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Protistology 12 (1), 38-46 (2018)
Protistology
The new and rare species of the testate amoebae (Amoebozoa: Arcellinida) from mountain lakes of Azerbaijan
Nataly Yu. Snegovaya and Elyana N. Tahirova
Institute ofZoology NAS of Azerbaijan, Baku, Azerbaijan | Submitted October 13, 2017 | Accepted December 23, 2017 |
Summary
A new testate amoebae, Awerintzewia minuta sp. n. and two rare species, Difflugia serbica Ogden and Zivkovic, 1983, and Difflugia biconvata Ertl, 1965 were found during a faunistic study ofthe testate amoebae in two high-mountain lakes in Azerbaijan. The morphology and biometrics ofthese testate amoebae were described by LM and SEM investigations. The genus Awerintzewia Schouteden, 1906 and two species: Difflugia serbica Ogden and Zivkovic, 1983 and Difflugia biconvata Ertl, 1965 are reported for the fauna of the Caucasus for the first time.
Key words: testate amoebae, systematics, Difflugia, Awerintzewia, Azerbaijan
Introduction
The fauna oftestate amoebae ofthe Nakhichevan Autonomous Republic has not been studied extensively. Literary sources mention only four species of testate amoebae (Arcella costata Ehrenberg, 1847, A. vulgaris Ehrenberg, 1830, Centropyxis aculeata (Ehrenberg, 1838) and Difflugia corona Wallich, 1864) from water reservoirs in the vicinity of Bichenek. The first information on the fauna of testate amoebae of the Western Azerbaijan was published by Veysig (1931) from Lake Goy-Gol. In the paper the author provided the data on 12 species of testate amoebae (Arcella discoides Ehrenberg, 1843, Centropyxis laevigata Penard, 1890, C. aculeata Ehrenberg, 1838, Difflugia scalpellum Penard, 1899, D. capreolata Penard, 1902, D. lemaniBlanc, 1892, D. manicata Penard, 1902, D. lithoplites Penard, 1902, D. acuminata Ehrenberg, 1838, D. pyriformis Perty, 1849, D. elegans Penard, 1890
and D. constricta Ehrenberg, 1841). In the early 21st century, Snegovaya and Alekperov (2005) carried out a research on testate amoebae in the Western Azerbaijan. As a result of this study, 70 species of testate amoebae were found, of which two new families, six genera, and 23 species were described.
As an outcome of recent processing of the available samples, a new species of testate amoebae from the genus Awerintzewia Schouteden, 1906 was discovered, as well as two rare species: Difflugia serbica Ogden and Zivkovic, 1983 and Difflugia biconvata Ertl, 1965 were for the first time recorded in the fauna of the Caucasus; their descriptions are given below.
Material and methods
In the summer of 2016, we had a chance to visit two high-mountain lakes — Lake Batabat
doi:10.21685/1680-0826-2018-12-1-3 © 2018 The Author(s)
Protistology © 2018 Protozoological Society Affiliated with RAS
Fig. 1. Location of Batabat Lake and Maralgol Lake in Azerbaijan.
(Nakhichevan AR) and Lake Maralgol (West Azerbaijan), where the samples were taken (Fig. 1). Brief characteristics of these water reservoirs are given below.
Batabat is a mountain lake in Azerbaijan, situated in the mountains of the Shakhbuz district of Nakhichevan along the right bank ofthe upper river of Nakhichevan-chay, west ofthe Bichenek passing. The lake is located at the altitude of2113 m above sea level, surrounded by alpine meadows, not far from the sources of the Kukuychay River (a tributary of Nakhichevan-chay). The lake is remarkable due to a floating peat island (Fig. 2).
Lake Maralgol is located in the Goygol region of Azerbaijan at the altitude of 1902 m a. s. l. The depth of the lake is 61.6 m, the length is 300 m, the width is 150 m, and the length of the coastline is 2282 m; the soil is sludgy. The lake feeds from three small rivers (Gasimov, 1972) (Fig. 2). The water transparency of the lake (Secchi depth) during the sampling period was 5.6 m.
Samples were taken from Batabat Lake (Shakhbuz distr., Nakhichevan AR) (N39°32'27.39"; E45°47'09.17"; 2120 m a. s. l.) and from Maral-gol Lake (Goygol district, West Azerbaijan) (N40°22' 39.11"; E46°18'52.41"; 1920 m a. s. l.) in July
Fig. 2. Batabat Lake (A, B), Nakhichevan AR and Maralgol Lake (C, D), Goygol district, Azerbaijan.
