Helminths of Big Game Mammals in South Dakota*

Major L. Boddicker and Ernest J. Hugghins
South Dakota State University,
Brookings, South Dakota 57006

Abstract 

A study was undertaken to determine the incidence, distribution, and relative importance of helminths in wild ruminants of South Dakota. Big game species examined and numbers of helminth species found were as follows: 83 white-tailed deer (5 species of nematodes, 3 of cestodes), 30 mule deer (3 spp. of nematodes, 3 of cestodes), 60 pronghorn antelope (13 spp. of nematodes, 2 of cestodes), 20 elk (3spp. of nematodes, 2 of cestodes), 5 bison (7 spp. of nematodes, 1 of cestode), 3 bighorn sheep (6 spp. of nematodes, 2 of cestodes ) , and one mountain goat (3 spp. of nematodes). There were new host records for several species of nematodes. The absence of trematodes was conspicuous. The pronghorn antelope was the most heavily parasitized of the 7 species sampled. Since they occur on livestock rangelands in the western part of the state, they may have some importance as reservoirs for helminths of sheep and cattle. The presence of lungworms , Protostrongylus spp., in the bighorn and mountain goat merits further investigation, as lungworrns have been implicated as limiting factors in populations elsewhere.

Reprinted from The Journal of Parasitology, Vol.55, No. 5, October 1969

Helminths of Big Game Mammals in South Dakota*

Seven species of big game mammals occur in South Dakota, viz., mule deer, white-tailed deer, pronghorn antelope, elk, mountain goat, bighorn sheep, and bison. All except bighorn are hunted, either in regular hunting seasons or in strictly controlled, limited hunts and herd thinning operations. Aside from the importance of these animals to sportsmen , many of them occur on rangelands utilized by domestic livestock and are of importance to stockmen. There has been no previous state-wide study on the parasites of these game mammals. This study was undertaken to determine the incidence, distribution, and relative importance of helminths in wild ruminants of the state.

A companion study involved a sampling of many of these same animals for pesticide residues, the results of which have been reported here (Greenwood et al., 1967; Moore et al., 1968).

Methods

Most of the visceral samples of the deer, pronghorn antelope, and elk were collected during the hunting seasons of 1964 and 1965, through the cooperation of hunters and of personnel in the South Dakota Department of Game, Fish and Parks. Viscera of bison were collected during operations in Custer State Park, Hermosa, South Dakota. The bighorn sheep, which died of natural causes, were from a herd in the Badlands National Monument. Viscera with data cards were placed in individual plastic bags and frozen until examination. Viscera examined included the following organs: gastrointestinal tract, respiratory system, urogenital system, and liver and heart when not retained by the hunter. The contents of the abomasum were screened through a No.25, 24-mesh Fisher sieve with openings of 707 m to remove fine debris. The screened material was placed in 1,000-ml cylinders filled with tap water, where much of the remaining debris floated to the top while helminths settled to the bottom. The supernatant was poured off, scanned for helminths, and discarded. The sediment was poured into a black-bottomed tray and examined carefully under a binocular micro- scope. The mucosa of the abomasum was examined also. The intestines were stripped from the mesenteries, and the contents flushed with tap water under pressure into a large pan. The contents were then examined using the technique of screening and sedimentation described above. Selected portions of mucosa were examined. Livers, kidneys, and hearts were cut open to examine larger cavities and then were cut into l-cm slices. Tracheae and bronchi were opened, and lung parenchyma was palpated carefully for hardened areas. Abnormal appearing tissues were examined microscopically.

* Parts of a thesis submitted by the senior in partial fulfillment of the requirements for the M. S. degree. Published with the approval of the Director of the South Dakota Agricultural Experiment Station as publication No.87 of the journal series.

Cestodes were flattened between glass slides, fixed, stained, and mounted on permanent slides. Nematodes were fixed in alcohol-formalin-acetic acid solution and then transferred to a glycerin- alcohol mixture. As the alcohol evaporated, the nematodes were brought gradually into pure glycerin for clearing and storage.

White-tailed deer, Odocoileus virginianus (Boddaert, 1184)
This animal is widely distributed in South Dakota, from the farm and prairie-lake country of the east to the open rangelands and forested Black Hills of the west. It comprises approximately three-fourths of the deer harvested annually by the hunters .in the state. The helminths recovered from 83 white-tailed deer are listed in Table I. Arthropod parasites from these deer have been reported previously (Boddicker and Hugghins, 1969)

Parasites of white-tailed deer have been extensively surveyed in North America. Anderson (1962a, b) has compiled comprehensive reviews of these parasitisms. Our study of white-tailed deer in South Dakota indicated that they were lightly parasitized. A new western distribution record is herein reported for Ostertagia odocoilei Dikmans, 1931 (USNM Helm. ColI. 66038, 66039), of which 24 specimens were found in one deer and 10 specimens in another from Lincoln County in eastern South Dakota. This species has been reported previously in white-tailed deer from Pennsylvania (Dikmans, 1931), Louisiana (Dikmans, 1933), New York (Dikmans, 1934), and Florida (Dinaberg, 1939) New distribution records for Dictuocaulus viviparus (Block, 1782) and Setaria cervi (Rud.,1819) are a1so reported.

