INTRODUCTION

Myxogastria (Mycetozoa) also called plasmodial slime molds are eukaryotic microorganisms that inhabit various terrestrial ecosystems. They have been classified as plants, fungi and protists at different times. Myxomycetes are plant-like in their manner of reproduction but resemble animals in the characteristics of their assimilative phase (Ranade et al., 2012). The organism exhibits two alternating phases in its life cycle, the assimilative phase and the sporulating phase. The assimilative stages; first mononuclear phase (amoeboid or flagellated), second multinuclear phase (plasmodium), and sporulating phase is fruiting bodies (sporophores) that contain spores (Clark and Haskins, 2015). In nature, slime molds typically live in cool, shady, moist places, such as on decaying logs, barks, wood and leaves. Slime molds feed on bacteria, protozoa and fungal spores (Novozhilov et al., 2017). Now there are about 1045 species world-wide (Lado 2005–2020) and 291 species in Turkey (Baba and Sevindik, 2019; Baba et al., 2020, 2021). Myxomycete studies were conducted in different regions of Turkey. But little work has been done in the Eastern Mediterranean region. This study aims to make a contribution to the myxobiota of Turkey.

MATERIALS AND METHODS

Myxomycetes were collected in three cities (Adana and Hatay) of the Eastern Mediterranean region of Turkey between 2015 and 2020 (Fig. 1). The fruiting bodies of myxomycete samples were collected from their natural habitat. In addition, dead plant materials, herbivorous and animal dung were taken for growing myxomycete in moist chamber cultures in laboratory. The samples were photographed and identified.

Fig. 1.
figure 1

Study area.

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Identification and photographing of myxomycetes samples were done with a light microscope (Olympus CX21), stereomicroscope (Euromex) and SEM of Mustafa Kemal University. In light microscopy, the capillitium, pseudocapillitium, columella, spore, shapes, color, size, ornamentation, branching shape, whether the columella is free or attached to the stem, pseudocapillitium features of species were observed. In stereomicroscope observation, fructification type, structure, shape, color, macroscopic measurements, lime color, and shape could be examined. Myxomycete samples were identified on the reference resources (Macbride and Martin, 1934; Martin and Alexopoulos, 1969; Farr, 1976; Thind, 1977; Martin et al., 1983; Lado and Pando, 1997; Ing, 1999; Neubert et al., 1995). Samples were arranged as fungarium material and kept in the Biology Department’s laboratory of Mustafa Kemal University Hatay-Turkey.

RESULTS AND DISCUSSION

The systematic of taxa is given according to the general literature (Adl et al., 2005; Schilde and Schaap, 2013). The taxa were listed below in alphabetical order together with descriptions, habitats, localities, collection dates, distribution at world and comments.

There were 291 Mycetozoa species in Turkey, 104 species in Physarida (Baba and Sevindik, 2019; Baba et al., 2020, 2021). With this study Physarida increased to 109 species, total number has reached to 296 in Turkey. Didymiidae family is readily distinguished from the Physaridae by the absence of lime from the threads of the capillitium. Now consisting of 4 genera and 39 species in Turkey (Baba and Sevindik, 2019; Baba et al., 2021).

Eukaryota

Protozoa

Amoebozoa

Mycetozoa

Myxogastria (Myxomycetes)

Order: Physarida

Family: Didymiidae

A. Peridium contains amorphous, calcareous deposits and double; lime present peridium and to the columella (when present); capillitium essentially non-calcareous and never with expanded calcareous nodes ……………………………….………………………… Diderma

a. Fruiting bodies are stalked sporangium; peridial layer double; columella distinct, cylindrical; capillitium sinuous and spores 8–9 (10) µm ...............………..……………………. Diderma montanum

