Universlty of Manltoba

THE HELMINTHOFAUNA OF SMALL BODENTS

IN SOUTHEBN I{ANTIOBA

A Thesis Presented, to the Faculty of Grad.uate Süud-les and. Research Universlty of Manltoba

fn Partlal F\r1fl1lnent of the Bequlremenüs for the Ðegree Master of Sclence

ffi urutvrRs/ryìs ,..# by 0i- tulANlTOBA Brian Blchard. Jaeobsenu ¿'. ¡{+i'r,rr ,-*d 11.

$Errlì.ÄçL

Eleven species of helminths (seven of cestod.es and. four of nematodes) were found in a total of 1081 specimens of five species of rodents from southern Manitoba. Six new host records were established. Focal distributions of cestodes were attributed, to their lif e cycles; a.nd foci of nematodes to the relative abundance of moisture in the habitats studied. Infections of Angrp r¡acrocephala and Capillaria hepatica varied seasonally. No statistic- aI evidence was found of positive or negative correlative occurrence between members of parasite pairs. CapilLeria hepatica was the only rodent parasiie found that is a potential human patnogen. Çuterebra sp. (Cuterebridae¡ Diptera) was found in 5.5% of rodents examined. 1L1 .

ACKNOl^ILEDGMENTS

I would. l1ke to express my sincere gratitud.e to Dr. G. Lubinsky, Associate professor of Zoology, - unlverslty of Manltoba for his assistance and. encourage; ¡nent in this stud.y. I am al_so ind_ebted to Dr. H. E. hlel-ch, Head., Ðepartment of ZooLogy, University of Manitoba, for his val-uable counsel. Thanks are d.ue to Dr. C. tüatts, Departnent of ãoology, University of Manltoba, Ðr. S. fverson of the ÏthiteshelL Nuclear Reaetor at Pinawa, Manitoba and. Dr. M. Levin of the Departnent of Botany, Unlversity of Manltoba. iv.

TABLE OF CONTENTS

TITLE PAGE i. ABSTRACT ii. ACKNOhILEDGI,[ENTS iii. TABLE OF CONTENTS iv. LIST OF TABLES vi. LÏST OF FTGURES vi1. TNTBODUCT]ON I

HïSTORICAL BEVIEI'Í 2

ÐESCRTPTION OF THE SUR\EY ABEAS l+ ïntrod.uction 4 Area I - Disturbed. Grassland. I+ Area ïI - Lakeshore Forest 10 Area ïïI - Backshore Marsh r3 Area IV - Open Fleld.s tt+ Area V - Aspen-Ash Forest 14

MATERÏALS AND METHODS I6 Collection of rod"ents I6 fd.entlficatlon of rod-ents 1B Exanlnation of hosts 18 Preparation of cestod.es L9 Preparation of nenatod.es 20 Tlssue sections 20 Id.entificatlon of helninths 2l Tabulation of data 2T

NOTES ON THE BIOLOGY OF THE ROSTS 26 Introd.uction 26 Peronyscus naFl culatus 26 Microtus pennsylvaniCus dnrnmond.l 27 CJ.ethrLonomys qapperi 27 30 Weo-zÐG-ffienis frrrtectanus 3o

NOTES- ON THE PABASITES FOIIND 37 fntrod-uction 37 And.rya baird-i 37 And-rya macrocephala 3B Paranoploc ephala lnfrequens ¿11 ParanopLoc ephalg variabili s l+z v.

îable of Contents (continued.)

C atenotaeni.a d.end.rl tica r+3 Hyd.ati gera taenlae f orn_i s 44 Taenia mustelae 46 ffialÏã-ffitica 54 Heliguosomum costellatum 63 Hellgnosouum nicroti 6t+ Syphacia obvelata 65

DÏSCUSSION 66

CONCLUSIONS 90 APPENDTX I 9?

APPENDIX Ï] 93 REFERENCES 9:t vi.

LIST OF TABLEg

ï. Previous surveys of the helnlnthofauna of 3 snall- rod-ents in Canad-a and. in the north central United. States.

II. Rodents recovered- fron each of the five 5 biotopes.

If I. Lisf of hosts and of their hel-minths. 2Lþ

fV. Lisü of helninths found. 3L

V. Helninth parasites of rod_ents from various 36 biotopes in southern Manitoba. VI. Record-s of Hyd-atigerg tâeniaeforn_is (Batsch , I+5 t7B6 ) in North Arnerican rod-ents. VII. Cestod.es found. 1n small rod.ents in Canada 6Z and. in the north central United. States. VIII. Nenatod-es found. in snal-l rodents in Canad_a 68 and. in the north central United" Süates. ïX. Instances of nultiple species paraslËisn, 8j',

X. Cases of human infection with Capillaria 8T hepatlca (Bancroft, tAg6).

Xf . Infectlons with Cuterebra in vol-es ln 96, North America during perlod-s of peak abund.ance. vii.

LTST OF F]GURES

1. Map of southern Manitoba showlng the trapping 6 areas. 2. Map of south hlinnipeg showing the Èrapping I areas of the d.lsturbed- grassland biotope. 3. Map of DeLta region showlng the positions of LI blotopes II and- III. 4. Data tabulation sheet. 22 5. Percentage lnfectlon of Mlcrotus pennsylvanlcus 28 d-rurnmond-l with helninths ln Manitoba,

6. Couposlte d"iagram of a volets dlgestive tract, 3l+ showlng the position of helnlnths.

7 . Mature segment of a sterile Andrya ma.crocephala. 39

B. (a) Scolex of a larva of Taenla mustelae. 50( (b) Rostellar hooks of T. mustelae 1,arva. 9. Llver of $icry!,gs pennsylvanicus d.runngnd.l 52 inf ected. wtth 1.anrae of Þggþ mustelae. 10. CJethrionogryg gapperi lorlngl infected. with 56 Capillaria Epg!!c3. lL. Close-up of the infected liver shown in 5B Figure 10.

!2. Longltud.lnal sectlon through Capill-aria hepgticg 6O in liver of Clethrignonys gapperi loringi.

L3. Cross-secülon through Capillaria hepatlca in 6O llver of Clethrlongmys gapperi lsægi.. vlii " I"ist of irigures (contlnued)

14. Seasonal variation in incidence in helmlnth infec- 7L tions in Ülethrionomys, Micfotus, ild Peromyscus in Þlanitoba- during L966 and L967.

L5. Proportion of adults in rodent populations from 73

southern lvianltoba in L967 .

L6. Seasonal variation in incidence of Andrya macro- 75 cephala infections in voles in l.{ichigan. (Rausch and Tiner, L949)

17. Seasonal varj-ation iri incidence in Andrya macro- 77 cepha.Ia infections-'in voles in Manitoba. i8. Seasonal vari-ation in incidence in Capillaria 80 hepatica inf ections in rod.ents from Delta (Area II) in L967. !9. Seasonal variation in incidence in Taenia mustelae 8Z infections in Microtus_ and Clethrionomvs in L966 and I9ó7. TNTRODUCT]ON

The helnlnthofauna of snall rod-ents has been well stud-led- ln the northern United. States and. ln easüern and western Cartada,but little 1s known of rodent helninths ln Manitoba and. Saskatchewan. The purpose of thls work rlüas, therefore, to extend- the knowledge of the d-istrlbution of these helnlnths in Manltoba. The results of this type of survey eire better und-er- stood- lf the habitat and- habits of the host are consldered, as the external environment often influeRees the host and. hence its paraslte tauna. Thls influence of hablüat ls reflecüed- not only ln the number and. variety of helninths lnfectlng the rod"ents, but also ln the seasonal changes of the paraslte faïna. Three other aspects of parasitlsn lfere also exa^nlned-: nulülple species parasltlsn, focal dlstributions of he]- ninths, and the exlstence ln Manitoba of rod.ent parasltes which are potential hunan pathogens. To obtaln the requlred. d.ata, rodents Îüere trapped- in five dlfferent blotopes ln southern Manltoba d-urlng May to Septenber ln ]-966 and. t96?. -2-

HTSTORTCAL REVIEW

The helninthofauna of snall rod_ents has been 1n- tenslvely stud.led ln the northern United. States, but only a few papers on the helnlnühs of Canad_ian rodents have been publlshed- (Table I). Prevlous Canadlan workers (35,46,53,7Q,90) were concerned. wlth either a speclfic rod.ent or a helninth (e.g.Iarval cestod.es). Schad. (89) and. Lublnsky (6Sl studled- the parasltes of several rodents, but gave no d.ata about dlfferences between blotopes, seasonal varlatlon, or nu1tlp1e species parasitlsn. In the Unlted States, Harkema (45) studied_ seasonal varlatlon ln helninth infections of the rabblt, but not of the rod.ents that he examined_. Rausch and_ Tlner (85) also stud.ied seasonal varlatlon, but d-1d not analyse ühe differences beüween helnlnth infections in the varlous biotopes which they examlned.. Kuns and. Bauseh (56) are the only knourn workers who analysed the d.lfferences between biotopes and. thelr influence on the parasltes of voles frorn these blotopes. The remalnlng Anerican workers have provld.ed- only lists of the rodents that they exa"uined. and. the parasites tnat they found-. My stud.y, therefore, represents probably ühe only : stud-y of this type in North Anerica, âs it exanines several aspects of parasltism. -3-

TABLE I.

Prevlous surveys of the helnlnthofauna of snall rod.ents in Canada and, in the north .central Unlted. SËates.

DATE

CAIVADA L933 Mcl,eod (70) Manltoba* 19 5L Knlght (531 Brltish Colunbia J-95,t+ Schad (89) N.E.Quebec & Labrad.or L956 Schad (90) S. Quebec l-957 Lubinsky (6Sl Alberta L959 Freenan and Ïi'Irlght (35) Onfarlo t966 Hnatiuk (46) Saskatchewan

UNITED STATES T9I5 Barker (7) United. States L936 Harkema (4Sl North ÇaroIlna t938 Erickson (29) Mlnnesota l-9t+2 Aneel (3) Mlchigan t9t+8 Bauseh and- Tlner (85) North-central States L9t+9 Ed¡¡ards (?6) New Tork tg50 Kuns and- Bausch (56') ï'Iyonlng l-952 Rausch (80) Alaska 1957 Dunagan (21+) Alaska t953 Read- and Ml1lenann (86) Callfôrnia t953 Slllnan (9LI) Mlchlgan ]955 HaII and. Sonnenberg (43)Mar¡land., Kentucky rg6o Grundmann (39) Utah t96z Lelby (58) Id.aho l-967 Kinsella (51) Montana *Mcleod. studled. only the genus- L+-

DESCBÏPÎÏON OF T}iE SUR\TEY ABEAS

Flve d.lfferent blotopes lrrere selected for this survey in ord.er to determlne how tlne parasitic fauna of rod.ents varies wlth the habltat of the host. These biotopes l^rere d.lsturbed. grassland, lakeshore foresü, backshore narsh, operl fleId.s, and. asBen-ash forest. The cllnate of ühe first three bioüopes is nearly id.entlcal-: the mean July tenperature 1s 68-690 P. and. the mean January üempe:rature 1-2o F. The frost-free season lasts 110-120 d-ays. Average annual preelpitatlon 1s 19-20 lnehes. The climate of the open fleld.s and. aspen- ash forest ls cooLer and. wetter¡ the mean July temperature is 66-6?o F. and that of January-l-Oo F. The frost-free season lasts 100-110 d.ays. Annual precipltation is 2I- 22 inches. These data are taken from neteorologleal record.s of the Meteorologlcal Div1s1on, Department of

i Transport and. are from record.ing sltes as elose as pos- slb1e Èo the collectlon or stud.y sites. The following d.escrlptlons of the trapplng areas lnclud.e Ëhe soiJ-, flora, amd. rodents. The rod.ents recovered. from each area are listed. ln Table II. Botanical nonenclature ls thaË used- by Scoggan (gZ).

