Fomina Y., Syarki M. The life cycle of the copepod Thermocyclops oithonoides (Sars, 1863) in Lake Onega // Principy èkologii. 2019. № 3. P. 144‒154. DOI: 10.15393/j1.art.2019.9082


Issue № 3

Original research

pdf-version

The life cycle of the copepod Thermocyclops oithonoides (Sars, 1863) in Lake Onega

Fomina
   Yuliya
Northern Water Problems Institute Karelian Research Centre, rambler7780@rambler.ru
Syarki
   Maria Tagevna
PhD, Northern Water Problems Institute Karelian Research Centre, msyarki@yandex.ru
Keywords:
zooplankton
population
age structure
seasonal dynamics
limnical heterogeneity
smoothing models
Summary: A study of the annual cycles of plankton community and its main elements is of particular relevance in the conditions of climate change and anthropogenic load. The copepod Thermocyclops oithonoides (Sars, 1863) is the main component of the pelagic zooplankton of Lake Onega and a valuable component of planktivorous fish diet. The life cycle of the crustacean populations from the central oligotrophic region of the lake and the large Petrozavodsk Bay was analyzed on the basis of long-term observations. T. oithonoides is found in plankton all year round. In winter, only stage IV-V copepodites are marked, which overwinter in the bottom layer. During the subglacial period, the abandance of the crustaceans reaches 25,3±4,8 th.ind./m3, biomass - 0,286±0,055 mg/m3. It was shown that population dynamics of T. oithonoides in the central part of the reservoir is dicyclic. In the bay, because of the favorable temperature regime, the crustacean can have di-and three cycles. The average long-term population maximums in the center of the lake reach 1,31 th.ind./m3 (abundance) and 0,009 g/m3 (biomass). In the Petrozavodsk Bay the values of population abundance and biomass of T. oithonoides are similar (1,36 ind./m3 and 0,013 g/m3, respectively). In June, adverse hydrochemical conditions in the bay inhibit the development of the crustaceans and cause a delay in its quantitative development. Comparison with the data of the last century showed that, despite the fluctuations in anthropogenic load and climate changes observed in recent decades, no noticeable changes in the nature of the annual cycles of Thermocyclops oithonoides have occurred.

© Petrozavodsk State University

Reviewer: V. K. Shitikov
Received on: 29 May 2019
Published on: 06 October 2019

Introduction

The Onega lake is the largest freshwater body in Europe and the European Northwest of Russia after Ladoga lake. Its ecosystem is influenced by climatic factors and anthropogenic load. The main sources of point pollution are industrial centers – Petrozavodsk, Kondopoga, Medvezhyegorsk. In general, on the most of water area plankton systems are in a natural state, have oligotrophic status. Onega lake is characterized by high water quality and low productivity (Онежское озеро..., 2010). In recent decades, climate fluctuations, an increase in average annual air temperature and precipitation have been observed in Karelia (Назарова, 2015). As a result, the duration of the ice-free period and the "biological summer" period increase (Филатов и др., 2014). In some areas of the lake there is an increase of the water organic matter content, suspended solids, chromaticity, total phosphorus, iron (Калинкина и др., 2019). Such changes cause the reaction of the plankton as a whole, and individual populations. The life cycles of copepods are synchronized with regular seasonal fluctuations in the environment (Nilssen, Wærvågen, 2000). For example, in lake Muggelse in Berlin, due to climate warming, in the crustaceans Thermocyclops oithonoides and Mesocyclops leuckarti the duration of the active plankton phase (a shift to earlier periods in spring and later in autumn) and an increase in the annual population peak were observed (Gerten, Adrian, 2002).

The species Thermocyclops oithonoides (Sars, 1863) belongs to the type arthropods (Arthropoda), class crustaceans (Crustacea), subclass Copepoda, order Cyclopiformes, family Cyclopidae (subfamily Cyclopinae), genus Thermocyclops Kiefer, 1927 (Определитель..., 2010).