A. Peridium contains stellate or angular lime crystals, fructification mostly sporangiate, capillitium not calcareous….....…………..………….……….....Didymium

a. Fruiting bodies stalked; stalk half or more of the total height, wrinkled, corrugated, darker and slightly wider, lighter upwards, completely covered with slightly indeterminate crystalline lime; true columella present, reaching to nearly the centre of the sporotheca; spores globose pale violet-grey, verruculose …………………………………..Didymium columellacavum

Family: Physaridae

A. Capillitium physaroid, consisting of a network of fine hyaline limeless threads with expanded calcareous nodes at some or all of the junctions; lime present in the peridium, capillitium and stipe in the form of amorphous granules, not crystalline ………..Physarum

a. Fruiting bodies sessile …………………………….…b

a. Fruiting bodies stalked; sporotheca subglobose or sub-depressed, prolates, about 0.5–0.9 mm in diameter, brown-orange or brown-yellowish color; peridium double or triple; capillitium dense, composed of numerous large, white, with pale yellow, rounded nodes and thin hyaline tubules ............…………… …………………………..................Physarum brunneolum

b. Fruiting bodies short plasmodiocarps; peridium double, outer layer white calcareous, thick, inner layer membranous; capillitium very abundant composed of short hyaline threads nodes are white; spores globose dark purple with a clearer zone, covered by warts ………………………………………..Physarum clavisporum

b. Fruiting bodies sessile or rarely short-stalked sporangium or short plasmodiocarpous; peridium single, a rather thick or slightly cartilaginous membrane, brown, white or ash-gray packed with small white; capillitium white lime nodes; spores triangular or quadrangular in optical section, with pale narrow ridges or lines …………………………Physarum spectabile

Diderma montanum (Meyl.) Meyl. (Fig. 2)

Fig. 2.
figure 2

Diderma montanum; (a) sporangium, (b, c) columella, (d, e) capillitium and spores in light microscope, (f, g) capillitium and spores in SEM.

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Description: Fruiting bodies sporangium, stalked, scattered or in groups. Sporotheca subglobose, flattened or umbilicate below, pearl-grey, pinkish-grey or off-white, 0.8–1 mm. Hypothallus disc-shaped, continuous under grouped sporocarps, reddish brown. Stalk shorter and usually paler than the sporocarp, pale or bright yellow-brown, slender or stout, packed with lime, indistinctly furrowed, 0.1–0.8 mm tall. Columella usually globose to subglobose on a restricted base or sometimes hemispherical, rather smooth, 0.4 mm diameter, brownish-red. Peridium double, the outer layer calcareous, thin, irregularly dehiscent and disintegrating before the inner layer, shining, brownish rose or flesh-coloured; the inner layer distinctly remote from the outer layer, membranous, brownish grey to cinereous. Capillitium consisting of slender branched and anastomosed towards the periphery, radiating outwards from the columella, loosely attached to the peridium, helicoidally wound or undulated; threads up to 400 µm long, 2 µm diam., dichotomously branched, sparsely interconnected, dark brown, purplish or hyaline threads, minutely scabrate, seldom with larger dark expansions. Spores dark brown nearly black in mass. Spores circular to egg-shaped in optical section, beige brown to greyish brown, pale brown, densely and rather minutely warted or minutely spinulose, 8–11 µm diam.

Specimens examined: Adana, Saimbeyli-Cöbük, on woods, Moist chamber technique, 38°02′40′′ N; 36°09′36′′ E, 1648 m, May 23, 2017, Baba 16.

Distribution: Belgium (Buyck, 1982), Costa Rica (Rojas et al., 2018), Finland (Harkönen, 1979), Japan (Emoto, 1977), Norway, Ukraine (Moreno et al., 2017), USA (Farr, 1976), Venezuela (Rojas et al., 2018).

Comments: The most common features of D. montanum is characterized by stalked sporocarps, double peridial layer, hemispherical columella.

