Effect of Food Composition and Temperature on in ...

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ration and clearance rate of medusa Aurelia aurita was tenfold and hundredfold higher when feeding on veligers of Bivalvia compared to small crustaceans.
ISSN 20751117, Russian Journal of Biological Invasions, 2014, Vol. 5, No. 1, pp. 49–55. © Pleiades Publishing, Ltd., 2014. Original Russian Text © G.A. Finenko, G.I. Abolmasova, N.A. Datsyk, Z.A. Romanova, B.E. Anninskii, 2013, published in Rossiiskii Zhurnal Biologicheskikh Invasii, 2013, No. 4, pp. 78–90.

Effect of Food Composition and Temperature on in situ Feeding Rates of Ctenophore Invader Mnemiopsis leidyi A. Agassiz G. A. Finenko, G. I. Abolmasova, N. A. Datsyk, Z. A. Romanova, and B. E. Anninskii Institute of Biology of the Southern Seas, National Academy of Sciences, pr. Nakhimova 2, Sevastopol, 99011 Ukraine email: [email protected] Received February 21, 2013

Abstract—The feeding rates of ctenophore Mnemiopsis leidyi were estimated using the data of the abundance and food composition in the inshore waters of the northwestern Black Sea in 2009–2010. The clearance rate varied in regard to the different foods. The maximum rates were observed when M. leidyi consumed Bivalvia veligers (400 L ind.–1 day–1); the minimum rates were observed when it fed on Copepoda (35 L ind.–1 day–1). The feeding rate increased in accordance with the water temperature in the range from 13°C to 27°C, but dropped when the temperature was higher than 27–28°C. These data were used to calculate the predatory impact of the M. leidyi population on the different groups of its prey and on the zooplankton community in total. The predatory pressure on each prey group and on the zooplankton community was significantly lower for the period of 2009–2010 compared to the previous years. This indicated the decrease in the predatory pressure of the M. leidyi population on the zooplankton community. Keywords: ctenophore, Mnemiopsis leidyi, food composition, clearance rate, feeding rate, daily ration, pred atory impact DOI: 10.1134/S2075111714010032

INTRODUCTION

ogy of prey and their behavior. As a rule, when the feeding of ctenophores was studied experimentally, copepods were the only prey; however, in natural con ditions, the food spectra of ctenophores comprise a list of food items. It was found that the feeding rates when consuming various prey might differ significantly. The ration and clearance rate of medusa Aurelia aurita was tenfold and hundredfold higher when feeding on veligers of Bivalvia compared to small crustaceans (Purcell, 1997). Therefore, the food composition may significantly alter the feeding rate, the grazing impact of the predator on the mortality rate of the functional groups of zooplankton, and, finally, the predator’s effect on the community structure. The study aims to define the feeding rates of differ ent prey groups by ctenophore Mnemiopsis leidyi in situ, as well as to track the effect of the temperature on the feeding rate and to assess the grazing pressure of the ctenophore population on various groups of mesozoo plankton and the plankton community in total in near shore areas of the Crimean coast of the Black Sea.

The abundance of particular ctenophore species and their frequency of occurrence in some areas of the World Ocean have increased during the last decades, and the geographical ranges are expanding, and this is leading to dramatic and irreversible changes in the ecosystems (Brodeur et al., 1999, Mills, 2001, Lynam et al., 2004; Purcell, 2005). Ctenophore Mnemiopsis leidyi penetrated into the Black Sea in the 1980s; it is colonizing the sea region by region and is appearing in many areas. This species has also colonized most of the southern European seas, i.e., the Sea of Azov, Sea of Marmara, Aegean Sea, Caspian Sea, differing with respect to the food and temperature regime; in 2006, it was found in the North Sea and the Baltic Sea (Boersma et al., 2007); in 2005–2009, it was discov ered in different areas of the Mediterannean Sea (Boero et al., 2009). Temperature is the limiting factor for the develop ing of the population of ctenophores (Kremer, 1994). High abundance and production of ctenophore Mne miopsis leidyi, five species of scyphoid medusae, six species of hydromedusae, and two siphonophora spe cies correlate with high water (Purcell, 2005). Never theless, the effect of the temperature on the metabo lism and feeding peculiarities of M. leidyi has been not studied yet in detail. Feeding rates of ctenophores, as well as of other animals, usually fall into a wider range than metabolic rates, which relates to the differences of the morphol

