Zooplankton communities in the Drake Passage through environmental boundaries: a snapshot of 2010, early spring

Hydrological setting

Distinct gradients of both temperature and salinity were detected along the transect between the stations 2275 and 2272 and north from the station 2263, where the SAF and the PF were located, respectively (Fig. 2, see also Tarakanov & Gritsenko, 2018). A steeper bathymetric gradient of both temperature and salinity was observed at three southern stations (2259, 2261 and 2263, Fig. 2). Station 2268 differed from the neighboring stations by lower salinity in the upper layer and by lower temperature in the ∼100–450 m depth range.

Integral community characteristics

A total of 60 zooplankton taxa (including 31 taxa of Copepoda) were recorded at 13 stations. Abundances and wet biomass values in samples varied from 6.6 ind m⁻³ and 0.75 mg m⁻³ (station 2271, the layer 296–1,000 m) to 4239 ind m⁻³ (station 2263, layer 0–50 m) and 1,883 mg m⁻³ (station 2270, layer 0–55 m). The values per station in the upper ∼300 m varied from 640 ind m⁻³ (station 2266) and 13.65 mg m⁻³ (station 2275) to 2,668 ind m⁻³ (station 2263) and 330 mg m⁻³ (station 2270). Prominent biomass peak was observed at station 2270 owing to large specimens of krill (Thysanoessa sp.) and fish larvae caught at in the layer 0–55 m (see Supplemental Information). After the krill and fish biomass was removed, the biomass trend became similar to the abundance trend with maximum values observed in the vicinity of the PF (Fig. 3).

The diversity values including both ES (100) and Shannon–Wiener indexes demonstrated clear decrease at station 2266 and near the PF zone (Fig. 3).

The most abundant taxa were Oithona sp. copepodites (up to 43% of total abundance) followed by ova of unidentified invertebrates, various stages of Ctenocalanus sp. and Clausocalanus sp., young unidentified copepodites of Copepoda, Appendicularia, Radiolaria, and Foraminifera. Ten most abundant taxa represented 93% of the total abundance and biomass (Table 3, Fig. 4). Proportions of the main dominant taxa at each station are shown in Fig. 4.

Analysis of samples (Analysis 1, water layers approach)

Cluster analysis of all samples revealed several distinct clusters corresponded to various water layers. Within the dendrogram based on quantitative square-root transformed data, four clusters named Upper, Middle, Lower and Bathyal were revealed (Fig. 5). A single sample (station 2266, the layer 55–200 m, named 2266 Middle) was different from other stations (Fig. 5A) due to the absence of Ctenocalanus sp. and several other less common taxa (Supplemental Information). Clusters were divided by the similarity value of 57. In case of quantitative presence/absence data, the clusters were similar, with additional one named Upper South (Fig. 5B). Community composition was significantly different among all stations, SIMPROF-analysis demonstrated π-values >5.3 (with the mean p-value 0.01); sample statistic was not reliable in case of comparisons with 2266 Middle cluster due to a single station in that cluster (Table 4). Vertical distribution of the revealed clusters along the transect is shown in Fig. 6.

Results obtained from square-root transformed data and from qualitative data were similar with the exception of three southern stations, located south from the PF, where the upper layers formed a separate cluster (Fig. 6). The 2266 Middle layer samples were not associated with any visible hydrological gradients (Figs. 3 and 6). The northern-most stations (2275 and 2272), and stations located north off PF (2265 and 2264) consisted of only two clusters (Upper and Lower).

Overall, the depth factor influenced species composition more significant than the latitude and the position in relation to hydrological fronts (Fig. 6). Particularly, mean Bray-Curtis similarity within each station was 39.68 ± 17.17 SD, whereas the similarity within each water layer was 66.99 ± 7.55 (in case of square-root transformed data). At the same time, certain latitudinal structure remained within some of the clusters, e.g., the subcluster of three stations south from PF (2259, 2261 and 2263) is clearly visible within Upper, Middle and Lower groups (Fig. 5A).

