ACTA ZOOLOGICA BULGARICA Acta zool. bulg., 65 (1), 2013: 27-36

Seasonal Dynamics of the Testate Amoebae Fauna (Protozoa: Arcellinida and Euglyphida) in Durankulak Lake (Northeastern Bulgaria)

Rositsa Davidova, Victor Vasilev

University of Shumen “Ep. K. Preslavsky”, Faculty of natural sciences, 115 Universitetsca Str., 9700 Shumen, Bulgaria; E-mail: [email protected]

Abstract: The seasonal dynamics of diversity, abundance and dominant structure of the testaceans in Durankulak Lake have been studied. The data showed that from January to October the species abundance increased gradually and reached average 3280 specimens/cm3. The greatest taxonomic diversity was observed in summer (49 species) and the smallest diversity was registered in winter (33). The results of the study showed that the maximum of the species richness and abundance varied in different stations and seasons – from 8 to 30 species and from 210 to 8310 specimens/cm³. From a total of 26 dominant species, only 2 had a high relative significance throughout the year – Trinema enchelys and Euglypha rotunda. Eight species grow significantly and were established as dominants only in some seasons. These are: Trinema lineare, Centropyxis platystoma and Difflugiella oviformis in winter, Corythionella georgiana in spring, Corythionella georgiana, Difflugia minuta, Euglypha acanthophora and Microchlamys patella in summer and Cyphoderia ampulla and Microchlamys patella in autumn.

Key words: Testate amoebae, Durankulak Lake, diversity,­ abundance, seasonal dynamics

Introduction An important trend in ecological studies of testate namics of the diversity and the abundance of the amoebae is investigation of the seasonal and annual species and the influence of different physicochemi- changes in community structure. Research in this cal environmental factors on it. Investigating testate area provide more accurate data about preferences amoebae fauna in different reservoirs Mo r a c z e w s k i for the environment requirements of separate species, (1962, 1965, 1967), Ja x (1992), Sc h ö n b o r n (1992a, their distribution in different habitats and allow to 1996), Vi k o l (1992), Ma z e i and Ts y g a n o v (2007), be make more certain conclusions about their role showed that the number of taxa and distribution of in natural ecosystems. The authors La m i n g e r (1971), species in freshwater ecosystems has its own spe- Ba b i t s k i y (1985), Sc h ö n b o r n (1992a, 1992b), Vi k o l cificity and are determined by particular abiotic and (1990) and Fo i s s n e r (1994) revealed different aspects biotic factors. However, the data of patterns of sea- of the ecology of testaceans in freshwater basins such sonal dynamics of testate amoebae communities in as annual production, annual change in density and lakes remain still fragmentary and incomplete. biomass, number of generations per year, mortality The purpose of this paper is to analyze the sea- rate and more. An object of study is as well the dy- sonal changes in the taxonomic diversity, abundance