AITEA r - pTSTUBBEp GRASgIAND Field.s of thls type were exarnined. at Emerson, Treherne, and. ïIinnipeg (Fig.1) : (a) So11: black and. fine-textured, overlaying a gTêX, TABLE 11. Rodents recovered. from each of the flve blotopes.

AREA ABEA AREA AREA AREA TOTAL ï IÏ TÏT TVV

Mlcrotus pennsylvanlcus d.n¡nnond.l Lt6S 1¿l 125 LL7 3 72t+

Clethrlogon¡i:s g. gapþerL 2 56 58 g. ggppe.rl lorlngi 2t6 ?20 lgægl,Egg g. manlculatus 1B 18 I \¡r B. nanJculatus balrd.l 2l+ 30 I Zaþus h. hud.sonlus I l+ Zapus hud.sonLus caupestris 4 2 6

Napeozapus lnsignis fnrtectanus l_ I

TOTALS L+73 258 Lzg L22 79 1061 -6-

Flg¡rre 1. Map of southern Manitoba showlng the Ërapplng areas.

-B-

Figure 2. Map of south tlinnlpeg showing the trapping areas of the disturbed. grassland. biotope.

-10-

molst cl,ay. Ðrainage T^ras good d.ue to the abundance of ad.joining ditches, (b) Flora: grass (Agropyron repang) and field. nelllot (wtelilotus al-ba) formed. a thick nat on ühe fields. Gold.enrod. (Soltaaso sp.) and. aster (e$ter ericoiges) Tüere common. Cockleburr (Xanthiun italicun) and. Runex crispus l¡¡ere scattered throughout the field.s. Bhus tlrphlna, wild rose (Rosa arkansana) , and- snow- berry (Synphoricarpos sp. ) were found. in localized. clumps. (c) Rod-ents: the maln rod.ent trapped. here was Mlcrotus pennsylvanlcus d.nrnnoEfJ.i (Aud.ubon and. Bachnan). A few specimens of E!@!gon6, gapper! loringl (nattey) and. Peromyscus nanlculatu.s bairdi ( Hay and. Kennicott,) I¡Iere also reeovered.. AREA TT - LATTESHOBE FOBEST This blotope was charactetized. by a sand- rld-ge that runs along the southern ed.ge of Lake Manltoba af Ðelfa. It is essentlally a fl-ood- plain that 1s flood.ed. every ten years (62) (r'ig.3). walker (fo6) d.escribed. fhe flora of the Delta Marsh in 1959, thls was laËer revised by Levln (62) ln 1968. (a) Soil: sand.y loam orx gravel and- coarse sandy beach d.eposits. Drainage is good- on the crest of the ridge and. poor at the ed.ges (b) Flora: the rld.ge is heavily wood.ed with green ash (Fraxinus penngglvanicS) and' Manitoba maple (ecer

-l*J ?-

negundo) ; cottonwood. (Populus d.eltold.es) was scaftered. along the rid.ge. Shrubs r^rere repre_ sented_ bV 7 species of willows (Sa1ix spp. ), choke cherry (PmnuE virglniana) , and. blackberry (Rubus pubescens). Couch grass (Agropyron repans) and. stlnging nettle (Urtlca d.iolca) r{rere the d.onlnant herbs (62). (c) Rod.ents: large populatlons of C. g. fggÞg! and 3. nl. balrdi were found. ln the forest. Snall nu¡¡l- bers of M. p. d.nrnnond.l were found. ln grassy areas of the forest.

AREA IIï - ÞACKSHOBE II{ARSH A portlon of the Delta marsh near the Unlversity of Manltoba Field. Station comprlsed. Area III. This was a backshore marsh separated. from Lake Ivianitoba by the sand_ rld.ge and lakeshore forest. (a) Soil: thin nuck and. peat d.eposits overlaying varlable glacf-al d.rift d.eposlts. The d.epËh of peat coverlng the mineral soil is var1ab1e, but 1s usually relatlvely th1n. Sone portions become d.ry as summer progresses. (b) FLora: the d.onlnant plant specles here is whitetop (Scholochloa festucacep) with late d.oninance by Sonehus arvensis. 3-I¡g4!!5, oomnuæ was scattered. throughout this portlon of the narsh. (c) Bod.ents:dense populations of lvl. p. d.rrnnond.l were found. In 1966 along with a feio C. g, slr¡gi. and -1¿l-

Zapus hud.sonlus carnpestris (preble) . Trapping failed. to yield any rod.ents in L96?.

AREA IV - OPEN FIELDS

These are sinllar to those of Area r, but mral and. situated. 1n the nlxed transltl or'!. zorle of eastern Manitoba at the hihiteshel-I Nuclear Reactor Establlshnent at pinawa (Fig.1) . (a) So11: the topsoll 1s d_ark and. covers a layer of elay. Drainage varies fron poor to good.. (b) Flora: the grass cover (Agropyron sp. ) was tall and. thick. sed.ge (carex spp.) occurred. in wetter areas. htl-llow (Salix sp.p.) was found. in the wetter fleld.s and. aspen (populus trenuloid.es) ln the d.rler. (c) Rod.ents: large populatlons of g. p. d.runmondl ¡¡ere found.. A few C1eührionomys gapperl gapperi (Vlgors) and Zapus hud.sonlus hud.sonlus (Zinner- nann) lrere also trapped..

ARNA V - ASPEN-ASH FOBEST Thls was situated. at Plnawa along the eastern bank of the Whiteshell Blver. (a) So11: sane as Elnat of Area IV. Drainage 1s good_. (b) Flora: heavlly wood.ed. with aspen poplar (populus trenulold.es) and ash (Fraxlnus sp. ). i,fhlte blrch (getula papyrlfera) and- bur oak (euercus macro-

carpus) were also present. Herbs T4rere represented -r5-

by polson ivy (nfius radlcans), sï¡aüp raspberry (Ar¡bus pubescens), and. wild strawberry (Fragarla virgLniana).

Peromysel¿g manieulatus manlculatus (Wagner) T^rere

found. wifh a few M. p. d.rtrnmond.l. One speclmen each of Z. þ. hud.sonius and. Napeozapug lnslgnis frutectanus (Jackson) were caughf. -t6-

MATEBIALS ATüD METHODS

COLLECTION OF RODENTS ïn ad.d.iü1on to personal ürapping ln Areas I, IIrand. III, rod-ents were obtalned. fron Dr. C. tfatts of the University of Manitoba Field. Statlon at De1ta, from Area III, and. fron Dr. S. Iverson of the TrlhlteshelL Nuc- lear Reactor at Plnawa fron Areas IV and. V. fn each lnstance the nethod.s of trapping and. preservatlon of material were d.ifferent, and. these w111 be d.escribed separately:

Personal lrapplgg: Three types of traps were used.: ' (a) Vlctor M-I snap traps with metal trlggers baited. with a mixture of peanut butter and. oatmeal (12), or plain oatneal. Both baits gave satisfactory results, though plain oatmeal was easier to store and hand.le. (b) Sherman live traps baited. wlth ühe above baits. These were metal box traps wlth sprlng d.oors: length ltt , ' wid.th Jrr, helght Jrr . These traps couId. be used- only ln spots shad-ed- fron the sunas they becane hoü in d.lrect sun- 11ght. (c) Metal cylind.ers 12'r 1ong, $n in d.ia^neter, open at one end. and. lnserted lnto the ground- flush with surface and. baited with peanut butter and. oatneal. This trap was patterned. after one d.eveloped by Buchner, Ig55 (11). Snap traps T4iere used. the nost often. Death was due usua11y,tobreakageoftheneckorspina1co1umn.No -I7 -

d.anage to viscera occurred. exeept ln a few casesrand. even then the parasltes were not harued.. A d-isad.vantage of the snap trap was tkraþ captured. rod-ents could. be carried. off or eaüen by pred.ators. This occurred. only in a small pereentage of cases: the head. was the only portion of the bod-y left in the trap; the d.igest- ive tract was lost. Care was taken to conceal the traps

so that they rrrere noü carried. off by bird.s of prey and. cror^rs as happened- 1n one fleld. in south¡resüern llriinnlpeg. The traps ¡¡ere placed. so as to obtaln the largest number of rod.ents: saturaüion ürapplng. The traps were placed. either ln long ror/vs along d.ltches, or in checker- board. fashlon at intervals of 5 to / yard.s 1n field.s. Traps 'hrere placed. In nearby runT,uays or suitabl-e looking spots. the end.s of each rorlr were rnarked. v,¡lth 3/8 incyt d.ianeter Oowels ll8 inches long with strlps of coloured. cloth attached- to the top. The traps ütrere inspected. in

early mornlng and. in evenlng, the rod.ents removed. and. placed. ln plastic bags, and. the traps rebalted.. Eaeh f1e1d. was trapped. for one ¡¡eek at a tlme. The rod.ents were brought to the laboratory and. sprayed wlth the lnsecticld.e rrBaidrr to k111 any ecüoparasites. If the rod-ents could. not be d.issected. lnned.iately, they were placed. in a 0c' .F. freezer in order to fteeze then as qulckly as possible. Material from Dr, C. Ïlatts: These rod.ents were trapped_ nalnly wlth Shernan live traps, placed. ln palrs at lntervals -18- of thlrty metres for populaüion stud.les; snap traps were also used- occaslonally. Anlnals captured. alive were kllled. by a sharp blow to the head., and. either frozen or preserved. in 15% forna11n. Aninals preserrred. 1n formalin r/vere üore d.ifflcult to examlne for helninths as the internal organs beca"ue rigid. Frozen aninars Ï¡ere satlsfactory for helninthological lnvestlgatlon though histological examinatlon showed. thaü the cells rÁrere d.a.naged.. Materlal fron Dr._S. Iverson: Museu¡n speclal snap traps baited. with a ¡alxture of peanut butter, oatmeal and bacon were used.. Trap llnes T4rere set out accord.ing to the nethod. of the Internatlonal Sna1l Mam¡nal Census. The anlmals were skinned. first, tagged., and. then frozen. Helnlnths Ìqere not d.a^naged. 1n all three nethod.s of trapping.

