Studies on the Parasitic Helminths of the North Central States. II

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Faculty Publications from the Harold W. Manter Laboratory of Parasitology Parasitology, Harold W. Manter Laboratory of

1949

Studies on the Parasitic Helminths of the North Central States. II. Helminths of Voles (Microtus spp.) Preliminary Report

Robert L. Rausch University of Washington, [email protected]

Jack Tiner University of Wisconsin, Madison

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Rausch, Robert L. and Tiner, Jack, "Studies on the Parasitic Helminths of the North Central States. II. Helminths of Voles (Microtus spp.) Preliminary Report" (1949). Faculty Publications from the Harold W. Manter Laboratory of Parasitology. 569. https://digitalcommons.unl.edu/parasitologyfacpubs/569

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. Rausch & Tiner in American Midland Naturalist (May 1949) v. 41, no. 3. Copyright 1949, University of Notre Dame. Used by permission.

Studieson theParasitic Helminths of the North CentralStates. 11.Helminths of Voles (Microtusspp.) PreliminaryReport

RobertRausch and JackD. Tiner* Departmentof VeterinaryScience, University of Wisconsin,Madison*

The helminthsof NorthAmerican mouse-like rodents have received little study. Previouswork has beenbased on low numbersof animalsexamined, and therehas beenlittle reference to theecology involved. The purposeof thispaper is to presentdata resulting from the examination of over600 voles, withspecial reference to host-parasiterelationships. Hall (1916) reviewedthe nematodesparasitic in rodents,and previous recordsof helminthsfrom voles are containedin the papersof Harkema (1936) and Erickson(1938). In additionto these,a numberof newspecies has beendescribed. No efforthas beenmade here to listall helminthspre- viouslyrecorded from voles, and onlythose of interestin connectionwith the presentwork are mentioned. Rodentsof thegenus Microtus are of mucheconomic importance in connectionwith agriculture, and for thisreason have been givenconsiderable attention.The fluctuationsof vole populations have long been observed, and a considerableamount of efforthas beenspent in attemptsto explaintheir populationbehavior. The bionomicsof voleshas beeninvestigated both in NorthAmerica and in Eurasia. The workof Hamilton(1937, 1941) in the easternUnited States has beenespecially complete, as has thatof Eltonand his co-workersin Europe. Much workon the ecologyof rodentshas been donein Russia,some of whichhas beenreviewed by Kalabukhov (1935), and by Elton (1942). Unfortunately,the Russian work has not beengenerally available. Voles lendthemselves especially well to studiesconcerned with population fluctuations,since the rise and fallof theirnumbers seems to occurwithin a spanof threeor fouryears, in contrastto thatof certainother species (snowshoehare, ruffed grouse, and others),which have a cycleof about10 years. In spiteof theiravailability in considerablenumbers, wide geographical distribution,and interestingpopulation behavior, very little has been done in the way of host-parasitestudies with voles. The workof Kirschenblatt (1938), concerningMicrotus socialis satunini Ogn., M. socialisschidlovskyi Arg., and M. arvalistranscaucasicus St., as well as otherrodents in the

* Now at Departmentof Zoology and Physiology,University of Illinois,Urbana, Illinois. ** Sectionon Parasitology.This worksupported in part by the ResearchCommittee of the GraduateSchool fromfunds supplied by the WisconsinAlumni Research Foun- dation. 665 Rausch & Tiner in American Midland Naturalist (May 1949) v. 41, no. 3. Copyright 1949, University of Notre Dame. Used by permission.

666 THE AMERICAN MIDLAND NATURALIST 41 (3)

Transcaucasusregion, is of especialinterest. We wereable to obtainthis paperonly in late 1947,through the kindnessof Dr. CharlesElton, as it doesnot appear to be availablein NorthAmerica. An efforthas beenmade to includethe points in Kirschenblatt'swork which are of interestin connectionwith the present paper. Accordingto Dr. H. A. Baylis(personal com- munication),voles in the BritishIsles havenot beenfound parasitized by helminthsto a degreeadequate to allowa profitablestudy of thistype. Elton and his associates(1931) carriedout such a studywith the woodmouse, Apodemussylvaticus L., a formin some wayscomparable to the North AmericanPeromyscus.

METHODS AND SOURCES OF MATERIAL The procedurefor collecting helminths was the sameas thatused in a previousstudy (Rausch and Tiner,1948). Afterthe voleswere weighed, theviscera were removed, and each organwas openedseparately in a clean dish of water. The contentsof each viscuswere examined under the low powerof the dissectingmicroscope, after any macroscopic forms present had beenremoved. It shouldbe notedhere that all theanimals examined were in a freshcondition; in the opinionof the writers,carcasses preserved in formalindo not give satisfactoryresults, although the use of preservatives maybe necessaryunder some circumstances. After their isolation, the hel- minthswere fixed in formalin-aceticacid-alcohol solution, and handledin the usualmanner. Voles wereordinarily captured by meansof snapmouse traps, set directly in therunways. Baited traps were rarely used. The collectingwas doneentirely by thesenior author from 1942 to 1945. From1945 to 1948,assistance was givenby thejunior author, and by other personsas notedin the acknowledgment.Some of the latter,particularly Messrs.L. H. and C. F. Troesch,have lent their assistance on occasionsince the inceptionof thisstudy. The Wisconsincollecting, in connectionwith thisstudy, was done by the senior author. The presentstudy is concernedmainly with a generalsurvey of the helminthsparasitic in voles,and withmore intensive work carried out locally in twoareas. For the surveywork, voles wereobtained from wherever possible, and specimenswere secured from the states of Ohio, Indiana,Illinois, Michigan, and Wisconsin.The numberof animalsfrom Indiana and Illinois,however, wasrelatively small. A fewvoles were examined from Manitoba, in addition to thosefrom the North Central States region. Whilethe Manitoba speci- mensdo notcome under the scope of thisstudy, helminth records from them are includedin orderto giveall possibleinformation, on distribution. A. totalof 648 voleshas beenexamined. Of these,570 wereMicrotus p. pennsylvanicusOrd; 46 wereM. ochrogasterWagner; and 32 wereM. penn- sylvanicusdrummondii (Audubon and Bachman). The localitiesin theNorth Central States region from which voles have Rausch & Tiner in American Midland Naturalist (May 1949) v. 41, no. 3. Copyright 1949, University of Notre Dame. Used by permission.

1949 RAUSCH ET AL.: HELMINTHS OF VOLES 667 beenobtained are shown in Figure1, accordingto countyin whichthey were found. Thesecounties, as numberedon themap, are as follows:

WISCONSIN 9. Hancock 17. Ingham 1. Vilas 10. Mason 18. Washtenaw 2. Fond du Lac 11. Piatt OHIO 3. Sheboygan 12. Champaign 19. Preble 4. Dodge 13. Vermilion 20. Franklin 5. Dane 14. Saline 21. Union 6. Waukesha INDIANA 22. Marion 7. Milwaukee 15. Tippecanoe 23. Morrow ILLINOIS MICHIGAN 24. Lorain 8. Cook 16. Cheboygan 25. Geauga Of thetwo local intensive studies, one wascarried out in InghamCounty, in southernMichigan (Figure 1, county17). A fairlyuniform field of about23 acres,adjoining, on thewest side, an extensivewoodlot, was used.

4 4~~~~~~~~2

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Fig. 1.-Map of the NorthCentral States region,showing counties from which voles weie collected. Rausch & Tiner in American Midland Naturalist (May 1949) v. 41, no. 3. Copyright 1949, University of Notre Dame. Used by permission.

668 THE AMERICAN MIDLAND NATURALIST 41 (3)

An openwoodlot about 50 yardswide ran across the south side of thefield, whilethe othertwo sides bordered cultivated fields. The vegetationof the area consistedof blue grass,Poa sp., withseveral species of annualsinter- spersed. Hawthornebushes, Crataegus sp., weredistributed throughout, as weresmall areas of pricklyash, Zanthoxylum americanus L., and Vibernum sp. Certainmoist areas supported heavy growths of Carexsp., whichalso appearedto be good vole habitat,especially during the winter.As faras could be determined,the vole populationwas uniformover the area when thestudy was begun. The fieldwas grazedby cattleduring the late spring and summer. The largerwoodlot, adjoining the west side of thefield, contained about 69 acres,and was of beech-hardmaple type. Severalareas within it were quitelow, and supportedheavy growths of Cephalanthusoccidentalis L. and Typhalatifolia L., amonga varietyof plants. Sincethis woodlot had been ungrazedfor a numberof years,and sinceconditions in generalwere favorable, severalspecies of mammalswere abundant. No mammalshad been removedby huntingor trappingfor a periodof yearspreceding this study. As willbe explainedfurther below, the helminthsof themammals resident in thiswoodlot were rather intensively studied, along with those of thevoles fromthe nearby field. The voleswere trapped from different parts of thearea in an effortto distributethe populationlosses due to trappingevenly over the wholearea, therebyminimizing the effort upon vole densities, and, in turn, upon the results obtained.It was theplan to trap30 voleseach month, as welldistributed overthis period as possible. A totalof 345 voleswas obtainedfrom the field,over a periodof 13 months.Figure 2 showsthe age compositionof theseanimals, according to percentageof thetotal in eachweight group. Observationson thehelminths of thisarea were begun in July,1945, and werecarried on throughJuly, 1946. The volesapproached and passeda peak in populationdensity during the time of thestudy, with the decline occurring 0. 0o 30 cc w 0 1 o 20

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0 5-10 11-15 16-20 21-25 26-30 31-35 36-40 41-45 46-50 51-60 BODY WEIGHT IN GRAMS Fig. 2.-Age compositionof the 345 voles collectedon the southernMichigan study area. Rausch & Tiner in American Midland Naturalist (May 1949) v. 41, no. 3. Copyright 1949, University of Notre Dame. Used by permission.

