SOME REMARKS ON THE THEORETICAL ASPECTS OF BACTERIALTAXONOMY

G. D. FLOODGATE1Department of Scientific and Industrial Research, Torry Research Station, Aberdeen, Scotland2

I. The Nature of Classification .............................................................. 277II. The Possibility of Making a BacterialTaxonomy.. 280

A. Using Phylogenetic Relationships ...................................................... 280B. Using Over-all Similarity .............................................................. 281

III. Taxonomic Problems in Bacteriology Arising out of the Use and Misuse of Words .... ........ 283IV. Addendum................................................................................ 289V. Acknowledgments......................................................................... 289

VI. Literature Cited..................................................................... 289

I. THE NATURE OF CLASSIFICATION.. . Species of things, are nothing else but

these abstract ideas."John Locke, 1689 (29).

According to the Encyclopaedia Britannica (21),"Classification is one method, probably the sim-plest method of discovering order in the world.By noting similarities between numerous distinctindividuals and thinking of these individuals asforming one class or kind, the many are in a sensereduced to one, and to that extent simplicity andorder are introduced into the bewildering multi-plicity of nature." Classification as discussed bylogicians and philosphers always involves group-ing individuals together, so that all members ofany one group have certain characters in common.When an attempt is made to classify living

things many complications arise, and the be-wildering multiplicity of living creatures is verydifficult to reduce to that order and simplicitywhich pleases the human mind. There appear tobe two schools of thought concerning biologicalclassification. Broadly speaking, the post-Dar-winian phylogenetic school is convinced thatthere is, in nature, an already existing, objectiveclassification which can be discovered by carefulsearch. This type of classification is, therefore,concerned with revealing "existing natural rela-tionships" and with the discovery of an or-ganism's "fundamental properties" and its "es-sential nature." Almost always, taxonomies ofthis type are closely allied to phylogenetics, andindeed some taxonomists define taxonomy in

1 Present address: Marine Science Laboratories,University College of North Wales, Menai Bridge,Anglesey, Wales, United Kingdom.

2 Paper for publication no. 61/15.

terms of phylogenetic relationships (44). AsHuxley (25) put it, "Fundamentally, the problemof systematics regarded as a branch of generalbiology is that of detecting evolution at work."The reason why taxonomy should be so closelyallied to phylogenetics is not clear. Gilmour (23)suggests that evolution simply took over the roleof special creation in some earlier taxonomicschemes, but there appears to be no logical reasonwhy taxonomy and phylogeny should be con-joined.

There can be no doubt that the phylogeneticview of taxonomy has enjoyed considerablesuccess, particularly in zoology and botany.However, it has two main difficulties. Firstly,it is not always possible to construct a classifica-tion based on phylogeny, even in botany andzoology. Clearly, wherever the phylogeny isspeculative, any taxonomy based on it must bespeculative also. In those instances, therefore, inwhich fossils are unknown or few in number, aphylogenetic taxonomy will be almost entirelyspeculative. To quote Huxley (25) again, "Thenin lower taxonomic categories such as species andsub-species, parallel mutation may make a phylo-genetic interpretation an almost impossible ideal,of little practical help or even theoretical signifi-cance. Even in larger groups, such as those ofhigher plants, phylogeny may be almost hope-lessly obscured by parallel or convergent evolu-tion, added to the lack of fossil material in earlyevolutionary stages. And further, taxonomy canonly represent phylogeny adequately when differ-entiation is divergent. Wherever it is reticulate,... our existing taxonomic methods inevitablyfail to denote phylogeny." This difficulty isrelevant to bacterial taxonomy and is discussed

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in more detail below (Part II). Secondly, it isworth examining such phrases as "fundamentalproperties" and "essential natures" and to ask,"To what are the properties fundamental or thenatures essential?" Clearly, they are not funda-mental to the life or the evolution of the or-ganism but are, in fact, fundamental or essentialto the purpose of demonstrating phylogeneticrelationships. Now this purpose can only belongto the classifier; that is, a subjective element hascrept into a scheme that was intended to bewholly objective. It is the purpose of the classifierthat decides what is to be called fundamentaland what is to be considered essential. This wasclearly recognized by Mill (34) in his essay onclassification. "We said just now that the classifi-cation of objects should follow those of theirproperties which indicate not only the mostnumerous, but also the most important peculiari-ties. What is here meant by importance? It hasreference to the particular end in view; and thesame objects therefore may admit with proprietyof several different classifications."The second school of thought is skeptical as to

whether any classification is completely objective,and doubtful if a "logical" classification is neces-sarily a phylogenetic one. As pointed out above,"logical" classification always involves groupingobjects together, so that all the members of anyone group have certain characters in common.Invariably, some characters are selected and usedto make the groups, all of the other characterspossessed by the object being ignored. Consider,for example, the case when two bacterial culturesare described as being exactly the same or exactlysimilar; that is, there is no difference betweenthem. In fact, they will be composed of differentcells, each made up of different molecules, willoccupy different places at different times, andwill have different histories. Clearly, "exactlythe same" means "exactly the same over theselected range of characters, the rest being ignoredas irrelevant in the particular context, or for theparticular purpose in question." Even this is notaccurate. Any two characters can only be shownto be approximately the same, that is, the samewithin acceptable limits. The grounds on whichthe selection of characters is made constitute asubjective element in classification, and thiselement is most easily recognized if thought of interms of the classifier's purpose. Except in thecase when an arbitrary selection is made, the useto which the classifier wishes to put his classifica-

tion will largely govern the choice of charactersHence the selection of characters is properly madeif the resultant groups fulfill the classifier'spurpose.

If this pragmatic view of taxonomy is adopted,certain conclusions of interest to microbiologistsfollow. Firstly, different purposes will give rise todifferent classifications. There will be not oneauthentic classification, but as many as there arepurposes, and all authentic for their purpose.However, it is most important to realize thatpurposes can be "wide" or "narrow," and ataxonomy devised for a "wide" purpose maysuffice for other narrower purposes, so that awide-purpose taxonomy of a "natural" kind(see Part III) may be so generally useful in manyfields that it is preferred over any one of thenarrower taxonomies. Secondly, the way toevaluate a classification is to decide upon itsdegree of success; that is, how far does it fulfill thepurpose for which it was devised? It is nonsenseto talk in this context of true or false classifica-tions, but only of useful or successful ones.Thirdly, the "lump or split" controversy isresolved. Bacteria should be lumped into largegroups or be split into smaller ones as is bestsuited to the purpose in mind. Fourthly, sayingsof the type, "morphology is fundamental," mustbe backed up by indicating implicitly or explicitlywhat morphology is fundamental to and why.Gilmour (23) has pointed out that each of

these philosophies of taxonomy is based on adifferent epistemological theory. In general, thephylogenetic school envisages the taxonomist ascompletely distinct from the objects he intends toclassify. He merely observes what is present inhis field of study and reports accurately what heobserves. He does not divide up the material heis classifying into different groups, but reports onthe divisions which he believes are already inexistence. There is inherent in this outlook aduality between the mind of the classifier (thesubject) and the sense data by which he becomesaware of the outside world of matter (the object).The epistemology of the pragmatic school oftaxonomy is somewhat different. Again there isa duality, but with very different subject andobject. The subject is the "I" of the classifier,which is not in this case a passive rep )rter butan active, reasoning agent, and the object nolonger consists solely of the data of perceived factsbut is composed of these data together with anelement supplied by the classifier. Thus, to use

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Gilmour's illustration, "the object we call a chairconsists partly of a number of experienced sense-data such as colours, shapes and other qualities,and partly of the concept chair, which reason hasconstructed to 'clip' these data together." Thedata are "given" once and for all, whereas the"clips" can be created and abolished at will, thebetter to give a more coherent picture of the ever-increasing data experienced. It will be noted that,in this view, the "I" of the classifier has played anactive part in "creating" a chair by providing theconceptual clip which holds the data together.