IDENT]F]CATION OF RODENTS Rod.ents were ld.entified- by eaclt collector. Those collected by nyself rôrere ld.entlfied. b¡r uslng both Peterson QÐ and. the Crid.d.le collectlon of the Unlversity of Manltoba Zoology Department. Bod.ents fron Pinawa were identlfied- by Dr. S. Tverson using Gund.erson and. Beer ( þ0 ) , Peüerson (7 5) , and. Bailey (6) , Dr, I¡,Iatt r s sources are unknolins.r

EXAMÏNATÏON OF HOSTS After the rod.ents were sprayed. to k111 ectoparasltes, -r9 ov after frozen speci¡nens had. tharried., they T,vere placed. ventral sid-e up on a d.issecting board., and. a mld-ventral lncislon nad.e fron the urinary papilla to the throat, and. skin reflected. to each side

A piece of abd.ominal nusculature was flrst removed- and. exanlned- for Trichinella by means of a.com- pressorium and- a d-issecting nlcroscope. The subcutane- ous tissue was then exanlned. for larval helnlnths, âs were the lungs, Iiver, spleen, raesenteries and. kldneys. The d.lgestlve tract rr¡as removed. and. placed in a 2.5/" aqlreous solution of IISCI'. The tract was sllt lengthwlse with flne scissors and exanined. for helminths. The intestinal contents were exa^mined. wlth a d.lssecting microscope on a black background.. Helninths were placed. and- into fresh MgCl.¿ solutlon al1owed. to relax and. d.ie. Cestod.es, after d.eath, rrrere conpressed. slightly between two mlcroscope slld.es and. fixed. in F,A.A. (l+0% formald.e- hyd.e 7-J c.c., )J/" etinanol 85 c.c., glaclal acetlc acld 5 c.c.). Encysted. cestod.es and. nematodes T/'rere fixed. ln F.A.A. or I0/" formalin.

PREPABATTON OF CESTODES The ad.ult cestod.es were: 1) washed. ln waüer to remove fixative, 2) transferred- to a Petri d.lsh wlth Ehrlichts haenatoxylin whieh had. only half the nornal amount of staln, 3) stalned- for twenty-four hours, -2O-

b) destained in acid. alcohol, 5) bLued in runnj-ng tap water, 6) dehydrated. in an ascending series of alcohol, 7) cleared in xylene, and 8) mounted in Per"roount. a nunrber of different mounting media were tried: Dpx, HistocJ-ad, crystalite, and Permount. The last gave the leaat shrinkage upon drying Encysted cestode larvae were removed from ùhe cyst and. cleared. in 851/o LacÏic acid U.aSçP¡* for twelve to twenty-four hours; the acid arso dissolved the carcareous corpuscLes. The larvae Èhen were praced on a slide in a drop of ractic acid and fl-attened by gently pressing the conerslip.

PREPARATIoN 0F NEI{ATOpqs Nematodes v4iere praced in a Lo'/t solution of grycerol Ín absolute alcohol Ín a syracuse watchglass. The watchglass was covered with a glass plate permÍtting the ethanor to etaporate slowly during three üo four weeks, leaving pure glycerol. Excellent resurts were obtaíned. by this method.

TISSUE SE, CTIONS Tissues hrere embedded. in paraprast and sections cut of 6-10 micra. These sections were stained with either Malroryis Triple stain, Ehrrichts or Heidenhainrs haema- to:cylin, -?t-

TDENTTFICATION OF HELMTNÎHS

Herninths were id.entlfied- using tlne zoology of Tape- ïrorns (108), the Nenatod-e parasltes of vertebrates (Lrz), original literature and. d.rar¡¡ings, and. eomparatlve speclnens,

TABULATTON OF DATA The species, sex, âg€ of reach rod_ent and. the presence and. posltlon of any heluinths were record.ed in a field. manual and- then üransferred. to a data sheet (Fig.4). -22-

Fig¡.lre 4. Data üabulatlon sheet. -2?-

Number

Day Rod.ent Species

Cesüod.es (Uo. ¡

Nenatod-es (No. ¡

Lari¡a]- Cestodes

Other Parasltes

Cuterebra (Uo.¡

þf9,OH o5o oP.Pct |' F'-t o $) çt H. o 5 o r-å

o H 'ErH. 5 5(+ vt

s) pË 5 Ë H (t'' o r-J

Flgure 4. -24-

TABLE TTT

L]ST OF HOSTS AND OF THE]R HELMINTHS

RODENTÏA

Fanily Crlcetid-ae Subfanily Crlceüinae 1) Peronyseus manlculatus b?lrdi (Hoy and. Kennicott) Capillarla hepatlca (Bancroft, L896) Subfanlly Microtinae 2) Ivlicrotus pennsylvanlcus d.nungond.i (Au¿ubon and. Bachnan) And-rya bairdi Schad., L954 A. macrocephala Douthltt, LgI5 Paran_oplocephafa infrequens (Douthitt,,l-9I5) E. variabilis (Douthitt,LgIs) Hyd.atigera taen-laeformis (Batsch, I?86) Taenla nustelae Gmelln, l?gO Caplllaria hepatlga (Bancroft, 1896)

Hellsmosonum cosjellalun (DuJard.ln, 1845 ) g. nicroll (Kuns and- Rausch, J-950) Syphacla obvelalg (Er¡ao1phi, 1802) 3) Clethrlogonys gapperi gapperi (Vigors) Angrya baird.l Schad., 1954 A. macrocephala Douthitt, \915 Catenoüaenia d"end.rlt1cg (Goeze, l-TBZ) Taenia mustelae Gmelin, L790 Capillarla hepatig (Bancroft, l-786) HeligErosonug nlcrotl (Kuns and. Bausch, l95O) Syphacia obvelata (nud.olpht, 1802) -25-

TABLE III ( continued,)

¿l) clethriononys gapperi lori.ngi (Bailey) And.rya nacrocephalg Douthitt, L9I5 Çatenotaenla {çpQ¡flige (Goeze, 1782) Laenla mustelae Gnelin, l-790 _?6-

NCTES Ti\i THE BIOLOGT OF THE HÛS.IS One thousand and sicty-one rodenis of five speci-es (eight subspecies) were examined. The f oll-owing section

gives brief notes on each of' these rodent species. The parasi.tes oí each host are l-isted in TabLes rrr and. rv¡ Additlonal findings on Peromyscus maniculatus baird.i are gi¡ren in Appendix f . Cricetidae

Peromuscus (tfagner , ]lg/5) Deer Mouse Two subspecies of this rodent were found in southern Manitoba: Peromvsçqs maq-rcgþ!-us maniculatus (ïüagner) at Pinawa, and PeromrÞcus maniculatu.s bairdi (Hoy and Kenni- cott) at Ilelba and in the disturbed grassl-and area (its typical ha.bita.t) of i'.innipeg and i,vestern lrtanitoba. Both subspecies wore restricted üo treed biotopes or to fields bordering on groves of Þopla.r. >pecimens of P. manicul-atus trapped in t,his survey were free of intestinal parasites (se,e rrppendix r), but 3 out of 24 specj-nens taken in the LakesÌiore i-orest were infected with the l-iver paraøite, capiiraria hepatisa. schad (89) also did not find iniestinal p:rrasites in pero- ntyscus from northeastern Quebec and Labrador, but found nerna-i,odes in Peromyscus .from the ivt;.,cÐonaid college -trbore- tunr in southern Quebec. Lubinsky (65) and F'reeman and !üright (lS) found !. irepatica. in p" m¡¡niculatus in Al-berta a-nd in rrlgonquin Park, Onta::io, respectively. rt is not clear why intesiinal parasites are so scå,rce i¡r this host. -27-

Mlcrotus pennsylvanicus d-rr¡mmond.l (eudubon and. Bachman, LB1U) Corynonly cal1ed. Dnrnnondrs nead_ow vole, thls rod.ent r^ras nunerous 1n open fieldsrand r:are 1n wood.ed. areas. . Ten species of helninths rlrere found. in 23.4ft of U. p. d.nrnmond.l (Fig.5). The nost frequent cestod.es lnfecting this host were Taenla nustelae (9.2%) and. And_rya macrocephala (9.I%). SyI¡hacla obvelata and. Helignosonuq nicrotl were the nost frequent nematod.es (?.0%). Seven out of 46J specinens of U. p. d.rummond.i from the 'tllinnlpeg area ürere infected_ wlth one to seven cysts of Hydatigera taeniaefornls. Four of 14 speclnens fro¡a the lakeshore forest at Ðelta T¡rere lnfected. with Capillarla hepati_ca. The flnd.ings of And.rya balrdi (0.5%), Capillarla hepatlca (0.6%), amd Heligmosonu¡ costellaüun (0.3%) in U. p. d.runmond.i are ne¡r host records.

Clethriononys gapperl (Vigors, 1830) Two subspecles of the red. back vole ?üere exanlned: Cle_thrlononfs gapperl e;apperi (Vlgors) at Plnawa, and. Clethriononys gapperi loringl (¡ailey) at Delta and. l¡,Iinnlpeg. Three species of cestod-es rrere found. in g. g, gapperi fron Pinawa: And.rya macrocephala, Çatenot?enla gendri-tica, and. Taenia nustel-ae; no nenatod.es ürere found.. These three eestod.es along wlth And.rya baird.å ?üere found. in 9. g. loringl at Delta, âs T¡rere the nematodes Capillaria heplica,, Hellgmosomun nlcroti, and- syphacla @. The findings of And.rya Þ$!i, Capillaria hepatlca,and HelleEngsgnwu microti ln C. g. forlngi are neï¡ host records, -28-

Figure 5. Percentage lnfection of Mlcrotus pennsylvanicus d.nrnnond.i with helninths in Manitoba. ft Infecteð.

g. nustelae

A. uacrocephaLa P. infrequens

I t:d g. oblrelata N) H' \o 0s I Ë ¡-j nlcrgtl o E. \^ E. taeniaeformls g. hepatica

A. balrd"å

AT II . costellatum P. varlabilis -30-

ZapodLdae

Zapus hud-sonius (Zinnelma;rT'rrt, 1?80 ) Zapus hud.soniug hud.sonius (Zinner¡nann) was taken at Plnawa in open field.s and. aspen-ash forest , zapug hud.sonlus canpestrls (Preble) at Delta in the marsh and. lakeshore forest. All ten speclnens collected. were free of parasites. Erickson (29) found" two specles of neuatod.es ln the intestine of Z. hud.sonir¡s. Freeman and. Wright (35) found. Capil-Laria hepatlca and- larval Taenia uustglae in the 11ver of thls rod.ent.

Napeozapus lnslgnls frruteetanus (Jackson) Only one specimen of this rare rod.ent was taken from an aspen grove at Plnanrla. It was free of parasltes. Free- nan and. !'Irlght (3il found. one lnfection of N, lnsignls wlth Caplllaria hepatlca in Algonquln Park, Ontario. -3L-

TABLE TV

LIST OF HELMTNTHS FOUND

CESTODA

Ord.er Cyclophyl-Iid-ea Braun, 1900 Faully Anoplocephalld.ae Cholod_.kovsky, lg1z Subfa"¡nlly Anoplocephalinae Blanchard., 1891

f ) Andrya balrd.i Schad., l95l+ Clethrlononys gapperi loringi - sna1l intestlne; Delta. New host record. Mlcrotus penËsllvanicus drunnond.i - small lntestine; I,rlinnipeg. NeT¡r host record.. 2) Andryg uacrocephala Douthitt, l9]-5 Cl-ethrlononys gapperl gapperi - snall intesüine; Pinawa. ClefhriononyE gapperÀ loringi - snall intestine; Delta.