1949 RAUSCH ET AL.: HELMINTHS OF VOLES 669

aboutMay, 1946. Observationsof otherssustained this conclusion. Accord- ingto Dr. D. W. Hayne (personalcommunication), this population peak was unusuallyhigh -the highestsince the year 1937. Whileno absolutecensus figurefor the area was obtained,it was obviousthat the voles were at first verynumerous, as attestedby well-wornrunways, abundant, fresh cuttings, and fecaldeposits. Also, thevoles could often be seenin placeswhere the vegetationwas not too abundant.The highpopulation level persisted through thewinter of 1946,but a precipitousdecline was noted in thespring, as mentionedabove. Fromthe time of thedecline on, specimens were obtained only withmuch difficulty. The contrastduring the late spring of 1946to conditionsof theprevious yearwas indeedgreat. Runwayshad becomepoorly defined from disuse, and cuttingsand feceswere not to be seen. This populationdecline took place early,before prolonged dry weather could have reduced breeding activity. No evidenceas to the cause of the declinewas obtained.In May, 1947,we againtrapped in thisstudy area, and it was evidentthat the vole population wasstill low. Sinceno trappinghad been done there during the previous year, thepopulation was undisturbed during this period. The ecologyof thehelminths of voles,or of any othergiven host, will neverbe adequatelyunderstood if theparticular host in questionis theonly one examinedfrom areas under investigation. It is probablysafe to assume thata mammalresident in a givenarea must suffer a degreeof exposureto helminthspecies which infect it rarelyor not at all. Much can be learned of theinterrelationships involved when it is knownjust which host species and whichparasites are present in a givenarea. We have,therefore, attempted to samplethe totalparasitic helminth fauna of areasstudied, whenever it was possibleto do so. To datethis holds true for areas in Ohio,Michigan, and Wisconsin;there was littleopportunity to studyother than voles from the areasin Illinoisand Indiana. Of the manybirds and mammalsexamined duringthe course of thesestudies, most will be consideredin futurereports. However,additional information is given here for two areas where intensive studieswere carried out. Fromthe Michigan study area (Figure1, countyNo. 17), thefollowing residentmammals were examined: opossum, Didelphis v. virginianusKerr; short-tailedshrew, Blarina brevicauda kirtlandi Bole and Moulthrop;raccoon, Procyon1. lotorLinnaeus; long-tailed weasel, Mustela frenata noveboracensis Emmons;skunk, Mephitis mephitis nigra Peale and Beauvois;house cat, Felis domesticusLinnaeus; woodchuck, Marmota m. monaxLinnaeus; chip- munk,Tamias striatusrufescens Bole and Moulthrop;red squirrel,Tamia- sciurushudsonicus loquax Bangs; fox squirrel, Sciurus niger rufiventer Geof- froy;eastern flying squirrel, Glaucolmys v. volans Linnaeus; prairie white-footed mouse,Peromyscus maniculatus bairdii Hoy and Kennicott;northern white- footedmouse, P. leucopusnoveboracensis Fischer; meadow vole, Microtus p. pennsylvanicusOrd; pinevole, Pitymys pinetorum scalopsoides Audubon and Bachman;house rat, Rattus norvegicus Berkenhout; house mouse, Mus mus- culusLinnaeus; jumping mouse,Zapus hudsonius breviceps Bole and Moul- Rausch & Tiner in American Midland Naturalist (May 1949) v. 41, no. 3. Copyright 1949, University of Notre Dame. Used by permission.

670 THE AMERICAN MIDLAND NATURALIST 41 (3) throp;cottontail, Sylvilagus floridanus mearnsii Allen. The hostnames for theMichigan mammals are according to Burt(1946). Host-parasiterelationships as observedon the Michiganstudy area are shownin Figure3 (partsA, B, and C). Cestodes,trematodes, and nema- todesrespectively are tabulatedso as to showthe hostspecies infected by each parasite,and theirrelative abundance in thesehosts. Only resident mammalstrapped in thefield or woodlotare considered.It,can be expected, in thecase of thisstudy area, that the voles were only rarely exposed to hel- minthsinfecting some of themammals living in thewoodlot. However, some of the woodlotinhabitants tended to rangeoutward into the surrounding fields. Only twomeadow voles were collected well inside the woodlot, and neitherwas infectedwith helminths. Only a fewmammals were regularly takenin thefield, along with the voles; they were jumping mouse, short-tailed shrew,prairie white-footed mouse, and housemouse. For the intensivestudy area in Wisconsin,a largemarsh of about350 acreswas chosen (Figure 1, countyNo. 5). Thismarsh was a ratheruniform bioticcommunity, isolated to a considerabledegree by the surrounding higher, heavilycultivated agricultural land. A spring-fedcreek flowed through the area,and thiswas further fed by springs arising within the marsh itself. The surfaceof thesmaller creeks bore dense growths of watercress, Radicula sp. The marshvegetation consisted to a largeextent of Phragmitescommunis (Reed), Typhalatifolia L., and Carexspp., interspersed with some Aster spp., Solidagospp., and otherplants. The creekbanks were grown to willow, Salix sp.,while other higher areas supported elderberry, Sambucus canadensis L., giantragweed, Ambrosia trifida L., and nettle,Urtica gracilis Ait. This areawas relativelyundisturbed by man, since no huntingor trapping had beendone for some years, and it was notused for any agricultural pur- pose; consequently,mammals were abundant here. This area in someways was moreinteresting than the Michigan area, since the voles occurred within the marshitself, and theircontact with the other mammals must have been moreimmediate. Althoughmammals were numerous in the marsh,the numberof species herewas smaller,limited in thisrespect by themuch more uniform habitat. The followingmammals, resident within the marsh, were examined: opossum, Didelphisv. virginianusKerr; short-tailed shrew, Blarina b. brevicauda(Say); commonshrew, Sorex c. cinereusKerr; raccoon, Procyon 1. lotorLinnaeus; least weasel,Mustela rixosa allegheniensis (Rhoads); mink,mustela vison letiferaHollister; skunk, Mephitis mephitis avia Bangs;house cat, Felis do- mesticusLinnaeus; woodchuck, Marmota monax Linnaeus ssp.; prairie white- footedmouse, Peromyscus maniculatus bairdii Hoy and Kennicott;meadow vole,Microtus p. pennsylvanicusOrd; muskrat,Ondatra z. zibethicaLinnaeus; house mouse,Mus musculusLinnaeus; cottontail,Sylvilagus floridanus mearnsiiAllen. In additionto theabove, the short-tailed weasel, Mustela c. cicognaniiBonaparte, was also residenthere, but none of thesewas collected. The sub-specificstatus of someof the Wisconsinmammals is not entirely clearat present. Rausch & Tiner in American Midland Naturalist (May 1949) v. 41, no. 3. Copyright 1949, University of Notre Dame. Used by permission.

1949 RAUSCH ET AL.: HELMINTHS OF VOLES 671

The host-parasiterelationships of thismarsh were particularly interesting, to a largedegree because of thecloser contacts of themammals with one another,as mentionedabove. Figure4 (partsA, B, and C) presentsa gen- eralpicture of theseinterrelationships. A single house mouse, infected with Aspiculurissp., was collected after Figure 4 wasprepared. Of themammals present in thisarea, only the muskrat was ratherclosely relatedto thevole (i.e. bothof thesubfamily Microtinae). If therewere any sharingof the helminthparasites by the differenthost species, one might expectthis to occurbetween the two microtine rodents, while parasite faunas wouldbe sharedto a muchlesser degree by more distantly related hosts. The resultsof ourexaminations indicated that weaknesses in hostspecificity barriers werenot necessarilyrelated to theamount of phylogeneticseparation of the hosts. Thus, we foundTrichuris opaca Barkerand Noyes,1915, and Hymen- olepisevaginata Barker and Andrews, 1915, infecting both the muskrat and the vole. The fourspecimens of the lattercestode taken from voles appeared to be abnormalin development,however, as willbe discussedfurther below. Entosiphonusthompsoni Sinitsin, 1931, an abundantparasite of the short- tailedshrew, an insectivore,was encounteredin threevoles. Quinqueserialis quinqueserialis(Barker and Laughlin,1911) was a commonparasite of the muskrat,but did not occurin voles;the latter were commonly infected with a relatedspecies, Q. hassalli(McIntosh and McIntosh, 1934). Quinqueserialis hassallihas been recordedfrom the woodchuckfrom the same marsharea (Rauschand Tiner,1948); however,comparison with specimens collected here fromvoles indicates that the wormsfrom woodchucks should be considered onlyas Quinqueserialissp. untiladditional material is availablefor study. In general,the findingsrelative to hostspecificity appear to parallelthose re- cordedin a previouspaper (Rausch and Tiner,1948). Furtherdata on this aregiven below, in thediscussions of theseparate helminth species.

REMARKS ON THE BIOLOGY OF THE HOST It seemsexpedient at thispoint to includesome information on thebion- omicsof voles. This has beenobtained mainly from an examinationof the literature,although some of ourown observations have been included. Most of theobservations made by variousworkers in theUnited States have been basedon thecommon meadow vole, Microtus p. pennsylvanicus.Such infor- mationmay be of use in betterevaluating the results of our investigations. Voles of thegenus Microtus are herbivorousmammals, common in both NorthAmerica and Eurasia. They feedessentially on grasses,and to a lesserdegree upon grain,tree bark, tubers, and othervegetable matter. In theNorth Central States, during the winter months, they are oftenfound in com shocks. As faras we havebeen able to learn,voles ingest very little animalmatter. Voles have a characteristicrapid rate of reproduction,and a shortlife span. Accordingto Hamilton(1937), who studiedthe commonmeadow vole,growth is veryrapid until about the 12thweek, when it is retardedand Rausch & Tiner in American Midland Naturalist (May 1949) v. 41, no. 3. Copyright 1949, University of Notre Dame. Used by permission.