27 Davidova R., V. Vasilev and dominant structure of testate amoebae in Statistical analysis was carried out using soft- Durankulak Lake – one of the natural lakes of the ware STATISTICA 6. firth type on the West coast of Black Sea. Along with Lake Shabla-Ezeretz it is the only coastal firth on Results and Discussion Bulgarian Black Sea coast which is preserved in a completely natural state. A total of 80 testate amoebae belonging to 19 genera were found in Durankulak Lake in the present study. The list of taxa, their abundance, relative significance Materials and Methods (D) and seasonal distribution in different stations of The materials were taken from five localities in the lake are presented in Table 1. Only seven or 8.8 % Durankulak Lake in 2010. It is a shallow firth, which of the species were established throughout the year. covers the coastal lowlands of some deep dry valleys, These are Difflugia pristis, Euglypha rotunda, E. tu- located in the utmost North-eastern part of Bulgaria berculata, Microchlamys patella, Tracheleuglypha (28° 33’ 43’’ Е, 30° 40' 30'' N). Durankulak Lake acolla, Trach. dentata and Trinema enchelys. can be defined as a reservoir with varying eutrophic and hypertrophic characteristics, depending on the Seasonal dynamics of the diversity and amount of biogenic elements and organic matter in abundance its waters. Its regime is characterized by periods of The seasonal changes in testate amoebae com- high water in spring months (average monthly maxi- munity at different stations of the lake had some mum in May), and periods of low water in summer particular characteristics­ and showed different and autumn months (average monthly minimum in trends (Fig. 2). So, maximal number of species were October). In the littoral zone it is overgrown with marked in summer in stations 2 (30 taxa) and 3 (18), aquatic vegetation – Phragmites australis, Typha in autumn in stations 4 (18) and 5 (15), or species angustifolia, Typha latifolia and Shoenoplectus tri- richness remains constant from January to August – queter (Ge o r g i e v 1998). The study sites were located station 1 (by 14 taxa) and decreases in October. The in different sampling stations (Fig. 1). abundance peaks were occurred in spring in stations The samples were collected four times a year 1 (1930 specimens/cm3) and 5 (5870 specimens/cm3) (in January, April, August and October) of bottom or autumn­ in stations 2 (8130 specimens/cm3), 3 sediments from the littoral zone of the lake at a (3930 specimens/cm3) and 4 (3490 specimens/cm3). depth of 0.5 to 1.0 m. Approximately 100 cm3 of the At station 4 there was a greater species richness and surface sediment was collected from each site. The abundance not only in October, but in January, com- material was fixedin situ with 4% formaldehyde and pared with that in April and August. In our opinion, examined in the laboratory. For each sample, five this trend is due to the strong development of differ- preparations of 0.1 cm3 of the sediment was studied ent types of algae observed in the station during the after homogenization. The number of the species cold period. found in it was calculated in specimens/cm³. For Summarizing the received data for the lake as a the purposes of quantitative and qualitative analysis whole, it can be said that the greatest taxonomic di- testate amoebae were observed with an optical versity was observed in the August (49 species) and microscope Amplival. the smallest – in January (33) (Fig. 3). The biggest The relative significance was used to determine species diversity in the summer is caused by the the dominant structure of testacean communities. appearance of many species with a low population The dominance was calculated by the formula: D = density, which not observed in the other seasons. n/N х 100, where n is the number of the specimens Only in summer 17 species were observed. These of every species and N is the total number of all are Arcella hemisphaerica f. undulata, A. rotundata, specimens. All species were divided into 4 groups, Centropyxis elongata, Cryptodifflugia compressa, according to the 4-grade classification of Ti s c h l e r Cyclopyxis kahli, Difflugia acuminata, D. cylindrus, (1955): subrecedent – with relative significance D. dragana, D. elegans, D. lanceolata, D. lacustris, < 1%; recedent – with relative significance 1-2%; D. oblonga, D. parva, D. pauli, D. sarissa, D. subdominant – with relative significance 2-5%; ventricosa and Difflugiella patinata. By comparison, dominant – with relative significance > 5%. only in winter and spring were found by 7 species,

