​​​Introduction

“I look at the term species, as one arbitrarily given for the sake of convenience to a set of individuals closely resembling each other, and that it does not essentially differ from the term variety, which is given to less distinct and more fluctuating forms. The term variety, again, in comparison with mere individual differences, is also applied arbitrarily, and for mere convenience sake.” -- Charles Darwin, 1859 (11)

Plant pathologists and fungal taxonomists have enjoyed a long history of mutually beneficial collaborations (1). However, this marriage of disciplines has not been without difficulties. One of the persistent causes of friction between the two groups has been the tendency of fungal taxonomists to change familiar names of plant pathogenic fungi, complicating the work of plant pathologists. In recent years, the stability of fungal names has been eroded further as new methodologies from molecular systematics, information technology, and the internet have contributed to rapid changes in fungal taxonomic systems.

Fig. 1. Symptoms and signs of powdery mildew of Mahonia aquifolium (Pursh) Nutt. Names applied to the causal organism include Microsphaera berberidis (DC.) Lév. and Erysiphe berberidis DC. Which, if either, name is correct? See the Appendix for a discussion of the answer to this question.

The issues of nomenclatural stability and how best to exploit new technologies in taxonomy underlie an extended debate in the taxonomic literature about the possibility of discarding the International Code of Botanical Nomenclature (subsequently referred to herein as “The Code”). The Code is the set of rules governing names for fungi as well as other organisms traditionally classified as plants, and has an intellectual pedigree that can be traced back to Linnaeus. Much of the discussion of shortcomings of the Code, and of possible alternative approaches to nomenclature, centers on a proposed nomenclatural code known as the PhyloCode (8). Basic features of this approach are unranked classification (eliminating ranked categories such as order, family, and genus) and definition of taxon names strictly on the basis of phylogeny. Although supporters of the PhyloCode seem mostly unperturbed by criticism of it (e.g., 7), perusal of recent papers provides convincing evidence that its proponents will be unlikely to sway the mass of taxonomic opinion in their favor (e.g., 3,17,29,31,33,35). In fact, the PhyloCode is one of a number of approaches that would eliminate named ranked categories (e.g., 14,27), and none seem to have gathered a strong following. Nonetheless, the fact that approaches such as the PhyloCode gained some initial attention and interest from mycologists (21) suggests that it would be helpful to plant pathologists to discuss issues responsible for some of the interest it aroused.

The present paper considers some issues fundamental to how plant pathogenic fungi are named and classified. As in any attempt to characterize a complex, centuries-old human endeavor, in discussing fungal nomenclature and taxonomy it is most efficient to deal with generalizations for which there are numerous exceptions. Some topics, such as how to deal with classification below the rank of species, are beyond the scope of this paper and are not included. Furthermore, the principle behind the old adage “hard cases make bad laws” also is relevant to the work of naming organisms. For readers wishing to delve into hard cases and other topics in more detail, the lists of references and internet links should provide good starting points. Readers unfamiliar with how the Code governs changes made to binomials (species names) are encouraged to see examples provided in the Appendix to the paper.

Taxonomy and Phylogeny

Since its pre-Linnaean origins, the practice of fungal taxonomy has been influenced by innovations such as the germ theory, the theory of evolution, simple and compound light microscopes, Mendelian genetics, electron microscopes, and other major currents in biological thought and technology (1). The second half of the twentieth century saw remarkable developments in taxonomic theory and the technologies used to put taxonomic theory into practice (e.g., 22,34). Applying the tools of molecular biology and information technology to fungal taxonomy has greatly increased the numbers of taxonomic questions that can be addressed, the rigor with which taxonomic analyses can be done, and the speed with which information is disseminated.

The new technologies are especially useful in studying phylogenic relationships of fungi. Great enthusiasm has developed for this kind of work and its application to fungal taxonomy. Some have gone so far as to define the purpose of fungal taxonomy as follows: “The central goal of taxonomic mycology is to create classifications that communicate understanding of fungal phylogeny” (21). The authors of that statement use it to support their assertion that the Code impedes progress by discouraging scientists from formally recognizing clades (monophyletic groups). Although their paper (21) is a thoughtful assessment of issues related to presenting phylogenetic hypotheses, it is based on a narrower view of fungal taxonomy than has traditionally characterized the discipline.

