John O, Whilaker,Jr. Department of Life Scieoces Indiaoa StateUniversitY Terre Haute, Indiana 47809 and ChrisMaser USDI Bureauol Land Managemeot Forestry and SciencesLaboratorY 1200 Jefferson\faY Corvallis,Oregoo 97331

Parasiticmites of voles of the genera Microtusand ClethrionomYsfrom Oregon'

Abstract speciesof voles trom Oteqon wcte L'l''f mor. imp.,narr rnrres.toJndin thc tur of seven Tl-c isabellint""r',\li ratk\ nu'1ta\n\'' b ,li. L. atrtb,n"l. Andt tde!dp;,r'.',it'"iii, nd.Erhiianl"'tt' ;,;";!.r,;1,",y;,;;;'ti;;(:'")iiti:;l::;:,x;';:;i:r,;:,4,01i"{,,,til;:'i!,i!;',:"",.1,';:..^'":"; ,t:,:::iii:i:,;j;.:'liy,::;,1';,:it*::,',i::;,,::;i.i;!!":,Ir''i',;.1"""fr':^:,7!;':"i'^'l;'::';' t"'+nl rhos. or A'b'v.i'nt'! athitc".a tn-ttautru" tnq .',:'Ii:l;. o, 14i.'n,,.,-spp an.r t";i,: o,totu.wcrecomp.rrcd"lT,:rii...ilX;JTAd\t:;::i;i:;;)iiif;\.,'rl;,T,T';T'5: mite'ru.'.,u*r' tn",,"r ii'l redt'ec 'ore Iil,lii,,:;i)^l*';i,,);l"Tr:'Th,..ii'ii".,i*'ilt,",i'ili Douslaslir trees, t;,ii",i,a,.i. *r,i.t riu",;ish-;b";" sround,piimarilr in larse P!e dat!1/g,1 / enzielii

lntroduclion 'toles' Longicaudts; tltlontar.e During studies of Oregon mammals, long-tailed Microtttt \oles' M talLrtertdt' w^ter voles,"l7. ntotatttts; creeping t'oles, Ll otegotti; Townsend cdlilomictt: and toles,. lL richarrhoal; california red-backed voles, clethrionont|s for the pteseoce of mites The sotrthern red-backecl \oles, C. gappe ' were examioed these voles Obscr- p."f"r" tf ,f-r" r,tay.tas to determioe the speciesof mites parasitizing of mite-{aunas cortelated q'irb . ",innr .r'"r" also made to determine how the composition rhe host relations, and rvith host-habitat relatiolships on the larger mites parasitiziog three other \Ve have Previously presented information albipet; ted tree voJe' specics of tol.s fr.r- Oregon: v'hite-foor ed vole, Atbotitnat (Vhitaker Maser 1979 ) The mite ). hugirur,lu,; and sage vole, Lagurar c rtltltr and lndrctLael'rpr f,,l.,n.i in g.eatest ,tuib"r, on all three of these voles was fdhrcnbolzi' A albipes' ar'd G\cyphagtt Sccondin number was Eurlptltur ! sp (nor parasitic) on hlftdaei on the other t*'o hosts. ',il:l;':fi':,1.i Pusc'isolrod t,:,#l't'*".?:iil'ii$dl'S'?i:"i1.fl1'v1',.J;ru:il**.''

1,12 Noth*,est Scieoce,Vol. 58, No 2, 1984 -

-jiii -j j.:i 11i .

!? :: :

.:3'' 2

':

! z :az= :- :n:! : i.!!_ 1z 1i.1i-:

,=a: ; i i!I::-- z

ParasiticMites of Voles 111 Materialsand Methods The voleswere caughtin museumsoap traps. Mites were collectedby brushing the voles *,ith a fine-bristled toothbrush,then examining them *'ith a 16-powerhaodlens while biowing the fur. Mites found by the latter method were picked off with forceps. This procedurewas satisfacroryfor the larger mites, but was not so effective for the smaller ones. Mites were preservedio 7O-perceotethanol, cleared and staioedin Nesbitt's solu- rion contaioing acid fuchsin,and mounted in Hoyer's solution.