T. oithonoides – Palearctic, euryotopic species, belongs to the cold-water complex of temperate latitudes 50-60º northern latitude (Пидгайко, 1984; Куликова, 2017). Crustaceans settled from the Ponto-Caspian region after the last glacial period (Nilssen, Wærvågen, 2000).

The crustacean finds optimal conditions at high dissolved oxygen contents. It lives at pH = 6.4–7.6. It is absent in dystrophic reservoirs, living mainly in eutrophic (mesotrophic) and oligotrophic lakes (Рылов, 1948). T. oithonoides belongs to species with average tolerance to disturbance of ionic composition of water (Калинкина, Куликова, 2009). This species has been recorded in Norway (Nilssen, Wærvågen, 2000), Estonia (Haberman, Virro, 2004), Germany (Adrian et al., 2006), Finland (Lehtovaara et al., 2014), in Pskov-Chudskoye lake on the border between Estonia and Russia (Хаберман и др., 2012). The mass species in Ladoga lake (Родионова, 2013). T. oithonoides occurs in lakes Vozhe and Lacha (Смирнова, 1978), in Kuibyshev (Тимохина, 2000), Gorky (Гусаков, 2005) and Rybinsk reservoirs (Лазарева, 2010), in Nero lake (Лазарева, Смирнова, 2008), etc. It is the most characteristic component of Karelian lakes, according to T.P.Kulikova (2004, 2007, 2010, 2012), this species was recorded in 409 reservoirs out of 556 studied. The crustacean is widespread from the littoral to the pelagic zone.

T. oithonoides is an important element of the trophic chain. It is an optional predator. It feeds on protozoa and young crustaceans. The nauplial stages use algae, protozoa and detritus for food (Монаков, 1976). The crustacean provides fish production in the lakes of taiga and subtaiga, forms the basis of the diet of grouse and smelt (Пидгайко, 1984). In the catches of Onega lake, fish-planktophags make up 50-85 % (Онежское озеро..., 2010).

The aim of the work is to study the life cycle of T. oithonoides in the pelagial of various areas of Onega lake.


Materials

The work is based on the material of complex surveys of the laboratory of Hydrobiology IVPS Karelian Scoentific Center of RAS from 1988 to 2017 during the growing season (June-October) (Сярки, Куликова, 2012; Сярки и др., 2015). Samples of zooplankton of the Central part of the lake were taken in pelagial areas similar in thermal and trophic properties (total 5 stations, 826 samples). Zooplankton of bays was studied on the example of Petrozavodsk Bay (2 stations, 641 samples) (Fig. 1).

The winter state is described on the basis of the materials obtained in the framework of the Russian-Swiss multidisciplinary project "Lake Ladoga: life under ice interaction of subglacial processes through global changes" 2015-2017 (on the same dates) at the Central part of the Petrozavodsk station lips. The winter condition is described from the materials obtained within the framework of the Russian-Swiss multidisciplinary project "Lake Ladoga: life under ice interplay of under-ice processes by global change" in March 2015-2017 (on the same dates) at the station in the Central part of the Petrozavodsk Bay.

Thermal regime in the Central part the lake and the Bay is different due to the high spatial heterogeneity of the lake. Thus, the thermal bar in the Petrozavodsk Bay finish in the third decade of May, and in the central region – in the middle of June (Fig. 2). The season temperature dynamics of Petrozavodsk Bay has its own characteristics associated with active hydrodynamics of the Bay.

The central area of the lake has now the oligotrophic status of the plankton system, as evidenced by the low total phosphorus (10 µg/l) and Chl a (2.7 mcg/l).

Chemical composition of waters of the Petrozavodsk Bay are formed mainly by river flow (95 % – Shuya river), enriched by biogenes, iron, and humus. In winter and in spring the water of Petrozavodsk Bay on 52-62 % is represented by Shuya water. The influence of river waters on the Bay is especially great during the passage of the thermobar and after it, when the water exchange with the central reach of the lake is limited, the hydrochemical conditions for zooplankton form unfavorable. After passage of thermobar the indicators of a chemical the water quality in the Bay is close to the lake. In summer and in autumn the share of lake waters reaches 82-86%. The Petrozavodsk Bay experiences significant anthropogenic pressure (industrial and domestic sewage, city drainage, storm water, water transport). The concentration of total phosphorus is 18 µg/l, Chl a content 3.3 µg/l, by these indicators the Bay has mesotrophic status (Крупнейшие..., 2015; Лозовик и др., 2019).

