Cross-Transmission Studies with Eimeria Arizonensis-Like Oocysts

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Cross-Transmission Studies with Eimeria arizonensis-like Oocysts (Apicomplexa) in New World Rodents of the Genera Baiomys, Neotoma, Onychomys, Peromyscus, and Reithrodontomys (Muridae)

Steve J. Upton Kansas State University

Chris T. McAllister Department of Veterans Affairs Medical Cente

Dianne B. Brillhart Kansas State University

Donald W. Duszynski University of New Mexico, [email protected]

Constance D. Wash University of New Mexico

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Upton, Steve J.; McAllister, Chris T.; Brillhart, Dianne B.; Duszynski, Donald W.; and Wash, Constance D., "Cross-Transmission Studies with Eimeria arizonensis-like Oocysts (Apicomplexa) in New World Rodents of the Genera Baiomys, Neotoma, Onychomys, Peromyscus, and Reithrodontomys (Muridae)" (1992). Faculty Publications from the Harold W. Manter Laboratory of Parasitology. 184. https://digitalcommons.unl.edu/parasitologyfacpubs/184

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. Parasitol., 78(3), 1992, p. 406-413 ? American Society of Parasitologists 1992

CROSS-TRANSMISSIONSTUDIES WITH EIMERIAARIZONENSIS-LIKE OOCYSTS (APICOMPLEXA) IN NEWWORLD RODENTS OF THEGENERA BAIOMYS, NEOTOMA, ONYCHOMYS,PEROMYSCUS, AND REITHRODONTOMYS(MURIDAE)

Steve J. Upton, Chris T. McAllister*,Dianne B. Brillhart,Donald W. Duszynskit, and Constance D. Washt Divisionof Biology,Ackert Hall, Kansas State University,Manhattan, Kansas 66506

ABSTRACT: Cross-transmissionexperiments were performedusing oocysts of an Eimeria arizonensis-likecoccidian from Peromyscusleucopus and Peromyscustruei, an E. arizonensis-likecoccidian from Reithrodontomys fulvescens, Eimeria baiomysis and Eimeria taylori from Baiomys taylori, Eimeria albigulae from Neotoma albigula, and Eimeria onychomysisfrom Onychomysspp., between representativesof the above host genera. The E. arizonensis-likecoccidian from R. fulvescens infected Reithrodontomysmegalotis, Reithrodontomys montanus,and Peromyscusleucopus. Oocysts of E. arizonensisfrom P. leucopuscould be transmittedto both P. leucopusand R. megalotus.Oocysts of E. baiomysis and E. taylori infected only B. taylori. Oocysts of E. arizonensisfrom P. trueiinfected P. trueibut not Neotoma mexicana or Onychomysleucogaster. Oocysts of E. albigulaefrom N. albigulawere infective for N. mexicana but not for P. truei or 0. leucogaster.Oocysts of E. onychomysisfrom Onychomysspp. infected 0. leucogasterbut not N. mexicana or P. truei. These results demonstratethat Peromyscusand Reithrodontomys,genera known to be relatedvery closely evolutionarily,are capableof sharingE. arizonensis,whereas morphologically similar coccidians(E. albigulae,E. baiomysis,and E. onychomysis)from more distantly related hosts, are probablydistinct and more stenoxenous.This also is the first reportof coccidiansinfecting species of Reithrodontomys.

