Secretive Slime Moulds: Myxomycetes of Australia

By Steven L. Stephenson

Neither plants, nor animals, nor fungi, the myxomycetes are a surprisingly diverse and fascinating group of organisms. They spend the majority of their life out of sight as single-celled amoeboid individuals in leaf litter, soil or decaying wood, foraging for bacteria and other simple life forms. However, when conditions are right, two individual cells come together to give rise to a much larger, creeping structure called a plasmodium, which produces the even more complex and often beautiful fruiting bodies. Indeed, the fruiting bodies of myxomycetes are often miniature works of art!

Their small size (usually only a few millimetres tall) and fleeting fruiting phase mean that these organisms, although ubiquitous and sometimes abundant, are overlooked by most people. However, recent research by a few dedicated individuals has shown that Australia has a very diverse myxomycete biota with more than 330 species, the largest number known for any region of the Southern Hemisphere.

This comprehensive monograph provides keys, descriptions and information on the known distribution for all of these species in addition to containing introductory material relating to their biology and ecology. Many species are illustrated, showing the diversity of their fruiting bodies, and greatly facilitating their identification.

This book will give naturalists a new insight into an often overlooked group of organisms in addition to providing an incentive to search for the many species which have undoubtedly thus far escaped notice.

• Language: English
• Publisher: CSIRO PUBLISHING
• Release date: Mar 1, 2021
• ISBN: 9781486314157

Steven L. Stephenson

Dr Steven L. Stephenson is a Research Professor in the Department of Biological Sciences at the University of Arkansas, USA.

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fusca

Introduction

Myxomycetes (also known as plasmodial slime moulds or myxogastrids) have been known from their fruiting bodies since at least the middle of the seventeenth century, when the first recognizable description of a member of the group (the very common species now known as Lycogala epidendrum) was provided by the German mycologist Thomas Panckow (Alexopoulos et al. 1996). However, since the fruiting bodies produced by some species of myxomycetes can achieve considerable size (those of Fuligo septica commonly exceed 10 cm or more in total extent), there is little doubt that myxomycetes have been observed in nature as long as mankind has existed. Evidence from molecular studies indicates that myxomycetes have a long evolutionary history and probably were present on the earth several hundred million years ago. Myxomycetes do not have a particularly attractive name, but many examples produce fruiting bodies that are miniature objects of considerable beauty. However, because of their small size, all but the largest and most conspicuous examples tend to be overlooked in nature.

Since their discovery, myxomycetes have been variously classified as plants, animals or fungi (Martin 1960). Because they produce aerial spore-bearing structures (fruiting bodies) that resemble those of certain fungi and also typically occur in some of the same ecological situations as fungi, myxomycetes traditionally have been studied by mycologists (Martin & Alexopoulos 1969). Indeed, the name most closely associated with the group, first used by Link (1833) more than 185 years ago, is derived from the words ‘myxa’ (meaning slime) and ‘mycetes’ (referring to fungi). However, myxomycetes are profoundly different from the ‘true’ fungi and actually belong to another kingdom, the Protista (sometimes called Protoctista).

Classification of the Myxomycetes

Approximately 1000 species of myxomycetes have been described to date (Lado 2005–2019), and the traditional classification used for the group placed these in six different taxonomic orders—the Ceratiomyxales, Echinosteliales, Liceales, Physarales, Stemonitales and Trichiales. Although this system of classification, which was based upon spore colour and easily discernible morphological features, has been used in all previous monographs of the myxomycetes, it does not properly reflect evolutionary relationships within the group. For example, the traditional order Ceratiomyxales (which consists of the single genus Ceratiomyxa with four species) is distinctly different from the other orders and is now assigned to a totally different taxonomic class, the Ceratiomyxomycetes. Based on a phylogeny constructed from 18S rDNA sequences (e.g. Fiore-Donno et al. 2005, 2008, 2010, 2013), myxomycetes in the other orders make up a monophyletic group which splits into two basal clades. The first clade (the subclass Columellomycetidae) consists mostly of members of the traditional orders Stemonitales and Physarales, which have dark (different tints of brown to black) spores, along with members of the traditional order Echinosteliales. The second clade (the subclass Lucisporomycetidae) includes the traditional orders Liceales and Trichiales with brightly coloured spores (including red, orange, purple, yellow and olive). However, the traditional orders no longer hold together in the manner in which they have been circumscribed in all earlier treatments of the myxomycetes. Instead, a number of superorders are recognized in each of the two subclasses, with each made up of several orders. For example, the subclass Lucisporomycetidae contains four orders, none of which corresponds exactly to any of the traditional orders, while the subclass Columellomycetidae contains five different newly recognized orders. The classification system used herein essentially follows that outlined by Leontyev et al. (2019)

The fact that the vast majority of myxomycetes can be assigned to one of two groups on the basis of the spore colour in mass is not a new concept. It was first proposed by Joszef Rostafinski (1874–1876) and then used in Arthur Lister’s A Monograph of the Mycetozoa (1894), which was the standard reference on the myxomycetes at the end of the nineteenth and during the early part of the twentieth century. This classic monograph first appeared in 1894, but revised and expanded versions were published in 1911 and 1925 by his daughter Gulielma Lister (Lister 1911, 1925). The 1925 edition is noteworthy in the context of the present monograph because it contains references to species of myxomycetes that had been reported from Australia prior to the third decade of the twentieth century.

