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8-1988

A Plea for Improved Presentation of Type Material for

Susan M. Bandioni University of New Mexico

Donald W. Duszynski University of New Mexico, @unm.edu

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Bandioni, Susan M. and Duszynski, Donald W., "A Plea for Improved Presentation of Type Material for Coccidia" (1988). Faculty Publications from the Harold W. Manter Laboratory of Parasitology. 160. https://digitalcommons.unl.edu/parasitologyfacpubs/160

This Article is brought to you for free and open access by the Parasitology, Harold W. Manter Laboratory of at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Faculty Publications from the Harold W. Manter Laboratory of Parasitology by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. J. Parasit.,74(4), 1988, pp. 519-523 ? AmericanSociety of Parasitologists1988

INVITEDCRITICAL COMMENT...

A PLEA FOR IMPROVEDPRESENTATION OF TYPE MATERIAL FOR COCCIDIA

Susan M. Bandoni and Donald W. Duszynski Department of Biology, The Universityof New Mexico, Albuquerque, New Mexico 87131

ABSTRACT: The "true"coccidia (phylum , suborder Eimeriina) constitute a largeand heterogeneous group of parasitic protozoa. Despite the large number of described species (ca. 1,650) and the medical and veterinaryimportance of some (e.g., Toxoplasma), 2 facts are clear: (1) the majority of coccidia species are probablyyet undescribed,and (2) the phylogeneticrelationships of those describedspecies are poorly known. Contributingto the latter dilemma is the lack of a traditionto provide type specimens by those who describe new species, even though the InternationalCode of Zoological Nomenclature specificallyrecommends the designationof a type specimen with the descriptionof a new species. With the publicationof a new edition of the Code (1985), explicit provisions are made for the unique concernsof taxonomists workingwith Protozoa. Here we remind those interestedin the taxonomy of coccidia of an alreadyestablished method for preserving oocysts in resin and, as an alternative,suggest the standardizationof a photographicprocedure through which type specimensof coccidian oocysts might also be submittedto and maintainedin accreditedmuseums. Thus, coccidia taxonomists should no longer have an excuse for their failureto designatetypes.