2016 (Fig. 1). Specimens were caught in micro-capillary tubes and studied in vivo and by means of the glycerol preparations. For scanning electron microscopy (SEM) the cells were transferred to a cover glass with micro-capillar tubes, dried and then coated with gold. The shell morphology was examined using a scanning electron microscope JEOL JCM-6000 operating at 5-15 kV. Statistics were calculated using the program Sigma Plot 12.5 (X: arithmetic mean; M: median; SD: standard deviation; SE: standard error; CV: coefficient of variation (%); Max: maximum; Min: minimum; N: number of specimens).
Descriptions and discussion
Amoebozoa Luhe, 1913, emend. Cavalier-Smith, 1998
Order Arcellinida Kent, 1880 Suborder Difflugiina Bovee, 1985 Family Diffflugiidae Wallich, 1864 Genus Difflugia Leclerc, 1815
Difflugia serbica Ogden and Zivkovic, 1983 (Figs 3, 4)
Description. Slides B1-B2. The shell ovoid with pointed fundus and short neck, rounded aperture. The shell is relatively large, laterally compressed. It is covered with a mixture ofsmall, large and flattened particles, forming the rough surface of the shell. The aperture is round, surrounded by the small and medium particles, with a small collar. Shell length 155—215 ^m, width 78—96 ^m, thickness 90—93 ^m, aperture diameter 41—56 ^m (Table 1). Our specimens differ from others by more rounded form and significantly smaller size of the aperture (Ogden and Zivkovic, 1983; Mazei and Tsyganov, 2006). Common species in the sample, found in the summer.
Distribution: former Yugoslavia (Ogden and Zivkovic, 1983; Ostojic et al., 2014), Belgium (Chardez, 1987), Bulgaria (Davidova et al., 2008; Todorov et al., 2008; Davidova, 2012; Davidova and Boycheva, 2015). In Azerbaijan this species was found in sediments of Batabat Lake (Shakhbuz distr., Nakhichevan AR). This is the first record of this species in the fauna of the Caucasus.
Difflugia biconvata Ertl, 1964 (Figs 5, 6)
Description. The shell egg-shaped, slightly flattened laterally with narrow equatorial area. Distal
Fig. 3. Difflugia serbica Ogden and Zivkovic, 1983, SEM photographs. A, F, J - Apertural view; B-E, G, I, K — broad lateral view; H — narrow lateral view; L — shell surface.
end is narrowed. The surface of the test is covered with a mixture of grains of sand, of varying size and shape. The aperture is round in shape, surrounded by fine grains of sand. Shell length 83.5—93.45 ^m, width 50.2—52.2 ^m, aperture diameter 20.3—21.7
^m (Table 2). Our specimens differs from other by more elongated form and significantly smaller size of the shell and aperture (Ertl, 1965; Mazei and Tsyganov, 2006). Common species in the sample, found in the summer.
Table 1. Biometric characteristics of Difflugia serbica Ogden and Zivkovic, 1983.
Character X M SD SE CV Min Max N
Length of the shell 186.500 184.00 17.335 5.482 0.092 155.0 215.0 10
Width of the shell 87.0 87.5 6.831 2.160 0.079 78.0 96.0 10
Thickness of the shell 92.2 93.0 1.229 0.389 0.013 90.0 93.0 10
Diameter of the aperture 47.2 46.0 4.849 1.533 0.103 41.0 56.0 10
Fig. 4. Basic morphometric characters of Difflugia serbica Ogden and Zivkovic, 1983. 1 — Length of the shell; 2 — diameter of the aperture; 3 — width of the shell; 4 - thickness of the shell.
Distribution: Slovakia (Ertl, 1965). In Azerbaijan this species was found in the sediments of Batabat Lake (Shakhbuz distr., Nakhichevan AR). This is the first record of this species in the fauna of the Caucasus.
Family Heleoperidae Jung, 1942 Genus Awerintzewia Schouteden, 1906
Awerintzewia minuta sp. n. (Figs 7—9) Diagnosis. The shell dorsally ovate form, laterally slightly compressed, covered by the mixture of fine quartz particles, idiosomes almost invisible under grains of sand. The base ofthe fundus covered with larger particles, and closer to the aperture of the test, the shell has a fairly smooth structure. Aperture is round, bordered by small particles, with small lateral notches. The diameter of the aperture is 11.4—12.6 ^m. Shell length 50.4—52.7 ^m, width 31.4—39.5 ^m (Table 3). Pseudopodia not observed. Awerintzewia minuta sp. n. differs from 2 known species of this genus by smaller cell size (Dekhtyar,
Fig. 5. Basic morphometric characters of Difflugia biconvata Ertl, 1965. 1 c Length of the shell; 2 — width of the shell; 3 — diameter of the aperture.
