II
TRANSMISSION AMONG AND BETWEEN SPECIES

Much public discussion has centered on whether transmission of B. abortus in the wild ever can be documented. This section reviews epidemiologic evidence of transmission and associated factors, including the role of bison and elk behavior and the effects of weather on animal movement in the GYA. The National Park Service's natural-regulation policy is discussed, as is the effect of B. abortus on reproductive potential of bison.

BISON, ELK, AND CATTLE

Brucellosis was discovered in bison on first testing in 1917 (Mohler 1917), and it has existed since as a self-perpetuating disease in that species. Thus, transmission from cattle introduced by Europeans to at least one wild species must have occurred and then transmission from cattle or from the infected wild species to other wild species to account for the disease in cattle, bison, and elk (Honess and Winter 1956). Meagher and Meyer (1994) note that there were probably multiple transmissions to bison, and Thorne et al. (1991) note that recovery of B. abortus biovars 1 and 4 in Wyoming and the presence of B. abortus widely over the GYA suggest multiple exposures in elk as well. It seems likely, in view of the early free-range management of domestic stock in the West, that original transmission of the disease from livestock to bison and elk occurred during intermingling in the free-roaming state. However, at the beginning of the 20th century, restoration programs for bison (Garretson 1938) and elk (Murie 1951) resulted in capture, handling, and relocation of large numbers of both species, so the possibility of transmission in captivity cannot be ruled out.

Transmission of brucellosis from captive bison to cattle in North Dakota



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II TRANSMISSION AMONG AND BETWEEN SPECIES Much public discussion has centered on whether transmission of B. abortus in the wild ever can be documented. This section reviews epidemiologic evidence of transmission and associated factors, including the role of bison and elk behavior and the effects of weather on animal movement in the GYA. The National Park Service's natural-regulation policy is discussed, as is the effect of B. abortus on reproductive potential of bison. BISON, ELK, AND CATTLE Brucellosis was discovered in bison on first testing in 1917 (Mohler 1917), and it has existed since as a self-perpetuating disease in that species. Thus, transmission from cattle introduced by Europeans to at least one wild species must have occurred and then transmission from cattle or from the infected wild species to other wild species to account for the disease in cattle, bison, and elk (Honess and Winter 1956). Meagher and Meyer (1994) note that there were probably multiple transmissions to bison, and Thorne et al. (1991) note that recovery of B. abortus biovars 1 and 4 in Wyoming and the presence of B. abortus widely over the GYA suggest multiple exposures in elk as well. It seems likely, in view of the early free-range management of domestic stock in the West, that original transmission of the disease from livestock to bison and elk occurred during intermingling in the free-roaming state. However, at the beginning of the 20th century, restoration programs for bison (Garretson 1938) and elk (Murie 1951) resulted in capture, handling, and relocation of large numbers of both species, so the possibility of transmission in captivity cannot be ruled out. Transmission of brucellosis from captive bison to cattle in North Dakota