28 Seasonal Dynamics of the Testate Amoebae Fauna (Protozoa: Arcellinida and Euglyphida) in Durankulak ...

Fig. 1. Map of the Durankulak Lake and location of the sampling sites. and only in autumn – 5 (Table 1). The species, which observed in other lakes as well. In a study of Lake were established only in one season represent 45% Mamri, Mo r a c z e w s k i (1962) indicated that the max- of all identified species in the lake. Their relative imum number of individuals, living in the benthal significance varies between 0.02% and 0.54% and was reached at the end of September and October. they belong to the group of recedent. The same author (Mo r a c z e w s k i 1967), studying the The abundance of testate amoebae in the lake seasonal dynamics of testate amoebae fauna of Lake was the lowest in January (average 2014 specimens/ Zegzre, found in some of the surveyed stations great cm3), then gradually increased and reached its peak in diversity of species in spring, which was consider- October – average 3280 specimens/cm3 (Fig. 3). The ably greater than that in summer and autumn. In a relatively high abundance in autumn, although the study of dynamics of testate amoebae fauna in sever- number of species during this season is lower than in al small ponds Ja x (1992) registered a clear trend of summer and spring, can be explained by the fact that increased number and biomass of testate amoebae in in this period some species develop significantly. winter and early spring. Investigating the reservoirs For example, Euglypha rotunda and Microchlamys of Dniester river basin Vi k o l (1992) found that in patella are present in testate amoebae communities some types of biotopes the number of testate amoe- throughout the year, but have the highest population bae increased from spring to summer and then fell density in autumn (average 866 specimens/cm3 and again in autumn. The maximal abundance the author 272 specimens/cm3 respectively). Cyphoderia am- registered in spring and autumn. Se r a f i m o v et al. pulla was also found with a significant number of in- (1995) indicated that the largest species diversity of dividuals (average 400 specimens/cm3) in October. testate amoebae in two quarry lakes of Sofia district The results of the study and analysis show is established during the summer and the beginning that the peak in development of testate amoebae in of the autumn. Analyzing the dynamics of testate Durankulak Lake varied in different stations and amoebae community in a sphagnum bog (Middle seasons and is associated with the availability of op- Volga region, Russia) from May to September Ma z e i timal conditions for them. and Ts y g a n o v (2007) received different results. In Such significant fluctuation in the species rich- some of the surveyed stations they found high val- ness and abundance in separate seasons has been ues ​​of species abundance in July-September, in other

29 Davidova R., V. Vasilev D 0.02 0.08 0.02 0.04 0.08 0.04 0.02 0.61 0.02 0.02 0.02 0.02 2.86 0.10 0.06 0.04 4.00 0.44 0.08 0.10 0.44 0.28 1.45 0.06 0.14 0.60 0.06 0.12 1.31 0.30 ------5 20 10 80 20 ------4 10 10 10 40 10 170 100 2000 ------3 30 50 40 10 410 October ------2 20 30 10 10 ------1 10 20 20 40 10 20 ------5 10 30 ------4 10 10 10 730 ------3 10 10 60 August ------2 10 10 20 10 10 10 10 60 170 150 ------1 40 30 10 10 ------5 20 30 230 ------4 ferent stations of the Durankulak Lake. 10 10 ------3 10 20 10 90 10 10 20 10 590 April ------2 80 40 80 10 60 ------1 40 30 10 ------5 120 ------4 20 370 ------3 20 10 10 January ------2 10 90 ------1 10 10 10 10 , 1955 , 1929 , 1857 , 1870 y r e , 1929 d d t e i n e i r e , 1929 h o m a s a n d , 1929 T , 1917 r e , 1959 , 1983 fl d r e a n , 1928 e , 1902 , 2005 d a i r & e n , 1929 s fl d f , 1879 a n r e d e , 1838 y a n d ll r e , 1928 g fl a y d . , 1830) S d e l h o m a s fl ., 1841) L , 1917 e i a n r e b , 1843 e r g e e n a r b T o n n e t P d b a n i c h o fl a i r e fl f , 1841) D , 1931 e r g a n , 1852 e h r e n , 1929 b Taxa h r e n fl r e a y h r e n , 1890) D D , 1918 e l r e , 1917 e r g d , 1954) O , 1929 d , 1929 ( E , 1902 E b ( E d , 1890) , 1890 e r t y d D a i r , 1929 h r e n r e a n d r e ., 1841) L , 1864) D d , 1954 a i r P f ., 1929) B a n d b f d fl r e E e n a r a y e fl i c h fl d h r e n a y a n a n h o m a s P compressa l e e e n a r l e n a r e n a r ll N georgiana ( E fl a n fl h r e n P a h o m a s (D e ( P e P fl T

e D Arcella discoides Arcella D. acutissima D Corythionella C. delicatula D. dificilis Cyphoderia ampulla P A. rotundata D C. aerophila Centropyxis aculeata Centropyxis Cyclopyxis eurystoma C. hirsuta D D. ampullula P Cryptodifflugia C. cassis ( W C. platystoma (P C. minuta D Difflugia acuminata C. ecornis ( E D. cylindrus ( T A. hemisphaerica C. kahli C. constricta C. sylvatica A discoides v. scutelliformis discoides v. A P C. cassis v.spinifera D A.gibbosa v.mitriformis C. elongata C. laevigata A. hem. f. undulata C. aerophila v. sphagnicola D v. C. aerophila Table 1. List of taxa and their abundance, relative significance (D) seasonal distribution in dif Table