1994; Mazei and Tsyganov, 2006). Common species in the sample, found in the summer.
Ecology. This species was found in the sediments of Maralgol lake (Goygol district, Azerbaijan). Common species in the sample, found in the summer.
Type location. Azerbaijan, Goygol district, N40°22'39.11"; E46°18'52.41"; 1920 m a. s. l., July 2016.
Etymology. The species is named according to its morphology — the small cell size.
Haplotype. The type specimen is stored in the collection of Dr. N. Snegovaya (Slides M1-M3), Institute of Zoology NAS of Azerbaijan.
Related species — similarities and differences. Awerintzewia minuta sp. n. differs from 2 known species of this genus — A. cyclostoma (Schouteden, 1906) Penard, 1920 and A. levis by smaller cell size (Dekhtyar, 1994; Mazei and Tsyganov, 2006) (Table 4).
References
Chardez D. 1987. Contribution a la connaissance des Thecamoebiens des de potslacustres. Acta Protozool. 26, 59—62.
Davidova R. 2012. Biotopic Distribution
Table 2. Biometric characteristics of Difflugia biconvata Ertl, 1965.
Character X M SD SE CV Min Max N
Length of the shell 93.51 93.450 7.975 2.522 0.085 83.5 107.0 10
Width of the shell 51.61 51.90 0.694 0.219 0.013 50.2 52.2 10
Diameter of the aperture 21.58 21.7 1.022 0.323 0.047 20.3 21.7 10
Fig. 6. Difflugia biconvata Ertl, 1965, SEM photographs. A, E — Narrow lateral view; B, C, F — apertural view, D — broad lateral view.
of Testate Amoebae (Protozoa: Arcellinida and Euglyphida) in Ovcharitsa Reservoir (Southeastern Bulgaria). Acta Zool. Bulg. 64, 13—22.
Davidova R., Golemansky V. and Todorov M. 2008. Diversity and biotopic distribution of testate amoebae (Arcellinida and Euglyphida) in Ticha Dam (Northeastern Bulgaria). Acta Zool. Bulg. Suppl. 2, 7—18.
Davidova R. and Boycheva M. 2015. Testate amoebae fauna (Amoebozoa, Rhizaria) from the benthal of Kamchia Reservoir (Eastern Bulgaria). Acta Zool. Bulg. 67, 375—384.
Dekhtyar M.N. 1994. The new and rare species of testate amoebae of the families Arcellidae, Centropyxidae, Lesquereusiidae and Hyalosphe-niidae (Rhizopoda, Testacealobosia). Zool. Zh. (Moscow). 73, 3—14 (in Russian with English summary).
Ertl M. 1965. Zur Kenntnis der Testaceenfauna der slowakischen Reisfelder. Hydrobiologia. 26, 13-20.
Gasimov A.G. 1972. The freshwater fauna of the Caucasus. Baku, Science (in Russian).
Mazei Y.A. and Tsyganov A.N. 2006. Freshwater
Table 3. Biometric characteristics of Awerintzewia minuta sp. n.
Character X M SD SE CV Min Max N
Length of the shell 52.92 52.7 1.399 0.442 0.026 50.4 53.4 10
Width of the shell 38.47 39.5 2.817 0.891 0.073 31.4 41.2 10
Diameter of the aperture 13.04 12.6 1.304 0.412 0.1 11.4 14.3 10
Fig. 7. Awerintzewia minuta sp. n., SEM photographs: A, D, E, I, G, K — broad lateral view, C, F, H, J, L — apertural view, B — shell surface.
testate amoebae. Moscow, KMK (in Russian).
Ogden C.G. and Zivkovic A. 1983. Morphological studies on some Difflugiidae from Yugoslavia (Rhizopoda, Protozoa). Bull. Brit. Mus. Nat. Hist. (Zool). 44, 341-375.
Ostojic A.M., Radojevic I.D. and Rakic M.P. 2014. Updated checklist of freshwater free-living unicellular handerotrophic protists of Serbia. Acta Zool. Bulg. 66, 347-358.
Snegovaya N.Y. and Alekperov I.K. 2005. Fauna of testate amoebae of western Azerbaijan rivers. Protistology. 4, 149-183.
Todorov M., Golemansky V. and Blagovest T. 2008. Diversity and biotopic distribution of testate amoebae (Protozoa: Arcellinida and Euglyphida) in the Batak Reservoir (Southern Bulgaria). Acta Zool. Bulg. 60, 115-124.