Historical Background in Australia

The first report of myxomycetes from Australia was by the Reverend Miles Berkeley (1839), who listed two species from Tasmania (but then known as Van Diemen’s Land) that had been collected by Robert Lawrence and Ronald Gunn and sent to William Hooker in Britain. The two species—Aethalium septicum (now known as Fuligo septica) and Stemonitis fusca—are both relatively common and form relatively conspicuous fruiting bodies. Later, Berkeley (1845) mentioned eight species (including Stemonitis fusca) identified from specimens collected by James Drummond in Western Australia and sent to Hooker. Drummond had arrived at the Swan River Colony in 1829 (May & Pascoe 1996), and the specimens of myxomycetes he sent to Hooker were collected at some point after this date. In another early report, Berkeley (1859) reported 16 species that had been identified from specimens collected by two amateur mycologists (Ronald Gunn and William Archer) in Tasmania during the period 1839-1843. Interestingly, two of these (the first described originally as Stemonitis echinulata but renamed Lamproderma echinulatum and the second described originally as Trichia metallica but now known as Prototrichia metallica) were new to science. Some years later, Berkeley (1881) also reported the first records from eastern Australia when he listed nine species from Queensland. Other reports prior to 1900 are those of Mordecai Cooke (1888a, 1888b, 1892) and Daniel McAlpine (1895). In his Handbook of Australian Fungi, Cooke (1892) listed approximately 50 species of myxomycetes for Australia. During the period 1900 to 1935, Cheesman & Lister (1915), Cheel (1918), Cleland (1927, 1935) and Fraser (1933) provided additional records, essentially doubling the total number of species known from the country. The best known region of Australia, based on collections made during the first half of the twentieth century, was in and around Sydney in New South Wales, for which Lilian Fraser (1933) listed a total of 88 species and varieties. Relatively few papers (e.g. Flentje & Jeffery 1952, Hnatiuk 1978, Cribb 1986, Stephenson et al. 1992, Cribb & Cribb 1992, Cribb 1993, Ing & Spooner 1994) relating to myxomycetes appeared during the major portion of the second half of the twentieth century. Only one of these (Ing & Spooner, who reported 16 species) mentioned more than a few species.

The first truly comprehensive checklist of the myxomycetes of Australia (Mitchell 1995) listed 146 species, 37 of which were new records for the country. May et al. (2003), in Volume 2B of Fungi of Australia, used this checklist as the basis for the information provided on myxomycetes. They indicated that 149 species had been reported for the country, but this total included several invalid names or forms no longer recognized as distinct species, reducing the actual number to 142. Since 1995, when the author of this monograph spent almost four months at the Australian Antarctic Division Station on Macquarie Island (Stephenson & Moreno 2006, Stephenson et al. 2007), surveys carried out at various localities throughout both mainland Australia and Tasmania (McHugh et al. 2003, 2009; Black et al. 2004; Jordan et al. 2006; Rosing et al. 2007; Davison et al. 2008; Stephenson et al. 2008; Wrigley de Basanta et al. 2008; Stephenson & Shadwick 2009; Wellman 2015, 2016, 2017; Davison et al. 2017, Stephenson & Stephenson 2019) have increased the number of species of myxomycetes known from Australia to more than 330, which is the highest total known for any region of the Southern Hemisphere. For example, only 196 species are known from New Zealand, where myxomycetes have been actively studied for more than a century (Stephenson 2003, Stephenson et al. 2009). The myxomycetes now known from Australia represent about a third of the approximately 1,000 species known worldwide and the total includes a number of examples (e.g. Alwisia lloydiae, Comatricha pseudonigra, Cribraria bicolor, Didymium macquariense, Elaeomyxa australiensis, Lepidoderma cristatosporum, Licea xanthospora and Trichia brimsiorum) described as new to science from material collected in the country (Stephenson & Moreno 2006, Moreno et al. 2007, Moreno et al. 2008, Stephenson & Novozhilov 2012, Davison et al. 2013, Leontyev et al. 2014, Moreno et al. 2018, Stephenson et al. 2018). Moreover, a number of specimens collected in Australia are problematic and have not yet been assigned to any currently recognized species. In some cases, these probably represent incompletely developed or aberrant specimens, but in some instances it is likely that they are undescribed species.

The most recent relatively extensive publication on the myxomycetes of Australia is the delightful little book by Sarah Lloyd, first published in 2014 and then in an expanded version in 2018 (Lloyd 2014, 2018). The book is based on specimens collected in Tasmania, and the expanded version considers more than 100 species, which are illustrated with excellent images. As a result of Lloyd’s efforts, the myxomycetes of the region of Tasmania in which she lives are now among the best known of any region of the entire country. She greatly expanded the list of species reported from Tasmania.

In addition to the data available for mainland Australia and Tasmania, surveys for myxomycetes have been carried out in two Australian oceanic island territories—Christmas Island (Shivas & Hilton 1990, Stephenson & Stephenson 2019) and Macquarie Island (Stephenson, Laursen et al. 2007)—that undoubtedly represent the two climatic extremes for the geographical region considered in this monograph. A recent trip to Norfolk Island (June 2019) by the author has provided additional records for that territory (Stephenson & Stephenson 2020).

Life Cycle

The life cycle of a myxomycete (Fig. 1) encompasses two very different trophic (or feeding) stages, one consisting of uninucleate amoebae, with or without flagella (the term ‘amoeboflagellate’ applies to both forms), and the other consisting of a distinctive multinucleate structure, the plasmodium (plural: plasmodia). It should be noted that much of what is known about the life cycle in myxomycetes has been derived from intensive studies of just two species (Physarum polycephalum and Didymium iridis), but it is assumed that all other species follow a similar pattern.

Figure 1. Generalized life cycle in the myxomycetes.

A. Group of fruiting bodies. B. Spore. C. A protoplast emerges from the spore. D. The protoplast can take the form of an amoeba (left) or a flagellated cell (right) during the first trophic stage (the term ‘amoeboflagellate’ applies to both forms). E. Under dry conditions or in the absence of food, an amoeboflagellate can form a microcyst, or resting stage. F. Compatible amoeboflagellates fuse to form a zygote. G. Zygote. H. The nucleus of the zygote divides by mitosis and each subsequent nucleus also divides without being followed by cytokinesis, thus producing a single large cell, the plasmodium. I. The plasmodium, which represents the second trophic stage in the life cycle. J. Under adverse conditions, the plasmodium can form the second type of resting stage found in myxomycetes, the sclerotium. K–L. Fruiting bodies develop from the plasmodium. During fruiting body formation, spores are produced.