In order to apply this reasoning to bacteriology,let it be agreed that strain A has the followingcharacteristics: it is a rod-shaped organism;motile by a polar flagellum; gelatin is liquefied;nitrate is reduced to nitrite and ammonia; glucoseis oxidized to 2-ketogluconic acid; blood serum isliquefied; growth is aerobic; optimal growthtemperature is between 20 C and 25 C; growth isdependent on the oxidation of exogenous organicsubstances. Now all these data may be held to-gether by a clip labeled Pseudomonas fluorescens,or two items only may be selected and clipped to-gether by "chemo-organotrophic mesophile." The"clip" that is used, that is, the category to whichstrain A is assigned on any particular occasion,will depend on the classifier's purpose.

It is now necessary to inquire into the purposesfor which taxonomies have been devised. Some ofthese are very limited or narrow purposes, such asthose devised to show ecological relationships inthe sea, soil, food, etc. The purpose of others is todivided bacteria into groups whose members havecertain physiological properties in common suchas mesophiles, thermophiles, psychrophiles,phototrophs, chemotrophs, etc. Now, althoughthese classifications are quite adequate for thepurpose of showing up certain ecological orphysiological relationships, they are found to bevery limited in scope and of little use outside theirimmediate application. Taxonomy, in the com-mon everyday use of the term, has a much widerscope; that is, the taxonomist is usually concernedwith a much wider purpose. The nature of thiswider purpose is indicated by the followingextracts from various thinkers."To conclude, this is that which in short I

would say viz., that all the great business ofgenera and species and their essences, amounts tono more but this, that men making abstract ideasand setting them in their minds, with names an-nexed to them, do therebv enable themselves to

consider things and discourse of them, as it werein bundles, for the easier and readier improvementand communication of their knowledge whichwould advance but slowly were their words andthoughts confined only to particulars" (29)."The general problem of classification ... may

be stated as follows: To provide that things shallbe thought of in groups, and those groups insuch an order as will best conduce to the remem-brance and ascertainments of their laws.... Theends of scientific classification are best answeredwhen the objects are formed into groups respect-ing which a greater number of general proposi-tions can be made, and these propositions moreimportant, than could be made respecting anyother groups into which the same things couldbe distributed" (34)."A natural system (of taxonomy) is then one

which enables us to make the maximum numberof prophecies and deductions" (25).

"Broadly speaking, the purpose of all classifica-tion is to enable the classifier to make inductivegeneralisations concerning the sense data he isclassifying" (23)."The value of classification is that it allowsgeneral statements to be made" (7).

Clearly, these authors all agree that the mostdesirable classificatory system is the one thatallows the most propositions to be made regardingits constituent classes. Consider, as an example,the classification of books. For most of the librar-ian's purposes, it is better for him to classifybooks by their subject rather than by theirauthors, because more valuable generalizationscan be made from "subjects" than from "au-thors." For instance, the following generaliza-tions can be made of the books in the sciencesection: they deal with the natural world and areconcerned with observable facts, the techniquesfor making these observations, and the way thefacts are treated; whereas the books in the musicsection will be concerned with note values, pitch,and orchestration and will treat facts in a wayvery different from the science section books.Classification of books by authors, however, willonly give information such as, "people whosename is MacAndrew write more books than thosewhose name is MacKenzie"! This will not bemuch use for most of the purposes for which thelibrary is used, though for certain specific pur-poses, e.g., a comparative study of the culture ofthe Scottish clans, it would be very useful. Whathas been done is to select those features of books

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which best provide a classification that allows thegreatest number of generalizations of the desiredtype to be made.

Likewise the most desirable bacteriologicalclassification is the one providing the greatestnumber of generalizations and predictions thatare of value in bacteriology as a whole, as well asin each of the various fields of bacteriologicalscience. In other words, the classification calledfor is the most natural one, to use "natural clas-sification" in its "logical" meaning (Part III).In addition, the classification should be stable,so that small changes in knowledge will not causegreat changes in the classification; at the sametime, the classification should be capable ofimprovement as knowledge increases.

II. THE POSSIBILITY OF MAKING A BACTERIALTAXONOMY

A. Using Phylogenetic RelationshipsIn Part I it was argued that the classifier's

purpose and consequent selection of charactersshaped each classification. To some extent theterm "selection of characters" is a misleading one.In the case of the narrower classifications, wherethe connection between the purpose and thecharacters is obvious, selection is possible andeasy, but where a wide purpose, such as thatdescribed in Part I, is involved, the interconnec-tion between the purpose and the characters ismore complex. As a result, it cannot be unequivo-cally deduced that a given selection of characterswill lead to the desired end. Hence, the selectionin this case has an element of trial and error, andthe suitability of any selection can only be dis-covered empirically. However, each possibleselection may usefully be examined to discoverthe probability of its success. Two such selectionswill be discussed in this section. The first of theseto be considered is the possibility of devising apragmatic classification by selecting those char-acters that substantiate bacterial phylogeny.That is to say, the question will be asked, "Is thepurpose of demonstrating phylogenetic relation-ships wide enough to cover the purposes of bac-teriology as a whole?" This is not a reversion tothe post-Darwinian phylogenetic point of view.No attempt is being made to discover a "given"classification in an objective world, but rather tocreate one for a stated purpose. If such a clas-sification can be made, two advantages follow.Firstly, although the theoretical approaches of

the phylogenetic and pragmatic taxonomistswould be different, in practice each would utilizethe same characters and form similar groups.Secondly, bacteriology would be brought intoline with other biological sciences. However,before this can be attempted, it is necessary toknow which characters point to bacterial phylog-eny, and this is the crucial difficulty. As pointedout above (Part I), unless phylogeny is wellauthenticated by the fossil record and is diver-gent, any classification based upon it will belargely speculative and of little value. It is reason-able to assume that bacteria have evolved inspite of the lack of direct evidence, because theypossess certain properties, such as the ability tomutate and compounds such as deoxyribonucleicacid, which form part of the evolutionary mecha-nisms of higher living forms.