The protozoan phylum Apicomplexa Levine, to developing methods to preserve coccidian 1970, comprises a large and heterogeneous group oocysts permanently or to other viable alterna- of obligate intracellular parasites including many tives. Consequently, reference collections of pre- species of medical and veterinary significance served specimens of eimeriid species do not ex- (e.g., , , , ist, with but few exceptions (e.g., Calyptospora Eimeria, and Toxoplasma). About one-third of empristica, see Fournie et al., 1985). the approximately 4,600 described species in the According to the most recent edition of the phylum are placed in a single family, , Zoological Code (Ride et al., 1985), a type spec- and the vast majority of these species are known imen serves as "the objective standard of refer- from a single life-cycle stage, the sporulated ence by which the application of the name it oocyst. It is the process by which new eimeriids bears is determined, no matter how the bound- are described that we wish to address in this aries of the taxon may change" (Article 61 (a), essay. p. 115). Thus, the type specimen is intended to be unchanging and objective, whereas the limits HISTORICALPERSPECTIVE of a nominal species are recognized to be sub- Although the names of apicomplexans reflect jective and transient. The type specimen, there- the use of the International Code of Zoological fore, serves as an anchor for the name, and to Nomenclature, the taxonomic procedure fol- some extent, it is the name (see Mayr et al., 1953). lowed in documenting the existence of new ei- The Bacteriological Code of Nomenclature meriid species has not been consistent with the (Lapage et al., 1975) allows, and indeed encour- intention of the Code. For example, the Code ages, the submission of cultures to a type culture explicitly recommends the designation of type collection. Apicomplexans cannot be cultured specimens for new species, but a type tradition axenically, and although some eimeriid species is lacking among taxonomists working with the have been cultured in host cells, the technical Eimeriidae. difficulties in culturing new species isolated from Historically, under the Zoological Code, "the wild animals preclude the routine submission of type is a specimen," with the implication that type cultures. the type specimen will be available for future Both the Botanical Code (Voss et al., 1983; study. Unfortunately, most scientists describing Article 9.3) and the Bacteriological Code (Rule new coccidian species have not devoted attention 18A) have made provisions for organisms that cannot be permanently preserved: drawings are Received 2 October 1987; revised 18 March 1988; acceptable as type specimens. Previous editions accepted22 March 1988. of the Zoological Code have allowed illustrations 519 520 THE JOURNALOF PARASITOLOGY,VOL. 74, NO. 4, AUGUST 1988 to serve as lectotypes, but have not addressed 165-166) would consider such names invalid. the issue of whether illustrations may serve as Under such a strict interpretation of the Code, holotypes. In the most recent version of the Zoo- the status of most of the species names in the logical Code (1985, Article 73 (a) (iv), p. 149) Eimeriidae would be uncertain. Indeed, the same the following statement is made, "Designation taxonomic practices are undoubtedly widespread of an illustration of a single specimen as a ho- among taxonomists working on other apicom- lotype is to be treated as designation of the spec- plexans; we are restricting our comments to a imen illustrated; thefact that the specimen cannot single family with which we are most familiar. be traced does not of itself invalidate the desig- Our objective in writing this essay, however, is nation (emphasis ours)." We interpret this to not to threaten to declare hundreds of species mean that illustrations are finally acceptable sub- names invalid, but to draw attention to the lack stitutes for type specimens. According to Article of a standard for the description of new eimeriids 72 (c) (v), p. 145, ". . . in the case of a nominal and to emphasize how this has impeded efforts species group taxon based on an illustration or to understand the systematic relationships among description . . ., the specimen illustrated or de- the genera and species within the Eimeriidae. scribed and not the illustration or description" Systematics, or "beta taxonomy" can only exist (is eligible as a name-bearing type). Regardless with a firm foundation of "alpha taxonomy" (and of whether the specimen or the illustration is nomenclature) to support it. If there is no means considered the type, it seems clear that the intent of comparing species (i.e., no reference collec- of the new edition of the Zoological Code is to tions), neither phylogenetic nor phenetic rela- provide mechanisms by which type specimens tionships among species can be discerned. The can be identified for more nontraditional animal literature on these organisms then can be only groups (e.g., protozoa). Whether we call them an endless series of descriptions and redescrip- holotypes, syntypes, or even phototypes (=icon- tions, with valueless speculation regarding the otype, see Frizzell, 1933) is of little concern to significance of real or imagined differences. us. The major point of this essay is that we use The uses of type specimens go beyond their the technology available to begin a type specimen importance in nomenclature, however, and thus tradition for the coccidia. the lack of a type tradition among biologists Given our conclusion that illustrations may be working with the coccidia has implications be- considered legitimate replacements for type yond the invalidity of the species names. Black- specimens under the Code, an additional prob- welder (1967, p. 166) identified 3 ways in which lem arises for biologists working on the coccidia. type specimens are useful to the scientific com- For an illustration to serve as a type, there is an munity. These uses of types will be considered, implicit requirement that the illustration be based using specific examples drawn from the taxo- on a single individual. Types serve as the "last nomic literature on apicomplexans. court of appeal" in disputes over the application First, in poorly known groups, type specimens of scientific names (Mayr et al., 1953). It is im- serve as "a source of unchallengeable characters" perative that an illustration intended to serve as (Blackwelder, 1967, p. 166) for the group. The a