Diderma Pers. genus is easily recognized by the double wall, smooth crustaceous layer of lime on the outer surface of the sporangium. Consisting of 12 species in Turkey (Baba and Sevindik, 2019). D. montanum is a characterized by short stalked, peridium double layer, columella is cylindrical, and capillitium sinuous. A close species is Diderma umbilicatum Pers., which has sporocarps 1–1.5 mm in diam., shortly stalked to almost sessile, globose to hemispherical, in groups and sometimes deformed due to mutual pressure; beige to light brown columella, rarely dark brown, globose to subglobose, 0.3–0.8 mm in diam., straight capillitium threads, hardly branched and spores 9–12 µm in diam (Singer et al., 2005). Diderma montanum is morphologically resembles to D. effusum (Schwein.) Morgan but is more plasmodiocarpous and has darker spores. Spores of this species are dark brown to blackish brown in mass, but spores in D. effusum are pale brown (Nannenga-Bremekamp, 1968). D. carneum Nann.-Bremek. is macroscopically close to D. montanum, but differs in the closely adhering peridium layers and in spore ornamentation (Buyck, 1982).

Didymium columellacavum Hochg., Gottsb. & Nann.-Bremek. (Fig. 3)

Fig. 3.
figure 3

Didymium columellacavum; (a) sporangium, (b) stalk and columella in light microscope and SEM, (c, d) capillitium, stellate lime crystals and spores in light microscope, (e, f) capillitium, stellate lime crystals and spores in SEM.

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Description: Fruiting bodies sporangium, gregarious, stalked, erect, 0.5–0.8 mm total height. Sporotheca conical to globose or subglobose, gregarious, 0.3–0.6 mm wide, 0.3–0.4 mm thick, white or pale grey, usually umbilicate below. Hypothallus discoid, membranous, oehraceous-brown to dark-brown, dark below containing refuse matter and obscured crystalline lime throughout. Stalk half the total height or more, 50–65% total height, rugulose, dark, black and a little wider, filled with refuse matter below, ochraceous brown, paler above, also with a little, obscured crystalline lime throughout. Columella clavate, in a closed umbilicus, subglobose, conical or cylindrical, sometimes with an expanded tip or rarely funnel-shaped, filled with air and with some angular lime crystals of 2–4 µm diam., variable in form and size, reaching to nearly the centre of the sporotheca, pale ochraceous, white to dark-brown, and hollow. Peridium membranous and hyaline, colourless and with thickened, reticulations covered with white stellate lime crystals. Dehiscense irregular. Capillitium profuse, delicate, hyaline to pale-purplish-brown threads, sparingly dichotomously branching and anastomosing, flexuose and in part undulate, radiating, branched 1–3 times, lightly attached to the peridium, with a few cross-bars, the tips hyaline. Spore-mass dark brown. Spores globose pale violet-grey, densely, palely, verruculose, 7–9 µm diam. Plasmodium unknown.

Specimen examined: Hatay Antakya, Habibi Neccar Mountain, on rotting leaves, Moist chamber technique, 36′09′′46 N, 36′10′′19 E, 400 m, April 21, 2016, Baba 65.

Distribution: Brazil, (Hochgesand et al., 1989), Peru (Lado et al., 2016).

Comments: The most common features of this species is characterized by its true columella and long stalk. Columella clavate, conical or cylindrical, reaching to nearly the centre of the sporotheca. Stalk rugulose, dark, black and a little wider below, and ochraceous brown or paler above.

Consisting of 25 species from Didymium Schrad in Turkey (Baba and Sevindik, 2019; Baba et al., 2021). D. columellacavum is characterized by its true columella. Contains the typical hollow club shaped columella, filled with lime crystals. The stalk is pale or ochraceous, darker and filled with refuse matter below, and the external surface covered with lime crystals, that are less abundant towards the base. The spores are warted and some warts are fused in a short subreticulate pattern (Lado et al., 2016). D. chrysosporum Lakh. & Mukerji seems closest to it, but it differs in having the peridial thickened areolae with depressions filled with lime crystals, slightly enlarged capillitium tips attached firmly to the peridial areolae and spores which bear warts up to 0.5 µm long. D. squamulosum (Alb. & Schwein.) Fries also is close to it, it has the columella often filled mostly with air too, but it differs in having distinct, rather wide, funnel-shaped tips with which some of the capillitium tubules are attached to the peridial areolae (Hochgesand et al., 1989). According to Clark and Haskins (2018) this species similar to D. chrysosporum and D. floccoides Nann.-Bremek. & Y. Yamam. D. chrysosporum does not have peridial areolae, spores more warted; D. floccoides; peridium dehiscing into small floccose platelets (Clark and Haskins, 2018).

