The Genera of Hyphomycetes
Introduction I. Overview tion, number of accepted species, anamorph–teleomorph connections (asexual reproductive structures linked to sexual reproductive structures), GenBank accession numbers for DNA barcodes, notes, and a bibliography. The targeted taxonomic level is explicitly the genus. The bibliographies for each genus include all relevant references to monographs, revisions or other publications that can be used to confirm genus identifications or identify individual species. Finally, because morphological variation in some hyphomycete genera is considerable, and can be deceptive, we include a few additional drawings or photographs illustrating the variation among species of some genera. The Synoptic Plates (pp. 481–866) contain line-drawings of the type or other representative species of most accepted hyphomycete genera, arranged according to morphological similarities. Some genera that do not lend themselves well to illustration (such as sterile, yeast-like or sclerotial genera) are not illustrated. To be successful with this book, you should study the arrangement of plates to understand the underlying logic necessary to use them for identification purposes. Each plate has a thumb tab on the margin of the page noting its major unifying features. These synoptic plates should help you distinguish similar genera, allowing you to compare genus concepts visually and intuitively without the need to consider the details and specialized terminology of the dichotomous keys. The Keys section (pp. 867–942) includes dichotomous or polychotomous keys to several ‘generic complexes’ or ecological groups, providing another way of arriving at a genus identification. Several keys were prepared for this book by taxonomic specialists, and we adapted others from the literature. The task of assembling a functional dichotomous key for all genera was not possible during this project, but we believe the included keys will be helpful. The Appendices (pp. 943–997) contain information extracted from the Dictionary, namely a putative classification that distributes hyphomycete genera into ascomycete or basidiomycete classes, orders and families suggested by their phylogenetic or teleomorphic relationships, a list of anamorph–teleomorph connections
Fig. 1. Early illustrations of hyphomycetes. A. Alternaria tenuis from Nees (1816). B. Tubercularia vulgaris from Tode (1790). C. Acremonium alternatum from Ditmar in Sturm (1817). D. Stachybotrys atra from Corda (1837). E. A Hypocrea perithecium in section, with its Trichoderma anamorph growing from the top, from Tulasne & Tulasne (1863).
3
Overview
This book is a gateway to a hidden world invisible to most people. Its purpose is to assist scientists, students, and other naturalists to identify hyphomycetes (microscopic fungi that are often called moulds) to the level of genus. You can reach this goal by learning the terminology and concepts presented in this Introduction, scanning the synoptic plates, or by using the selection of dichotomous keys in the fourth part of the book. The Dictionary provides concise information on each genus and directs you to literature on species identification. This section also includes information on substrates, geographical distribution, teleomorphs, synanamorphs, DNA barcodes and the phylogenetic position of each genus. Our book is a complete revision and expansion of Carmichael, Kendrick, Conners & Sigler’s 1980 work Genera of Hyphomycetes, which was itself based on a book chapter by Kendrick & Carmichael (1973). We incorporated and expanded on successful elements of these works, added new features, and updated information to facilitate study of these fungi. The book contains four main sections, three appendices, and a glossary. In the Introduction (pp. 1–60), we present basic information on the naming, biology and taxonomy of hyphomycetes. If you are unfamiliar with these organisms, careful reading of this section is essential. Even if you are experienced with these fungi, this section will provide insight into the suites of traits used to characterize the accepted genera and how we use these to arrange them for identification purposes in the synoptic plates. The Introduction provides overviews of: (1) the history of the classification of hyphomycetes; (2) the rules that govern their names; and (3) the characters that are used to classify and identify them. We conclude with an explanation of the organization of the Dictionary, including definitions of the many abbreviations, and recommendations to other helpful books and Web sites. The Dictionary (pp. 61–479) contains text records for every described genus of hyphomycetes (to the end of 2009, with some coverage for 2010 and 2011). Each genus record contains full bibliographic details, synonymies, key word descriptions that summarize genus concepts, details of substrates, geographical distribu-
What are fungi?
Seifert, Morgan-Jones, Gams & Kendrick arranged by teleomorph genus, and a list of synanamorph connections. The Glossary (pp. 961–977) is an alphabetical list of additional specialized terms used in this book, along with their definitions, to assist with the interpretation of genus descriptions and dichotomous keys. We have not written a section on methodology, but some information is provided in text boxes in the plates, as listed on p. 481.