Plasmodia are motile, and those of some species can reach a size of a metre or more in total extent. A large example contains many thousands of synchronously dividing nuclei. Under favorable conditions, a plasmodium gives rise to one or more fruiting bodies containing spores. The transformation from plasmodium to fruiting body is a remarkable process. A plasmodium is mobile and essentially shapeless, but the fruiting bodies derived from it have an intricate structure and often are objects of considerable beauty. The transformation begins with the plasmodium becoming immobile and then undergoing the changes in form necessary to produce the fruiting body. Sometimes the fruiting body is the same colour as the plasmodium from which it was derived, but at other times this is not the case. The colours displayed by plasmodia range from essentially colourless to black, but many examples are some shade of white, yellow or orange, with colours such as or maroon red less common (Fig. 2A–D). Although the changes involved are considerable, the entire process can take place rather quickly. It is not unusual to observe an active plasmodium one day and discover that it has given rise to fully mature fruiting bodies the next day. The stages in the development of the fruiting bodies of Stemonitis axifera are illustrated in Fig. 3A–F.

Figure 2. Plasmodia of various myxomycetes, illustrating some of their range of form and colour. A. Photo: © J. Van Der Heul. B. Photo: © S.L. Stephenson. C. Photo: © S. Young. D. Photo: © J. Van der Heul.

Figure 3, A–F. Development of fruiting bodies in Stemonitis axifera . Photos: © S. Lloyd.

Presumably, the spores produced in the fruiting body of a myxomycete are largely wind-dispersed and complete the life cycle by germinating to produce the uninucleate amoeboflagellate cells (Stephenson et al. 2008). These feed and divide by binary fission to build up large populations in the various microhabitats in which these organisms occur. Ultimately, this stage in the life cycle gives rises to the plasmodium. This process can result from gametic fusion between comparable amoeboflagellates or it can be apomictic (Collins 1980, 1981).

Under adverse conditions, such as drying out of the immediate environment or low temperatures, a plasmodium may convert into a hardened, resistant structure called a sclerotium (plural: sclerotia), which is capable of reforming the plasmodium upon the return of favourable conditions. In addition, amoeboflagellate cells can undergo a reversible transformation to dormant structures referred to as microcysts. Both sclerotia and microcysts potentially can remain viable for long periods of time and probably are rather important in the continued survival of myxomycetes in some ecological situations and/or microhabitats. Presumably, this is the case in the arid habitats so common over much of Australia.

Structure of the Fruiting body

Until recently, identification of myxomycetes was based almost exclusively upon features of the fruiting body (Martin & Alexopoulos 1969, Stephenson 2011), which can range in size from microscopic examples that are virtually impossible to detect in the field to plate-sized or even larger structures that are difficult to overlook, even by someone who knows nothing about these organisms. Fruiting bodies (also called sporocarps or myxocarps) are usually classified into one of four different types or forms based on their overall morphology. Typical examples of each of type are relatively easy to distinguish, but some species of myxomycetes regularly produce what appears to be a combination of two different types, and the extent to which one type or the other predominates apparently is at least somewhat dependent upon the environmental conditions under which they are produced. The most common type of fruiting body is the sporangium (plural: sporangia), which may be sessile or stalked and can be found in a wide variety of different shapes and colours. The actual spore-containing portion of the sporangium, as opposed to the entire structure, is referred to as the sporotheca (Lado & Pando 1997) or sporocyst (Poulain et al. 2011). In those sporangia that have a stalk, the latter is usually vertical or nearly so, with the sporotheca normally at the apex. Sporangia usually occur in groups, since they are derived from separate portions of the same plasmodium, but this is not the case for the very smallest examples, in which a microscopic plasmodium gives rise to a single minute sporangium. A second type of fruiting body, an aethalium (plural: aethalia), is a more-or-less cushion-shaped structure that is presumed to be, at least in many instances, masses of completely fused sporangia. Aethalia can be quite large, with those of some species commonly exceeding several centimetres or more in total extent. A third type of fruiting body is the pseudoaethalium (literally a ‘false’ aethalium), which consists of a mass of sporangia closely crowded together but not fused to form a single structural unit. Pseudoaethalia are comparatively uncommon. Most examples are sessile, but a very few are stalked (although the ‘stalk’ involved has a different origin than for a stalked sporangium). The fourth type of fruiting body is a plasmodiocarp, which is almost always sessile. Plasmodiocarps take the form of the main veins of the plasmodium from which they were derived. Most examples are relatively simple somewhat elongated to sparsely branched structures, but a few examples form an elaborate network on the substrate upon which they occur.

A typical fruiting body consists of as many as six primary structural components—hypothallus, stalk, columella, peridium, capillitium and spores (Fig. 4). However, not all of these are present (or evident even if they are present) in all types of fruiting bodies. Moreover, in some species a pseudocolumella or pseudocapillitium also may be present.

Figure 4. Structure of the fruiting body of a myxomycete.

A. Hypothallus. B. Stalk (sometimes this can extend into the spore mass as a columella, as shown in the figure). C. Sporotheca. D. Peridium. E. Capillitium. F. Spores.

The hypothallus is a layer of material, deposited by the plasmodium when the latter gives rise to fruiting bodies, that forms an extension of the base for one or more fruiting bodies and, in doing so, connects the stalk (if this structure in present) to the substrate. The hypothallus may be dull or brightly coloured, thin or thick and delicate or relatively coarse. In a very few species, it is so thick that the fruiting bodies appear to be immersed in the hypothallus. The stalk (also referred to as a stipe) is an exceedingly important characteristic for identification. It can vary in length, thickness, colour, composition and texture. In most species the stalk is opaque, but in some species it is translucent. The stalk also may be coated with lime or filled with granular or spore-like structures. The peridium (plural: peridia) is a covering that encloses the spore mass of the fruiting body. It may or may not be evident in a mature fruiting body. In some species, the lower portion of the peridium persists as a calyculus, a cup-like structure that encloses the bottom of the spore mass. The presence or absence of the calyculus is an important diagnostic feature in identification for some groups of myxomycetes. This also applies to the way in which the fruiting body opens. The peridium may split open along clearly discernible lines of dehiscence, as a pre-formed lid, or in an irregular manner. In an aethalium, the relatively thick covering over the spore mass is usually referred to as a cortex rather than a peridium. The columella is an extension of the stalk upwards into the sporotheca, although it may differ in structure and appearance from the stalk. Although usually readily apparent, in some sessile fruiting bodies the columella may take the form of a dome-shaped structure on the inside of the peridium where the latter is in contact with the substrate. The pseudocolumella is a columella-like structure that is present within the sporotheca but does not attach to the stalk. A pseudocolumella is found only in some members of the family Physaraceae. The capillitium consists of thread-like elements that are found within the spore mass of a fruiting body. Many species of myxomycetes have a capillitium, either as a single interconnected network or as many free elements called elaters. The capillitium may be smooth, sculptured or spiny. In the family Physaraceae, the capillitium may consist entirely of lime or be limeless either in part or completely. These distinctions are exceeding important for identification in this group of myxomycetes. The capillitium may be attached to the columella, pseudocolumella or the inner surface of the peridium. What has been referred to as a pseudocapillitum (literally a ‘false capillitium’) is present in the aethalia and pseudoaethalia produced by some of the larger members of the order Reticulariales. The elements that make up the pseudocapillitium have been considered to represent the remnants of the peridia of individual sporangia that fused together to form a single unit structure (Stephenson & Stempen 1994). However, very different types of pseudocapillium exist, and more research is needed to determine their origin and true nature (Fiore-Donno et al. 2013, Leontyev, Schnittler et al. 2014).

