Analysis of microzooplanktonic populations in Terra Nova polynya and comparison with similar polar systems

Microzooplankton (MCZ) results from all heterotrophic organisms (protozoa and early larval forms of metazoans) between 20 and 200 µm in size. From a trophic point of view, it constitutes a key link in the marine trophic network as it is able to prey on organisms smaller than the typical prey of mesozooplankton and, in turn, is actively preyed upon by the latter, thus acting as a true trophic intermediary between bacteria, nanoplankton and mesozooplankton. The MCZ consists of ciliates (aloricates and loricates), heterotrophic dinoflagellates, other protozoa (foraminifera, radiolarians) and micrometazoa (early larval stages). Analysis of data from all previous Antarctic campaigns in the study area showed a change in the composition of the MCZ with a marked decrease in the tintinnid fraction. In particular, integrated values over the first 100 m showed a shift from a maximum of 270 ind.L-1 in 1988 to an order of magnitude lower in recent campaigns. A link between the change in the composition of the microzooplanktonic population and ongoing climate change was hypothesized. The purpose of the project was to analyze the trend of microzooplanktonic populations in the BTN polynya in order to implement the data already in our possession from seven oceanographic cruises (1988, 1990, 1994/95, 1997/98, 2001, 2003, 2006) carried out under PNRA.

The objectives of the research can be summarized in four main points:

1. To determine the abundance, composition and biomass of the MCZ of the polynya of Baia Terra Nova.

2. To compare the data obtained with the historical series already in our possession in relation to ecosystem responses to climate change.

3. To study the trophic characteristics (mixotrophy vs autotrophy) of the main components (dinoflagellates, ciliates) in order to obtain a better characterization of the marine trophic network.

4. Compare the data obtained with those of other Arctic areas in order to determine variability at the regional scale.

As part of the 2009/A1.08 project, 61 samples were analyzed for qualitative-quantitative analyses of microzooplanktonic populations and 7 samples were analyzed for in vivo population analyses, with emphasis on heterotrophic dinoflagellates. During the 2011/12 campaign, the closure of the pack in front of the Italian Base Mario Zucchelli forced the operational unit to sample from the ice at two stations (Tergeste and T10) located in Tethys Bay. The two stations were opened thanks to cores drilled into the pack. The diameter of the holes was found to be about 1 meter with a thickness of about 2 meters. Thus, of the 61 samples, 28 were taken under the ice at Tergeste and T10 stations and 33 in the marine area in front of Mario Zucchelli Station (ASPA Protected Area No. 161) (Fig. 1). Samples were taken both within and in areas adjacent to the ASPA (carried out by other operational units). Five liters of water were taken for each sample using a Niskin bottle, both under ice and offshore.

Seven samples for in vivo determination were collected, using an Apstein screen, under ice only and analyzed directly at the Italian Base Mario Zucchelli. Samples taken with the plankton screen were observed under an epifluorescence microscope for the detection of the presence of chlorophyll in dinoflagellates. A Leica microscope with I3 filter series (BP 450-490 exciter filter, RKP510 chromatic beam splitter, LP 515 barrier filter) equipped with camera was used. For each sample taken for qualitative-quantitative analysis of microzooplanktonic populations, 5 l of seawater was collected. They were concentrated in the laboratory with a 10-μm mesh and reduced to 250 mL, the latter of which was fixed with a CaCO3-buffered formaldehyde solution (final concentration 4%). Sub-samples of various aliquots (10-100 ml) were sedimented and then examined on return to Italy by sedimentation chambers with a Leica DMI 3000B inverted microscope at a magnification of 200X according to the method of Utermöhl (1958). The entire surface of the sedimentation chambers was examined. For each taxa, the biomass was estimated from the measurements of each organism made using a micrometer inserted in the eyepiece. The biovolumes thus obtained were multiplied by conversion factors and the biomass, expressed in µgC L-1, was extrapolated.

Qualitative analyses carried out on in vivo samples at the Mario Zucchelli base showed the presence of tintinnid ciliates belonging to the genera Laackmanniella and Cymatocylis with the species L. naviculaefera and C. drygalskii and heterotrophic dinoflagellates belonging mainly to the genera Protoperidinium and Gyrodinium. Epifluorescence microscope analysis confirmed the absence of chlorophyll in several species of dinoflagellates in the samples. In particular, the genus Gyrodinium with the species Gyrodinium lachryma among the thecated dinoflagellates and the genus Protoperidinium, with the species P. incertum, P. antarcticum, P. pseudoantarcticum, P. applanatum and P. defectum, among the thecated dinoflagellates, were consistently found to be lacking chlorophyll. The microzooplanktonic population, in all the samples examined, varied from a minimum of 8 ind.L-1 (St. T10.1, 125 m, 12/15/2011) to a maximum of 7523 ind.L-1 (St. SMN, 13 m, 01/28/2011).

The quantitative analysis carried out at the OGS, showed the dominance of heterotrophic dinoflagellates with the maximum value of 6855 ind.L-1 at the intermediate elevation of the SMN station on 01/28/2011. In general, dinoflagellates also reached high values at the other stations, at the surface and intermediate elevations, while the lowest values were always found at the bottom elevations, with an absolute minimum of 2 ind.L-1 at 190 m at station TER.4 on 12/27/2011. Aloricated ciliates were the second most abundant group, with values varying between 0 and 369 ind.L-1 (St. SMN, surface, 01/28/2011). Tintinnids presented values ranging from 0 to 320 ind.L-1 ( St. SMN, 13 m, 28/01/2011) while micrometazoan larvae were always less than 100 ind.L-1.