Consider the following statements on the nature and purpose of fungal taxonomy:

“A taxonomic system is generally considered to have two functions. The first function is to provide an index to species. Taxonomic categories--genera, families, and orders--are pigeon-holes in which species may be filed and by means of which they may be located again for future reference. The second function is to show the phylogenetic relationships among these species.” -- E. S. Luttrell in 1958 (24)

“The serviceable products of taxonomic research are classifications which make it possible to gain a conception of the relationships of organisms, to permit reasonably ready identification, to give geographical distribution and host or substrate range, and to serve as a source of information concerning the important literature related to the organisms studied.” -- G. B. Cummins in 1947 (10)

“Utility may perhaps sound strange and may seem to some to be a very low aim in science, but in the end utility will carry the day ... for systematic botany is a means, not an end. [Its] true object should be to map out the vegetable kingdom in such a way that all known plants are grouped as clearly and distinctly as possible in order that the horticulturalist, the forester, the physiologist, may be able to obtain the facts needed by them in their work.” -- W. G. Farlow in 1898 (15)

I believe that the views of the three preceding mycologists are representative of those of most fungal taxonomists involved in the work of describing, naming, and classifying fungi from the mid-19th century to the present. The task of establishing groups based on inferred phylogenetic relationships certainly is consistent with the views expressed. However, stronger emphasis is placed on providing users of taxonomic information with the ability to identify organisms and on organizing information about them for efficient retrieval. The pragmatic approach of these authors reflects the reality that for most scientists working with fungi a phylogeny-based classification of fungi is a means to an end rather than an end in itself. Consider another point made by Luttrell (24):

“Taxonomic categories are much more than mere compartments into which species may be placed. The Erysiphales, the Uredinales, the Peronosporales, for example, are much more nearly scientific laws than scientific pigeon holes. Each of these names is a shorthand expression of a great mass of mycological data ... The characterizations even of species may well be considered generalizations from the facts concerning groups of individuals.”

Phylogeny is of significance to taxonomists and users of taxonomic information because taxonomic categories that reflect phylogenetic relationships are more powerful tools--they contain more information--than categories that do not reflect phylogenetic relationships. To illustrate the point using a non-fungal example, vampire bats and house sparrows both fly, but being able to distinguish one as a mammal and the other as a bird provides a person with more information than if they were lumped together into a single category of “flying animal.”

Using a slightly more mycological example, recognizing that oomycetes are more closely related phylogenetically to algae than to Ascomycetes provides insights into physiology and genetics that have practical as well as academic significance. The current approach (2) of separating oomycetes from Fungi provides more precision in what is meant by the names applied to both groups, and improves the resulting taxonomic classification by making it more useful for more purposes. But, even before oomycetes were so effectively dissected out of the Kingdom Fungi, scientists were able to use profitably the classification systems that treated them as fungi. Phylogenetic information improves taxonomic systems, but the quality of taxonomic systems is measured in relative rather than absolute terms. Ultimately, one system is judged superior to another if it is more useful in some way that is important to a user than another system.

In fact, although evolutionary relationships per se fascinate fungal taxonomists (including the present author), they are of relatively little interest to most scientists working on fungi, including plant pathologists. Consider another of Farlow’s (15) observations made nearly 40 years after the appearance of The Origin of Species:

“... theoretical considerations with regard to evolution play a much less important part than they used to ... although hypothetical genealogies and family trees of the banyan type appear at not infrequent intervals in botanical journals, they are quite overshadowed in general interest by the papers on cytology, life histories, and physiology. That was not the case in the [eighteen] sixties when nothing compared to interest with the question of the origin of species. While we cannot be too grateful to Darwin for having opened our eyes to see the value of evolution in general, the majority of the active botanists of the present day find too many other pressing questions to be solved to be able to dwell on evolution to the same exclusive extent as did the botanist of the last generation.”

