Contributions to our
understanding of trichomycetes have come from a large number of
individuals, as can be confirmed by perusing the world literature
linked to this treatise. The historical sketch that follows will
be limited to the relatively few individuals who have made
especially notable contributions or who have in some way
influenced concepts or helped to establish trends within the
field. The reader is referred to publications by Duboscq et al.
(1948), Manier (1950, 1969b), and Moss (1972) for additional
comments of a historical nature, particularly concerning the
earlier developmental years. We are indebted to Mlle. Manier for
some of the biographical information in this chapter. Manier
(1969b) offered the opinion that trichomycete studies can be
conveniently divided into four periods of development, an opinion
that the writers share and follow in this presentation. These
periods are defined not so much by the span of contributions by
individual investigators as they are on new discoveries and
emphases within each time frame.
The period 1848 to 1904 was initiated by Joseph Leidy's discovery of several species of Eccrinales within the hindguts of millipedes and a beetle and publication of their descriptions under the generic name Enterobryus (and Eccrina, now a synonym). Leidy, a noted American naturalist with a talent for investigating new organisms ranging from bacteria and nematodes to fossil mammals, thought these eccrinids were colorless algae related to the Confervaceae. Thus began a conflict on the concepts of relationships of such gut inhabitants, now known as the Trichomycetes, which is still not fully resolved (see Chapter 12). Charles Robin (1853), in his classic book on "plants" that parasitize man and animals, discovered in France another species of Enterobryus, but thought Leidy's organisms and his might be related to the fungal order Saprolegniales. Shortly thereafter, in the 1850s, a different kind of arthropod associate, which lived on the exoskeleton of a variety of aquatic arthropods, was discovered in Europe by Lieberkühn and, independently, by Schenk; it was named Amoebidium parasiticum by Cienkowski a few years later. This organism was variously ascribed to the algae, lower fungi, or protozoans by these and other biologists of that period. In 1895, Hauptfleish described a second genus of Eccrinales, Astreptonema, from the hindgut of an amphipod, and suggested his new species belonged to the Saprolegniaceae. This ended the first period, covering more than half a century, wherein two different groups but very few species of these unusual organisms were found, studied, and debated.
The period 1905 to 1928 was marked by the discovery of numerous other Eccrinales, primarily by French protozoologists, most of whom were interconnected through their professional interests and careers. The most notable collaborators of this period were L. Léger and O. Duboscq; the latter had been Léger's student at Grenoble. In 1905 the two initiated a series of morphological and taxonomic studies on eccrinids from marine crustaceans, millipedes, and hydrophilid beetles. These and subsequent studies by Léger and Duboscq eventually culminated in their 1948 monograph, published posthumously with Odette Tuzet. In 1906(a), Edouard Chatton began the most thorough investigations of the time on the biology of Amoebidium species, including a few experimental studies on host specificity and the effects of environmental parameters on morphological development. In 1927, Raymond Poisson started publishing on new genera and species of eccrinids from amphipods and isopods, and his later studies through the mid-1930s were expanded to include other groups of trichomycetes as well. The major contributions from 1905 to 1928 by these French biologists were the discovery and study of species of Eccrinales and Amoebidiales, the establishment of some early classification systems for the known species, and the consensual belief that they were some kind of fungi. The only mycologist to study any of the gut fungi during this period was Roland Thaxter, who described Enterobryus compressus (= Passalomyces compressus) from the passalid beetle.
The period 1929 to 1959 began with the discovery of the first species of Harpellales, Harpella melusinae, by Léger and Duboscq. That same year (1929) they also named the only endocommensal genus of Amoebidiales, Paramoebidium, and Poisson described the interesting eccrinid genus Parataeniella (Parataeniellaceae). Two years later Poisson discovered the genus Asellaria, which is now placed in the last of the four orders of trichomycetes, the Asellariales. Léger began a series of publications in 1932 with Marcelle Gauthier, who had been his assistant at Grenoble, describing many new genera of branched Harpellales (Legeriomycetaceae), and Gauthier by herself published on several new taxa of this order. By 1947, when Tuzet and Manier discovered the eccrinid genus Palavascia (Palavasciaceae), representatives of all presently recognized families had been described.