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was reported by Flagg (1983). The strongest evidence of transmission between free-roaming bison and elk comes from Grand Teton National Park (GTNP) and National Elk Refuge (NER) in the Jackson area of Wyoming (Williams et al. 1993, 1997). A small herd of bison was established in the wildlife park at GTNP in 1948 and in 1963 was found to be infected by B. abortus. All adults were removed, and calves were vaccinated. Brucellosis-free bison were introduced from Theodore Roosevelt National Memorial Park in 1964. This population was tested thereafter; calves were vaccinated, and all seropositive animals were removed. The last identified reactor was removed in 1967, and all adult bison tested negative in 1968. Late in 1968 and in 1969, some bison escaped from the wildlife park, and attempts were made to return them to the park. By 1970, however, nine bison were free-roaming because they could not be recaptured. The herd subsequently grew in numbers (Peterson et al. 1991b). About 1980, the animals began to winter on the NER, where they came into contact with winter-fed elk that were known to be infected with brucellosis. Cattle were not present on NER. In 1989, 11 of 16 bison collected on NER tested seropositive for brucellosis. On the basis of their modeling results, Peterson et al. (1991b) believed that the bison became infected in about 1980, and they noted that the bison herd first wintered on the NER, a potential source of B. abortus from winter-fed elk, in 1979-1980. Because the GTNP bison herd is isolated from the YNP bison herd by the continental divide, infection in GTNP bison is assumed to have derived from their contact with infected elk on the wintering grounds. Although the possibility of brucellosis having survived in the bison at the time of their escape from the wildlife park cannot be ruled out, transmission from elk seems more probable. Two horses contracted brucellosis in the Jackson, Wyoming, area, where the only known source of the disease was elk on the winter feeding grounds (see p. 35, ''True Prevalence"). One of the most contentious issues—because it is key to determining the need for control of the disease in GYA wildlife—is the probability of transmission of brucellosis between free-roaming bison and domestic livestock. Nearly all parties to the controversy agree that the risk of transmission of brucellosis from bison to cattle in the GYA is small, but not zero. Defining small depends on whether transmission has occurred in the past and, if so, how often. That is key to determining the need to control brucellosis in bison. Advocates of no control maintain adamantly that no case of transmission of brucellosis from bison to cattle in the free-roaming state in the GYA ever has been documented. Advocates of the need to control the disease in bison to protect livestock in the surrounding areas maintain equally stoutly

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that there is clear epidemiologic evidence that transmission from wildlife has occurred at least six times in the recent past, two of which might have been due to bison. EPIDEMIOLOGIC EVIDENCE OF TRANSMISSION FROM WILDLIFE TO CATTLE The differing interpretations of epidemiologic evidence on the two sides of the issue are the crux of the controversy. This evidence is summarized in a field report submitted to APHIS in December 1996. Between about 1961 and 1989, cattle on six ranches in the GYA became seropositive for brucellosis after testing brucellosis-free. One of the ranches was east and five were west of the continental divide in the Jackson Hole region. The evidence consisted of seropositive tests for brucellosis in cattle herds in which the disease had not previously been present, and no known source of infection occurred in cattle in the local area or in stock imported to the properties. On each of five ranches, a single outbreak occurred. On the sixth ranch, brucellosis appeared in a cattle herd in about 1961 (the exact date is not known); it was thought to have been eliminated, and the herd was found again to be seropositive when retested in 1969. One outbreak in 1988 and another in February 1989 (Cariman 1994) led to a court case in which the Parker Land and Cattle Company sued the U.S. government for damages for failing to control elk movements from the NER to private lands (Parker vs. U.S.A. and Peck vs. U.S.A. 1992). The court concluded that the brucellosis outbreak was most likely caused by contact with infected elk or bison but the plaintiffs failed to prove that the elk or bison came from the NER, GTNP, or YNP. Several elk winter feeding grounds operated by the Wyoming Game and Fish Department are between the Parker ranch and the NER. No outbreak of brucellosis in cattle in that problem area has been reported since 1989. Cattle producers in the GYA routinely vaccinate their herds for brucellosis. Vaccination is required in Idaho and strongly recommended in Montana and Wyoming. In four of the cases, anecdotal evidence was provided that elk were adjacent to or moving onto the property; the other two cases included anecdotal evidence of elk and bison presence. Most of the elk were associated with various winter feeding grounds on which elk concentrations foster transmission of B. abortus. Free-roaming elk herds, thought at the time of the first reports not to carry brucellosis, were found on further testing to have a relatively high proportion of seropositive individuals. By 1977, brucellosis had been detected on feeding grounds (Thorne et al. 1997). The bison in