Levine et al. (1957) named 10 new species of polar bodies; size, shape, texture of oocyst resid- Eimeria from 52 rodents representing 25 species uum) dependent upon the host in which it is in 8 genera caught on the north rim of the Grand found (Levine et al., 1957; Levine and Ivens, Canyon, Arizona. Three of these, Eimeria albig- 1960, 1963). In addition to morphological dif- ulae, Eimeria arizonensis, and Eimeria onycho- ferences between isolates of E. arizonensis from mysis, along with Eimeria baiomysis Levine, different host species, there are differences also Ivens, and Kruidenier, 1958, are similar or in- in the electromorph banding patterns between distinguishable morphologically, based on the populations of E. arizonensis from different host original descriptions and drawings, even though species (Reduker et al., 1987; Wash et al., 1990). they were found in rodents of several genera Originally described from Peromyscus truei (Levine et al., 1958; Kruidenier et al., 1960). (Shufeldt, 1885), E. arizonensis has been re- These 4 taxa were given separate specific epithets ported since not only to infect rodents of at least in the original descriptions, presumably based 4 other species of Peromyscus but also of Chae- on the traditional concept that rodent coccidia todipus and Dipodomys (Levine et al., 1957; Le- are highly host specific, at least within a given vine and Ivens, 1960, 1963; Ford et al., 1990). host genus. Since the original descriptions, pub- To complicate matters further, most redescrip- lished surveys and experimental studies have tions of E. arizonensis differ enough to suggest clouded the boundaries between these forms. For there may be multiple species confused as 1. Giv- example, E. arizonensis is reported to produce en the morphological similarities with the other oocysts that differ morphologically in several fea- 3 species, doubt can be cast on their validity as tures (oocyst wall smooth to pitted; number of separate species and several questions arise. First, is each form a valid, morphologically similar host- specific species? If not, do these constitute a sin- Received26 August1991; revised 1 November 1991; gle, highly euryxenous species? Or, finally, are accepted 1 November 1991. some of these where- * valid, host-specific species, Renal Metabolic Laboratory(151 -G), Department as others represent more euryxenous forms? The of VeteransAffairs Medical 4500 South Lan- Center, collections and cross-transmission caster Road, Dallas, Texas 75216. experiments t Departmentof Biology,The Universityof New Mex- described here attempt to alleviate some of the ico, Albuquerque,New Mexico 87131. confusion due the eimerians in murid hosts. 406 UPTONET AL.-CROSS-TRANSMISSIONSTUDIES WITH EIMERIA IN RODENTS 407

TABLE I. Wild-caughtmurid rodents from which oocysts of various Eimeria species were isolated to use in cross-transmissionexperiments.

Collection Primary isolate Hosts Locality Date Eimerian isolated number

Reithrodontomys fulvescens Hood Co., Texas April 1988 Eimeria arizonensis- 1 laceyi like Baiomys taylori taylori Dallas Co., Texas January 1990 Eimeria taylori 2 B. t. taylori Dallas Co., Texas March 1988 Eimeria baiomysis 3 B. t. taylori Dallas Co., Texas January 1990 E. baiomysis 4 B. t. taylori Johnson Co., Texas November 1987 E. baiomysis 5 Peromyscus leucopus leucopus Dallas Co., Texas April 1988 E. arizonensis-like 6 Peromyscus truei truei Sandoval Co., New Mexico August 1984 E. arizonensis-like 7 Neotoma albigula albigula Soccoro Co., New Mexico May 1982 Eimeria albigulae 8 Onychomys arenicola (2)* Hidalgo Co., New Mexico July 1981 Eimeria onychomysis 9* Onychomys leucogaster (3)* Motley Co., New Mexico May 1980 E. onychomysis 9* Onychomys torridus (3)* Hidalgo Co., New Mexico May 1983 E. onychomysis 9*

* Oocysts from all 8 animals and 3 host species combined as 1 isolate.