type specimen represent a single individual be- monotypic family Spirocystidae Leger and Du- cause of the danger of basing a composite illus- boscq, 1915, is sometimes cited as an example tration on 2 or more species, a situation that of just how little is known about some apicom- would become a nomenclatural nightmare. Yet, plexans (Levine, 1982, 1985). The type and only composite drawings of sporulated oocysts are the species, Spirocystis nidula Leger and Duboscq, standard form of presentation oftaxonomic find- 1911, was observed only once by the original ings in descriptions of new eimeriid species. This authors. Although later attempts to find other is not meant to imply that composite illustrations examples of this species were unsuccessful, Leger have no value in coccidian taxonomy; rather, this and Duboscq (1915) published their original very useful means of presenting taxonomic in- findings. The meront stage of this organism does formation should be supplemented by material not resemble any known coccidian, and the less subject to errors of interpretation. oocysts, with their "vermicular sporozoites," bear The Zoological Code does not explicitly ad- a striking resemblance to nematode eggs. In short, dress the question of the validity of names es- there is little in the evidence provided that would tablished without the designation of type speci- allow this organism to be placed in the phylum mens. Some authors (see Blackwelder, 1967, pp. Apicomplexa with any degree of confidence. If a BANDONIAND DUSZYNSKI-OOCYST DESCRIPTIONS AND COCCIDIAN TAXONOMY 521 type specimen existed, it would be possible to replicationof an experiment in another labora- reexamine the organism and check some of the tory, and it serves as a supplement to the peer more questionable(or dubious) characters;this, review process. in turn, would allow a reevaluationof the status The importanceof type specimens(and indeed of Spirocystis.In the absence of a type specimen of taxonomy)goes beyond their necessity in sys- tradition,descriptions such as this one are main- tematics. Good taxonomy is an integral aspect tained in the literaturebecause there is no alter- of the scientific method for experimentalbiolo- native. Unfortunately,the evidence presentedfor gists. In order to draw generalconclusions from the existence of Spirocystisis not much weaker an experiment it is necessary to know that the than the evidence presentedfor the existence of organismsunder study representa homogeneous many other coccidian species. group. All other investigations of eimeriid coc- Second,in studiesof intraspecificvariation (and cidia, whether biochemical, physiological, im- even interspecificsimilarities), the type specimen munological, etc., are undermined by a shaky represents"one point which unequivocablyfalls taxonomic foundation. within the species" (Blackwelder,1967, p. 166). Presentlythere are several factors related to in- PROPOSEDSOLUTIONS traspecificvariation that raise problems in ei- What then can be done to promote progress meriid identification when studying sporulated in eimeriidtaxonomy and systematics?The pub- oocysts from wild animal populations.Although lication of the newestedition of the International the variationsseen between individuals within a Code of Zoological Nomenclature (Ride et al., speciesare not uniqueto coccidiansas organisms 1985) should usher in a new era in protozoan (note, for example, the greatdifferences between systematics.Historically, the ZoologicalCode has breeds of dogs), coccidian taxonomists need to been inadequate for these organisms and, as a be reminded of their existence. For example, consequence,has been applied in a rather hap- oocysts of one eimerianmay vary greatlyin size, hazard fashion. Now, for the first time, explicit but otherwise be indistinguishable from each provisions are made for the unique concerns of other (e.g., oocysts of Eimeria separata Becker taxonomistsworking with protozoa.For the new and Hall, 1931, vary in size by as much as 40% provisions in the ZoologicalCode to be put into over patency;Duszynski, 1971) or oocysts pre- practice, we must require a reevaluation of the sumed to represent one species may be highly taxonomic proceduresused with groups such as polymorphicwithin the same or closely related the Eimeriidae.Perhaps of greatestimportance, host species (e.g., Eimeria reichenowiYakimoff then, is the need to create an awarenessamong and Matschoulsky,1935; Parkerand Duszynski, biologistsworking with eimeriids of the value of 1986). In addition, the role of evolution in the designatingtype specimens. Buildinga type tra- morphologicsimilarity of differentspecies in the dition will require not only the designation of same host (e.g., chickeneimerians; Joyner, 1982) holotypes for new species, but also the designa- and the fact that some species can infect unre- tion of lectotypesor neotypesfor existingnames. lated host species (e.g., Eimeria chinchillae De In addition, type species need to be designated Vos and Van der Westhuizen, 1968, see De Vos, for the known genera. 1970; Eimeria tamiasciuri Levine and Ivens, Methods of permanentpreservation of cocci- 1965, see Vance and Duszynski, 1985, and Hill dian oocysts now exist (Marchiondo and Du- and Duszynski, 1986) must be recognizedas con- szynski, 1978, 1988), so there is no longer any foundingfactors when describingnew coccidian reason not to begin to designatetype specimens species from sporulatedoocysts from wild ani- for those speciesthat can be handledin this man- mals. The existenceof a type specimentradition, ner. In addition, the new provisions of the Zoo- especially if large reference collections of logical Code regardingillustrations provide an voucher specimens were available for study, alternative:photography offers many of the ad- would greatlyaid our dealing with such compli- vantagesof preservedspecimens at a fractionof cating factors. the cost of the methods employed by Marchion- Finally,the third way in which type specimens do and Duszynski(1978). Thus, when describing can be useful to the scientificcommunity is that new species one could preparea series of pho- types serve as a means of checkingthe accuracy tomicrographs,chosen carefully to illustrate as of publisheddescriptions (Blackwelder, 1967, p. many featuresof the new species as possible, and 166). This is in some ways comparable to the perhapsmounted on poster board with the nec- 522 THEJOURNAL OF PARASITOLOGY,VOL. 74, NO. 4, AUGUST 1988