30 Seasonal Dynamics of the Testate Amoebae Fauna (Protozoa: Arcellinida and Euglyphida) in Durankulak ... D 0.02 0.37 0.02 0.02 0.20 0.54 0.02 2.78 0.04 0.04 0.04 0.06 0.08 0.02 0.04 0.04 0.86 0.14 2.76 0.06 3.56 0.28 0.52 0.46 0.28 2.08 1.59 1.39 0.02 1.43 ------5 10 30 10 10 30 20 160 ------4 20 70 140 ------3 40 30 90 70 240 October ------2 10 90 ------1 30 10 30 ------5 10 10 430 ------4 ------3 20 10 40 10 80 30 10 340 1180 August ------2 70 10 50 10 20 20 30 20 30 10 210 1760 ------1 30 40 ------5 20 60 250 160 1370 ------4 10 40 50 280 ------3 20 20 10 April ------2 10 40 20 30 40 50 ------1 60 30 10 10 ------5 190 200 120 350 ------4 30 20 80 290 ------3 30 140 January ------2 20 40 30 50 80 ------1 70 , 1958 , 1849 h o m a s e r t y T , 1983 e n , 1983 d , 1877 g y e n , 1983 d , 1965 d , 1955 , 1983 e i ., 1841) P e n g i c d o r n v h r g b k o , 1926 h o m a s v , 1954) O Taxa i , 1965 , 1837 , 1831 r e , 1965 , 1902) G .-L. & , 1931 c h ö n , 1918 , 1890 d d i n & T ., 1864) L , 1899) O , 1902 d a ï S , 1879 d o r n e r g d , 1918 d a n o r n & Z a i r , 1902 , 1890 y ll b , 1954) O b T f , 1909 h o m a s b d d , 1902 , 1890 a r d a fl , 1950 j , 1983 , 1902 , 1902 e n e n a r a i r d i d e e i e n a r a y u n , 1983 u f d d d p o n n e t e n a r l e n a r a s h e n ( P g P c h ö n h r e n e n d a y S c h ö n e n a r e n a r P i a m C d l h o m a s g e n a r e n a r g e n a r e n a r L acanthophora ( E D. dragana O D. lucida P D. minuta R D. gramen P D. pauli O D. levanderi D. lanceolata D. elegans P D. oblonga E D. lobostoma L D. stoutii O D. petricola D. globulosa D D. pusilla P D. glans P D. ventricosa D D. manicata P D. horrida S Difflugiella angusta D. globularis ( W D. pristis P D. lithophilla D. oviformis B Euglypha ( T D. microstoma D. sarissa D. patinata S D. lacustris ( P D. parva ( T D. pulex P Table 1. Continued. Table