II. Classification and phylogeny A. What are fungi? Mycologists define true fungi as heterotrophic, absorptive eukaryotes, generally with cell walls of β-glucan and chitin (although a few have lost chitin or even their entire wall during evolution). Fungi are generally aerobic, their organelles including mitochondria with flat cristae, and peroxisomes (although two small extant groups are obligately anaerobic and have lost these organelles). Fungi lack plastids. The earliest fungal cells had a single backward directed flagellum, but most extant fungi have lost this feature. The somatic expression of most fungi is hyphal, and the linear growth and branching of hyphae give rise to mycelial colonies that are extensive in some cases, but the fungal spectrum also includes many nonhyphal forms, and some extremely reduced unicells (see Cavalier-Smith 2001, Blackwell et al. 2006). By these criteria, estimates of the number of fungal species generally vary from 1.5 to 15 million species, with fewer than 100,000 presently described (Hawksworth 2001). Although linked by their evolution, fungi are still diverse, particularly when you consider the giant colonies of Armillaria at one end of the spectrum (the ‘humungous fungus’), and Nosema, an intracellular insect pathogen, or the unicellular Pneumocystis, which causes pneumonia, at the other. Traditionally the group was even more heterogeneous, because fungi, slime moulds, and bacteria were sometimes lumped together as members of the Phylum Thallophyta of the plant kingdom. As related by Whittaker (1969), various authors suggested that fungi were not plants up to two centuries ago, and that slime moulds should be excluded from the fungi. It was not until the advent of the electron microscope in the 1950s that the majority of biologists accepted the fundamental separation between what was first presented
Fig. 2. Triposporium elegans, as illustrated in Corda’s Prachtflora europäischer Schimmelbildungen (1839).
as Lower Protists (bacteria and prokaryotic blue-green algae, which are now often called the Prokaryota) and Higher Protists (eukaryotic organisms: fungi, protozoa, and algae). Subsequently, the Lower Protists, the Fungi, and the Protozoa were recognized as separate Kingdoms (Whittaker 1969). In general, we now recognize that living things have evolved into three phylogenetic domains, a) Eukarya (eukaryotes), b) Bacteria and c) Archaea. The fungi are a phylogenetically coherent, kingdom-level subgroup of eukaryotes. The slime moulds have been accepted as protozoa by protozoologists (e.g., Kudo 1946) ever since de Bary (1859, Fig. 4A) first named them Mycetozoa. However, mycologists are reluctant to disown them, probably because it is they, and not protozoologists, who study this group. Here, we prefer to call the well-known ‘plasmodial slime moulds’ Phylum Mycetozoa (increasingly known as Myxostelida, or informally myxostelids) rather
Fig. 3. Early mycologists who had a profound influence on hyphomycete taxonomy. A– C.H. Persoon (1761–1836). B– E.M. Fries (1794–1878). C– J.H.F. Link (1767–1851). D– A.C.J. Corda (1809–1849). E– P.A. Saccardo (1845–1920) (public domain).
4
The Genera of Hyphomycetes project, and provides a comprehensive overview of all fungal groups from a phylogenetic perspective (Spatafora 2005, Blackwell et al. 2007, Hibbett et al. 2007). The latter project provides the basis for most of the larger scale phylogenetic trees presented in this introduction, which show the relationships of selected hyphomycete genera in the series starting with Fig. 6.
B. What are hyphomycetes? Hyphomycetes make up the majority of what are commonly called moulds1, and some are regarded as the weeds of the fungal kingdom. In addition to growing on many natural substrates such as plant tissues (Fig. 5), wood and bark (Fig. 7), dung (Fig. 12), insects and other arthropods (Figs 14, 22), and other fungi (Fig. 16, 38B) including lichens (Fig. 18), and in a diversity of ecological habitats, moulds are involved in food spoilage, contaminate many manufactured materials such as wood, paper and textiles, and are frequent visitors to the human indoor environment. Some hyphomycetes are asexually reproducing parts of the life cycle of sexually competent ascomycetous and basidiomycetous fungi. The asexually, or mitotically, reproducing structures are called anamorphs; the sexually reproducing, or meiotic, counterparts of the same life cycle are called teleomorphs. Together, these forms of sporulation make up a whole fungus, or holomorph (Fig. 4, Hennebert & Weresub 1977, Weresub & Hennebert 1979). In some cases, anamorph and teleomorph develop side-by-side, but more commonly they mature at different times, or on different substrates. Historically, the establishment of anamorph–teleomorph connections was difficult. Although thousands of connections are known, the majority of hyphomycetes remain orphaned. It seems almost certain that many anamorphs have permanently lost the potential to mate or to develop a teleomorph, and must be regarded as anamorphic holomorphs. Mycologists must classify such anamorphic holomorphs pragmatically, using whatever characters are available. Mycologists generally recognize three major groups of anamorphic fungi. None of these three groups is a homogeneous, phylogenetically based taxon: they are polyWe consider ‘mould’ the correct spelling for a fungus, reflecting its etymological origin from the English ‘moul’, different from ‘mold’, i.e. a container for making a shape.
