Figure 2a shows total length-mass relationships of solitary and aggregate salps, as well as both forms combined used in our experiments performed during two expeditions, while mass-specific respiration rates as a function of the salp experimental density are presented in Fig. 2b. For comparative purposes, Fig. 2b also includes previously published relationships. The wide range of respirometer volumes and salp sizes used in our experiments allowed obtaining the values ranging from 2.0 to 90.4 gWW·l−1. The data from Pavlova (1975) included two species of salps from the Mediterranean Sea with experiments conducted at 20°C (and adjusted to 3°C) with Cw ranging from 0.017 to 9 gWW·l−1 (Fig. 2b). Finally, recalculated data from Ikeda (1974) summarized the relationship obtained for six tunicate species (five species of salps and one species of pyrosomes) in the tropical Pacific with Cw varying between 0.7 and 20 gWW·l−1. It appears that mass-specific respiration rates of subtropical and tropical tunicates are in good agreement with our data for aggregate salps. The exponents are –0.84 for solitary and –0.91 for aggregate salps (Fig. 2b). The exponents for the correlations of the mass-specific respiration rates and individual body mass are –0.09 and –0.06, respectively (Fig. 3b), indicating that mass-specific respiration rates of salps are almost independent of the body mass. As shown earlier, the dependence of the mass-specific rates of metabolism on the salp unit mass concentration has proven to be stronger than the traditional correlation with the individual body mass (Minkina and Samyshev 2004). It is noteworthy that the mass-specific respiration rates of S. thompsoni aggregates had a weaker relationship with the salp unit mass in comparison to solitary forms.
Table 2
Correlations for the rate (R) and specific rate (R/W) of respiration of salps and some tunicates and their wet weight (W), according to our own and literature data recalculated for a temperature of 3°C
Source | Species | Temp., оС | Numb. meas. | Wet weight range W, g | R, µg O2 / (ind·h), R/W, µg O2 / (g·h) | Coef. of correlation r2 |
Ikeda (1974) five species of tunicates | Thalia democratica Salpa fusiformis Pegea confederata (solitaries) | 17.3 17.3 25.7 | 3 2 3 | 0.1-5.86 | R = 5.23 W 0.68 R0 = 5.94 W 0.93 R/W = 5.23 W −0.32 R0/W =5.94 W−0.071 | 0.972 |
0.964 |
0.883 |
0.137 |
S. fusiformis Iasis zonaria | 17.3 27 | 4 1 | 0.1-4.53 | R = 6.71 W 0.46 R0 = 0.28 W 1.00 | 0.733 0.956 |
Pyrosoma vericilatum | 25.7 | 2 | | R/W = 6.71 W−0.54 | 0.790 |
(aggregate) | | | | R0/W =5.54 W−0.0025 | 0.0001 |
Pavlova (1975) | Salpa democratica, | 20 | 20 | 0.005- | R = 6.95 W 0.39 | 0.658 |
| Salpa maxima | | | 0.33 | R0 = 6.29 W 0.96 | 0.891 |
| | | | | R/W = 6.95W −0.62 | 0.828 |
| | | | | R0/W =7.46W 0.25 | 0.254 |
Abolmasova (1978) | S. maxima S. democratica | 15.2-15.6 | 17 | 0.011-0.1 | R=10.81 W 0.975 | - |
Ikeda and Mitchell (1982) | S. thompsoni | -1.1 | 12 | 2.25-11 | R=4.4-12.4 | - |
| S. thompsoni, | -1,1 | 12 | average 5.7 | R=2.29 W 0.74 | 0.972 |
| Ihlea racovitzei | | 4 | 0.4-11 | | |
| (solitaries, two aggregate specimens) | | | average 1.5 | | |
Cetta et al. (1986) | S. fusiformis, | 16.5 | 15 | 0.5-7.2 | R=6.85 W 0.68 | 0.89 |
| aggregate | | | | | |
| S. fusiformis | 16.5 | 10 | 2.1-20.8 | R=14.4 W 1.15 | 0.95 |
| solitary | | | | | |
| S.maxima | 24.5 | 16 | 1.3-14.2 | R=14,63 W 1.22 | 0.88 |
| aggregate, the specimens were with the filled intestines | | | | | |
| S. maxima, | 24.5 | 9 | 0.1-5.9 | R=6.43 W 1.04 | 0.87 |
| aggregate | | | | | |