31 Davidova R., V. Vasilev D 0.22 0.44 0.40 0.04 6.00 0.06 0.02 0.02 0.02 2.23 0.22 1.87 1.29 0.54 0.14 1.35 0.89 2.72 32.93 15.41 ------5 15 10 40 30 640 160 ------4 18 10 30 60 30 450 190 140 3490 ------3 16 38 70 40 780 430 310 3930 1290 October ------2 13 30 30 380 100 170 8130 2920 4330 ------1 11 10 10 210 ------5 12 50 20 20 10 10 10 10 620 ------8 4 20 10 20 30 840 ------3 18 49 50 40 10 340 450 170 2860 August ------2 30 80 50 10 20 820 720 570 6530 1560 ------1 14 20 80 10 70 40 20 10 1450 1040 ------5 13 20 70 20 30 5870 3590 ------4 10 30 10 30 820 350 ------3 40 17 10 20 190 340 180 1560 April ------2 15 10 80 640 150 1340 ------1 14 10 10 50 110 170 200 1190 1930 ------5 12 80 70 40 10 930 100 100 2310 ------4 16 60 10 80 10 110 110 380 320 560 100 2550 ------3 33 15 70 10 50 30 290 510 660 100 100 100 2130 January ------2 17 20 10 60 40 50 240 270 100 460 150 1720 ------1 14 20 10 50 70 10 50 10 30 1000 1360 , 1955 , 1970 , 1907 h o m a s , 1938 , 1874 , 1902 T . ,1885 ) , 1878 d r e , 1962 z e y d l v d , 1964 & a c h ., 1877) e m a n s k y , 1890 e i a n , 1881 e z l e n a r d ) c h u r c d o , 1955 fl 3 , 1911 w e r i n t z e w k a n o e d l . & L o n n e t A a D h a r l e n a r B , 1841 Taxa V a r a n e k

( C , 1902 i n h o m a s e n a r T d d ., 1838) L T b , P , 1959 a r , 1890 j , 1890 e s d u e n a r d l S compressa h r e n D a i arcelloides o n n e t hemisphaerica P e n a r ( E e n a r ,1932 ,1911 B P r e ll d a n fl e o c k e r e Abundance (specimens/cm E. filifera E. rotunda W E. rotunda Total species Total Euglyphella delicatula P lineare Tr. Schaudinnula irregularis ( A Paraquadrula irregularis Tr. enchelys Tr. Tracheleuglypha acolla Tracheleuglypha patella Microchlamys Phryganella Pseudodifflugia Plagiopyxis declivis C v.truncatum lineare Tr. Tracheleuglypha dentata Tracheleuglypha Phr. paradoxa P Phr. Psammonobiotus linearis G E. tuberculata Pl. minuta Trinema complanatum P Trinema C D E. tuberculata minor E. tuberculata Table 1. Continued. Table

32 Seasonal Dynamics of the Testate Amoebae Fauna (Protozoa: Arcellinida and Euglyphida) in Durankulak ...

Fig. 2. Seasonal dynamics of the species’ diversity (A) and abundance (specimens/cm3) (B) of testate amoebae in studied stations.

in October, a half (6) of all found species here were dominant – Centropyxis cassis, Difflugia levan- deri, D. pristis, Centropyxis aculeata, C. aerophila and C. constricta. In Station 2, ten species formed the dominant structure. Tr. enchelys was dominant throughout the year, E. rotunda prevailed in January, August and October, M. patella – in January, April and August, Pl. declivis – in January and April. The species Trinema lineare and Centropyxis platys- toma were dominant only in January, Arcella hemi- sphaerica and Cyclopyxis eurystoma – in April, and Euglypha acanthophora and E. tuberculata – only Fig. 3. Seasonal dynamics of the species’ diversity and in August while in the other seasons were not found. average abundance (specimens/cm3) of testate amoebae in In Station 3, Tr. enchelys dominated throughout the Durankulak Lake. year again. E. rotunda occurred from January to August, and during the three seasons was dominant. stations – high number at the beginning of the sea- In January, a high relative significance had Tr. lin- son, and yet in other – absence of clear tendencies in eare. Corythionella georgiana and Pl. declivis de- abundance dynamics. The greatest number of spe- veloped greatly in April, and Difflugia minuta, D. cies was found in August. pristis and Psammonobiotus linearis – in August. In autumn it was established the most dominant, which Sea­sonal dynamics of the dominant structure ordered by reducing their relative significance were The results of analyses of seasonal­ dynamics of M. patella, Ps. linearis, Arcella hemisphaerica, E. the dominant structure at different sta­tions are repre- tuberculata and Difflugia pulex. In Station 4 nine sented in Fig. 4. Our inves­tigation showed that there species were dominants. Tr. enchelys prevailed are seasonal changes in the dominant­ species com- in January, April and October. Tr. lineare, C. plex. In Station 1 eleven species were dominants. platystoma, E. rotunda and Difflugiella oviformis Trinema enchelys was dominant from January to formed dominant complex in January, Difflugia August. Dominants, but with significantly lower pulex prevailed in April. Corythionella georgiana relative significance were alsoEuglypha tuberculata predominated only in August and Cyphoderia am- v. minor, Euglypha rotunda and Plagiopyxis declivis pulla prevailed in October. In Station 5 there were 6 in April and Microchlamys patella – in August. dominant species in January, with E. rotunda being Because of the small number of specimens established the one with the most significant presence. The other