Bearing in mind Farlow’s comment on the relative significance of evolutionary relationships, it is interesting to note Hibbett and Donoghue’s (21) finding after surveying fungal taxonomic papers that “few fungal phylogenetic studies result in formal taxonomic proposals”. I suspect that a major reason new phylogenetic information is not immediately translated into name changes is that taxonomists realize that their work must address the needs of a broad constituency of users. Reflecting current phylogenetic information is one goal of a taxonomist, but it can be of less importance than stability, practicality, and simplicity. This reluctance to change established taxonomic concepts immediately upon availability of new information is nothing new; most monographs and many taxonomic papers include information suggestive of taxonomic changes that authors prefer to defer until more evidence is available (e.g., the discussion on Diatrype stigma calling attention to anamorphic differences and their possible taxonomic significance [19]). Progress in fungal taxonomy, especially when determining how to use new characters or approaches to data analysis, is generally measured in generations of scientists rather than months or years. The reasons for this have more to do with the small numbers of taxonomists relative to the numbers of organisms to study than impediments to making new names caused by the Code.

I suspect that the present wave of enthusiasm (which, by the way, I share) for phylogeny is an echo of the original one that that Farlow described occurred upon publication of Darwin’s On the Origin of Species. New, powerful technologies have renewed our hope in making sense of fungal evolution and we seem to be re-experiencing the kind of extreme enthusiasm with which scientists greeted Darwin’s work. Are we also destined, like Farlow, ultimately to see work on fungal evolution “quite overshadowed in general interest by the papers on cytology, life histories, and physiology”?

Names as Representing Taxonomic Hypotheses

As noted above, Luttrell (24) suggested that “taxonomic categories are much more than mere compartments,” and are “much more nearly scientific laws than scientific pigeon holes.” Although I agree with his main point, I would restate it to say that taxonomic names represent hypotheses rather than scientific laws. Hypotheses are subject to testing, and much of the work of taxonomic revision centers on testing, accepting or rejecting old hypotheses, or proposing new ones (13). A name, particularly a binomial name applied to an organism, is in fact an abbreviated abstract of an argument proposed to support a taxonomic hypothesis. Perhaps it would be more accurate to say that we apply names to taxonomic hypotheses rather than to organisms.

Names described according to the Code refer to ranked categories to which organisms are assigned. Ranked categories, as noted by Davis and Heywood (12), “can only be defined by their position relative to other categories.” If you change one part of a classification system constructed with ranked categories, a cascade of classificatory ripples can affect other parts. Abandoning classifications involving named, ranked categories has the apparent virtue of simplification (8). There is a cost, however, in such a change because named, ranked groupings offer users with convenient labels to information-rich units of classification (28). It takes more effort to maintain a classification system based on named, ranked categories but so far it seems most taxonomists believe it is worth the trouble (13).

The Code enables taxonomists (despite being separated widely in space or time) to collaborate in proposing and refining taxonomic hypotheses which are represented by names. Authors proposing a name according to the Code’s requirements provide readers with information as to the kind of hypothesis being proposed (a species, a genus, etc), along with information supporting the hypothesis. The supporting information, termed the protologue, includes a range of materials such as the description, illustrations, references, the diagnosis (a summary of significant descriptive features rendered in Latin), and the type specimen to which the hypothesis is forever connected (23). The protologue can be viewed as the evidence marshaled in support of the taxonomic hypothesis represented by the name being proposed.

The processes and information required by the Code simplify greatly the use of names and understanding the hypotheses they signify. Some examples follow: Requiring effective publication means that work is accessible to other researchers. Providing a Latin diagnosis in addition to the longer description, written in an author’s native language, simplifies communicating across language barriers. Designating type specimens allows subsequent researchers to study the material used by the original author. The effect of such activities is to enable subsequent authors to more clearly understand and therefore confirm or reject names (and the hypotheses they signify). This collaborative approach to hypothesis generating and testing, made possible by the Code, has been used so successfully by so many collaborators (the vast majority of whom have never met each other) in so many countries speaking so many languages and representing so many cultures, and over such a long time (a quarter of a millennium if you trace its history to Linnaeus) that it is easy to take it for granted.