The absence of trematodes was of interest, since Erickson et al. (1961) reported Fascioloides magna (Bassi, 1875) to be a common parasite of white-tailed deer in neighboring Minnesota.

Mule deer, Odocoileus hemionus , (Rafinesque, 1832)
The range of the mule deer overlaps that of; the white-tailed deer in South Dakota, but the mule deer is not as abundant. Mule deer are most numerous on the prairies west of the Missouri River and in the breaks of the Missouri River and its tributaries.

Arthropod parasites from these deer have been reported previously (Boddicker and Hugghins, 1969) .The incidence of parasitism in the mule deer was somewhat higher than in white-tailed deer but infections were relatively light. The three helminths showing highest incidence were species known to occur in domestic livestock, namely, Thysanosoma actinioides Dies., 1834; Taenia hydatigena Pallas, 1766; and Haemonchus contortus (Rud., 1803) .

Pronghorn antelope, Antilocapra americana (Ord, 1815)

Pronghorn antelope are abundant on the western rangelands of South Dakota. Reports of explorers during the mid-nineteenth century indicated that pronghorns exceeded bison in numbers over the entire territory at that time. With the coming of civilization, their numbers dwindled almost to the point of extinction in South Dakota, until protective legislation was enacted in 1911. They recovered slowly, and in 1941 annual fall hunts were initiated after a closed season of 30 years. The pronghorn population in 1964 was estimated to be nearly 25,000 animals, and more than 6,000 of them were harvested by hunters that year. Pronghorn antelope, cattle, and sheep often share the same range. They have been found to carry many of the same helminths, according to Ransom (1911) , Dikmans (1939) , and Goldsby and Eveleth (1954). Helminths have been shown to cause death in lambs and pronghorn kids sharing the same range in South Dakota (Bever, 1950) and in Wyoming (Honess and Winter, 1956).

Only one animal was free of helminths; most were heavily parasitized. The four helminths found most frequently were Haemonchus contortus, Pseudostertagia bullosa ( Ransom et Hall, 1912), Ostertagia ostertagi (Stiles, 1892), and Nematodirella longissimespiculata (Romanovitsch, 1915) .The first three species occurred in the abomasum, the fourth in the duodenum. When these parasites were present in large numbers, hemorrhagic lesions were observed in the mucosa.

The finding of Cooperia sumabada Antipin, 1931, constitutes a new host record (USNM Helm. Coll. 65937) According to Allen and Becklund (1958) and Becklund (1963), C. surnabada probably is conspecific with C. mcmasteri Gordon, 1932, but the former was described in Russia and its type or authenticated specimens have not been available for study. These species under one or the other name have been reported from cattle in a number of states (Becklund, 1964) but not from wild ruminants. Becklund (1963) stated further that these species have been confused with the common species, C. oncophora ( Railliet, 1898) .The finding of Setaria cervi (USNM Helm. Coll. 6.5934) constitutes another host record. These nematodes we found in seven pronghorns, usually occurring along the mesenteries in the coelomic cavity.

Cestodes were not as numerous as nematodes in the antelope. The sheep tapeworm, Moniezia expansa (Rud., 1810), was found in 16.7% of the 60 pronghorns examined. This parasite was considered by Honess and Winter (1956) to be a serious pest of young deer and pronghorns in Wyoming during the summer and fall, but serious effects were not observed in our South Dakota study. Since the fringed tapeworm, Thysanosoma actinioides, is widespread in sheep of western South Dakota, special vigilance was exercised for this parasite in the pronghorns. It was found in only four of the 60 pronghorns examined. Moreover, it occurred only in the small intestine rather than in the bile passages of the liver the common site in sheep. It is of interest that the fringed tapeworm was not reported from pronghorns in neighboring North Dakota by Goldsby and Eveleth (1954), nor from neighboring Wyoming by Honess and Winter (1956) , during their extensive investigations; these findings strengthen the impression that the fringed tapeworm is an infrequent parasite of pronghorns. This view was held by Allen and Samson (1960) in New Mexico until they examined nine pronghorns from the same locality and found them heavily infected with fringed tapeworms, thus showing that under some circumstances pronghorns may harbor much heavier infections than indicated by prior reports.