Physarum brunneolum (W. Phillips) Massee (Fig. 4)

Fig. 4.
figure 4

Physarum brunneolum; (a, b) sporangium, (c, d) capillitium, lime granules and spores in light microscope, (e) spores in SEM, (f) capillitium, lime granules and spores in SEM.

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Description: Sporocarps scattered or gregarious, but not crowded, short-stalked colored, globose to turbinate, 0.8–1.7 mm in total height, shining dark yellow-brown. Sporotheca subglobose or sub-depressed, prolates, about 0.5–0.9 mm in diameter, brown-orange or yellowish brown color, orange-yellow turning yellowish brown at the apex, smooth or somewhat rough, bright. Hypothallus small, dark. Stalk rugose, dark, short, furrowed, cylindrical, erect, longitudinally grooved, 0.2–0.5 mm long, 0.1–0.15 mm wide, brown-orange, orange yellow, brown-red or dark brown. Peridium double or triple, thick, smooth or polished, yellow brown, the outer layer cartilaginous, crustose, smooth, orange yellow, middle layer calcareous, white, the inner layer white, calcareous, membranous, colourless, dehiscence irregular or stellately. Columella absent, sometimes presents a pseudocolumela. Capillitium dense, composed of numerous large, white, with pale yellow, rounded nodes and thin hyaline tubules of 1.5 μm wide, irregular lime nodes, numerous, white, irregular calcium, internodes thin and short. Spore-mass brownish black. Spores globose, free, light brown, dark brown, black, 7–10 (12) µm, warted or spiny. Plasmodium yellow.

Specimen examined: Hatay Antakya, Kömürçukuru, on leaves of Pinus brutia Ten. Natural, 35°53′20′′ N; 36°05′28′′ E, 579 m, April 24, 2015, Baba 389.

Distribution: Argentina (Lado et al., 2014), Australia (Mitchell, 1995), Chile (Lado et al., 2013), Costa Rica, Colombia, India, Japan (Farr, 1976), Mexico (Estrada-Torres et al., 2009), Peru (Treviño-Zevallos and Lado, 2020), USA (Poulain et al., 2011), Venezuela (Lado et al., 2013).

Comments: The most common features of P. brunneolum; has brown-orange or brown-yellowish color, characterised by thick, crustose and shining the brown outer peridial layer and reddish-brown stipe.

Physarum clavisporum G. Moreno, A. Sánchez, A. Castillo & Illana (Fig. 5)

Fig. 5.
figure 5

Physarum clavisporum; (a, b, c) sporocarps, (d, e) capillitium, lime granules and spores in light microscope, (f, g) capillitium, lime granules and spores in SEM.

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Description: Fruiting bodies isolated to gregarious, or forming small groups, sessile, 0.7–2 × 0.7–1 mm, globose to ovoid or forming short sinuous to straight plasmodiocarps. Hypothallus whitish to slightly straw yellow. Peridium double, outer layer white calcareous, thick, slighty warted to almost smooth, inner layer membranous, thin, hyaline to slightly greyish. Capillitium very abundant composed of short hyaline threads approximately 1 µm diameter, attached to thick capillitial nodes and peridium. The nodes are white and composed of globose calcium carbonate which break easily, especially when under pressure, their morphology is variable subglobose to elongate (60–90 × 30–70 µm diam.) and completely filling the interior of the sporocarp. Spores in mass dark violaceous. Spores globose dark purple, with a paler area, 8–12 (13) µm diam., covered by densely and regularly warts, or consists of thick, laxly and irregularly distributed bacula with a paler area.