The Code’s rules for binomials allow them to be changed in order to reflect new taxonomic hypotheses. Having an orderly process to govern such changes helps ensure that a reader can interpret a binomial in an unambiguous fashion. (For examples of how binomials change according to requirements of the Code see the Appendix.) Nonetheless, name changes complicate life for users of taxonomic systems, particularly when changes affect binomials used to designate species. Some name changes (those involving nomenclatural synonyms) are occasioned when names are proposed or changed in ways that violate provisions of the Code. Such situations can be avoided, or at least minimized, by following the Code. Name changes that reflect differing taxonomic opinions, termed taxonomic synonyms, are a different matter; they are a natural result of ongoing research obtaining new data or analyzing existing data to yield new interpretations. Differences of opinion about what constitutes a species (i.e. the species concept) frequently are at the heart of such situations. Although one might believe that the problem of species concepts would have been solved by now, species concepts remain the subject of disagreement.

Species Concepts and Their Discontents

Mayden (25) distinguished more than 20 species concepts in the literature, many of which continue to have proponents. The biological species concept, which many biologists of my generation grew up learning and believing in, is under increasing criticism (e.g., 26,30) because it essentially ignores a major part of the planet’s biota-asexually reproducing organisms. In a book-length debate (38) among several theorists who argued in support of five competing species concepts, a significant outcome from the exchange of arguments was that nothing seemed to sway the debaters from the belief that, in the words of Cracraft (9) “My concept is the best.” Taylor et al. (36) suggested that fungal species concepts will be improved by basing them on analyses of multiple gene phylogenies, seemingly an extension of an old concept familiar to morphological taxonomists that “the more characters, the better.” Other recent reviews of species concepts employ more traditional approaches (20,32) but also seem to suggest that the solution to the problem lies in the kinds and/or amounts of data used to construct a species concept. All of these reviews are interesting, informative, and useful. However, the current situation with respect to species concepts seems largely unchanged from the time when Darwin made the following assessment:

“It is really laughable to see what different ideas are prominent in various naturalists’ minds, when they speak of 'species'; in some, resemblance is everything and descent of little weight--in some, sterility an unfailing test, with others it is not worth a farthing. It all comes, I believe, from trying to define the indefinable.” (cited in 14)

In two sentences Darwin neatly encapsulates the crux of the problem. The three leading approaches to defining species that he mentions--phenetic (resemblance), phylogenetic (descent) and biological (sterility)--ultimately fall short because, although each is based on some attribute of organisms, no single criterion is sufficient to address the complexity inherent in making sense of biological diversity. Consider Farlow’s (15) comments on the problem:

“... what we botanists call species are really arbitrary and artificial creations to aid us in classifying certain facts which have been accumulated in the course of time, and nothing more ... Whether or not species really exist in nature is a question which may be left to philosophy. Our so-called species are only attempts to arrange groups of individual plants according to the best light we have at the moment, knowing that when more is known about them our species will be remodelled [sic]. We should not allow ourselves to be deluded by the hope of finding absolute standards; but it should be our object to arrange what is really known, so that it can be easily grasped and utilized.”

I would suggest that the best way to understand a species concept in fungi is to pay attention to how fungal taxonomists actually behave when they publish their work. Here, for example, is the entire section entitled “The species concept” from a recent authoritative review (5) of the taxonomy of Erysiphales:

“The following features are the base for differentiation purposes of species in powdery mildew fungi: symptoms on host; morphology and biometry of anamorphs (mycelium, appressoria, conidiophores, conidia, germination) and teleomorphs (ascomata, appendages, asci, ascospores); biological specialization; distribution.

The general species concept should be based on morphology; therefore, species should be characterized and distinguished by morphological features, whereas morphologically indistinguishable biological races should be classified as formae speciales, ‘Intermediate’ taxa, which are biologically specialized but only slightly distinguished in morphology, may be classified as varieties.”

This description of the authors’ species concept is a straightforward account that provides a reader with a clear idea of what constitutes a species in their work. Other taxonomists working in other groups of fungi might use different approaches. The situation statement made by Fischer and Shaw (16) in prefacing their own description of species concepts in smut fungi remains relevant. They (16) noted that “It has gradually come to be recognized that the criteria which are valid in delimiting species vary in different groups of organisms”.

Artful Taxonomy

Probably anyone who has taken one or two college biology courses has encountered the aphorism “taxonomy is an art rather than a science.” As the science behind the technologies available to taxonomists has progressed it has been tempting to forget that a taxonomic system is a synthesis of data from other disciplines. Trying to assess taxonomic work using the conceptual tools appropriate for physics or chemistry is probably destined for failure because taxonomy is more akin to literature than to the physical sciences.