Ml_c_rotus pennyslvanicus d.-nrnnond.å - snall intestine ; Delta, Plnawa, Ì,Iinnipeg. 3) Paranop_looepha.Ia lnfrequens (Douthitt, 1915) Microfus pennsylvanicus drumnond.i - lleocaecal Junction and- caecun¡ t'Iinnlpeg. 4) Paranoplocephal-a variabil-is (Douthltt, L9l5) Microtus penng¿lvglricus È889.49i - ileocaecal junctlon and. caecum; lrllnnipeg. Famlly Catenotaenlidae Ward.le and. Mcleod-, 7.952 5) Catenotaenia dendrltice (Goeze, I-TBZ) Clethriononys gapperi gapperi - snall intesülne; Pinawa. Clethrlonomys gapperi loringl snal-l lntestine¡ Delta. -32-

TABLE IV (continued)

Family Taeniidae Lud¡oÍg, 1886 6) Hydatigera taeniaeformis (Batsch, 1786) (Iarvae) MicrotEs pennsylvanicus drummondi - l-iver; trrlinnipeg. 7) Taenia mustelae G¡re1in, L79O (l-arvae) Clethri-onoml¡s gapperi gapperi - liver; Pinawa. Clethrionomys Êapperi loringi - liver; Delta. Microtus pennsylvani-cus drunmondi - li-ver; Delta, Pinawa, hlinnipeg.

NEMATOÐA

Order Eunematoda irüard, L9L6 Superfamily Trichuroidea Railliet, L9I6 FamíIy Trichuridae Railliet, l-gLS Subfamily Capillariinae Railliet, L9I5 8) Capillaria hepatica (Bancroft, I896) Clethrionomvs sapperi loringi - liver; Delta. lvlicrotus pennsvlvanicus d.rummondi - liver: De1ta. New host record. Peromyscus maniculatus bairdi - líuer; De1ta. Superfamily StrongyloÍdea lfeinland, 1858 Fanily Trichostrongylidae Leíper, L9I2 Subfamily Heligmosominae Travassos, I91¿l 9ù Heliemosomum costellatum (Dujardin, I8l+5) fficrotus pennsylvanicus drummondi - small interbine; Pinawa. New host record. -33-

TABLE IV (continued)

IO) Heli.gmosomum mÍcroti (Kuns and Rausch, I95O) clebhrionomys gapperi loringi - duodenum; Delta. New host record. Superfanity Ox¡rroidea Railliet, L9L6 Famity UxYuridae Cobbold, 18óL Subfanily Syphaci-inae Railliet, L9L6 11) Syphacia obvelata (nudolphÍ, 1802) clethrionomys Eapperi loringi - caecum; Ðelta. Mierotus pennsylvani-cus d'rummondi - caecum; Emerson and WinniPeg. -3t+-

Flgure 6. Conposite d.iagrarn of a volers digesfive Eract,, showing the position of helninths. I I ¡------LlVgf: Ir/

¡ U) t¡t I

Small inüestine ,32 cm, ) : A-C ß cm. ): e ostell at um H.Fellsmosomqg nicrotl nrp lF-õil)

dat D- - L nfre oue ns

Caecum (2.j cm. ) : Svphac la ob vel at a

Flgure 6. - 14!tF_v

Hel¡ninth parasiües of Rod-ents from Various Biotopes in Southerrr lvianitoba

AREA Ï AREA I] AREA ]II AREA IV AREA V Parasite and" Host Disturbed. Lakeshore Ba.ckshore Cpen Aspen-Ash Grassland- Forest Marsh Field-s Forest

IT of N int" of N fr int, of N /" inf " of N /" inf " of /" into ft

Cestod.es Andrva bairdi M" 'o.l d.:rummond-l o.?t a o4%"'r 465 -- 9" €. ].oringi 2,6! r;/" 216 A" macrocepha]a J J - Lþ65 12 Br r25 6. Bt 2 tt? 33,3t?7 ,2% 3 lT 1) o d.rr:mrnond-i s,3! ,y z5.o[tt "6fi rl+ " 3.0% ú/" Co" Ao gaPPeri L2.9! 2'3ft 216 C. Ao loringi z|.t# S tuø 56 pa.iranõptãc q e@_ f r e ugqs I'f. þo d-nrmnond-i ? "3! L.2% I+65 P, variabilis- I I{n þn d-rumnond-i o,zt o.z% 465 L^) o\ Catenotaenla. d.endritica -L ga"'operi I.?L I"7% 56 I C" A. @ C. Ao ].oringi 1"93 a.9% ?L6 sv¿atleela ffiformis o t+65 I't. þ' d.run¡nond-i 1"51 "6% Tagria np,slel-.ae t 1+.3[-L d-nrrnmond.i g.0t L.3ft 465 18.7t t{ r25 r"gft l17 . .L ----1t1. 1). : 2 56 Cn A. gaPPeri J. "L+/" g. go loringi I.gT o "g% 216 Nematod.es Caoillaria hePatica M' 1). drumnoi1d]. zB.6*::z,t% at+ Lvz 2L6 g" go lorlngi " 5i 3.1+:% P. $e baird.i 12 ,5! 6 .B% 2Lt, He]-imosorotm ffielratum = tr? I1.'o" d.rr.Ln¡aond-i 1,?t L2% H. a]"croEl- -ffi d-rrurnmond-i 10.6t 125 9' .$' ]--o.ringi 0, gt 0 "6% 216 ^rr Svphacia obvelata J _-- o +65 i\In þ. d-:r.lmmondi 2 êl+,: "7% -t. g' g" ]-or-i,ng.i 1. g: o ,9/" 216

Stand.ard error = _37_

NOTES ON THE PABASITES FOUND

Eleven species of helminths infected. the rod.ents exa:nlned.: seven of cestod.es and four of nematodes. rn this chapter will be dlscussed. my find.ings, prevlous find,lngs in North Anerica, and the taxonouy of each parasite. (lhe posltion of each paraslte in the host is glven ln Flg. 6)

CESTODA

1. And.rya baird.i Schad-, I95L+ Find.lngs 1n southern Manltoba:

hllnnipeg: M. pennsylvanlcus 3 of 465 rc.?%) Delta: C. gapperi lorlngi 3 of Lt? Q.6%) No. of ind-ivld.uals per host: I Location in host: snall lntestine A. baird-l was d.escribed fron M. chrotomhinus 1n northern Quebec (89) but has not been reported. since. The flndings of A. baird-l in M. pennsylvanlcus and e. galrperi are therefore nerv host record.s. å. þ!3g¡ is sinllar to And.rya prinordialis Douthitt, L9l5 ln having unilaterally arrangeð, genltal pores, but 1t lacks the prostate gland- which was d_escrlbed_ in the latter species by Douthitt. Rausch (80) saw a prostate gl-and- in A. prinord-ialls. 4. bairdi may be a junior synonym of A. primord-iaIis as Douthltt (23) may have nistaken an enlarged external seninal vesicle for the prostate gland. In ny naterlal this veslcle was often greatly d.istend.ed. with speru or looped- over itself , and could- be -38-

rnistaken for a prostaüe gland.. An exarninaü1on of ma¡ny specimens of both specles is necessary to solve thls problen. 2. And-rya nacrocephala Douthitt, l-gl-5 Flnd.ings in souühern Manitoba:

trriinnipeg: M. peng€ylvani,_qlrs 43 of 465 ( 9.3%) Delta3 g. g. loringl 28 of 216 (J'}.g/"') Plnawa: 9. g. gapperl 14 of 58 (23.3%) U. pennsylvanicus 7 of 120 ( 7 .5/r) No. of indlvlduals per host: 1 13 Locatlon in host¡ snalI lntestine A. macrocephala ls the nost connon cestod_e of mlcrotine rod.ents ln North America. Its hlgh morpho- loglcal variability has Ied. to the d-escrlptlon of several species wlth overlapping characteristics

(Rausch and Schl1ler (Bþ), Rausch (BO¡ ). The tf,pe ..¡,:r' host of A. uacroceBþIa is Geonys bursarius. In l-gJ-s, Douthitt (Zl) described- A. transl-ucida fron the sane host. Kirshenblat (52't Oescrlbed A. caucasica from Mlcrotus socialis and Crlcetulus nlgratoriug ln lrans- caucasia. Kirschenbläût subd.iv1d.ed. the genus And.rya into two subgenera: And.rya and Apostand.rya, placlng in ühe latter the species A. gæIgggBþþ, A. translucid.a and. A. 999.3Ê@. In l-9l+7, Hansen (¿!¿p) descrlbed a. nicrotl frou M. ochrogaster; in 19¿18, Bausch (77) d.escribed A. ond.atrae fron Ond.atra zibethlcus; and Soltys (99) d.escrlbed. -39-

Figure 7. Maüure segment of a sterile And.r.va qAgroc ephal_a. -¿lo-

Flgure 7 " -4r

A. blalowlezensls fron Mlcrotus arvalls 1n poIand.. Bausch and Schiller (84) regard.ed. A. mlcrotl, A. ond"atrae, and_ A. caucasica as junlor synonyns of A. nacrocephalg. Rausch (8e¡ in r95? showed. tyøt a. bla- lowlzensls is norphologically id-entlcaL with A. nacrocephala and ad-d-ed it to the list of synonyns of A. nacrocephala. Rausch and. schlller (sÀl) found- tha"t certaln indi- vld.uals of A. nacrocephàla are sterlle and. their proglotüid.s becone elongated due to the absence of ova (Flg.Z). This can be explained. by the following: the uterus of A. nacrocephala 1s a transverse sac; when 1t 1s ful1 of eggs lt exerüs a lateral pressure and. the proglottids become wid.e and. short. tühen the proglottid" is sterile, no lateral pressure is exerted and. it becones elongated.. Two speclmens of A. nacrocephala ln one M. pennsyl- vanleus extend-ed" into the stomach. This may have been d.ue to movenent of the worns after death of the host or to antlperistalsls in the norlbund. aninals. 3. Parangplocg'ohala infrequens nouthitt, IgI5 Flnd.lngs in southern Manitoba:

!ülnnlpeg: M. pennsylvanicus 3I+ of 465 Q. j%')

No. of ind-lviduals per host: 1 7 Location in host: ileocaecal Junctlon and. caecum In the present survey P. infrequens was found_ only in the greater lflnnlpeg aTea, and. only in I[. pennsylvanlcus. Anoplocephala lnfrequens, A. variabills, and.