Veysig S.Y. 1931. Goy-gol Lake. Hydrobiological Essay, Baku. pp. 3-46.
Chardez D. 1987. Contribution a la connaissance des Thé camoebiens des dé p ô tslacustres. Acta Protozool. 26, 59-62.
Davidova R. 2012. Biotopic Distribution of Testate Amoebae (Protozoa: Arcellinida and
Fig. 8. Basic morphometric characters of Awe-rintzewia minuta sp. n. 1 — Length of the shell; 2 — width of the shell; 3 — diameter of the aperture.
Euglyphida) in Ovcharitsa Reservoir (Southeastern Bulgaria). Acta Zool. Bulg. 64, 13—22.
Davidova R., Golemansky V. and Todorov M. 2008. Diversity and biotopic distribution of testate amoebae (Arcellinida and Euglyphida) in Ticha Dam (Northeastern Bulgaria). Acta Zool. Bulg. Suppl. 2, 7—18.
Davidova R. and Boycheva M. 2015. Testate amoebae fauna (Amoebozoa, Rhizaria) from the benthal of Kamchia Reservoir (Eastern Bulgaria). Acta Zool. Bulg. 67, 375—384.
Dekhtyar M.N. 1994. The new and rare species of testate amoebae of the families Arcellidae, Centropyxidae, Lesquereusiidae and Hyalosphe-niidae (Rhizopoda, Testacealobosia). Zool. Zh. (Moscow). 73, 3—14 (in Russian with English summary).
Fig. 9. Awerintzewia minuta sp. n., light microscope photographs. A-F — lateral view. Scale bars: 10 ^m.
Ertl M. 1965. Zur Kenntnis der Testaceenfauna der slowakischen Reisfelder. Hydrobiologia. 26, 13-20.
Gasimov A.G. 1972. The freshwater fauna ofthe Caucasus. Baku, Science. (In Russian).
Table 4. Diagnostic characters of species from the genus Awerintzewia Schouteden, 1906.
Characters A. minuta sp. n. A. cydostoma A. levis
Shell size, ^m, shell surface Length 50.4-53.4 ^m, width 31.441.2 ^m; shell of dorsally ovate form, laterally slightly compressed, covered by the mixture of fine quartz particles, idiosomes almost invisible under grains of sand. The base of the fundus covered with larger particles, and closer to the aperture of the test the shell has a fairly smooth structure. Length 135-180 ^m, width 120-132 ^m; shell large, of trapezoidal form, covered with large grains of sand. Length 168-192 ^m, width 120129 ^m; shell large, of ovoid form, flattened, incorrectly rectangular plates cover the shell, grains of sand singly occurred.
Aperture form and size, ^m The aperture is round, bordered by small particles, with small lateral notches, 11.4-14.3 ^m in diameter. The aperture is broadly oval with small lateral notches, the edge of the aperture consists of thin small plates, 40-52 ^m in diameter. The aperture relatively small, wide elliptic, with smooth margin, without lateral excisions.
References This paper Dekhtyar, 1994; Mazei and Tsyaganov, 2006 Dekhtyar, 1994; Mazei and Tsyaganov, 2006
Mazei Y.A. and Tsyganov A.N. 2006. Freshwater testate amoebae. Moscow, KMK (in Russian).
Ogden C.G. and Zivkovic A. 1983. Morphological studies on some Difflugiidae from Yugoslavia (Rhizopoda, Protozoa). Bull. Brit. Mus. Nat. Hist. (Zool). 44, 341—375.
Ostojic A.M., Radojevic I.D. and Rakic M.P. 2014. Updated checklist of freshwater free-living unicellular handerotrophic protists of Serbia. Acta Zool. Bulg. 66, 347—358.
Snegovaya N.Y. and Alekperov I.K. 2005. Fauna of testate amoebae of western Azerbaijan rivers. Protistology. 4, 149-183.
Todorov M., Golemansky V. and Blagovest T. 2008. Diversity and biotopic distribution of testate amoebae (Protozoa: Arcellinida and Euglyphida) in the Batak Reservoir (Southern Bulgaria). Acta Zool. Bulg. 60, 115-124.
Veysig S.Y. 1931. Goy-gol Lake. Hydrobiological Essay, Baku. pp. 3-46.
Address for correspondence: Nataly Yu. Snegovaya. Institute of Zoology NAS of Azerbaijan, AZ 1073, pr. 1128, kv. 504, Baku, Azerbaijan; e-mail: snegovaya@yahoo.com