In general, taxonomic work can be characterized as consisting of three kinds of activities:

Perceiving: I prefer “perceiving” to “observing” because it emphasizes that taxonomic data are generated through the senses--microscopes, hand lenses, and gene sequencers all are aids used to extend the kind of data our senses are able to receive.

Interpreting: Raw data need to be assessed in order to use them to draw conclusions. Comparisons, statistical analysis, tree-building, etc, all are approaches to using data to determine patterns that are informative and can be used to propose, test, accept, or reject taxonomic hypotheses.

Communicating: Interpretations of the data obtained during an investigation must be shared with others. Classification systems, including the categories, names, and other features that characterize them are tools for communication. Nomenclatural systems such as the Code serve the goal of improving communication by providing mechanisms and means of sharing information effectively and efficiently.

The art of taxonomy has to do with the choices a taxonomist makes in how to carry out each of these three tasks. What kind of data will be obtained? How will they be interpreted? How will the interpretations be organized for communication? The choices one makes may be dictated by some facts of circumstance such as available equipment or funding, but even so there is a strongly subjective element. Species concepts, and systems of nomenclature and classification, are tools for communication. These tools probably reflect more closely the characteristics and complexities of the human mind and patterns of human communication than of the organisms we classify.

How then does one evaluate the quality of taxonomic work? It would seem to me that there are two main criteria.

One criterion is the internal integrity of a piece of work. This criterion seems to receive the most attention. Were data obtained and analyzed properly? Are conclusions logical, well-supported by data and analysis? Are conclusions communicated clearly and effectively? In other words, were procedures for generating data, analyzing data, and communicating conclusions used properly?

Another criterion is perhaps more difficult to assess but it is critical: is the work useful to the audience for which it was intended? In other words, does the work enable the user to solve problems, make predictions about biology of organisms, or accomplish other tasks that they could not do without the work? And how does it compare with other available taxonomic work?

Fungal Taxonomy and Plant Pathology

“Everything that is known is comprehended not according to its own nature, but according to the ability to know of those who do the knowing.” -- Boethius, ca. 524 (37)

To extend Boethius’s idea to fungal taxonomy, what we know about fungi reflects what we are able to learn. As we continue to develop new technologies for generating data, new concepts for analyzing data, and a more comprehensive body of information about increasingly diverse fungi, our approaches to classifying them and applying names to species will continue to change. Species concepts, nomenclatural systems, and classifications are dynamic, not static. I believe the following ideas provide a framework for considering how to use and improve taxonomic systems for plant pathogenic fungi:

1) The most meaningful measure of quality of a taxonomic or nomenclatural system is how useful it is relative to the needs of a user. The best taxonomic system or nomenclatural system, judged relative to those available for comparison, is that which most effectively meets the needs of the most users who use it for the greatest number of purposes.

2) Most users of taxonomic and nomenclatural systems are not interested in phylogeny per se, but rather in a range of activities such as determining the characteristics and distribution of an organism, predicting some aspect of its biology, or organizing and retrieving information efficiently. Phylogenetic information is valuable as a means to the end of improving classification, rather than itself being the end goal.

3) The use of named, ranked taxonomic categories has persisted for centuries because they communicate more information, and hence are more useful to more users, than unranked categories. A classification system with unranked or unnamed categories tailored to meet the needs of an audience interested primarily in phylogenetic research (or any other single class of users) will be of limited use or interest to the majority of users.

4) Ranked categories, including that known as the species (which is designated by a binomial), are best viewed as taxonomic hypotheses. A critical, but seemingly frequently overlooked, role of the Code is to help ensure that taxonomic hypotheses, such as those represented by binomials, are proposed effectively and unambiguously for review, testing, and adoption or rejection by the scientific community. By fulfilling this role successfully, the Code has facilitated collaboration among thousands of taxonomists for generations and has resulted in an enormous body of taxonomic and biologic information that is accessible to the scientific community.

