SEROLOGIC SURVEY OF TOXOPLASMA GONDII IN GRIZZLY BEARS (URSUS ARCTOS) AND BLACK BEARS (URSUS AMERICANUS), FROM ALASKA, 1988 TO 1991 Author(s): Bruno B. Chomel, Rndll L. Zrnke, Rickie W. Ksten, Philip H. Kss, nd E. Mendes Source: Journl of Wildlife Diseses, 31(4):472-479. Published By: Wildlife Disese Assocition https://doi.org/1.7589/9-3558-31.4.472 URL: http://www.bioone.org/doi/full/1.7589/9-3558-31.4.472 BioOne (www.bioone.org) is nonprofit, online ggregtion of core reserch in the biologicl, ecologicl, nd environmentl sciences. BioOne provides sustinble online pltform for over 17 journls nd books published by nonprofit societies, ssocitions, museums, institutions, nd presses. Your use of this PDF, the BioOne Web site, nd ll posted nd ssocited content indictes your cceptnce of BioOne s Terms of Use, vilble t www.bioone.org/pge/terms_of_use. Usge of BioOne content is strictly limited to personl, eductionl, nd non-commercil use. Commercil inquiries or rights nd permissions requests should be directed to the individul publisher s copyright holder. BioOne sees sustinble scholrly publishing s n inherently collbortive enterprise connecting uthors, nonprofit publishers, cdemic institutions, reserch librries, nd reserch funders in the common gol of mximizing ccess to criticl reserch.
Journl of Wildlife DIseses, 31(4), 1995, pp. 472-479 Wildlife Disese Assocition 1995 SEROLOGIC SURVEY OF TOXOPLASMA GONDII IN GRIZZLY BEARS (URSUS ARCTOS) AND BLACK BEARS (URSUS AMERICANUS), FROM ALASKA, 1988 TO 1991 Bruno B. Chomel, Rndll L. Zrnke,2 Rickie W. Ksten, Philip H. Kss, nd E. Mendes 1 University of Cliforni, School of Veterinry Medicine, Deprtment of Popultion Helth nd Reproduction, Dvis, Cliforni 95616, USA 2Alsk Deprtment of Fish nd Gme, 13 College Rod, Firbnks, Alsk 9971, USA ABSTRACT: We tested 644 serum smples from 48 grizzly bers nd 4 blck bers from Alsk (USA), collected between 1988 nd 1991, for Toxoplsm gondli ntibodies, using commercilly vilble ltex gglutintion test (LAT). A titer 64 ws considered positive. Serum ntibody prevlence for T. gondii in grizzly bers (Ursus rctos) ws 18% (87 of 48). Prevlence rnged from 9% (seven of 77) on Kodik Islnd to 28% (15 of 54) in northern Alsk. Prevlence ws directly correlted to ge. No grizzly bers <2-yer-old hd T. gondli ntibody. High ntibody titers were found minly in grizzly bers cptured north of the Arctic Circle. Antibody prevlence in blck bers ( Ursus mericnus) from Interior Alsk ws 15% (six of 4), similr to the prevlence in grizzly bers from the sme re (13%; five of 4). Key words: Toxoplsmosis, Toxoplsm gondii, grizzly ber, Ursus rctos, blck ber, Ursus mericnus, serologic survey, prevlence, Alsk. INTRODUCTION There re n estimted 3, grizzly bers (Ursus rctos) in Alsk (USA) (Hummel nd Pettigrew, 1991) nd less thn 1, in the other 48 continentl U.S. sttes. Popultions of blck bers (Ursus mericnus) were estimted to be between 3, nd 4, in the United Sttes including 14, in Alsk (Hummel nd Pettigrew, 1991). As predtors nd scvengers, bers might come in contct with zoonotic disese gents such s Toxoplsm gondii, Mycobcterium tuberculosis, Coxiell burnetii, Yersini