672 THE AMERICAN MIDLAND NATURALIST 41 (3) the animalsare consideredmature. Bailey (1924) foundthat female voles maybe sexuallymature at 25 daysof age,while the males may be fertileat 45 daysof age. Accordingto thedata presentedby Hamilton(1937), age and weightof volesare closelycorrelated, allowing one to determinerather closelythe ages of animalsexamined. This wouldbe of valueif an attempt weremade to learnsomething of the effectsof hostage on helminthinfec- tionsin theseanimals. The olderanimals apparently die each yearduring the late summeror fall,and onlythe animalsborn late in the seasonare able to survivethe winter.Baker and Ransom(1938) found,with Microtus agrestis L. in Europe,that the olderanimals die in aboutOctober. We havefound very fewlarge adults during the wintermonths over the region where this study was made;the great majority of animalsconsisted of subadults.We found thisto be trueeven during the timesof highpopulation density. We did observe,however, in Microtuspennsylvanicus drummondii and M. ochrogaster,that large adult animals were present during the wintermonths of 1947-48,even though the populations were known to be quitelow. Hamilton(1937) listedthree factors as contributingto the short life span of thevole: 1) theattainment of sexualmaturity at a veryearly age; 2) ex- tremeprolificacy; 3) little cessationof activityin the searchfor food. Accordingto thesame author (1941), thelength of thebreeding period of volesin theeastern United States is correlatedwith population density; breeding may continueon throughthe winterwhen the populationdensity is nearingthe peak. Hamiltonalso stated"the number of youngin a litter varieswith the population level of themice, large litters predominating when miceare abundant." Populationdensities and reproductiveactivity in volesdiffer greatly from one area to anotherat thesame time. For example,it was seen,during the winterof 1947-48,that Microtus p. drummondii,in Manitoba, and M. ochrogaster,in Indianaand Illinois,were breeding at a highrate. This occurred, eventhough the voles were at a lowpoint in populationdensity. In Wiscon- sin,on theother hand, where a largenumber of voleswas examinedduring thesame period, not a singlelarge adult was observed. Furthermore, examinationof thetrapped animals failed to discloseperforate vaginae, placental scars, pregnancy,or evidenceof anybreeding activity in themales. We are of the opinion,therefore, that nearly all theanimals present at thistime were non- breedingadults. It shouldnot be assumed,however, that these observations on Microtusp. drummondiiand M. ochrogasterare necessarily comparable to thosemade pre- viouslyon M. p. pennsylvanicus. RESULTS The varioushelminth species obtained are discussedseparately below. The numbersin parenthesesfollowing the parasitename refer to Figure1, in whichthe distribution of the helminths is shown. In showingthis distribution,the speciesof Microtusis not considered;however, Table I liststhe parasitesaccording to hostspecies in whichthey occurred, along with certain otherdata. Rausch & Tiner in American Midland Naturalist (May 1949) v. 41, no. 3. Copyright 1949, University of Notre Dame. Used by permission.

1949 RAUSCH ET AL.: HELMINTHS OF VOLES 673

CESTODA In general,cestodes of thefamily Anoplocephalidae Fuhrmann, 1907, are commonparasites of voles,while cestodes belonging to othergroups are rare. This appearsto be trueof thecestodes of Eurasianvoles, as well.

ANOPLOCEPHALIDAE 1. Andryamacrocephala Douthitt, 1915. (Fig. 1, counties12, 17, 20, 21).-First describedfrom Geomys bursarius (Shaw), thiscestode is a commonparasite of voles,from which it has beenrecorded by Rausch(1947). AlthoughAndrya spp. havepreviously been recorded from Microtus, specific determinationswere not made. Erickson(1938) recordedAndrya sp. from Microtusp. pennsylvanicusand fromClethrionomys g. gapperi Vigors; however,according to his description("a shortbroad cestode was removedfrom the cecum. . . "), he apparentlywas dealingwith a speciesof Paranoplo- cephalaLuehe, 1910. Anotherspecies, Andrya primordialis Douthitt, 1915, has also beenre- cordedfrom voles. Rankin(1945) recordedthis cestodefrom Microtus longicaudus(Merriam) and fromM. montanus(Peale), fromthe state of Washington.Douthitt (1915) recordedit fromM. p. modestus(Baird), fromColorado. It seemsevident that A. primordial'sis rare or does not occur in theregion where the present study was made. Althoughwe havenot recordedAndrya macrocephala from a numberof localitiesfrom which voles were examined, it is, neverthe.ess,very common in someareas. Sincesome of our collectionsfrom certain areas were made duringthe winter months only, when this cestode is rarelyfound, it is probablethat the examination of volescollected during the summer months would showit to be commonin otherareas also. It mightbe mentionedhere that Geomysbursarius, from which it wasdescribed, and of whichit seemsto be a commonparasite (Douthitt, 1915) is foundonly over the westem edge of the regionconsidered in thisstudy. Exceptfor a specimenof Microtusp. drummondii,which contained 6 worms(5 of whichwere immature), no morethan 4 wormswere removed from a singlehost. The averagenumber per infected animal,based on 345 volesfrom southern Michigan, was 1.6 worms. Data obtainedfrom the Michigan study area make apparent certain char- acteristicsof Andryamacrocephala infections in thecommon vole. The peak of infectionwas observedto occurduring the monthof August,with very littleparasitism by thiscestode during the wintermonths. Figure 5 shows thecourse of such infections. Immature worms were again found in thespring, suggestingthat the infected intermediate hosts are rarely available to thevoles dluringthe winter.No differencesin age susceptibilitywere observed. The lifecycle of cestodesof thegenus Andrya remains unknown, but it wouldseem likely that mites serve as the intermediatehost, in viewof our knowledgeof thelife cycles of othermembers of thesub-family. The ecology of suchmites would be of muchimportance in the epizootology of thecestodes forwhich they serve as intermediatehosts. Krull(1939) foundthat oribatid mites,which serve as the intermediatehosts of Moniezia,Cittotaenia, and Rausch & Tiner in American Midland Naturalist (May 1949) v. 41, no. 3. Copyright 1949, University of Notre Dame. Used by permission.

674 THE AMERICAN MIDLAND NATURALIST 41 (3) others,were most abundant on grassafter a heavyrain, and thatthey retained theirgreatest constancy where moisture was abundantenough to encourage grassgrowth. According to the same author,the mitesare not reduced greatlyby cold,wet weather of a week'sduration, or by a dryperiod of a month'sduration, provided these changes occur during the springor early summer.Krull also foundthat the mites were more abundant in thespring thanin winter,and thatthey were more abundant on thegrass early in the morningthan they were during the day. The peakabundance of suchmites on grassprobably corresponds closely to theperiod of greatestactivity of the voles. It seemsprobable that mites would often be ingestedwith the grass uponwhich voles feed. It is of interestto note the resemblanceof the courseof infectionof Andryacaucasica Kirschenblatt, 1938, in Microtussocialis, to thatof the presentspecies in M. p. pennsylvanicus(Kirschenblatt, 1938; graph 6, page 22). In bothcases, infections were low during the winter months. Kirschen- blattalso reporteda lowaverage number of worms(less than2) perinfected host. One mightsay thatA. caucasicain theTranscaucasus region fills an ecologicalniche very similar to thatoccupied by A. macrocephalain north- centralNorth America. 2. Andryamicroti Hansen, 1947. (5).-A singlecestode referable to this specieswas collectedduring February,. 1948, at Madison,Wisconsin. Hansen (1947) describedA. microtifrom Microtus ochrogaster in Nebraska. Recently,through the kindness of Dr. ReinardHarkema, we had theoppor- tunityof examiningwhat appears to be thisspecies from the cotton rat, Sig- modonh. hispidusSay and Ord. The infectedanimals had beencollected in Wake County,North Carolina. This speciesis uncommonin theNorth CentralStates region, according to theresults of thepresent study. There is a strikingmorphological similarity between Andrya caucasica Kirschenblattand A. microti;however, evidence is hardlyadequate at present to considerthem identical. As faras wehave been able to observeso far,cestodesof thegenus Andrya are not affected morphologically bythe host species in whichthey occur. It seems,however, that the rather closely related species foundin NorthAmerican rodents (A. macrocephalaDouthitt, 1915); A. microtiHansen, 1947; A. ondatraeRausch, 1948) shouldbe carefullystudied whena largevolume of materialbecomes available for comparison. 3. Andryasp. (17, 20).-Five specimensof cestodes of the genus Andrya wereobtained from voles collected in centralOhio and southernMichigan. None of thesecontained gravid segments, although mature segments were present.The materialwas not adequateto allowfor specific identification, althoughit is possiblethat these represented atypical specimens of A. macrocephala.Morphologically they did notagree closely with this species, however. 4. Paranoplocephalatroeschi Rausch, 1946. (1, 4, 5, 6, 8, 16, 17, 18, 21, 22).-Found in or nearthe cecum of thehost, this cestode was themost commonfound parasitic in voles. Hansen (1947) reportedP. troeschifrom Microtusochrogaster from Nebraska, and it is possiblethat the previously Rausch & Tiner in American Midland Naturalist (May 1949) v. 41, no. 3. Copyright 1949, University of Notre Dame. Used by permission.