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both cases would have come from the GTNP herd, in which 69% of individuals tested in 1988-1989 were seropositive for brucellosis (Peterson et al. 1991a,b; Williams et al. 1993, 1997). Those six cases of purported transmission of brucellosis from wildlife to cattle are based on circumstantial evidence. The facts were derived from field operations of the federal-state cooperative program to eliminate brucellosis from domestic cattle in the United States. The data never were intended to meet the standard of scientific research, and inconsistent record retention resulted in further gaps in the documentation. The cases were summarized after the fact, some without supporting documents, which were discarded in the meantime. The only thing definite is that cattle in the herds tested seropositive for brucellosis. Assuming that elk and bison were in contact with cattle, there is no way to determine whether they were infective at the time and whether opportunity for transmission presented itself. Similarly, the possibility of infection from cattle is difficult to eliminate entirely, because it is always hard to prove that an event did not happen. Some observers have noted that in states that have eliminated brucellosis from cattle in the past, occasional outbreaks are typical for some time after a state has been declared class-free by APHIS. That is because the disappearance function of the disease does not decline to zero at a constant rate but rather has a tail of gradually decreasing probability. Given the pattern of outbreaks in cattle in the GYA, with no new cases since 1989, this area might simply be mimicking the temporal pattern observed elsewhere where transmission from wildlife was not an issue. Or it could be maintained that the lack of outbreaks since 1989 is attributable to diligent cattle vaccination by ranchers. Given the ambiguity allowed by epidemiologic evidence in this situation, wildlife cannot be determined to be the source of brucellosis infection in these six cases. BISON AND ELK BEHAVIOR AND TRANSMISSION Considerable caution should be exercised in extrapolating results from cattle to bison beyond the consideration of a long, separate evolutionary history. There are fundamental differences between how cattle are managed and the natural behavior of free-roaming bison in the GYA. First, domestic bulls are placed with cows in lower relative numbers (typically 1:20 to 1:30) than the sex ratios of unmanipulated bison of about 1:1, or slightly skewed toward females (Meagher 1973; Van Camp and Calef 1987; Berger and Cunningham 1994). Second, domestic bulls are placed with cows only during the breeding

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period, then removed; the bison sexes can intermingle throughout the year. Third, courtship is perfunctory in domestic stock because the highly skewed sex ratio largely eliminates male-male competition. Bison males compete strongly for females, and dominant bulls form close "tending bonds" with estrous females that last several days, during which the male is never more than several meters away from the female. Younger males might maintain tending bonds with females at an earlier stage; thus, females can have multiple consort males in close attendance before and leading up to breeding. The chance of nonvenereal transmission between the sexes is increased because of this protracted courtship behavior. Still, the two most probable sources of B. abortus transmission are abortion or birth when infectious materials are in the environment. Because of long exposure of bison to B. abortus, they respond to it more like chronically infected cattle herds in which selection for genetic resistance has occurred. In about 75 years, only four cases of abortion in YNP have been recorded (Rhyan et al. 1994); of course, regular surveillance is impossible given the large numbers and scattered distribution. The real number, therefore, has to be greater. But if abortion were common, many more cases would be expected to have been reported. In two cases, abortion sites remained culture positive for B. abortus for at least 2 wk (J. Rhyan, USDA, pers. commun., 1998). Abortion among elk on the NER and Wyoming Game and Fish Department feeding grounds has been estimated at 7% (Smith and Robbins 1994) to 12.5% (Herriges et al. 1991) of pregnancies. Given such a high abortion rate and the high concentration of animals, transmission is highly likely. Indeed, Thorne et al. (1997) suggest that any elk that lives a long life and winters on a feeding ground is likely to become infected. Also important is the difference in probability of association between elk and bison and cattle. Elk usually move away from areas used by cattle (Skovlin et al. 1968; McCullough 1969; Oakley 1975; Long et al. 1980; Mackie 1985), and this would reduce the contact between the two species. Bison, in contrast, are behaviorally dominant over cattle and respond to them aggressively if they approach within 5 m (Van Vuren 1982). However, they tolerate them when in proximity, and in one case, Van Vuren (1982) observed a domestic cow that joined a bison social group for 7 days. In normal birth, the probability of transmission of B. abortus to cattle is influenced by the birthing behavior of bison and elk. Wild ungulates are categorized by birthing behavior as hiders or followers (Lent 1974). Hiding and following are major strategies used by mothers to avoid predation on their offspring. Hiders use dispersion, crypsis, and concealment to prevent discovery of offspring by predators, whereas followers depend on precocial offspring

