Diversity and distribution of testate amoeba (Testaceae) in the moss Pleurozium schreberi

Ingrida Satkauskienė,

Jurgita Rutkauskaitė-Sucilienė

Vytautas Magnus University, K. Donelaičio St. 58, 44248 Kaunas, Lithuania

Testate amoebae are worldwide-distributed protists living in soils, freshwaters, and wetlands, but their presence and diversity in Lithuania are poorly known. The published information mainly reflects collections from freshwater, meanwhile knowledge about the diversity of these protozoa in bryophytes remains limited. To overcome this limitation, a study was conducted on the moss Pleurozium schreberi by sampling it from several localities to provide information on the distribution of testate amoebae and the composition of the species. In this study, 19 species of testate amoebae were recorded. The species richness varied from six to 15 species per sample. The most frequently occurring testate amoebae were eurybiont species Corythion dubium, Trinema enchelys, Euglypha strigosa, Centropyxis aerophylla-complex, and Euglypha laevis. The most diverse genus was Euglypha (five species). The  peculiarities of habitats and environmental contamination are possible factors that determined the character of the composition and structure of testate amoebae communities. These data help to improve knowledge of the geographical distribution of testate amoebae in eastern Europe and their diversity in Lithuania.

Keywords: testates, amoebae, indicators, moss, Pleurozium

INTRODUCTION

Testate amoebae (TA) are unicellular protozoans enclosed in a test and living in various aquatic ecosystems (Beyens, Meisterfeld, 2001; Smith et al., 2008); they also inhabit soils, Sphagnum, and other mosses (Sandon, 1927; Warner, 1987).

Testate amoeba communities play an important role in regulating the  microbial food web structure (Gilbert et al., 1998a; Lamentowicz et al., 2013; Meyer et al., 2013). A characteristic feature of TA is the shell consisting of inorganic or organic particles, usually containing the species-specific character, and providing protection against unfavourable environment. The shells of TA preserve well in sediment and can indicate a wide variety of environmental conditions. In addition, a short life cycle, abundance in the environment, worldwide distribution, sensitivity to environmental conditions, and rapid generation times renders TA adequate bioindicators (Charman, 1997; Booth, 2001; Patterson, Kumar, 2002; Nguyen-Viet et al., 2007; Mitchell et al., 2008). As one of the most common terrestrial living environments of TA, mosses are well known bioaccumulators and are used in air quality biomonitoring studies (Aceto et al., 2003). Lacking the roots, moss absorbs water and nutrients, including pollutants, from the atmosphere. Their leaves do not possess a foliar cuticle or thick cell walls as natural barriers. Moreover, the  configuration of moss tissues and its cell organisation assure a  high surface/mass ratio and a  direct exposure to the external environment and, hence, to pollutants. The monitoring of the air quality by using moss together with its inhabitants TA could be an eco-friendly method for obtaining qualitative and quantitative data (Freitasa et al., 2022). On the other hand, it is known that moisture is often identified as the most important factor controlling the composition of the testate amoebae community (Mitchell  et  al., 2000; Booth, 2002; Kishaba, Mitchell, 2005; Bobrov  et  al., 2013). Less known are the environmental factors - openness of habitats, pH, shadow, type of soil, or pollution - that have a greater impact on TA communities. Taking this into account, it is evident that a deeper understanding of the diversity and distribution of moss microfauna is a prerequisite for the use of microfauna in environmental monitoring. This study was focused on the investigation into the composition and diversity of TA communities and their distribution in the  moss Pleurozium schreberi (Brid.) Mitt., sampled in clean and polluted habitats.

MATERIAL AND METHODS

Study area

Lithuania is in the  eastern part of Europe on the coast of the Baltic Sea in the temperate climatic zone (56°00'N and 24°00'E). Moss was sampled in the central part of Lithuania, dose to the  largest cities Vilnius and Kaunas. Presumably polluted sites were chosen along motorways with intensive traffic, while clean sites for sampling were selected in parks and forests located far away from pollution (Table 1).

