Micrasterias foliacea [var. foliacea] Bailey ex Ralfs, 1848

Levanets, Anatoliy & Janse van Vuuren, Sanet, 2023, Morphology, taxonomy, biogeography and ecology of Micrasterias foliacea Bailey ex Ralfs (Desmidiales, Zygnematophyceae), PhytoKeys 226, pp. 33-51 : 33

1. Micrasterias foliacea [var. foliacea] Bailey ex Ralfs, 1848

Micrasterias foliacea [var. Micrasterias foliacea foliacea ] Bailey ex Ralfs, 1848. "The British Desmidiaceae ": 210, tab. 35, fig. 3.

Synonyms.

M. foliacea Bailey in lit. cum icone 1847; M. foliacea Bailey ex Ralfs f. α typica Turner, 1892. " Algae Aquae Dulcis Indiae Orientalis": 94, tab. 6, figs 12-14; M. foliacea Bailey ex Ralfs var. granulifera J.A. Cushman, 1908. “Rhodora” 10(114): 111.

The earliest description of M. foliacea var. granulifera by Cushman (1908) is doubtful, and no drawings or micrographs were provided. Cushman (1908) indicated that var. Micrasterias granulifera granulifera is similar to the type, but in addition the surface is covered with large irregularly disposed granules. Later, Krieger (1939) classified this variety as a synonym of the type variety, which is currently accepted.

Morphology.

Fig. 1 illustrates the morphology of M. foliacea var. foliacea found in the Mozambique samples. It is the only species of Micrasterias where the cells are permanently attached to each other to form a ribbon-like chain, which may consist of 2-100 cells. The cells are nearly square (sub-quadrate) with deep constrictions at the sinus. Each semicell is sub-divided into three lobes, two of which are lateral and the third apical (polar). The lateral lobes are further sub-divided into smaller lobes and lobules by means of incisions of various depths. The polar lobes are narrow with a pair of pointed extensions at each end. The polar extensions interlock where neighbouring cells are attached to each other. The cells are 70-80 µm in length and 65-80 µm wide (isthmus 13-16 µm). The morphology of specimens in our samples corresponds to the original description by Ralfs (1848) and later descriptions, such as those provided by Kim (2013) and Ribeiro et al. (2015).

A description of Ling and Taylor (2000) of a form of M. foliacea recorded from the Northern Territories in Australia indicated a simpler form with less divided lateral lobes and one, instead of the usual two, triangular process on the face of the polar lobe. Cell length without processes was 66-67 μm, and with processes 91-95 μm; width was 102-109 μm; apex 38-43 μm and isthmus 14-15 μm.

Distribution.

A map, illustrating the geographical distribution of M. foliacea , is presented in Fig. 2 . This figure shows that variety Micrasterias foliacea (type) is widely distributed, being present on most continents. It is, however, only recorded from the eastern side of North America and, surprisingly, it is completely absent from European countries. Palamar-Mordvintseva (1984) speculated that this species can possibly be found in future in the rice fields of southern Ukraine, but according to the general known distribution of this species it is doubtful that this statement is true. A detailed list, with references, of all localities where this variety was found is presented in Suppl. material 1.

Habitat and ecology.

From intensive literature searches it is clear that the habitats of free-living M. foliacea are exceptionally diverse. It can be found in plankton and periphyton of a variety of different lentic and lotic water bodies. Lentic (stagnant) water bodies include wetlands, marshes, various types of swamps (e.g., peat swamps) and ponds (including irrigation and oxidation ponds, rainwater ponds, rock ponds, fishponds, and small ponds in botanical gardens), reservoirs, deltas, floodplains, lagoons and lakes (including crater lakes), flooded savannahs and meadows, and in ditches associated with paddy (rice) fields. It is most common in small and shallow (<1 to 2 m) ponds, but it was also occasionally found at the embankments of larger standing water bodies, e.g., Lake Laguna de Bay in the Philippines (4-6 m deep; Behre 1956). Lotic habitats include cobbles, streams, rivers, and irrigation canals. In addition, it was also recorded from a tropical estuarine mangrove swamp in Nigeria with high conductivity levels (Table 1 ; Ubong et al. 2017). In these habitats, it often occurs between floating algal masses. In terrestrial habitats it may be found amongst moist mosses, growing on the surface of rocks, or inhabiting wet soils.

Besides being free-living, it can also be found as epiphytes on aquatic plants ( Jena and Adhikary 2011). It is frequently found living on Utricularia species, such as U. flexuosa ( Lütkemüller 1900; Turner 1892) and U. fasciculata ( Turner 1892). It was also found on leaves of Hymenachne amplexicaulis ( Salazár Pereira 1991; Salazar 2006/2007) and the stems and roots of submerged Ipomaea reptans ( Bourrelly 1975). It was common in samples that were obtained when the roots of Eichhornia crassipes , Pistia stratiotes , Salvinia molesta and submerged aquatic macrophytes were squeezed out ( Bicudo and Sormus 1982; Rai et al. 2008; Paudel 2017). The species was also found in the stomachs of catfish Synodontis schall and S. nigrita ( Lalèyè et al. 2006).