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(offspring that can stand soon after birth), which can run with the mother to escape predators. Hiding is characteristic of species that have access to concealment cover in their habitat. Following is characteristic of herding species; herding is usually associated with open habitats that lack concealment cover and is itself a strategy for countering predators (McCullough 1969; Hamilton 1971). Elk are classic hiders (Geist 1982). Females approaching labor isolate themselves from the herd (often moving several kilometers away) and seek cover in vegetation or broken terrain to give birth (Johnson 1951; McCullough 1969). After giving birth, the cow meticulously cleans the site (Livezey 1979; Clutton-Brock et al. 1982) and then moves the calf several hundred meters away to hide (Altmann 1952; Clutton-Brock et al. 1982). The sanitation of the birth site by the mother is thorough. Females search the ground and consume small bits of birth tissue (Livezey 1979) and grass stained by fluids (Clutton-Brock et al. 1982). Bauer (1995) reported, "As we watched, the cow not only devoured the placenta and birth membranes, but also seemed to be eating the earth and grass that were saturated with birth fluids." Fraser (1968) noted that hiders eat afterbirth materials more for protection of the young than for physiologic reasons and that removal of vegetation and soil would remove any traces of scent from the site. Indeed, the entire suite of behavior of the elk cow and calf at birthing is linked to concealing the presence of the calf from predators. The calf hides alone while the cow feeds or beds in the vicinity, returning only long enough to nurse (McCullough 1969). The mother licks the calf's perineum during suckling; this stimulates voiding, after which she ingests the feces and urine (Arman 1974). The hidden calf remains motionless if approached during the first 3 or 4 days of life, running only at the last instant if hiding fails; the cow defends the calf from predators (Murie 1951; McCullough 1969). The cow and calf usually rejoin the herd in 2 or 3 wk after birth (Altmann 1952, McCullough 1969). The evolution of antipredator behavior in elk has resulted fortuitously in behavior that reduces the likelihood of B. abortus transmission. The dispersed birthing area and sanitation of the birth site result in a low probability that other animals will come into contact with infectious birth products. The consensus of respondents to the National Research Council questionnaire was that B. abortus is not self-sustaining in elk herds that are not concentrated on winter feeding grounds. That is cited as the reason that the elk in the northern Yellowstone herds that are not winter-fed have a seropositive rate of only 1-2% (M. Meagher, USGS., pers. commun. as cited by Smith and Robbins 1994; Rhyan et al. 1994), whereas those using winter feeding

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grounds in the southern part of the GYA have an average seropositive rate of 34%. A somewhat higher seropositive rate (5 of 126, or 4%) in northern-range elk was reported by Thorne et al. (1991), but this could reflect sampling error. In contrast with elk, bison offspring are followers, as is consistent with the highly developed herding social structure in this species (McHugh 1958; Meagher 1973; Lott 1974). Pregnant females separate from nonpregnant females to form nursery herds (McHugh 1958; Lott and Galland 1985; Meagher 1986; Berger and Cunningham 1994). Females give birth either alone or in small subgroups and might seek cover, depending on what is available in the environment occupied by the nursery herd at the time of birth (McHugh 1958; Lott and Galland 1985). Nevertheless, birth occurs either in or close to the herd. Mean time from birth to standing by the calf is about 11 minutes and from birth to nursing about 32 minutes (Lott and Galland 1985). The mother usually consumes the afterbirth (McHugh 1958; Fraser 1968; Lott and Galland 1985; J. Berger, U. Nev., pers. commun., 1997). However, detailed observations of how thoroughly the site is cleaned are not available. In bison, consuming the afterbirth might be related mainly to hormonal and physiologic needs; the antipredator benefits of consumption would seem minimal in a species that lives in large herds in open areas and has offspring that are conspicuously different from the adults. For bison calves, the major antipredator protection is the herd. Calves are protected from predators not only by their ability to run with the herd, but also through defense by the large, formidable mothers, whose common interest—protection of young from predators—presumably is the selective advantage of forming separate nursery groups in the first place. If consumption of the afterbirth in bison is related to hormonal factors rather than predator avoidance, it might be that the birth site is not so well sanitized as by elk. Giving birth within the herd concentrates the afterbirth in space and increases the likelihood of encounters with other herd members and roving males. That increases the probability of transmission of B. abortus associated with birth products among bison and to other species that might accidentally or purposefully encounter the nursery herd area. The dispersed distribution of birthing in elk, in conjunction with their thorough cleansing of the site, makes the probability of transmission of B. abortus among elk or from elk to other species, lower than for bison. Abortion by B. abortus-infected females is a more serious risk factor for disease transmission than is normal birth. Abortion is spontaneous and typically occurs in the third trimester of pregnancy. That timing places most abortions in the winter when both bison and elk are concentrated, some on