1
Fig. 4. The first anamorph-teleomorph connection. A. Discovered by Anton de Bary (1831–1888) (public domain). B. Aspergillus anamorph (green) and Eurotium teleomorph (yellow) in one agar colony. C. Conidiophores of Aspergillus anamorph of Eurotium. D. Eurotium teleomorph, optical section of ascoma on left, ascospores in asci on right. The teleomorph and anamorph together comprise the holomorph.
5
What are hyphomycetes?
than Myxomycetes or Myxomycota, because the endings ‘-mycetes’ or ‘-mycota’ imply a fungal nature, and we refer them to Kingdom Protozoa. The ‘cellular slime moulds’ (Phylum Dictyostelida), the ‘net slime moulds’ (Phylum Labyrinthulida) and the ‘endoparasitic slime moulds’ (Phylum Plasmodiophorida) are now also classified in the Kingdom Protozoa. Even with slime moulds excluded, the organisms we generally call ‘fungi’ are not monophyletic. Organisms that look distinctly fungal under the light microscope, because in many cases their colonies are built up of branching hyphae, are now placed in two different Kingdoms. The ‘water moulds’ and ‘downy mildews’ of Phylum Oomycota (and the tiny Phylum Hyphochytriomycota) are now understood to belong in Kingdom Chromista (sometimes called Stramenipila), the Kingdom that also contains the diatoms and the brown algae. These Chromistan pseudofungi differ from true fungi in many important ways: their heterokont flagellation, a wall chemistry that includes cellulose, somatic ploidy, mitochondrial cristae, lysine biosynthesis, etc. After the slime moulds and the pseudofungi are excluded, the true Fungi comprising the Kingdom Eumycota remain, as defined in the first paragraph of this section. The hyphomycetes are all members of this Kingdom, but they are found in two different Phyla, the Ascomycota and the Basidiomycota. We currently recognize six Phyla (also known as Divisions) in Kingdom Eumycota or the Fungi (see Kendrick 2010): Phylum Chytridiomycota Phylum Zygomycota Phylum Glomeromycota Phylum Ascomycota Phylum Basidiomycota Phylum Microsporidia (recently recognized as reduced or secondarily simplified fungi, but still under zoological nomenclatural rules). The phyla Ascomycota and Basidiomycota together comprise the subkingdom Dikarya. It is unnecessary for us to describe and differentiate the major fungal groups here. Motivated readers can pursue this matter in Cavalier-Smith (2001), Kirk et al. (2008), and Kendrick (2010), or other modern general mycology texts. The Nov.–Dec. 2006 issue of Mycologia includes the results of the ‘Assembling the Fungal Tree of Life’
What are hyphomycetes?