The years 1929 to 1959 were primarily a period of description and enlargement of the number of known species and host types, as well as studies on the morphology and ecology of these fungi. There was a growing realization that the trichomycetes had a worldwide distribution, thanks to the curiosity of many scattered investigators who became aware of their existence. This awareness was aided by the publication of the first comprehensive treatment of the eccrinids (considered then to be the Eccrinales and Amoebidiales) by Duboscq, Léger, and Tuzet in 1948. They introduced the term Trichomycetes and provided a classification of all genera recognized at the time, but the body of the monograph excluded what are now called the Harpellales and Asellariales. Odette Tuzet had served as Duboscq's assistant at the Mediterranean laboratory of the University of Paris at Banyuls, and some years later she became head of the invertebrate zoology laboratory at the Université de Montpellier (later to become part of the Université des Sciences et Techniques du Languedoc) where Duboscq had been located from 1903 to 1926. Duboscq died in 1943, and using in part his extensive notes, Tuzet and Léger completed the 1948 monograph. Léger passed away in Grenoble a few months before it came off the press.
Jehanne-Françoise Manier in 1950 (1951) published the thesis of her Docteur d’État, which she earned from the University of Paris under Mlle. Tuzet. It was a major publication on trichomycetes, for it covered all groups of these fungi. Mlle. Manier worked in Tuzet's laboratory in Montpellier, in time becoming a Maitre de Recherches of the Centre National de Recherches Scientifiques. Tuzet and Manier started publishing a series of jointly authored papers in 1947, and this continued for two decades. After 1950 Manier, by herself and with her students and other collaborators, published extensively on many aspects of the biology of trichomycetes, and she was undoubtedly the most influential investigator of these fungi in Europe on her retirement in 1981.
The period 1960 to 1985 represents a time of considerable change and maturation in trichomycete studies. In 1960 Howard C. Whisler, then a graduate student at the University of California at Berkeley, reported the successful isolation of the first trichomycete, the ectocommensal Amoebidium parasiticum. These axenic isolates permitted Whisler to conduct the first in vitro experiments on the nutrition of Amoebidium and to study under controlled conditions the factors that lead to amoebagenesis. Three years later the entomologists Clark, Kellen, and Lindegren in the Fresno mosquito laboratory in California isolated the first two species of the endocommensal genus Smittium from mosquito hindguts. This was followed by Lichtwardt's isolations of many strains of several species of Smittium from various kinds of dipteran larvae and, by Peterson, of species of two monotypic genera, Genistelloides and Capniomyces, from stonefly nymphs. The Smittium isolates have served as the basis for a variety of experimental studies, reviewed in Chapter 9.
Lichtwardt's interest in the trichomycetes began with the Eccrinales when he was a graduate student at the University of Illinois, and his investigations expanded to all of the families of trichomycetes after he joined the faculty of the University of Kansas. There he was fortunate to direct the studies of a number of graduate students who contributed materially to our understanding of the biology of trichomycetes, primarily through the use of experimental methods, but also by investigating the fine structure of cultured and uncultured species. These students, listed chronologically, were David F. Farr, Mary E. Chapman, Vijay K. Sangar, Marvin C. Williams, A.M. El-Buni, Thaddeus R. Preisner, Anne M. Starr, Si-nan Dang Mayfield, Bruce W. Horn, and Stephen W. Peterson.
Early in the 1960s, before axenic cultures of the gut fungi were generally available, Manier, Tuzet, and collaborators began laboratory studies on cross-infestation and host specificity of trichomycetes (Chapter 6). In the mid 1960s electron microscopic studies began with Farr's work on cultured Smittium culisetae and electron micrographs of Enterobryus oxidi by Tuzet, Manier, and Oustau. Such studies were extended very soon to many other species by investigators in France, the United States, and England. Stephen T. Moss was a student at the University of Reading in the early 1970s when he completed his dissertation on the fine structure, ecology, and general biology of trichomycetes, and he has since provided some of the most elegant electron micrographs and interpretative studies of some of these fungi. Moss spent 18 months in the mycology laboratory at the University of Kansas after earning his degree, and this led to several collaborative studies with Lichtwardt that continued after Moss's return to England.
By 1960 the taxonomy of trichomycetes had become confusing, if not rather chaotic, for the literature contained many illegitimate type species and ill-defined or synonymous genera. Manier and Lichtwardt attempted to rectify this problem by publishing a manuscript in 1968 (1969) that dealt with the trichomycetes to the generic level. In 1969(b) [1970(b)] Manier published a paper on the Trichomycetes of France, and it has remained the major monograph on the systematics of these fungi prior to the present worldwide treatise. Aspects of the biology of the trichomycetes were reviewed by Lichtwardt in 1976 and by Moss in 1979. Another publication of note in the 1970s was Jolly Hibbits' (1978) publication on marine Eccrinales, based on her Master's thesis done under the direction of Whisler at the University of Washington.