MATERIALS AND METHODS Morphologic comparisons Natural hosts and primary parasite isolates Measurementswere made on oocysts and sporocysts Feces and intestinal contents were collected from of E. arizonensis,E. arizonensis-likeoocysts, and E. wild-caughthosts of 5 genera representing6 species baiomysis using an ocular micrometer.All measure- (TableI). Feces fromhosts wereplaced in separatepetri ments, representingthe mean of 30 under a 100 x oil dishes in a thin layerof 2.5%(w/v) aqueouspotassium lens, are in micrometers(um) followed by the ranges dichromate(K2Cr207) and kept at ambient tempera- in parentheses.For E. arizonensisisolated from P. leu- ture (ca. 21-23 C) for 6-10 days to allow oocysts that copus, the 30 measurementswere taken from 10 oo- werepresent to sporulate.Eimerians isolated from these cysts from isolate 6 and 20 weretaken from isolate 6A. naturally infected hosts were used either directly as For E. arizonensis-likeoocysts, 10 oocysts measured inocula in cross-transmissionexperiments or were in- were from isolate 1 and 20 were from isolate 1A. For oculatedinto conspecificor congenericanimals to in- E. baiomysis, 10 oocysts were measuredfrom isolates creaseoocyst numbers.The resultingpools of oocysts 3, 4, and 5 each. For E. albigulaeand E. onychomysis, were designatedas 15 isolates (1, 1A, 1B, 2, 3, 4, 5, 6, the oocysts in these isolates generally conformed to 6A, 7, 7A, 8, 8A, 9, 9A) (Table II). These oocyst iso- those describedby Levine et al. (1957). lates/fecalsuspensions were stored in refrigerators(4- 6 C) until they were used in experimentalinfections. Experimental inoculations The presumedidentity of each isolate, the host from All animalswere housed in plasticcages with prester- whichit was isolated,the recipienthost speciesto which ilized wood shavingsand given waterand commercial it was transferredexperimentally, the age and number rodent mash ad libitum. They were exposed to 12-hr of oocysts used as inoculum, and the consequenceof light/dark cycles in rooms maintained ca. 20-23 C. each experimentalinoculation are given in Table II. Priorto inoculation,oocysts of an isolate were washed 2-3 x in tap water,counted with a hemacytometer,and Secondary parasite isolates then inoculated per os by stomach tube into experi- Isolate 1A was collected from the feces of 2 adult mental hosts. Feces from inoculated hosts were col- Reithrodontomysmontanus griseus Bailey, 1905, in- lected in 2 ways. For isolates 1 through6A, recipient fected with isolate 1. Isolate 1B was derived from the hosts were maintainedin plastic cages. On the appro- passageof isolate 1A throughReithrodontomys mega- priate days postinoculation (dpi), each animal was lotis (Baird, 1858). Isolate 6A came from laboratory- picked up, which resultedin its defecating,and these rearedPeromyscus leucopus (Rafinesque, 1818) inoc- pellets then were examined for oocysts. For isolates 7 ulatedwith isolate 6. Isolate 7A was collectedfrom the through9A, recipienthosts were placed in wire mesh feces of 5 laboratory-rearedP. truei inoculated with hangingcages and all feces for each host werecollected isolate 7. Isolate 8A was collectedfrom an adult, wild- every 24 hr and examined for oocysts for 20 dpi. caughtNeotoma mexicana Baird, 1855, inoculatedwith Fecal pellets were examined for the presenceof oo- isolate 8; prior to inoculation the rodent was main- cysts using sucroseflotation (specific gravity 1.30) fol- tained in the laboratoryfor several months and was lowed by microscopicexamination using Nomarski in- coccidia-free.Isolate 9A came from the feces of 2 coc- terference-contrastoptics. Oocysts were allowed to cidia-freeOnychomys leucogaster (Wied, 1841), main- sporulate in petri dishes in a thin layer of feces/di- tained in the laboratory,that were inoculatedwith iso- chromate(see above) and reexaminedmicroscopically late 9. Note (Table I) that isolate 9 came from the 6-10 days later to confirm identificationof each coc- combined feces of 8 specimens of Onychomysrepre- cidian. senting 3 species. This was done becauseall 8 original Laboratory-rearedICR outbredMus musculusLin- hosts each had only a very few sporulatedoocysts of naeus, 1758, were purchasedfrom Harlan Sprague- E. onychomysis. Dawley (Indianapolis,Indiana) and were 2-4 mo old 408 THEJOURNAL OF PARASITOLOGY, VOL. 78, NO.3, JUNE1992

TABLE II. Experimental protocol for inoculation of Eimeria specimens into various rodents.

Inoculation Recipient* Age of dose Days post- Oocysts Isolate oocysts (number of inoculation present (+) number Eimeria sp. Donor host* Species Number (days) oocysts) examined or absent (-)

1 E. arizonensis Reithrodontomysfulvescens R. montanus a 2 330 10,000 1-20 + Days 4-14 1A E. arizonensis Reithrodontomys montanus a R. megalotis b 2 300 2,000 5 +, + P. leucopust 2 300 2,000 5 +, + Mus musculus 2 300 2,000 5 1B E. arizonensis Reithrodontomys megalotis b P. leucopus 1 168 2,000 5 + B. taylori 1 168 2,000 5, 7, 9 2 E. taylori Baiomys taylori P. leucopust 2 27 2,000 5, 8 R. megalotis 1 27 2,000 5, 8 P. leucopust 1 167 500 5, 7, 9 B. taylori? 1 167 500 5, 7 , + 3 E. baiomysis B. taylori P. leucopus 1 725 1,500 5, 8 R. megalotis 1 725 1,500 5 4 E. baiomysis B. taylori P. leucopus 1 13 2,000 5, 8 5 E. baiomysis B. taylori P. leucopus. 1 978 2,000 5, 7, 9 , - B. taylori? 1 978 2,000 5, 7 +, + 6 E. arizonensis Peromyscus leucopus P. leucopus c 1 461 400 5, 6 -, +