Qualitative analyses showed the presence of heterotrophic dinoflagellates belonging mainly to the genera Protoperidinium and Gyrodinium. Among the dinoflagellates always well represented Gyrodinium lachryma, Protoperidinium incertum, P. applanatum and P. defectum. Particularly noteworthy is the high value of P. defectum in the st. SMN where, with 4600 ind.L-1, it accounted for more than half of the population of heterotrophic dinoflagellates. Among the aloricate ciliates present were the genus Litonotus and Gymnozoum with the species G. sympagicum and G. viviparum. Tintinnids were represented by the genera Cymatocylis, Codonellopsis, Coxiella laackmanniella and Salpingella. The most prevalent species were C. drygalskii and L. naviculaefera. Micrometazoan larvae were not found to be very abundant, only Limacina helicina (pteropod) and Copepod naupli were found to be present at almost all altitudes. Foraminifera were not found, and among Heliozoa only Sticholonche zanclea was reported. Biomass varied from 47 x 103 pgC L-1(T10.1, 125 m) to 84 x 106 pgC L-1(TER11, 20 m). In particular, the latter particularly high values in terms of carbon can be attributed to the presence of the pteropod Limacina helicina which, with its size, influenced the total biomass value.

With particular reference to the samplings taken under the ice, particularly low values were always noted, both in terms of abundance and biomass. The microzooplankton population varied from a minimum of 8 ind.L-1 (T10.1, 125 m on 12/15/11) to a maximum of 774 ind.L-1 (TER.5, 50 m on 2/01/12). Generally, maxima were found at the surface on the first sampling days (16/12, 18/12 and 22/12) and then shifted to 50 m on subsequent samplings (27/12, 2/01 and 6/01). Quantitative analysis showed the dominance of heterotrophic dinoflagellates with the maximum value of 592 ind.L-1 (TER.2, surface of 18/12/2011 and TER.5, intermediate of 2/1/2012). The minimum values were always found at the bottom elevations (190 m). Aloricate ciliates were the second most abundant group, with values ranging between 0 and 79 ind.L-1 (TER.5, 100 m). Tintinnids and micrometazoan larvae were low in abundance with the maximum value of 94 and 20 ind.L-1, respectively. Qualitative analysis indicated the presence of tintinnid ciliates belonging to the genera Laackmanniella and Cymatocylis with the species L. naviculaefera and C. drygalskii and heterotrophic dinoflagellates belonging mainly to the genera Protoperidinium and Gyrodinium. Among dinoflagellates always well represented Gyrodinium lachryma, Protoperidinium incertum, P. antarcticum, P. applanatum and P. defectum. Micrometazoan larvae were not found to be very abundant, with Limacina helicina (pteropod) and Copepod naupli present mainly at intermediate elevations, while Foraminifera were not found. Among the aloricate ciliates present is the genus Gymnozoum with the species G. sympagicum and G. viviparum. Some of the identified species are considered sympagic species, and comparison with material from different environments, such as the Weddell Sea, was used for their correct classification. At the below-ice stations, Tergeste and T10, biomass values varied from a minimum of 47 x 103 pgC L-1 (T10.1, 125 m) to a maximum of 5.6 x 106 pgC L-1 (TER.5, 50 m). At these two stations, the biomass showed particularly low values, generally less than 1 µgC L-1, due to the fact that the microzooplanktonic stand, consisting mainly of small heterotrophic dinoflagellates, did not yet have tintinnids and micrometazoan larvae.

In light of the results obtained, a comparison could be made between the microzooplanktonic population present under the ice (December 2012), in newly opened areas (January 2012), and in ice-free waters sampled during the 2011 campaign. During the period considered, the microzooplanktonic community showed a seasonal evolution, both in terms of abundance and biodiversity. In the early austral summer, under the ice, the population showed very low values along the entire column. At stations newly opened by the ice, abundances reached values more except at bottom elevations where they never exceeded 150 ind.L-1. Abundance and the number of taxa increased in the stations that had been free of ice for the longest time, reaching even at the bottom values up to 870 ind.L-1. The composition of the below-ice stand was different from that of the open sea, both in terms of abundance and diversity with the dominance of heterotrophic dinoflagellates and aloricate ciliates. The presence of ice affected the entire column, reducing its production, particularly at the deep elevations. Tintinnids were absent under the ice and their abundance increased as the season continued, showing the highest values at stations sampled in late January. Tintinnids presented the highest values in the intermediate waters (MIW) while, in the bottom samples, characterized by the presence of ISW, the abundance always remained very low.

The conducted study emphasized how microzooplankton is influenced by environmental variables and how the community largely depends on the sampling period. In particular, ice opening and elapsed time seems to be the most important factor in the evolution of the microzooplankton population.

Monti M., Zoccarato L., Fonda Umani S. (2016) Microzooplankton composition under the sea ice and in the open waters in Terra Nova Bay (Antarctica). Polar Biology. http://doi.org/10.1007/s00300-016-2016-9.