1949 RAUSCH ET AL.: HELMINTHS OF VOLES 675 mentioned"Andrya sp.," recordedby Erickson(1938), was identicalwith this species. The maximumnumber of thisspecies of cestodeobtained from a single hostwas 8, withan average(based on 345 animalsfrom the Michigan study area) of 2.2 per infectedanimal. As faras couldbe determined,host age has littleor no effecton infectionswith this cestode. Thesecestodes appear to be eliminatedfrom the host during the months of earlyspring (i.e. pre- viousto thefirst of June). It was of interestto notethat the heaviest infections with this parasite wereobserved during the winter months, with the highest percentage of animals infectedduring the months of Decemberand January(see Figure5).

w w (.jr1bJ U) O w I)

CESTODEPARASITES oonz Xoz3?o-1 IZEQI O

Andryc macrocephala --] | | t mr C ittotaenia sp. Paranoplocephalatroeschi Paranoplocephalaspp. Qochoristicaokiahomensis*s -~~~~~~~~Hymenolepis diminuta : Hymenolepisfraterna Hymenolepisanthocephalus Hymenolepissp.ll l Mesocestoides loatus() Taenia taenioeformis v v Taenia pisiformis

sCOMMON LJ sUNCOMMON O= ACCIDEN TAL Fig. 3.-Host-parasiterelationships on the Michiganstudy area. Part A. CESTODA.* * The helminthnames used in thesecharts have been checked,and, as far as could be determined,are valid. Rausch & Tiner in American Midland Naturalist (May 1949) v. 41, no. 3. Copyright 1949, University of Notre Dame. Used by permission.

676 THE AMERICAN MIDLAND NATURALIST 41 (3)

Duringthe courseof thisstudy, this cestode was not collectedfrom voles beforethe month of October,or afterthe month of May. Whileoccasional infectionsmay occur during the warmer months of theyear, they must indeed be rare. Verysmall specimens of Paranoplocephalatroeschi, with only the begin- ningof strobilae,were found during the earlierpart of thewinter. It was also notedthat immature worms were found in largernumbers in a single hostanimal than were those with gravid segments. This suggeststhat only a fewworms may be ableto survive,even though the initial infection be much heavier.We did notfind any immature worms after the month of February. This cestodemust mature very rapidly, and musthave a veryshort life span. It wouldalso seemthat mites function as theintermediate host of Paranop- locephalatroeschi, although there is no definiteevidence for such an assump- tion. It appearsthat the intermediate host of thiscestode is notavailable to

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TREMATODEPARASITES 0oen eOIAOztil LZZ -,LIrO

Brachylaemus virginianus Entosiphonus thompsoni Panopistus pricei Hasstilesia tricolor Echinostoma revolutum [ ] Paragonimus sp.() Euryhelmis monorchisLJ

Alaria taxideae Fibricola cratera l|1 Fibricola nana a3 Pharyngostomoides ovalis _-

*= COMMON IZ=U NCOMMON O ACCIDENTA L

Fig.3.-Host-parasite relationships on the Michigan study area. PartB. TREMATODA. Rausch & Tiner in American Midland Naturalist (May 1949) v. 41, no. 3. Copyright 1949, University of Notre Dame. Used by permission.

1949 RAUSCH ET AL.: HELMINTHS OF VOLES 677

w w CI) w11

I) 0OJJ ,, W O Z : w?

0 z~~~W Z TI<:OX CE?I O(OW H O J

N\1EMATODE PARASITES on c D LL I I

Ancylostoma sp. Uncinaria lotoris

Obeliscoides cuniculi

Trichostronqylus calcaratus Molineus patens

Lonqistriata caudabullata Citellinema bifurcatum Nematospiroides sp.

Dictyocaulus viviparus

Cruzia tentaculata Passalurus ambiquus

Aspiculuris sp. [] z Enterobius sciuri . .0 Syphacia obvelata o Heterakis spumosa Toxocara mystax

Ascaris columnaris Z 0 Porrocaecum sp. Physaloptera turqida z z Physaloptera maxillaris Physaloptera rara Physaloptera limbata Mastophorus muris z Spirura talpae 0

Rictulari a sp. [ Capillaria mustelorum

Fig. 3.-Host-parasiterelationships on the Michiganstudy area. Part C. NEMATODA. Rausch & Tiner in American Midland Naturalist (May 1949) v. 41, no. 3. Copyright 1949, University of Notre Dame. Used by permission.

678 THE AMERICAN MIDLAND NATURALIST 41 (3) thevoles during the warmer months of theyear, and this is suggestiveof some veryinteresting ecological factors upon whichthis must be dependent. Whetherthese factors are connectedwith seasonal variation in hostbehavior, or withphysiological or immunologicalpeculiarities of the definitivehost, is unknown. Paranoplocephalatroeschi is morphologicallyvery close to P. brevis Kirschenblatt,1938. AlthoughKirschenblatt's paper was citedat the time P. troeschiwas described (Rausch, 1946), it wasnot yet avalaible. It can be seenthat these worms appear to fillsimilar ecological niches in theirrespective regionsof distribution,and thismay be veryimportant in establishingrela- tionships.Kirschenblatt's graph 3 (page 18) givessome information on the behaviorof P. brevisin thehost (Microtus). It is probablethat further study willshow that P. troeschishould be considereda synonym of P. brevis;however,additional material for comparison is neededto establishthis. 5. Paranoplocephalaspp. (1, 2, 3, 4, 5, 10, 12, 14, 16, 17, 18, 21, 22).- When P. troeschiwas describedthe attendantexamination of a fairlylarge seriesof cestodesfrom voles revealedthat specific differences often were most difficultto delineatein the genus Paranoplocephala.This, with the present confusionof names,would indicatethat furtherwork on this group is badly needed. We expectto presentfurther data on this problemin the future. Because of the presentstatus of these cestodes,specific determinations are not indicatedhere. A large species of Paranoplocephalawas occasionally-foundin the duo- denumof the host,just belowthe stomach. In no case was morethan a single wormfound per host animal. What appearsto be anotherspecies was found lower in the small intestine. In general,these cestodeswere uncommonin voles,and nothingwas observedconcerning their epizootology.

DILEPIDIDAE 6. Choanotaeniasp. (12).-A single worm belonging to the genus ChoanotaeniaRailliet, 1896, was removedfrom the intestineof a specimen of Microtus ochrogaster,collected at Champaign,Illinois. The hooks appearedto be 26 in number,and werearranged in a double row; theyaveraged 30 , in length. The testesaveraged 31 in number,and the cirrussac meas- ured from80 to 115 , in length. No gravidsegments were present. This. may representan accidentalinfection.

HYMENOLEPIDIDAE 7. Hymenolepisfraterna Stiles, 1906. (21) .-A singlecestode, without a scolex,was obtainedfrom a vole collectednear Marysville,Ohio. It seemed to agree in all respectsto H. fraterna.Hymenolepis fraterna was commonly seen as a parasiteof the house mouse,but it cannotbe considereda common parasiteof the voles of thisregion. Hughes (1940) recordedthis cestodeas occurringin a Europeanvole, Microtusagrestis L., however.

1949 RAUSCH ET AL.: HELMINTHS OF VOLES 679 each containingtwo cestodes of thisspecies, were collected on thesouthern Wisconsinstudy area. Althougha commonparasite of muskratsover the NorthCentral States region, it mustbe consideredaccidental in voles. The cestodesfrom the voles were rather small for this species (80 to 130 mm),but in generalwere typical in theirmorphology. However, it wasnoted thatin no case had anyeggs developed, although proglottids had beenshed fromall fourstrobilae. This is perhapsfurther evidence that the vole is an abnormalhost for this parasite. 9. Hymenolepissp. (13) .-Five specimensof a cestodebelonging to this genuswere obtained from a volecollected in easternIllinois. Unfortunately, thehooks had beenlost from the scolices, and thematerial is notconsidered adequatefor specific identification.

TAENIIDAE 10. Taenia taeniaeformis(Batsch, 1786). (1, 8, 12, 17, 22).-Stro- bilocerciof thiscestode were rather common in theliver of volesfrom some areas. The distributionwas, however, quite local. This is notreadily under- stood,since there must be littledifference in the housecat populationover the regionunder consideration. Feral cats werepresent over most of the areasconsidered, and, in mostcases, vole habitat areas were readily accessible to cats fromnearby farms. In northernWisconsin (Figure 1, number1) whererather a highincidence of infectionwas observed, it is possiblethat the bobcat,Lynx rufus Schreber, might also haveacted as thedefinitive host for thiscestode. Rollings(1945) reportedTaenia taeniaeformisto be a fairly commonparasite of thebobcat in Minnesota.No informationis yet available on Wisconsinbobcats. On theMichigan study area theselarval cestodes were first seen in voles in November,and duringeach month thereafter until the last of May. The largestpercentage of infectedanimals was seenduring the month of January. A somewhatparallel situation was observedin thefox squirrel, concurrently trappedin the adjacentwoodlot, although a smallernumber of animalswas infected(Rausch and Tiner, 1948). In thevoles from this area the maximum averagenumber of cystsper animalper monthcoincided with the peak in incidenceof infection.Although this parasite was foundin the liverof a muskratfrom the southern Wisconsin study area, it wasnot observed there in voles. Feralhouse cats, collected on theimmediate study area, were found to be infectedwith cestodes of thisspecies, and othercats, not captured,were fromtime to timeseen on thearea. A totalof 26 houserats was examinedfrom a farmin centralOhio, and it wasfound that 21 of thesewere infected with larval cestodes of thepresent species. A totalof 35 volesexamined from the samefarm area failedto discloseany infections by this parasite. Egg densityper given unit area probably decreasedvery rapidly as distancefrom the farmbuildings increased. Unfortunately,enough rats living in thefields away from the buildings could notbe obtainedto allowfor a comparisonunder these conditions. A cysticercusbelonging to thegenus Taenia was taken from the liver of a specimenof Microtusp. drummondii,collected near Winnipeg,Manitoba. Rausch & Tiner in American Midland Naturalist (May 1949) v. 41, no. 3. Copyright 1949, University of Notre Dame. Used by permission.

680 THE AMERICAN MIDLAND NATURALIST 41 (3)

This cysticercuswas not identifiedto species. Two rowsof hookswere present,with 12 in eachrow. The largerhooks averaged 72 tsin length,while thesmaller ones averaged 49 p,.