As we consider how best to improve fungal taxonomy and nomenclature, the value of the current Code should not be underestimated. Fungi are numerous, diverse, and complex organisms, and we still know very little about most of them. Plant pathogenic fungi are the subject of attention of a very diverse group of scientists who play critical roles in international trade, production of vital foodstuffs and other plant products, and who help ensure that plant-based industries are economically and environmentally sustainable. Any successful taxonomic and nomenclatural system for plant pathogenic fungi will need to be useful to scientists engaged in this enormous range of activities. Such a system also will need to be flexible enough to accommodate new information, and structured in such a way that users have access to the history of concepts and conclusions that underlie the application of a particular organism’s name or names. The current Code accomplishes these objectives so successfully that it is easy to take it for granted and to forget that it developed slowly through the efforts of generations of taxonomists. Authors cited in the preceding extended quotations have provided us with a legacy of careful reasonability that is worth emulating, and examples of innovative taxonomic thought that pursued progress but did not neglect utility for the sake of novelty.

Acknowledgments

The author appreciates the helpful comments and suggestions for this paper received from Joe Ammirati, Lori Carris, Ginger Harstad Glawe, David Livesay, David Nanney, Jack Rogers, and Kathleen Sayce.

Additional Resources

CABI Bioscience Databases

International Code of Botanical Nomenclature

PhyloCode

A guide to Botanical Nomenclature (A Tennessee Tutorial, R. H. Petersen)

USDA-ARS Systematic Botany and Mycology Laboratory

Literature Cited

1. Ainsworth, G. C. 1976. Introduction to the History of Mycology. Cambridge University Press. Cambridge.

2. Alexopoulos, C. J., Mims, C. W., and M. Blackwell. 1996. Introductory Mycology, 4th Ed. John Wiley and Sons, Inc. New York.

3. Berry, P. E. 2002. Biological inventories and the PhyloCode. Taxon 51:27-29.

4. Braun, U. 1987. A monograph of the Erysiphales (powdery mildews). Beih. Nova Hedwigia 89:1-700.

5. Braun, U., Cook, R. T. A., Inman, A. J., and Shin, H.-D. 2002. The taxonomy of powdery mildew fungi. Pages 13-55 in: The Powdery Mildews: A Comprehensive Treatise. R. R. Bélanger, W. R. Bushnell, A. J. Dik, and T. L. W. Carver, eds. American Phytopathological Society, St. Paul, MN.

6. Braun, U., and Takamatsu, S. 2002. Phylogeny of Erysiphe, Microsphaera, Uncinula (Erysipheae) and Cystotheca, Podosphaera, Sphaerotheca (Cystotheceae) inferred from rDNA ITS sequences-some taxonomic consequences. Schlechtendalia 4:1-33.

7. Bryant, H. N., and Cantino, P. D. 2002. A review of criticisms of phylogenetic nomenclature: is taxonomic freedom the fundamental issue? Biol. Rev. 77:39-55.

8. Cantino, P. D., and de Queiroz, K. 2000. PhyloCode. Online.

9. Cracraft, J. 2000. Species concepts in theoretical and applied biology: A systematic debate with consequences. Pages 3-14 in: Species concepts and phylogenetic theory: A debate. Q. D. Wheeler and R. Meier, eds. Columbia University Press. NY.

10. Cummins, G. B. 1947. Some problems in mycological taxonomy. Mycologia 39:627-634.

11. Darwin, C. 1859 (facsimile edition 1964). On the Origin of Species: A Facsimile of the First Edition. Harvard University Press. Cambridge, MA.

12. Davis, P. H., and Heywood, V. H. 1973. Principles of angiosperm taxonomy. Robert E. Krieger Publishing Co. Huntington, NY.

13. Dominguez, E., and Wheeler, Q. D. 1997. Taxonomic stability is ignorance. Cladistics 13:367-372.

14. Ereschefsky, M. 1999. Species and the Linnaean hierarchy. Pages 285-305 in: Species: New Interdisciplinary Essays. R. A. Wilson, ed. MIT Press. Cambridge, MA.

15. Farlow, W. G. 1898. The conception of species as affected by recent investigations on fungi. Proc. Amer. Assoc. Advanc. Science 47:383-402.

16. Fischer, G. W., and Shaw, C. G. 1953. A proposed species concept in the smut fungi, with application to North American species. Phytopathology 43:181-188.

