Helminths in coyotes

NOTE

Helminths in coyotes (Canis latrans Say), wolves (Canis lupus L.), and red foxes (Vulpes vulpes L.) of southwestern Manitoba W. M. SAMUEL, S. RAMALINGAM Department ofZoology, University of Alberta, Edmonton, Alta., Canada T6G 2E9 AND

L. N. CARBYN

Can. J. Zool. Downloaded from www.nrcresearchpress.com by 50.99.94.101 on 10/14/16 For personal use only.

Canadian Wildlife Service, Edmonton, Altu., Canada T5J IS6 Received April 14, 1978 W. M., S. RAMALINGAM, and L . N . CARBYN.1978. Helminths in coyotes (Canis SAMUEL, l a r r ~ n sSay), wolves (Cnnis 11cpu.s L.), and red foxes (Vulpes vulpes L.) of southwestern Manitoba. Can. J. Zool. 56: 2614-2617. Forty-three coyotes, 12 wolves, and 6 red foxes from an area around Riding Mountain National Park in southwestern Manitoba were examined for parasitic helminths. Eleven, 8, and 5 species were found in coyotes, wolves, and red foxes, respectively. Alaria marcianae, Alaria arisaemoides, and Toxuscoris leoninu were found in all three host species; Echinococcus granulosus, Taeniu hydutigena, Uncinariu .srenocep/zala, and Oslerus (Oslerus)osleri in wolves and coyotes; and Echinococcus multiloculuris in coyotes and red foxes. Taeniupisifbrmis and T. leonina were the most prevalent species in coyotes; E. multilocularis and E. grunulosus, the most numerous. Echinococcus grtrnulosrrs was the most prevalent and numerous species in wolves. Alariu tnarciunae and T. leoninu were found in all red foxes. The significance of the coyote as a major definitive host o f E . m~rltilocularisin southwestern Manitoba is discussed.

SAMUEL, W. M., S . RAMALINGAM et L. N . CARBYN. 1978. Helminths in coyotes (Cunis latrans Say), wolves (Cunis lupus L.), and red foxes (Vulpes vulpes L.) of southwestern Manitoba. Can. I. Zool. 56: 2614-2617. Quarante-troiscoyotes, 12 loups et 6 renards roux captures dans une region avoisinante du Parc National Riding Mountain, dans le sud-ouest du Manitoba, ont ete examines afin d'en etudier les parasites. Onze especes parasitent le coyote, 8 le loup et 5 le renard roux. Alaria marciunae, Alaria arisaemoides et Toxu.scoris leonina se retrouvent chez les trois h6tes; Echinococcu.~ grunulosus, Taeniu hyctutigenu, Uncinariu stenocephc~laet Oslerus (Oslerus)osleri parasitent le loup et le coyote, Echinocc~ccusmultilocularis, le coyote et le reward. Tuenia pisiformis et T. lronina sont les especes les plus frequentes chez le coyote alors qu'E, multilocularis et E. granulosus y sont les plus abondantes. Echinococcus grunulosus est a lafois I'espece la plus frequente et la plus abondante chez les loups. Alariu marcianae et T. leonina ont It6 retrouvees chez tous les renards roux examines. La discussion polte notamment sur I'importance du coyote comme h6te terminal principal d'E. multiloculuris dans le sud-ouest du Manitoba. [Traduit par le journal]