Table 1. The sites and location of moss (Pleurozium schreberi) sampling and the pH of the measured samples

Sites of moss sampling Location latitude/longitude Comments on sampling site pH of moss
11 Motorway Vilnius-Utena (A14) 55°06’46.4”N
25°22’44.6”E
The motorway A14 (Vilnius-Utena) is characterised by intensive traffic (more than 5988 vehicles per day according to road transport analysis in 2018). Moss was sampled from the ground 2 m from the highway. 7.1
22 Verkiai Regional Park (Vilnius) 54°45’37.7”N
25°18’24.3”E
More than 76% of the park area is covered by the mix of pine trees and deciduous trees. Sandy soil was dry in the sampling site. 6.73
33 A street in Verkiai Regional Park 54°45’09.7”N
25°17’48.9”E
Žaliuju ežeru Street crosses Verkiai Regional Park. Traffic is not very intensive. Biotopes on roadsides are similar to those in the whole of the park. Moss was sampled from the roadside (0.5 m). 6.35
44 Trakai National Park (Trakai region) 54°39’34”N
24°54’13”E
Pines with a mix of deciduous trees (the northern part of the park). Soil moist, fertile. 6.4
55 Road Vievis-Trakai (No. 107) 54°40’07.9”N
24°54’29.9”E
Road Vievis-Trakai crosses Trakai National Park (traffic intensity about 3000 vehicles per day). Moss sampled from the ground in the 15th km. 6.5
66 Sereikiskiai Park (Vilnius) 54°41’0”N
25°17’49”E
The Park is composed of a mix of deciduous and pine trees (Pinus silvestris, Betula pendula, Picea abies, Populus tremula). 6.39
77 Pilénai Forest (Kaunas region) 54°57’32.0”N
24°01’17.0”E
Pinewood with a mix of deciduous trees Pinus silvestris, Betula pendula, Picea abies, Populus tremula, Alnus glutinosa, Fraxinus sp.). 6.7
88 Motorway Kaunas-Daugavpils (A6) 54°58’43.5”N
24°05’24.7”E
Traffic intensity about 27,719 vehicles per day. Moss sampled from beside Pilénai forest, in the 11th km. 6.63
99 Pine forest (Kaunas region, Radikiai) 54°57’21.0”N
23°58’27.8”E
Moss was sampled in a pine forest with a mix Sorbus aucuparia, Quercus sp. Soil sandy loam. 5.8

Laboratory procedures

Two moss samples from the each of the nine sites were collected in September-October 2018 from the ground (approximately 3 g of moss at each site). All sampling data are presented in Table 1.

Before analysis, moss samples were stored at the temperature of 4°C. Later 2 g of moss were used to measure pH using the Mettler Toledo SevenMulti pH meter S40-K (Sigma-Aldrich, Germany).

The mosses (1  g) were chopped finely by scissors and covered with distilled water. After 1-2 min. of intensive shaking in a jar with a  lid (for separation of testate amoebae from the moss), the moss was squeezed and filtrated through the  planktonic sieve. The  filtrate was concentrated with a  centrifuge at 1500  rpm for 2 min. The supernatant was removed and the debris was analysed with a compound microscope (BM2000) equipped with a  digital camera (Moticam 3.0 MP). No fewer than 150 specimens of live individuals and empty shells were counted in each sample and identified at 100×, 400× magnifications. The  obtained values of the number of amoebae were evaluated in 1 g of the substrate. Identification of specimens was based on the  keys of Ogden, Hedley (1980), Patterson, Headley (1992), Charman et al. (2000), and Clarke (2003).

Numerical analyses

The diversity and distribution of testate amoebae were evaluated using relative abundance of species (pi), species richness (S) and Shannon-Wiener's (H) index (Magurran, 2004). The relative abundance of species (pi) was calculated by the formula:

pi = ni/N × 100%

where ni is the number of individuals of a testate amoebae species found in the studied sample, N is the total number of all individuals. Species that had pi > 5% were considered as dominant.