The consequences of the studies from 1960 to 1985 include a better appreciation of the complexities of the relationships between the trichomycetes and their arthropod hosts (Chapter 8). Sweeney's (1981a) discovery and axenic isolation of Smittium morbosum substantiated earlier reports from Italy and Russia that some species were highly lethal to mosquito larvae in laboratory cultures, and at the same time demonstrated that within the wide range of trichomycete species not all were necessarily benign. Another form of pathogenicity in species of Harpellales was elucidated when Moss and Descals determined that one type of fungal cyst that had been reported infecting the ovaries of adult blackflies was, in fact, a stage in the cycle of Harpella melusinae. Subsequently, it was found that other Harpellales living in aquatic insect larvae had this same pathogenic stage which serves as a mechanism of dissemination when the infected adult, though sterile, "oviposits" the cysts in new breeding sites (Chapter 8).
That Harpellales might also benefit their hosts was demonstrated when Horn raised mosquito larvae of Aedes aegypti on defined media deficient in particular nutrients (Chapter 8). Larvae artificially infested with the harpellid Smittium culisetae survived better and matured faster than those without the fungus, demonstrating that metabolites manufactured by the fungus could benefit the host when they were deprived of certain essential nutrients. Thus, the type of symbiotic relationship between gut fungi and their hosts may depend upon particular circumstances.
The period 1986 to date began with the publication by Lichtwardt (1986) of the first comprehensive monograph on Trichomycetes, which is now revised with Matías J. Cafaro and Merlin M. White while working on their Ph.D. degrees in Lichtwardt’s laboratory. As indicated in the Preface to the Revised Edition, support from the National Science Foundation, especially through an NSF PEET award (DEB 9521811), has led to an accelerated pace of studies on the biology and systematics of gut fungi. Involved in this project, in addition to the co-authors of the present monograph, have been Co-PI, Leonard C. Ferrington, Jr., Roger D. Grigg, J.K. Misra, Alexandra Gottlieb, Claudia López Lastra, María Gabriela Mazzucchelli, Amy L. Slaymaker, and Barbara L. Hayford. New knowledge about Trichomycetes has come from several collaborators or associated researchers during the past decade and a half. These include Kerry L. O’Donnell, Stephen W. Peterson, Bruce W. Horn, and Marvin C. Williams. (See web page www.nhm.ku.edu/~fungi.)
Many additional biologists who were not active in working with gut fungi prior to 1990 have taken up studies on Trichomycetes, some of whom have contributed valuable publications. Among others, these include P.H. Adler, J. Aoki, C.E. Beard, G.L.Benny, R.E. Campos, C.-Y. Chien, M.H. Colbo, J.-A. Frost, J.J. García, J. Girbal, L.-H. Hsieh, E.S. Labeyrie, M. Ladle, A. Maciá, J.W. McCreadie, T.M. McInnis, D.P. Molloy, S. Santamaria, H. Sato, N. Shimada, D.B. Strongman, and M.R. Taylor.
The species richness of Trichomycetes has become evident only in recent decades as new geographical areas have been studied by various investigators. Explorations have included not only new regions of Europe and North America, but also Costa Rica and Puerto Rico in the Neotropics, Hawaii, Japan, Taiwan, and many countries in the Southern Hemisphere, including Australia, New Zealand, Chile, Argentina, and South Africa. These studies have enhanced our understanding of trichomycete distribution, host types and specificity, and have contributed to an understanding of their biogeography. New genera and species have been cultured axenically, and have provided specimens for molecular studies. Use of immunoelectrophoresis and isozyme analyses have more recently given way to DNA techniques that have shed better insight into the relationships of Trichomycetes with other fungi and to the phylogeny of species within the Class (Chapters 9, 12). These new studies are having a pronounced effect on the classification of Trichomycetes.
During the past six years several articles and one small book covering aspects of the ecology, biology, or systematics of Trichomycetes have appeared. These were published by Taylor et al. (1995), Lichtwardt (1996), Misra (1998), Moss (1998), O’Donnell et al. (1998) Slaymaker et al. (1999), Beard and Adler (2000), Misra and Lichtwardt (2000), Benny (2001), and Lichtwardt (2001).