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artificial feeding grounds. Abortion occurs out of synchrony with the social structures of normal birth and decoupled from the usual entraining of endocrine activity that regulates normal birthing behavior. Concentration of animals on winter feeding grounds or, in bison, by the natural herd structure greatly increases the potential for contact with aborted fetuses and other afterbirth products. In addition, disruption of normal hormonal controls results in retention of placentae in bison and failure of the females to clean up the birth products. Retained placentae in bison can attract the attention of other herd members and roving bulls and extends the exposure period of B. abortus in time and space. Elk apparently do not retain the placenta after abortion, and they can reach it and remove it before it hits the ground (Thorne et al. 1978, 1997). In their study of penned elk, Thorne et al. (1978) reported that aborting females attempted to eat their fetuses but that they might have been only partially consumed. In this captive herd, other females were observed to investigate and lick the partially expelled fetuses during abortion. Intact fetuses and afterbirth remaining at the abortion site would greatly increase the probability of transmission between animals. Furthermore, at the typical time of abortion, winter temperatures and moisture would favor survival of B. abortus in the environment, as would sequestration of B. abortus in larger masses of birth tissue not consumed by the female. TRANSMISSION BY OTHER SPECIES OF UNGULATES Other wildlife species have the potential to contract and transmit brucellosis (see review of Remontsova 1987). Other wild ungulates in the GYA—mule deer, white-tailed deer, antelope, and bighorn sheep—have never been documented to harbor the microorganisms (McKean 1949; Steen et al. 1955; Shotts et al. 1958; Trainer and Hanson 1960; Rinehart and Fay 1981; Jones et al. 1983; Gates et al. 1991; K. Aune, Mont. Dept. Fish, Wildlife, and Parks, pers. commun., 1997). Moose are known to contract the disease, although moose living in an area where cattle were heavily infected by B. abortus tested seronegative (Hudson et al. 1980). None of several dozen moose tested in the GYA was seropositive (T. Thorne, Wyo. Game and Fish, pers. commun., 1997). Moose are considered a dead-end host for brucellosis and are not thought to be a threat to transmit the disease. They do not seem to be involved in the epidemiology of brucellosis. Moose are typically solitary, and yet the rare occurrence of brucellosis in moose, a species that does not usually carry or perpetuate the disease, illustrates the possibility of transmission of B. abortus among the species that do. Surveillance for the disease in