 

Fig. 1. Location of stations on Lake Onega: 1 – stations in Petrozavodsk Bay; 2 – stations in the central part

 

Fig. 2. Average water temperature (variable averages): 1 – Petrozavodsk Bay; 2 – central part


Methods

Zooplankton samples were taken by Jedi’s plankton net (with a hole diameter of 100 microns) fractionally by layers (0-5, 5-10, 10-25, 25-50, 50-75, 75-100 m) and was fixed by the 4 % formalin. The collection and processing of material was carried out according to the standard method (Методические рекомендации..., 1984).

The number of T. oithonoides was calculated by size and age groups: younger copepodites (stages I–III), older copepodites (IV-V stages), males, females, females with eggs. Nauplius were not identified to species and were not accounted.

When scaling of the zooplankton biomass, the sizes and individual weights calculated for Onega Lake were used (Куликова, Сярки, 1994).

For comparability of data from districts with different depths the quantity values in a water column under a square meter were analyzed.

The smooth curves of the seasonal dynamics of the indicators were obtained by smoothing the time series (from 1988 to 2017) using the moving average method with a step of 7 elements. For this, the data series were ranked by indicator of seasonality (a day from the beginning of the year). Due to the irregularity of the series, the moving average method in the modification of double smoothing was used (Сярки, 2013).


Results

T. oithonoides is found in the plankton year-round. In winter, only copepodites of stage IV–V have been recorded, which hibernate in the bottom layer. In the subglacial period, the number of crustaceans is 673.5 ± 125.7 specimens/m2 (25.3 ± 4.8 specimens /m3), biomass is 7.61 ± 1.42 mg/m2 (0.286 ± 0.055 mg/m3). The share of T. oithonoides in plankton in average abundance is 3.5%, and in biomass - 1.5%.

In the first decade of June in central part of the lake a number of crustaceans in average is 4.2 thousand specimens/m2 (0.06 thousand specimens/m3), the biomass of 0.05 g/m2 (0.001 g/m3). The basic role in the population at this time is played by old copepodites, the proportion of which is about 90 %. In Petrozavodsk Bay values of the number are close - 4.3 thousand specimens/m2 (0.16 thousand specimens/m3) and biomass 0.07 g/m2 (0.003 g/m3), primarily due to adult crustaceans and junior copepodite stages (about 40 % each age group) (Fig. 3, 4).

In late June – early July in the center of lake the number of males and females increases, and in the first decade of July their maximum number is registered – 5.8 thousand specimens/m2 (0.08 thousand specimens/m3), by biomass-0.09 g / m2 (0.001 g/m3). In the first decade of August there is a second maximum of adult crustaceans, which is almost two times more than the first (the number of 10.6 thousand specimens/m2, or 0.26 thousand specimens/m2, biomass 0.15 g/m2, or 0.004 g/m3). For juniors and adult copepod, the waves of generations are also good expressed.

In Petrozavodsk Bay the active development of T. oithonoides populations begin with the half of the first decade of July. Similar delay of summer development in the Bay was noted in copepod crustacean Eudiaptomus gracilis (Фомина, Сярки, 2018). Developmental delay in June may be associated with adverse hydrochemical conditions in the period of the thermobar and after its passage. Active development of the population at the beginning of July can be connected with hydrodynamics of waters in the Bay and with the transfer of crustaceans by the currents from the Central reach of the lake. The generation waves are weakly expressed for older copepodites, for younger copepodites and adult crustaceans they merge (не понял фразы в русском варианте).