Specimen examined: Hatay, Samandağ, on barks with Didymium megalosporum Berk. & M.A. Curtis, Moist chamber technique, 36°07′44′′ N, 35°58′20′′ E, 177 m, July 21, 2019, Baba 1.

Distribution: Chile (Lado et al., 2013), Peru (Lado et al., 2016), Portugal, Spain, USA (Moreno et al., 2009).

Comments: The most common features of P. clavisporum are fruiting bodies generally forming short sinuous to straight plasmodiocarps. The spores are dark purple brown and with a paler area.

Physarum spectabile Nann.-Bremek., Lado & G. Moreno (Fig. 6)

Fig. 6.
figure 6

Physarum spectabile; (a, b) sporocarps, (c,d) capillitium, lime granules and spores in light microscope, (e) capillitium, lime granules and spores in SEM, (f) spores in SEM.

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Description: Fruiting bodies sporangium and short plasmodiocarpous, gregarious to crowded, sessile or rarely short-stalked, spherical to oblong, somewhat laterally flattened, pulvinate sometimes heaped 0.4–1 mm diameter, up to 2 mm long and 0.3–0.5 mm high, almost smooth, white. Hypothallus membranous, pale brown, inconspicuous, translucent, gradually merges into the stalk, containing a little granular matter. Stalk white, irregular, flattened, grooved, sometimes common to several sporothecae, 0.1–0.4 mm in height. Columella absent, central white limy pseudocolumella is often present. Peridium single, a rather thick or slightly cartilaginous membrane, brown, white or ash-gray packed with small upto 0.8 micron in diameter, white lime and with small rounded scale-like patches of lime globules. Dehiscence irregular, beginning with the apical part, lower part often persists as a cup. Capillitium in opened sporothecae pale, with many small rounded or elongate, sometimes branched white lime nodes, the nodes irregular, about 20 μm across diameter and 60–80 μm long, rugged pseudocolumella, the nodes connected by very delicate tubules. Spore-mass dark brown or black. Spores very dark purple-brown, ±triangular or quadrangular in optical section, with pale narrow ridges or lines, the remainder densely and minutely papillose, 12–14 µm diam. Plasmodium not observed.

Specimen examined: Hatay, Defne, Harbiye, on barks and wood with Didymium difforme (Pers.) Gray, Moist chamber technique, 36°07′47′′ N 36°08′39′′ E, 244 m, February 12, 2019, Baba 6.

Distribution: Argentina (Lado et al., 2013; Lado et al., 2016), Brazil, Canary Islands (Nannenga-Bremekamp et al., 1984), Chile (Lado et al., 2007), Madagascar (Yatsiuk et al., 2017), Mexico (Rollins and Stephenson, 2013), Morocco, Norway (Yatsiuk et al., 2017), Papua New Guinea, Peru (Lado et al., 2016), Russia (Gmoshinskiy et al., 2017), Spain, Ukraine (Yatsiuk et al., 2017), USA (Lado et al., 2007).

Comments: The most common features of this species is slightly compressed laterally sporangia. Hypothallus membranous. Spores very dark purple-brown, triangular or quadrangular in optical section, with pale narrow ridges or lines and evenly warted.