pestis, Leptospir spp., Trichinell spp., Brucell spp., nd Frncisell tulrensis (Ruppner et!., 1982). Toxoplsmosis is protozon zoonosis found throughout the world (Dreesen, 199). Infection by the intrcellulr prsite, T. gondii, ws reported to be prevlent in mny wrm blooded species, including humns (Dubey nd Bettie, 1988). The role of wildlife in the epidemiology of the disese hs not yet been fully investigted. Wildlife species could serve s intermedite reservoir hosts for the orgnism (Dubey nd Bettie, 1988). Bsed on serologic studies, mny wildlife species (Frnti et!., 1975; Riemnn et l., 1975) hve been implicted, including mny furbering species (Dreesen, 199) in the epidemiology of toxoplsmosis in the United Sttes. Blck bers (Ursus mericnus) with serologic evidence of exposure were reported from Ontrio, Cnd (Quinn et!., 1976), s we!! s Florid (Burridge et!., 1979), Idho (Binninger et!., 198), Cliforni (Ruppner et!., 1982), nd Pennsylvni of the USA (Briscoe et!., 1993). None of 21 polr ber (Ursus mritimus) ser co!- lected in n re 25 km north of Jmesonlnd, Greenlnd, hd Toxoplsm spp. ntibodies (C!usen nd Hjort, 1986). Serologic evidence of exposure hs been reported in one cptive polr ber (Kiupel et!., 1987). The only known c!inicl cses of toxoplsmosis in bers were reported in young cptive Kodik bers (Ursus rctos middendorffi) kept t the Rostock Zoologicl grden in Germny (Kiupel et!., 1987). More recently, T. gondii ws isolted from five hunter-ki!!ed blck bers from Pennsylvni (Dubey et!., 1994), nd during the hunting seson of 1993, vible T. gondli were isolted from 1 of 28 blck bers from Pennsylvni (Dubey et!., 1995). Reports of Toxoplsm spp. exposure in nim!s nd humns in Alsk re limited. 472
CHOMEL Er AL-TOXOPLASMA SPP. AN11BODIES IN ALASKAN BEARS 473 Serologic evidence hs been reported for indigenous Alsk ntives (Peterson et!., 1974), nd in moose (Alces lces) (Kocn et l., 1986). There lso ws histologic evidence in hrbor sel (Phoc vitulin richrdii) (VnPelt nd Dieterich, 1973). Our objective ws to determine the ntibody prevlence of T. gondii in free-rnging grizzly bers (Ursus rctos horribilis) nd blck bers from Alsk. MATERIAL AND METHODS Personnel of the Alsk Deprtment of Fish nd Gme nd the U.S. Fish nd Wildlife Service cptured 48 grizzly bers nd 4 blck bers in the course of performing popultion ecology studies. Some bers were cptured more thn once; 644 serum smples were vilble for testing. Smpling ws opportunistic. Seventy-six blood smples were collected from 4 blck bers between 1988 nd 1991 in Interior Alsk on the Tnn Flts, south of Firbnks (63#{176}Nto 66#{176}N,145#{176}Wto 15#{176}W)(Fig. 1). The 568 grizzly ber blood smples were collected between 1988 nd 1991 from eight different geogrphicl res (Fig. 1). In southern Alsk, 79 serum smples were collected on Kodik Islnd (57#{176}N to 58#{176}N, 152#{176}W to 155#{176}W),nd 86 smples cme from the Alsk Peninsul (Ktmi Cost nd Blck Lke) (56#{176}Nto 59#{176}N, 153#{176}W to 159#{176}W).In Interior Alsk, 53 serum smples were collected in the Tnn Flts, Denli Prk nd Firbnks res (64#{176}Nto 66#{176}N,147#{176}Wto 153#{176}W). In