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moose or other wildlife species that are dead-end hosts might be a way of estimating the probability of rare events of transmission among bison, elk, and cattle. POTENTIAL ROLE OF CARNIVORES IN TRANSMISSION Predators can become infected with B. abortus, and they are potential reservoirs for transfer to other species. The most thorough work on B. abortus in carnivores is the study done on coyotes by Davis et al. (1988). They fed macerated cattle fetal material infected with B. abortus to 40 brucella-negative coyotes, and 32 became seropositive. They also found that B. abortus can pass through the digestive tract of coyotes and remain viable in feces and urine. In each of four trials, 10 exposed coyotes were put in 1-hectare pens with six uninfected heifers. B. abortus transmission occurred in three heifers in one trial, and they aborted. No transmission occurred in the other trials; 3 of 24 heifers were infected overall. The heifers probably became infected through contact with urine or feces of coyotes (D. Davis, Texas A&M, pers. commun., 1997). Coyotes can potentially serve as a bioassay for B. abortus; a survey of two-thirds of the counties in Texas showed that seropositivity in coyotes corresponded to the known distribution of brucellosis in cattle (D. Davis, Texas A&M, pers. commun., 1997). Transmission in the Davis et al. (1988) study occurred under confinement at artificial densities of both coyotes and cattle. Although it does verify the possibility of transmission, that cannot be translated into probabilities of transmission under natural range conditions. Carnivores of YNP—including grizzly bears, black bears, wolves (Canis lupus), coyotes, and foxes (Vulpes fulva)—are known to contract brucellosis (Zarnke 1983; Remenëtïsova 1987; Morton 1989; Johnson 1992), presumably through consumption of infective tissues during predation and scavenging. Of 122 grizzly bears tested in Alaska, six were seropositive (Zarnke 1983). Current estimates of grizzly bear population size in the GYA are around 300 (Eberhardt and Knight 1996). There were an estimated 650 black bears in the GYA in the late 1970s (Cole 1976), but their numbers might have declined (Schullery 1992). YNP has no current estimate of black bear numbers; they are considered common in the park (Gunther 1994), but they are seldom mentioned with reference to brucella transmission. Wolves were extirpated from the GYA by the early 1930s and have been reintroduced only recently (Weaver 1978; Yellowstone Science 1995; Bangs and Fritts 1996). Consequently, the ecosystem role of wolves has been missing for many years and

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is only now being re-established. The current wolf population is about 100. Coyotes are ubiquitous in the GYA. Any debilitation due to brucellosis (Tessaro 1987; Thorne et al. 1997) would predispose adult elk and bison to predation. Grizzly bears, wolves, and coyotes scavenge and all are predators on calves. Scavenging makes them vulnerable to contact with products of birth and abortion, the likely route of acquisition of B. abortus, but it is highly unlikely that these species directly transmit the bacterium back to ungulates. They are considered dead-end hosts. Transmission of B. abortus by carnivores through transport of infective materials from birth or abortion sites to other areas, however, is a concern. Carnivores could have positive and negative effects on the dynamics of B. abortus. On one hand, by consuming products of birth and abortion they remove the bulk of infectious materials from the site and expose remaining B. abortus on the soil and vegetation to light and desiccation, to which they are vulnerable (Mitscherlich and Marth 1984). Although it has not been quantitatively documented, known carnivore behavior makes the existence of a healthy complement of predators almost certain to be a major factor in reducing the probability of B. abortus transmission within the wildlife community and between wildlife and domestic stock. Predation and scavenging by carnivores likely biologically decontaminates the environment of infectious B. abortus with an efficiency unachievable in any other way. On the other hand, carnivores might contribute to transmission probabilities by transporting infectious materials from one site to another. Particularly troublesome is the possibility of transporting such material between exclusive wildlife and cattle areas kept geographically separated by management. No data are available to address this question directly; the potential risk must be evaluated on the basis of what is known about the behavior of these carnivores. Ordinarily, urine and feces from predators would be unlikely routes of direct transmission of B. abortus because the number of organisms shed is small in relation to the infective dose for cattle (Morton 1989), and cattle, bison, and elk would not be attracted to or likely to come into contact with them accidentally. However, one exceptional circumstance should be noted. B. abortus apparently can pass through the gastrointestinal tract of predators and survive in their feces (Davis et al. 1988). Under some conditions of mineral deficiency, domestic cattle show depraved appetite, or pica, in which they consume a variety of atypical objects (Church et al. 1971). Similarly, wild ruminants commonly visit mineral licks and consume soil during some times of year, usually during periods of rapid growth in the spring. Rodents and rabbits are well known to consume bones and antlers, presumably for the