FIGURE1. Suggested format for beginning a type specimen tradition among coccidiologists. A plate of photomicrographs of representative oocysts showing main distinguishing features of each new species. essary structural, host, and locality data on the type (=phototype) series consisting of oocysts back (Figs. 1, 2). If we standardize the size, the probably represents a more realistic goal. If rep- poster can be submitted to, and maintained in, utable journals made the designation of type accredited museums just as slides of helminth specimens (including type species for new gen- types are catalogued currently. Two copies of the era) a requirement for publication (as most al- phototypes should probably be submitted so that ready do for helminths), there would no longer one set remains permanently in the repository be an excuse for the failure to designate types. while the other would be on loan. Ideally, ha- Type specimens are not a panacea: there is some pantotypes, composite types in which all stages information that cannot be obtained from pre- in the life history are represented, should be sub- served specimens or photomicrographs. Indeed, mitted as advocated by Williams (1986). For there is much to be gained by the collection of many coccidia spp. this would be next to im- fresh material. However, type specimens repre- possible, however, and the deposition of a syn- sent a point of common ground for discussion,

DATE SUBMITTED: 5 August 1987 COCCIDIAN SP: Eimeria tadarida TYPE HOST: Tadarida femorosacca (Merriam) DEPOSITED IN MUSEUM?: Museumof Southwestern Biology Division of Mammals The University of NewMexico MUSEUM #: MSB#53835 (female) Albuquerque, NM37131 COLLECTOR, #, DATE: J. Haydock, #282, 27 October 1980 TYPE LOCALITY: MEXICO,Sonora: 19.3 kmE Alamos by road Rio Cuckujaqui OTHER COCCIDIANS PRESENT? None PREVALENCE: 1 of 1 from Sonora; 0 of 17 from Baja California Norte, MX OTHER HOSTS WITH THIS SP: None to date

NATIONAL MUSEUM #: REFERENCE OF ORIGINAL DESCRIPTION: Duszynski,D. W., D. W. Redukerand B. B. Parker. 1988. Eimeria from bats of the world. II. A new species in Tadarida femorosacca from SonoraTMexico. Journal of Parasitology 74:000-000. LEGENDFOR FIGURES OF SYNTYPES.x1600. Bar 10 um. 1. Note striated appearance of oocyst wall. 2. Note tiny Stieda body (arrow) and vacant space below pointed end of sporocyst (also seen in 1 and 3) that is probably a substieda body. 3. Note fragments (arrow) that may be 1 of 3 polar bodies or part of fragmented oocyst residuum. 4. Mammillatedouter wall of oocyst.