6A E. arizonensis P. leucopus c P. leucopus 2 461 400 5, 6 +, +, + B. taylori 1 111 2,000 5, 7, 9 R. montanus 1 111 2,000 5,7 +, + 7 E. arizonensis Peromyscus truei P. truei d 5 <180 3,000 1-20 All + Days 4-16 7A E. arizonensis P. truei N. mexicana e 1 <180 3,000 1-20 0. leucogaster f 2 <180 3,000 1-20 -, 8 E. albigulae Neotoma albigula N. mexicana e 1 <180 3,000 1-20 + Days 3-15 8A E. albigulae Neotoma mexicana 0. leucogaster f 2 <180 3,000 1-20 -, - P. trueid 5 <180 3,000 1-20 All - 9 E. onychomysis Onychomys spp. 0. leucogaster f 2 <180 3,000 1-20 +, + Days 2-11 9A E. onychomysis Onychomys leucogaster N. mexicana e 1 <180 3,000 1-20 P. trueid 5 <180 3,000 1-20 All -

* Names followed by same letter indicate the same animals. t Same animals. Inoculated first with isolate 1B and then reinoculated 28 days later with isolate 2. : Same animal. Inoculated with both isolates simultaneously. ? Same animal. Inoculated with both isolates simultaneously.

at the times of inoculation. Peromyscus leucopus were Baiomys taylori (Thomas, 1887) were F, generation all F2 generation and part of a captive breeding colony offspring from animals collected from Dallas County, at Kansas State University. Feces from the cages of Texas. Mice were 5-10 mo old when used as recipient these animals have been checked periodically over the hosts. Each was placed in a separate cage, and feces last 2 yr and no coccidian oocyst has ever been seen. were examined daily for 1 wk to assure the absence of The P. truei recipients were all Fl generation, labora- extraneous infection prior to its inoculation. tory-reared mice derived from the parents from which Uninfected control animals could not be used for all isolate 7 was obtained. These mice had been checked inoculation experiments because of the difficulty in numerous times before inoculation to assure they were obtaining some animals. However, pairs of uninfected coccidia-free. P. leucopus, housed separately from experimental hosts, To obtain large numbers of isolate 1, 2 adult R. were used as controls for experimental inoculations montanus griseus were collected from Dallas County, with isolates 1A, lB, 2 (167 days), 5, 6, and 6A. An Texas. Feces of both animals were checked daily for individually housed R. megalotis collected in Kansas 14 days prior to inoculation with oocysts of isolate 1. also was used as a control during inoculation of isolate Following inoculation of these 2 mice, feces were 1A. One B. taylori, a littermate of the other pygmy checked daily for unsporulated oocysts to determine mouse used, served as control for inoculations with prepatent and patent periods. Other specimens of isolates 2 (167 days) and 5. For controls, feces were Reithrodontomys used for inoculations were adults col- examined, as above, on the same day(s) that experi- lected from Osborne and Pottawatomie counties, Kan- mentally infected hosts were examined. sas. These mice were placed in individual cages and Voucher specimens of rodents are deposited in either their feces examined for oocysts at 1, 4, and 11 days the Arkansas State University Museum of Zoology, the postcapture. Inoculations using Kansas mice were at Texas Tech University Museum, or in the University 11 days postcapture. of New Mexico Museum of Southwestern Biology. UPTON ET AL.-CROSS-TRANSMISSIONSTUDIES WITH EIMERIA IN RODENTS 409

TABLE III. Measurementsof oocyst featuresof Eimeria species collected from Peromyscusleucopus, species of Reithrodontomys,and Baiomys taylori.*

Oocyst source Parameter Baiomys taylori Peromyscus leucopus Reithrodontomys spp.