Unfortunately, with certain notable exceptions,such as Bisset (5) and Krassilnikov (28), fewbacteriologists have made a serious study ofphylogenetics. The best that has been achievedso far is to demonstrate the possible relationshipbetween very distant groups, and even here thereis considerable difference of opinion. No detailedpicture is available, nor is this surprising. Fossilsare almost unknown, although some workers haveobserved fossilized bacterial remains in rock (35,51). Embryology, which is so valuable to thetaxonomist of higher organisms, is lacking, eventhough some life cycles which might give in-formation of this type have been observed fromtime to time. The result has been that most ofthe arguments regarding the evolutionary pathtaken by bacteria have been "arguments byanalogy." This type of argument is, of course,quite legitimate in scientific discussion; indeed,the above argument for bacterial evolution issuch a case, but there is always the difficulty ofknowing if the analogy is a sound one. In bacterialphylogeny this takes the form of knowing whichend of a graded sequence of changes is the begin-ning and which the finish. Thus, frequently lifehas advanced from the simple to the complex, butprogressive loss of characters is also known. Abacteriological example of this dilemma is thesequence of nutritional changes discussed byWilson and Miles (50) and they wisely cautionagainst stating firmly which end of the series isthe advanced and which the primitive stage.Similarly, as creatures evolve into more and morespecialized ecological niches, plasticity in metabo-

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lism tends to be replaced by a rigid metabolism,but, as has been recently suggested, metabolicplasticity in bacteria may convey a positiveselective advantage and represent a highlyevolved state (48). Hence, while bacterial phylog-eny will doubtless advance in the future, at pres-ent it is difficult or even impossible to base aclassification on it.

B. Using Over-all SimilarityIn recent years, several workers have been

attempting to classify various items by groupingthem together according to their over-all simi-larity or natural resemblance, this quality beingmeasured by mathematical and statistical tech-niques (11, 13, 33, 36, 43). This type of classifica-tion has been introduced into bacteriology bySneath (42) and the following discussion appliesto his method of analysis. This kind of classifica-tion is unusual in that, instead of a number ofobservable characters, only one abstract pa-rameter, the over-all similarity, is used for makingthe groups. A consequence of this and of the waythe over-all similarity (S value) is derived is thattwo organisms with the same S value, when com-pared with a third organism, may differ in theirfeatures, that is, in the observed characters whichhave been employed in compiling the S values.For example, the organisms TV8, LG12, andSL13 reported by Sneath (42) have the followingvalues: S8.12 = 83, S12.13 = 83, but S8.13 = 78. Ifstrain TV8 and SL13 did not differ in any featureover the range involved, then of course S8.13would equal 100. The groups that are formed bythis technique are composed of strains which havea high but unspecified S value in comparison witheach other and with the group as a whole. Theydo not, therefore, form a species in the sense thateach member of the group possesses a certainpattern of previously chosen observable char-acters but, being aggregations of very similarstrains, they have some of the characteristics ofa species group (see Part III). Even so, to avoidconfusion, it would be better to adopt the wordsuggested by Sneath (41) and refer to a groupformed by this procedure as a pleiston.

If classification is to be made on the basis ofover-all similarity, the method of calculating theS value should be carefully studied. It shouldbe noted that the features to be used must besuitable for recording in terms of plus (+) orminus (-). However, this limitation is not a verystringent one as most of the features in common

use can be so designated. Next, there is the diffi-culty of deciding what one feature should be.The working definition of a feature as suggestedby Sneath (42) is, with certain reservations, "athing about which one statement can be made."It might be contended that it would be betterto define a feature in terms of enzymes or, betterstill, in terms of genes, because the genes are, ina sense, the "ultimate features." Since onlypragmatic criteria are to be applied in evaluatinga feature, "better" can only mean "leading to amore useful classification." Until a classificationbased on enzymic or genetic features has beenworked out and tested, there is no way of decidingif they are better, that is, more useful features,though there appears to be no theoretical reasonfor believing so. Certainly collecting the data forsuch a classification would be more difficult thancollecting the simple elements that make up thebulk of the features in present use. Furthermore,the simple, mechanical progression of gene toenzyme to enzymic product can not be main-tained. It has been shown (14, 15) that bacteriawith the same genotype may be maintained withdifferent phenotypes, so that "ultimate" is aninadmissible term in this context.

There is also the problem whether complexessuch as the gylcolysis cycle should count as onefeature or whether each step should count as afeature. In one sense it does not matter, since inworking out the S value, each feature, whethersimple or complex, of any one strain is comparedwith the corresponding feature of another strain,and no comparison is made between the featuresof the same strain. This is why complexes whosedetailed steps are unknown may be used asfeatures as well as simple, well-established, one-step biochemical reactions. Nevertheless the morefeatures that are used, the more refined the Svalue becomes, so that, in those cases when acomplex may be broken down into its constituentsteps, it is better to count each step as a feature.Another problem concerns the "value" of each

feature. According to the Adansonian method,all features count as of equal value, whateverthe differences between them. This is because,for the purpose of gauging the similarity betweentwo strains, they are of equal value. Any onefeature, say Gram's stain, has neither more norless ability to make strain A similar to strain Bthan has any other feature, say, penicillin sen-sitivity. As pointed out above (Part I), "exactly

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the same" means exactly the same over the rel-evant properties, the rest being ignored. The onlyrelevant property in this case is the ability toindicate similarity as measured by the formulafor compiling the S values. All the differences inquality between a morphological feature and abiochemical one, or between biochemical featuresof different kinds, are ignored because they areirrelevant in this context.Every classification will inevitably be biased,

or weighted, to a greater or lesser extent. It isimportant, therefore, to know just how biased anyparticular classification may be and whether ornot the bias serves any useful purpose. Threekinds of bias may be distinguished. Firstly, thereis a legitimate bias that may be deliberately putinto a classification to suit the classifier's purpose.It has already been suggested that, if bacterialphylogeny were well enough developed, a biastoward phylogenetics could lead to a satisfactoryclassificationl Again, when Adansonian methodsof classification are used, the bias is toward over-all similarity. Briefly, the legitimate bias of aclassification may be said to be closely linked tothe purpose for which the scheme was devised.A second kind of bias is a deliberate illegitimate

bias put into a classification to suit preconceivednotions or irrational prejudices as to what istaxonomically important. All deliberate weightingof characters which cannot be justified in termsof adequately thought out taxonomic principlescomes into this category. It is true that, in acertain sense, Adansonian methods give somecharacters zero weight. These are those characterswhich are as yet unknown or have been omitted;but this is quite different from giving some ob-served characters, but not others, widely differingweights.

Thirdly, there is an "accidental bias" which isdue to the interests of the workers who havestudied the strains involved. It is a very unfortu-nate fact that almost all bacteriologists eitherhave seen in bacteria convenient tools for thestudy of biochemistry, biophysics, or genetics orhave been concerned with the application ofbacteriology in medicine, food technology, soilscience, and so on, rather than with the study ofbacteria for their own sake. The result has beenthat the characters used to make taxonomicgroupings have been chosen, more or less ac-cidentally, to assist the classifier in the particularbacteriological application he had in mind. Thatthis situation persists can be seen from the report

of a recent conference in which Billing (4) writes,"It was evident ... that the approach of eachworker to questions of classification and differ-entiation depended on the particular problemsencountered in his own field." Classification byover-all similarity can also suffer from this sortof bias if the features are all or mostly of one ortwo types, i.e., all or mostly morphological,serological, etc., so that the similarity is no longerover-all. Although each feature by itself is equalto every other feature, the cumulative effect of anumber of features of one sort is to introduce abias very like accidental bias. The effect of ac-cidental bias on taxonomy is similar to that ofdeliberate illegitimate bias in that an undesirableweighting is introduced. The most obvious wayto avoid accidental bias is to take the features atrandom, but there is always the possibility that arandom choice might be selective in its effect; i.e.,a random selection could turn up only mor-phological features, or mostly biochemical onesplus a few immunological ones. The larger thenumber of features available, the less chancethere is of this happening, but clearly there isalways a possibility of introducing some bias inone direction or another. A better approach mightbe to make a stratified random selection, i.e., totake one random selection from morphologicalfeatures, another from biochemical, and so on.But whatever way the features are chosen, someaccidental bias will always be present, becausewhat is known about any organism will inevitablyreflect the interests of the people who havestudied it. Furthermore, bacteriologists willprobably be unwilling to abandon Gram's stainand the familiar biochemical tests which might beomitted by a random selection. These difficultiescan be avoided, and unwanted bias reduced to aminimum, simply by taking all the data that areavailable about a strain into consideration.