11. ?Cladotaeniasp. (5, 13, 17, 21).-A fewvoles were found to be infectedwith very small cysticerci, which occurred in theliver. Two speci- mensfrom voles collected in southemMichigan had hooksabout 16 /x in length,arranged in a doublerow. On the southernWisconsin area, a relativelyheavy infection was noted. Of the43 volestaken on themarsh, 12 wereinfected, with an averageof 3 cystsper infected animal. The hooksof these,also arrangedin a doublerow, measuredabout 23 ju in length.The livercysts were quite small, and com- monlymeasured about 2 mm.in diameter.With the possible exception of one muskrat,no otherhost animal from this area was foundinfected by these cysticerci. It is possiblethat these cysticerci were larval cestodes of thegenus Clado- taenia;it is hopedthat this can be determinedby feedingexperiments with hawks. In theWisconsin marsh, hawks (Circus, Buteo, Accipiter) were usu- allyabundant, and perhapsconditions in thisarea allowed a betteropportunity forvole infections with this parasite. Experimental work by one of us (R. R.) has shownthat these cysts are not larvaeof owl cestodes(Paruterina); this workwill be reportedseparately.

TREMATODA Duringthe courseof the presentstudy, only two speciesof trematodes werefound which could be considerednatural parasites of voles. One of these,Quinqueserialis hassalli (McIntosh and McIntosh,1934), was widely distributed,and occurredin a numberof localitieswhere habitat seemingly was favorableto the intermediatehost. A second,Mediogonimus ovilacus Woodheadand Malewitz,1936, was recorded only from Washtenaw County, Michigan,from which locality it was firstdescribed. Three infections by a thirdspecies, Entosiphonus tbompsoni Sinitsin, 1931, could only be regarded as accidental.Price (1931) reportedMicrotus pennsylvanicus to be thenat- ural hostfor Schistosomatium douthitti (Cort, 1915); it is possiblethat we haveoverlooked infections of thisparasite. Thatvoles have few trematode parasites is notsurprisinig, considering their diet,and the factthat in generalthey inhabit areas which are not favorable habitsfor snails. NOTOCOTYLIDAE 12. Quinqueserialishassalli (McIntosh and McIntosh,1934) (4, 5, 15, 18, 21).-The onlycommon trematode found in voles,this species appeared to be abundantonly locally, although it has beenrecorded from voles over a widegeographical area (Harwood,1939). The distributionof thisparasite seemsto be limitedto areaswith aquatic habitat suitable for a snailinterme- diatehost. On thesouthern Wisconsin marsh, a highpercentage of voles(46 percent) wasinfected. The trematodesaveraged 8 perinfected host, with a maximum numberof 37 in a singlehost. Muskratswere not found to be infectedwith Rausch & Tiner in American Midland Naturalist (May 1949) v. 41, no. 3. Copyright 1949, University of Notre Dame. Used by permission.

1949 RAUSCH Er AL.: HELMINTHS OF VOLES 681 thisparasite; they were, however, heavily infected with a memberof thesame genus,Quinqueserialis quinqueserialis (Barker and Laughlin,1911). The latteroccurred in verylarge numbers (average for 6 infectedmuskrats: 406 worms). More thana thousandof thesetrematodes were removed from the cecumof a singlemuskrat. Voles trappedon the Wisconsinmarsh during the wintermonths were foundto be heavilyinfected by Quinqueserialishassalli. Whether these in- fectionshad carriedover from the previousfall, or whetherthey obtained duringthe winter months, is notknown. A fewimmature trematodes found duringJanuary and Februaryindicated that infective stages were available to thevoles to at leastsome degree during the winter. It mightbe mentioned herethat open water was alwayspresent in thismarsh, because of the con- tinualflow from the springs. Although the investigation here has so farbeen carriedthrough only one springseason, evidence so farwould indicate that thereis a decreasein infectionby this parasite during this time.

PLAGIORCHIIDAE 13. Mediogonimusovilacus Woodhead and Malewitz,1936. (18).- Two of fourvoles secured from Washtenaw County, Michigan, were infected by thishelminth. This speciesappears to be veryrestricted in its distribution, sincewe did notencounter it elsewhere in theregion considered. In onecase, more than 50 wormswere taken from cysts in the liverof a youngvole (28 grams), while3 specimenswere taken from the bile duct of a second animal. In the firstcase, a few of the trematodeshad migratedthrough the bile duct into the small intestine,probably after the death of the host. Our observations on this species agree withthose made by Woodhead and Malewitz (1936). We observedalso that the matureworms in the case of the heavierinfection were much smallerthan were those fromthe bile duct of the second animal. The infectedanimals were captured along a river.

Part of the liverof the animalshowing the heavierinfection was sectioned, and a few observationswere made on the reactionof the host tissueto this parasite. The wormshad been well walled off,and were surroundedby a capsule of connectivetissue. Many eggs, found outside the capsule, were also beingwalled off,and a heavydeposition of a black pigmentwas seen in the area withthe eggs. There was a metaplasiaof the biliaryepithelium, and some pressurenecrosis of the livercells. The cellularreaction was moderate, consistingmainly of macrophages. Eosinophileswere not observed. This appeared to be the most pathogenicparasite encountered by us duringthe course of the presentstudy, although it does not seem probablethat there would be any serious result to the host, unless infectionswere extremely heavy. A photomicrographof a typicalliver section is givenin Figure6.

BRACHYLAEMIDAE 14. Entosiphonusthompsoni Sinitsin, 1931. (5).-This trematodewas takenonly fromthe voles of a singlelocality, and mustbe consideredpurely accidentalin thevole. Two of theinfected voles contained a singleworm each, Rausch & Tiner in American Midland Naturalist (May 1949) v. 41, no. 3. Copyright 1949, University of Notre Dame. Used by permission.

682 THE AMERICAN MIDLAND NATURALIST 41 (3) whilea thirdharbored two worms.The wormsappeared to be normalin development;all weremature, with numerous eggs in theuteri. Entosiphonusthompsoni was a verycommon parasite of the short-tailed shrewover the entireregion considered in thisstudy. However,the short- tailedshrew was not abundantin the marshfrom which the infectedvoles weretaken. Anothershrew, Sorex c. cinereus,was quiteabundant in the area,but onlyon one occasionwas thisspecies found to be infectedwith E. thompsoni;in thiscase, a fewsmall, immature worms were collected. Krull (1933) has recordedthis trematode from the white-footed mouse, Peromyscus leucopusnoveboracensis.

NEMATODA Nematodeswere found to be verycommon parasites of voles,although theydiffered considerably in varietyand numberfrom one area to another.

TRICHOSTRONGYLIDAE 15. Nematospiroidessp. (5, 17, 18).-This nematodewas takenfrom 9 animalsof the345 examinedfrom the southern Michigan study area, and from27 of the43 volesfrom the Wisconsin study area. In general,it was an uncommonparasite. The numberof wormsper infected host was much higherin theWisconsin area, ranging from 1 to i78 (average:13), whilein the Michiganarea it rangedfrom 3 to 31 (average:6) per infectedhost. Dikmans (1940) describedtwo NorthAmerican species of Nemato- spiroides,bringing the number in thegenus to 3. Unfortunately,our speci- mensdo not agreewith any of the describedspecies. They appearto be nearestto N. carolinensisDikmans, 1940, in thatthey possess a separatedorsal rayin thebursa, and havespicule lengths ranging from 1.9 to 2.4 mm.long in maleswhich were 5.1 to 7.4 mm.in length.Nematospiroides carolinensis was describedfrom Clethrionomys from North Carolina. No nematodesof thisgenus were found in anyother hosts collected from the marsh where the heavyinfections occurred in Microtus,although N. longispiculatusDikmans, 1940,was foundin bothmuskrats and volescollected in Washington,D. C., andin New Jersey(Dikmans, 1940). Spurlock(1943) did some experimentalwork with the relatedspecies Nematospiroidesdubius Baylis, which occurs as a parasiteof housemice and otherrodents. He foundthat some strainsof laboratorymice were moresusceptible than others, but was unableto drawany conclusionscon- cerningacquired resistance. When largenumbers of larvaewere given, the mortalitywas high. The infectionwith this species of helminthapparently lastsfor at least8 months. Spurlockalso foundthat after the eggs of Nematospiroidesdubius hatch, the free-livingstage is passedin moistfecal material. The larvaeare infec- tiveabout 6 daysafter the deposition of thefeces, and are foundat thattime on thesurface of thefecal mass. Kirschenblatt(1938) has givenfurther observationson thedevelopment of Nematospiroideslarvae in Microtus. Elton,Ford, and Baker(1931) studiedthe parasitesof someEuropean rodents,and foundNematospiroides dubius to be a commonparasite of the Rausch & Tiner in American Midland Naturalist (May 1949) v. 41, no. 3. Copyright 1949, University of Notre Dame. Used by permission.

1949 RAUSCH ET AL.: HELMINTHS OF VOLES 683 woodmouse,Apodemus sylvaticus, but did notfind it in eitherClethrionomys or Microtus.In 692 specimensof woodmouse,they found an incidenceof infectionof 85 per centin adultanimals. They also reporteda highinci- denceduring the summer and earlyautumn. The seasonalvariation in incidenceof infectionwith N. dubiuswas directlydependent upon age distributionof theanimals, and, therefore, directly correlated with the breeding cycle. The questionarises whether this is also trueof the courseof infectionin Microtus.

w LU I- cn D AndryW 0LJ_

(/C) w

Andryamicrotif) 0 d ocr

Cittotaeniasp. Parcanoplocephalatroeschi Paranoplocephala sp. a ] Protogynellablarinae[] Hymenolepisevaginata ( )

Hymenolepi s sp. ]

Mesocestoides variabilis | a Taenia tae'niaeformis* L TAenya pmsiformis Cladotaenia sp.