Oocyst size 24.3 x 20.0 24.3 x 19.8 24.1 x 20.2 (20-30 x 17-24) (21-27 x 17-22) (20-30 x 17-26) Oocyst SIt 1.2 1.2 1.2 (1.1-1.3) (1.1-1.4) (1.1-1.5) Oocyst residuum (OR) diameter 7.0 8.3 8.2 (6-9) (7-10) (4-12) Number OR globules 1-10 1-50 1-30 Oocyst outer walls Light-moderate pitting Smooth-moderate pitting Smooth-moderate pitting Polar granulef 2.0 2.1 2.3 (1-3) (2-3) (2-3) Sporocyst size 11.9 x 8.2 11.4 x 7.8 11.4 x 7.9 (10-14 x 7-9) (11-13 x 7-9) (10-14 x 7-9) Sporocyst SIt 1.45 1.5 1.5 (1.3-1.6) (1.3-1.6) (1.3-1.55) Stieda body size 1.6 x 2.8 1.6 x 2.4 1.5 x 2.6 (height x width) (1-2 x 2-4) (1-2 x 2-3) (1-2 x 2-3) Sporozoite size? 15.8 x 3.4 14.0 x 3.2 14.6 x 3.2 (14-18 x 3-4) (11-17 x 3-4) (13-18 x 3-3.4) Refractile body size 5.5 x 3.0 6.3 x 3.2 5.9 x 3.1 (5-6 x 2.8-3.2) (5-8 x 2-4) (5-7 x 3-4)

* Measurements are means in micrometers (n = 30) with ranges in parentheses. t SI, shape index (length/width). t Long axis measurement. ? Size in situ.

RESULTS coccidian, Eimeria taylori McAllister and Up- Oocysts we isolated from hosts of 5 genera, ton, 1988, to infect P. leucopus as well as B. Baiomys, Neotoma, Onychomys, Peromyscus, taylori. However, it too was not infective for P. and Reithrodontomys, were morphologically leucopus or R. megalotis. Isolate 6, E. arizonensis similar to those of E. arizonensis, described orig- from P. leucopus, was infective for 2 P. leucopus inally from species of Peromyscus. Detailed and for 1 R. megalotis but not for B. taylori. structural comparisons were made among 3 of Isolate 7, E. arizonensis from P. truei, was in- our isolates from 3 closely related hosts (Table fective for P. truei but not for N. mexicana or 0. Isolate E. from Ne- III), and photomicrographs of isolates from each leucogaster. 8, albigulae genus can be compared in Figures 1-15. otoma albigula Hartley, 1894, was infective for N. Sporocysts were lemon-shaped, with globular mexicana but not for 0. leucogaster or P. oocyst residua (either homogeneous or frag- truei. Isolate 9, E. onychomysis combined from 8 3 of mented), and usually 1 (but up to 4) polar gran- specimens representing species Onycho- ule(s) was present. Stieda bodies were promi- mys, was infective for 0. leucogaster but not for N. nent, sub- and parastieda bodies absent, and mexicana or P. truei. sporozoites each possessed a large, posterior re- DISCUSSION fractile body, but no anterior body. The only notable difference was that the Stieda body as- Dogma dictates that eimerians are highly host sociated with sporocysts ofE. baiomysis was more specific, being limited naturally to a narrow range flattened than those on sporocysts from speci- of host species, usually congenerics or, less fre- mens of Peromyscus, Neotoma, or Reithrodon- quently, only to conspecifics (Marquardt, 1973; tomys (cf. Figs. 1, 4, 10 vs. 9). Joyner, 1982). However, during the last 2 de- Isolate 1, from Reithrodontomys fulvescens J. cades, there have been both cross-transmission A. Allen, 1894, was transmissible to R. mega- studies (Todd and Hammond, 1968a, 1968b; de lotis, R. montanus griseus, and P. leucopus but Vos, 1970; Mayberry and Marquardt, 1973; not to M. musculus or B. taylori. Isolate 3, E. Mayberry et al., 1982) and observations from baiomysis, readily infected B. taylori but not P. wild-caught rodents (Vance and Duszynski, 1985; leucopus or R. megalotis. McAllister and Upton Hill and Duszynski, 1986; McAllister and Up- (1988) reported a morphologically dissimilar ton, 1988; Ford et al., 1990) that suggest some 410 THEJOURNAL OF PARASITOLOGY,VOL. 78, NO. 3, JUNE 1992

FIGURES1-9. Nomarski-interferencecontrast photomicrographsof sporulatedoocysts of various Eimeria species from rodents. 1-3. Eimeria arizonensis from Peromyscus leucopus. 4-6. Eimeria arizonensis from Reithro- dontomys fulvescens. 7-9. Eimeria baiomysis from Baiomys taylori. Scale bar = 10 Am for all figures. Abbre- viations: or, oocyst residuum; pg, polar granule; sb, Stieda body; sr, sporocyst residuum.