Nevertheless, the most important questionstill remains, and this is to inquire if classificationby over-all similarity gives rise to a taxonomyfrom which many useful generalizations andpredictions can be derived. This question can onlyfinally be answered by devising such a classifica-tion and showing that it works. However, someindication of the answer can be obtained from aconsideration of the following points. Firstly,since the data which are used to compile the Svalues are taken from as many facets of bacteri-ology as possible, the classification is likely to beadequate for each separate field of bacteriological

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investigation and for the discipline as a whole.In this way, the classification will provide a com-mon language for all bacteriologists, whateverparticular interests they may have.

Secondly, because many data are used to makethe groups, a large number of generalizations canbe made about each member of the group, suchas the correlation between its features and theprobability of its possessing any one of a largenumber of features. For these reasons too, gen-eralized inductions of the kind, "there are moreorganisms of Type A in a particular ecologicalsituation than Type B," will be informative.Prediction as to the probable role of either typemay be possible. Such prediction would of coursealways be subject to an error introduced by thedifference between the laboratory conditions andthe particular ecological situation in question.

Thirdly, in general, organisms that have arecent common ancestor are closely alike. Hencebacterial strains arranged by similarities will tendto represent the terminal branches of a phylo-genetic tree. It follows that this type of taxonomywill be useful in phylogeny.

Fourthly, since the similarity between strainsis expressed numerically, the difference betweenthem can be expressed in the same way. Thesedifferences may be represented in a multidimen-sional space, so as to show the relative positionof each strain to every other strain. This expres-sion of the relative positions of strains in termsof over-all similarity is more precise than thevague term "intermediate" that is in common use(see also Part III).

Fifthly, the classification will be stable. As newfeatures become available they will alter slightlythe S values between each pair of strains, so thatnew information will refine the classification butnot drastically alter it.To the practical bacteriologist, however, the

most important function of taxonomy is to enablehim to identify an unknown isolate. When theover-all similarity method is employed, once thegroups are decided upon, they are surveyed to seewhich features occur most frequently in each ofthe groups, and these are considered diagnostic.For computing the S value, every feature had tobe treated as of equal weight to every otherfeature, but for identification certain features areweighted, that is, they are more important thanothers. Because a pleiston is not "a rigidly definedspecies" (see Part III), any one of its memberstrains may or may not possess certain diagnostic

features. These, therefore, can only be reportedin such terms as "usually present" or "sometimespresent." Better still, the frequency of the occur-rence of any feature is expressed in terms ofprobabilty, so that the description will read thatfeature A is present in pleiston X with a proba-bility P, feature B with probability Q, and so on.Obviously, the diagnostic features are those withthe highest probabilities. There is a theoreticalpossibility of an organism belonging by its over-all similarity to a certain pleiston but possessingfew or even none of the diagnostic features of thegroup. This organism could only be identified bydetermining its similarity relationships and sofinding the group to which it belonged. Fortu-nately, this is very unlikely to happen. Finally,once the S values have been compiled and sorted,a line will have to be drawn to separate eachpleiston from the next. Each pleiston would thenreceive the name of any nomenclatural type strainthat fell within it. The line should, if possible,be drawn through the "point of rarity" (41). Butalmost certainly it will appear very difficult,on occasion, to justify why a particular strainshould be on one side of the line, and so called byone name, rather than on the other side of the lineand called by another name. If the pragmaticview of taxonomy is held, the only justificationthat will be necessary is to show that the line isdrawn in such a way as to provide a maximallyuseful taxonomy, for in a pragmatic classificationthe line is merely a convenient device for theassistance of scientists, not a fact of nature. Ofcourse considerable skill and experience in thewhole of bacteriology will be required in decidingwhich of the possible lines is the most useful.

III. TAxONOMIC PROBLEMS IN BACTERIOLOGYARISING OUT OF THE USE AND

MISUSE OF WORDS

Scientific discussion depends for its value onthe careful use of words, and it is worth while,therefore, to examine some of the words used inbacteriological taxonomy. The thesis that manyof the present controversies in biological clas-sification are semantic in origin has been arguedby several authors (9, 10, 24, 31). In addition,Crawshay-Williams (17) concluded from hisinteresting and stimulating analysis of the struc-ture of controversy that unfactual arguments inscience, i.e., those that cannot be settled by ex-periment, are due to a failure to make empiricaljudgments (such as are involved in taxonomy)

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according to the double criterion of appeal topurpose or context as well as according to fact.This failure leads to arguments about words ap-pearing as arguments about facts. An attempt willbe made in this section to show in a simple waythat bacteriological taxonomy is also subject tolinguistic confusion.One incipient verbal controversy concerns the

word "classify" itself. To classify is "to arrangeor distribute in classes according to a method orsystem" (40). The arranging, as it were, bringsthe classes into "existence." But "to distributein classes" presupposes that the classes havealready been formed. Clearly items cannot bedistributed into "nonexistent" classes. Thissecond meaning of classify is very close to "iden-tify," which has the special biological meaningof "to refer a specimen to its proper species" (40).The term "bacteriological classification" could,for the sake of clarity, be confined to the gather-ing of bacterial strains into groups according to apredetermined plan, such as their phylogeny orover-all similarity. Identification could be con-fined to the process of adding new members to thegroups once they have been formed. On this de-finition the classification process must precedethe identification process. The opposite view hasbeen expressed by Brown (8), possibly becausehe used "identify" in a different sense. Of course,the same characters used to form a group may be,and in some classifications are, those used foridentification, but the intellectual processes ofclassifying and identifying remain distinct.The word "relationship" can also be a cause

of confusion in bacteriology because what isdenoted by the word varies with the context inwhich it is used. For example, strain A is saidby one author to be related to strain B, by whichhe means that they have a similar pattern ofresults over a certain series of tests. Anotherauthor says that, on the contrary, A is related tostrain C but not B, by which he means that Aand C have a similar pattern of results over asecond series of tests. The situation becomesmore confused when either author assumes thathis particular series of tests is superior to theother's without stating why he considers it tobe so. Perhaps he may hint that his series givesa "natural" classification without indicatingwhich meaning of "natural" he has in mind. Thedanger is that this controversy is then treated asif it were a scientific one involving observable