The Physaridae family is easily distinguished from Didymiidae by the presence of lime in the capillitium. Now consisting of 8 genera and 65 species in Turkey (Baba and Sevindik 2019; Baba et al., 2021). Physarum Pers. consisting of 39 species in Turkey (Baba and Sevindik 2019; Baba et al., 2021). P. brunneolum has stalked and colored sporocarps, subglobose or prolate, brown-orange or brown-yellowish color, smooth or somewhat rough, bright. Characterised by thick, crustose and shining the Diderma-like, brown outer peridial layer and membranous inner peridium, more or less stellate dehiscence small, reddish-brown stipe, an occasional pseudocolumella, dense, almost badhamioid capillitium, and dark, coarsely marked spores are the salient diagnostic features of this species (Martin et al., 1983). When opened by irregular dehiscence from above, the persisting cup-like base of the sporangium recalls Leocarpus fragilis (Dicks.) Rostaf. but then again the capillitium is different. This species confused with L. fragilis but that has a very different capillitium with jagged, yellowish nodes. This species is typical of the dry evergreen oak-pine forests of much of Mediterranean Europe (Ing, 1999). P. brunneolum easy to confuse with Craterium aureum (Schumach.) Rostaf. but C. aureum has only one layer in the peridium (Poulain et al., 2011) and colour of sporophores totally different. P. brunneolum seems to be most similar species to P. andinum A. Ronikier & Lado. Sporocarps are similar, both species usually sporocarpic and stalked. However, P. brunneolum is smaller, P. andinum is larger. The peridium of P. brunneolum is shiny and yellow-brown, and P. andinum is yellow to whitish, usually darker at the base. The dehiscence of P. brunneolum is stellate but P. andinum is irregular. P. brunneolum also has dark brown spores (Ronikier and Lado, 2013).

P. clavisporum is spread throughout the European and American, mediterranean area and as it has been confused with the two previously cited species (P. bitectum G. Lister and P. bivalve Pers.) possibly has a wider distribution (Moreno et al., 2009). This is a rare species. Macroscopically, P. clavisporum are almost indistinguishable from P. bitectum, but spore ornamentation in P. clavisporum is prominent spines and uniformly distributed warts in P. bitectum. The spores are dark purple brown colour with a paler area, bearing dispersed and prominent spines, and the spore surface covered by tiny densely distributed warts visible only by SEM. But the spines of the spores are formed of spines or bacula instead of the pila with widened to slightly coralloid apex of the type material (Lado et al., 2016).

The distinctive feature of P. spectabile is evenly warted and angular dark spores with pale narrow lines. P. spectabile is very like P. bubalinum Farr, from which it differs in the not even slightly compressed laterally sporangia and in the very dark angular spores. Sporocarps of P. spectabile are greyish and often laterally compressed. Capillitium formed by small, globose, white nodes (Moreno et al., 2018). Physarum atacamense D. Wrigley, Lado et Estrada, P. straminipes Lister, and Badhamia melanospora Speg. are species with angular spores and appear on similar substrates. P. atacamense can be easily distinguished from the rest, because it usually forms sporocarps on long stipes and the spores have dark lines (spores of P. spectabile have pale lines) (De Basanta et al., 2012). P. straminipes also has a yellow, weak stipes and forms sporocarps on straw and another grass litter (Ing, 1999). B. melanospora has a completely different badhamioid capillitium (Gmoshinskiy et al., 2017). This is one of the most common species on cacti and succulent plants. It has very variable characters, and can be sessile or with a well defined calcareous stalk. It can be confused with P. straminipes Lister, but the latter has a non-calcareous membranous extension of the hypothallus and not a stalk. Even when P. spectabile is sessile, the narrow pale bands on the usually angular spore separate these species (Nannenga-Bremekamp et al., 1984). P. spectabile is recognized due to its very dark spores with pale bands and small rounded lime nodes (Yatsiuk et al., 2017). In South America P. spectabile has mostly been reported as a succulenticulous species inhabiting leaves of Opuntia sp., Agave sp., Yucca sp., etc. However, in Europe it is repeatedly found on wood debris of deciduous trees such as Populus tremula L. and P. canadensis Moench. (Yatsiuk et al., 2017).

CONCLUSIONS

As a result of this research, 5 new records were added to Myxobiota of Turkey. The number of recorded Mycetozoa in Turkey has increased to 296.