Introduction

The ~ u r v o s eof this study is to determine the helminih faunas in several species of carnivores of wolves (Freeman et 01.; Holmes and Podesta 1968; Manitoba and 'Ompare between hosts and with results of other published Choquette et al. 1973), coyotes (Freeman er 1961; Holmes and Podesta 1968), and red foxes studies. Materials and Methods (Baron 1970) in Canada. Only one, Baron (1970), includes data from Manitoba. These surveys The coyotes and foxes used in this study were obtained from (Baron excluded) related the parasites found to the various areas within 50 km of Riding Mountain National Park, Manitoba, from November 1975 to March 1976. The area is food habits of the host. The results of these and dominated by agricultural lands that are interspersed with aspen Other studies (Erickson 1944; Butler and ~ ~ u n dstands and a network of small lakes and ponds. The Park lies mann 1954: Gier and Ameel 1959: Rausch and within the southern fringe of the boreal forest and contains ~ i l ~ i a m s o1959; n ' Rausch and Richards 1971) in- elements of the central gksslands in the southwest; the eastern dicate that the helminth fauna of coyotes and red deciduous forest is represented in the southeast. Coyotes and foxes were from areas south of the Park, while all foxes varies between regions studied, while that in but one wolf that was killed on a road in the park came from wolves is similar and predictable throughout North immediately adjacent to the park. Eight wolf carcasses America. were obtained from a trapper and two were poisoned with

several studies are available on the helminths of

TABLE 1. Helminths recovered from 43 coyotes, 12 wolves, and 6 red foxes of southwestern Manitoba (1975-1976) Coyotes


inf. Trematodes Alaria marcianae (2)* Alaria arisaemoides (2)

37 44

Cestodes Echinococcus granulosus (2) Echinococcus multilocularis (2) unidentified Taenia sp. (2) Taenia pisijormis (2) Taenia hydarigena (2) Taenia crassiceps (2)

9 23 9 67 7 0

Nematodes Toxascaris leonina (2) Uncinaria s~enocephala(2) Oslerus (Oskrus) osleri (4) Physaloptera sp. (1) Capillaria sp. (3)

65 28 47 7 2

Red foxes

Wolves

% inf.

md (range)

15.5 (1-101) 79 (3-673)

9 9 83 0 18 0 27 9

675 (374458) 888 (12 - 57 270) 4 . 5 (4-57) 9 (1-150) 5 (2-10)

4 (1-39) 12.5 (1-126) 4 (1-20) 3 (1-9) 1 (1)

9 36 9 0 0

md (range) 35 9

810 (20 - 126 000) 6 (1,ll) 5 . 5 (2,9) 1 5 1 (1-448) 3

% inf. 100 83 0 50 17 0 0 33 I00 0 0 0 0

-

md (range) 5 (1-10) 13 (1-90)

275 (1 1 - 354) 1 30 ( 1 9 4 1 ) 11 (5-66)

)

NOTE:% inf., percent infection. md median intensity. *Numbers in parentheses after hamis indicate location in host: (1) stomach, (2) small intestine, (3) large intestine, (4) lungs.

strychnine. Eleven wolves were collected during the winter of 1975-1976; one wolf was collected on November 17, 1977. According to radio-telemetric studies (Carbyn 1978), wolves spent most of their time in the Park. Carcasses were frozen until necropsy. Some organs such as liver, heart, spleen, and kidney were first examined macroscopically and then sliced into pieces to detect the presence of helminths. A small piece of diaphragm of less than 2cm2 was placed and pressed between two glass slides and examined under the compound microscope for larvae of Trichinellu spiralis (Owen, 1835). The lungs were injected with tapwater via the trachea until they were fully distended. The water was expelled by squeezing the lungs and the major air passages exposed. The water and the exposed respiratory tract were examined for the presence of parasites. The digestive tract was divided into various parts and perfused with tap water which was checked later for helminths. Helminths were detected by the aid of a dissecting microscope or with a magnifying light ( 2 x ) against a black background. Dilution counts (10 to 20% using tap water) were employed when high numbers (several thousand) of Echinococcus (Rudolphi, 1810) were encountered. Trematodes and cestodes were fixed in alcohol-formalin-acetic acid (AFA) and a few in each sample were stained in Harris or Delafield's hematoxylin. All specimens were mounted in balsam. Cestodes were identified using stailled specimens in good condition and by comparing rostellar hooks with known specimens. Hooks were mounted in aquamount. Approximately 100 Echinococcus were identified to species from animals with high numbers of this genus. Nematodes were fixed in glycerine-alcohol, cleared in lactophenol-beechwood creosote, and mounted in glycerine. Representative specimens of all species have been deposited in the United States National Helminthological collection (accession Nos. 74703-74723) and in the parasite collection of the Department of Zoology, University of Alberta.