The maximum development of populations of T.oithonoides in central district and Petrozavodsk Bay falls at the beginning of August. In the center of the lake the number of crustaceans can reach 46.4 thousand specimens /m2 (1.31 thousand specimens /m3), biomass – 0.39 g/m2 (0.009 g/m3), in the population of T. oithonoides in the Petrozavodskaya Bay these values are close – 35.6 thousand specimens/m2 (1.36 thousand specimens/m3) and 0.34 g/m2 (0.013 g/m3) respectively.

 

 

     

Fig. 3. Abundance dynamics (N, thousand specimens/m2) of Thermocyclops oithonoides age groups in Petrozavodskaya Bay (А) and in the central part of Lake Onega (B): 1 – adults; 2 – senior copepodites; 3 – young copepodites

 

In autumn for crustaceans the share of adults decreases, and the share of copepodites on the contrary, increases (Fig. 4). Older copepodites go into diapause and migrate to the bottom layer. At this time, in the structure of the crustacean population in Petrozavodsk Bay the share of younger copepodites is greater than in the central region of the lake. Perhaps this is due to a more favorable thermal conditions in the Bay, when crustaceans in warm years can give not two generation, as in the center of the lake, but three. According to V.M.Rylov (1948), T. oithonoides is dicyclic, in some lakes it is monocytic. In Karelian lakes the species can be polycyclic (Филимонова, 1965). Nilsen and Wærvågen (2000) noted that in Norway lakes in the life cycle of T. oithonoides there may be two or three generations a year depending on the annual fluctuations of water temperature.

 

Fig. 4. Population structure (%) of Thermocyclops oithonoides in Petrozavodsk Bay (А) and in the central part of Lake Onega (Б): 1 – adults; 2 – senior copepodites; 3 – young copepodites

 

 Petrozavodsk Bay warms up a month earlier than the central district. Since the development rate of T. oithonoides depends on temperature, reproduction of crustaceans in the bay begins in may (позволил себе поставить точку в середине фразы, которая находится в левом столбце снизу стр. 127, чтобы текст приобрел смысл). The proportion of egg-bearing females in the Bay in the beginning of June and the end of August is 50 % of the total number of females. In early June in the center of the lakes the proportion of egg-bearing females is average 5 %, but in July their number is increasing dramatically. The short vegetation period causes the synchronization of reproduction in females (Fig. 5).

 

Fig. 5. Proportion of oviparous females of Thermocyclops oithonoides: 1 – Petrozavodsk Bay; 2 – the central parts of Lake Onega

 

Significance of T. oithonoides in zooplankton changes during the vegetation period. The least role in the community of Petrozavodsk Bay and the central part of the lake, the crustaceans play in late June – early July. The greatest value of T. oithonoides in the bay is observed in the first decade of August and in the beginning of October (according to number – 24%, to biomass – 8%), in the central region – in early June and early September (according to numbers – 26 %, to biomass – 11 %). In relation with the small size of the crustaceans (average weight of adults 0.015 mcg) by biomass it plays a smaller role.


Discussion

The results got showed that in recent years (2014-2017) seasonal dynamics in crustaceans T. oithonoides is within its interannual variability. There were no definite trends in fluctuations of population and biomass due to climate change and seasonal shifts, as well as anthropogenic load. In seasonal dynamics of T. oithonoides from the central district of the lake and Petrozavodsk Bay the differences were found. So, in the cold-water of the central part the life cycle of crustaceans has double cycle character and in the bay with favorable temperature conditions it is double- and three- cyclic. The present work is the initial stage of detailed research of the annual cycle of planktonic crustaceans and in the future will allow to use modern life cycle models (regression, stochastic or simulation), allowing to make a forecast for seasonal development of the population at different-temperature regimes and trophic conditions.


Conclusions

The copepod T. oithonoides is a major component of the zooplankton of lake Onega and an important food object for planktophagous fish. Life cycle of crustaceans in cold-water oligotrophic area of the lake has a double-cyclic character, in the large Petrozavodsk Bay due to the favorable temperature regime, double- and three-cyclicity is possible.

