

Environmental conditions in 2014 likely facilitated phytoplankton blooms dominated by smaller species, primarily cryptophytes (Moline et al. 2004; Mendes et al. 2013). While we did not analyze phytoplankton community structure, small species such as prymnesiophytes and cryptophytes may have been the dominant species in 2014. E. superba do not graze efficiently on most assemblages of prymnesiophytes or crytophytes, even when chl a concentrations are high (Haberman et al. 2003).

Phytoplankton communities composed of smaller species are advantageous to salps, which graze more efficiently than E. superba on smaller particles (Moline et al. 2004). Although salp abundance among sampling stations during the study was highly variable between years, salps were more than twice as abundant in 2014 (2014: 10.12 ± 22.77 ind. m^− 2 (SD); 2016: 4.16 ± 5.79 ind. m^− 2 (SD)). Because phytoplankton communities dominated by prymnesiophytes and cryptophytes are grazed at low rates, these ecosystem conditions may sustain high chl a concentration and may negatively impact primary and secondary consumers (Mendes et al. 2013).

Atmospheric and ocean circulation patterns were different in 2016 as a result of the extreme ENSO event. Spatial shifts in the subtropical and polar front jets during ENSO-positive events result in colder, icier conditions in the Atlantic sector of the Southern Ocean and warmer, less icy conditions in the Pacific sector (Yuan 2004). The dip in the subpolar jet toward the tip of the Antarctic Peninsula during ENSO-positive conditions intensifies the Weddell gyre, causing WSSW to flow into the northern Antarctic Peninsula region (Loeb et al. 2009; Reiss et al. 2009). We observed evidence of WSSW in the survey area in 2016 consistent with previous observations from the survey area of deep UML depths and low chl a concentrations associated with ENSO-positive conditions and WSSW intrusion (Reiss et al. 2009).

WSSW is iron-enriched (Reiss et al. 2009; Ardelan et al. 2010), which favors the growth of larger phytoplankton cells (Helbling et al. 1991). Chl a concentration has been shown to be inversely related to phytoplankton biovolume, with low concentrations of chl a related to high concentrations of larger-celled phytoplankton (Felip and Catalan 2000). Although we did not measure water-column iron in this study, the observed environmental conditions in 2016 are consistent with the massive diatom bloom that occurred around the northern Antarctic Peninsula in spring and summer of 2015/16 (Costa et al. 2021).

Annual differences in source carbon

E. frigida, E. superba post-larvae and larvae, and T. macrura were all enriched in δ¹³C in 2016, while E. crystallorophias and E. triacantha showed no differences in δ¹³C between years. In polar environments, higher values of δ¹³C generally indicate increased feeding on sea-ice resources compared to water-column resources (Frazer 1996), but may also indicate increased benthic feeding (France 1995) or feeding in highly productive areas (Fischer 1991).

E. crystallorophias are mostly found at the southernmost stations of the survey area, while E. triacantha are mostly found at the northernmost stations. In 2016, neither species was common around the tip of the peninsula or in the eastern Bransfield Strait, where WSSW has the strongest influence during ENSO-positive events (Reiss et al. 2009; Dotto et al. 2016; Moffat and Meredith 2018) and where differences in environmental conditions between years were most likely to impact the δ¹³C signal of food resources. Conversely, E. frigida, E. superba post-larvae, and T. macrura were distributed more broadly across the continental shelf area and likely encountered a feeding environment that was influenced by the WSSW intrusion into the survey area and the diatom bloom that occurred earlier in the year. We found that ratios of fatty acids (FA) indicative of diatom consumption in E. superba post-larvae were high in 2016 relative to 2014, suggesting diatoms were abundant in the survey area in 2016 (Walsh et al. 2020). These results indicate that δ¹³C enrichment in E. frigida, E. superba post-larvae, and T. macrura occurred either through consuming diatoms directly, or through consuming diatom-dependent prey.

Although E. superba larvae were also enriched in δ¹³C in 2016, ratios of FA indicative of diatom consumption in larvae were identical between 2014 and 2016 (Walsh et al. 2020), suggesting that although diatoms were abundant in 2016, larvae did not rely on them for nutrition. E. superba post-larvae may perform deep vertical migrations (> 1000 m) and feed on benthic resources (Schmidt et al. 2011), and while E. superba larvae may also feed on benthic resources during winter (Daly 2004), their vertical migration patterns are poorly understood and may vary by region. Given the lack of extensive sea ice in both years and the presence of larvae over the continental shelf and slope, we propose that larvae were likely enriched in δ¹³C as a result of benthic feeding; however, future studies should focus on vertical migration patterns in E. superba larvae to understand the extent to which larvae exploit benthic resources.

Annual differences in trophic position

E. frigida were enriched in δ¹⁵N by 1‰ in 2016 and were the only species with a significant difference in δ¹⁵N values between years. While this difference may reflect a larger contribution of heterotrophic prey in E. frigida in 2016, it does not represent a full trophic level shift. Mean differences in δ¹⁵N values between years for all other species ranged from 0.06‰ (E. triacantha) to 0.4‰ (T. macrura), indicating that differences in environmental conditions and in the phytoplankton community between years had a negligible effect on trophic position.