Elk, Cervus canadensis (Erxleben, 1777)

Elk formerly were distributed over the entire state but were exterminated by 1900. A herd was reestablished in Custer State Park in 1914. The Park herd is maintained at about 600 animals by holding a controlled hunt each year. Approximately an equal number of elk roam the Black Hills outside the Park, and a limited number of permits are granted annually to control them. New host records are reported for two nematodes, Nematodirella longissimespiculata (USNM Helm. Coll. 65939) and Nematodirus helvetianus May, 1920 USNM Helm. Coll. 59375). Five of the elk harbored the fringed tapeworm, Thysanosoma actinioides, in the small intestine.

Bighorn sheep, Ovis canadensis Shaw, 1804

Although once common in South Dakota, the last native bighorn was shot in 1924 in the Badlands. In the winter of 1963-64, 22 bighorns from Colorado were introduced into the Badlands National Monument in an effort to reestablish them in that area. Two of the animals died in May and June, respectively, 1964, only a few months after having been released in South Dakota. The lungs of both sheep were heavily infected with Protostrongylus rushi Dikmans, 1937 (USNM Helm. Coll. 58237). There were large triangular areas of discolored lung tissue containing worm eggs and larvae, and adult worms were found in bronchioles and bronchi. This appeared to be a typical lungworm-pneumonia complex as reported by various authors. Pneumonia was the cause of death in the first sheep, as determined by Dr. G. S. Harshfield, veterinarian at South Dakota State University. Several investigators have elaborated upon the importance of lungworms in bighorns, such as Honess and Winter (1956) in Wyoming, Pillmore (1961) and Moser (1962) in Colorado, Forrester and Senger (1964) in Montana, and McCullough and Schneegas (1966) in California. Becklund and Senger (1967) in their checklist of bighorn parasites summarized the reports of lungworms from this host in North America.

Mountain goat, Oreamnos americanus (Blainville, 1816)

Mountain goats in South Dakota are restricted to a small area in the highest and most rugged portions of the Black Hills. They are not indigenous. The herd got its start in 1924 when a few goats escaped from Custer State Park Zoo and made their way to the Harney Peak area. They reproduced until the herd numbered approximately 350 animals. Because of the limited range, overcrowding, and a fluctuating population, we were interested in sampling the goats for helminths.

The most important finding in the 1.5-year- old male goat examined was the presence of the lungworm, Protostrongylus stilesi Dikmans, 1931 (USNM Helm! Coll 6.593.5) .The lungs had large swollen areas of hardened tissue along the psterior borders of the lobes. Examination revealed large numbers of embryonated eggs and larvae, as well as portions of adult worms in the parenchyma. Hanson (1949) stated that his examinations of fecal samples from the goats in the Black Hills revealed no lungworm larvae. Although there are numerous reports of P. stilesi from bighorn sheep (summarized by Becklund and Senger, 1967, in addition to our report from bighorns in this paper), this appears to be the third report of the species from mountain goats, the other reports being those of Cowan (1951) and Kerr and Holmes (1966).

The abomasum contained about 100 specimens of Ostertagia circumcincta (Stadelmann, 1894) , which apparently has been reported only twice previously from mountain goats (Cowan, 1951; Kerr and Holmes, 1966), although this species seems to be widely distributed in both wild and domestic ruminants of North America as indicated by Ransom (1911) and Dikmans (1939) .This situation seems to be true also in the Andean region of South America, as 0. circumcincta has been reported from vicunas, alpacas, llamas, sheep, and goats in the Peruvian highlands (Chavez and Zaldivar, 1967) .

American bison, Bison bison (Linnaeus, 1758)

The last large-scale buffalo hunt in the United States took place in northwestern South Dakota (then Dakota Territory) in 1881 near the present site of Lemmon. Five calves from this famous "Last Hunt" (popularized by the MGM movie) were taken to the Dupree Ranch on the Cheyenne River and allowed to run with cattle. Progeny from these bison, together with bison purchased from the Sioux Indians on the Pine Ridge Reservation, were placed in the newly established Custer State Park in the Black Hills in 1914. Thus this herd, which is maintained at approximately 1,200 animals, may be classed as indigenous to the state.

Ostertagia bisonis Chapin, 1925, was present in the abomasum of three bison, the heaviest concentration being approximately 50 nematodes in one animal. This appears to be the only report of this species in bison since Chapin's (1925) original description, although it has been reported from cattle by Dikmans (1942), Olsen (1949), Honess and Bergstrom (1963), and Worley and Sharman (1966) .The latter two reports implicated O. bison is with bovine gastritis. Since the inadequate original description had led to some confusion by various workers, Becklund and Walker (1967) redescribed O. bisonis utilizing some of our specimens. They stated that our male specimens (USNM Helm. Coll. 59384 and 59387) were found to be considerably larger than the paratypes.