Seifert, Morgan-Jones, Gams & Kendrick phyletic assemblages, with lower-case initial letters and not italicized, as indicated here: •blastomycetes: asexually reproducing yeasts, including some ascomycetes, i.e., Saccharomycetales, and some basidiomycetes (i.e., Urediniomycetes such as the Sporidiales, Ustilaginomycetes, and in the Agaricomycetes the Tremellomycetidae such as the Filobasidiales). •coelomycetes: pycnidial and acervular fungi, most ascomycetous, a few basidiomycetous. •hyphomycetes: moulds lacking pycnidial or acervular fruiting-bodies (conidiomata), most ascomycetous, some basidiomycetous. This book deals only with the third group. Hyphomycetes are defined as those usually hyphal anamorphs in which the conidia (mitospores) or other reproductive bodies (bulbils, sclerotia) are developed ‘out in the open’. This is in contrast to the conidia of the coelomycetes, which develop inside an initially closed structure. Anamorph genera based on sterile mycelia and on mycelia producing only bulbils or sclerotia are also often dumped into the hyphomycetes (as the ‘Agonomycetes’), faute de mieux. Some of these genera are listed in the Dictionary, although generic names applied to sterile thalli or mycelium of lichenized fungi are not included. The name Deuteromycota (or Deuteromycetes) was long used for the anamorphic fungi and is still regrettably common. We consider this term archaic and misleading, because it implies that hyphomycetes and coelomycetes represent a phylum equivalent to the other six. As Kendrick (1981, 2005), Taylor (1995) and others insisted, this completely artificial construct should be abandoned. The anamorphs of the Phylum Zygomycota, and of the classes Urediniomycetes and Ustilaginomycetes (Phylum Basidiomycota), are traditionally referred to the appropriate holomorphic taxa in these Phyla, and are not usually included in the hyphomycetes although they could be mistaken for such based on their appearance. Because of morphological similarities between anamorphs of some Zygomycetes and some hyphomycetes, there are several genera that were originally described as members of one group but later shown to belong to the other. Anamorphic forms of the Zygomycota are mentioned in this book when they are morphologically similar to hyphomycetes. The morphological distinctions between the hyphomycetes and the other two groups, blastomycetes and coelomycetes, are not absolute, and intermediates occur.
Anamorph genera such as Geotrichum, Hormonema, and Aureobasidium, are usually placed in the hyphomycetes but could almost equally well be considered blastomycetes. Except for a few mycelial yeasts such as Geotrichum, we do not attempt to deal with the asexual yeasts (anamorphs of the Saccharomycetales and Sporidiales), whose reduced morphology often does not lend itself to micromorphological identification. They are monographed in other publications (e.g., Barnett et al. 2000, Kurtzman et al. 2010). Although there are groups of ascomycetes with predominantly hyphomycetous anamorphs and other groups with predominantly coelomycetous anamorphs, other groups exhibit both types of anamorph. Some species produce both hyphomycetous and coelomycetous synanamorphs (e.g., many strains of the hyphomycete Epicoccum nigrum produce a coelomycetous synanamorph classified in Phoma). Thus, the difference between these two morphological groups is phylogenetically ambiguous, but for morphological identification purposes the distinction is critical. Pycnidial and acervular anamorphs are usually considered to belong to the coelomycetes while sporodochial anamorphs are classified in the hyphomycetes. However, intermediate forms occur between these three types of conidiomata (see Kendrick & Nag Raj 1979). The coelomycetous conidiomata known as acervuli are defined partly on their location in host tissue. Such conidiomata either cannot be formed in agar culture (cf. Barron 1968, pp. vii and 6), or they instead produce discrete conidiophores or sporodochium-like conidiomata that are similar to hyphomycetes. In our list, we include less complete documentation for some genera with acervular conidiomata when we thought this might be useful (e.g., Colletotrichum), but we neither intended nor attempted to cover coelomycetes. An identification guide to genera and species of coelomycetes, with many illustrations, was published by Sutton (1980), and illustrations of many species appear in the multi-authored Icones Generum Coelomycetum (Morgan-Jones et al. 1972–1981) and in the superb book by Nag Raj (1993) on coelomycetes with appendaged conidia.
C. Historical trends in hyphomycete taxonomy As with most organisms, the first taxonomic research on hyphomycetes occurred in central and northern Europe, and was followed by explorations in North America. Although there were sporadic surveys in other parts of
Fig. 5. Hyphomycete colonies on plants. A. Monilinia fructigena brown rot of plums (B. Kendrick). B. Bud blast of Rhododendron caused by Seifertia azaleae (P. Crous). C. Ramularia diervillae leaf spots on Diervilla lonicera. D. Fusarium graminearum on maize (AAFC).
