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. 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.

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).

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.

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.

A map, illustrating the geographical distribution of M. foliacea, is presented in Fig. 2. This figure shows that variety 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.

Figure 2. 

Worldwide distribution of different varieties of Micrasterias foliacea.

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 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).

M. foliacea Bailey ex Ralfs var. β Wallich, 1860. “Annals and Magazine of Natural History” Series 3, 5: 280, tab. XIV, figs 1–4; M. foliacea Bailey ex Ralfs f. β elongata Turner, 1892. “Aquae Dulcis Indiae Orientalis”: 94.

This variety was originally described by Wallich (1860) as “var. β”. A later study by Turner (1892) revealed the same alga, but he described it as “forma β elongata”. In his monograph, Krieger (1939) indicated the same algal species as “var. elongata Turner”.

The prominent feature of M. foliacea var. elongata is the largely developed, triangular terminal lobe, with an outward directed base, emarginate at its angles and centre and furnished with two short stout teeth placed obliquely to each other (comparable to that of M. baileyi). The central emargination of this lobe is deep and rectangular and the entire lobe projects very slightly beyond the apices of the lateral lobes. The margins of the filament are parallel and direct, the fronds tabular, and divided by a very deep constriction into two dichotomously incised segments, the ultimate subdivisions of which are emarginate. In the Bengal variety, the teeth-like projections next to the terminal lobe are acutely angular, instead of being rounded and, as in the case of Onychonema, the projecting processes, by which cohesion is either secured or increased, overlap each other alternately in adjacent fronds. The cell length is 85–90 μm, width 70–75 μm, width of isthmus 11–13 μm, width of apex 32 μm, width of polar lobes 15 μm (Wallich 1860; Turner 1892).

This variety seems to be endemic to southeastern tropical Asia (Lower Bengal, India; Fig. 2 and Suppl. material 2), where it was found in the 1800’s by Wallich (Wallich 1860). A single record of this variety from Sierra Leone (Woodhead and Tweed 1958; Suppl. material 2) is doubtful, because descriptions and illustrations of the cell morphology, as well as information about the sampling site, are absent.

No information is available in the literature about the habitats or ecology of this variety.

This variety differs from the type by the presence and distribution of warts, situated in a row from the isthmus to half the length of the sinus. There is also a wart on the basis of the upper side lobes. Cells are 120–124 μm long, 115–120 μm wide, polar lobes are 53–57 μm wide, isthmus is 20–22 μm wide (Zalocar de Domitrovic 1981).

The variety is endemic to South America and was only found in tropical areas of Argentina (Fig. 2 and Suppl. material 2 for more information).

M. foliacea var. multiornata was found in a wetland for which no ecological data is available.

PhycoBank registration: http://phycobank.org/103725.

Nodular cell wall thickenings are unique morphological features of this variety and therefore it is proposed to raise taxonomical status of this form to the variety.

This taxon was described by Karl Behre (1956) as “forma nodosa” based on cell morphology – it differs from the type by the presence of nodular wall thickenings. Usually, thickenings are located on the inner corners and opposed points of adjacent lobes. Sometimes adjacent lobes are connected by ridge-like thickenings. It was noted that this variety is not a teratological form, because similar wall thickenings were found in numerous cells collected in several sites. Also, no transitional forms were seen between the nodular and the typical forms and the two forms occurred side by side in some samples. Dimensions: 70–74 x 80 μm, isthmus 16 μm.

Variety nodosa was rarely encountered, and only recorded from a few islands in Indonesia and the Philippines (southeastern Asia; Fig. 2 and Suppl. material 2 for more information).

In all cases M. foliacea var. nodosa were found in lake environments. In the Philippines the water bodies were characterized by clear water, covered by plants, containing detritus and other remains of higher plants. In Indonesia it was recorded from a crater lake (Suppl. material 2). No data on physico-chemical environmental variables was present for these water bodies.

Islam and Begum (2004) published a paper on Micrasterias Agardh from selected areas of Bangladesh and described a new variety of M. foliacea (var. spinosa). This varietal designation was invalid and was not designated in accordance with Art. 40.6 of ICN (Turland et al. 2018). In addition, the varietal name “Micrasterias foliacea var. spinosa Islam & Ashrafi” was invalid as Micrasterias foliacea var. spinosa Levanets and Guiry (2021) had priority. A new name, in honor of National Professor of Bangladesh, Abul Khayer Mohammed Nurul Islam, was therefore proposed for this variety (Levanets and Janse van Vuuren 2023).

This variety differs from the type because there are numerous spines on the cell wall. The cell wall is covered with many stout, curved spines, unequal in size. The incision between the lobes is usually wide open. Cell length 33–76 μm, width 34.5–77 μm, isthmus 5.0–11.5 μm (Islam and Begum 2004).