The Shannon index (H) measures the diversity of a species in a community and is calculated thus:

H = -Σpi * ln(pi)

where p is the proportion (n/N) of individuals of one species found in community (n) divided by the total number of individuals found (N).

The Simpson index (D) is a dominance index as it gives more weight to common or dominant species:

D = 1 - ∑ni (ni - 1)/N (N - 1)

where n is the number of individuals of each species and N is the total number of individuals of all species.

RESULTS AND DISCUSSION

Overall results: species composition

A total of 19 taxa were found in the 18 samples analysed (Table 2). Species Hyalosphenia papilio and Amphitrema flavum were represented by few individuals found in the moss from beside the road Vievis-Trakai, which were only included in the general list of species but not analysed further. Some amoebas from the genus Euglypha and Nebela tincta species complex were identified only to the  genus level. The taxa of Nebela collaris-tincta group and Tracheleuglypha dentata were considered occasional, occurring in one to two sampling sites. The dominant species in the moss Pleurozium schreberi were Corythion dubium (21.15%), Trinema enchelys (20.34%), Euglypha strigosa (16.46%), Centropyxis aerophila-complex (11.40%), and Euglypha laevis (10.77%). The genus Euglypha was represented by five species.

Table 2. Diversity and abundance (relative abundance) of testate amoebae in different localities of Lithuania

Localities Taxa Pine forest (Radikiai) Sereikiskiai Park Pilénai forest Trakai National Park Verkiai Regional Park Vievis- Trakai road Street in Verkiai Regional Park Motorway Kaunas-Daugavpils Motorway Vilnius-Utena
N(pt)
Assulina muscorum Greeff, 1888 164 (23.1) 5 (0.56) 46 (9.27) 155 (1.61) 8 (1.48) 82 (7.79)
Centropyxis aerophile-complex 49 (6412.90) 123 (16.83) 137 (15.44) 64 (12.88) 39 (4.83) 58 (10.78) 30 (2.85) 57 (22.8) 5 (1.92)
Cyclopyxis eurystoma Deflandre, 1929 59 (8.31) 52 (7.11) 78 (8.79) 55 (11.06) 12 (1.48) 7(1.30) 23 (2.186) 36 (14.4) 4 (1.53)
Arcella vulgaris Ehrenberg, 1830 11 (1.50) 5 (1.01)
Galeripora arenaria (Greeff, 1866) (Gonzalez-Miguéns et al., 2021) 10 (1.13) 3 (0.60) 13 (1.61) 7(1.30) 7 (0.66) 17 (6.80)
Neb da collaris-tincta group 36 (7,51)
Nebela collaris (Ehrenberg, 1848) 8 (1.61)
Corythion dubium Taranek, 1871 284 (49.85) 60 (6.76) 66 (13.28) 420 (52.10) 24 (4.46) 188 (17.87)
Corythion pulchellum Penard, 1890 (? ) 12 (1.69)
Difflugia sp. Leclerc, 1815 9 (1.27) 9 (1.23) 23 (2.59) 10 (2.01) 14 (2.60)
Euglypha sp. (E. citiate?) Genus Euglypha Dujardin, 1841 45(6.19) 22 (8.43)
Euglypha strigosa (Ehrenberg, 1848) 62 (8.73) 312 (42.68) 60 (6.76) 100 (20.12) 65 (8.06) 73 (13.57) 135 (13.21)
Euglypha laevis (Ehrenberg, 1845) 26 (3.66) 82 (11.22) 93 (10.48) 30 (6.03) 142 (17.61) 78 (14.50) 80 (7.60)
Euglypha tubercolata Dujardin, 1841 22 (3.01) 40 (15.32)
Euglypha compressa Carter, 1864 4 (0.80) 27 (5.02)
Euglypha sp. 80 (9.02) 120 (48)
Trinema complana-tum Penard, 1890 120 (16.41) 13 (1.46) 6 (1.21) 47 (5.83) 106 (10.07) 10 (3.83)
Trinema lineare Penard, 1890 5(2) 30 (11.49)
Trinema enchelys (Ehrenberg, 1838) 195 (21.98) 55 (6,82) 191 (35.5) 397 (37.74) 15(6) 150 (57.47)
Trinema galeata (Penard, 1890) Jung, 1942 133 (14.99) 51 (10.26) 45 (8.36)
Tracheleuglypha dentata 13 (2.62) 6 (1.12)
Total abundance 710 731 887 497 948 538 1048 250 261
Species richness S 9 8 12 15 9 12 9 6 7
Dominance_D 0.76 0.74 0.86 0.88 0.74 0.81 0.78 0.69 0.3762
Shannon index_H 1.72 1.61 2.17 2.32 1.68 1.97 1.78 1.39 1.328