MATERIALS AND METHODS The food spectra and feeding rates of ctenophore M. leidyi in natural conditions were studied from March 2009 through September 2010. The cteno phores carrying the prey in the gut were sampled at three stations located in the shelf zone of the Black Sea in the vicinity of Sevastopol. The animals were fixed in 4% formaldehyde solution. The number of prey and 49

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Copepoda Cladocera Bivalvia veligers Oikople dioica

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ly

120 100 80 60 40 20 Ja n. M ar . Ap r. M ay Ju ne

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Fig. 1. The ratio of particular groups of zooplankton in the gut of M. leidyi (a) and in the zooplankton community of the shelf area (b) (mean ± SD) in January–September 2010.

species composition were assessed in a Bogorov cham ber under a stereomicroscope by the standard count ing method. The clearance rate (the water volume cleared from the food particles, the number of the par ticles is equal to the number found in the ctenophore gut) and daily ration were calculated from the original data and the results of the laboratory experiments on egestion rate (Finenko et al., 2010). The wet weight of the larvae (10 mm) was assessed using the regression equation referring to the body length and weight (Finenko et al., 2003). The dry weight was 2.2% of the wet weight, disregarding the ctenophore age. The zooplankton was sampled simultaneously to the catches of ctenophores at a single monitoring sta tion located in the shelf zone by a Juday net (total ver tical tow, from the bottom to surface, 60–0 m). The samples were fixed in 4% formaldehyde solution and processed in the laboratory by a weightcounting method. The total biomass of mesozooplankton was calculated using the abundance and individual body weight of each zooplankton species and their stages (Petipa, 1957). The food items were set as every zoop lankton species except dinoflagellate Noctiluca scintil lans and ctenophores. The grazing pressure of the ctenophores on the total zooplankton community and its particular groups was calculated using the data on the clearance rate, abundance and size structure of M. leidyi, and the species composition of mesozooplankton during the study period.

Statistics were performed using the builtin options of Microsoft Excel 2002. RESULTS Mesozooplankton was the food of ctenophores during the whole observation period; in particular, the ctenophores consumed all developmental stages of plankton copepods Acartia clausi and A. tonsa, Oithona similis and O. davisae, Calanus euxinus, cla docerans Penilia avirostris and Pleopis polyphemoides, appendicularians Oikopleura dioica, and meroplank ton—veligers of Bivalvia and Gastropoda (Fig. 1). The ratio of copepods in the ctenophore gut decreased from the winter period to the summer from 70–80% to 30% of the total abundance; the opposite pattern was observed for cladocerans (from May through Septem ber). Similar changes were tracked in the plankton of the shelf zone. Larvae of bivalves and O. dioica were a significant part of the food in different seasons: the maximum ratio of veligers was found in April (18%) and July (22%) and of appendicularians in March– April and September (10–11%), coinciding in both cases with the maximum presence in the plankton community. The feeding intensity on different prey expressed as clearance rate depends on the species of the prey other things being equal. The maximum rates were observed when ctenophores fed on larvae of Bivalvia (400 L ind.–1 day–1); the minimum rates, when feed ing on copepods (about 35 L ind.–1 day–1). The clear ance rate when feeding on copepods differed signifi cantly from the other types of the prey (p < 0.01); the differences were insignificant when feeding on Cla docera and veligers of Bivalvia and appendicularians (p > 0.05). We have to note that the variability even within the same type of prey (Cv > 80% for Copepoda up to 242% for Bivalvia), as well as for different prey types (Fig. 2). The relationship between the clearance rate and body carbon of the prey was studied for three temper ature ranges (11–15, 19–25, and 26–29°C) for four prey groups (copepods, cladocerans, veligers of Bivalvia, and total mesozooplankton) (Fig. 3). The clearance rate increases in all three cases together with the individual body weight of ctenophores and when they consume Copepoda, Bivalvia, and total mesozo oplankton; it remains the same for each temperature range when feeding on Cladocera (Fig. 3b). Since copepods are always found in the gut, the overall pattern of the relationship between the clear ance rate and factors (ctenophore individual body weight, abundance of prey, and water temperature) was analyzed for this case (Fig. 4). As was cited above, a tendency of the clearance rate to increase together with the individual body weight of ctenophores (Fig. 4a) and the stability of this feeding parameter in all the variety of food concentrations (Fig. 4b) are seen.