facts. Actually, it is an artificial one which arises,not out of the facts, since these can easily beverified by experiment, but out of the differentuse each author makes of the word "related."When, therefore, two species are said to be re-lated it is important to indicate the kind of re-lationship involved, whether attributional orgenealogical or some other kind. This is par-ticularly important when a genus is defined as agroup of related species (3).Of all the words in the taxonomist's vocabu-

larly, probably the most difficult to define is"species." The perplexities which bacteriologistsencounter in trying to give the word an exactmeaning are well known (16, 38, 46, 50). A specieshas been described as more real or as having"a greater degree of objectivity" than any othertaxon (25), but it has also been called a man-madefiction (10, 45). Again, according to one author(6) a species is a dynamic system, but accordingto another it is as outdated as phlogiston (18).Further, a meaning given to "species" in onebiological discipline may not be used at all inanother. For example, the bacteriologist doesnot usually refer to interbreeding or exchange ofgenetical material when describing the meaningof species as other biologists sometimes do, thoughrecently an attempt has been made to introducespecies in this sense in bacteriology as well (37).Yet again, some bacteriologists have considereda species to be a discrete segment of a phyleticline evolving independently of other segments(5, 28).

Nevertheless, in spite of these difficulties someof the linguistic problems connected with thisword may be examined with advantage. Onesuch problem is whether or not a species is anobjective entity in the natural world, that is,one that can be examined or described by themethods of science. Suppose it is granted thata species is such a natural objective entity, whatare the properties possessed by all species thatmakes them recognizable as species? What arethe empirical techniques that demonstrate theseproperties (for unless such techniques are avail-able, there is no scientific way of demonstratingwhether any given "event" is a species or not)?Alternatively, in the terms of Gilmour's epis-temology (Part I), what are the sense data thatare clipped together by the term "species"?Clearly, there are no tests which demonstrate aspecies as a member of a class of objective enti-

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ties in the way that there are tests which demon-strate, say, an acid. It can therefore be concludedthat a species is not an objective entity.

Yet, from another point of view, any par-ticular species, say, Pseudomonas fluorescens, maybe thought of as all the bacteria that may legiti-mately bear that name. Suppose for a momentthat all of these bacteria could be gathered to-gether at one place and at one time. It wouldthen be possible to refer to the assembled multi-tude as a species. There would be no doubts asto their objectivity; they would be seen, smelt,and, no doubt, declared a public nuisance!Whence any members of this conglomerationthat are now in any laboratory may be said tobe part of an objective entity.Now this contradiction is due to the different

uses made of the word species. In the first case,the argument implied that a species is a kind ofthing whose properties are amenable to the scien-tific method. In the second instance, the argu-ment involved the proposition, "let all of thebacteria that may properly be called by any onelegitimate binominal constitute a species."Clearly the controversy under discussion evapo-rates once the meaning of the term is defined.It follows that the meaning of species varies withthe sense an author wishes to convey. Any in-quiry as to what a species is "really" or "in fact,"or as to what the essential features of a "truebacteriological species" are is pointless. The termspecies is applied on different occasions to differ-ent "events." Words, like species, are verbaldevices by means of which different events maybe conveniently associated by the same term.

Before any progress can be made, then, agree-ment must be reached on the meaning that theword is to convey. One suggested meaning is"let each distinct kind of bacterium be called aspecies" (3). This definition is deficient in somerespects. Firstly, in this paper, all the assemblagesof bacteria which result from sorting them ac-cording to a particular purpose or a particularselection of characters, have been called groups.Each group might instead have been called aspecies, since each group is a distinct kind ofbacterium, and indeed, in one or two instancesin earlier parts of this paper the two words havebeen used synonymously. On this definition, aspecies is as vague a term as a group. Secondly,by this definition, any distinct kind of bacteria,say the autotrophs, constitutes a species. But

most bacteriologists do not think of categoriesof this kind as constituting a species. LikewiseKauffmann (27) claims that he is justified incalling each serotype of the Salmonella group aspecies, since each is a distinct kind of bacterium.These objections indicate that the definitionunder review is not full enough, and must beamplified. The obvious way to amplify it is tostipulate the way in which the distinction is made.Thus the distinction could be made on morpho-logical or physiological grounds, so that the defi-nition could become "a species is a class (sortor kind) of bacteria with a common morphology"or "a species is a class (sort or kind) of bacteriawith a common physiology" or "a species is adistinct kind of bacterium, the distinction beingmade in such a way that the species is a unit ina natural classification." (The terms "commonmorphology" and "common physiology" areadmittedly vague, but are sufficiently precisefor the present purpose.) The word species wouldthen admit of several different usages, such asmorphological species, physiological species, natu-ral species, and so on. A similar situation existswhen this word is applied to multicellular or-ganisms (2, 12, 30, 32, 47). Difficulty arises whenone meaning of species is confused with anotherone; when, for instance, a morphological speciesis assumed to be a natural species (but see below).Of course it may be, but it also may not. It isthe untested assumption that leads to confusion.To reduce the indeterminacy of the word

species even further, its use could be confinedto one particular meaning and the "naturalspecies" meaning would be the obvious choice.Unfortunately "natural" itself as used in classifi-cation has several meanings (see below). Sup-posing, on the one hand, that the phylogeneticmeaning of natural is chosen, then a specieswould be defined as "a phylogenetically distinctkind of bacterium," and since phylogenetic dis-tinctions are difficult or impossible to make withcertainty in bacteriology (Part IL), few bacterialspecies could be described. Suppose, on the otherhand, that the "logical" meaning of the word isselected; the definition then becomes, "a speciesis a distinct kind of bacterium in a natural classi-fication, the distinction being based on the char-acters selected to form the classification." Un-fortunately a logical classification which issufficiently natural to serve most bacteriologicalpurposes has not yet emerged either, although

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over-all similarity may eventually lead to one(Part II).Again Principle 7a of the International Code

of Nomenclature of Bacteria and Viruses (26)rules that the species is the basic category of thetaxonomic hierarchy, but Principle 7d allowsthat the definition may vary "according to in-dividual opinion and the state of the science."It can be deduced from several places in theInternational Code of Nomenclature (26)-e.g.,Principle 11 with its annotations and Rule 9with its annotations-that the meaning givento the word species throughout the Code is thata species consists of a nomenclatural type culture(specimen, preparation, illustration, or descrip-tion) together with those cultures considered tobe closely associated with it. The manner of theassociation, that is, the relationship between amember of the species and the nomenclaturaltype, is not indicated. Since the relationshipmay be attributional, genealogical, genetical,or of some other sort, attributional species, geneo-logical species, and genetical species are possible.Which use of the word indicates the basic cate-gory of the taxonomic hierarchy?

Until agreement is reached, then, as to themeaning to be given to the term species, bac-teriologists will no doubt continue to use theword in several ways, such as giving it the under-defined connotation of a distinct kind of bac-terium or by confining the term to various usagesas in morphological species, physiological species,and so on. In the first case "species" will besynonymous with "group." In the second case,it will be important to make clear which kindof distinction is being employed at any one time,and to avoid applying one meaning of "species"when another is intended.