A single male specimen of Ostertagia trifurcata Ransom, 1907 (USNM Helm. Coll. 59388) was found with an infection of 0. bisonis. The spicules were 25 m longer than those of O. bisonis and the gubernaculum was larger. This constitutes a new host record for O. trifurcata. According to Becklund (1962, 1963) the close resemblance between males of O. trifurcata and Teladorsagia davtiani An. dreeva et Satubaldin, 1954, has resulted in the deposition in the U. S. National Museum Helmithological Collection of many specimens of T. davtiani misidentified as O. trifurcata, so that many reports of the latter species from 11 states including Alaska are invalid.

Cooperia oncophora was present in three bison, the numbers being less than 50 per animal. The specimens were identical to those described by Cram (1925) as C. bisonis, but Gilmore and Allen (1960) clarified the status of this species as being a synonym of C. oncophora of cattle. A similar species, C. surnabada Antipin, 1931 (USNM Helm. Coll. 59374) was found in one bison, constituting a new host record. This species also was found in a pronghorn (discussed above).

A single male specimen of Chabertia ovina (Fabricius, 1794) was recovered from the cecum of one bison. This nematode has been listed from a variety of wild and domestic ruminants (Ransom, 1911; Yamaguti, 1961; Becklund, 1964) , but this report apparently is a new host record for bison.

Discussion

This was the first extensive parasite study conducted on the seven species of wild ruminants occurring in South Dakota. The cervids (white-tailed deer, mule deer, and elk) were lightly parasitized, and there appeared to be little harmful effect. Among the bovids, the most important finding was the presence of lungworms, Protostrongylus stilesi and P. rushi, in the bighorn sheep and mountain goats. These parasites have been demonstrated to be limiting factors in populations of these ruminants elsewhere, and the infection in the respective herds of wild sheep and goats in South Dakota merits further attention, particularly in view of the restricted range of the herds.

The American bison harbored several species of stomach worms which are potentially damaging, the most notorious being Haemonchus contortus. The bison also harbored Ostertagia bisonis, a nematode which has recently been found associated with bovine clinical helminthiasis in neighboring Wyoming (Honess an ales Bergstrom, 1963) and Montana (Worleyan and Sharman,1966).

The antilocaprids were by far the most heavily parasitized of the wild ruminants, both as to number of species of parasites and level of parasitims. The pronghorns rank next to deer in importance as big game mammals are South Dakota. Only the deer and the pronghorns enjoy wide distribution within the state and utilize large areas of range occupied by domestic livestock.

The disparity in parasite burdens in these two kinds of wild ruminants may be a reflection of their differences in food habits. Pronghorns feed upon short prairie forage which would increase their chances of picking up nematode eggs and larvae, as well as oribatid mites containing Moniezia. It is highly probable that the pronghorns and domestic livestock pass many helminths to each other.

Several new host records are reported namely, Nematodirella longissimespiculata and Nematodirus helvetianus from elk; Cooperia surnabada and Setaria cervi from pronghorn antelope; Ostertagia trifurcata, Cooperia surnabada and Chabertia ovina from American a bison. A western distribution record is Osterstagia odocoilei from white-tailed deer. This is only the third host record for Protostrongylus stilesi and Ostertagia circumcincta from mountain goats.

The paucity of platyhelminths in comparison to nematodes was noteworthy. No trematodes were found, which might be due in part to the semi arid nature of much of the habitat. Although no liver flukes were found, it should be mentioned that hunters often retained the liver, so that many more gastrointestinal tracts were examined than livers.

The incidence of the fringed tapeworm, Thysanosoma actinioides, was of interest because this is a very common parasite of domestic sheep on the western range. Light infections were found in white-tailed deer, mule deer, elk, and pronghorn antelope in South Dakota. It has been reported from pronghorns (Gilmore and Allen, 1960) and elk (Wilson, 1969) in New Mexico, from mountain goats in Alberta, Canada (Kerr and Holmes, 1966), and from bighorn sheep in several western areas from Arizona to British Columbia (Becklund and Senger, 1967) .There has been speculation as to whether this tapeworm was indigenous to wild ruminants in the west before domestic livestock was introduced (Allen, 1959), having first been recovered from a Brazilian deer in 1824. Chavez and Zaldivar ( 1967) have reported the fringed tapeworm as being widespread in sheep of the Peruvian highlands but have not reported it from the llama group (neither from domestic llamas and alpacas nor from wild guanacos and xicunas examined for parasites) The life history has long been a puzzle. Allen (1959) infected psocids experimentally, but there is still a question as to the natural intermediate host of this interesting tapeworm.