Resultsand Discussion Data for five speciesof Micrat&r an{f m'o speciesof Clethrionomls are given in tables 1 and 2 aod, for coparativepurposes, mites that occurredat rates of 10 percentor more oo any ooe speciesare listed in order of decreasingabundance (Table 3). The numbersof speciesthat occurredon 10 percent or more of the samplesranged fton-rm,o to four (Table 3). (LilrroplJotu! maxicatutt rvasomitted from consideration becauseir appearedthat it, along with some of the other small mites, was too often ovetlooked.) T*'o o{ the hostsexist under specializedconditions: (1) largarn.t, *4trch occursio areasunusually arid for a vole, r'as one of the voles least commonly iofested by mites (only two speciesof mites occured on 10 percentor more of the sample), and (2) Atiborimu longicatdus,which occurshigh in Douglas-fir (Psearlotnga tterzzietiil ttees,yielded mites of only five species,including a myobiid mite, Radt'otdiaarborimut, tecentlydescribed as a result of thesestudies (Fain aod rJfhitaler 1975). lztgartr catta' tnr harboredmites of 10 speciesalthough only 2 were common. Except fot llicrottt longicardu, which aiso had 2 speciesof commonly occrrrriogmites, the other hostshad 3 or 4, and ,1 to 18 total species. Overall,hosts rvith mote numerousspecies also had a higher proportion of commonly occurring mites. The averagetotal numbers n'ere 8, 8.8, and 12.3 speciesof mires on hosts*'ith 2 (t:2 ), a (.n-4), ar'd4 (n:4'1 commonlyoccrrring mires. Andtolaelaps t'ahtenholzi was the most abundant parasite on three of the hosts; Laelapr kochi on three; and Haentoganavu reicli, H. occidentalit,Echinonlttat itabil' lintu, and Haemogarialassp. ++2each one ooe (Tabte3). Awlrcclaelapt t'ahrenboLziis a widely distributed, abuodant spc.ciesand is found on r wider range of hoststhan is any other parasiricmite in North America (Whitaker and rVilson 1974). k may, howwer, representa complex of spectes.Anfuolaelapt fa/: renl:olzi w,asthe only mite found on all 10 volesconsidered here (Tab1e3), and occurred at ratesgreater than 10 perceot on voles of all the 10 speciesconsidered, ranging from 10.5 pefcent oa Alicrohu otegoni to 88.2 percenton Arborinu.t longicaulat. It was the mSorex yaqainae by \Whitaker el al (1980). The specimensiovolved all appearedto be the speciesof Haentogantattt repotted here

1:]'4 S(hitaker and Maser 'E y" i

n.nnn n- ii +

6 .E

: .: d -oo

? :r,. a

4.,

:

;

ParasiricMires of Voles l+5 as Haemoganaws sp. #2. Haemogamawt ambalansaPParently has not been found in Oregoo. qumbers The three speciesof Haemogamaws exhibited much variation in among the IO \oles. Hdemogamavtssp. #2 was not taken on six of the hosts;had a low prevalence (less thao 10 perceot infestation) on two, and occrrrredcommonly ot only two, Cletb' tionom"w californicas attd Arborimus albipet. Haemogamans occid'entalfu,a commofl parasiteof rvesternsmalL mammals, occurred on six of the hosts. It was nor the predomi- .ru.rt -ite oo any, but was the secondmost common oo Mictottts tichatdt'oni ar,d hI otegoni rt occurredat a high meao number per individual (361 ) on M richatdtotti' Haentogannuts rcidi was ttot recorded from three of the host species,occutred at a low rare ori three. aod was commoo on Mictotas townsend,M richadsoni, ar,d Clethriono" ?nlr gdppei. One vole, Arborima.t lortgicaudat,had to Haemogatttarzrat all, whereas Mirrit)t nnrtencli and M tichardrcni had two (H occid'entalitard' H reidi in each case). Three species,Micratrs ?nontdnaJ)M. lotgicaudat' ar,dI'lg'rw c/rttat J,had zerc, ooe, or rwo speciesof Hllemogdmd[Lr,but [one occurredat high rates Echinonysstrtisabellirus occufrd oo five of the species,commonly ot thrce, Micto' tut )4outdttltJ,.\1. touu,e'di, aod Cletlt,ionon)' SalPeri Laelapsala&ensis and,/orL kochi occurredcommonly on five sPecies,all Mictant' Laelaptkochi was found on all the speciesof Mlcro,us excePtM tichardtoni and only on this genus- It had the highest percentageo(currence in three of the species'but was fourth on r1{.touttten'Ci. The mean number per host was rather high in all cases,ranging from 0.87 in M, ,otunserzclito 164 rn M longicaadu. Laelapsalatkemi' often common on voles.was first ot llictotus richatdtoni' and third on M montal?a!aod occulred at high rates (both in percent occulrenceand means). This species,however, did not occur oo afly of the other eight voie species The ooe myobiid iocluded as commonly found was Radfotdia arborimat (Fain and \y,rhitaker1975 ). describedas a result of thesestudies. Gllclphaga: hlpulaei wasrhe secondmost widely occurring species,found on oioe of the hosts (none was found on M longicatulutq. It was the secondmost commonly occurring speciesot Arborinns lottgicatdas and ot lzgttttts lt occurredac a flequency of 10 peiceot or more on six of the h osts' Clethriononyt calit'otnictt, C gapperi' Micro' tu.r richatdtotti, Arbotimus albipet, A longicaudus'tnd I'agaLltrc rtttt'lrt' Mites of the genusEuyparusihts are not parasitic Nymphs are common on small (probably mammals. bnt their relationship to the host is not knowo' Eatypausitat more than one species)occurred on six of the voles,aod oo more than 10 perceotof the individr-ralsof fovt: Micto'at otegoni' cletbrirtnottt)'rcalilonicut' Mictotur ichardntti' and Atborintat albipet lt s'as secondin occurtenceon Clelhrionomyr caliJornicat atd Athorittur albiper. At leastone speciesof histiostomatidmite occurtedon three of the speciesand at the 1O-percenttate oo ^Iicrcla! tichadnni and Arborinttt longicauda:' Histiostomatidsare phoretic in the deutonymphalstage on a variety of animal hosts' Thus. there was some similarity berween the host communities,but by no meaos cao it be said that mites moved freely betweenhosts lf that wete the case'mite com' rnlrniLresrhould he similar'As a meantol (omparingcommuniLy "trutru'e' miret nere (Table No two host spectes listed bv decteasingPelceot occultence for each host 3) lrlcl the sameorder of rrcurreoce of mites' nol eveo the samemites in differiog order' As mentioned before,Arbotinur Longicaudttdiffers the most ecologicallyfrom the