The spores of myxomycetes range in size from slightly less than 5 µm to occasionally more than 15 µm in diameter, with most species producing spores 10 plus or minus 2 µm in diameter (Schnittler & Tesmer 2008). Nearly all spores are more-or-less globose, and most are ornamented to some degree. Spores that appear to be entirely smooth are rare. Spore ornamentation can range from almost smooth to punctate (marked with very small dot-like warts) to distinctly warted (with short blunt projections), spiny (with sharp pointed projections) or reticulate (covered by a network of ridges). Warts or spines vary in size from small (minutely warted or spiny) to relatively large (coarsely warted or spiny) and may be scattered uniformly over the surface of the spore or occur in clusters. Some spores are characterized by a variant of one or more of these morphological expressions. Although spore colour in mass is the first feature that needs to be taken into consideration, spore ornamentation and spore size also are very important in identification.

Collecting and Studying Myxomycetes

The methods typically used for collecting myxomycetes in the field are rather similar to those used for macrofungi. At a particular locality, the opportunistic protocol described by Cannon & Sutton (2004) is often used to search for the fruiting bodies of myxomycetes. Particular attention tends to be directed towards microsites (e.g. the lower surface of large pieces of coarse woody debris) that are likely to retain some moisture even when the surrounding habitat is quite dry. When fruiting bodies are found, small portions of the substrate upon which the fruiting bodies occur are removed and placed in a collecting box (most often a plastic box with individual compartments) to be transported back to the laboratory. In the laboratory, portions of the substrate with fruiting bodies present are allowed to dry out at room temperature and then glued onto pieces of stiff paper (i.e. index card stock or something similar) placed in small pasteboard boxes. After this process, identification of particular specimens is usually carried out using standard monographs (e.g. Martin & Alexopoulos 1969, Stephenson 2003) on the myxomycetes. Unlike the fruiting bodies of macrofungi, which can undergo major changes in size, colour and general appearance when they are dried, those of myxomycetes are not greatly affected by drying. Each boxed specimen is labelled with such information as the name (i.e. genus and species) of the myxomycete, the type of substrate upon which the fruiting bodies occurred, the locality where it was collected, the date of collection, the collector’s name and collector’s number and the name of the person who identified the specimen if other than the collector. Because the boxes used as storage containers for specimens of myxomycetes are relatively small (often no larger than a matchbox), it is possible to store a considerable number of specimens in a rather limited space. Once a specimen of a myxomycete is thoroughly dry, it is fairly resistant to most of the insects and other pests that often plague collections of preserved biological specimens. If handled and stored properly, myxomycetes will remain suitable for study for many years.

The moist chamber culture technique as it applies to myxomycetes (Gilbert & Martin 1933, Stephenson & Stempen 1994) provides a convenient and often very productive method of supplementing field collections. In arid environments such as those found over much of Australia, virtually all records of myxomycetes are likely to be obtained from moist chamber cultures. In addition to the microhabitats listed in the preceding section, the technique also can be used to study the myxomycetes associated with several other microhabitats in which these organisms are known to occur. These include the lianas found in tropical forests (Wrigley de Basanta et al. 2008), the inflorescences of large herbaceous plants (Schnitter & Stephenson 2002) and the woody twigs that occur on the forest floor (Stephenson, Urban et al. 2008).

Moist chamber cultures are relatively easy to prepare. The first step simply involves finding some container that can serve as a potential culture chamber. Disposable plastic Petri dishes have been widely used, but just about any type of container or shallow bowl that can be covered with a top or lid will work just as well. Once a suitable container has been selected, the bottom is lined with a piece of absorbent paper (paper towels work quite well) trimmed to the appropriate size. After the paper is in place, samples of the dead plant material (e.g. pieces of bark, litter or dung) to be investigated are placed in the container so that they cover most of the bottom without overlapping to any great extent. Enough water is then added to cover the sample material and the top or lid placed on what has become a moist chamber culture. The next day, most of the water in the container is poured off and the cultures containing the completely saturated sample material are set aside and disturbed as little as possible. Isolation of myxomycetes in moist chamber cultures is usually carried out at ordinary room temperatures under diffuse light. After a period of no more than a week, the culture is observed under a stereomicroscope in order to see if any myxomycetes (either plasmodia or fruiting bodies) are present. When mature fruiting bodies are detected, they are removed and handled in the same manner as already described for specimens collected in the field.

It is not unusual for the pH of the water in the moist chamber culture to be determined just before it is poured off. The pH of the substrates potentially available to myxomycetes in nature is a very important factor influencing their distribution (Härkönen 1977, Stephenson 1989, Wrigley de Basanta 2000). Although many species of myxomycetes appear to have a relatively wide pH tolerance, this is not the case for all species. For example, Härkönen (1977), who measured the pH of substrates upon which fruiting bodies occurred in a study of the distribution patterns of myxomycetes associated with the bark of living trees in southern Finland, concluded that species of myxomycetes have different pH optima and amplitudes. In her study, some species seemed to prefer acidic substrates, whereas others never developed under low pH conditions. Stephenson (1989) found the same to be true for both bark and forest floor litter in a study carried out in the eastern United States.