*-COMMON EJ:UNCOMMON O= ACCIDENTAL

Fig.4.-Host-parasite relationships on the Wisconsin study area. PartA. GESTODA. Rausch & Tiner in American Midland Naturalist (May 1949) v. 41, no. 3. Copyright 1949, University of Notre Dame. Used by permission.

684 THE AMERICAN MIDLAND NATURALIST 41 (3)

Erickson(1944) reportedthat, in the snowshoehare, Lepus americanus Erxleben,the helminthparasites are mostabundant during the peak of the populationcycle of the host. Elton,Ford, and Baker (1931) foundthat therewas a higherpercentage of woodmiceinfected by Nematospiroides dubius at thetime of highdensity just before the mortality occurred, but no unusual increasein numberof worms per infected animal. Kirschenblatt(1938) found,with the same parasite,also in the woodmouse,that the number of wormsranged from 11 to 86, withan averageof 34 perinfected animal. He foundlarger infections in mountainforest areas thanin opencountry, and consideredthe moistwoods to be moresuitable

0cr cI T m o3 ow3 F- L.LJLLj 0 H

W~-00 ~ o-Owoo

TREMATODE PARASITES o e220

Entosiphonus thompsoni Panopistus pricei I Hasstilesia tricolor Echinostoma revolutum Euparyphium melis Plagiorchis proximus Quinqueserialis quinqueserialis Quinqueserialis hassalli Quinqueserialis sp. Alaria minuta AlIaria s p. F Fibricola cratera 6

*=COMMON E=UNCOMMON O ACCIDENTAL

Fig. 4.-Host-parasiterelationships on the Wisconsinstudy area. Part B. TREMATODA. Rausch & Tiner in American Midland Naturalist (May 1949) v. 41, no. 3. Copyright 1949, University of Notre Dame. Used by permission.

1949 RAUSCH ET AL.: HELMINTHS OF VOLES 685 habitatfor larval development. We observedheavier infections and a higher incidenceof infectionin thesouthern Wisconsin area, where the habitat was muchwetter than in theMichigan area. Our observationsseem to agreewith thoseof Pearse(1930) in respectto thegeneral relation of thehelminths to thehabitat of the host. It is ofinterest that we have never taken this nematode fromanimals of any specieswhich were trapped within forest areas. We havenot yet examined enough infected voles to allowany observations on age susceptibility.Elton, Ford, and Baker(1931) showed,in thewood- mouse,that the infection with this nematode increases with the age ofthe host.

16. Longistriatadalrymplei Dikmans, 1935. (4).-Althoughit has been reportedfrom several localities (Dikmans, 1935), thisnematode was found to be uncommonin thevoles of the regionconsidered here. Infectedanimals weretaken only at HoriconMarsh, Wisconsin, from Microtus p. pennsylvanicus. Otherfoci of infectionmay occur in theregion studied, but, if so, they wereoverlooked because of therelatively small number of animalsexamined. The lifecycle of a relatedspecies, Longistriata musculi Dikmans, 1935, has beenstudied by Schwartzand Alicata (1935), and it was foundthat larvaemay gain entranceto the hosteither by wayof ingestionor through theskin. It seemsprobable that voles can withstandfairly heavy infections with thisparasite, without serious result. The infectionswe observedwere medium; themaximum number of wormsseen in a singlehost was 48.

17. Dictyocaulusviviparus (Bloch, 1782). (17).-Two males and a singlefemale, the lattercontaining many embryonated eggs, were recovered by one of us (R. R.), apparentlyfrom the cecumof a vole fromsouthern Michigan.Before the worms were fixed, the absence of a separatedorsal lobe in thebursa and theheavy spicules of the males were noted. The problemof identificationwas transmittedto the juniorauthor. The findingof bursate strongyloidworms in theintestinal tract suggested that they belonged to the familyTrichostrongylidae Leiper, 1912. Detaileddrawings were made, and a searchthrough the literature was undertaken in an effortto determinetheir systematicposition. This provedto be quitewithout result until similarity was noticedbetween the dorsal rays of the bursa in ourdrawings and thoseof Dikmans(1936; Fig. 1, No. 11). A subsequentcomparison of our specimens withD. viviparusfrom domestic cattle indicated that they belonged to this species. Our materialwas thensent to Dr. Dikmans,who replied that he couldonly confirm the identification. BothDr. Dikmansand Dr. G. R. LaRuecautioned the authors that con- taminatedequipment or faultylabeling might have beena sourceof error. However,cattle were not autopsied in thesame building where the voles were examined,and petridishes used by us wereused in additiononly for bac- teriologicalpurposes. The factthat the worms were studied while still alive seemsto precludeany possibility of faultylabeling. We had no doubtsas to theirsource while in theprocess of identifyingthem. We feelobliged to as- Rausch & Tiner in American Midland Naturalist (May 1949) v. 41, no. 3. Copyright 1949, University of Notre Dame. Used by permission.

686 THE AMERICAN MIDLAND NATURALIST 41 (3) sume,therefore, that the worms actually were present in theintestinal tract of thevole. It wouldseem that the vole had ingestedthe worms as larvae,and that

w: O

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(I) *w 0WY'zCt wo~ NEMATODEPRASITES QOW I1IZ 3 Ir

Nematoslroldo sp.. |bOa - Trichostrongyluscalcaratus Molineus patens F Citellinema bifurcatum Nematospiroides sp. Syphacia obvelata Syphacia peromysci Toxocara mystax Physaloptera turgida Physaloptera maxillaris Physaloptera rara Pseudophysaloptera soricina Capillaria muris-sylvatici Capillaria mustelorum Capillaria sp. Capillaria sp. Filaroides martis Trichuris opac.a

E=COMMON W]=UNCOMMON O ACCIDENTAL

Fig. 4.-Host-parasiterelationships on the Wisconsinstudy area. Part C. NEMATODA. Rausch & Tiner in American Midland Naturalist (May 1949) v. 41, no. 3. Copyright 1949, University of Notre Dame. Used by permission.

1949 RAUSCH ET AL.: HELMINTHS OF VOLES 687 theyhad grownto maturityin its cecum. Sincevoles reduce their food to rathersmall size beforeit reachesthe stomach, it does not seemlikely that suchlarge worms could have been ingested intact. Beef cattle were pastured in the same fieldwhere the vole was collected.We do not knowif these animalswere infected with Dictyocaulus viviparus. It is of interestthat Dougherty (1946) has decidedthat there is morpho- logicalevidence for classifying the genus Dictyocaulus in theTrichostrongy- lidae. OXYURIDAE 18. Syphacia obvelata (Rudolphi, 1802). (1, 2, 3, 4, 5, 7, 8, 12, 13, 15, 16, 17, 18, 20, 21, 22).-The mostcommon helminth encountered in the voles of this region,S. obvelatawas widelydistributed. It was also recorded fromMicrotus pennsylvanicus drummondii, from near Winnipeg,Manitoba, and was observedin the house rat in Michigan,Ohio, and Wisconsin,and in the housemouse in Illinois. The life cycle of this nematodeis direct (Lawler, 1939), and theredoes not appear to be any immunitydeveloped, age or otherwise,according to what has been learned from work with other rodents (Culbertson,1941; Taliaferro,1929). Syphacia obvelata was found throughoutthe year. On the southern Michigan study area, it was found,during the firstsummer, that relatively few animalswere infected, but the averagenumber of wormswas high. Later, duringthe winter,a largeproportion of the populationwas infected,but with a loweraverage number of wormsper infectedanimal. Of the 345 voles collectedfrom this area, 30 per centwere infected with this parasite. The average numberof wormsper infectedanimal was 15.5, witha maximumnumber of 242 wormsoccurring in a single host. On the Wisconsin area, wherethe habitatwas much wetter,30 per cent of the animalsalso wereinfected. In this latterarea, Syphaciaperomysci Harkema, 1936, occurredcommonly, and apparentlywas parasiticonly in Peromyscusspp. Kirschenblatt(1938; graph 12, page 36) found the peak of infection duringthe spring,in Microtus,with the maximumaverage number of worms per animal at thistime, also. He observedtwo peaks of infection,one in the springand one in the fall,in Mus musculussubsp. Syphacia stroma (von Lin- stow, 1884) showed, in the woodmouse,a behaviorsimilar to that of S. obvelatain M. musculussubsp. Male worms were rare, a conditionpreviously noted by other workers (Hall, 1916), but in a few cases a majorityof wormswas males. Kirschen- blatt (1938; page 36) stated "I found males more than once, and furthermore in some cases the numberof males exceededthe numberof females. Frequentlyit happened that the males were not found in the presenceof females. The males of S. obvelatado not appear to be a rarity,as it seems that one would judge fromthe data of Linstow,Hall, and Schultz. But evi- dentlythey live a considerablyshorter period than the females. It was im- possibleto establishany rule as to the relationshipof the numberof males to the femalesin the variousseasons of the year. The absenceof males seems especiallystrange in the comparativelylarge materialthat Schulz had. One Rausch & Tiner in American Midland Naturalist (May 1949) v. 41, no. 3. Copyright 1949, University of Notre Dame. Used by permission.