rodent coccidians are more general in their host some species seem to exhibit a great deal of phe- requirements and may be able to infect animals notypic plasticity in the structure of their spor- in several genera or even in different families. ulated oocysts, not only among and within host When working with coccidians from wild an- species, but also in oocysts from the same host imals, the problem of correctly identifying the (e.g., Parker and Duszynski, 1986; Gardner and coccidians found is compounded by the fact that Duszynski, 1990). A similar situation occurs in UPTON ET AL.-CROSS-TRANSMISSIONSTUDIES WITH EIMERIA IN RODENTS 411

FIGURES10-15. Nomarski-interference contrast photomicrographs of sporulated oocysts of various Eimeria species from rodents. 10-12. Eimeria albigulae from Neotoma albigula. 13-15. Eimeria onychomysis from Onychomys leucogaster. Scale bar = 10 ,m for all figures. Abbreviations: or, oocyst residuum; pg, polar granule; sb, Stieda body.

1 of the most ubiquitous coccidians found in Mexico, found E. arizonensis-like oocysts in 41 murid rodents, E. arizonensis. Oocysts of this of 102 (40%) specimens of Peromyscus (Pero- form were said to be "composed of a single myscus eremicus (Baird, 1858), Peromyscus smooth layer, lined by a thin membrane"; they maniculatus (Wagner, 1845), P. truei) and pro- also usually had "a single large, clear, colorless vided a "combined" redescription based on mea- residual globule, about 3.6 ,um in diameter" surements/observations of nearly 500 sporulated (Levine et al., 1957). Later, Levine and Ivens oocysts. These observations lead to the conclu- (1960) reported E. arizonensis from species of sion that E. arizonensis is not exceptionally spe- Peromyscus in Illinois. In P. maniculatus the oo- cies specific and that it is a highly polymorphic cyst wall was described as "slightly to moderately form similar to Eimeria opimi described from pitted" and the oocyst residuum as a "cluster of South American fossorial rodents (Gardner and large, homogeneous granules/globules"; whereas Duszynski, 1990). This may be true, but the pos- in P. leucopus in Illinois, the oocysts had walls sibility also exists that the variation seen in spor- that were "sometimes smooth, but usually more ulated oocysts of E. arizonensis actually repre- or less pitted" with oocyst residua of "a single sents several isolates of 1 species or several species large, waxy-appearing globule about 4." Reduker that are morphologically similar. et al. (1985), surveying species of Peromyscus Finally, to further complicate an answer to the from the southwestern U.S.A. and northern question, "What is the real E. arizonensis?" sev- 412 THEJOURNAL OF PARASITOLOGY,VOL. 78, NO. 3, JUNE 1992 eral species of coccidia described from murid to be infective for 0. leucogaster.We are aware, rodents are reportedto have sporulatedoocysts however, that other factors (e.g., unknown im- that are nearlyidentical to those of E. arizonen- mune status of our recipients) may have influ- sis; among these are E. albigulae from N. albigu- enced the negative results we saw, and that just la, E. baiomysis from B. taylori, and E. onycho- because a few recipienthosts do not become in- mysis from 0. leucogaster.Unfortunately, the fected does not necessarilymean that under nat- descriptions of these forms are inadequate by uralconditions, wheremillions of randomcross- today's standardsand only line drawingsexist in transmissionevents take placebetween hosts that the originaldescriptions; there is no originalpub- occupy similar space and time, that such suc- lished photographor phototype on deposit with cessful host transferscould not occur. any accredited national museum (see Bandoni Oocysts of E. baiomysis, although also mor- and Duszynski, 1988), so that oocysts repre- phologically