Analysis of stations (Analysis 2, horizontal gradient approach)

After combining the samples within the upper 300 m, the depth factor was removed from the analysis (Fig. 7). Both square-root transformed and quantitative data showed that four southernmost stations formed one cluster (South), while most of other stations formed another cluster (North). In addition, the square-root transformed data demonstrated a third cluster (stations 2267 and 2268). The quantitative data demonstrated two more clusters, each consisting of a single station: the northernmost station 2275, (Subtropic) and the station 2268 (Fig. 7). Clusters were divided based on Bray-Curtis similarity levels of 76% and 83% for the square-root-transformed and for the presence-absence data, respectively. Thus, the plankton assemblages within the upper 300-m layer showed dependence on hydrological fronts position, especially when the presence/absence data were analyzed.

Comparison of zooplankton communities with environmental characteristics

Distinctive relation was found between the depth and total zooplankton abundances (Table 5). Abundances of certain taxa, including Metridia curticauda, Lucicutia sp. and Gaetanus sp. increased with depth, while abundances of pteropods, polychaetes, nauplii, Calanus simillimus and copepodites of Oithona sp. decreased with depth. Significant correlations, both positive and negative, were found between the chlorophyll concentrations and the abundances of several copepod species, larvae, Appendicularia and Tomopteris sp. (Table 5). The highest correlation values were observed when we used the chlorophyll data calculated for October for the entire upper 300-m layer. Integral community characteristics did not show any reliable correlation with chlorophyll except the total biomass, which was positive but not reliable (p = 0.087). A single taxon showed positive correlation with latitude (Clausocalanus brevipes) (Table 5). In addition, a clear linear dependence of Bray-Curtis similarity level on distance between the stations was observed (Fig. 8). The values of Pearson correlation were small (R-values −0.29 for square-root transformed abundance data and −0.40 for presence-absence data), but reliable (p-values 0.0094 and 0.0003, respectively). Despite the difference in mean similarity between the presence/absence and square-root-transformed abundance data, the linear trends of both sets demonstrated the same angles (Fig. 8).

We provided the SIMPER analysis between the station groups divided by the SAF and the PF (Table 6). Taxa responsible for most taxonomical dissimilarity between these boundaries were Oithona sp., Ctenocalanus/Clausocalanus copepodites, Oncaea sp. Ctenocalanus sp. and Oithona frigida. These taxa contributed >90% to the total dissimilarity between the stations.

The most abundant taxa (including Oithona sp., Ctenocalanus sp., Appendicularia, Foraminifera, Radiolaria, for density values see Supplemental Information) were concentrated in the center of the CCA plot, demonstrating no significant deviations to either of environmental axes (Fig. 9A). Several less abundant species were located at plot margins, including three taxa found in the deepest layers (Lucicutia sp., Mormonilla sp., Metridia curticauda) and taxa found only at northern stations (e.g., Rhincalanus nasutus, Salpae). Several taxa depended on Chlorophyll axis (Tomopteris sp., Calanus simillimus) (Fig. 9A). Samples tended to arrange along the Depth axis rather than along the Latitude axis (Fig. 9B). Overall, the depth gradient was more significant than the latitude and other gradients (Figs. 9A and 9B).