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minerals in them. In a mineral-deficient area in south Texas, cattle were observed to consume coyote droppings (D. Davis, Texas A&M, pers. commun., 1997), which commonly contain small mammal bones, a mineral source. Also, reindeer penned with foxes consumed fox feces (Morton 1989). If such behavior occurred in a brucellosis area, the probability of transmission of B. abortus from predators to herbivores could be substantially increased. Whether such behavior occurs in bison, elk, or cattle in the GYA is unknown. A more important concern with predators is their transport of infected ungulate-carcass materials from a death or abortion site to other areas. Internal organs of large animals are usually consumed first, and skeletal muscle and other body parts later (E. Gese, NWRC, Ft. Collins, Colo., pers. commun., 1997). Heads, bones, and other hard materials are consumed last or not eaten at all. Coyotes and wolves sometimes transport pieces of carcasses short distances to nearby preferred microsites to complete consumption, but this would spread the bacteria only locally and not greatly increase the likelihood of transmission. Grizzly and black bears are not known for transport of carcasses or parts from the site of death; they do not usually move carcasses elsewhere to cache them, although they sometimes cover the carcass at or near a kill site (Craighead et al. 1995), which might preserve B. abortus for longer periods. They usually feed on site. Bears are followed by dependent offspring and do not provision. Longer-distance transport could occur as a result of caching carcass parts and provisioning pups sequestered in dens; these behaviors are shared by coyotes, wolves, and red foxes. Parts of carcasses carried by mouth (usually pieces containing bones, which afford structural integrity) can be transported great distances. Soft tissues may be consumed and subsequently regurgitated at the den. Caching has been reported in wolves (Murie 1944; Mech 1970; Harrington 1981), coyotes (Weaver 1977), and especially red foxes (Vander Wall 1990). Caching—thought to be a way to extend the time that food is preserved, to protect it from competitors, and to hedge against difficult hunting times—seems to be most common in populations with smaller home ranges and greater population densities. In Alaska, wolves often disperse and cache chunks of caribou, burying them in soil or in creeks covered with moss (K. Taylor, Alaska Dept. of Fish and Game, pers. commun., 1997). Recently in YNP, wolves were observed to kill a pronghorn fawn and cache the carcass (F. Camenzind, Jackson Hole Conservation Alliance, pers. commun. 1997). Foxes, which have relatively small home ranges, cache frequently, coyotes less commonly, and wolves least commonly. The potential for B. abortus transmission by red foxes (Johnson 1992) should be considered more carefully, given their well-developed caching behavior (Vander Wall

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harvest from other herd units. From feedground classification counts, they suggest that maximum sustainable yield is nearer 20%. In either case, the harvest rate on this population is relatively high. In the northern herd, by comparison, the annual kill in recent years has been about 1,800 in a population of 16,000 (11%) (Yellowstone National Park 1997). It is clear that in contrast with the northern herd, which is limited mainly by natural phenomena, the other herds using the GYA are limited mainly by human harvest. Thus, they are more stable from year to year in their likelihood of contact with cattle and with the consequent possibility of transmission of B. abortus. Essentially, they come out of the YNP area, pass through a hunting zone, and are intercepted by winter feeding areas. To the extent that feeding areas do not stop movement, elk are hazed to return to them from private lands. Although the other herds are more predictable from year to year, the sheer numbers of elk, their proximity to grazing allotments, cattle trailing areas, and private ranches, and their relatively higher seropositive rates means that the relative risk of transmission of B. abortus from elk to cattle is greater than for the northern herd elk. Effects on Reproductive Potential Two questions arise when considering whether B. abortus affects the reproductive potential of bison generally, and specifically bison in the GYA. The first question is whether B. abortus lowers the reproductive rate. That question would be consistent with the traditional use of the term potential in wildlife management, in which it is viewed as the maximal possible rate of reproduction (Leopold 1933). By that definition, the answer to the question is yes because any abortion or lowering of the probability of survival of offspring—the usual manifestation of brucellosis in bison, as in cattle and elk—would reduce the maximum. However, such a strict definition probably is not the most relevant in the context of brucellosis in bison in the GYA. The second question deals with whether brucellosis affects the population dynamics of bison, and this is more relevant to the current issues in GYA. The question is whether brucellosis lowers reproductive performance sufficiently to constitute an important factor in population dynamics in bison and thereby alters the population trend over time. Controlled research on the magnitude of brucellosis effects is lacking, but it can be estimated from the modeling results of Peterson et al. (1991b). They modeled bison populations (females only) under brucellosis-free and brucellosis-infected states. Their projections for a brucellosis-free population