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Daily ration is the second key parameter of the feeding intensity, calculated as the derivative of the clearance rate and the food concentration. In contrast to the values of the clearance rate, the daily ration has a closer correlation with the predator body weight, especially for the wide range of individual weights at high water temperature, when small animals play a sig nificant role in the community together with the large ones (Fig. 6). The relative daily ration of ctenophore varied from 0.05 to 39% (average 4.8 ± 1.1%) at 10– 15°C, from 0.25 to 153% (average 16.3 ± 4.7%) at 19– 25°C, and from 0.25 to 16.3% body carbon (average 19.8 ± 8.4%) at 26–29°C. The calculated equations for each prey type com prising such parameters as clearance rate, ctenophore individual body weight, water temperature, and size structure and population density of ctenophores (Fig. 7) were later used to assess the grazing pressure on partic ular groups and the total zooplankton community by the population of M. leidyi during the summer period (May–September) of 2009–2010 (Fig. 8). All the types of zooplankton prey were consumed with low intensity, less than 3% of abundance of cla docerans and veligers of Bivalvia per day, and even 1% of copepods. In 2010, the consumption of cladocerans by ctenophores was significantly higher than other zooplankton groups. The grazing pressure on the total zooplankton community by the ctenophores was low for the summer periods of 2009 and 2010 (3.8 ± 1.3% and 6.6 ± 1.2%, respectively), even though a slight increase was observed in late July–August (Figs. 8, 9). The summer average abundance and biomass of the ctenophores were almost the same during these years

Clearance rate, L ind.–1 day–1 500 n = 42 400 300 n = 36

n = 52

200 n = 69

100 0

Copepoda Bivavia Cladocera Oikopleura dioica

Fig. 2. Clearance rate of M. leidyi (mean ± SD) when feed ing on different groups of zooplankton.

When analyzing the effect of temperature on the feeding rates, the temperature was grouped into three ranges: (1) 10–15°C (average 13°C), (2) 19–25°C (average 22°C), and (3) 26–29°C (average 27.5°C) (Fig. 4c). The maximum effect of the temperature on the ctenophore’s feeding intensity is observed for the range from 13 to 22°C (Q10 = 4.5) (Fig. 5); when the water temperature exceeds 27°C, the feeding rate decreases. The temperature coefficient Q10 of the clearance rate is about 1.5 for the whole range of tested temperatures (13–27°C). Probably, 24–25°C is the optimal temperature for M. leidyi feeding.

1000 100 10 1 0.1

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Fig. 3. Relationships between the clearance rate and body carbon content of M. leidyi when feeding on Copepoda (a), Cladocera (b), Bivalvia veligers (c), and natural zooplankton community (d) in three temperature ranges. RUSSIAN JOURNAL OF BIOLOGICAL INVASIONS

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(49.8 and 53.2 ind. m–2 and 39.1 and 37.9 g m–2, respectively). Regard must be paid to the seasonal dynamics of M. leidyi population in 2009, when the maximum biomass of this species was registered in the shelf area during the winter period, in February (about 200 g m–2); in summer, it did not exceed 100 g m–2. In both years, the abundance of M. leidyi during summer (May–September) was significantly lower compared to the previous years (on average, 146 and 39 ind. m–2 in 2009–2010 compared to 250 ind. m–2 in 2008). We name the appearance of another ctenophore, Beroe ovata, during the reproduction period of M. leidyi as the main reason, since the former species feeds on the latter. Therefore, the population of M. leidyi had the least grazing pressure on the zooplankton community during the study period in the research area.