6
The Genera of Hyphomycetes
Early hyphomycete taxonomy
Sordariomycetes Laboulbeniomycetes Leotiomycetes Geoglossomycetes
Lecanoromycetes
Pezizomycotina Eurotiomycetes
Ascomycota
→Fig. 20
Lichinomycetes Dothideomycetes Arthoniomycetes Pezizomycetes Orbiliomycetes Saccharomycetes
Saccharomycotina Taphrinomycotina
Agaricomycetes
Agaricomycotina
Basidiomycota
Dacrymycetes Tremellomycetes Ustilaginomycetes Exobasidiomycetes Pucciniomycetes Agaricostilbomycetes Microbotryomycetes
Ustilaginomycotina Pucciniomycotina
Fig. 6. Phylogenetic tree showing the relative arrangement of major classes and orders of the Dikarya, based on a multiple gene analysis. Taxa with a high concentration of hyphomycetous anamorphs are in green text. For all tree figures, methods and statistics are given in Appendix 5.
the globe, it was not until the mid-twentieth century that the moulds of the Indian subcontinent and then Japan and New Zealand were studied with any intensity. In the 1980s, many apparently endemic genera and species were described from the Caribbean (especially Cuba). In the 1990s, international interest in biodiversity stimulated studies of the hyphomycetes of Asia (especially Hong Kong and Thailand), South Africa, and in recent years China. As a consequence, we have the most comprehensive knowledge of the hyphomycetes of the northern temperate regions and less developed understanding of many tropical and subtropical areas. Several regions are still essentially unexplored.
Most early mycologists, including Tode (1791, see Fig. 1B), Persoon (1801, Fig. 3A), Link (1809, Fig. 3C) and Fries (1832, Fig. 3B), included hyphomycetes in their classification systems. A remarkable degree of subtlety of description was achieved with a hand lens, and many of the genera and species proposed by these authors are still used today. The pioneer in the microscopic study of hyphomycetes was A.C.J. Corda (Fig. 3D), whose Icones Fungorum (Fig. 1D, 1837–1842), Prachtflora (Fig. 2, 1839), and contributions to Sturm’s Deutschlands Flora (1829–1837) were the first glimpses into the microfungal realm. Corda’s drawings and paintings of hyphomycetes and coelomycetes were sometimes fanciful but commu-
Fig. 7. Hyphomycete colonies on wood. A. Trichoderma sp. B. Bispora antennata (W. Gams). C. Cladosporium sp. D. Conoplea juniperi (K. Hodge, K. Loeffler).
7
Conidiomata
Seifert, Morgan-Jones, Gams & Kendrick
Fig. 8. Some conidiomatal types in hyphomycetes. A–F. Synnemata. A, B. Determinate with terminal, slimy conidial masses. C–E. Indeterminate with terminal and subterminal conidiogenous cells. F. Branched. G–J. Sporodochia in cross section. J. With cupulate hymenium, somewhat intermediate between typical sporodochia and acervular conidiomata.
nicated the complexity and beauty of these microfungi for the first time (Fig. 2). Preuss and Ditmar (in Sturm 1851, see Fig. 1C) improved the accuracy of the microscopic drawings. Then the Tulasne brothers (1861–1865) published magnificent microscopic illustrations prepared with a drawing prism (Fig. 1E), showing for the first time the physical connections between certain anamorphs and associated teleomorphs. Below, we focus on the two major historical developments that continue to be relevant to modern hyphomycete taxonomy, the sporological system developed by Saccardo and his followers, and the ontogenetic system developed by Hughes (1953) and subsequent workers. 1. The Saccardoan system The most successful early efforts in the taxonomy of hyphomycetes used characters that parallelled traits also
emphasized in teleomorph classifications. Saccardo (Fig. 3E) was an assiduous mycologist (1845–1920) who Latinized and compiled all published descriptions of fungi in a series called Sylloge fungorum hucusque cognitorum, which eventually spanned 26 volumes (some later volumes completed by his relatives or colleagues). Saccardo developed a system for classifying all fungi according to fruiting-body type, pigmentation, and spore morphology (the ‘sporological’ system). The taxonomic practice of establishing a rigid hierarchy of morphological characters and then sorting organisms according to a strict interpretation of these phenotypes, regardless of whether the result is a phylogenetically natural classification, is often called ‘pigeon-holing’. Despite its artificiality, the practicality of Saccardo’s system made it very useful and it was applied by Clements & Shear (1931) in their influential book The Genera of Fungi. This system was also applied
Fig. 9. Sporodochial hyphomycetes. A. Bactridium flavum. B. Trichoderma spirale. C. Tubercularia vulgaris (yellow) and its teleomorph Nectria cinnabarina (red). D. Myrothecium inundatum.
8