FIGURE2. Suggested format for beginning a type specimen tradition among coccidiologists. Proposed data sheet that could be attached to the back of the posterboard with the representative oocysts. This poster, in some standardized size (e.g., 15 x 22.5 cm), could be submitted to accredited national museums for all new species descriptions. BANDONIAND DUSZYNSKI-OOCYSTDESCRIPTIONS AND COCCIDIANTAXONOMY 523 and only when the designation of type specimens LAPAGE,S. P., P. H. A. SNEATH,E. F. LESSEL,V. B. D. is mandatory can the current state of eimeriid SKERMAN,H. P. R. SEELIGER,AND W. A. CLARK 1975. International code of nomenclature Biologists working with the (EDS.). systematics change. of bacteria and statutes of the International Com- Eimeriidae would do well to heed the advice of mittee on Systematic Bacteriology and statutes of Ferris (1928, p. 105): "The proper aim [of tax- the Bacteriology Section of the International As- onomy] is not to name species, but to know sociation of Microbiological Societies. The Amer- them." ican Society for , Washington, D.C., 180 p. LEGER,L., AND 0. DUBOSCQ. 1915. Etude sur Spi- ACKNOWLEDGMENTS rocystes nidula Leg. et Dub. schizogregarinedu Lumbriculusvariegatus Mull. Archiv fur Protis- Discussions with many colleagues helped shape tenkunde 35: 199-211. the ideas presented here and these individuals LEVINE,N. D. 1982. Taxonomy and life cycles of the P. L. also provided much encouragement. In partic- coccidia. In The biology of the coccidia, Long (ed.). University Park Press, Baltimore, pp. 1-42. ular we would like to thank Drs. T. L. Best, D. . 1985. Phylum II. Apicomplexa Levine, 1970. R. Brooks, J. 0. Corliss, S. S. Desser, R. Fayer, In Illustrated guide to the protozoa, J. J. Lee, S. J. R. Lichtenfels, S. J. Mackiewicz, A. A. Mar- H. Hutner, and E. C. Bovee (eds.). Society of Pro- chiondo, and M. A. Pritchard and the helpful tozoologists, Lawrence, Kansas, pp. 322-374. A. AND D. W. DUSZYNSKI.1978. comments of our 5 referees. MARCHIONDO, M., Permanent light microscopy slides of Eimeria nieschulzioocysts. Journal of Parasitology64:163- 164. , AND . 1988. On the status of Eimeria LITERATURECITED nieschulzioocysts embeddedin resin eleven years BLACKWELDER,R. E. 1967. Taxonomy: A text and ago: A permanent method for preserving coccidian referencebook. John Wiley & Sons, New York. oocysts. Journal of Parasitology 74: 740-742. DE Vos, A. J. 1970. Studies on the host range of MAYR,E., E. G. LINSLEY,AND R. L. USINGER. 1953. Eimeriachinchillae De Vos and Van der Westhui- Methods and principles of systematic zoology. zen, 1968. OnderstepoortJournal of Veterinary McGraw-Hill Book Company, Inc., New York. Research37: 29-36. PARKER,B. B., AND D. W. DUSZYNSKI.1986. Poly- DUSZYNSKI,D. W. 1971. Increasein size of Eimeria morphism of eimerian oocysts: A dilemma posed separataoocysts during patency. Journalof Par- by working with some naturally infected hosts. asitology 57: 948-952. Journal of Parasitology 72: 602-604. FERRIS,G. F. 1928. The principlesof systematicento- RIDE, W. D. L., C. W. SABROSKY,G. BERNARDI,AND mology, Vol. V, no. 3. StanfordUniversity Pub- R. V. MELVILLE(eds.). 1985. International code lishers, BiologicalSciences, pp. 101-169. of zoological nomenclature, 3rd. ed. H. Charles- FOURNIE, J. W., W. E. HAWKINS, AND R. M. worth and Co. Ltd., Huddersfield, England, 338 p. OVERSTREET. 1985. Calyptosporaempristica n. VANCE,T. L., AND D. W. DUSZYNSKi. 1985. Cocci- sp. (:Calyptosporidae) from the liver dian parasites (Apicomplexa: Eimeriidae) of Mi- of the starheadtopminnow, Fundulusnotti. Jour- crotus spp. (Rodentia: Arvicolidae) from the United nal of Protozoology32: 542-547. States, Mexico and Japan, with descriptions of five FRIZZELL, D. L. 1933. Terminology of types. The new species. Journal of Parasitology 71: 302-311. AmericanMidland Naturalist 14: 637-668. Voss, E. G., H. M. BURDET,W. G. CHALONER,V. HILL,T. P., AND D. W. DUSZYNSKI.1986. Coccidia DEMOULIN,P. HIEPKO,J. MCNEILL,R. D. MEIKLE, (Apicomplexa:Eimeriidae) from sciurid rodents D. H. NICHOLSON,R. C. ROLLINS,P. C. SILVA,AND (Eutamias, Sciurus, Tamiasciurusspp.) from the N. GREUTER.1983. International code of botan- westernUnited States and northernMexico with ical nomenclature. Bohn, Scheltema & Holkema, descriptionsof two new species. Journalof Pro- Utrecht/Antwerpen, Dr. W. Junk, Publishers, The tozoology 33: 282-288. Hague/Boston. JOYNER,L. P. 1982. Host and site specificity. In The WILLIAMS,R. B. 1986. Hapantotypes: A possible so- biologyof the coccidia,P. L. Long(ed.). University lution to some problems of parasite nomenclature. Park Press, Baltimore,pp. 35-62. ParasitologyToday 2: 314-316.