Western Alsk, 4 serum smples were collected from Sewrd Peninsul (64#{176}3 N to 66#{176}3 N, 162#{176}Wto 168#{176}W)nd 99 smples from Notk river dringe (67#{176}45 to 68#{176}3 N, 156#{176}Wto 162#{176}W). In Northern Alsk, serum smples were collected from three different res, 133 smples in northwestern Alsk (68#{176}3 N to 71#{176}N,159#{176}Wto 163#{176}W),six smples in north centrl Alsk (Prudhoe By, Ded Horse; 7#{176}2 N, 148#{176}W), nd 72 smples from northestern Alsk (68#{176}3 N to 7#{176}3 N 141#{176}Wto 147#{176}W). Blood smples were collected in glss tubes by femorl, sphenous or cephlic venipuncture. Serum ws seprted by centrifugtion nd stored t -2 C until tested. Blood smples were collected from 25 (63%) of the 4 blck bers more thn once over the four-yer survey: two bers hd blood smples collected four times, seven bers hd blood smples collected three times nd 16 bers hd blood smples collected twice. Among the 48 grizzly bers, blood smples were obtined three times from nine bers nd twice from 68 bers. Serum smples were tested between April nd June 1992 by ltex gglutintion (LAT) using the commercil kit Toxotest-MT Eiken (Eiken Chemicl Co, Ltd., Tokyo, Jpn). A titer 64 ws considered positive, in ccordnce with the mnufcturer s instructions. Titers of 16 nd 32 were reported s wekly positive. Ages were estimted by exmining cementurn nnuli of prernolr teeth for blck bers (Stoneberg nd Jonkel, 1966) nd grizzly bers (Crighed et!., 197). For this nlysis, blck bers were clssified in four inclusive ge groups: to 2 yr old, 3 to 4 yr old, 5 to 7 yr old, nd 8 yr old. Grizzly bers were clssified into five inclusive ge groups (McGuire nd Servheen, 1992):.5 to 2 yr (young bers), 2.5 to 4 yr (end of puberty), 4.5 to 8 yr (reproductively mture bers), 8.5 to 12 yr (prime reproductive cpbility), nd 13 yr (old bers). Grizzly bers from the Sewrd Peninsul nd McKinley Prk ll were reported s dults (4.5 yers). Yer of collection is not necessrily indictive of yer of exposure. However, in this study, test results were ssigned to yer of collection. Dt concerning species, sex, ge, geogrphicl loction t time of blood collection, nd dte of blood collection were nlyzed using Epi Info version 5.1 (Den et l., 199). Frequency distributions were obtined nd chi-squre tests of homogeneity for 2 x 2 contingency tbles were used to evlute the sttisticl significnce of ny ssocitions. RESULTS Serum ntibody prevlence for T. gondii in grizzly bers from 1988 to 1991 ws 18% (87 of 48) (Tble 1). Prevlence rnged from 9% on Kodik Islnd to 28% for northern Alsk (Tble 1). There ws distinct geogrphic pttern of incresing ntibody prevlence (P =.4), s prevlence incresed grdully from southern Alsk (14%) nd Interior Alsk (13%) to western Alsk (17%) nd northern Alsk (25%). Prevlence in mles (34 of 183,19%) ws similr to the prevlence in femles (53 of 297, 18%). In blck bers, T. gondii ntibody prevlence ws 15% (six of 4) (Tble 1). This prevlence ws simi!r to the prevlence (five of 4, 13%) observed in grizzly bers cptured in the sme geogrphicl re (Interior Alsk). Prevlence in mles (two of 18, 11%) ws lower thn in femles (four of 22, 18%).