Annual differences in body condition

In 2014, environmental conditions likely resulted in an ecosystem-wide shift in the phytoplankton community to small species, leading to less-efficient grazing and bottom-up effects on the body condition of all euphausiids, despite their varied habitats, feeding strategies, and life histories. In 2016, all species except E. triacantha had higher lipid content. The high iron concentration present in WSSW may have resulted in lipid-enriched diatom assemblages. Cellular FA concentrations in diatoms grown in an iron-rich environment are higher than in diatoms grown in an iron-limited environment, and copepods that fed on iron-enriched diatoms had higher total FA concentrations than those that fed on iron-deficient diatoms (Chen et al. 2011). Diatom consumption has also been linked to higher growth rates in E. superba post-larvae (Pond et al. 2005).

While high lipid content in 2016 suggests that E. crystallorophias and T. macrura fed to some extent during winter, their improved body condition may reflect more favorable feeding conditions in their respective habitats during the previous spring and summer. Both species may not feed consistently throughout winter and instead store more than half their lipid as wax esters, which are a long-term form of energy storage and which allow them to maintain high levels of lipid throughout winter in preparation for spawning prior to the spring phytoplankton bloom (Hagen and Kattner 1998; Ju and Harvey 2004). Source carbon and trophic position were nearly identical in E. crystallorophias between years, yet lipid content nearly doubled in 2016, suggesting that prey quality was the driving factor in lipid accumulation in southern sampling areas. T. macrura varied in source carbon between years but trophic position remained consistent, suggesting that their nearly two-fold increase in lipid content resulted from either primary or secondary consumption of diatoms during the spring/summer diatom bloom.

E. frigida and E. superba store lipid as triacylglycerol (Phleger et al. 1998), which is a short-term form of energy storage (Nicol et al. 2004), and therefore cannot rely on lipid accumulated during spring and summer to survive winters with low productivity. The nearly two-fold increase in lipid content in E. superba post-larvae in 2016 was likely the result of directly feeding on diatoms throughout the winter. In contrast to E. superba post-larvae, which aggregate in the Bransfield Strait during winter (Reiss et al. 2017), E. frigida are considered an oceanic, “cold water” species (Mackey et al. 2012; Loeb and Santora 2015) and are generally found over the northern area of the continental shelf. Diatoms may have been less abundant in areas where E. frigida are common because of less influence of WSSW and an onshore-to-offshore gradient in large to small phytoplankton cells (Montes-Hugo et al. 2008). Little is known about the overwintering strategies of E. frigida; however, this species was enriched in both δ¹³C and δ¹⁵N in 2016, yet had only a moderate increase in lipid content, indicating that they may have been secondary consumers of diatoms.

While E. superba larvae had increased lipid content in 2016, the difference was unremarkable compared to euphausiids that likely consumed diatoms at some point prior to or during winter, suggesting that benthic resources were suboptimal compared to pelagic resources in 2016.

E. triacantha are distinct among the five euphausiids with respect to habitat and diet. They are considered an oceanic, “warm water” species and are distributed across the most northern areas of the continental shelf and slope and are found mostly in the Drake Passage (Mackey et al. 2012), where they perform deep diel vertical migrations (Loeb and Santora 2015). E. triacantha are mostly carnivorous and have coarse mesh-size filter baskets for feeding (Loeb and Santora 2015), and may be unable to graze efficiently on small phytoplankton cells. While other omnivorous or carnivorous species may be secondary consumers of diatoms, E. triacantha gain lipid independent of diatom availability (Stübing and Hagen 2003).

E. triacantha also differ from other euphausiids in their phenology. E. triacantha are the only euphausiids with considerable temporal overlap of their adult stage with E. superba larvae (Loeb and Santora 2015). Positive correlations between abundance anomalies of E. triacantha and E. superba larvae have been observed over 17 years of U.S. AMLR Program summer surveys, suggesting that E. superba larvae, primarily furcilia stages, may be a primary prey item for E. triacantha during late winter (Loeb and Santora 2015).

Patterns of lipid accumulation in E. triacantha between years may have been related to the degree of habitat overlap between E. triacantha and E. superba larvae. In 2014, these species had a high degree of overlap in dietary source carbon, suggesting that both fed in the water column on suboptimal resources and that E. superba larvae were an available prey item for E. triacantha. However, in 2016, benthic feeding in E. superba larvae may have made them unavailable as a prey item for E. triacantha, which are not common over continental shelves (Mackey et al. 2012). Although E. triacantha store a small proportion of their lipid as wax esters (Phleger et al. 1998), the sharp decline in lipid between 2014 and 2016 suggests that E. triancantha must continue to feed to some degree throughout winter, and that they may have a substantial impact on E. superba populations around the northern Antarctic Peninsula.

Implications

Of all euphausiids in this study, E. triacantha may be the most negatively affected by changing conditions around the Antarctic Peninsula. Under warming conditions, both E. triacantha and E. superba are expected to shift their distributions south, although not to the same extent (Mackey et al. 2012). E. triacantha will likely remain farther north (Mackey et al. 2012) and are projected to have reduced habitat overlap with E. superba in the future.