Scope of this Monograph

The geographical region considered in this volume includes the six Australian States, the Northern Territory, the Australian Capital Territory and both the immediate offshore islands (e.g. Kangaroo Island, Melville Island and Fraser Island) as well as the oceanic island territories of Christmas Island, Macquarie Island and Norfolk Island. The best known of these with respect to myxomycetes is Macquarie Island, which was subjected to an intensive survey in 1995. As is the case for any country, some regions of Australia have been subjected to much more study than others, with northern Queensland, New South Wales, northern Tasmania and the southern portion of Western Australia representing the most prominent examples.

For each of the species considered herein, information is provided on (1) the proper taxonomic name according to the nomenclatural standard (Lado 2005–2019) currently being used for myxomycetes along with details relating to the publication of this name, (2) all relevant synonyms that have been applied to records of the species from Australia, (3) the type locality, (4) a number of sources of previously published illustrations of the species in question, (5) a complete description of the morphology of the fruiting body, (6) the habitats with which it is usually associated, (7) the first known report from Australia along with the states and/or territories for which the species has been recorded, and (8) comments on various noteworthy features of the species that might be helpful in making an identification. In addition to this information, dichotomous keys are provided that should enable the reader to identify virtually all of the species of myxomycetes known from Australia at the time the monograph was prepared. No monograph of this magnitude is ever complete, and there are certainly some species that are not considered herein. The primary criterion used to include a particular species was that the latter was represented by one or more specimens in a recognized herbarium. However, a number of species were included because they have been reported in print from Australia. Specimens of the vast majority of the species treated in this monograph have been examined by the author, but this is not the case for some of the very oldest records and an appreciable number of the more recent records. As such, there is a possibility that some specimens have been misidentified and the species to which it was referred has yet to be recorded from Australia. Nevertheless, this monograph represents the most comprehensive body of information yet assembled on the myxomycete biota of Australia.

Distribution, Ecology and Importance

Due to the fragile nature of the fruiting body, fossil records of myxomycetes are exceedingly rare. Domke (1952) described a species of Stemonitis and Dörfelt et al. (2003) a species of Arcyria from Baltic amber dating from the Eocene. The maximum age that could be assigned to either of these fossils would not exceed about 50 million years, and the two fossils were almost indistinguishable from their modern counterparts. Phylogenetic reconstructions based on molecular data appear to indicate that the ancestors of myxomycetes may have existed on the earth even before the colonization of land by plants (Fiz-Palacios et al. 2013). Although this seems somewhat problematic, myxomycetes certainly have a long evolutionary history, and at least some representatives of the group occur in virtually every terrestrial habitat examined to date. Moreover, under favourable conditions, these organisms can be relatively common, which suggests that they cannot be ignored as an insignificant component of the earth’s biota.

Although generally regarded as terrestrial, a few species have been recovered from aquatic habitats (Lindley et al. 2007, Winsett & Stephenson 2013), and Dyková et al. (2007) reported that they had identified a possible myxomycete living as an endocommensal of a sea urchin in the Adriatic Sea. Temperature and moisture are thought to be the main factors limiting the occurrence of myxomycetes in nature (Alexopoulos 1963), and species richness tends to increase with increasing diversity and biomass of the vascular plants providing the resources (various types of decaying plant material) that support the microorganisms upon which the two trophic stages (amoeboflagellates and plasmodia) in the life cycle feed (Madelin 1984, Stephenson 1989). Bacteria apparently represent the main food source for both trophic stages, but plasmodia also are known to feed upon yeasts, algae (including cyanobacteria), and fungal spores and hyphae (Lazo 1961, Stephenson & Stempen 1994, Smith & Stephenson 2007). The plasmodia of some species of myxomycetes (e.g. Badhamia utricularis, Fuligo septica and Physarum polycephalum) are known to be capable of producing exoenzymes, thus enabling them to literally consume the fruiting bodies of true fungi. Although the feeding activities of such plasmodia can be quite spectacular, myxomycetes are thought to spend the majority of their life cycle in the amoeboflagellate trophic stage.

Koevenig & Liu (1981) reported carboxymethyl cellulase activity in Physarum polycephalum. This would suggest that at least some myxomycetes might use cellulose as a nutrient source and thus play a role (probably rather limited) in the breakdown of the dead plant material with which these organisms are commonly associated. However, this aspect of the ecology of myxomycetes has received little study.

Microhabitats for Myxomycetes

The fruiting bodies of myxomycetes are especially common in forest ecosystems, where they have been recorded from all of the microhabitats present (Stephenson & Stempen 1994). These include coarse woody debris (decaying wood) on the forest floor, the bark surface of living trees, ground litter, aerial litter (dead but still attached plant parts above the ground) and the dung of herbivorous animals. A few species are found in association with bryophytes and living vascular plants. Each of these microhabitats tends to be characterized by a distinct assemblage of species (Stephenson 1988, 1989; Stephenson & Stempen 1994). Myxomycetes also appear to be among the more common organisms in soil. In fact, recent evidence suggests that they are the most important amoeboid predators in most soils (Urich et al. 2008), making up perhaps half of the protozoan component represented by soil amoebae (Feest & Stephenson 2014). As such, they undoubtedly play a major role in such essential processes as nutrient cycling (Stephenson, Fiore-Donno et al. 2011).