474 JOURNAL OF WiLDLIFE DISEASES, VOL. 31, NO.4, OCTOBER 1995 Krno Firbnk decresed from 22% (45 of 26) in 1988 to 16% in 1989, 14% in 199 nd 15% in 1991. The highest yer- nd loction-specific prev!ence (38%) ws observed in 1988 in the western Arctic (Tble 2). Age of the bers t the time of bleeding ws determined for 6 (93%) of the 644 blood smples col!ected; 44 grizzly bers were reported only s dults. Sixty-five (93%) of 7 young grizz!y bers (.5 to 2 FIGURE 1. Loction of study sites where grizzly ber (Ursus rctos) nd blck ber (Ursus mericnus) ser were collected for toxoplsmosis survey. For grizzly bers, A: Kodik Islnd; B: Alsk Peninsul; C nd D: Interior Alsk; E: Sewrd Peninsul; F: Notk River dringe; C: Western Arctic; H: Estern Arctic. For blck bers: D: Interior Alsk. High Toxoplsm spp. ntibody titers ( 1,24) were found minly in grizzly bers. Eight (73%) of 11 of these bers were cptured north of the Arctic Circle (Fig. 2). One blck ber from Interior Alsk hd n ntibody titer of 4,96. Twentynine grizzly bers (6%) nd one blck ber (2.5%) hd only wekly positive ntibody titers. Overll, 5.4% of the grizzly bers serum smples (31 of 568) nd 4% (three of 76) of the blck bers serum smples hd wekly positive ntibody titers. Yer-specific prevlence in grizzly bers yers o!d) were from interior Alsk (n = 31 bers) or the Notk River dringe (n =34 bers). Antibody prevlence in blck bers vried from 4% (one of 26) in the to 2 yrold group to 1% (two of 2) in the 2.5 to 4 yr-old group, 18% (three of 17) in the 4.5 to 8 yr-old group, 11% (one of nine) in the 8.5 to 12 yr-old group nd 25% (one of four) in the 13 yr-old group. There ws no significnt difference in ntibody prevlence between dults nd young blck bers. Men (± SE) ge of positive grizzly bers ws 12 (±.6) yr wheres the men ge of negtive grizzly bers ws 8 (±.3) yr (P <.5). Adult grizzly bers were four times more like!y to hve been exposed thn juveniles (reltive risk (RR) = 4.6,95% confidence intervl (CI) = 2.1 to 8.22). Toxoplsm gondli ntibody prevlence incresed with ge, from % (zero of 6) in the to 2 yr-old group to 8% (eight of 97) TABLE 1. Antibody prevlence of Toxoplsm gondil in grizzly bers (Ursus rctos horribilis) nd blck bers (Ursus mericnus) from Alsk by geogrphicl origin nd by sex, 1988 to 1991. Prevlence Species Site Mle Femle Totl U. rctos A /1 () 7/67 (1) 7/77 (9) B 6/36 (17) 1/5 (2) 16/86 (19) C, D 4/17 (23) 1/23 (4) 5/4 (13) E 2/16 (12) 7/24 (29) 9/4 (23) F 3/34 (9) 9/53 (17) 12/87 (14) C 1/42 (24) 13/54 (24) 23/96 (24) H 9/28 (32) 6/26 (23) 15/54 (28) U. mericnus C, D 2/18 (11) 4/22 (18) 6/4 (15) Totl 36/21 (18) 57/319 (18) 93/52(18) Loction of site of cpture given in Figure 1. Number positive/number tested (percent positive).