M. foliacea var. nurulislamii was found only once in Bangladesh (Suppl. material 2).

It was found in a ditch. No ecological information is available.

Each semicell is rectangular and the cell wall bears one to three small spines along the sinus, as well as on the upper margin of the upper lateral lobe near its base and the lower margin of the lower lateral lobes near the isthmus (Kim 2013, 2014). The presence of the spines on the upper and lower margins of the lateral lobes, as well as the incision which separates the polar lobe, is regarded as the major difference between this variety and the type (Nordstedt 1869; Zalocar de Domitrovic 1981).

In Asian specimens of both the specific form and var. ornata a peculiar phenomenon, never seen in any American specimens, was observed. This is a warping of the surface of the filament, resulting in the twisting of the side (edge) view of the chains into a sinusoidal curve which is sometimes quite pronounced. It is caused by the curving and dishing in opposite directions of the right and left lateral lobes of one semicell, those of the other semicell being curved and dished in the reverse manner (Scott and Prescott 1961). Illustrations of these twisting of the chains can be found in Scott and Prescott (1961).

Although variety ornata is less widespread than var. foliacea, it is also widely distributed throughout the world. Similar to the type, it was not recorded anywhere in Europe and in North America it was only recorded from northwestern Canada and two eastern states of the USA. It is more abundant in South America, Africa, and Asia and it was also recorded from Australia. The distribution of var. ornata is illustrated in Fig. 2 and more details regarding its patterns of distribution are presented in Suppl. material 3.

Variety ornata was recorded from a wide range of different ecological niches – it was found in different types of freshwaters, both standing (rainwater pools, rock ponds, rice fields, reservoirs, lakes, swamps, wetlands, flooded savannahs and lagoons) and flowing (creeks, moderate to rapidly flowing rivers). It was growing on the leaves of Hymenachne amplexicaulis (Poaceae) by Salazár Pereira (1991) and Salazar (2006/2007). It was also found in a coastal area in Nigeria (Kadiri 2002).

According to Kim (2013) this variety occurs mostly in oligo-mesotrophic, neutral-alkaline water bodies. The variety had a rare abundance in a natural oligotrophic pond on Jeju Island (South Korea), with pH ranging between 6.1 and 7.5 and conductivity between 44 and 108 μS/cm (Kim 2014). In Venezuela it was found in a flooded savannah which was acidic, with a low salinity and a high biomass of macrophytes (Salazár Pereira 1991; Salazar 2006/2007).

M. foliacea var. quadrinflata differs from the type in having two large, prominent semi-ellipsoidal hollow swellings at the base of the lateral lobes, each bearing a long spine at the narrow ends. In addition, there may or may not be, four other long spines on each semicell, two adjacent to each of the swellings. Cells are 69–72 μm long and 63–72 μm wide. The isthmus is 12 μm wide and the teeth are 15–18 μm long (Scott and Prescott 1961).

The distribution of this variety is plotted in Fig. 2 (with more detailed information in Suppl. material 2). It is limited to the Hindustan and Indochina peninsulas and Indonesian archipelago and was recorded from India, Indonesia, Malaysia and Thailand.

Variety quadrinflata was found in freshwater lakes, rivers, reservoirs, swamps and wetlands (India, Indonesia and Malaysia), as well as in a rice paddy field in Thailand.

In Malaysia, the shallow parts and edges of the Tasek Bera swamp lake were covered with Lepironia articulata associations. Aquatic plants such as Utricularia spp., Hydrilla sp., Nymphoides indica and Pandanus helicopus were present in still water areas, while Utricularia sp., Cryptocoryne griffithii, Scirpus confervoides and Pandanus helicopus were present in running water (Ratnasabapathy and Kumano 1974). At the time of sampling the temperatures ranged between 23.4 and 33.4 °C (in still water) and between 23.8 and 26.9 °C (in running water) and the pH ranged between 4.7 and 5.3 Ratnasabapathy and Kumano 1974). In South Sumatra it was also found in acidic waters in Lebak Danau (pH between 5.0 and 5.5; Scott and Prescott 1961).

The variety differs from all other forms because the isthmus is widely opened and due to the large width of the gap between the subterminal and terminal lobes. Pairs of prominent sharp teeth are borne on either side of the isthmus and on both sides of the base of terminal lobes. Cells 72–75 μm long., 68–70 μm wide, isthmus 8 μm wide (Prowse 1969).

Its current known distribution is limited to only one location in the Malayan peninsula (Suppl. material 2 and Fig. 2).

Variety spinosa was commonly found, together with var. quadrinflata, in the Tasek Bera forest swamp lake for which ecological conditions are described in the paragraph on var. quadrinflora above.