As already noted, the trophic stages of myxomycetes feed mostly on bacteria. In the soil, a major portion of the nutrients present is immobilized in microbial biomass, with the biomass of bacteria being especially important because of their incredible abundance. These nutrients are released from the bacteria through predation, a process that has been termed the ‘microbial loop’ (Bonkowski & Clarholm 2012). Myxomycetes, as one of the more important groups of amoeboid predators in most soils, are therefore responsible for mediating the flow of nutrients from bacteria and other decomposers to the soil and then to plants and higher trophic levels, obviously including the animals that feed upon plants (ultimately involving humans in some instances!). Despite their importance and abundance, myxomycetes are often overlooked in this context because the primary focus of scientists tends to be on soil fungi and bacteria. However, the results obtained from the few studies that have been carried out (e.g. Glücksman et al. 2010) suggested that differences in the taxonomic composition of the assemblage of myxomycetes found in a given soil can have a significant effect on the community structure of the bacteria present. Moreover, Feest & Stephenson (2014) indicated that certain soil amendments, especially the application of the herbicide Dalapon, affected populations of soil myxomycetes. In an earlier paper, Feest & Madelin (1988) reported that populations of soil myxomycetes are clearly dynamic and undergo seasonal changes, a phenomenon that would not seem surprising. Because of the extreme difficulty in studying this system, this aspect of soil ecology is still a ‘black box’ with respect to our overall understanding. Nevertheless, there seems to be abundant evidence that myxomycetes are an absolutely essential biotic component of most soils.

In tropical and temperate rain forests of the world, the presence of an assemblage of vascular and nonvascular epiphytes on the branches and to some extent the trunks of trees contributes to the development of a layer of accumulated organic matter derived from decaying epiphytes, partially decomposed tree bark, insect frass and intercepted litter. This microhabitat, which has been referred to as ‘canopy soil’ (Stephenson & Landolt 2011) is known to represent an ecologically important subsystem of the forests in which it occurs but remains understudied for most groups of microorganisms. Interestingly, Stephenson & Landolt (2015) reported that they recovered myxomycete plasmodia in samples of canopy soil collected in eleven different localities throughout the world, and two of these localities were in Northern Queensland. They went on to indicate that myxomycetes did not appear to be particularly common in this microhabitat but were consistently present in low numbers. Only rarely could the plasmodia be induced to produce fruiting bodies, so the species found in canopy soil could not be determined. However, their data do extend the range of microhabitats known to support myxomycetes and suggest yet another aspect of these organisms that warrants additional study.

The myxomycetes associated with coarse woody debris are the best known ecological assemblage, since they tend to be among those characteristically producing fruiting bodies of sufficient size to be detected easily in the field (Martin & Alexopoulos 1969). Many of the more common and widely known myxomycetes, including various species of Arcyria, Lycogala, Stemonitis and Trichia, are predominantly wood-inhabiting (lignicolous). The amoeboflagellate stage of myxomycetes is actually quite common in wood, although this fact was clearly established only recently (Taylor et al. 2017). It is now known that many thousands of amoeboflagellates can occur in a cubic centimetre of coarse woody debris, where they feed upon the other microorganisms (presumably mostly bacteria) present. It seems likely that the myxomycetes occurring in coarse woody debris mediate the flow of nutrients from bacteria to higher trophic levels in the same manner described above for soil.

Much less is known about the myxomycetes associated with the microhabitats represented by the bark surface of living trees, ground litter, aerial litter and the dung of herbivorous animals. The primary reason for this is that many of the species involved are rather inconspicuous or sporadic in their occurrence and thus difficult to detect in the field. As described in the previous chapter, the myxomycetes associated with these microhabitats are best studied with the use of the moist chamber culture technique.

It should be noted that dung as a microhabitat for myxomycetes has received very little study in Australia in contrast to the bark of living trees, ground litter and aerial litter. Cribb (1993) mentioned that Physarum compressum appeared on a sample of emu dung placed in a moist chamber culture. There seem to be few other reports relating specifically to the myxomycetes associated with dung, although Davison et al. (2008) included some samples of dung in their survey of the myxomycetes of the Simpson Desert. Since dung has been shown to represent a microhabitat of some importance to myxomycetes in deserts (e.g. Novozhilov et al. 2006), additional study definitely seems warranted.

General Patterns of Distribution

Although the myxomycetes are a truly cosmopolitan group of organisms, it does not follow that all species can be found everywhere. Many of the more common species are exceedingly widespread and probably can be collected just about anywhere in the world, but some species appear to be largely or completely restricted to temperate regions of the world and others have been collected only in the tropics. Interestingly, several species that are commonly encountered in temperate regions of the Southern Hemisphere are comparatively rare in temperate regions of the Northern Hemisphere. Two prominent examples are Trichia verrucosa and Metatrichia floriformis. Just why this should be the case is completely unknown. One group of myxomycetes is restricted to subalpine areas of mountains, where its members are found fruiting along the margins of melting snowbanks in late spring and early summer (Ing 1999, Tamayama 2000, Stephenson & Shadwick 2009). The species that occupy this rather special and very limited habitat are usually referred to as ‘snowbank’ or ‘nivicolous’ myxomycetes. They constitute a distinct ecological group, since they produce fruiting bodies only during the relatively brief period of time when the special microenvironmental conditions apparently required for their growth and fruiting exist. During the remainder of the summer, the species of myxomycetes found in these subalpine areas are very much the same as those collected at lower elevations in the same regions. In Australia, suitable habitats for snowbank myxomycetes occur at higher elevations in the Snowy Mountains and the Victorian Alps. The area around Mount Kosciuszko yielded a number of new records for Australia (and in some instances for the Southern Hemisphere) as a result of a survey carried out in 2004 (Stephenson & Shadwick 2009).

Because myxomycetes are almost invariably associated with relatively moist conditions, one might not expect these organisms to occur in arid habitats. However, the number of species reported from arid habitats is surprisingly high (Blackwell & Gilbertson 1980, Novozhilov et al. 2006, Lado et al. 2007). The most productive substrates for myxomycetes in such habitats include the dead parts of living plants, animal dung, and the bark of living shrubs and trees (Schnittler & Novozhilov 2000, Schnittler 2001). Field collections are usually limited to periods of no more than a few days or weeks immediately following a period of significant precipitation, but myxomycetes are exceedingly common in moist chamber cultures prepared with samples of dead plant material collected from arid habitats.