17. Forey, P. L. 2002. PhyloCode-pain, no gain. Taxon 52:43-54.

18. Glawe, D. A. 2003. First report of powdery mildew of Mahonia aquifolium caused by Microsphaera berberidis (Erysiphe berberidis) in North America. Online. Plant Health Progress doi:10.1094/PHP-2003-0206-01-HN.

19. Glawe, D. A., and Rogers, J. D. 1984. Diatrypaceae in the Pacific Northwest. Mycotaxon 20:401-460.

20. Harrington, T. C. and Rizzo, D. M. 1999. Defining species in the fungi. Pages 43-70 in: Structure and Dynamics of Fungal Populations. J. J. Worrall, ed. Kluwer Academic. Dordrecht.

21. Hibbett, D. S., and Donoghue, M. J. 1998. Integrating phylogenetic analysis and classification in fungi. Mycologia 90:347-356.

22. Hillis, D. M., Moritz, C., and Mable, B. K., eds. 1996. Molecular systematics. 2nd Ed. Sinauer Associates, Inc. Sunderland, MA.

23. Kirk, P. M., Cannon, P. F., David, J. C., and Stalpers, J. A. 2001. Ainsworth and Bisby’s Dictionary of the Fungi. 9th Ed. CABI Publishing. Wallingford.

24. Luttrell, E. S. 1958. The function of taxonomy in mycology. Mycologia 50:942-944.

25. Mayden, R. L. 1997. A hierarchy of species concepts: the denouement in the saga of the species problem. Pages 381-424 in: Species: The Units of Diversity. M. A. Claridge, H. A. Dawah, and M. R. Wilson, eds. Chapman and Hall, London.

26. Mayr, E. 2000. A defense of the biological species concept. Pages 161-166 in: Species Concepts and Phylogenetic Theory: A Debate. Q. D. Wheeler and R. Meier, eds. Columbia University Press. NY.

27. Mishler, B. D. 1999. Getting rid of species? Pages 307-315 in: Species: New Interdisciplinary Essays. R. A. Wilson, eds. MIT Press. Cambridge, MA.

28. Moore, G. 2002. Down with the Kingdom (Phylum, Class, and Order too). Science. 297:1650-1651.

29. Moore, G. 2003. Should taxon names be explicitly defined? Botan. Rev. 69:2-21.

30. Nanney, D. L. 1999. When is a rose? The kinds of Tetrahymena. Pages 93-118 in: Species: New Interdisciplinary Essays. R. A. Wilson, ed. MIT Press. Cambridge, MA.

31. Nixon, K. C., Carpenter, J. M., and Stevenson, D. W. 2003. The PhyloCode is fatally flawed, and the “Linnaean” system can be easily fixed. Botan. Rev. 69:111-120.

32. Petersen, R. H., and Hughes, K. W. 1999. Species and speciation in mushrooms. BioScience 49:440-452.

33. Schuh, R. T. 2003. The Linnaean system and its 250-year persistence. Botan. Rev. 69:59-78.

34. Stevens, P. F. 2000. Botanical systematics 1950-2000: Change, progress, or both? Taxon 49:635-659.

35. Stevens, P. F. 2002. Why do we name organisms? Some reminders from the past. Taxon 51:11-26.

36. Taylor, J. W., Jacobson, D. J., Kroken, S., Kasuga, T., Geiser, D. M., Hibbett, D. S., and Fisher, M. C. 2000. Phylogenetic species recognition and species concepts in fungi. Fungal Genet. Biol. 31:21-32.

37. Watts, V., transl. 1999. Boethius: The Consolation of Philosophy. Rev. ed. Penguin. London.

38. Wheeler, Q. D., and Meier, R. 2000. Species Concepts and Phylogenetic Theory: A Debate. Columbia University Press. NY.

Appendix

The following examples illustrate how a binomial designates both qualities of uniqueness and affinity, how the Code determines how names are changed to reflect differing taxonomic hypotheses, and how binomials and author citations can be used to decipher a sequence of taxonomic hypotheses regarding an organism in the literature. Examples below are drawn from exemplary work by Braun and co-authors (4,5,6) that readers are encouraged to consult for additional examples of nomenclatural practice involving the plant pathogenic Erysiphales (powdery mildews).