Madin and Purcell (1992) | Cyclosalpa bakeri | 11 | 27 | 0.01–0.1 | R=13.3 W 1.16 | 0.92 |
Igushi and Ikeda (2004) | S. thompsoni, | 1.0-1.7 | 6 | 1.45-63.7 | R/W=1.132 W −0.15 | 0.99 |
| solitary | Av. 1.3 | | | | |
| S. thompsoni, | 1.0-1.7 | 25 | 0.35-27.65 | R/W=0.89 W −0.03 | 0.94 |
| aggregate | Av. 1.3 | | | | |
Our data | S. thompsoni, | 3 | 41 | 0.4-17.4 | R = 21.96 W 0.91 | 0.36 |
| solitary | | | | R0 = 49.07 W 1.04 | 0.57 |
| | | | | R/W = 22.21W −0.09 | 0.006 |
| | | | | R0/W = 49.07 W 0.04 | 0.0016 |
| S. thompsoni, | 3 | 13 | 0.28-6.24 | R = 30.72 W 0.75 | 0.40 |
| colonial | | | | R0 = 25.77 W 1.07 | 0.78 |
| | | | | R/W = 30.72 W −0.25 | 0.065 |
| | | | | R0/W = 25.77 W 0.07 | 0.014 |
For meaningful comparisons, only mass-specific respiration rates normalized by the constant concentration were used. For all mass-specific respiration rates, the basic concentration of gWW·l−1 was employed as given in the formula (2). The specific respiration rate results against salps' wet mass are shown in Fig. 3b and presented in Table 1. The table summarizes the respiration rate regressions as a function of the individual body mass presented in comparable units and adjusted for temperature differences in experiments. The correlation coefficients show that the data scattering (Fig. 3b) significantly decreased as compared to that in Fig. 3a. A similar tendency can be observed in the results of calculations using the live mass concentration according to Ikeda (1974) and Pavlova (1975) (Table 2 and Fig. 3b). It appears that temperature and mass adjusted values from tropics to polar regions are broadly comparable. However, the values for the tropical Pacific tunicates, according to Ikeda (1974), were slightly lower. The data by Ikeda and Mitchell (1982) for S. thompsoni obtained in the temperature range–0.5 to +1.8°C, were also below values obtained in our study (Fig. 3a, Table 2). This discrepancy seems to be due to both the interspecific differences and the possible inhibition of tunicate activity in their habitat before catching.
After correcting the mass-specific respiration rates of Antarctic salps for the experimental concentration and individual body mass of specimens, it became possible to delineate variability associated with the time of the day. This allowed us, for the first time, to assess the circadian rhythm of the mass-specific respiration rates of both solitary and aggregate forms of S. thompsoni (Fig. 4, Table 3). Both forms showed similar diel respiration patterns, but solitary forms had nearly double mass-specific respiration rates compared to aggregate forms (Fig. 4). The lowest respiration rates in both life forms of S. thompsoni were observed in the morning hours 4:00-5:00. The highest or elevated values in oozoid's respiration were observed in the evening (18:00-22:00), at night (23:00-24:00) and midday (11:00-15:00), while the aggregate's respiration picked in the evening (20:00) and before the noon (11:00). The average metabolic rates calculated for the salp density in respirometers equal to 3 gWW.l−1, irrespective of the individual body mass, were 79.5 and 41.5 µg O2·g−1·h−1 in oozoids and blastozoids, respectively (Table 3). These values are taken as the statistical "norms" (or as 100%) for the salp forms in our further calculations.
Table 3
Diurnal variability of the specific energy metabolism rate (RT/W, µg O2·g−1 WW·h−1) in the Antarctic salp Salpa thompsoni during March-April 1998 and March 2002. The temperature in the experiments is 3°C and C0=3 g−1 wet weight·l−1 (N = sample size, σ = standard deviation, tα = 90% confidence interval)