Zooplankton community abundance, biomass and diversity

Zooplankton abundance, biomass and biodiversity obtained in this study from the Drake Passage are in agreement with those reported in the previous investigations (Table 7) (Żmijevska, 1987; Ward et al., 2007; Mackey et al., 2012; Hosie et al., 2014). In particular, similar abundances were previously reported for eastern areas of Drake Passage and deep regions around South Georgia (294–2,445 ind m⁻³) by Ward et al. (2007). Our data do not allow us to reveal any temporal changes in terms of integral community characteristics within the Drake Passage. In a few studies zooplankton abundances were reported to be lower, which can be explained either by sampling season (the abundance in winter months in upper water layers is lower than during spring-summer) or by different sampling methods (e.g., video recorders may underestimate the abundance) (Atkinson & Peck, 1988; Hosie et al., 2014). Stupnikova & Vereshchaka (2013) reported the biomass range from 1.2 to 65.7 mg ww m⁻³ with the highest values observed in the PF zone. In our samples biomass values were higher and varied from 13.7 to 330 mg/m³ (Fig. 3). However, the highest values were recorded at two stations, owing to dominance of euphausiids and fishes. After we removed these taxa from the dataset, the biomass values were reduced to 58.4 mg/m³, similar to the values published by Stupnikova & Vereshchaka (2013). Stupnikova et al. (2018) also reported relatively low diversity in the Drake Passage epipelagic zone compared to other areas of Southern Ocean. Shallow shelf regions around the Drake Passage, not sampled in our study, are characterized by higher abundance and biomass values comparing to deep-sea areas (Ward et al., 2007; Mackey et al., 2012).

Biodiversity values including the Hurlbert rarefaction and Shannon–Wiener index decreased around the Polar Front in our survey, although taxonomical richness remained nearly constant (Fig. 3). Theoretically, one could expect certain increase of the biodiversity within the PF owing to polar and subpolar faunal mixing. Higher biodiversity values around the PF were previously reported from the Drake Passage (Stupnikova & Vereshchaka, 2013) and other areas of Southern Ocean (Hunt & Hosie, 2005). However, increased gradients within the PF seem to be unfavorable for many taxa and cause changes in zooplankton communities, which may be reflected in biodiversity decrease. The decrease of biodiversity in our survey could be also explained by the dominance of Oithona sp. copepodites contributing almost 45% to the total abundance at the PF stations (Supplemental Information).

Taxonomical structure of zooplankton communities along the transect

A set of dominant taxa was nearly constant in our dataset with Oithona sp. copepodites prevailing at every station. Together with planktonic ova, these taxa contributed more than 55% of the total abundance (see Table 3). The main differences between the clusters were in proportions of Oithona sp. and several other taxa abundances (see Table 6). Most of the previously published investigations do not report this level of dominance, which can be explained by different sampling season and larger mesh size of the nets (Mackintosh, 1937; Atkinson & Peck, 1988; Pakhomov & McQuaid, 1996; Takahashi et al., 2010; Mackey et al., 2012). The dominance of Oithona sp. (identified as Oithona similis) was previously reported by Żmijevska (1987) and Stupnikova et al. (2018), probably due to similar sampling season. The Oithona similis dynamics was clearly demonstrated by Hosie et al. (2014), with a rapid increase of abundance in November and following decrease in January. Significant contribution of Ova and copepodites is a clear sign of the spring (an indication of increasing production). Apart from seasonal changes some long-term changes leading to the dominance of small copepod species (like Oithona spp.) were reported by Takahashi et al. (2010) in the Drake Passage. The authors compared their recent data with the results of Discovery Expedition described by Hardy (1936). However, the changes can be also explained by the different mesh size of the plankton nets (Takahashi et al., 2010).

Other taxa in our samples represented well known species mentioned in many investigations. No significant changes in species structure were found in this study compared to the previous investigations (Mackintosh, 1937; Voronina, 1984; Żmijevska, 1987; Pakhomov & McQuaid, 1996; Stupnikova & Vereshchaka, 2013). However, a lot of taxa were identified only to a family or class level, so we have no information on possible changes in species abundances within the major taxonomic groups (Supplemental Information).