The average annual population maxima in the center of the lake in number reach 1.31 thousand specimens/m3, in biomass – 0.009 g/m3. The values for the population in the Petrozavodsk Bay are similar, in number – 1.36 thousand specimens/m3, in biomass – 0.013 g/m3, respectively. In June, adverse hydrochemical conditions in the bay inhibit the development of crustaceans and cause a delay in its quantitative development. Fluctuations of anthropogenic load and climatic changes do not yet affect the nature of the annual cycle of crustaceans in lake Onega.


References

Adrian R., Wilhelm S. and Gerten D. Life-history traits of lake plankton species may govern their phenological response to climate warming, Global Change Biology. 2006. Vol. 12. P. 652–661.

Filatov N. N. Ruhovec L. A. Nazarova L. E. Georgiev A. P. Efremova T. V. Pal'shin N. I. Climate change impact on the lake ecosystems of the North of European Russia, Uchenye zapiski Rossiyskogo gosudarstvennogo gidrometeorologicheskogo universiteta. 2014. No. 34. P. 48–55.

Filimonova Z. I. Lower crustaceans of the plankton in the lakes of Karelia, Fauna ozer Karelii. Bespozvonochnye. M., L.: Nauka, 1965. P. 111–146.

Fomina Yu. Yu. Syarki M. T. The life cycle of the copepod Eudiaptomus gracilis (Sars, 1863) in Lake Onego, Principy ekologii. 2018. No. 3. P. 92–105. DOI: 10.15393/j1.art.2018.7842.

Gerten D., Adrian R. Species-specific changes in the phenology and peak abundance of freshwater copepods in response to warm summers, Freshwater Biology. 2002. Vol. 47. P. 2163–2173.

Guidelines for the collection and processing of materials in hydrobiological studies in freshwater. Zooplankton and its products.. L.: GosNIORH, 1984. 33 p.

Gusakov V. A. Meiobenthos of the Gorky Reservoir, Biologicheskie resursy presnyh vod: bespozvonochnye. Rybinsk: Izd-vo OAO «Rybinskiy dom pechati», 2005. P. 98–141.

Haberman J., Virro T. Zooplankton, Lake Võrtsjärv. Tallinn: Encyclopedia Publishers Ltd, 2004. P. 233–251.

Haberman Yu. Virro T. Blank K. Zooplancton, Pskovsko-Chudskoe ozero. Tartu: Eesti Loodusfoto, 2012. P. 285–306.

Kalinkina N. M. Kulikova T. P. Evolutionary conditioning of response to changes in ionic composition of water in hydrobionts: on the example of freshwater zooplankton, Izvestiya RAN. Ser. biologicheskaya. 2009. No. 2. P. 243–248.

Kalinkina N. M. Tekanova E. V. Sabylina A. V. Ryzhakov A. V. Changes in the hydrochemical regime of Lake Onega since the early 1990s, Izvestiya RAN. Ser. geograficheskaya. 2019. No. 1. P. 62–72.

Kulikova T. P. Syarki M. T. Size and weight characteristics of mass species of crustaceans and rotifers in Lake Onega (reference and information material). Petrozavodsk: Karel'skiy nauchnyy centr RAN, 1994. 16 p.

Kulikova T. P. Zooplankton of the water bodies in the northern part of the Ladoga Lake basin. Petrozavodsk: KarNC RAN, 2012. 192 p.

Kulikova T. P. Zooplankton of the water bodies of the Lake Onega basin. Petrozavodsk: KarNC RAN, 2007. 223 p.

Kulikova T. P. Zooplankton of the water bodies of the Republic of Karelia (Russia): History of research, main areas of research, species composition, bibliography. LAP LAMBERT Academic Publishing, 2017. 125 p.

Kulikova T. P. Zooplankton of the water bodies of the White Sea basin. Petrozavodsk: KarNC RAN, 2010. 325 p.

Kulikova T. P. Zooplankton of water bodies of the Shuya river basin. Petrozavodsk: KarNC RAN, 2004. 124 p.

Lake Onega. Atlas. Petrozavodsk: Karel'skiy nauchnyy centr, 2010. 151 p.