A variety of aquatic plants inhabit waters in which M. foliacea var. foliacea was found. Shallow water was often dominated by species of Nymphaea and Utricularia ( Schumacher 1956; Thomasson 1966; Ratnasabapathy and Kumano 1974; Turner 1892; González 2009). Other dominant species include those of Pistia and Salvinia ( Ngearnpat et al. 2008; González 2009). In deeper waters Brasenia schreberi , Cabomba caroliniana , Nuphar orbiculata , Nymphaea odorata and Utricularia purpurea were common ( Schumacher 1956). During the current study Nymphaea dominated the macrophyte community at the sampling site in Botswana.

The abundance of M. foliacea var. foliacea may range from extremely rare, present in low to moderate quantities ( Behre 1956) or it may be common ( Scott and Prescott 1961; Prowse 1969; Kadiri and Opute 1989; Kadiri 2002; Islam and Ifranullah 2006). Other authors described it as abundant ( Kim 2014), or sometimes dominant ( Medvedeva 2007; Ekhator et al. 2013).

Variety Micrasterias foliacea can be found in a wide pH range and a literature overview, presented in Table 1 , shows that it is present in both acidic (min pH 4.7; Malaysia), as well as alkaline waters (max pH 8.3; India). Results from the literature review contradict a finding made by Prescott and Scott (1943) who stated that the acidity of water in which M. foliacea grows, varies between pH 5.8 and 6.4 (rarely as high as 6.8), and that this species’ distribution is so specifically related to the chemistry of the water that it can be used as an indicator organism for soft and highly acid waters. After the study of Prescott and Scott (1943) the species was frequently recorded in waters with pH values around 8 (Philippines, India, Nigeria, USA; see Table 1 ), indicating that it can also tolerate and thrive in alkaline waters and that it is thus not suitable as an indicator organism. Table 1 also indicates alkalinity ranges of water in which the species was recorded and, in accordance with the findings of Förster (1982), several published results show that it is usually found under neutral to alkaline conditions.

It was found in both winter ( Islam and Ifranullah 2006) and summer ( Thomas et al. 2003; Prasertsin and Peerapornpisal 2018) seasons throughout the world. In India it was found during pre-monsoon, monsoon, post-monsoon and winter seasons ( Kalita et al. 2016). Water temperature ranged between a minimum of 8 °C (India) and a maximum of 35 °C (Guinea), although it was most frequently recorded in moderate to high water temperatures, ranging from 23-27 °C (Table 1 ).

Typical conductivity levels of freshwater are below 1 500 µS /cm, while typical sea water has a conductivity value of about 50 000 µS /cm. M. foliacea was usually found in freshwater with relatively low conductivity values (<327 µS /cm; Table 1 ), but cells were also found in some estuaries, archipelagos and marine waters ( Chung et al. 1965; McAlice 1975; Opute 1992; Kadiri 2002; Li et al. 2011; Ecology and biodiversity of Lower Ganga River basin 2012; Silveira 2012; Opute and Kadiri 2013; Dayala et al. 2014; Mama et al. 2016; Ubong et al. 2017). Average conductivity values in the tropical estuarine mangrove swamp (Nigeria) in which it was found by Ubong et al. (2017) was in the order of 50 000 μS /cm, showing its ability to survive in saline water. It is, however, suspected that its presence in estuaries and oceans may be the result of outflows from the rivers.

Table 1 shows nutrient ranges (phosphate-phosphorus, nitrate-nitrogen) of water in which M. foliacea was recorded. Based on these nutrient concentrations, it was mostly found in oligotrophic to slightly mesotrophic water ( Kim 2014; Ali et al. 2016).

Dissolved oxygen concentrations ranged from 1.7-8.0 mg/L in water in which M. foliacea was recorded. It was mostly found in low turbidity (high transparency) waters ( Williamson and Marazzi 2013; Ali et al. 2016; Ubong et al. 2017; Prasertsin and Peerapornpisal 2018). However, in Thailand it was found in muddy, pale yellow-brown water with transparencies less than 1 m ( Hirano 1975) and in the middle reaches of the Niger River in Mali it was found in polluted, cloudy, muddy water having a sandy substrate ( Couté and Rousselin 1975).

Figures

Figure 1. Morphology of M. foliacea var. foliacea found in samples from Mozambique A six cells illustrating chain formation B two adjacent cells indicating the interlocking polar extensions C morphology of a single cell. Scale bars: 30 µm.

Figure 2. Worldwide distribution of different varieties of Micrasterias foliacea.