------,-- CHOMEL Er AL-TOXOPLASMA SPP. AN11BOOiES IN ALASKAN BEARS 475 U C > Q. >,. C 4 &..._.,, Region nd ber species FIGURE 2. Antibody titers to Toxoplsm gondii in blck bers (BB) nd grizzly bers (CB), by regionl loction, Alsk, 1988 to 1991. Vrition in titers is illustrted by htching in boxes. in the 2.5 to 4 yr-old group, 12% (11 of 89) in the 4.5 to 8 yr-old group, 2% in both the 8.5 to 12 yr-old group (2 of 11) nd in the >12 yr-old group (34 of 167). Very low ntibody titers (titer = 16) were observed minly in old bers, s nine of the 11 bers with such titer, nd for which specific ge ws determined, were more thn 1-yr-old. Among the 77 grizzly bers bled more thn once, 17 bers (22%), rnging from 2 to 2 yrs old, hd t lest one positive smple for T. gondii. Nine grizzly bers were positive t two or three different bleedings, including two young femles which hd high titers ( 1,24). The seven other bers were more thn 1-yr-old (rnge 1.5 to 2 yr) t time of the first bleeding. Among the 25 blck bers bled more thn once, six (24%) bers, rnging in ge from 1 to 12 yr, hd T. gondii ntibodies titer 1:32. Three of these six blck bers converted from negtive to positive or wek positive during the smpling period. Two other bers, initilly positive, becme wekly positive, nd one blck ber which ws positive becme negtive. DISCUSSION Grizzly bers nd blck bers, like mny other scvenger species, re susceptible to T. gondii infection. Dubey et!. (1994) isolted T. gondii from five bers from Pennsylvni, confirming nturl infection. We observed n ntibody prevlence in blck bers of 15%. This prevlence ws within the rnge of the 27% (4 of 149) which ws previously reported in Cliforni (Ruppnner et!., 1982), nd the 8% (23 of 33) reported from Idho (Binninger et!., 198), but lower thn the 44% (seven of 16) reported from Ontrio, Cnd (Tizrd et!., 1976), the 8% (535 of 665) reported from Pennsylvni by Briscoe et!. (1993) nd the 8% (257 of 322) reported by Dubey et l. (1994), lso from Pennsylvni. The men prevlence in grizzly bers ws 18%. This is the first report of serologic evidence of exposure in grizzly bers. The lower prevlence of T. gondii n-
476 JOURNAL OF WiLDLIFE DISEASES, VOL. 31, NO. 4, OCTOBER 1995 { 1.. ạ ( N N -u ) ) ) ) I- C) C) C) - C ) C ) C ) - C) - - c - o e - C) C ) ) C) Lf) C) - N N - N C) C ) C) - - C - if) (I) Cl) ZZZg - - L()C) -4.-(.-.. - -. -C I C) ) - - - - - Cl) (I) C ) Oc N Z Z - C 1CI NC ) _-C )ei -O - OC1.-.1 CI).5-kf)- )).-. Lf).1.1 -ic )C 5 - e, it) -.-.-. -.-.. -. -.--. -. -. C.1C.1C ) C ) C. ( C E ) ) ). ạ. zz Cl) tibodies in blck bers from Alsk thn in blck bers from Pennsylvni my hve resulted from the lower sensitivity of the LAT used in our study when compred to other serologicl tests such s the modified gg!utintion test (MAT) (Dubey et!., 1994). Dubey et!. (1995) reported seroprevlence of 79% in blck bers from Pennsylvni by MAT (Dubey nd Desmonts, 1987), but the prevlence ws only 32% (nine of 28) when using the sme LAT we used. Furthermore, the isoltion of T. gondii from six bers without LAT ntibodies is evidence tht this test ws not s sensitive s the MAT (Dubey et!., 1995), but such dt were not vilble t the time we performed our study. We considered positive ny serum smple with titer 1:64, s recommended by the mnufcturer for species other thn humns. It my hve been more ccurte to consider positive ny LAT 1:16; five of the six bers reported by Dubey et l. (1995), for which T. gondii ws isolted, hd LAT titer of 1:16. All six