Results and Discussion All wolves, foxes, and 42 of 43 coyotes had helminths; most (40143 616 wolves) had multiple infections. The mean number of species for coyotes, wolves, and foxes was 3.6,

2.0, and 3.7, respectively. A maximum of six species was found in three coyotes, three in three wolves, and five in one fox. Although 10 and 4 coyotes had Echinococcus multilocularis Leuckart, 1863, and E. granulosus (Batsch, 1786), respectively (Table I), none had both. The same was true for coyotes with the genus Taenia L., 1758: 28 had only T. pisiformis (Bloch, 1780), 3 had only T. hydatigena Pallas, 1776, and 3 had Taenia sp. The trematodes Alaria marcianae (LaRue, 1917) and A . arisaemoides Augustine and Uribe, 1927 were recovered from all three canids.' Frogs, the second intermediate host of these Alaria, or a wide variety of carnivorous or omnivorous vertebrate transport hosts (see Pearson 1956) must be part of the diet of all three canids in southern Manitoba. We found a few rodents, but no frogs in the stomachs of the coyotes and foxes. Rausch and Williamson (1959) mentioned the possibility that rodents could serve as transport hosts for A . marcianae. Alaria arisaemoides is apparently rare in wolves having been found only once previously (Choquette et al. 1973). Taenia pisiformis and E . multilocularis were the most prevalent cestodes in coyotes. While E. multilocularis has been reported from coyotes only once previously (Leiby et al. 1970), similar prevalences of T. pisiformis have been reported for coyotes of Alberta and elsewhere (see Holmes and Podesta 1968). Leiby et al. (1970) found E. mul-

-

'We agree with Dubois (1970) in considering that Aluriu umericana Hall and Wigdor, 1918 is a synonym ofA. marcianae based on variation in measurements of important characters such as thickness of the wall of the ejaculatory pouch.


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CAN. J . ZOOL. VOL. 56, 1978

tilocularis in only 7 of 171 coyotes in the northcentral United States, but attributed this low prevalence to the facts that most coyotes examined came from regions of low prevalences of the cestode in the intermediate hosts and were collected during winter, a period when E. multilocularis is least prevalent in the definitive host. They suggested that "the coyote would probably serve as the principal natural definitive host ... [in areas] where the red fox is not abundant and the population densities of coyotes are relatively high." Coyotes are common and foxes are rare in Riding Mountain National Park (Carbyn, unpublished data). Since many of the coyotes were trapped very close to the Park boundary, they came from areas essentially fox free. Echinococcus multilocularis was not encountered in coyotes from the forested areas of Alberta (Holmes and Podesta 1968) or Ontario (Freeman et al. 1961), suggesting that E. multilocularis is limited to the agricultural regions of central Canada. Samuel (unpublished data) recovered 3300 E. multilocularis from a coyote of the aspen parkland of central Alberta in winter, 1973. This is the third report of E. multiloculuris in red foxes of Canada, the others coming from Saskatchewan (Hnatiuk 1969; one fox) and south-central Manitoba (Baron 1970; one fox). Echinococcus multilocularis is widely distributed in the agricultural biomes of the north-central United States and south-central Canada. The most easterly reports have been from Minnesota, Iowa, and Manitoba (Leiby et al. 1969; Leiby et al. 1970; Baron 1970), while the westerly reports have been from Montana and Alberta (Seesee and Worley 1976; Holmes et al. 1971). Rausch (1967) proposed that the endemic focus of E. multilocularis in central North America is either disjunct from the tundra (that is, with the intervening taiga and (or) boreal forest serving as ecological barriers) or it may be the southern extremity of a continuous distribution from the tundra. Results of the present study do not resolve this issue; however, they do present the first evidence of E. multilocularis within the southern fringe of the boreal forest. Critical survey data are required from more northerly forested regions of Manitoba (see Fig. 3, Rausch 1967). Echinococci(s granulosus was the most prevalent and numerous cestode of wolves. A wolfmoose (Alces alces (L.)) or wapiti (Cervus elaphus L.) cycle for E. granulosus is to be expected in Riding Mountain Park (see discussion of Samuel et al. 1976).