Lazareva V. I. Smirnova S. M. Crustaceans and rotifers, Sostoyanie ekosistemy ozera Nero v nachale XXI veka. M.: Nauka, 2008. P. 175–210.

Lazareva V. I. Zooplankton structure and dynamics in the Rybinsk reservoir. M.: Tovarischestvo nauchnyh izdaniy KMK, 2010. 183 p.

Lehtovaara A., Arvola L., Keskitalo J., Olin M., Rask M., Salonen K., Sarvala J., Tulonen T., Vuorenmaa J. Responses of zooplankton to long-term environmental changes in a small boreal lake, Boreal environment research. 2014. 19 (suppl. A). P. 97–111.

Lozovik P. A. Zobkov M. B. Borodulina G. S. Tokarev I. V. Effects of external water exchange between bays of lakes on chemical indicators of water, Vodnye resursy. 2019. T. 46. No. 1. C. 91–101.

Monakov A. V. Nutrition and nutritional relationships of freshwater copepods. L.: Nauka, 1976. 170 p.

Nazarova L. E. Precipitation in Karelia, Trudy Karel'skogo nauchnogo centra RAN. 2015. No. 9. P. 114–120.

Nilssen P., Wærvågen S. B. Superficial ecosystem similarities vs autecological stripping: the "twin species" Mesocyclops leuckarti (Claus) and Thermocyclops oithonoides (Sars) – seasonal habitat utilisation and life history traits, J. Limnol. 2000. Vol. 59 (2). P. 79–102.

Pidgayko M. L. Zooplankton of the waterbodies in the European part of the USSR. M.: Nauka, 1984. 208 p.

Rodionova N. V. Zooplancton, Ladoga. SPb.: Nestor-Istoriya, 2013. P. 298–306.

Rylov V. M. SR. The fauna of the USSR. Crustaceans, freshwater cyclopoida. T. III. Vyp. 3. M.; L.: Izd-vo Akademii nauk SSSR, 1948. 318 p.

Smirnova T. S. Zooplankton of Vozhe and Lacha lakes, Gidrobiologiya ozer Vozhe i Lacha v svyazi s prognozom kachestva vod, perebrasyvaemyh na yug. L.: Nauka, 1978. P. 102–130.

Syarki M. T. Kulikova T. P. Zooplankton of Lake Onega: Svidetel'stvo o gosudarstvennoy registracii bazy dannyh No. 2012621150. Pravoobladatel': Federal'noe gosudarstvennoe byudzhetnoe uchrezhdenie nauki Institut vodnyh problem Severa Karel'skogo nauchnogo centra RAN (IVPS KarNC RAN) (RU). Data registracii v reestre baz dannyh 9 noyabrya 2012 g.

Syarki M. T. Tekanova E. V. Chekryzheva T. A. Pelagial plankton of Lake Onega: Svidetel'stvo o gosudarstvennoy registracii bazy dannyh No. 2015620274. Pravoobladatel': Federal'noe gosudarstvennoe byudzhetnoe uchrezhdenie nauki Institut vodnyh problem Severa Karel'skogo nauchnogo centra RAN (IVPS KarNC RAN) (RU). Data registracii v reestre baz dannyh 13 fevralya 2015 g.

Syarki M. T. The study of the seasonal dynamics traits of plankton using the duble-smoothing method, Principy ekologii. 2013. No. 1 (5). P. 61–67.

The identification key for freshwater invertebrates of Russia and adjacent territories. V. 1. Lower invertebrates. M.: Tovarischestvo nauchnyh izdaniy KMK, 2010. 495 p.

The largest lakes-reservoirs of the North-West of the European part of Russia: current state and changes in ecosystems under climate variability and antropogenic impact. Petrozavodsk: Karel'skiy nauchnyy centr RAN, 2015. 375 c.

Timohina A. F. Zooplankton as a component of the Kuibyshev reservoir ecosystem. Tol'yatti: IEVB RAN, 2000. 193 p.


Displays: 1805; Downloads: 381;