Spatial Distribution Patterns

A major challenge for researchers is determining just which factors in nature are responsible for determining the spatial distribution patterns of particular species, and this is especially true for microorganisms. Although the fruiting bodies of myxomycetes are often large enough to be detected with the naked eye, these organisms spend most of their life cycle as microbes, when it is difficult if not impossible to quantify or even determine their presence or absence in a particular habitat or microhabitat. Historically, studies of distribution patterns in myxomycetes have focused primarily on the assemblages associated with different microhabitats such as coarse woody debris, ground litter or the bark surface of living trees (e.g. Stephenson 1988, 1989). However, in spite of the studies that have been carried out, our knowledge relating to the ecological requirements of particular species of myxomycetes remains very fragmentary, and only a few taxa have been subjected to fairly detailed investigations (e.g. Stephenson et al. 2019). Practically all of these investigations have been limited to data on the occurrence of fruiting bodies, and almost nothing is known about the ecological distribution of the two trophic stages (amoeboflagellates and plasmodia) in the life cycle.

Prior to about half a century ago, distribution data for myxomycetes were based entirely upon field-collected specimens, but more recent studies have incorporated the use of moist chamber cultures (Stephenson & Stempen 1994), and about 40% of all species of myxomycetes are known primarily or even exclusively from specimens appearing in cultures (Schnittler et al. 2015). Species lists are now available for a number of regions of the world (e.g. arctic and boreal zones [Stephenson et al. 2000], Africa [Ndiritu et al. 2009] and the Neotropics [Lado & Wrigley de Basanta 2008]). This is quite unlike the situation that exists for most other protists, for which distributional data are often very limited. A number of recent ecological investigations have gone beyond merely recording the myxomycetes present in a particular locality and have applied modern methods of community ecology to the study of these organisms (e.g. Stephenson 1988; Stephenson et al. 1993; Schnittler 2001; Rojas & Stephenson 2011).

Although recording (and sometimes quantifying) the occurrence of fruiting bodies provides a very worthwhile set of data, it has become increasingly apparent that the trophic stages of myxomycetes, especially the amoeboflagellates, have a much wider distribution in nature than is reflected by records of the fruiting bodies. With the use of molecular techniques, certain free-living amoebae (formerly treated as members of the now invalid genus "Hyperamoeba") were identified as myxomycetes by Fiore-Donno et al. (2010). These organisms have been recovered from artificial as well as natural aquatic environments, but there is no evidence that they ever produce fruiting bodies. Strains of the amoeboflagellates of other species of myxomycetes that have lost the ability to form fruiting bodies are conceivable. Studies that have used molecular methods to investigate the presence of myxomycetes in alpine soils (Kamono et al. 2013) and decaying wood (Clissmann et al. 2015) recovered numerous genetic sequences not yet known from fruiting bodies.

The body of data relating to distribution patterns of myxomycetes in Australia is still rather incomplete, and there are large areas of the country where little or no collecting has been carried out. The primary reason for this is that the number of individuals working with myxomycetes is very small. Australia is not the only region of the world where this is the case, and there are whole countries for which the myxomycetes are very poorly known. Hopefully, the publication of this monograph will result in greater interest in the myxomycetes of Australia.

Substrate pH

The body of information available in the literature consistently indicates that substrate pH represents one of the most important factors affecting the distribution of myxomycetes and thus the composition of the assemblages of species associated with a particular habitat or microhabitat. Some species are regularly reported from substrates characterized by a wide range of pH values. A noteworthy example is the exceedingly common and widespread Arcyria cinerea, which is almost invariably reported in any survey carried out for myxomycetes. This species is often abundant as both field and moist chamber culture collections. Other species seem to be restricted to a much narrower pH range. This is the case for species in such genera as Comatricha and Paradiacheopsis, which tend to be restricted to relatively acidic substrates (pH <5.0 and sometimes <4.0). In contrast, most of the species in such genera as Physarum are associated with more basic substrates (pH >5.0 and often >6.0). The substrates available for myxomycetes in some of the more arid areas of Australia are typically characterized by values of pH >6.0, and the pH of dung sometimes can exceed a pH of 8.0.

The spores of myxomycetes are small enough to be transported by the wind, and it is thought that this accounts for spore dispersal in most instances, although animals also can serve as vectors of spores. In theory, the potential for long-distance dispersal by means of spores (Kamono et al. 2009) would seem to provide myxomycetes with the potential to occur anywhere on the earth, but the actual distribution of most species is usually determined by the availability of suitable microhabitats for their establishment, growth and development (Schnittler & Novozhilov 2000). However, as mentioned earlier, some species are predominantly subtropical or tropical, whereas others are restricted to temperate regions of the world (Stephenson, Schnittler et al. 2008). Some species have been shown to be restricted to a single more limited geographical area (e.g. Leontyev et al. 2015). Low temperatures certainly limit the formation of fruiting bodies in tropical species, which sometimes appear in greenhouses in temperate regions of the world. However, habitat preferences are currently known only from fruiting bodies. Future studies that make use of direct environmental sampling using molecular techniques may provide a very different picture of myxomycete distribution.

Interactions of Myxomycetes with Other Organisms

It is not surprising that various types of interactions exist between myxomycetes and certain other organisms. For example, myxomycetes are known to provide food, shelter and a breeding place to various insects and other invertebrates. Among the most commonly encountered insects associated with myxomycetes are small beetles, often referred to as ‘slime mould’ beetles. Representatives of a number of different taxonomic families of beetles have been collected from the fruiting bodies of myxomycetes. In the Northern Hemisphere, members of the family Leiodidae are especially common associates of myxomycetes, but too few data are available to know just what groups are important in the Southern Hemisphere. It is not unusual to encounter a beetle or two in a large fruiting of Stemonitis, and their ‘entry holes’ are sometimes evident in the peridium of aethalia of Lycogala, Tubifera or Reticulara. In many instances, beetle larvae are present, which suggests that adult beetles located and deposited their eggs in the fruiting body. The beetles (both adult and larvae) feed upon the spores and probably play some role in spore dispersal for certain species of myxomycetes. Other insects known to feed upon myxomycetes are flies and springtails, and mites (a group of non-insect invertebrates) are often found associated with myxomycetes. Slugs also have been reported to actively feed upon myxomycetes (Keller & Snell 2002).