We assumed the existence of two main boundaries along the transect represented by the SAF and the PF delimiting the zooplankton communities. Hosie et al. (2014) proposed a model predicting the spatial distribution of zooplankton communities in the Southern Ocean for each month. According to their data, the PF doesn’t act as a boundary for the surface mesoplankton communities. Instead, according to the model published, a significant boundary in the vicinity of the SAF may be expected. Our data suggest that there are two clear boundaries across the Drake Passage: first located at the SAF and the second (and more strong) at the PF. These boundaries are most conspicuous when clustering the upper 300 m layers combined (Fig. 7), but they are also visible within each of the revealed samples clusters including Upper, Middle and Lower clusters (Fig. 5). Species responsible for the SAF-boundary are the same in our samples and in Hosie et al. (2014), including Foraminifera and Clausocalanus brevipes which are more abundant south from the SAF, and Calanoides acutus, Calanus propinquus, C. simillimus and Ctenocalanus sp. which are more abundant north from the SAF (Table 6, Supplemental Information).

Dependence of plankton assemblages structure on vertical (depth) and horizontal (frontal zones) gradients along the transect is very representational (Fig. 6). Correlation of the similarity index and latitudinal distance between the stations indicates a presence of clear latitudinal gradient (Fig. 8). However, in this study the communities are more dependent on depth than on latitude or frontal zones. According to the primary data published by Żmijevska (1987) the geographical position of stations and the proximity of coast play more important role than depth within the upper 500 m. In other areas (e.g., south off Africa) the latitude gradient is far more significant than depth (Vereshchaka et al., in print). However, when only qualitative presence/absence data are considered (and all the quantitative, e.g., abundance data, excluded), epipelagic layer south of the PF formed a separate additional cluster (Fig. 6B). Therefore, the qualitative taxonomical composition is affected by both depth and frontal zones (the former is dominant), while the quantitative structure of the communities is mainly a function of depth, i.e., of trophic gradient from surface to bottom.

The influence of temperature, salinity, depth and chlorophyll

Zooplankton in the Antarctic is known to respond to various environmental factors, including temperature, water acidification, depth, thickness of sea ice etc. (reviewed by Constable et al., 2014). The most significant factors affecting macro- and mesozooplankton distribution in the Southern Ocean are currents and fronts (Pakhomov & McQuaid, 1996). In our study this influence was less significant, partly due to peculiarity of the frontal structure in the Drake Passage (Stupnikova et al., 2018). As a result, depth was the major environmental factor influencing the spatial distribution of zooplankton, followed by salinity and temperature (see previous subsection).

In our samples notable was station 2268 creating a separate cluster (Fig. 7), probably due to the lower salinity and temperature values (Fig. 2). According to hydrological profiles this station may represent remains of a gyre or a meander. These structures frequently formed in the Drake Passage consist of waters different by salinity and/or temperature from the surrounding water masses (Olbers et al., 2004).

In contrast to previously published data (Vereshchaka et al., 2016; Vereshchaka et al., 2017; Vereshchaka, Lunina & Sutton, 2019), no significant correlations were found between total plankton biomass (in either of layers) and surface chlorophyll concentration (Tables 2 and 5). The best R-values were obtained for only a few taxa when analyzing the chlorophyll data for October, before the local spring bloom (see Table 2, Moore & Abbott, 2002; Demidov, Mosharov & Gagarin, 2012). The satellite chlorophyll estimation is known to be an inaccurate method comparing to direct measuring due to the ignorance of sub-surface chlorophyll and certain imperfection of algorithms. These facts may often lead to underestimations of the chlorophyll values in some areas (Garcia, Garcia & McClain, 2005; Zeng, Xu & Fischer, 2016; Brewin et al., 2017). However, despite the disadvantages of satellite chlorophyll data, our results may be a consequence of seasonal cycles of dominant zooplankton species in the Southern Ocean. Most species migrate from deep waters to the surface during different periods of biological spring and concentrate in the upper 100–200 m layer by December (Hardy & Gunther, 1935; Mackintosh, 1937; Voronina, 1984). It is likely that during the time of our survey a significant part of zooplankton remained below the sampling layers and the actual biomass was underestimated.