688 THE AMERICAN MIDLAND NATURALIST 41 (3) cannotescape the thought that the males as a resultof theirsmall size were lostin thewashing of the gut with water, according to themethod of helminth- ologicalinvestigation of Skrjabin, or theyburst in thewater and wereuseless forfurther systematic study." SPIRURIDAE 19. Mastophorusmuris (Gmelin, 1790). (17).-An uncommonparasite of volesof thisregion, Mastophorus muris (=Protospirura muris; see Chitwood,1938) wasfound only in southernMichigan, and occurredin only 2 percent of the345 animalsexamined from this study area. This helminth was collectedduring the winter, spring, and summerof 1946. Accordingto Hall (1916) afterLeuckart (1867) andMarchi (1871), theeggs of M. muris are ingestedby beetlesof thegenus Tenebrio, and in fiveweeks encapsulated larvaeare foundin thebody cavity. Baylis (1931) statedthat meal beetles and a cockroach,Blatella germanica (L.), probablyact as the intermediate hostsfor M. murisnear human habitations, but thatother insects probably replacethem in moreremote areas. Whetheror not volespurposely ingest suchinsects is notdefinitely known. Kirschenblatt(1938) statedthe lengthof life of theseworms is com- parativelylong, apparently not less than a year,and that the number of worms doesnot depend upon definite seasons. In the fewvoles infected with this parasite, no evidenceof any patho- genicitywas observed,since neither local lesions nor deteriorated physical con- ditionof thehost were evident. Lesions such as thosecaused by Physaloptera spp.in someof theirrespective hosts were in no case evidentin thestomachs of theinfected animals. The heaviestinfection, with 17 largefemale and 3 maleworms, was observed in a femalevole. Thisanimal, collected on July21, 1946,weighed 63 grams,and contained9 nearlyfull-term fetuses. The average numberof worms,for the fiveinfected animals, was 7.

60 - Andrya macrocephala

p. ~~~~-- Paranoplocephala troeschi

50 -

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JULY AUG SEPT OCT NOV DEC JAN FEB MAR APR MAY JUNE JULY Fig. 5.-Seasonal variationin Andryamacrocephala and Paranoplocephalatroeschi infectionsin voles. Based on 345 volesexamined from the Michigan study area. Rausch & Tiner in American Midland Naturalist (May 1949) v. 41, no. 3. Copyright 1949, University of Notre Dame. Used by permission.

1949 RAUSCH ET AL.: HELMINTHS OF VOLES 689

TRICHURIDAE 20. Capillaria muris-sylvatici(Diesing, 1851). (5).-We know littleso far about thisnematode, which was recordedfrom a singlearea in Wisconsin. We are indebtedto Mr. Clark P. Reed, Rice Institute,for the identification of nematodesof the genus Capillaria. This species was not recordedfrom hostsother than voles. Althoughaccurate counts were difficult,infections with Capillaria muris- sylvaticiapparently consisted of up to about 40 worms. The data given by Kirschenblatt(1938) on membersof the genusCapillaria from Russian rodents mightbe mentionedhere. He gave informationon C. hepatica Bancroft, 1893, in the snow-mouse,Chionomys nivalis Mart., and on C. gastricaBaylis, 1926, in Microtussocialis. He stated (page 30) that "younginfected specimens (of Microtus) weighingfrom 21 to 27 gramswere found only in Feb- ruary;in the rest of the year only old infectedanimals were encountered. Evidentlythe durationof the life of the wormis great,therefore the exten- sivenessof the infectionincreases with age." The same author observeda similarbehavior of C. hepaticain Chionomys(graph 8, page 28). 21. Trichurisopaca Barker and Noyes, 1915. (5, 18) .-Whipworms which belonged to this species were collected fromboth the vole and the

Fig. 6.-Photomicrographof a liversection trom a vole infectedwith Mediogonimtus ovilacus. x70. Rausch & Tiner in American Midland Naturalist (May 1949) v. 41, no. 3. Copyright 1949, University of Notre Dame. Used by permission.

690 THE AMERICAN MIDLAND NATURALIST 41 (3) muskratfrom the southern Wisconsin marsh area, and from a volefrom south- ernMichigan. Of theanimals examined, the voles harbored a largernumber of wormsper infected animal than did themuskrats; however, a much larger numberof voleswas examined. Of the43 volesfrom the marsh area, 11 were infected,while 4 of the 6 muskratsexamined were infected. Infections in theformer host ranged from 1 to 26 (average:9.6) perinfected animal, while in the muskratinfections ranged from 2 to 12 (average:4.6) per infected animal. Recordsof Trichurisfrom the muskratdo not appearto be numerous. Dr. E. W. Priceinformed us thatthe U. S. NationalMuseum Helminth- ologicalCollection has onlya singlevial of whipwormsfrom the muskrat, collectedin Maryland.It appearsto us thatthe vole maybe a moreim- portanthost for T. opacathan is themuskrat. Hall (1916) has pointedout that there is a discrepancybetween the meas- urementsin Barker'sdrawings and text. Throughthe courtesy of Dr. H. W. Manter,University of Nebraska, type specimens of Trichurisopaca were made availableto the writers.Figures 1 and 3 are essentiallycorrect, and are drawnto the samescale, although the cloacal tube of themale in Figure1 was confusedwith the spicule. No specimenscould be foundwhich corre- spondedto Figure2, but it showsmore accurately than Figure 1 thedetails of the posteriorend of the male,provided that the scale (Figure2) is changedto readapproximately ".37 mm." The spicule.lengthgiven in the textshould be correctedto read"1.35 mm." Additionalwork will be neces- saryto adequatelyredescribe T. opaca,and to determineits affinities with other speciesof Trichurisfrom rodents.

22. Trichurissp. (9, 11).-In additionto theaforementioned T. opaca, femalesof a Trichurissp. werecollected from Microtus ochrogaster in Illinois. The absenceof male specimensprevented our determiningtheir specific identity. DISCUSSION AND CONCLUSIONS Fromthe foregoing material, it is evidentthat much is yetto be learned concemingthe helminthsparasitic in voles,to say nothingof the parasites of wildlifein general.However, only long-term studies can makesubstantial contributionstoward solutions of the basicproblems involved. At present, nothingdefinite can be said concerningthe effectof helminthparasites on populationfluctuations of rodents. Duringthe courseof our workwe have not beenable to observeany definiteconnection between population density of volesand parasitedensity. Bothquantitative and qualitativedifferences in helminth infections appear to be seasonalor geographical innature. This opinion is sustainedby the previous workon the helminthsof sciurids(Rausch and Tiner,1948). One is muchimpressed by thelocalized nature of infectionswith certain helminthsover the NorthCentral States region. This is especiallymarked in the case of certainvole parasites,such as Trichurisopaca, Mastophorus muris,Capillaria-muris sylvatici, Longistriata dalrymplei, and Mediogonimus Rausch & Tiner in American Midland Naturalist (May 1949) v. 41, no. 3. Copyright 1949, University of Notre Dame. Used by permission.

1949 RAUSCH ET AL.: HELMINTHS OF VOLES 691 ovilacus.This phenomenonwas pointed out by Kirschenblatt (1938), andwas statedas followsin his summary:"Dabei hattees sich erwiesen,dass die Invasionder miuseahnlichenNagetiere mit Parasiten nicht nur in verschie- denenOrtschaften eine verschiedeneist, sondern sich auch in verschiedenen Kolonienin ein und derselbenOrtschaft unterscheidet. Die Unterschiedein der Invasionder Nagetiereaus einerKolonie werden im Allgemeinendurch die Altersunterschiedeverursacht und hangenvon der Jahreszeitab." He statedfurther that: "Die Helminthen-faunader mauseahnlichenNagetiere in der Umgebungvon Tbilisiist im Friihling(Mai) am reichstenund am verschiedenartigsten,im Sommer (Juli) dagegenam atrmstenund am wenig- stenverschiedenartig. Sommerhitze und Trockenheithemmen die Invasion derNagetiere mit den meisten Helminthen-Arten. Deshalb stellt der Sommer in den SteppenTranskaukasiens eine solche Jahreszeit dar, wahrend welcher die Nagetieresich spontan von den meistenHelminthen befreien." The occurrenceof Nematospiroidessp., Trichurisopaca, and Capillaria muris-sylvaticiin the isolated marsh in southernWisconsin, and theirapparent rarityin the surroundingareas, may be evidenceof environmentalinfluence. The importanceof habitatin the case of certainother helminths is self- evident.As has beennoted by otherwriters, anoplocephaline cestodes occur mostabundantly in animalsfrom areas suitable to free-livingmites; the heavi- estinfections being observed in animalsfrom areas with heavy stands of grass. Withthe exception of Mediogonimus ovilacu;, we were unable to determine thatthe helminths parasitic in voleshad anydeleterious effect upon the host. Evidenceseems to substantiateresults obtained from the studyof sciurid helminths(Rausch and Tiner,1948)-i.e. manyhelminths probably can be consideredinnocuous when the hostis livingin its naturalstate; many of theseshould possibly be consideredmore nearly commensals than parasites. It was notedthat there was a greaternumber and varietyof helminths presentin thenorthwestern part of theregion considered, with fewer in the easternand. southern parts. This wasalso observedin thecase of thesciurid parasites.It maybe thatdrainage and heavycultivation of thesoutheastern partof the regionhas exertedconsiderable influence on someof the vole parasites,which appear to requirea fairlywet habitat. However, the number of hostsso far examinedis hardlylarge enough to allow any conclusions concerninghelminth distribution. Not onlycan new host-and new distributionrecords be obtainedfrom nearlyevery area whereintensive studies are made,but newspecies are also oftenfound, indicating that our knowledge of theNorth American helminth faunais stillquite incomplete. Especially is littleknown of theepizootology of helminthsparasitic in wildbirds and mammals,and in connectionwith this, thereis muchopportunity to makevaluable observations on the basis of season-to-seasonstudies. SUMMARY A totalof 648 volesof threespecies, collected since 1942 from the states of Ohio,Indiana, Illinois, Michigan, Wisconsin, and fromManitoba, has been examinedfor helminth parasites. Special reference has beenmade to host- Rausch & Tiner in American Midland Naturalist (May 1949) v. 41, no. 3. Copyright 1949, University of Notre Dame. Used by permission.

692 THE AMERICAN MIDLAND NATURALIST 41 (3)

parasiterelationships, and detailedinformation has beengiven for two areas whereintensive studies were made. A totalof 21 speciesof helminthswas collected,some of whichare recordedfrom voles for the first time. The helminthspecies encountered have beendiscussed separately in thetext. Informationhas beengiven on seasonalvariation in infectionswith certain helmiths.There is evidencethat season of theyear and geographicallocation havemuch influence on kindand numberof helminthsparasitic in voles. As faras we havebeen able to determine,most of thesevole parasites have little or no harmfuleffect upon the host.