Taenia krabbei Moniez, 1879, is probably absent from the Riding Mountain area. Its absence in an area where moose and wolves coexist is unique considering the many reports of high prevalences of T. krabbei in these hosts in the boreal forests of Canada. Wolves with T. krabbei could enter the area from the northern boreal forests from time to time, but for unknown reasons the parasite has not become established. The fact that wolves of the Park have tended to eat more white-tailed deer and wapiti than moose in recent years (Carbyn 1978) could be involved. Cysticerci of Taeniu krabbei have never been reported from wapiti or whitetailed deer (Odocoileus virginianus (Zimmermann)) (Holmes and Podesta 1968; see Samuel 1972). Based on literature and results of this study, Toxascuris leonina is not a common parasite of wolves in the southern portion of their range; it is common in wolves of Alaska (Rausch and Williamson 1959) and the tundra of the Northwest Territories (Choquette et al. 1973). Results of the present study in Manitobaare similar to those for wolves and coyotes of Alberta and other areas; that is, "wolves and coyotes are susceptible to infection with the same helminths" (Holmes and Podesta 1968). Seven of 12 helminths identified in this study were found in both hosts. Thus, the differences in prevalence are probably due to differential exposure, "caused by differences in food availability and (or) food habits" (Holmes and Podesta 1968). The low prevalences of T. leonina and Alaria spp. in wolves of Riding Mountain Park suggest that wolves there consume relatively few small rodents, while the higher prevalences of rodent-transmitted helminths in coyotes and foxes possibly reflect the higher intake of small mammals by them. Such food habits have been reported for wolves (Pimlott 1967) and coyotes (Fichter et al. 1955). Rausch and Richards (1971) found a high percentage of rodents in the stomachs of red foxes of northern North Dakota. Percentage infection of the rodent-transmitted parasites in their study was 70, 27, 11, 55, 42 and 97% for E. multilocularis, T. crussiceps (Zeder, 1800), Mesocestoides kirbyi (Chandler, 1944), Alaria arisaemoides, A . marcianae, and Toxascaris leonina, respectively. This is the first published paper dealing with helminths of coyotes and wolves of Manitoba. Results support the conclusion of Holmes and Podesta (1968) that the relative frequencies of helminths with different intermediate hosts appear to generally reflect the diet of the wild canid in question.

NOTE


They also suggest that the coyote and red fox are major definitive hosts of E. multilocularis in southwestern Manitoba. Acknowledgements We gratefully acknowledge the trapping efforts of N . Brazeau, Erickson, Manitoba, and the technical assistance of S. Rickabaugh and M. Barker, University of Alberta. R. L. Rausch, University of Saskatchewan, and A. Johnson, University of South Dakota, kindly provided specimens of A . murcianae from a coyote of Oregon, an experimentally infected dog and cat, and a naturally infected gray fox, Urocyon cinereoargenteus (Schreber). BARON,R. W. 1970. The occurrence of Echinococcus multiloc~rlarisLeuckart, 1863 and of other helminths in the red fox, Vulpes vulpes, in southern Manitoba. Can. J. Zool. 48: 1132. BUTLER,J. M., and A. W. G R U N D M A N1954. N . The intestinal helminths of the coyote Canis 1atrun.s Say, in Utah. J . Parasitol. 40: 440-443. CARBYN,L. N. 1978. Preliminary analysis of wolf-ungulate interactions with specific reference to moose in Riding Mountain National Park, Manitoba. Proc. 13th Annu. N. Am. Moose Workshop Conf., April, 1977, Jasper, Alta. pp. 283-289. CHOQUETTE.L. P. E., G. G. GIBSON,E. KUYT,and A. M. PEARSON.1973. Helminths of wolves, Canis lupus L., in the Yukon and Northwest Territories. Can. J. Zool. 51: 1087- 1091. DUBOIS, G. 1970. Synopsis des Strigeidae et des Diplostomatidae (Trernatoda). Deuxieme partie. Mem. Soc. Neuchatel. Sci. Nat. 19(2): 259-727. ERICKSON,A. B. 1944. Helminths of Minnesota Canidae in relation to food habits, and a host list and key to the species reported from North America. Am. Midl. Nat. 32: 359-372. FICHTER,E., G. SCHILDMAN, and J. H. SATHER.1955. Some feeding patterns of coyotes in Nebraska. Ecol. Monogr 25: 1-37. FREEMAN, R. S., A. ADORIAN, and D. H. PIMLOTT.1961. Cestodes ofwolves, coyotes, and coyote-dog hybrids in Ontario. Can. J . Zool. 39: 527-532.