oF ê,1Áilf'roÐa -42- bitis borealis Ìüere d-escribed by Douthlüt In L9I5 from Geomys bursarius in Minnesota (23) . He also record_ed. A. variabllis from Evotomys (CleühriononyE) in North Dakota. In L927, Baer (tl) placed. the above three species ln the genus ParanopLocephala, aïd. at the sane tlne syno- nynized. P. variabiliE with P. lnfrequens. Rausch (?6) d-escrlbed. P. troeschl fron M. pennsylvanlcus in Mlchlgan and- Ohlo in l-946. (Bausch gave two üype locall_ties for thls cestod-e. ) In l-94?, Hansen (¿l¿+) reestablished- P. variabills as a valld. species on the basls oî a skirt- like projecüion of the posterior margin of the proglot- fid.s of P. lnfrequens. Bausch and. Schiller (B¿l) regard.ed. B. froeschl as a junior synonym of l. infrequens and raised- P. variabllis borealls to ful} speclfic rank as tt E. borealig. Rausch (80¡ reassessed. the posltlon of Åa borealls and- conclud.ed., ir¡ L952, that it was Itonly a stage in the growth of P. varlabllisft. þ. lg@ocephala varlabllls Ðouühitt, tgt5 Find.lngs ln southern ManiEobiat Itinnipeg¡ M. pennsylvanlcus 1 ot 465 (0.2/,) No. of lndlvid.uals per host: 1 Location 1n host: lleocaecal Junctlon The taxonoulc posltion of !. varlab1l1s was alread.y d.iscussed- in the section d-eallng with P. infrequens. P. varlabills showed. the sane peeullarities wiüh regard. üo loealitles, hosts, aïd. location in the host. Rausch (80) showed. Ln 1-952 that P. variabills varies consld-erably ln size wlth age. Unfortunately, üÍ naterlal was insufficient _t+l_

for fhe stud.y of thls varlabil-ity. P. varlgbllis was reported. fron hosts other than Microtus: Synaptonys eooperl fron southern Ïl-Ilnois (80), Thomouyg talpold.es from Mlchlgan (BO) and. Al-berta (65), Dicrostogyx hud-sonius fron Labrador and- northeastern Quebec (89), and. Phenacomyx inte¡med.ius fron Alberta (65). 5. Catenotaenia d-endrltlca Goeze, l-782 Flnd.lngs ln southern Manltoba: Delta: C. gapperi lorlngi Lt of 2t6 (l.g/") Plnawa: C. g. gapperi 1 of 58 (I.?%) No. of lnd.ivid-uals per host: 1 6 Locatlon in host: snalI lntestine lhis cestod-e was found. only 1n Clethriongp gæE5!. Table VII shows tfÞt C. d.end-rltlca ls to sone extent spe- ciflc for this host, though it was reported. fron Peromyscus maniculatus by Leiby (58) from Id.aho in lg62 (see also Append-lx I), Thls paraslte ls rare (81), but nay occur frequently in sone foei, âs shoum by Schad. (89). Catenotgenia den9rltica was d.escrlbed. from Sclurus vulsaris ln Europe (38). In 1941, Mclntosh (69) d-escrlbed. g. linsd.a1el fron Callfornia pocket uice and- kangaroo rats (69). Schad (89), afËer conparlng ¡neasurenents given by Joyeux and. Baer (l+8), Yanaguti (111), Mclntosh (69), and. Voge (105) conclud.ed. that C. linsd.alel Mcfntosh 1s a junlor synonJrm of g. d.endritica Goeze. g. d.end.rltica exhibits consid.erable morphological varlation. Bausch (79) stated. that rrin varlous anoplo- cephallne genera, lnclud-lng Catenotaenla, the lack of -Ltl+-

constant characters, for exanple rostellar hooks, nakes it necessary to pay partlcular attentlon to varlation when specific d.lfferentlation is attenpted.. fn Cateno- taenia 1t would seem ad.visable to consider the state of strobilar contraction, as the relatlve positlon of or- gaïs are often greatly lnfluenced. by this. Any 1ot of naterial consistlng of strobllae elther uniformly con- tracted. or relaxed. could. convey an impression whlch nlght lead" þo an erroneous conclusion ln regard. to spe- ciflc c}:aracterizatiotilt . Differences in norphology caused. by contractlon or relaxation of the cestod.e nay also account for the wid.e norphologlca1 varlation reported in And-rya macrocs¡phala. 6. Hyd.atigera taeniaeforuis (Batsch, l?86) Flndlngs in southern Manitoba¡ Irrllnnipeg: M. pennsylvanlcug d.ruumondi 7 oî 46J 0"5/r) No. of lnd.ivld.uals per host: r7 Locatlon in host: liver Hydatlgera taenlaefgrnls is a cosmopolltan parasite frequently found rrear hunan habitation. The ad.ult worm parasitlzes house cats, feral cats, and musteLlds. The l-arva is found. in the I1ver and. ln the mesenteries of rod.ents, and seld-on in the spleen (101)" It is a stro- bilocercus enclosed" in a large, yeIlowlsh cyst, 10 to 15 nlllimetres in d.laneter. ft becomes infecülve after slxty d.ays of growth. The occurrence of H. taeniaeformis in North Anerlcan rod.ents is summarlzed. 1n Table VT. TABLE VT Record.s of Hyd"atlgera taenlaefornis (Batsch, r?96) rn North anerlcan rod.ents

HOST DATE AUTHOR LOCALTTT

Mus nusculus Lgog Mccoy (68) Callfornia r9J.9 Hall (42]' rrUnlted Statest' l-936 Harkena (45) N. Carolina 19sll HalI and Sonnenberg (41) Maryland. 1957 Lubinsky (65) Alberta t963 Lublnsky x Manltoba

Battus norveglcus I tgtg Hall (locelt) (t+2) rrUnited Statesrr È Ln L936 Harkena (t+5) N. Carollna I L9slt' Hall and. Sonnenberg (lÐ) Kentucky Ond.atra zlbethlcus Lg32 Law and- Kenned.y (57) Ontarlo Lg42 Aneel (3) Mlchlgan t949 Edwards (26) New York tg 5t Knlght (53) Brltlsh Colunbla L958 Lublnsky x Quebec (tte Perrot) Hicrotus pennsylvanlcus L938 Erlckson (29) Mlnnesota t9t+9 Rausch and" Tlner (85) North Central States l-967 Klnsella (51) Montana Selurrrs carol-lnensis t936 Harkena N. Carollna Ë. nlger L934 Dobrovsky and Harbough (ZI) Kansas l.g30 Martin (6?) Nebraska -Lt6-

7. Taenla mustelae Gnelin, I?90 Find.lngs 1n southern Manltoba: Ï,llnnlpeg: U. pennsylvanicus 4Z of 465 ( g.O%) Delta: C. g. lorlngi LV of 216 ( t.a{¡ U. ÞennsYlvanicus 23 of L39 u6.6%) Plnawa: C. g. gapperi Z of SB ( j.3F") g. pennsylvanicrrs J of 1,20 ( l+.2%) Location ln host: liver Goeze (38), in I?BZ, found_ a d.elicate tapeworn 1n the broum weasel, but d"ld. not name it. He also found. tapeworms 1n the ferret and narten. Gnelin (36), in 1790, oh the basls of Goezets d-escription establlshed- a neÌû specles, Taenia nustelae, and regard.ed. the cestod.es fron the weaser (Muslela vulgarls), ferret (l[ustela Tlutorlus), and the marten (Mustela nartiE) as cospeclfic. In 180J, Zeð,er (1f3) established. a neT¡r genus, IÏalys1s, wlth type specles of E. mustelae, arrd. assumed. th,aþ Ëhe cestod-es fron the narten and. ferret r^rere separate species, naning then S. martls and. H. putorli. Rudolphl (BZ) described. ln 1810 as ¡rarned. cestod.err, Taenra inüemed.ia fron t'I{usÈela @gt' and stated. that thls species has large hooks. He regard-ed. G¡nelin¡s d-escription of !. nustelae as insufficlent, but thought tyLat Gmelinrs cestod.es may have been 1d-ent1cal to hls T. inter- B.g!þ. He also regard.ed. as 'tspecles dubiaetf T. putorii (H.putorii ) and t'!. Mustelae glfg@t' . Nlne years later, in 1819, in his trEntozooruu synopsis'r, Budolphi (BB) sunmarized. the literature on _L+7 _ g. interned.ia and. on unarued. cestod.es from mustelld-s, and. d-escribed. Taenia brevlcollis fron Mustela ermlnea,and. g. tenulcollis from t'@þþ PutoLiifr and. t'SEgþþ Vulgaristl Thus, Btrd-o1ph1 bel1eved. thiÐ,E at least three species of cesËod.es occurred- in mustelld.s, one with rostellar hooks, and- two unarmed. il Kuchenmeister fn L955 (54), found. in mice an unarmed- larval- tapeworn whlch he naned" CysticercuF lnnonlnatus hypud-aei-. In L856, Leuckart (61) pointed. out thtat thls was probably the larrra of g. tenuieollls of mustelld.s. Two ll years later, Kuchernmeister (55) found. this cysticercus in the 1lver of Talpa europaea, and- showed. tkrat Cyslicercus ta]-pae, Rud.olphl 1819n a d.ublous species fromthe same host, and. believed. to be hookless by Bud.olphl, had. hooks and. was 'to il probably id.entlcal C. lnnominatus, bIE@$, Kuchenmeister L855. In 1910, Thlenenann (fO3) reexanined. Rud-olphits type speclmens of ad-uIt cestod"es from nustelidsin the Vienna lf Museum, and. agreed- wiüh Kuchenmelster (55) and. LeucJr'art (61) thaü T. lgter$ed"la has relaËively large and character- istic hooks, and. 1s read.lly d.istinguishable from both T. tenulcoII_ig and T. brevicollls. Thlenemann also stud.ied. Bud.olphirs type specimens of Cystercercus talpae and noted- thelr slnilarity to adult T. tenuicollis Hudolphl, l8lp and I. brevicollls Bud.,1819. Baer (5), Ca.neron and- Parnell (1/), and. Joyeux and. Baer (48) regard.ed. T. Eg!g$þ as a junlor synony¡n of g. tenuicollis. The fact that the -/+8- hooks of !, tenuicollis drop oíf easily had led to the oplnion that this species was unarmed. Therefore, Joyeux and Baer (l+8), Ln L934, regarded ån armed cestode which they founci in weasels as a new subspecies, T. tenuicollis EË. årmata. In LS10, Rudolphi described a larval cestode from cattle which he named Cysticercus lggufgoll-i-g. Hughes (l+7), in 194I, pointed. out that the specific name of T. !Bn¡ri_q-o.Uj-s Rud,;r'r1819 is pre-occupied by Cystlcercus a"***"U. 1810, and proposed therefore for T. tenuicollis a new name - Taenia jp¡1e¡¿5iana. In 1956, Ireeman (ll+) reviewed the 1ùterature on cestodes from mustelids and stated that, according to the laws of priority, the valid name for Èhe smaLL-hooked taeninoid cestode of the European brown weasel is f. mustel-ae Gmelin, L79O. Larvae of I, mustel"ae vüere first reported from North America by Skinker (97) in 1935 from the liver of Ontario muskrats; she also found the adult worm in mink. Ïn 1942, .Aneel (3) found T. musgelae larvae in muskrats fronr southern and central Michigan. Rausch (80), in L952, corrected identificaLions of larvae to !. mustelae which he had pre- viously described as Clgdotaenia in Michigan and Alaska n8, 85) and added Clethrionglnys gutilus dawsoni-, Lemmus lrimucgonatus alascensis, and iviÍcrotus miurus !.apçêþ! from Alaska to the list of hosts. Locker rc3) reported l-arvae of T. mustelae frorn Micro- tus oecomomus in 4,Jaska, Ondatra z_f@higus- osoyoos-ensis, _t+9_

g. pennsylvanicus uodestus, and. peromyscus nanlculatus artgnislae 1n Montana; the mountaln beaver Aplod-onlia rufa and !. nanicul-atus rubid.us 1n oregon. she arso found the adul-t cesüod.es in Mustela erninea invicþa and. Mustela vison in Montana.