Finally, "species" (in the underdefined vaguesense of a distinct kind of bacterium) differs intwo ways from "species" as used in logic. Firstly,in the hierarchical classificatory scheme of thelogician each class in the hierarchy is "species"to the class above it and "genus" to the classbelow it, so that the terms "genus" and "species"are not confined to the two lowest classes of thescale. A second, more important difference isthat in logic any particular species is definablein the sense that it includes only those objectspossessing the property or character on whichthe division is made and rigidly excludes allothers. But in biology, particularly bacteriology,such rigid classes are not found to be useful be-

cause of the multitude of exceptions. A glanceat any standard manual which describes namedbacterial strains will show that words such as''usually," "probably," "sometimes," and so onare used in the descriptions. But these descrip-tions are on occasion called definitions. Clearly"definition" here has a special meaning.

It has been the experience of taxonomiststhat some of the groups of bacteria with whichthey have dealt have been sufficiently homo-geneous for their definition (using the word inthe special sense) to be made fairly rigid, whilein other groups much looser definitions havebeen advantageous. When it was found that thedefinition was becoming very loose, the wordspecies, as such groups are usually called, mayhave been abandoned and "species-group" substi-tuted instead. The only difference between aspecies and species-group seems to be one of therigidity of definition, and there is no clear demar-cation between them.

Since in the special sense, a definition doesnot rigidly demarcate what is defined, the ques-tion must be asked as to whether there is anylimit to the looseness of a definition, and whetherthe definition of a group or species should be asloose or as tight as possible. If the pragmaticview of taxonomy is adopted, it is soon clearthat these questions are more apparent than real.The looseness or tightness of the definition ofthe group would be that looseness or tightnesswhich produces the best classification, bearingin mind the purpose for which the classificationwas devised.

Another word which has several meanings isthe word "type." As pointed out in the annota-tions to Recommendation 8a(2) of the Inter-national Code of Nomenclature (26), the use ofthis word with two very different meanings is amajor source of confusion. The Code (26) thenrecommends a preferred use as in "type species"or "nomenclatural type" and a second, less de-sirable use as in serotype, morphotype, biotype,and phagotype. The word, however, is also fre-quently employed in two more senses. Firstly,there is the meaning of a recognizable kind orsort as in "a new type of bacteria." Secondly,there is the meaning set out in the followingpassage from Whewell (49).

"Though in a natural group of objects a defini-tion can no longer be of any use as a regulativeprinciple, classes are not therefore left quite loose,

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without any certain standard or guide. The classis steadily fixed, though not precisely limited; it isgiven, but it is not circumscribed; it is determinednot by a boundary line without, but by a centralpoint within; not by what it strictly excludes butby what it eminently includes; by an example,not by a precept; in short, instead of a Definitionwe have a Type for our director.The Type is an example of any class, for instance

a species of a genus, which is considered as emi-nently possessing the character of the class. Allthe species which have a greater affinity with thistype-species than with any other, form the genus,and are ranged about it, deviating from it invarious directions and different degrees. Thus agenus may consist of several species which ap-proach very near the type, and of which the claimto a place with it is obvious, while there may beother species which straggle further from thiscentral knot and which yet are clearly moreconnected with it than with any other. And evenif there should be some species of which the placeis dubious, and which appear to be equally boundto two generic types, it is easily seen that thiswould not destroy the reality of the generic groupsany more than the scattered trees of the inter-vening plain prevent us speaking intelligibly of thedistinct forests of two separate hills.The type of species of every genus, the type-

genus of every family is then one which ispossessed of all the characters and properties ofthe genus in a marked and prominent manner....The type must be connected by many affinitieswith most of the others of its group; it must benear the centre of the crowd and not one of thestragglers. "

At the risk of being tedious, it might bepointed out that Whewell is here using definitionin the same way as a logician and not in thespecial way discussed above: "class" in this pas-sage indicates a sort or kind, not the taxon be-tween an order and a division. Now the use of"type" in the above passage, indicating an orga-nism which is typical of the taxon to which itbelongs, is current among bacteriologists. Afterall, it is not altogether strange that types shouldbe typical. But the preferred use of the term,as in nomenclatural type, may well indicate anorganism which is not typical. As stated in thenote to Principle 11 of the International Codeof Nomenclature (26), "The nomenclatural typeis not necessarily the most typical or repre-sentative element of a taxon. It is merely thatelement with which the name of a taxon is perma-nently associated." "Typical" in the first sen-

tence of this quotation is the adjective derivedfrom type and is given its usual connotation,so that in this one sentence "type" and "typical"have two different meanings. It is acknowledgedthat the nomenclatural type concept is a usefuldevice to bring order to nomenclature and isfound in all the biological Codes, but needlessconfusion arises because a word which is in gen-eral use is employed in a specialized way, insteadof a new word being coined to convey the new,specialized meaning. A further point of interestis the reference in Opinion A (26) and Opinion 11(20) of the Judicial Commission to "type orstandard cultures." The addition of the wordstandard suggests that "type" here refers to amodel or perfect example of the organism. Sucha concept is nearer Whewell's "type" rather thannomenclatural "type." This viewpoint is rein-forced by the suggested designation of standardtypes for certain species groups, subspecies (va-rieties), and serotypes in Draft Proposal 5 (19)of Opinion 11. Since nomenclatural types apper-tain only to recognized taxa, and since neitherspecies groups nor serotypes are so recognized,it is reasonable to infer that standard types arenot nomenclatural types. But against this, thefinal form of Opinion 11 (20) refers only to thetype or standard culture of species. Clearly,then, the use of "type" in anything but its every-day sense is liable to lead to confusion. Schopf(39) has suggested the term "nomenifer," mean-ing name bearer, instead of nomenclatural type,and such a proposal is surely worthy of seriousconsideration.Another task in this analysis of the meaning

of taxonomic words is to inquire into the mean-ing of "natural" and "artificial" as applied toclassification. This subject is discussed at somelength by Gilmour (22). The word "natural"itself is unfortunate in that it has very manymeanings, as a consultation of the dictionaryshows. In addition, it has emotional overtonesfor the biologist. Students of nature naturallyprefer to deal with natural things. For most tax-onomists during the last century, a natural classi-fication has generally been considered to be onebased on phylogenetic relationships. Thus inzoology, the classification based on mechanismsof reproduction is considered to be a naturalclassification, because this attribute is said toindicate the phylogenetic relationships with someprecision, whereas classification based on loco-

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motion is said to be artificial because locomotionis less often an indication of phylogenetic re-lationships. Sometimes natural classification isdescribed as being allied to a scientific, philo-sophical approach to living things, while arti-ficial classifications are made for some "practicalhuman purposes" (21). To the pragmatic tax-onomist, however, the terms natural and artificialclassification are retained with the same usageas in logic; i.e., a natural classification is one thatserves many purposes and an artificial classifi-cation is one that serves only a limited numberof purposes. A third meaning has sometimesappeared in the bacteriological literature, carry-ing the sense that the classification in question,though neither phylogenetically nor logicallynatural, corresponds with a very ill-defined some-thing in nature.The phylogenetic classifications of the botani-

cal and zoological sciences are, of course, naturalones in the logical as well as the phylogeneticsense, in that such classifications have servedmany purposes. Nevertheless, there is no reasonto believe that these classifications are logicallythe most natural ones that can be devised. Soalso, because bacteria cannot be classified phylo-genetically, it does not mean that a logicallynatural bacterial classification is impossible.