Diversity and distribution of testate amoeba (Testaceae) in the moss Pleurozium schreberi

Note: Relative abundances exceeding 5% are in bold. The integral characteristics are given per one microbiotope (sample) on average.

However, it should be kept in mind that, due to the cryptic taxa and adaptive polymorphism, taxonomic uncertainty is valid for some taxa of TA listed below (Schönborn, 1992; Mulot et al., 2017; Bobrov, Mazei, 2004; Roland et al., 2017). Thus, it is possible that Corythion dubium identified in this study may represent not just one but several taxa. The abundance of Trinema enchelys presents a similar case: its abundance identified in this work can be shared with very similar T. lineare (Roland et al., 2017).

A complete list of taxa is presented in Table 2.

All testate amoebas found are mostly registered eurybionts living in soils, moss, and ponds (Chardez, 1967; Mazei, Belyakova, 2011; Mieczan, Adamczuk, 2015; Souto et al., 2021). Testate amoebae of the families Trinematidae and Euglyphidae prevailed in the moss Pleurozium schreberi. They represented typical soil testate amoebae communities (Bobrov et  al., 1999; Mitchell et al., 2008). TA identified as Centropyxis aerophila complex (Foissner, Korganova, 2000) was the most frequent taxa in the moss Pleurozium schreberi in all investigated sites. The taxa of the  genus Nebela, which usually are inhabitants of Sphagnum (Gilbert, Mitchell, 2006), were found in moss Pleurozium schreberi as well, but only in habitat, covered by mixed forest (Trakai National Park) and containing humid and fertile soil.

Distribution and diversity of testate amoebae in polluted and clean sites

Species richness of testate amoebae in moss P.  schreberi varied from 6 to 15. The  highest richness (15 species) was established in the samples of Trakai National Park, meanwhile the samples collected beside the Vilnius-Utena motorway were represented only by six taxa.

Sixteen species (and three groups of testate amoebae identified to the genus level) of testate amoebae were found in clean sites. The following seven species dominated (constituted >5%) here: Corythion dubium (21.99%), Euglypha strigosa (15.87%), Centropyxis aerophila-complex (10.91%), Euglypha laevis (9.88%), Assulina muscorum (9.80%), Cyclopyxis eurystoma (6.78%), and Trinema enchelys (6.62%).

Fourteen species (and two groups of testate amoebae identified to the  genus level) of testate amoebae were found in the moss in polluted sites. The composition of the taxa of testate amoebae was similar to that of clean sites, but the prevalence of the species was different (Fig. 1).

For example, Corythion dubium constituted 21.98% in the  moss of clean sites, meanwhile their abundance decreased almost by half in contaminated moss and constituted only 10.10%. Trinema enchelys composed 6.62% in clean sites, and dominated (35.90%) in contaminated sites. In agreement with other authors (Nguyen-Viet et al., 2008; Mieczan, 2009; Qin et  al., 2016; Heinemeyer, Swindles, 2018; Freitasa  et  al., 2022), Corythion dubium and Trinema enchelys occur in sites contaminated with heavy metals.

The Shannon diversity index varied from 1.39 to 2.32, with the  highest value in Trakai National Park and the  lowest (H = 1.39) in the  moss collected beside the  motorway Vilnius-Utena with intense traffic (Table 2, Fig. 2).