Time of day | Solitary salps | Aggregate salps |
RT/Wav | N | σ | t α | RT/Wav. | N | σ | t α |
0:00 | 132.4 | 22 | 158.4 | 55.5 | 38.5 | 6 | 39.7 | 26.6 |
1:00 | 58.6 | 26 | 52.3 | 16.9 | 34.5 | 6 | 34.1 | 22.9 |
2:00 | 64.2 | 21 | 110.7 | 39.7 | 51.7 | 7 | 56.9 | 35.4 |
3:00 | 75.2 | 19 | 89.4 | 33.7 | 45.4 | 7 | 39.9 | 24.8 |
4:00 | 37.7 | 17 | 35.7 | 14.2 | 27.4 | 7 | 24.5 | 13.4 |
5:00 | 33.9 | 17 | 32.8 | 13.1 | 22.8 | 7 | 19.8 | 12.3 |
6:00 | 55.6 | 21 | 64.3 | 23.1 | 18.9 | 7 | 17.5 | 10.9 |
7:00 | 50.6 | 18 | 57.7 | 22.4 | 21.4 | 7 | 16.7 | 10,4 |
8:00 | 62.9 | 19 | 52.6 | 19.8 | 25.4 | 7 | 19.3 | 12.0 |
9:00 | 43 | 20 | 41 | 15.1 | 19.8 | 5 | 19.7 | 14.5 |
10:00 | 39 | 13 | 24.5 | 11.2 | 38.0 | 3 | 60.5 | 57.4 |
11:00 | 87.8 | 7 | 137.9 | 85.7 | 88.2 | 7 | 89.5 | 55.7 |
12:00 | 52 | 8 | 39.3 | 22.9 | 29.2 | 8 | 27.5 | 16.0 |
13:00 | 104.7 | 19 | 104.2 | 39.3 | 58.0 | 8 | 42.8 | 24.9 |
14:00 | 91.1 | 21 | 93.9 | 33.7 | 43.3 | 6 | 31.5 | 21.2 |
15:00 | 88.5 | 18 | 93.6 | 36.3 | 39.6 | 8 | 38.4 | 22.3 |
16:00 | 61.6 | 25 | 77.4 | 25.5 | 32.3 | 9 | 24.9 | 13.7 |
17:00 | 73.4 | 29 | 91.9 | 28.1 | 33.0 | 10 | 36.0 | 18.7 |
18:00 | 150.5 | 24 | 148.2 | 49.8 | 52.8 | 5 | 32.0 | 23.5 |
19:00 | 107.1 | 24 | 108.6 | 36.5 | 26.2 | 4 | 18.4 | 15.1 |
20:00 | 68.8 | 19 | 56.1 | 21.2 | 96.4 | 7 | 78.3 | 48.7 |
21:00 | 125.5 | 12 | 166.9 | 79.2 | 65.0 | 6 | 110.3 | 74.1 |
22:00 | 106.6 | 21 | 181.7 | 65.2 | 65.1 | 8 | 73.6 | 42.8 |
23:00 | 136.5 | 23 | 190.4 | 65.3 | 23.5 | 6 | 18.2 | 12.2 |
Average daily values | 79.5 (“norm”) | 463 | 33.6 | 11.3 | 41.5 (“norm”) | 161 | 20.8 | 7.0 |
Based on the obtained data set (Table 1), we have constructed maps of the spatial variability in S. thompsoni energy metabolism (EM) near the South Orkney and Elephant Islands (Fig. 5, insert) and in the Bransfield Strait (Fig. 6, insert). In 1998, positive deviations of salp EMs (Table 1, Fig. 5f) were observed in the dynamically active area near Elephant Island. A fragment of the cyclonic meander of the Southern branch of the Antarctic Circumpolar Current (ACC), which contained the Weddell Sea waters, was registered in this area (for details see Lomakin and Samyshev 2004). The flow width was 20-25 miles, and the surface velocity reached 40-50 cm·s-1. In this area, there was the greatest abundance of salps ever recorded here, mostly oozoids with concentrations of up to 120 gWW·m−3 (Lomakin and Samyshev 2004) (Fig. 5d). The maximum specific rate of EM here was 2.8 times higher (with a deviation of 184%) as compared with the "statistical norm" in the southwestern part of the surveyed area. This area coincided with very low phytoplankton biomass (15-190 mg∙m−3) indicative of the active grazing of salps (Fig. 5e).
The water dynamics north of the South Orkney Islands was set by a wavy meander flowing around the islands with a powerful anticyclonic topographic gyre observed about 200 miles north of them. It was formed through the interaction of the Southern branch of ACС with the Peary Seamount, which suggests the quasi-stationary and topographic nature of this gyre (Lomakin and Samyshev 2004). The maximum salp concentrations (up to 32 gWW∙m−3) were observed in the central part of the warm topographic gyre directly above the Peary Seamount (Lomakin and Samyshev 2004). This was accompanied by the lowest phytoplankton concentrations (13.5 mg∙m−3) and minimum EM values (~ –25%) (Table 1, Fig. 4c). In the southeastern part of this area, where salp biomass was the lowest, the phytoplankton concentration reached 1200 mg∙m−3, and the EM rates were close to the "statistical norm" (–4%) (Fig. 5b).