Freeman (34) examined. 1562 rod.ents fron ontarlo and- Michlgan, attd. found. &6 lnfected. wiüh f . nusterae. These were Citgllgs frar:kl1n1i, Eutanlas mininus, $ryþ monax, Tanias striatus, ilethrlononys gapperi, Mlcrotus penE- sylf'anicus, Peronyscus sp., Peronyscus manlculatus, Synapt'omys cooperå, and- Zapus hud.sonlus. Two l-arval forns of g. ¡austelae with dlfferent hook lengths infect rodents; these are often called. the European and. North Amerlcan varieties. The European varieËy has hooks wiÈh a!1 average length of 2O u. The J:arvae which

Bausch (78,85) at flrst nlsid.entified. as Clad_otaenla had. hooks either 16 or 20 u 1ong, This r,ras the flrst report of both types of larvae in North American rod_ents. f also found. both forus ln Manitoba rod.ents. At De1ta,

only the European varieËy was found., while at pinawa and. üIinnlpeg both varieties r4rere present. The neasurements of the larval hooks (Fig.B) were as follows: A. Larvae with large hooks:

No. of hooks exanined- z 3l+5 (11'5 scoleces ) No. of hooks per seolex: l+0-56 (nean r+6.3) Mean lengthr 22.I ! 0.1 u ...... :1:.. . ..: : . ..:..: ...., :

-50-

Figure B. (a) Scolex of a larva of

Taenla nustel-ae ( x IZJ ) (b) Bostellar hooks of

g. uustelae larrra ( x 550 ) -

Fig. I (a).

w,.ë # '"&.{:

Fig. I (b). -12 -

Figure 9. Liver of Microtus pennsylvanicus d-rtrnnond-i lnfected wifh larvae of Taenla nusüelae ( x 2 ),

-54-

B. Larvae with suall hooks: No. of hooks exanined z ?3 e scoleces) No. of hooks per scolex: LlZ ana bh Mean length: ].6.6 ! 0.1 u A s-fest showed. that in ny naterial no signiflcant difference existed in the hook lengths of the two rows in either forn of larvae (z= 0.J-5UZ) . An unusual feature of g. uustelae ]p¡vae- ls that the large-hooked. variety is a cystlcercus (ffg.9) r^rhereas the snall-hooked. rarvae can be either cysticerci or coenuri¡ i.ê. either uniscolex or nulüiscolex larvae. Previous authors (i4, 63', gz) d.tscussed. this phenonenon in detail. Freeman (34) found. th¿-t, uniscolex larvae, fed- to nink, greT,r lnto adults whlch prod.uced. rarvae of both types.

Of the seven sma11-hooked. larvaê lnfections, one was unlscolex, six nultiscolex. unfortunately, only two of the coenurl had. scoreces wlth fu11y-d.eve1oped. hooks.

NE}4ATODA

B. Capillaria hepatica (Bancroft, fB96) Findings in southern Manltoba:

Delta: M. penns¿lvanlcus 4 of l-39 ( Z.gF") g. g. lorlnsl 103 of 218 (t+Z.S%) P. maniçqtatug 3 of 24 (1,2.5%) No. of indlvid-uals per host: inpossible to d.etermlne Location in host: liver This paraslte was d.iscovered" in 1896 1n the liver .JJ

of a rat and naüed Trichocephalus hepatlcus. In IpI6, Hall (&r¡ created- for it the genus Hepaticora. rn L931,

Baylls (B) reexamlned. the morphology of H. hepatica and. showed. that lts generic clnaracteristlcs coincid_e with those of the genus capillarla, and tLtat ühe creaüion of a neT¡¡ geÌlus for 1t was unjustifled.. Flrlotte (33) found C. hepat:þa in broi¡nr rats on the samplls of Macdonald college, euebec. LaT¡r and. Kenned.y (57) reported. trte patasite ln nuskrats ln ontarlo. Free- nan and. Trfrlght (35) f ound. it in Cleührlonouys gapperi, Migrotus p. penEsylvanlcus, NaI¡S¡ozapus insignls algonquln- ensis, Ondatra zibethlcus, Peronyscus 4aniculatus and. Synaptomys g. cooperl. ïn Manitoba, C. hepatis¡a was found. only in rod_ents trapped- along the Delta sand. rid.ge, and d.id. not occur in those collected. in the nelghbourlng Delta marsh. Calle (16) recently reported the l1fe cycle of g. hepatica as d.irect, requiring only a single hosü whose liver contains both the ad.ult parasltes and, thelr ova (¡'igs.10-13). The cycle starts when the host d.1es, d.econ- poses, and. thus l-lberates the ova, or when the host is eaten by another aninal tlnat passes the und.lgested ova in the faeces and. d-issemlnates them in the soil. Und_er favourable cireurnstances the ova enbryonate wiüh1n J0 days, and. become infectlous. The life cycle is conpleted when aninals or nan becone infecüed. by ingesting food contaninated- with the embryonated. ova. Following inges- - 5o-

Figure 10. C_lethfriononys gapperl loringi infected with CæiÏtar,ig hepatica.

-58-

Figure 11. Close-up of the lnfected. llver shown in Figure 10 ( x Z ).

-60-

Figure 12. Longltud-inal secfion through Capil]-aria hepg¿t_ica ln liver of Clethrionouys gapperl lorineå ( x 100)

Figure lJ. Cross-section through Capill-arl.a Ltepatj.ca 1n liver of Clethrlonouys gappsrrl loringl (x500) -6t-

Fig. J-2.

Fig. 13, -62-

tlon, the juvenlles hatch ln the intestine, penetrate into the intestinal wa1I and. nigrate to the liver vla the portal ve1n. a few juvenlles may pass the porÈa1 filter and- be carried. to the lungs, kid.neys or other organs. In ühe llver, the Juveniles mature and. nate withln approxinately one nonth. Thousand.s of ova are d.eposited in the llver and remain there untir the d.eath of ühe host. Accord-ing to Freenan and. tfright (35\, infection takes place in the winter with the release of eggs fron the liver d.ue to cannibalism as a result of starvatlon. Fig. L7 lnd.lcates that infectlon d.oes not þake place 1n the winter buü in late July and- Augusü ln Manltoba. fnfec- tlons are heavy in the spring (i.e. large nunbers of worns), light in nid-suülner, and. heavy in autumn; I d.id" not f1nd. lnfectlons of Peronyscus until september, l:96?. The intenslty of infection may be d-irectly proportional üo the nunber of infected. lndivid.uals ln the rod.ent population. Freernan arid. Wright (] 5) stated: t'The d.aþa fron A1- gonquin Park are in narked. contrast to those collected by Pavlov in Russla. In L952 awö. L953 he trapped_ uice fron July through Septenber and found. a strlklng rise 1n the incid-ence of g. hepatica in the young of the year aü the beginning of september. Pavlov conclud.ed. ühat variatlons in the lncid.ence of this parasite, anong the three species of rodents that T4rere infected., were d.ue partly to the _63_ kind.s of food.s eaten and. partly to where they lived. since mlce 11ving in a flood. biotope lnaö. a higher incl- d.ence þ}:an those in a d.ry biotopê... the incid.ence of Peromyscug naniculatus (in ontarlo) varles directly wiüh the d.ensity of the hosü. The eggs must be released. from an infected. host by cannibalisn.t'

9. Helignosonun costellatr.¡_u (DuJard.ln, lB¿15) Findings ln southern Manltoba: Pinara¡ M. pennsylvanlcus ? of 120 (L.Z%) No. of ind.ivld.uals per host z 2 - 4 Location in hosü: snall intestine Heligmosomun costeLlatun 1s a comnon parasite of European voles,occurring ln all vegetational zones 1n Europe. In Norüh A.merlca it was reported. only from I.llyonlng (56), Alaska (80), and. Montana (5I). fn hlyoning, Kuns and Bausch found. this nematod.e in alpine and. sub- alpine meado¡rs, and. not in the lowland.s; Klnse1la (5I) reported. H. costellaüun from one Mlcrotus longlcaudus near Mlssoula, Montana. Although Kinsella d.oes not d-escrlbe the biotopes in which he Ërapped., they lle ln the Bitüerroot Mountains, and- lt ls probable that this nenatod.e was found. in a blotope sinilar to thet reported. by Kuns and. Rauseh. Erhard.ova (28) found. this parasite in all vegetational zones of the High Tatra Mountains aî Czechoslo- vakia. Jn the Jeseniky Mountalns, Tenora (100) found.

H. costeLlatum ln the uountaLn zone; he also found. it _64_

1n the alpine and- subalplne zones of the Liptovske HoIe Mountalns in Czechoslovakia (101). In Manitoba, E. costellatum was found_ only 1n open field.s at Plna¡ra. The flnd.lng of this nematod.e in Mlcrotus pennsylvanlcus d.runmond.l is a new host record..

10. Helignosolnun nicloti (Kuns and Rausch, L950) Flnd-ings in souühern Manltoba: Delta: U. @ 14 of t39 {.l-}.L%) g. g. lorinel 2 of 216 (0.9%)

No. of ind.ivld.uals per host z 2 5 Location 1n host: snal-l inüestlne

He-llgmosonun g@LL vûas first d.escribed. fron trùyon- 1ng voles as NenaËgspiroiges microti (56). It is a smaIl, spirally-coi1ed., blood--red- nematod.e inhabitlng the an- terior end" of the snall intestine. It differs from other species of the genus in the length of its splcules which are 2.OB 2.20 mm. long. Skrjabln, Shikhobalova, and. Shul.tts (98) in I)J4, placed. Nenatospiroides 1n the genus Hellgnosonum. E. microti was not includ.ed. in the revision of the genus Heliguosouun because of lack of conparatlve material. N. nlcrotl was placed. in this genus only in l-96? by Kinsella on the basis of exanination of a large materlal. In Manitoba, I found. H. mierotl only at Delta. Its find-ing ln Cletlriononys ggpperi lorlngi is a new host reeord.. -65-

11. Syphacla obvel-ata (Rud_olphi, 1802) Find.ings 1n southern Manltoba: De1Ëa¡ g. g. gapperi 4 of 21.6 (I.9%) Irlinnipeg: M. pennsylvanicus Al of 465 Q.4%) Emerson: M. pennsylvgnieus 1 of 1 No. of lnd.ivld_uals per host: 1 Z (fenales only) Location in host: snall lntesüine and. eaecum Syphaclg obvelata occurs usually in large numbers in a high percentage of rod_ents. fn the Unlted. States, this parasite is comnon; in Canad.a, 1t was found. only by Schad. (89i ln northeastern euebec and- Labrad.or. Schad (90) also found. a closely related. species, g. peromysci, iri BLI'.2% of Peromyscus naniculalus in southern Quebec. Rausch (80) reported. þhÐt Ë" g@þÞ is a common parasife of microtine rod_ents in Alaska. -66-