The fruiting bodies of myxomycetes provide an organic substrate subject to being colonized by fungi. The majority of these fungi also occur on other types of substrates, but some species seem to be restricted to myxomycetes (Rogerson & Stephenson 1993). These ‘myxomyceticolous’ fungi have received relatively little attention, but a few species are not uncommon. This is the case for Polycephalomyces tomentosus, which frequently occurs on old fruiting bodies of such species as Metatrichia floriformis and Trichia verrucosa.

Myxomycete–Human Relationships

Since most people are not even aware that myxomycetes exist, one would anticipate that these organisms would not have any direct impact on humans. A few species (e.g. Physarum cinereum and Diachea leucopodia) sometimes produce numerous fruiting bodies on living plants, including various ornamentals, the grasses of parks and lawns, and agricultural crops. However, very little if any damage is done to the plants involved, and the fruiting bodies are washed away with the first rain (Stephenson & Stempen 1994). The rather large fruiting bodies of Fuligo septica are not uncommon on piles of compost or on the layer of mulch that is placed around the bases of trees and shrubs in parks and urban areas. These fruiting bodies, which sometimes can reach the size of a dinner plate and are bright yellow when fresh, are so conspicuous that they are unlikely to be missed by even the most casual observer. However, just as in the case of their smaller counterparts, these larger fruiting bodies are soon washed away by rain.

Although it is difficult to think of myxomycetes as food for humans, a few of the very largest species, including Fuligo septica and Reticularia lycoperdon, are consumed by some of the indigenous people of southern Mexico. The very early developing fruiting bodies are collected, fried along with such other food items as onions and peppers and eaten on a tortilla (Keller & Everhart 2010). The consistency of the fruiting body at a very immature stage, when it is still developing from the plasmodium, is not unlike that of a scrambled egg. The cooked myxomycete has been reported by some people to taste something like an almond.

Interestingly, myxomycetes have been shown to bioaccumulate heavy metals such as zinc, cadmium, iron, manganese and strontium, sometimes to amazingly high levels. For example, the fruiting bodies of Fuligo septica have been reported to contain levels of zinc higher than 3,000 mg/kg (dry weight) as opposed to the much lower levels (10–160 mg/kg) found in vascular plants collected from comparable habitats (Stijve & Andrey 1999). Stephenson & McQuattie (2000) suggested that myxomycetes might have some potential value as biomonitors of heavy metals in environmental assessments.

Myxomycetes are known to produce novel secondary compounds that display various types of biological activity (Steglich 1989, Ishibashi 2005, Dembitsky et al. 2005). For example, exopolysaccharides isolated from myxomycetes have been demonstrated to possess antibiotic activity against fungi and bacteria (Huynh et al. 2017). In general, most bioactive compounds from myxomycetes have been shown to display their strongest inhibition effects on gram-positive bacteria, with low or no inhibition effects on gram-negative bacteria (Tran & Adamatzky 2017). Inhibitory effects on fungi appear to vary considerably for the (still relatively few) species of myxomycetes that have been evaluated (Herrera et al. 2011). However, antifungal activity has been reported to be clearly present for compounds derived from such species as Physarum polycephalum, and these compounds appear to have potential for treating the yeast Candida albicans, the most prevalent cause of fungal infections in humans (Huynh et al. 2017),

Other bioactive compounds have been shown to exhibit inhibitory activity against a number of human cancer cells lines. Anticancer compounds include various alkaloids (e.g. arcyriaflavin C and makaluvamine A) and cycloanthranilylproline (fuligocandin B), all of which have been isolated from the plasmodia or fruiting bodies of myxomycetes (Tran & Adamatzky 2017). Some of these compounds have the potential of being developed into drugs that would warrant clinical trials, with the possibility of ultimately being becoming important in medicine. This has already been demonstrated in a few instances. For example, beta-poly (L-malic acid) harvested from a microplasmodial culture of P. polycephalum can be used for the synthesis of polycefin, which has been used as an effective drug delivery system for treatments of brain tumors (Lee et al. 2006).

One of the more remarkable results of medical importance obtained thus far was reported by Loganathan (1998), who found that 3,4-dihydroxyphenylanine (L-DOPA), a neurotransmitter precursor used in the treatment of Parkinson’s disease, possibly could be produced at a commercial scale from compounds obtained from the myxomycete Stemonitis herbatica. It is likely that other species of myxomycetes could be used in the same manner.

The plasmodium of some myxomycetes such as Fuligo septica, Physarella oblonga and Physarum polycephalum can reach a considerable size, and plasmodia are known to be rich in lipids. Tran et al. (2012) evaluated the potential of P. polycephalum as a possible source of lipids that could be converted into biodiesel. They found that the major lipids found in the plasmodium of P. polycephalum plasmodia are triglycerides, which are ideal for the production of biodiesel. Other microorganisms (e.g. algae) have been evaluated for their potential for producing biodiesel, but myxomycetes have an advantage because the plasmodium lacks cell walls, making the extraction of lipids a more efficient process.

In brief, myxomycetes are neither pathogenic nor currently of any economic value, but they may end up being important to mankind in ways that one could never have imagined! As such, they serve as an example of the need to examine other understudied groups of microorganisms for their potential usefulness to humans.

Eumycetozoa

Phylum Eumycetozoa L.S.Olive, The Mycetozoans: 4 (1975).

The phylum Eumycetozoa, as considered herein, consists of the monophyletic assemblage represented by three taxonomic classes. These are the Dictyosteliomycetes (the dictyostelid cellular slime moulds or just simply dictyostelids), the Ceratiomyxomycetes and the Myxomycetes. Only the last two of these classes are treated in this monograph. As mentioned earlier in this book, the organisms placed in the class Ceratiomyxomycetes are now regarded as representing a sister group to the ‘true’ myxomycetes, which belong to the class with the same name. However, members of the Ceratiomyxomycetes have always been studied along with the myxomycetes and included in virtually every publication dealing with the latter. This is the same approach used herein.

The Dictyosteliomycetes, although related to the myxomycetes, are fundamentally different in both their life cycle and overall morphology. These organisms are common to sometimes abundant inhabitants of forest soil and leaf litter (Stephenson & Stempen 1994), where they feed primarily on bacteria. However, both the vegetative stage and the reproductive stage in their life cycle are microscopic