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GIER,H. T., and D. J . AMEEL.1959. Parasites and diseases of Kansas coyotes. Kansas State Univ. Agric. Exp. Stn. Tech. Bull. 91. H N A T I U KJ., M. 1969. Occurrence of Echinococcus multilocularis Leuckart, 1863 in Vulpes fulva in Saskatchewan. Can. J . Zoo1.47: 264. HOLMES,J. C., J . L. MAHRT,and W. M. SAMUEL.1971. The occurrence of Echinococcus multilocularis Leuckart, 1863 in Alberta. Can. J. Zool. 49: 575-576. HOLMES,J . C., and R. PODESTA.1968. The helminths ofwolves and coyotes from the forested regions of Alberta. Can. J . Zool. 46: 1193- 1204. LEIBY,P. D., W. P. CARNEY, and C. E. WOODS.1970. Studies on sylvatic echinococcosis. 111. Host occurrence and geographic distribution of Echinococc~tsmultilocularis in the north central United States. J. Parasitol. 56: 1141-1 150. LEIBY,P. D., G . LUBINSKY, and W. GALAUGHER. 1969. Studies on sylvatic echinococcosis. 11. The occurence ofEchinococclts multilocularis Leuck. 1863, in Manitoba. Can. J . Zool. 47: 135-139. PEARSON. J . C. 1956. Studies on the life cycles and morphology of the larval stages of Alaria urisaemoides ~ u ~ u s 6 nand e Uribe, 1927 and Alaria cunis LaRue and Fallis, 1936 (Trematoda:Diplostornidae). Can. J. Zool. 34: 295-387. RMLOTT,D. H. 1967. Wolf predation and ungulate populations. Am. Zool. 7: 267-278. RAUSCH,R. L. 1967. On the ecology and distribution of Echinococcus spp. (CestodxTaeniidae) and characteristics of their development in the intermediate host. Ann. Parasitol. Hum. Comp. 42: 19-63. RAUSCH,R. L., and S. H. RICHARDS. 1971. Observations on parasite-host relationships of Echinococcus multilocularis Leuckart. 1863. in North Dakota. Can. J. Zool. 49: 1317-1330. RAUSCH.R. L.. and F. S . L . W ~ L L ~ A M S1959. O N . Studies on the helminth fauna of Alaska. XXXIV. The parasites of wolves, Canis lupus L. J. Parasitol. 45: 395-403. SAMUEL, W. M. 1972. Taenia krabbei in the musculature of moose. A review. R o c . 8th Annu. N . Am. Moose Workshop Conf., Thunder Bay, Ont. pp. 18-41. S A M U E LW. , M., M. W. BARRETT,and G. M. LYNCH.1976. Helminths in moose of Alberta. Can. J. Zool. 54: 307-312. SEESEE,F. M., and D. E. WORLEY.1976. The occurrence of Echinococcus multilocularis Leuckart , 1863 (Cestoda:Taeniidae) in the red fox, Vulpes vulpes L., in southwestern Montana. Proc. Mont. Acad. Sci. 36: 145-149. - -