bers hd positive MAT. Yer-specific ntibody prevlence vried by loction: % to 2% in blck bers nd % to 38% in grizzly bers. No specific pttern ws noted. There ws no significnt difference (P >.5) in ntibody prevlence by sex for either grizzly or blck bers; this differed from reports by Binninger et!. (198) in blck bers in Idho. Prevlence vried between geogrphic res. In grizzly bers, prevlence incresed from south (14%) to north (25%). Such n increse eventully could be relted to higher prevlences in wildlife on which grizzly bers preyed nd scvnged. First exposure to T. gondii seemed to occur minly fter 2 yr of ge in grizzly nd b!ck bers. Apprently, opportunity for exposure ws high in grizzly bers, bsed on the incresing ge-specific ntibody prevlence. Low ntibody titers were observed minly in very old grizzly bers; this probbly ws relted more to residul ntibodies thn cross-rectivity with other prsitic orgnisms. In flse positive cses, one would expect to hve wekly positive
CHOMEL Er AL-TOXOPLASMA SPP. AN11BODES IN ALASKAN BEARS 477 results evenly distributed in ll ge groups. Our results were in greement with those of Binninger et l. (198) who reported tht older bers hd greter prevlence of T. gondii due to longer exposure potentil. Such n observtion lso ws reported in grizzly bers for infectious cnine heptitis (Zrnke nd Evns, 1989). Bsed on our test results on seril smples, we believe tht infection occurred during the study s well s re-infection or rectivtion of brdyzoites. Age-relted prevlence increse lso hs been described in Alsk ntives (Peterson et l., 1974). These villgers routinely te moose, reindeer (Rngifer trndus) nd ber met. Flesh sometimes ws eten rw, or lightly cooked, prticulrly while on hunting expeditions. Such eting hbits could explin T. gondii exposure mong indigenous humns throughout Alsk. There ws limited dt on the serum ntibody prevlence of toxoplsmosis in vrious wildlife in Alsk. Prevlence ws 23% mong 11 free-rnging moose from the Susitn River, the Alsk Peninsul, nd the Keni Peninsul (Kocn et!., 1986). Bers certinly could be exposed from consumption of infected rodents or wild herbivores. The highest T. gondii ntibody prevlence observed in grizzly bers ws in geogrphic res where cribou nd reindeer were bundnt (Dvis, 198). Therefore the higher infection rte in grizzly bers could be ssocited with higher prevlence in reindeer. Such hypothesis ws bsed on the fct tht Brucell spp. ntibody prevlence in reindeer nd humns ws lso the highest in northern Alsk where the mjor herds rnged (Huntley et l., 1963). In grizzly bers, Brucell spp. infection occured when eting infected reindeer or cribou (Neilnd, 1975). Brucell spp. ntibody prevlence in grizzly bers provided support for such hypothesis (Zrnke, 1991). Therefore, serologic surveys in reindeer nd cribou popultions would be useful to determine if our hypothesis ws vlid. Serologic surveys could provide evidence tht toxoplsmosis ws trnsmitted to bers vi nturl predtor-prey cycle involving lrger prey species. Serologic surveys nd body infesttion surveys should be conducted lso in other prey species of grizzly bers, such s smll rodents, to determine their respective role in the trnsmission of the infection to bers. Reports from countries round the polr circle provided evidence for such cycles between rodents nd crnivores in Norwy (Kpperud, 1978), nd in Siberi, Russi (Rogtykh et!., 1977). Rogtykh et!. (1977) nd Gluzo (1977) reported tht in the Timyr nd Khnty-Mnsiik regions, Russi, 