It is also worth noting that since logicallynatural classifications differ from logically arti-ficial ones only in the number of purposes theyserve, no particular classification can be said tobe completely natural or wholly artificial. Forthis reason, the bacterial classifications in generaluse at the moment can be said to be natural toa certain degree. The number of purposes that aclassification must serve before it is called naturalis a matter of personal choice, and is unimpor-tant. The classification which the taxonomistseeks is the most natural, the most all-embracing,that he can devise. His endeavor is to expandthe amount of knowledge that his classificationcan organize. The bacteriologist engaged in non-taxonomic pursuits would obviously prefer touse the most natural taxonomy available in orderto communicate his knowledge to others engagedin different facets of bacteriology and to integratetheir findings with his. But when a bacteri-ologist finds that a wide-purpose, natural tax-onomy does not assist him, there is no reasonwhy he should not use a narrow-purpose, arti-ficial taxonomy. Indeed, this is what he does.

Lastly, to conclude this semantic section, itwould be worth while to analyze the terms "inter-mediate" and "bacterial spectrum." Both theseconcepts are of course metaphors, based on thenotion that similarities and dissimilarities canbe likened to the closeness or distance betweentwo points. "C is an intermediate" means thatC can be placed on the line between A and B,but there is no indication whether it is nearerA than B. When D is an intermediate also, itsposition is unknown not only with respect to Aand B but also with respect to C. In short, theterm "intermediate" does not convey muchinformation. The "spectrum" is a slightly moreelaborate example of the same metaphor and isoften used when a large number of organisms isbeing considered. It should be noted, however,that since a linear metaphor is being used, thevarying property should also be linear. Thus,in the series ABCD, the property representedby the distance AD should equal the sum of thedistances A to B, B to C, and C to D. The spec-trum analogy should only be used when a prop-erty is steadily gained, steadily lost, or changesin some regular way. This regularity is often notconsidered when the term spectrum is used andit thus loses meaning. Similarity values whichare derived from the Adansonian method ofclassification change in a regular way, and theyhave the advantage that when C is said to beintermediate between A and B, the relative po-sitions of A, B, and C are known. It is foundthat these values cannot be held to fall on astraight line, however, and the spectrum analogybreaks down and is replaced by a multidimen-sional space. Hence, as already pointed out(Part II), classification by over-all similarityhas the advantage of enabling the classifier toknow the relative position of his organisms moreexactly than at present, and the indeterminacyof the terms "intermediate" and "spectrum" issuperseded.

There can be little doubt, then, that severalwords are used by bacteriologists in severalsenses, or with diffuse meanings, and this is ahindrance to clear expression and thinking. Un-fortunately, taxonomists often attempt to confinea word which is in general use to one technicalmeaning. Sometimes this does not matter. Con-fusion is not likely to arise, because one ofAristotle's predicables, genus, is given a technicalmeaning in biological taxonomy. But other words.

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for example, class, variety, type, group, phase,form, state, and stage, which are valuable to thebacteriologist in their common everyday sense,have a recommended taxonomic use set out inthe International Code of Nomenclature of theBacteria and Viruses (26). Anyone, therefore,who wishes to follow the code-a duty especiallyincumbent upon every author of a paper in tax-onomy-is left with a much reduced vocabulary,which may in fact be inadequate for what hewishes to convey. A better procedure would beto coin new words wherever this is possible.

IV. ADDENDUM

Since the foregoing essay was submitted forpublication, the Society for General Micro-biology has compiled its Symposium on MicrobialClassification (1). The authors of several papersin the Symposium have put forward with greatclarity many of the arguments proposed in thisessay. To express the same thoughts again, how-ever, can do no harm and might indeed be valu-able. Other contributors have put forward apoint of view different from that taken here.Bisset, for example, is far more optimistic of thechances of developing a phylogenetic classifi-cation than is suggested in Part IIA of this essay.It is also clear from the Symposium that thenewer fields of bacteriological study, such ascomparative biochemistry and intracellular mor-phology, are beginning to provide valuable datafor the taxonomist.One very useful contribution to the philo-

sophical aspect of taxonomy was made by Cainduring the discussion on the Symposium whenhe distinguished between "arrangement" and"classification." One might say that arrangementrepresents the objective side of taxonomy whileclassification represents the subjective. Thus,organism A is similar to organism B to a certainextent, which can be called X. Given a stableorganism and stable conditions (see below), thenwhoever examines A and B will find they havethe same similarity, X, to each other; that is,the arrangement of A to B is constant. Butwhether X is of such a value that A and B areto be included in the same or different classes(in its usual, not nomenclatural, sense) is a matterfor the subjective judgment of taxonomists. Asstated earlier in this paper, the lines drawn be-tween classes are devices for the convenience ofscientists, not facts of nature. Put in terms of

the epistemology discussed in Part I, the experi-enced "given" sense data and their derivatives(such as S values) give rise to the arrangement,while conceptual clips are employed for the for-mation of classes, that is, for classification.To some extent, the Symposium extended the

taxonomists' vocabulary. The term phenetic hasbeen suggested to describe a classification basedon over-all similarity. If the proposition putforward in part IIB of this essay, that a taxonomybased on over-all similarity leads to a multi-purpose or logically natural taxonomy, is correct,then phenetic classifications would be identicalwith the multipurpose ones of this paper.During the discussion of the Symposium,

Silvestri added the word "stable," whether ap-plied to a bacterial character or to a classification,to those words used in taxonomy with severalmeanings. What is called stable depends on thetime scale involved. Ultimately all things areunstable in a changing universe. By a stablecharacter, bacteriologists usually mean one whichdoes not change during the period in which theyare interested in it.

V. ACKNOWLEDGMENTSThis work was financed by the Development

Commission and was carried out by a ResearchFellow of the Department of Bacteriology, Uni-versity of Aberdeen, as part of the research pro-gram of the Department of Scientific andIndustrial Research (Crown Copyright reserved).

VI. LITERATURE CITED

1. AINSWORTH, G. C., AND P. H. A. SNEATH,[ed.]. 1962. Microbial classification. Cam-bridge University Press, Cambridge.

2. ALVAREZ-LoPEz, E. 1954. Apuntes para unboceto de la teoria de la especie. Bol. Soc.esp. Hist. nat. sec. biol. 51:5-49.

3. BREED, R. S., E. G. D. MURRAY, AND N. R.SMIrH. 1957. Bergey's manual of determina-tive bacteriology. 7th ed. The Williams &Wilkins Co., Baltimore.

4. BILLING, E. 1960. The bacterial genera Pseu-domonas and Achromobacter. Nature 188:25-27.

5. BISSET, K. A. 1952. Bacteria. E. & S. Living-stone Ltd., Edinburgh.

6. BLAIR, W. F. 1956. The species as a dynamicsystem. Southwestern Nature 1:1-5. Ab-stracted by Biological Abstracts, 1957,31: abstr. no. 33435.

7. BROWN, C. B. 1950. Science: its method and

1962] 289

on May 16, 2020 by guest

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nloaded from

G. D. FLOODGATE

its philosophy. George Allen & Unwin,Ltd., London.