1,16 \fhitaker aod Maser oe

ia

=. 3,E

E;

*-

,g ! 'i?:=E=E:"'-^ : 3g EEEE;::.q-' z : c; I a2 !.c; ,7 - Eq .; : {a :; :i:: ii .E:j i I i.E a 1 i :.;3=t-:f: ?:ii;'- i=l .:t:::;:

= - .--= ;;:::;:,fY: --l

3 6l -l z tl i': i r= ,=:F- =- al :T::::E:: "l ,_ t, i 5l = : :: =,=E:: - al = az' - a 2;. : :. 'ztiLt!= .=:a1: ::1!:t-.=

."!l F ! Z ! 2i'*=

i=:'-=;:= .-l tj:j:Ei.: Z; y 'e= : a1a"1a:.'=: :l 6l -:.

ParasiticMites of Voles I11 other vole species,a separation reflected io the mite community becauseooly five species of mites were taken. The rwo most widespread mites, l. t'ahrenholzi and G. hypadaei, u'ere the only speciesthat rxcurred in a relatively large percentage of the individuals. There was a close relationship of mite communities between M;crot i tabvlend; and ]1. ntontanlLJ. Seven speciesof mites were found on M, tounvndi and on ltr{, tnotltanl/Jj six of them occurred oo borb, but Haenagarnasas sp. #2 occurred only on ,;l{. totantendi and Laelap.r alatke is crc:urreC,only on,trI. rltotlttttLlr!. The ciose mite community rela- tionship benveen M. toun.rendi and M, monrdlutr is plausible because both species of voles ate constrained by runrvays and inhabit moist to *'et ateas, and they share rvidc' ranging mite species rhat occur on both sides of the Cascade Range- llaentogtnattt sp. #2. on the orher hand, occurs only rvest of the Cascade crest, as does its hosr, M. tortn :entii- aod, Laelapt alaskentit occurs frorn the crest of the CascacleRange eastsard, as does its host, M. 11loltlat/t! (Maser and Storm 1970). A second close mite communiq. relationship was that bem'een Clethrionottl.r cdifor' ttictt and Arbotitltu aLbipet. Five speciesoccurred ot A. albipet. The same five species occurred on C. c,tLifonacttt, plus trro additiooal sPe.ies: Httewogd rdttu rcic]i anC,IIae' i)tagdt)tdt/tt sp. +2. Both C. calilornicrs and. A. albipet are largely fosrcrial and share a similar geographical distribution-soltth of the Columbia Rivet from the crest of the Cas- cacle l{aoge rvest*.ard. They are, in fact, sympatric in some areas.That C cdliforxiuu he.d rwo adrlitional mite speciesis not surprising becausethis vole has a wider larirude of habitats than d.oesA. albipet (Maser er al. 198I). llictottr otegotti atd. lL richtdroni also showed community similatities. Each hacl ser,en mites species. five shared. if. oregoti is largely fossorial and is not closely tiecl ro above{ronnclruoway systems. lI. tichatdtoni, oo rhe other hand, is primarily a semi- aquaric stream chvelierof dre high Cascades(above 6,000 ft.). and is nore rigidly gov- erned by its abovegrouncl runways. These voles are sympatric. hon'ever, in sone lorver elevetion arcasalong the uestern flank of the Cascades(N{aser and Stotm 1970). Cletlttionow\.t gdpprri sho$'ed similarities s'ith Ldgtttu c/t/ldt/./.\. Clethriorolttj'.1 .(rrtrrl hafbored four speciesof mites. These fout and one additional species*'ere found on L. .tlrtatni. tScrrhC. gdfPcri and,L. ctttatut occLrr east at the Cascade Range anrl are nerrorvlv alloprtric in portions of tbe Blue Mountains of northeasternOregon. Tltc llictotr.r /otLgic,ntltt mite community diffeted considerably from othet ]Iicrottt.r communiries. trIi.rattt lalryi.caxdzr,in Oregon, consists of four clearly defined sub- ,speciesrhlt essentialiyrepresent four differenr geographical areas (Hall 1981, Maser end Storm 1970). The subspecies.abdint, cx.ctrsonly io northwesternOregon. west