TABLE I.-Summary of Results.

No. ex- No. in- Host amined Parasite fected

Microtusp. pennsylvanicus .. 570 Andrya macrocephala. 59 A ndrya microti.------1 AndryaspF.4------.------4 Paranoplocephalatroeschi .------90 Paranoplocephalaspp .- 32 Hymenolepisfraterna .------1 Hymenolepisevaginata .------2 Taenia taeniaeformis.------43 Cladotaeniaspp .- ...... 13 Quinqueserialishassalli . 21 Mediogonimusovilacus . 2 Entosiphonusthompsoni . 3 Nematospiroidessp. - 32 Longistriatadalrymplei . 3 Dictyocaulusviviparus .-1 Syphacia obvelata 145 Mastophorusmuris .-6 Capillaria muris-sylvatici. 18 Trichurisopaca .------. 11

Microtusp. drummondii.------32 Andrya macrocephala.------.- 1 Taenia sp.- ...... - 1 Syphacia obvelata.------3

Microtusochrogaster .------46 Andrya macrocephala.------5 Paranoplocephalasp .- ...... 9 Choanotaeniasp .-.------.- 1 Hymenolepissp -.- ...... -1 Taenia taeniaeformis .. 1 Cladotaenia sp--... 1 Quinqueserialishassalli .. 1 Syphacia obvelata .. 13 Trichurissp--. .. . --2 Rausch & Tiner in American Midland Naturalist (May 1949) v. 41, no. 3. Copyright 1949, University of Notre Dame. Used by permission.

1949 RAUSCH ET AL.: HELMINTHS OF VOLES 693

ACKNOWLEDGEMENTS The writerswish to expresstheir appreciation of the generouscooperation extended by the ConservationDepartments of Michiganand Wisconsin,which has made it possibleto obtainmany of the animalsneeded for these investigations. The WisconsinConservation Departmentis also supportingthe vole studybeing carried out in the pine plantationof easternWisconsin, some of whichmaterial is includedhere. We are especiallyindebted to Dr. P. A. Hawkinsfor manyhelpful suggestions and otheraid givenin connectionwith the portionof this workdone in southernMichigan. Dr. JohnEmlen and Dr. D. W. Hayne have also givenvaluable suggestions during the courseof thiswork. Severalindividuals have renderedvery valuable assistance in helpingus to obtainvoles forstudy; in this regardwe are indebtedto Messrs.Richard Sutton, L. H. Troesch,C. F. Troesch,R. W. Nero, N. C. Negus, Q. H. Pickering,George Arthur, Paul Springer, JohnGoodman, and Dr. C. M. Kirkpatrick. Dr. Louise A. Scherger,Mr. Felix Hartmeister,and Mr. Lloyd Ottesonhave given muchtechnical assistance. Dr. BannerBill Morganand Mr. C. P. Read have verykindly identifiedcertain of the nematodesencountered. The seniorauthor feels deeply indebted to the late ProfessorAldo Leopold formany valuablesuggestions and encouragementin connectionwith these investigations.

REFERENCES

BARKER, F. D. 1915-Parasites of the Americanmuskrat (Fiber 2.ibethicus).J. Parasitol. 1: 184-197. BAYLIS, H. A. 1931-Notes on some parasiticworms from Norwegian rodents. Annals and Mag. Nat. Hist. ser. 10, 7: 175-176. BLAIR, W. F. 1940-Home rangesand populationsof the meadowvole in southernMich- igan. Jour.Wildl. Mngt.4: 149-161. BURT,W. H. 1946-The mammalsof Michigan.288 pp. Ann Arbor. CHITWOOD, G. B. 1938-The statusof Protospiruravs. Mastophoruswith a consideration of the speciesof thesegenera. Livro Jub. Prof. Travassos, pp. 115-118. DIKMANS, G. 1935-New nematodesof the genusLongistriata in rodents.Jour. Wash. Acad. Sci. 25: 72-81. 1936-A noteon Dictyocaulusfrom domestic and wild ruminants.Ibid., 26: 298- 303. 1940-A note on the generaNematospiroides Baylis, 1926, and Sincosta Roe, 1929 (Nematoda, Heligmosomidae),with descriptionsof two new species of Nematospiroides.Proc. Helm. Soc. Wash. 7: 79-82. DOUGHERTY, E. 1946-A reviewof the genus CrenosomaMolin, 1861 (Nematoda: Trichostrongylidae);its history,taxonomy, adult morphology,and distribution. Ibid. 12: 44-62. DOUTHITT 1915-Studies on the cestodefamily Anoplocephalidae. Ill. Biol. Monogr. 1: 5-96. ELTON, C. 1942-Voles, mice,and lemmings.496 pp. Oxford. , E. B. FORD, J. R. BAKER AND A. D. GARDNER 1931-The healthand parasites of a wild mousepopulation. Proc. Zool. Soc. London,1931, pp. 657-721. ERICKSON, A. B. 1938-Parasites of some MinnesotaCricetidae and Zapodidae, and a host catalogueof helimnthparasites of nativeAmerican mice. Amer Midl. Nat. 20: 575-589. 1944-Helminthinfections in relationto populationfluctuations in snowshoehares. Jour.Wildl. Mngt.8: 134-153. HALL, M. C. 1916-Nematode parasitesof mammalsof the ordersRodentia, Lagamor- pha, and Hyracoidea.Proc. U. S. Nat. Mus. 50: 1-258. Rausch & Tiner in American Midland Naturalist (May 1949) v. 41, no. 3. Copyright 1949, University of Notre Dame. Used by permission.

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HAMILTON, W. J. 1937-Growthand lifespan of the fieldmouse. Amer. Naturalist 71: 500-507. - 1941-Reproductionof the fieldmouse Microtuspennsylvanicus (Ord). Cornell Univ. Ag. Exp. Sta., Mem. 237, pp. 3-23. HANSEN, M. F. 1947-Three anoplocephalidcestodes from the prairiemeadow vole, withdescription of Andryamicroti n. sp. Trans. Amer.Micr. Soc. 66: 279-282. HARKEMA, R. 1936-The parasitesof some North Carolina rodents.Ecol. Monogr.6: 151-232. HARWOOD, P. D. 1939-Notes on Tennesseehelminths. IV. NorthAmerican trematodes of the subfamilyNotocotylinae. Jour. Tenn. Acad. Sci. 14: 421-437. HUGHES, R. C. 1940-The genusHymenolepis Weinland, 1858. Okla A. and M. Col- lege Agr. Exp. Sta. Tech. Bull. 8, pp. 5-42. KALABUKHOV, N. I. 1935-("On the causes of fluctuationsin numbersof mouse-like rodents.Review of the literature.")Zoologicheskii Zhurnal 14: 209-242. (In Russian). KIRSCHENBLATT, J. D. 1938-Die Gesetzmaessigkeitender Dynamikder Parasitenfauna bei den maeuseaehnlichenNagetieren (Muriden) in Transkaukasien.Diss. Univ. Leningrad,pp. 5-92. (In RuLssian,German summary). KRULL, W. H. 1933-The white-footedmouse, Peromyscus leucopus noveboracensis, a new hostfor Entosiphonus thompsoni Sinitsin, 1931; Brachylaemidae.Proc. Helm. Soc. Wash. in J. Parasitol.20: 98. 1939-Observationson the distributionand ecologyof the oribatidmites. Jour. Wash. Acad. Sci. 29: 519-528. LAWLER, H. J. 1939-Demonstrationof the life historyof the nematodeSyphacia obvelata Rudolphi,1802.) J. Parasitol.25: 442. MCINTOSH A. AND G. E. MCINTOSH 1934-A new trematode,.Notocotylus hassalli n. sp. (Notocotylidae)from a meadowmouse. Proc. Helm. Soc. Wash. 1: 36-37. PEARSE, A. S. 1930-The ecologyof the internalparasites of Nigerianrodents and in- sectivores.Jour. Elisha MitchellSci. Soc. 45: 221-238. PRICE, H. F. 1931-Life historyof Schistosomatiumdouthitti (Cort). Amer. Jour.Hyg. 13: 685-727. RANKIN, J. S. 1945-Ecology of the helminthparasites of small mammalscollected from NorthrupCanyon, upper Grand Coulee, Washington.Murrelet 26: 11-14. RAUSCH, R. 1946-Paranoplocephalatroeschi, new speciesof cestodefrom the meadow vole,Microtus p. pennsylvanicusOrd. Trans. Amer.Micr. Soc. 65: 354-356. 1947-Andrya scittrin. sp., a cestodefrom the northernflying squirrel. J. Parasitol. 33: 316-318. 1948-Notes on cestodesof the genusAndrya Railliet, 1883, withthe description of A. ondatraen. sp. (Cestoda: Anoplocephalidae).Trans. Amer.Micr. Soc. 67: 187-191. - AND J. D. TINER 1948-Studies on the parasitichelminths of the NorthCentral StatesI. Helminthsof Sciuridae.Amer. Midl. Nat. 39: 728-747. ROLLINGS, C. T. 1945-Habits, foods and parasitesof the bobcatin Minnesota.Jour. Wildl. Mngt.9: 131-145. SCHWARTZ, B. AND J. E. ALICATA 1935-Life historyof Longistriatamusculi, a nematode parasiticin mice.Jour. Wash. Acad. Sci. 25: 128-146. SPURLOCK, G. M. 1943-Observationson the host-parasiterelations between laboratorv miceand Nematospiroidesdubius Baylis. J. Parasitol.29: 303-311. WOODHEAD, A. E. AND H. MALEWITZ 1936-Mediogoninius ovilactu; n. g., n. sp. Ibid. 22: 273-275.