8. BROWN, J. H. 1953. Classification of the genusStreptococcus. Report to the sub-com-mittee on Streptococcus. Intern. Bull.Bacteriol. Nomen. and Tax. 3:170-174.

9. BURMA, B. H. 1949. The species concept: asemantic review. Evolution 3:369-370.

10. BURMA, B. H. 1954. Reality, existence andclassification. A discussion of the speciesproblem. Madrono 12:193-209.

11. CAIN, A. J., AND G. A. HARRISON. 1958. Ananalysis of the taxonomists' judgement ofaffinity. Proc. Zool. Soc. London 131:85-98.

12. CHOZALSKY, L. I. 1957. The structure of speciesand its course of differentiation (in Russian).Vestnik Leningrad. Univ. 21:155-158.

13. CLIFFORD, H. T. 1955. An index for use inquantitative taxonomic problems. NewPhytologist 54:132-137.

14. COHN, M. 1958. On the differentiation of apopulation of Escherichia coli with respectto 8-galactoside formation. In W. D. Mc-Elroy and Bentley Glass, [ed.], Symposiumon the chemical basis of development.Johns Hopkins Press, Baltimore.

15. COHN, M., AND K. HORIBATA. 1959. Inhibitionby glucose of the induced synthesis of f3-galactoside-enzyme system of E. coli.Analysis of maintenance. J. Bacteriol.78:601-612.

16. COWAN, S. T. 1955. Symposium. The principlesof microbial classification. Introduction.The philosophy of classification. J. Gen.Microbiol. 12:314-321.

17. CRAWSHAY-WILLIAMS, R. 1957. Methods andcriteria of reasoning. Routledge and KeganPaul, London.

18. DAVIDSON, J. R. 1954. A dephlogisticatedspecies concept. Madrono 12:246-251.

19. EDITORIAL BOARD, International Commis-sion. 1953. Summary of opinions and pre-liminary statements. File No. 54. Intern.Bull. Bacteriol. Nomen. and Tax. 3:82.

20. EDITORIAL BOARD, International Commission.1954. Nomenclature of species in the bac-terial genus Shigella. Opinion 11. Intern.Bull. Bacteriol. Nomen. and Tax. 4:148--149.

21. ENCYCLOPAEDIA BRITANNICA. 1947. Encyclo-paedia Britannica, Ltd., London.

22. GILMOUR, J. S. L. 1937. A taxonomic problem.Nature 139:1040.

23. GILMOUR, J. S. L. 1940. Taxonomy andphilosophy. In J. Huxley, [ed.], The newsystematics. Oxford University Press,Oxford.

24. GREGG, J. R. 1950. Taxonomy, language andreality. Am. Naturalist 84:419-435.

25. HUXLEY, J. 1940. Introductory: towards thenew systematics. In J. Huxley, [ed.], Thenew systematics. Oxford University Press,Oxford.

26. JUDICIAL COMMISSION. 1958. In R. EBuchanan, S. T. Cowan, T. Wiken, and W.A. Clark, [ed.], International code of nomen-clature of the bacteria and viruses. IowaState University Press, Ames, Iowa.

27. KAUFFMANN, F. 1959. On the principles ofclassification and nomenclature of Entero-bacteriaceae. Intern. Bull. Bacteriol.Nomen. and Tax. 9:1-8.

28. KRASSILNIKOV, N. A. 1949. Determination ofBacteria and Actinomycetes. Akad. NaukU. S. S. R.

29. LOCKE, J. 1689. An essay concerning humanunderstanding. 25th ed. (1825). ThomasTegg, London.

30. MANTON, I. 1958. The concept of the aggregatespecies. Systematics of to-day. In OlovHadberg, [ed.], Proceedings of a symposiumheld at the University of Uppsala in com-memoration of the 250th anniversary of thebirth of Carolus Linnaeus. Uppsala andWiesbaden.

31. MAYER, E. 1949. The species concept:semantics versus semantics. Evolution3:371-372.

32. MEGLITSCH, P. A. 1954. On the nature ofspecies. Systemat. Zool. 3:49-65.

33. MICHINER, C. D., AND R. R. SOKAL. 1957. Aquantitative approach to a problem inclassification. Evolution 11:130-162.

34. MILL, J. S. 1862. A system of logic. 5th Ed.Parker, Son and Bourn, London.

35. OPPENHEIMER, C. H. 1958. Evidence of fossilbacteria in phosphate rocks. Inst. of MarineSci. 5:156-159.

36. RAO, C. R. 1948. The utilisation of multiplemeasurements in problems of biologicalclassification. J. Roy. Stat. Soc., Ser. B.10:159-193.

37. RAVIN, A. W. 1960. The origin of bacterialspecies. Bacteriol. Rev. 24:201-220.

38. RAZUMOVSKAYA, Z. G. 1957. On species inmicro-organisms. Vestnik Leningrad. Univ.27:144-146.

39. SCHOPF, J. M. 1960. Emphasis on holotype(?). Science 131:1043.

40. Shorter Oxford English dictionary. 1947.corrected 3rd ed. Oxford University Press,Oxford.

41. SNEATH, P. H. A. 1957. Some thoughts onbacterial classification. J. Gen. Microbiol.17:184-200.

42. SNEATH, P. H. A. 1957. The application of

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br.asm.org/

Dow

nloaded from

THEORETICAL ASPECTS OF BACTERIAL TAXONOMY

computers to taxonomy. J. Gen. Microbiol.17:201-226.

43. SOKAL, R. R., AND C. D. MITCHENER. 1958.A statistical method for evaluating syste-matic relationships. Kansas Univ. Sci. Bull.38:1409-1438.

44. SPRAGUE, T. A. 1940. Taxonomic botany withspecial reference to the angiosperms. InJ. Huxley, [ed.], The new systematics,Oxford University Press, Oxford.

45. TURRILL, W. B. 1951. More new systematics.A quotation from a book under review.Nature 168:1097-1098.

46. VAN NIEL, C. P. 1948. The classification andnatural relationships of bacteria. ColdSpring Harbor SymposiaQuant. Biol. 11:285-301.

47. VAN STEENIS, C. G. G. T. 1958. Specific de-limitation with special reference to tropicalplants. Systematics of today. In OlovHadberg, [ed.], Proceedings of a symposium

held at the University of Uppsala in com-

memoration of the 250th anniversary of thebirth of Carolus Linnaeus. Uppsala andWiesbaden.

48. VOGEL, H. J. 1957. Repression and induction,a control mechanism of enzyme biosyn-thesis: the "adaptive" formation of acetyl-ornithase. In W. D. McElroy and BentleyGlass, [ed.], Symposium on the chemicalbasis of heredity. Johns Hopkins Press,Baltimore.

49. WHEWELL, W. 1858. History of scientificideas, Chap. 2. cited by Mill (34).

50. WILSON, G. S., AND A. A. MILES. 1955. Topleyand Wilson's principles of bacteriology andimmunity. 4th ed. Edward Arnold, Ltd.,London.

51. ZOBELL, C. E. 1957. Annotated bibliographyon paleoecology of bacteria. Treatise on ma-

rine ecology and paleoecology. Mem. Geol.Soc. Am. 67:693-698.

19621 291

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