DISÜUSSIQN

Seven species of cestodes ¿nd four of nematodes were found in the present survey. 0n1y two of these r4rere presend in aII fise biotopes; Andrya macrocephala and Taeni.a mustelae:. The other parasi.tes were found in either one or two biotopes. Tables VII and VIII show that in the areas of Nor:þh America chosen for comparison, 19 species of cestodes and 24 of nematodes have been found in the genera of rodents examined in l{anitoba. The parasites found. in southern lVianitoba have already been reported from one or more areas of Canada and the north- central United States where surveys of this type have been conducted. The parasti.e fauna of southern l\'lanitoba rodents has only one unexpected omissi-on, the absence of the cestode HymenoLepis horrid.a. It wilt probably be found in Mani- toba rodents as it has been reported from several adjacent areas (tabte vrr ) . Foci of iglection: i-ocal d'istributions (i'e' areas with very high frequencies of occurrence of a parasite) were found of the cestodes Paranoplocephala ilgqque.rìsr B. variabilis, and Sdatigera taeniabformis; and the nematodes Capillaria hepatica, Ileligmosomum costellatum, and $. microti, No Íoci of other parasites rnlere found. The intermediaie hosts of che two species of Paranoe plocephala are unknown and no speciÍic reason can be given TABLE VIT

Cestod-es Found- ln Snall Rod.ents in Can^ad.a anð. the North Central Unlted. States

€ s Í.{o Ê -E € d qq o õ b d bo o +r qp .d o rð e Ë È' Ð fr Sq ${ o o .d o õ .ã r{ ql LtÞ-1* d+ .!t .Ç^ S1. S^ {5^ H^ ç FF| QGo.l 1ì:{ 'qq õ¡* õv-r Fo1 H¡ õ¡9 .d. r-lo d .æ Éc"t Þ-O\ ötJ-\ ,Ãæ- fiñ ör¡ hùi na?rocç8ry+e cu cM 4. pl.iTordig.tls crq M M M 4.. u I c c c p c O. Pte4oPenþdend.rttlgaçnoanoüa"enia peromyscl p { ¡ 9-. rp: Clad.otaenia globlfera nÞ ntr C. uirsoevi C MMMM evaslnata åivngnolglrsH. ftatetna - M .hI.- norrr-da M c c cM M @lnfrequeng M M M M M M P.variabilis M M M ParuffiãlFauschl nÞ M M Taenla V¿ nustelae CM CM CMp CMPZ p CM

C: Clethrlononys qapperi P: Peromyscus naniculatus IVls ][iCrOtUS SPP. ál tapu"s hud-sonius -

- TABLE VITI

Nenatod'es Found- ln snall Bod.ents ln canada and. the North central unlted states

"Ð o d ${ C) g .p do o p d od@ 'l)r{() d C) b0 ØÉc od-oHF{c) d 5 .rl od.;{ Fl G "q P.t¡cr .o C) a FË8 .rl :.!. o Þr aJner].caïa + e CMP P cw7, . nurls-syl-vatlca¡a;m""- 1cüyocaulus P M viv M I eliglnosomì.lm c o\ cosEe @ . M M M I .d-ublus M . nlcrotl CM M IiI ilonffiEa o.ar-rymþr-er- M Ivlastophorìrs ¡uur1s cz M t{ Monllifornls sp. ¡-Þ NJp:ffipFEññ'ffilus sp. D¡ Pelodera sp. CM Protospinra nurls c P. numidlca P Et o1 clffiñÏã-c orad.ens 1 s M P f7 Spiuracerca zaÞL ZJ ffis Z Syphacla obvelata CM M peronysci M MCM M M g. P P S. saJîorod"inl I-ï) Trichurls or,aca- M M _69-

for the foei of these two parasltes in the d.isturbed. grasslands. The flnd.ing of Hydatigera taenlaeformls only ln the d.isturbed. grassland.s of hrlnnlpeg probably ls d.ue to the restrictlon of the d.efinltive host (¡'elis donesticus) to areas of hunan habitation. Nenatod.es r¡r1üh focal d-istributions found. in this Sunrey have d-lrect 1ife cycles. Local conditlons favourable to the survival of infective eggs and. larvae strongly influence the occurrence of such parasltes (56). Kuns and. Bausch (56) found- t\'øt, 1n the cases of Hel1eng-

sonurn cosfellatun and. H. mlcrotl trpermanent d.anpness and. coolness. . .wou.ld- perhaps account for better survival of nenatod.e eggs and. larvaer'. Rausch and. Tiner (S5) found. that abund.ance of vole parasltes (both cestod.es and. nenatod.es) d.epend-s upon nolsture. The blotopes where Capillaria hepaticg and- Helignosomun T^rere found. were danp. The effect of d.a"npness 1s best illustrated. by the üwo species of Heligmosonum. At Delta, two ad.Jacent biotopes were stud.ied.: backshore marsh and. Iakeshore forest. A statistically hlgher infection rate for H. m:þ¡ioti was found. in the marsh than ln the forest *""u d.rainage was good.. Siullarly, at Pinawa, H. costellatum was found in vol-es inhabitlng d_anp fleId.s but not ln voles 1n the ad-joinlng and. d.rler aspen-ash forest. These observations supporü the opinions expressed by Kuns and_ Bausch, and. Rausch and. Tiner. -70-

SeasonaL bariation: My data show that the frequency of helmj.nth infections of lvlanitoba rodents varies from month to month, and year to year. Tiris depends upon numerous factors, such e.s seasonaL a.nd annuar variations in the density of the host populations, and the l-ife cycles of the parasites. The high i-ncidence (percentage of infected animals) of herminrhs durlng lvlay (I¡ig. l-4) is;orobably due to a persd-stance of the previous autumnrs j-nfecti-ons. The steep fall- i-n June reflects the large numbers of young rod.ents (uninfected) in the populations stud.ied (l¡ig. I5). A rise in incidence occurred in July, L966 and a prateau in July, 1967, when the first young rod.ents became infected.. The drop in incidence in mid-summer is probabry caused by the great proportion of young i.n rodent populations at this time of the year. These young became infected. in l_ate summerr âs shown by the abrupt rise of the curve in August- Spptember. rf sampring were carried out during the winter, the highest j-ncidence probably wour-d be found in the period. November to April. Elton, lord and. Baker (ZT), in 1931, studied infections with i{glirorosomum dgbir.¡m of Apo4emus syrvaticus, the cld iiiorld counterpart of peromysçus. They found a peak in the first quarLer of' the year, and a low in the thÍrd quai'ter. My results resembre those of Elton, i'ord, and Baker.

seasonal variation in rodent parasitism has not been -7+-

!.igure li¡. seasonar variations in incid.ence in her-minth

infecÈions in crethriqnomvs, Microtus, and Peromvscus in tr4anitoba during 196ó and :t967. -72-

+ 1966 r00 -A- I 9 6 7

80 I t I ì E 7C) I c, \ I u o óo

..- 50 N 4,o

0 MAY JUNE JULY AUG S E PT

Flgure 1Il. -73-

îiì'igure :-'5. Proportion of adults i-n rodent populations

from southern l,lanitoba in L967 . -71+-

CN E:{ t-¡ â \q&0

MAY JUNE JULY AUG SEPT

Flgure IJ. -75- ',¿

Irigure 1ó. Seasonal variation in incid-ence in Andrya nacrocephala infections in voles in Michlgan after Rausch and Tiner, L9l+9. c o {r 30 o o rÞ .: o\ 20 ! { O. I

JASON DJ FMATIIJJ

Figure 16. -77 -

'irigure 1/. sea.-sona-L va*iaiion in incidence in Ancirya macrocephala infections i-n voles in i^a_nito_ ba" 50 o tg66 -A- 196? 40 E o Þ 30 ¡ \l u @. o I r¡ 20 a: ï__¡_Í a à-e t0 Â--r-rr-_r.__{a

0 MAY JUNE JULY AUG S EPT Figure 17. -79-

T/ìrel1 studied. 1n North a:nerica. Rausch and- Tiner (BS) in 1949 conducted. a su::rrey of Microüus sp. 1n the North central unlted- states. They chose a 23 acre fleld. in I{ichigan for extensive stud.y. Three hund.red_ and. forty_ five voles were removed. at a uniforrn rate for thirteen monfhs. rf we conpare Bausch and. Tinerrs curre for And-ryF, nacrocephala (Fie.r6) to ours (Fie.!,3), üre see t]:aþ they are slnllar. Their results and. nine tor l'96? show increases in incld.ence fron May to July. My l'966 results are sI1ght1y dlfferent in t]nat no helninths r{ere found. ln August, though 6f voles ürere exanined.. The above three curves show marked_ sinllarlty ln the period. Au.gust to Septenber. Differenees between my results and. those of Rausch and Tiner can probably be attributed. to d.ifferlng age composition of the rod-ent population. Freenan and. hiright (35) stud.led. seasonal variations in the occurrence of caplllari? hepatica ln rod.ents in Algonquin Park, Ontario, ifi f956 (fa¡le IIf , p.3?Z). Although thelr sanples T¡rere taken from several areas and were smaII, the authors stated- that r' lf age structure of the Peromyscus nanigulatus populatlon ls ignored., there is a pronounced. d.ecllne ln incid.ence fron May through sepfemberrr. such a d.ecline 'hras observed. al_so in Manitoba (Fig.18). rt end.ed. in august, however, and. was foIlowed. by a sharp rise in incid_enee in Septeuber. Harkena (l+5) stud.ied. seasonar variation in the paraslte -80-

Figure 18. seasonal variation in incidence in capirl-aria hepatica infections in rodents from De1ta (Area rI) in L967. -81 -

r 00

70 ! g 3 óo c 50 N 40

o M AY JUNE JULY AUG S E PT Fieure I 8. -82-

Figure 19. seasonaL variations in incidence i-n Taenia mustelae infections in Microtus and clethrionomys ín 1966 and L967. 30 -a- 1966 -(t o -A- I 9 67 ! +24 @ I l'¡) o I 'l .: l0 -- -- -A__.\t. \ N -lli , MAY JUNE JUIY AUG SEPT Flgure 19, -8,l+- fauna of rabbits (Svlvilazus floridanus mallurus) from October, L933 to August, L93b. He observed peaks in April or May for Cittotaenia pectinata. Trichostrongylus affinis, and !. calcaratus. ttNo seasonal variation for Hasstilesia tri.color, Hymenolepis dinínuta, larval tape- vtorms, Trichosomoides crasaicauda and Heterakis spumosa uras demonstrated.rl Boughton (10), ln L932, reported that in lrlesteBn Canada, snowshoe rabbits develop an almost complete re- sistance to Cittotaenia ¡'¡ith a change in diet in late July and August to fruit and berries. As was pointed out in the section dealing with Capillaria hepatica, Pavlov concluded that infections with ühis nematode ürere correlated to some extent with the dieü. Seasonal variations in incidence of infection with Taenia mustelae (Fig. 19) were not found. It may be concluded that seasonal changes in helninth infections are due to: age composition of the rodent popula- tj.ons, sources of infecti-on, and probably changes in diet.

Uultiple species parasitism: In thÍs survey, several instances of multÍp1e species parqsitism r^iere found (taUte IX). A maximum of four helminth species was present in one host. Pavlovski (22) applied the term parasitocoenosis to the entire parasite population of one host. Dogiel (ZZ¡ stated: trthat the entire quantitative and qualitative copposi- tion of the parasÍte population of various hosts is determined TABLE IX

Instances of lir.iltiple Species Parasitism.