Winter sea ice is strongly related to E. superba recruitment (Siegel and Loeb 1995; Loeb et al. 1997, 2009; Atkinson et al. 2004; Saba et al. 2014); however, extensive winter sea ice does not necessarily translate into high abundances of E. superba larvae around the northern Antarctic Peninsula (Walsh et al. 2020). Therefore, although ENSO events result in colder, icier conditions in this region, the strong influence of the positive SAM may mean that ice cover will be more variable and perhaps more mobile in the future. Abundant E. superba larvae may not be available to E. triacantha every winter because of the unpredictable nature of sea ice around the northern Antarctic Peninsula. Additionally, a substantial proportion of E. superba larvae around the northern Antarctic Peninsula may not be the result of local production, but rather may be transported to this region from “upstream” areas farther southwest along the peninsula (Siegel et al. 2003; Siegel 2005; Conroy et al. 2020). Larvae may advect northeast in ocean currents, and increasing evidence suggests that larvae are also transported within sea ice (Meyer et al. 2017; Veytia et al. 2021). While ENSO events increase sea ice extent around the northern Antarctic Peninsula, they have the opposite effect along the western Antarctic Peninsula because of the weakened polar front jet and the anomalous heat flux to this area from the north (Yuan 2004). Increased presence of CDW on the western peninsula shelf resulting from other modes of climate forcing (i.e., the SAM) may further reduce sea ice cover along the western Antarctic Peninsula (Vaughan et al. 2003). Decreased sea ice cover in these upstream regions may have negative consequences in the future for E. triacantha around the northern Antarctic Peninsula if they do rely on E. superba larvae as a primary prey item during winter.

The projected future warming around the Antarctic Peninsula may have substantial bottom-up effects on zooplankton populations. While some species have been well studied and their responses to environmental change can be reasonably predicted, others have not been studied enough to ascertain how their populations may change in response to changes in their habitat and food sources. Species with higher thermal tolerances or with broader distributions and diets (i.e., T. macrura) may fare better than species that are stenothermic or that consume a more limited diet (i.e., E. crystallorophias, E. frigida, and E. superba) (Jonhston et al. 2022). The projected increase in the frequency of ENSO-positive events may benefit the adult stages of all euphausiids around the northern Antarctic Peninsula except E. triacantha, which may be negatively impacted if E. superba larvae become less available in E. triacantha habitat in the future. Future studies should target poorly-understood species such as E. triacantha to ascertain how climate change will shape the future of the Antarctic pelagic ecosystem.

Acknowledgments

We thank the crew and the scientific support staff of the U.S. National Science Foundation vessel RVIB Nathaniel B. Palmer, as well as all of the technicians over our five winter surveys for their hard work, enthusiasm, and dedication while collecting and processing samples at sea. We especially thank Anthony Cossio, Kim Dietrich, Ryan Driscoll, and Rachel Pound. We would also like to thank Drs. Douglas Krause and Jefferson Hinke for helpful feedback and advice during manuscript preparation.

Author Contributions

JW collected samples, conducted laboratory analyses, analyzed data, and wrote the manuscript. CR assisted in statistical analyses and provided feedback. All authors read and approved the manuscript.

The authors have no financial or proprietary interests in any material discussed in this article.

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No competing interests reported.

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published 06 Apr, 2023

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Editorial decision: Major revision
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You are reading this latest preprint version

Extreme ENSO conditions have contrasting effects on Antarctic euphausiid body condition during winter

Status:

Journal Publication

Version 1

Abstract

Figures

Introduction

Materials And Methods

Survey area and general survey design

At-sea sampling

Stable isotope analysis

Lipid analysis

Data analysis

Results

Environmental differences between years

ENSO indices between years

Water column properties along the EI transect and the Bransfield Strait

Stable isotopes

Dietary carbon sources (δ¹³C)

Trophic position (δ¹⁵N)

Body condition (lipid content)

Discussion

Annual differences in environmental conditions and the biological community

Annual differences in source carbon

Annual differences in trophic position

Annual differences in body condition

Implications

Conclusions

Declarations

References

Additional Declarations

Status:

Journal Publication

Version 1

Extreme ENSO conditions have contrasting effects on Antarctic euphausiid body condition during winter

Status:

Journal Publication

Version 1

Abstract

Figures

Introduction

Materials And Methods

Survey area and general survey design

At-sea sampling

Stable isotope analysis

Lipid analysis

Data analysis

Results

Environmental differences between years

ENSO indices between years

Water column properties along the EI transect and the Bransfield Strait

Stable isotopes

Dietary carbon sources (δ13C)

Trophic position (δ15N)

Body condition (lipid content)

Discussion

Annual differences in environmental conditions and the biological community

Annual differences in source carbon

Annual differences in trophic position

Annual differences in body condition

Implications

Conclusions

Declarations

References

Additional Declarations

Status:

Journal Publication

Version 1

Dietary carbon sources (δ¹³C)

Trophic position (δ¹⁵N)