similar to those of E. arizonensis, senting the original forms seen cannot be com- have Stieda bodies that are slightly more flat- pared directly. tened (cf. Figs. 1-6 vs. Figs. 7-9). Our transmis- In an attempt to help unravel the mystery of sion experimentsfurther suggest that the 2 are E. arizonensis,we did some initial cross-trans- distinct species. In addition, the transmission mission studies using E. arizonensis-likeoocysts studiesbetween specimens of Baiomysand Pero- from various hosts and passed them to other myscussuggest that the reportof E. tayloriin P. hosts. Ourresults must be interpretedcautiously, leucopuswas a misidentification(McAllister and given the shortcomingsof the experimentalde- Upton, 1988). It appearslikely that these oocysts sign. These resultssuggest the following:Eimeria in P. leucopuswere those of Eimeria langebarteli arizonensis-likeoocysts are capable of infecting Ivens, Kruidenier,and Levine, 1959. Thus, even a broad rangeof hosts in at least 2 genera,Pero- though B. taylori is considered a close relative myscus and Reithrodontomys.Although these of P. leucopus,our resultsare consistentwith the data are in contrastto the traditionalconcept of genetic analysis by Yates et al. (1979) that sug- species or genus specificityamong the coccidia, gests both generaare less closely relatedthan are it is not surprisinggiven that these genera are Reithrodontomysand Peromyscus. closely relatedevolutionarily (Hooper and Mus- ser, 1964; Carlton, 1980). On the other hand, ACKNOWLEDGMENTS oocysts of E. albigulae, E. baiomysis, and E. Collectionsin Kansas were under 88- onychomysis,all structurallysimilar to E. ari- permits and SC-046-90 from the Kan- zonensis, appear to be separatespecies, at least 122, SC-055-89, sas of Parks and Wildlife to basedon the limited numberof recipientanimals Department S.J.U. we used and the fact that some of them had to C.T.M. thanks the Texas Parks and Wildlife PermitSPR- be reinoculatedwith different forms/species at Departmentfor ScientificCollecting of Creekand Rus- differenttimes during their captivity. These re- 0390-027, personnel Georges sell ranchesfor on their sults also suggestthat E. arizonensis-likeoocysts allowingcollecting prop- and T. for assistance reportedby Ford et al. (1990) from heteromyids erties, J. McAllister, III, with This also was sup- of the genera Chaetodipus and Dipodomys are collecting. study partly NIH-DHHS 5 RR-08139- most likely not E. arizonensis. In addition, we portedby grant S06, 07 to the of New Mexico W. Du- speculatethat should E. arizonensis-likeoocysts University (D. and T. L. be recoveredfrom golden mice, Ochrotomysnut- szynski Yates). talli (Harlan, 1832), they most likely will rep- resentthe same parasitespecies found in species LITERATURECITED of Peromyscus and Reithrodontomys. Golden BANDONI, S. M., ANDD. W. DUSZYNSKI.1988. A plea mice are consideredthe closest living relative to for improved presentatiion of type material for An of (Carlton, 1980). coccidia. invited critical comment. Journal Peromyscusspecies Parasitology 74: 519-523. Although the oocysts of E. albigulae (see Re- CARLTON, M. D. 1980. Phylogenetic relationships in duker and Duszynski, 1985: figs. 1, 2) and E. neotomine-peromyscine rodents (Muroidea) and arizonensis from species of Peromyscus and a reappraisal of the dichotomy within New World Reithrodontomys(Figs. 1-6) are indistinguish- Cricetinae. Miscellaneous Publications of the Mu- seum of Zoology, University of Michigan 157: 1- able, our modest cross-transmissionexperiments 146. suggest they are host-specific forms. Also, oo- DE Vos, A. J. 1970. Studies on the host range of cysts we isolated from 0. leucogasterappear only Eimeria chinchillaede Vos and Van der Westhui- UPTONET AL.-CROSS-TRANSMISSIONSTUDIES WITH EIMERIA IN RODENTS 413