40 0 40

DISCUSSION 80

120 200 160 Copepoda abundance, 103 ind. m–2 (c) Specific clearance rate, L mg C–1 day–1 80 60 40 20 0 13

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27.5 Temperature, °C

Fig. 4. Relationships between the clearance rate and body carbon content of M. leidyi (a), copepod abundance (b), and water temperature (c); (a) and (b) refer to the temper ature range of 15–19°C.

Q10 5 4 3 2 1

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Fig. 5. Temperature coefficient Q10 for the clearance rate of M. leidyi feeding on zooplankton (temperature range of 13–27°C).

Assessment of the feeding rates by studying the content of the gut characterizes the peculiarities of the animal’s feeding during the study period and in the study area, since it comprises the data on the realtime consumption of different prey presented in certain concentrations in natural conditions. Opposite to the studies in situ, the laboratory feed ing experiments may lead to artifacts owing to the lim itation of both feeding volume and type/concentration of prey. The results of such experiments may be extrap olated widely, although the data on the gut content are limited by the specific area of sampling and environ mental conditions during the field research. The last approach demands much time and effort, since a sig nificant number of specimens must be caught, includ ing ample amounts of most of the prey types; however, such method gives uptodate information about the feeding status of the population and the trophic rela tionships in the plankton food chain in the particular area of the sea. According to our data, the food spectrum of cteno phores inhabiting the shelf area of the Black Sea dur ing the study period was represented by a high number of different types of prey; the types of prey changed in accordance with the season. Copepods were the main food items in winter and spring, comprising 40–70% of total prey number in the gut. Cladocera were the dominant prey in summer, despite the fact that their abundance in the plankton community was nearly the same as the abundance of copepods. The veligers of mollusks were present in a higher number compared to their ratio in the plankton community. Along with that, their ratio in the total ration was lower than that found individually in the gut. The veligers carry a more robust shell compared to the exuviae of plankton crus taceans, so the egestion rate (time of food processing in the gut) is elongated. On average, the plankton crus taceans passed the ctenophore gut in 1 h at 22 ± 2°C, but it took 6 h for veligers.

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EFFECT OF FOOD COMPOSITION AND TEMPERATURE Ration, % C body day–1 1000 DR = 6.85 C–0.49 2 100 r = 0.081 10 1 0.1

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Fig. 6. Relationship between the relative daily ration and body carbon of M. leidyi in three temperature ranges.

Fig. 7. Abundance (a) and biomass (b) of M. leidyi and abundance of zooplankton and water temperature (c) in the shelf areas of the Black Sea in 2009–2010.

The differences in the catching efficiency of vari ous prey are linked with the behaviour of these animals (swimming speed, ability to escape predators, and the frequency of encountering them) and with the aggre gation density (spatial distribution). On the other hand, exploiting different methods of capturing prey, by ciliate covering of auricules when catching small and weakly motile prey (fish eggs and veligers of Bivalvia) and by the seizure by the oral lobes of large fast moving animals (copepods), may also precondi tion the effectiveness and rate of prey capture (Wagett and Costello, 1999). Small moving organisms, such as mollusks veligers, are caught more frequently than adult copepods (Larson, 1987). This fits nicely the data on the capture effectiveness, when mollusk veligers have no chance to escape being eaten by ctenophores when encountered (100% effectiveness), but Rotatoria Brachionus plicatilis and adult copepods Acartia tonsa are caught with less effectiveness, 70 and 47%, respectively (Madsen and Riisgård, 2010). Regard must be paid to the weak correspondence between the clearance rate and ctenophore body weight in different temperature conditions; however, the range of individual weights differed within these groups. The widest range (body weight of 4.6–50.2 mg C ind.–1, body length of 22–70 mm) referred to the observation per