of rhc Casca,leRenge. rlllroll.r longicatdrr.11tg lt;ce1r extends from northwesrernCali fornia northrvard inco south$'estern C)regon, but onlv along the coast. Il;ctutli lonli ttrttlrtr ( ,\L lottgictacltr.r utotdax') occuts east of the Cascade Mountaios. thro!8hout thc renqelands,lf centrol anrl southeasternOregon. Of the four subspecies,ahdittr ,::cctt' pics rhc settest arels prittarily ripatiao areas and is not depenclenton ruo*avs. Thc srrbs;rccies.,tit{://t!ictft, inhabits grassyareas ancl is dependeoton abovegroun.lrunu'ays ,\[iLrat//.r/at]qicrt!drt l:dli is essentiallya speciesof grassy riparian areas n'ithin rhe conifcrolrs foresr an.l mal'or me,vnot be dcpendent on aLrovegrounclrun*ays. The sub species.lonqic,trltr \ aordas), occLrrsfrom riparian areas in poodetosa plne. Piut foltlrrortt. forests int,:r dry sagebrush.Artenisia spp., regions. This subspeciesis nor consrreinedby runs a!s. Tire mites from ll. /otty,icucltr came from clifferent subspecies

I rs \\'hitaker and Maser from widely scatteredlocalities within Oregon which, when coupled with the small samplesize (28), may accountfor lack of similarity wirh other Microhts comm:unities. Finally, Arborimat longicaudusis not ooly the most specializedvole withio the state but also the most widely removed from the other voles ( Johnson 1973). The laner is tlue becauseit is the only vole that is almosrstrictly arboreal (Maser et al. 1981). Even its cogener,A, albi.pet,is primarily rerestrial (Johnson and Maser 1982, Yoth et al. 1981). Thus it is not surprising that this communiry is quite different from others. The mosr similar commuoities were not of the taxonomicallymost closely related forms. The Microtus longicaud.zzrcommuniry differed considerably from the other Mictotas commtr,ities. The two speciesof Clethrionoxzysshared ooly one major mite species.Mitesof C, cal.ifornicaswete si.mllarto thoseof A. al&lpar. The secondspecies of Atbotim*t, A. longicaadus,was the most ecologicallyisolated species of all. This anaiysis indicatesa rather low degree of similariry between these voles' parasicecommunities, and also relatively little similarity betvreentaxonomically relatecl forms. Parasitic or phoretic speciesnot previously reported from Oregoo are Lljpadryit miles, Dermacantt ood,atrae,ar'd Myocoptet idponenJir. New parasiticor phoretic host records ate: E*btachylaelapsdebilh, Haenoganavr occideotalfu,Glycyphagus hypadaei, Detmaca,tushyland.i (?), atd Li.rtrophorut uexi- canusot Mia,otus montana[; all the records from Microtat orcgoni, exceptA, lahret halzi; all record,sfrom Microtas tolauend.i, exceptHaemoganatat; Ealaelaptnablularit on Micrctur longicaud,r.s;And.rolaelapt fahrenholzi, Haemogamatu occidentalh,H. rcidi. Mycoltet japonensis,Glycyphagu.r hlpudaei, and Littrophorul nzexicaxtt ftom Micro- tus richardrcni; and all records from Clethrionomyt californicut, except Eclsittony.rsa: obsoletus. Although somesense cao be made from our analysisof the mite communiry relation- ships from the 10 speciesof voles that we examined,there are some apparentproblems with the interpretation of such data. Larger host samplesizes are necessary,parricularly in an uea as diverse as Oregon becauserhe hosts were collectedthroughout the State. The communitiesshould be analyzedon the basisof host subspecies,georgraphic distri- bution, habitat affioities, and physiographicprovinces (Franklin and Dyrness 1973, Maser and Storm 1970).