zen, 1968. OnderstepoortJournal of Veterinary , D. J. NASH, ANDB. PLAN. 1982. Ge- Research37: 29-36. netic dependenttransmission on Eimeriaseparata FORD,P. L., D. W. DUSZYNSKI,AND C. T. MCALLISTER. from Rattus to three strains of Mus musculus,an 1990. Coccidia (Apicomplexa)from heteromyid abnormalhost. Journalof Parasitology68: 1124- rodents in the southwesternUnited States, Baja 1126. California,and northernMexico with three new MCALLISTER,C. T., ANDS. J. UPTON. 1988. Eimeria speciesfrom Chaetodipushispidus. Journal of Par- taylori n. sp. (Apicomplexa:Eimeriidae) and E. asitology 76: 325-331. baiomysis from the northern pygmy mouse, Baio- GARDNER,S. L., ANDD. W. DUSZYNSKI.1990. Poly- mys taylori (Rodentia: Cricetidae),from Texas, morphism of eimerian oocysts can be a problem U.S.A. Transactions of the American Microscop- in naturallyinfected hosts: An example from sub- ical Society 107: 296-300. terraneanrodents in Bolivia. Journal of Parasi- PARKER,B. B., AND D. W. DUSZYNSKI.1986. Poly- tology 76: 805-811. morphismof eimerianoocysts: A dilemma posed HILL, T. P., AND D. W. DUSZYNSKI.1986. Coccidia by working with some naturally infected hosts. (Apicomplexa:Eimeriidae) from sciurid rodents Journalof Parasitology72: 602-604. (Eutamias, Sciurus, Tamiasciurusspp.) from the REDUKER,D. W., AND D. W. DUSZYNSKI.1985. Ei- westernUnited States and northernMexico with meria ladronensisn. sp. and E. albigulae (Api- descriptionsof two new species. Journal of Pro- complexa:Eimeriidae) from the woodrat, Neoto- tozoology 33: 282-288. ma albigula (Rodentia: Cricetidae). Journal of HOOPER, E. T., AND G. G. MUSSER. 1964. The glans Protozoology32: 548-550. penis in neotropical cricetines (family Muridae) , ANDT. L. YATES. 1987. Evolutionary with comments on classification of muroid ro- relationships among Eimeria spp. (Apicomplexa) dents. MiscellaneousPublications of the Museum infectingcricetid rodents. Canadian Journal of Zo- of Zoology, University of Michigan123: 1-57. ology 65: 722-735. JOYNER L. P. 1982. Host and site specificity.In The , L. A. HERTEL,AND D. W. DUSZYNSKI.1985. biologyofthe coccidia,P. L. Long(ed.). University Eimeria spp. (Apicomplexa: Eimeriidae) infecting Park Press, Baltimore,Maryland, p. 35-62. Peromyscusrodents in the southwesternUnited KRUIDENIER,F. J., N. D. LEVINE,AND V. IVENS. 1960. States and northern Mexico with descriptions of Eimeria (Protozoa:Eimeriidae) from the rice rat two new species. Journal of Parasitology 71: 604- and pygmy mouse in Mexico. Transactions of the 613. Illinois Academy of Sciences 52: 100-101. TODD,K. S., JR., ANDD. M. HAMMOND.1968a. Life LEVINE,N. D., AND V. IVENS. 1960. Eimeria and cycle and host specificity of Eimeria callosper- Tyzzeria (Protozoa: Eimeriidae) from deermice mophiliHenry, 1932 from the Uinta groundsquir- (Peromyscusspp.) in Illinois. Journal of Parasi- rel Spermophilusarmatus. Journalof Protozool- tology 46: 207-212. ogy 15: 1-8. , AND . 1963. Eimeria siniffi sp. n. and , AND . 1968b. Life cycle and host spec- E. arizonensis (Protozoa: Eimeriidae) from ificity of Eimeria larimerensisVetterling, 1964, deermice in British Columbia. Journalof Parasi- from the Uinta groundsquirrel Spermophilus ar- tology 49: 660-661. matus. Journalof Protozoology15: 268-275. , AND F. J. KRUIDENIER.1957. New VANCE, T. L., AND D. W. DUSZYNSKI.1985. Coccidi- species of Eimeria from Arizona rodents. Journal an parasites(Apicomplexa: Eimeriidae) of Micro- of Protozoology4: 80-88. tus spp. (Rodentia:Arvicolidae) from the United , AND . 1958. New species of States, Mexico, and Japan with descriptions of five Eimeria (Protozoa:Eimeriidae) from Mexicanro- new species. Journal of Parasitology 71: 302-311. dents. Transactionsof the Illinois Academyof Sci- WASH, C. D., D. W. DUSZYNSKI,AND T. L. YATES. ences 50: 291-298. 1990. Enzyme variation of Eimeria arizonensis MARQUARDT, W. C. 1973. Host and site specificity. from Peromyscustruei and P. boylii. Journal of In The coccidia, D. M. Hammond and P. L. Long Protozoology 37: 536-540. (eds.). University Park Press, Baltimore, Mary- YATES, T. L., R. J. BAKER, AND R. K. BARNETT.1979. land, p. 23-43. Phylogenetic analysis of karyotypic variation in MAYBERRY,L. F., AND W. C. MARQUARDT. 1973. three genera of peromyscine rodents. Systematic Transmission of Eimeria separata from the nor- Zoology 28: 40-48. mal host, Rattus, to the mouse, Mus musculus. Journalof Parasitology59: 198-199.