The obtained results are in agreement with other authors who report that TA diversity was lower in the most polluted places with higher concentrations of Cu, Pb and Zn (Wanner et al., 2020; Payne, 2010; Nguyen-Viet et al., 2007).

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Fig. 1. The distribution of testate amoebae (pi, %) in the moss Pleurozium schreberi in clean and polluted sites

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Fig. 2. Diversity of testate amoebae in the moss Pleurosium schreberi in clean sites and beside motorways

Environmental acidity impacts TA diversity and distribution (Charman, Warner, 1992; Booth, 2002; Mitchell  et  al., 2000 Lamentowicz, Mitchell, 2005), but in this study, pH of the moss was quite similar in all sites, and thus it did not have a decisive impact on diversity. Rather, it is possible that the  variation of diversity in the communities of testate amoebae were determined by the fertility of the soil and the humidity level, which is closely related to the site being open or hidden in shadow. Obviously, the canopy of trees in Trakai National Park creating shadow for the  moss helps to maintain humidity, while fallow leaves fertilise the soil. These conditions create a suitable habitat for the moss and its inhabitants, testates amoebae. Simultaneously, the shadowless habitats on the roadsides, with fluctuating humidity and contaminated by heavy metals, could have been an important factor determining lower richness and diversity of TA species.

CONCLUSIONS

This study describes for the first time the peculiarities of the communities of testate amoebae that form in moss Pleurozium schreberi biotopes in central Lithuania. All testates amoebae found are eurybionts. The values of the indices of species diversity and richness in polluted sites were lower than in clean sites. The possible factors that determine the diversity and structure of testate amoeba communities in moss include forest covering, properties of soil, and pollution of the habitats with heavy metals.

Received 17 July 2022

Accepted 18 August 2022

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* Corresponding author. Email: ingrida.satkauskiene@vdu.lt

Ingrida Satkauskienė, Jurgita Rutkauskaitė-Sucilienė

KIAUTINIŲ AMEBŲ (TESTACEAE) ĮVAIROVĖ IR PASISKIRSTYMAS SILSAMANĖJE (PLEUROZIUM SCHREBERI)

Santrauka

Kiautinės amebos (Testaceae) yra visame pasaulyje paplitę protistai, gyvenantys dirvoje, gėluose vandenyse, pelkėse, samanose ir kerpėse, tačiau jų įvairovė ir pasiskirstymas Lietuvos buveinėse tirtas mazai. Daugiausia paskelbta informacijos apie gėlame vandenyje gyvenančias kiautines amebas, o zinios apie sių pirmuonių įvairovę samanose yra ribotos. Samanos, gebančios akumuliuoti įvairias medziagas is aplinkos, yra zinomos ir naudojamos kaip bioindikatoriai aplinkos monitoringuose. Kiautinės amebos, gyvenančios samanose, taip pat galėtų būti panaudotos kaip indikatoriai, tačiau iki siol nėra aisku, kokie aplinkos veiksniai daro poveikį kiautinių amebų pasiskirstymui ir įvairovei. Sio tyrimo metu, siekiant nustatyti kiautinių amebų rūsinę sudėtį, įvairovę ir pasiskirstymą, buvo surinkti silsamanės (Pleurozium schreberi) mėginiai is kelių vietovių (svarių ir salia magistralinių kelių). Is viso surasta 19 kiautinių amebų taksonų, o mėginiuose taksonų (rūsių) skaičius svyravo nuo 6 iki 15. Dazniausiai pasitaikė sios kiautinės amebos eurybiontų rūsys: Corythion dubium, Trinema enchelys, Euglypha strigosa, Centropyxis aerophylla rūsių kompleksas ir Euglypha laevis. Euglypha gentis buvo įvairiausia ir atstovaujama penkių rūsių. Buveinių ypatumai ir aplinkos uzterstumas gali turėti įtakos kiautinių amebų bendrijų sudėčiai ir pasiskirstymui.

Raktazodziai: kiautiniai, amebos, indikatoriai, silsamanės, Pleurozium