Acknowledgments rVe thank Alex Fain (Instirut de Medicine Tropicale Prioce Leopold, Anrwerpen) for identifying some of rhe smaller mites, and Nixon Wilson (Department of Biology, University of Northern Iowa,Cedar Falls) for examinationol usrneof the Haettoganttrsttl arrdEchinonystut. Gerald Krantz (Departmenrof Entomology,Oregon StateUniversity, Corvallis), Dooald K. Grayson (Department of Anthropology,University of Washing- ton, Seattle),and Robert L. Rausch (Division of Animal Medicine, Schoolof Medicine, Uoiversity of \Washington,Seattle) critically read and improved the manuscirpt. Phyllis Taylor-Hilt (Bureau of Land Management,Forestry Sciences Laboratory, Corvallis, Ore- eon) rlped rariousdrafrs of chemanscripr. 'We are grateful for the help.

LiteralureCited Fain, A., and I. O. \Thitaker, Jr. 1975. Two new specic: of Myoiidae fron North American rnam mals (Acarina). Bull. Ann. S{x. r. belse Ent. III: t7-65.

PrrasjticMires of Voles I49 Franktin, l. F. and C. T. Dyrne$. 1971. Natural vegetatiodof Oegon and Washingtoo. USDA For. Serv.Gen. Tech. Rep. PNrV-8, 417 p. Par. Northwest For. and Radge Exp. Stn., Port- Iand,Oregoo Hall. E. R. 1q81 The ma.mmalsof North America. Vol. II (sec.ed.). John \(iley & Sons,N. Y. 777-824.. "lohflson. M L. 1971. Charactetsof the heathervole, Phenacomys,aod the red te vole, Arborimat. i. uammal. 54: 219"244. Johnsori,M. L., aod C. Maser. 1982. Generic relationshipsol Phenacomys,/rirer. Nonhw. Sci. 56t 11-19. Maser,C., and R. M. Storm. 1970. A key to Microtinae of the Pacific Northwest (oregon, wash- ingron,ldahor. Pubt.by O.S.U.Book Stores.Inc. Corvallrs,Oregon. Mascr, C., B. R. Mate, J. F. Franklin. aod C. T. Dyrness. 1981. Natural History of Oregorl Coast mammals.USDA For ServGen Tech Rep PN1v-133,496 p. Pac.Nofthwest lor. lrld Range Exp. Stn., Portland, Oregon. Voth. E. H., C. Maser, aod M. L. Johnion. 1981. Iood hablts of Arborimas albiper, the athhe footed vole, in Oregon. Northw. Sci. 57: 1'7. Vhitaker, I. O., Jr., aod C. Maser. 1979. Parasiticmites of voles of the generaArbotimus aod, Iagarxs in Oregon. Northv/. Sci. 53: 224-22/. Vhitaker, J. O., Jr., G. L. Tieben, and C. Maser. 1980. Mites ( excluding chiggers) from the fur ol five spcies of westernOregon shrews. Northw. Sci 54: 26-29 \trhiraker, J. O., Jr., and N. Vilson. 1914. Host aod distribution lists of rnites (Acari), parasis- tic and phoretic, in the hair of wild animals of North America, north of Mexico. Amer. Midl. Nar.91: 1-67.

Receioed,lane 4, 1982 Accepted, lor publicatioa SeprenLber24, 1982

'!0hitaker 150 aod Maser