formed at 11–15°C. The ctenophores studied at 19– 25°C were smaller (body weight of 0.6–35.0 mg C ind.–1, body length of 11–50 mm). When the ctenophores reproduce in summer at 26–29°C, the population comprises the smallest (young) specimens, so the indi vidual weight decreases greatly to 1.0–20.0 mg C ind.–1. Probably, the narrow range of individual weights dif fering only tenfold preconditioned the low correlation coefficients between the studied parameters. Never theless, the relationship between the body weight and the clearance rate was significant at the temperature of 10–15°C for copepods, bivalve veligers, and total zooplankton; as well, this was true for copepods at 26– 29°C (p < 0.05). Even higher significance was found between the daily ration and body weight at 16–19°C and 26–29°C (p < 0.001). In general, the values of the clearance rate, assessed by the ctenophore gut con tent, were higher than those calculated from the experimental data, when the animals were limited in space (kept in containers) (Finenko et al., 2005; Pur cell, 2009; Granhag et al., 2011). Studies of the temperature effect on the feeding parameters of jellyfish and ctenophores are lacking. During acute experiments when ctenophores M. leidyi from the Caspian Sea were acclimated briefly to water temperature ranging from 12 to 27°C, the temperature

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Daily uptake, % of abundance Copepoda Cladocera 25 Bivalvia 20 Zooplankton (food items) 15 10 5 0 2009 2010 Years

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Fig. 8. Daily consumption of certain groups of zooplank ton and total zooplankton community (mean ± SD) by the population of M. leidyi during the summer periods of 2009–2010.

(b) Daily uptake, % of zooplankton abundance/days 25 20 15 10

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Aug. 31

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Dates Fig. 9. Seasonal grazing of the zooplankton community by M. leidyi (mean ± SD) in the shelf areas of the Black Sea in 2009 (a) and 2010 (b).

effect on the clearance rate was significant; i.e., Q10 was 3.81 for the range of 12–20°C and 1.91 at 20– 27°C (Rowshantabari et al., 2012). This is close to our data obtained for natural conditions. The egestion rate decreased in accordance with the temperature increase (Q10 = 1.67 for the whole range of studied temperatures). However, simultaneously to the decrease in the egestion rate, the number of prey increased; i.e., M. leidyi of 5mm body length con sumed 1.4 Acartia at 12°C in ten minutes and 3.5 copepods during the same period at 27°C. Proba bly, the lower Q10 of the egestion rate in comparison to Q10 of the clearance rate was linked to the number of prey, especially for small ctenophores. The feeding intensity of M. leidyi decreased when the temperature

was higher than 27°C; a similar tendency was observed earlier (Purcell, 2009). In 2010, when the surface water layer was warmed to 30°C, most of the cteno phores stayed lower, in the water layer of 25–60 m (S. Ignatyev, personal communication); we assume such fact as proof of the negative effect of high temper ature on M. leidyi. In addition, the fecundity of this species during that period was the lowest, about five eggs per day. Considerable data exist for the temperature effect on the animal metabolism. It was found that the respi ration and excretion rates depended on the water tem perature: Q10 was 2.1 at 7–23°C (Svetlichny et al., 2004), and it was even higher, 4.0, at 10.3–24.5°C (Kremer, 1977). The respiration rate of another cteno phore species, Beroe ovata, increases as the tempera ture increases from 10 to 28°C independently of the individual body weight; the average Q10 was 2.17 ± 0.5 (Svetlichny et al., 2004). According to our data, the values of Q10 for the clearance rate of M. leidyi in nat ural conditions was significantly lower, 1.5 at 13–27°C and about 1.0 at high temperatures (22–27°C). Unlike the common theory of tight dependence of the metabolic rates on the environmental temperature in ectotherms, some exceptions exist (Purcell, 2009). Particularly, the respiration rates of three jellyfish spe cies, Aurelia sp., Chrysaora sp., Cyanea sp., and cteno phore M. leidyi obtained in experiments where the water temperature was close to natural did not depend on this factor; i.e., they did not follow the common rule found during acute experiments when the animals were acclimated to a certain temperature for a short period of time. Unfortunately, the lack of an ample amount of data does not allow us to draw any conclu sions on applying such a rule to the feeding parameters of ctenophores. However, regard must be paid to the different reaction to the temperature of the acclimated specimens and those used in acute experiments, which is related to the physiological adaptation to the envi ronmental temperature. Feeding on specific prey types, the population of ctenophores may alter the composition of mesozoo plankton community, which, in turn, may lead to the changes in the food chain. Uptaking certain species and groups with different intensity and altering the zooplankton community, the ctenophores may also affect indirectly the species composition and size structure of the phytoplankton community. When the ctenophores feed on fine filtrators, mostly Cladocera, they may promote developing the growth of small phy toplankton species. The interannual variability of the grazing pressure of M. leidyi on different groups of prey was well pronounced during the study period. In particular, 20% of veligers of Bivalvia and Cladocera were consumed daily in 2008 (Finenko et al., 2013), but only 2–5% in 2009 (original data). Generally, the grazing pressure on the total zooplankton community was significantly lower in 2009–2010 (3.8 and 6.6%, respectively), compared to 2008 (12.7% of total abun dance per day). This was preconditioned by a low pop