Inhibition of the salp population, e.g. negative deviations of EM rates from the "statistical norm", was also observed in early autumn 2002 in the Bransfield Strait (Fig. 6). In the western part of the strait, there were sharp seabed troughs with a depth of up to 1000 m compared to the general average depth of about 200-300 m. This area is also characterized by the highly indented coastline and the presence of numerous islands (Artamonov et al. 2003). Such geography favors the stagnated eddy formation resulting in the long-term accumulation of salps potentially creating food shortages (Fig. 6a). In the center of the quasi-stationary gyre situated in the middle of the Bransfield Strait, the maximum salp concentrations reaching 2.89 gWW·m−3 of salps were observed. They decreased towards the periphery of the gyre to 1.42 mgWW∙m−3. Salp biomass strongly negatively correlated to the phytoplankton standing stock, 22.7 mg∙m−3 vs 788 mg∙m−3 in the center and outside the gyre respectively (Fig. 6b). Indeed, negative salp EM values (up to –70%) coincided with the center of the gyre, indicating the inhibition of salps' activity likely due to the food shortage. At the periphery of the gyre and beyond it, the salp performance appeared to be at the "statistical norm" (see inserts in Fig. 6a, b).
According to our calculations, the energy costs in the experiments at 3°C with the live mass concentration of 3 gWW∙l−1 in the whole range of sizes accounted for 26.0% and 13.6% of the body carbon content in solitary and aggregate salps, respectively. For S. fusiformis from the tropical Atlantic in the temperature range 13.5-19.5°C, the similar demands accounted for 21.3% and 9.7% of the body carbon in oozoids and blastozoids, respectively (Cetta et al. 1986). However, the daily energy expenditures in solitary S. cylindrica at 24°C in the same work was ~ 99%. High scatter in the results may be due to the species-specific energy costs linked to the minimum nutritional needs of salps. For example, for the Mediterranean S. fusiformis at 16°C, the daily food requirements averaged 107-117% of the body carbon content (Cetta et al. 1986). For comparison, the daily food needs of S. thompsoni calculated from the stomach pigment fluorescence accounted for 5-75% of their body carbon contents (Pakhomov et al. 2002; 2006).
Earlier we discussed possible mechanisms behind the effect of organisms' density on the specific respiration rates in aquatic organisms (Minkina and Pavlova 1995; Minkina 2007). It is known that a universal regulator of chemical reactions rates is the concentrations of reactants. The regulation of rates of biological processes through the concentration of biomaterial appears to be a manifestation of the same law (Khailov et al. 1999). When we assess the respiration intensity of salps at 3 oC at various salp concentrations (Fig. 2b and according to formula (2)) for solitaries with the respirometer salp densities 2.93-90.43 gWW.l−1 daily respiration rates would have accounted for 26.5-1.5% of their body carbon content. The same was true for the blastozooids: 1.97-14.17 gWW.l−1 and 19.9-3.2% carbon content accordingly. Currently, density effects of the metabolic rates for salps were not well studied although feeding rates of gelatinous invertebrates could be affected by the volume of, and thus the animal density in, the incubation container (Scolardi et al. 2006). Unlike salps and other marine invertebrates (e.g. Minkina and Pavlova 1995; Khailov et al. 1999), experiments with the Antarctic krill did not confirm the reduction in their respiration rates at increasing densities in a large (105 l) flow-through respirometer (Swadling et al. 2005). Nevertheless, it has been proposed that krill school density may impact school oxygen concentrations and thus krill respiration rates (Brierley and Cox 2010).
The lack of studies of the density effects may be due to the adoption of the physiological rules of larger animals (fish, mollusks, large crustaceans) for the zooplankton organisms. In small invertebrates, the basal metabolism covers the minimal energy needs and is measured using stationary and starved animals (Vinberg 1956). The basal metabolism can subsequently be used to assess minimal food requirements. The routine metabolism (often considered to be higher than the basal metabolism because organisms are not stationary) is generally measured using organisms that have restricted, due to the experimental setup, movements. While routine metabolism is often used as the total metabolism, the latter should include both basal and active metabolism that accounts for the organisms' active movement (Vinberg 1956). It appears that in the majority of experiments to estimate routine metabolism there are no regulations about the density of organisms in incubation chambers and it is chosen subjectively by the individual researchers. This leads to highly variable outcomes that allow building regressions between metabolic rates and experimental temperature likely leading to erroneous results if the density of organisms is not considered. The introduction of respirometers with polarographic sensors allowing to monitor continuously the incubation container oxygen concentrations (Samyshev 2002; Minkina and Pavlova 1995) helped to address the issue of handling stress, organism adaptation to the experimental conditions, and the animal behavior during the experiment (Samyshev et al. 1980), which is impossible to disentangle in the classical Winklers' end-point measurement method. For example, the respiration rate measurements of S. thompsoni at -1.9 – -2.0 oC in the Ikeda and Bruce (1986) experiments yielded very low (2.3-2.8% of body C) daily respiration demands. It is not clear if such low metabolic needs are driven by the very low experimental temperature (it is clear at the lowest range of this species tolerance, Foxton (1966)) or high organism density in the experimental containers, or both (Ikeda and Bruce 1986).