Consider the following name, which has been applied to a powdery mildew fungus attacking plant hosts in the family Berberidaceae (Fig. 1):

Microsphaera berberidis

The capitalized first name refers to the genus; the second name (the epithet) is that of the particular species. The genus name indicates affinities--in this case the name Microsphaera indicates that this particular organism exhibits features common to other organisms also classified in that genus. That this organism is regarded as a distinct species is designated by the epithet berberidis. The complete version of the name is the following:

Microsphaera berberidis (DC) Lév.

In addition to the information provided in the first version of the name, this one informs the reader that the species first was recognized as distinct by de Condolle; and that Léveillé subsequently reclassified it in the genus Microsphaera. In other words, Léveillé hypothesized affinities for the species that differed from de Condolle’s proposal. Following the rules of the Code, de Condolle’s name appears in parentheses to indicate that he originally described the species, and Léveillé’s name follows at the end to indicate that he transferred this species to the genus Microsphaera. Thus, the information in the binomial and associated author names provides readers with information on the history of the name (and the taxonomic concepts it represents). Attaching author names to the binomial also has the benefit of reducing the confusion that can arise if the same names for genus and species are used by different authors to mean different things.

Searching for the literature in which the binomial originally was proposed is simplified further by citing bibliographic information along with a name, such as done by Braun (4) in his monograph on Erysiphales:

Microsphaera berberidis (DC) Lév., Ann. Sci. Nat., bot., 3 sér., 15, p. 159, 831 (1851)

In the same publication, Braun lists the following name as a synonym of Microsphaera berberidis:

Erysiphe berberidis DC., Fl. Fr. 2, p. 275 (1805)

Two basic kinds of synonyms exist--nomenclatural and taxonomic. Nomenclatural synonyms are those that violate requirements of the Code and therefore cannot be used.

Taxonomic synonyms are alternative names that reflect differences of taxonomic opinion. The Code does not specify which taxonomic synonym (and the underlying taxonomic hypothesis it signifies) must be used, except for requiring that the name proposed first to designate a taxonomic concept must be used if more than one such name exists. In other words, the Code does not dictate taxonomic opinion; instead, taxonomic hypotheses are accepted or rejected on their own merits by the scientific community.

In the current example, Erysiphe berberidis is regarded by Braun as a taxonomic synonym of Microsphaera berberidis. Erysiphe berberidis has the status of basionym, meaning that it is the first name applied unequivocally to this organism. In an interesting taxonomic twist, Braun and Takamatsu (6) recently recommended using Erysiphe berberidis for the species in question. This proposal was based on recent work on ITS sequences which they interpreted to justify a genus concept different than that used by Léveillé. Because Erysiphe berberidis was the earliest name (the basionym) applied to this organism, the protocol described by the Code requires that in this instance it is the name to be used. If a subsequent researcher wished to emphasize that they were following Braun and Takamatsu’s taxonomic approach, they might indicate this by modifying the name to the following:

Erysiphe berberidis DC. fide Braun and Takamatsu

Alternatively, if one wished to continue to use Léveillé’s concept, there is no reason specified by the Code that would require one to use the more recent taxonomic proposal (or, as suggested here, taxonomic hypothesis). Since Braun and Takamatsu (6) did not cite a nomenclatural reason for dropping de Condolle’s designation of this organism, but rather a re-interpretation of the organism’s affinities based on new information, a user is free to consider their suggestion and to decide whether to accept their taxonomic hypothesis or not. One can even take the non-committal approach of using a name that has become widespread while indicating that a newer proposal has been made and is under consideration as I did in a recent report (18) where I used Léveillé’s binomial but also cited Braun and Takamatsu’s use of de Condolle’s.

A further means of avoiding ambiguity is to cite the publication used to identify an organism (for example, a monograph). This can be helpful because later authors sometimes augment or alter a describing author’s concepts, causing a binomial to be used in more than one sense.

Another set of issues arises if one considers ranks above the genus level. For example, over a period of years Braun and co-authors (4,5) described differing suprageneric groupings that reflected the ongoing modification of their taxonomic concepts. By reading the arguments they used to support changes at these ranks, one can learn much about the evolution of the authors’ thinking about powdery mildew classification. To repeat Luttrell’s (24) observation about suprageneric groupings: “Each of these names is a shorthand expression of a great mass of mycological data”.