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ulation density of M. leidyi during the summer due to the early appearance of Beroe ovata. As was found earlier, the critical abundance of ctenophores that allowed sustaining the zooplankton community might not exceed 14 g/m3 or 420 g/m2 (if most of the population inhabit the water layer of 0–30 m) (Finenko et al., 2013). According to our recent data, the biomass of M. leidyi population did not exceed this level even during its abundant development. CONCLUSIONS 1. The food spectrum of Mnemiopsis leidyi changes from year to year: in 2009, copepods prevailed in the gut; in 2010, cladocerans (up to 60% of total prey number). Oikopleura dioica comprises 2–5% of the consumed items during the last years. 2. Water temperature and individual body weight have a minor effect on the feeding intensity in the tem perature range of 22–27°C. The abundance of prey is the limiting factor affecting the quantity of consumed food. 3. Grazing pressure of M. leidyi on all the groups of mesozooplankton (Copepoda, veligers of Bivalvia, Cladocera) was lower during the summer periods of 2009–2010 compared to the previous years because of its low population density; this is evidence of the decrease in the grazing pressure of ctenophores on the mesozooplankton community. ACKNOWLEDGMENTS This study was supported by the EU Seventh Frame work Program (FP7), project PERSEUS no. 287600. REFERENCES Boero, F., Putii, M., Trainito, E., et al., First records of Mnemiopsis leidyi (Ctenophora) from the Ligurian, Thyrrhenian, and Ionian Seas (Western Mediterranean) and first record of Phyllorhiza punctata (Cnidaria) from the Western Mediterranean, Aquat. Invasions, 2009, vol. 4, pp. 675–680. doi 10.3391/ai.2009.4.4.13 Boersma, M., Malzahn, A.V., Greve, W., et al., The first occurrence of the ctenophore Mnemiopsis leidyi in the North Sea, Helgol. Mar. Res., 2007, vol. 61, no. 2, pp. 153–155. Brodeur, R.D., Mills, C.E., Overland, J.E., et al., Evidence for a substantial increase in gelatinous zooplankton in the Bering Sea, with possible links to climate change, Fish. Oceanogr., 1999, no. 8, pp. 296–306. Finenko, G.A., Abolmasova, G.I., Romanova, Z.A., et al., Population dynamics of the Ctenophore Mnemiopsis leidyi and its impact on the zooplankton in the coastal regions of the Black Sea of the Crimean coast in 2004– 2008, Oceanology (Engl. Transl.), 2013, vol. 53, no. 1, pp. 88–97. Finenko, G.A., Romanova, Z.A., Abolmasova, G.I., et al., Influence of nutrition conditions on consumption rate and digestion of Mnemiopsis leidyi, Mor. Ekol. Zh., 2005, vol. 4, no. 1, pp. 75–83. RUSSIAN JOURNAL OF BIOLOGICAL INVASIONS

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Translated by D. Martynova Vol. 5

No. 1

2014