33 Davidova R., V. Vasilev

Fig. 4. Relative abundance of the dominant species in the studied stations in different seasons.

5 species – Difflugia pulex, D. minuta, D. pristis, of the stations. Eight species grow significantly and Difflugiella oviformis и Centropyxis platystoma were established as dominants only in some sea- were either not found or were found with very few sons. Thus, in winter Trinema lineare, Centropyxis specimens in the other 3 seasons. Tr. enchelys and platystoma and Difflugiella oviformis also became Difflugia glans were most prominent in April. In dominant, and the same happened to Corythionella August over 69% of the specimens belonged to one georgiana in spring. The highest number of domi- species – D. gramen. In October the dominance nants was found in summer when Corythionella was distributed among 5 species, with M. patella, georgiana, Difflugia minuta, Euglypha acantho- Difflugia microstoma and Cor. georgiana being the phora and Microchlamys patella also became domi- most significant. The same species were not found nant. In autumn, a significant growth was registered or were present with insignificantly small numbers in Cyphoderia ampulla and Microchlamys patella. in the other seasons. Many species developed intensively only in some sta- From a total of 26 dominant species found in tions and in different seasons. For the rest of the time different stations and seasons, only 2 had a high rel- they were present in testate amoebae communities, ative significance throughout the year. These were but with insignificant abundance. These were Trinema enchelys, which dominated in all stations Difflugia pristis – dominant in January at Station 5, in the spring and whose abundance was maximal in August at Station 3 and in October at Station 1; in April, and Euglypha rotunda – with maximum Euglypha tuberculata dominant in April at Station number of specimens observed in October. After 2 and in October at Station 3; A. hemisphaerica – that the number of specimens of the latter slightly in August at Station 3 and in October at Station 2; decreased, but remained significant throughout the Psammonobiotus linearis – in August at Station 3 winter, when the species prevailed in most (80%) and in October at Stations 3, 4 and 5; D. pulex – in

34 Seasonal Dynamics of the Testate Amoebae Fauna (Protozoa: Arcellinida and Euglyphida) in Durankulak ...

January at Stations 4, 5 and in October at Station 3; species throughout the year and explained it with Plagiopyxis declivis – in January at Station 2 and in the lack of a stable community of testate amoebae April at Stations 1 and 2; C. platystoma – in January in the stations. Ma z e i and Ts y g a n o v (2007) found at Station 2 and in April at Stations 1 and 2; D. glans that a characteristic feature of seasonal changes in – in April at Station 5; D. microstoma dominant in different biotopes in a sphagnum bog is replacement October at Station 5. of species composition. The present research also The studies of the dynamics of dominant species showed that in the studied stations of Durankulak complexes of testate amoebae in freshwater reservoirs Lake the dominance is not clearly expressed and the in different seasons are scanty. Investigating several dominant structure is not uniform – in different sea- small ponds, Mo r a c z e w s k i (1965) registered a sons testate amoebae communities are dominated by lack of a clear and constant dominant structure in different species. the studied stations, which he explained with the significant fluctuation of water level in different seasons. Later, in Lake Zegzre, Mo r a c z e w s k i (1967) Acknowledgements: This study was carried out under a project again observed a consistent change in the dominant N RD-07-336 / 2011 funded by the University of Shumen.

References

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