Number of Speci-es of Parasites Host 123 l+ Tota1

27 Glethrionomys gar¡peri- Il+5 104 I 1 278 I @ \¡t Microtus pennsj¡Ivanicus 553 Lt+4 tg 7 I 721+ I

Peromyscus maniculatus )+5 3 48

TotaIs: 7 t+3 25t 46 1050 -8b-

not onry by the ecorogical factors and conditions which the hostr âs the micro-environmemt, has to offer, but also by the character of the interrelati.ons between the indivi- dual species included in the parasitocoenosis. Ehese lnterrelations are Ín some Ínstances antagonistic, the presence of some species preventing the occurrence of members of another. l{hen the rerationship is of a synergistic charadter, one parasite increases the chances of the existence of thr other.tl To test for these two effects among the helminths of Manitoba rodents, the observed cases of infection with üwo species of helminths vúere compared statisticalry with the expected number of cases. 0n1y in the Andrya macrocephala - capilLaria hepati.ca parasitocoenosis Ì,.ras a significant difference found between the expected and observed, infections. This positive eomel-ation can only suggest the presence of synergism: the hÍgh infection rate with Capillaria hepatica in one biotope will influence the results of a statistical testr âs it is so much hÍgher than that of Andrya macrocephala (approximately 3 times as great for Clethrionomvs gapperi, the dominant rodent in the lakeshore forest). Synergism and antagonism can be stûdied only exper- imentally (ZZ). Positive and negative correlations in the occurrence of parasite pairs may depend. upon such factors as the use of the same intermediate hosts, habits of the definltive or intermediate hosts, and. rocal envir- _öòq t_

mental- infl-uences on eggs and larvae.

Rodent parasites as human pathogens: 0f the parasites found in this survey, only capilraria hepatica 1s a potential human parasite, According to Calle (f6), genuine and spurious human infection wÍtþ this parasite should be care- fully distinguished. rn genuine infection the parasites are present in the liver- where they deposit theír ova. clinical manifestations of infection develop, but the ova are not passed in the faeces. rn spurious infection, the ova are simpry passing through the digestive üract following the ingestion of an i.nfected liver. rn the chagres River region of Panama, nine cases of such spurious infections with c. hepatica were found among ffO persons exa.mined (3t). An- other report from the same region (lZ) mentions 1ó spurious infections among the 19¿l persons examined. Two cases of spurious infeGtion ürere described by McQuown (Tzt in r,ouis- iana, in patients who aüe gravy made from squirrer rivers. Genuine human cases of hepatic capíllaríasis are listed in Table x. 0f the eight cases, sÍx were diagnosed at necropsxr and the remaining two (those from soutb Africa and North carorina) by biopsy. One survÍvor was treated. with dithiazanine iodide (Uelvex), and the oüher received. no therapy. The absence in southern Manitoba rodents of Echino- coçcus mul-tilocul-aris which uses rodents as intermediate hosts and whieh is highly pathogenic to man, is noteworthy. -Bg-

TABLE X

Cases of Human Infection with Capillaria hepa-tiga

LOCALITT AUTHOR AND BEFERENCE lgTt+ Ind ia MacArthur (66) L95O Louislana, U.S .4. McQuown (72) l95l+ Maryland.¡ U.S.A. otto et aI (74) Ig5t+ Turkey îrhan et al (10ll) W56 Hawali Ewing et aI (:O) 195? Johannesburg, S. Africa Cochrane eþ al (19) lg59 Loulslana, U.S.A. Iliard et a1 (fO7¡ :196l North Carolina, U.S.A. Calle (16) _89_

This cestod,e was reported in L952 by Rausch (80) from Microtus oeconomus from St. Lawrence Island in the Bering Sea; by Rausch (Sf) from Arctic foxes from Resolute Bay¡ CornwaLlis Island.; by Choquette et al (18) from EskÍmo Point, North Ilrjest Territories; Ln L964 by l''eiby and olsen (óO) in Red foxes in North Ðakota; by Leiby $9) tn L965 Ín Microtus pennsvLvaniçgq and Sg,rnIgU. maniculalhrs, also in North Dakota. Recently, Hnatiuk W6) found it in an U. pennsylvanícus in Saskatchewan. one would expectt therefore, to find $. nultilocularis in Manítoba rodents. Despite the examination of 1061 rod.ent livers from southern Manitoba, I was unable to find it. -9o-

COi\ùCLUS]ÛNS 1) trlleven species of helminths (seven of cestodes and four of hematodes) were found in three species of Manitoba rodents. 2) Ten specimens of Zapus hudsonius examined were free of helminths. 3) The findings of Andrya bairdi, Capillaria hepatica, and Helignosomum coste]latum 1n Microtus pennst¡lvanicus dIqEgA!{i represent new host records. [) The findings of And.rya bairdi and HeliernEsomurq microti in ClethrÍonomys gapperi- loringi represent new host records. 5) The helminthofauna of rodents from different bÍo- topes varies both in the number of species present and Ín the incidnece of infection. The disturbed grassland and lakeshore forest areas had seven species of helminths each" whlle the other areas had three each. Andrya macfo- cephala and Taenia mustelae were the only parasites common to all five biotopes. 6) l-oeal distributions of cestod,es are probably due to the presencer or absence, of the other hosts involved in the parasíte life cycles. iioci of nematodes, however, are most lii

7) A focus of CCBlltaria hepatica was found in the Delta l-akeshore forest, where +7.5/; of Cfethriotto*uu gappe_ri l-oringi were infected. 8) Seasonal variati-on in the percent infection of rodents was studied in L966 and 1967. This variabion üIas attributed to age composltúion of the rodent poputa- tion and their feeding habits. 9) No statistical evidence of correlative occurrence of members of the parasite pairs was found.

10) The only rod.ent parasite found that may be pathogenic to humans was qep¿Jlarlg hepatlca. ' -92-

APPENDIX_l

On June 3O, f968 I examined 98 Peromvscus nianiculatus bairdi from gravel plts near stonewal 1, Manitoba. In seven of them, gatggotaenia dend.ritica (Goeze, L782) was found in the small intestine. The finding of this cestode int.g.bairdiisanewhostrecordrandonlythesecond finding of this parasite in PeromvscuÊ in North America' -er-

APPENDIX II

Parasltism of Voles by Cuterebra sp. (Diptera: Cuterebrid.ae)

During the course of the helninthologlcal survey' parasitisu of vol-es l^Iith Larrae of Cuterebra (Myiasis) was noted. Three previous instances of C$terebra nyiasis 'were record.ed- in Manitoba. In 19þ0, A11en (2) recorded- a case of nyiasis in a house mouse. Mct,eod- (73) also found. infectlons in a house mouse anð. a nink; and. Buchner (13)' in l-958, observed. myiasls ln Microtus pennsylvanlcgs d.nrn- EgË, Clethrlgnonys gapperi logingi, and. Peromyscus nani- culatug balrÈi. Other record.s of Cuterebga parasitisn are summarized. 1n Table XI. Life cycle: The Cuterebrld-ae are known only from North and- South Anerlca apd. usually have a single generafion per yeaT tltat is well synchronized. with the actlvity of their hosts. Adult cutsrebra hateh from puparia in June or Ju1y. They ovlposit near the shelter or over-winter sites of the host. LaTvae hatch fron the eggs and. sonehow reach their host while 1n the early first instar. They enter the host through the skln and. burrow inËo the subcu.tane- ous tissues. They remain near the site of initlal pene- tration or wand-er elsewhere. A hole appears at the rest- 1ng slte for respiration and waste renoval-. As the larva d.evelops through the second- and. third- instars, it increases _e&_

in bulk, reachl:ng a weight of one gram or nore. After a maturatlon period, of approximately twenty-eieht d-ays, the larva emerges from its host, burrows into the soil, anid. soon pupates. It overüiinters ln this stage and. emerges as the ad-ult fly ln next June or Ju1y.

Results¡ Sixty voles out of a |',ohal- of 1061 were infected. wlth Cuterebra: flfty-slx @!gg l¡ennsylvanicus, three clethriononJrs gapperl, and one SergJ€S nanlcglatls. Elghty-one larvae were found in @!gg @, wlth a nea;tT of 1 .4J per inf ected. an1mal. This flgUre faLls w1ühin ühe 1.0 to 1.8 range record.ed. by l¡,Iecker (fO9) fn Lg62, and- close to the 1.6 larvae per host as record.ed- by Sillnan (gil in t955. The highest nunber of larvae per ind-lvid.ua} was five, and. the lowest,one; this is not the highest record.ed, âs Sillnan (95) found- one ærog¿S trith seven bots. I found_ wøt 36 (60/") of the infected. rod.ents were males and, 24 (Llo%) ïIere fenales . Goertz (37) record'ed- slnllar percentages: 6?ft nales and. JB/" females. Sealanderts eÐ flnd_ings also showed a higher lnfection for males, but Sillnan (95) reported- the opposite for S@@ aFgTS- tifrons in whlte-footed- nice. I,rlecker (109) found' no cor- relation with sex. In ;1966, the flrst lnfection wlth Cuterebra was observed. on Jul-y 22; in 196?, oh Ju1y 26. Peaks in infectlon were found. 1n the first week of August 7n 1966, and -e5- the thlrd. week of August 1n L967. Thls coincldes with the r,,iork of several authors (3?, 93, 95, !Q2, 109). other workers (J-, 20, 91) observed- peaks fron Septenber to October, but their work was d-one in a more southern latitud.e. The later peaks probably refl-ect a cllnatic d.ifference and. nay be related. to the larval d-iapause d.lscovered. by Slllnan (96) . Of the infectlons, only two were observed' to be scrotal, all others being located. at the anüerlor end, of the body. The |awae were a]j- atranged- nearly paralIel to the longltud.inal axis of the host, âs noted by Sillnan OÐ. Second"ary abscesses l,vere also noted- in a number of gases, and may be d.ue üortin siturr d-eath of the l-arvae or an iUnunologlcal reaction by the host. The wounds l^Iere surround.ed" by a Large atea of thick connectlve tlssue.

Dlscusslon¡ The infections of voles r,rrith Cuterebrg, are probably d.ue to 9. .Ë@, Èhough the larvae were not id.entified. to species. Buchner (13) stated. E]nat rf thls species ls the only nember of the family that has been coll-ected- in the Prairle Provlnces, so that lt 1s 1ike1y þi¡at al-l the foLlowing records of cuterebrlds pertain to the species C. gglgggff . -96-

TABLE XI

Infections wlth Cuterebra in voles in North Anerica, d.uring perlod-s of peak abund"ance.

AUTHOB HOST TNFECTTON LOCALTÎY

Scott and- Snead- (91) Peronyscus 30-35% fowa Dalmat (20) 3B/" Iowa Test and Test (l-02) tt 29% fnd-iana Sl11nan (95) il ?B/" Ontario

Ì¡Jecker (109) " LþB/" Mlchlgan Abbott and. Parsons (1) r! ??/" Massachusetts Seal-and.er (93) 32% Ontario Goertz (37) tt 7-IB% oklahona Goertz (locciË) Neotgna 2?/" oklahoma _yb-

Befe_re$ces

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