4% of the reindeer hd serologic evidence of Toxoplsm spp. exposure. Toxoplsmosis is mintined by lemmings (Lemmus lemmus) nd trnsmission to indigenous people occurs vi reindeer met which is normlly eten rw (Rogtykh et l., 1977). Leonov nd Akin shin (1975) reported low ntibody titers in humns, reindeer, nd rodents from the Chukotk Peninsul nd Wrngel Islnd, Siberi. Indigenous Alskns s well s visiting hunters should be educted s to the risks ssocited with the consumption of rw or incompletely cooked ber met. In Alsk, toxoplsmosis should be considered long with trichinellosis s zoonosis trnsmitted by consumption of undercooked ber met. As dvocted by Briscoe et l. (1993), ll met should be thoroughly cooked. The internl temperture of met should rech 66 C for 3 mm (Dubey et l., 199). LITERATURE CITED BINNINGER, C. E., J. J. BEECHAM, L. A. THOMAS, AND L. D. WINWARD. 198. A serologic survey for selected infectious diseses of blck bers in Idho. Journl of Wildlife Diseses 16: 423-43. BRIscoE, N., J. C. HUMPHREYS, AND J. P. DUBEY. 1993. Prevlence of Toxoplsm gondii infections in Pennsylvni blck bers, Ursus mencnus. Journl of Wildlife Diseses 29: 599-61. BURRIDGE, M. J., W. J. BIGLER, D. J. FORRESTER, AND J. M. HENNEMANN. 1979. Serologic survey for Toxoplsm gondii in wild nimls in Florid. Journl of the Americn Veterinry Assocition 175: 964-967. CLAUSEN, B., AND P. HJORT. 1986. Survey for n-
478 JOURNAL OF WiLDLIFE DISEASES, VOL. 31, NO.4, OCTOBER 1995 tibodies ginst vrious infectious disese gents in muskoxen (Ovibos moschtus) from Jmesonlnd, northest Greenlnd. Journl of Wildlife Diseses 22: 264-266. CRAIGHEAD, J. J., F. C. CRAIGHEAD, JR., AND H. E. MCCUTCHEN. 197. Age determintion of grizzly bers from fourth premolr tooth sections. The Journl of Wildlife Mngement 34: 353-363. DAVIS, J. L. 198. Sttus of rngifer in the USA. In Proceedings of the second interntionl reindeer/cribou symposium, E. Reimers, E. Cre, nd S. Skjennenberg (eds.). Direcktortet for vilt og Ferskvnnsfisk, Trondheim, Norwy, pp. 793.. 797, DEAN, A. C., J. A. DEAN, A. H. BURTON, AND R. C. DICKER. 199. Epi-Info version 5.1: A word processing, dtbse, nd sttistic progrm for epidemiology on microcomputers. USD, Inc., Stone Mountin, Georgi, 384 pp. DREESEN, D. W. 199. Toxoplsm gondli infections in wildlife. Journl of the Americn Veterinry Medicl Assocition 196: 274-276. DUBEY, J. P., AND C. P. BEATTIE. 1988. Toxoplsmosis of nimls nd mn. CRC Press Inc., Boc Rton, Florid, 22 pp.,and C. DESMONTS. 1987. Serologicl responses of equids fed Toxoplsm gondli oocysts. Equine Veterinry Journl 19: 337-339. A. W. KOTULA, A. SHARAR, C. D. ANDREWS, AND D. S. LINDSAY. 199. Effect of high temperture on infectivity of Toxoplsm gondli tissue cysts. The Journl of Prsitology 76: 21-23. J. C. HUMPHREYS, AND P. THUILLIEZ. 1995. Prevlence of vible Toxoplsm gondli tissue cysts nd ntibodies to T. gondli by vrious serologic tests in blck bers (Ursus mericnus) from Pennsylvni. The Journl of Prsitology 81: 19-112. N. BRISCOE, R. GAMBLE, D. ZARLENGA, J. C. HUMPHREYS, AND P. THULLIEZ. 1994. Chrcteriztion of Toxoplsm nd Trichinell isoltes from muscles of blck bers in Pennsylvni. Americn Journl of Veterinry Reserch 55: 815-819. FRANTI, C. E., C. E. CONNOLLY, H. P. RIEMANN, D. E. BEHYMER, R. RUPPANNER, C. M. WILLADSEN, AND W. LONGHURST. 1975. A survey for Towplsm gondil ntibodies in deer nd other wildlife on sheep rnge. Journl of the Americn Veterinry Medicl Assocition 167: 565-568. CALuzo, I. C. 1977. Voprosy ekologii toksoplzm (Toxoplsm gondli) (Problems of the ecology of toxoplsms (Toxoplsm gondli)) [In Russin with English summry.] Protozoology 3: 159-168. HUMMEL, M., AND S. PETTIGREW. 1991. Wild hunters, predtors in peril. Roberts Rinehrt Publishers, Niwot, Colordo, 251 pp. HUNTLEY, B. E., R. N. PHILLIP, AND J. E. MAYNARD. 1963. Survey of brucellosis in Alsk. The Journl of Infectious Diseses 1 12: 1-16. KAPPERUD, C. 1978. Survey for toxoplsmosis in wild nd domestic nimls from Norwy nd Sweden. Journl of Wildlife Diseses 14: 157-162. KIUPEL, H., D. RITSCHER, AND C. FRICKE. 1987. Toxoplsmose bei jungen Kodikbren (Ursus rctos middendorffi). Erkrnkungen der Zootiere. Verhndlungsbericht des 29. Interntionlen Symposiums #{252}ber die Erkrnkungen der Zootiere. Crdiff. Akdemie-Verlg, Berlin, Germny, pp. 335-34. KOCAN, A. A., S. J. BARRON, AND J. C. Fox. 1986. Antibodies to Toxoplsm gondli in moose (Alces kes L.) from Alsk. Journl of Wildlife Diseses 22: 432. LEONOVA, T. A., AND S. D. AKINSHINA. 1975. Nturl nidl infections on the territory of northestern Asi [In Russin]. In Prziticheskie orgnizmy severo-vostok Azii. Akdemiy Nuk SSSR, DFnevostochnyi Nuchnyi Tsentr Vldivostok, Russi, pp. 289-33. MACGUIRE, L. A., AND C. SERVHEEN. 1992. Integrting biologicl nd sociologicl concerns in endngered species mngement: Augmenttion of grizzly ber popultions. Conservtion Biology 6: 426-434. NEILAND, K. A. 1975. Further observtions on rngiferine brucellosis in Alskn crnivores. Journl of Wildlife Diseses 11: 45-53. PETERSON, D. R., M. K. COONEY, AND R. P. BEASLEY. 1974. Prevlence of ntibody to Toxoplsm mong Alskn ntives: Reltion to exposure to the Felide. The Journl of Infectious Diseses 13: 557-563. QUINN, P. J., R.. RAMSDEN, AND D. H. JOHNSTON. 1976. Toxoplsmosis: A serologicl survey in Ontrio wildlife. Journl of Wildlife Diseses 12: 54-51. RIEMANN, H. P., J. A. HOWARTH, R. RUPPANNER, C. E. FRANTI, AND D. E. BEHYMER. 1975. Toxoplsm ntibodies mong bobcts nd other crnivores of northern Cliforni. Journl of Wildlife Diseses 11: 272-276. ROGATYKH, N. A., S. I. KONOVALOVA, AND L. V. TOBOL SKAYA. 1977. Toxoplsmosis in the extreme North (estern Timyr) [In Russin with English bstrct]. In Problemy epidemiologii i profilktiki PrirodnoOchgovykh Boleznei v Zpolyr e. Omskii meditsinskii Institute, Omsk, Russi, pp. 126-134. RUPPANER, R., D. A. JEssuP, I. OHISHI, D. E. BEHYMER, AND C. E. FRANTI. 1982. Serologic survey for certin zoonotic diseses in blck bers in Cliforni. Journl of the Americn Veterinry Medicl Assocition 181: 1288-1291. STONEBERG, R. P., AND C. J. JONKEL. 1966. Age determintion of blck bers by cementum ly-
CHOMEL ET AL-TOXOPLASMA SPP. ANI1BODIES IN ALASKAN BEARS 479 ers. The Journl of Wildlife Mngement 3: 411-414. TIZARD, I. R., J. B. BILLETT, AND R.. RAMSDEN. 1976. The prevlence of ntibodies ginst Toxoplsm gondil in some Ontrio mmmls. Journl of Wildlife Diseses 12: 322-325. VAN PELT, R. W., AND R. A. DIETERICH. 1973. Stphylococcl infection nd toxoplsmosis in young hrbor sel. Journl of Wildlife Diseses 9: 258-261. ZARNKE, R. L. 1991. Serologic survey for microbil pthogens. Federl Aid in Wildlife Restortion. Finl report. Projects W-22-6, W-23-1, W-23-2, W-23-3 nd W-23-4. Alsk Deprtment of Fish nd Cme, Firbnks, Alsk, 58 pp. AND M. B. EVANS. 1989. Serologic survey for infectious cnine heptitis virus in grizzly bers (Unsus nctos) from Alsk, 1973 to 1987. Journl of Wildlife Diseses 25: 568-573. Received for publiction 12 Decemben 1994.