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can be used to estimate the impact of brucellosis on the growth rate of the GTNP bison population (69% seropositive for B. abortus) from the 1970 escape of five female founders to the total 1989 female population. This result can be derived from their Figure 7 (panel B). The annual growth rate projected by their model was 15.48%, whereas the realized rate was 14.45%, 1.03 percentage points lower. Simple models that assume infection rates between about 10% (GYA culture-positive rate) and about 50% (GYA seropositive rate) and loss of the first calf after infection show that reduction of population growth rate because of brucellosis would be only a few percent unless the survivorship of reproducing females were extremely low, an unlikely possibility for the hardy, long-lived bison. Empirical results bear out that conclusion. Bison populations in YNP and GTNP (and herds elsewhere) have continued to increase despite being infected with B. abortus (Figure II-2) unless artificially controlled or reduced by severe winter conditions (Dobson and Meagher 1996). In YNP, artificial removal has been important in holding bison population growth to near zero at times, particularly from 1935 to 1965, when the herd was managed to number around 400, and in the past few years (Figure II-2). Among natural variables, winter mortality is clearly the most important, but production of forage in summer also might contribute to the dynamics of the herd (Meagher 1973). Only for a bison population in a marginal habitat where it would be barely capable of holding its own would brucellosis be the deciding factor in survival of the herd. YNP is not marginal habitat. Elk, like bison, will suffer decline in potential elk population growth due to abortion. Although the data for elk show greater variance than those for bison, the persistent increase in numbers of elk after declines have resulted in brucellosis being considered unimportant as practical matter. RISK OF TRANSMISSION The risk of transmission is determined largely by the number of abortions that occur, the presence and survival of B. abortus in placental exudates, and the exposure of a susceptible host through an appropriate tissue barrier. Aborted placentae might contain as many as 1013 B. abortus per gram of tissue (Davis et al. 1995). Direct evidence of transmission from various wildlife species to cattle has been difficult to establish. Despite circumstantial and epidemiologic evidence of transmission, many still believe that bovine brucellosis never has been proved to be linked to free-ranging elk or bison. The detection of transmission of B. abortus from an infected animal to a

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susceptible domestic cow is complicated by lack of clinical signs in infected cattle, geography, predation of the placenta and fetus, and birthing characteristics of the infected animal. Those and other factors complicate determination of risk of transmission. The perception of, for example, some members of animal-welfare groups, is that transmission is extremely rare and might never occur. The perception of others, such as some ranchers in or near the GYA, is that seroreactive cattle do appear in their herds and that those cattle have been infected with B. abortus from either elk or bison. Bison to Cattle Under natural conditions, the risk of transmission from bison to cattle is very low, but the appropriate quantitative risk assessments have not been done; one, by a multiagency group, is under way (E. Williams, U. Wyom., pers. commun., 1997). Free-ranging bison or elk might have served as the source of B. abortus infection in six cattle herds in the GYA (GYIBC 1997), but as noted earlier, the evidence is ambigous. Transmission of brucellosis from naturally infected captive bison to cattle has been reported; captive bison under range conditions in North Dakota were in contact with beef cattle during the winter (Flagg 1983). Bison-to-cattle transmission in Arkansas has also been reported. The risk of transmission of B. abortus from infected bison to cattle is a major part of this study. Brucellosis has been transmitted from bison to cattle under experimental conditions, and brucellae were transmitted from infected bison to seronegative cattle when the animals were confined together in pens (Davis et al. 1990). YNP bison herds have had little or no contact with outside bison since the early 1900s. Serologic surveys show seroprevalence rates of 20-73% (Rush 1932; Tunnicliff and Marsh 1935; Clark and Kopec 1985; Pac and Frey 1991; Aune and Schladweiler 1992; Aune et al. 1997). The number of abortions or fetal deaths per 100,000 bison births since brucellosis was first detected in 1917 is not known, and individual cases of transmission, especially in early periods, will likely never be determined. In the past decade, two cases of abortions due to B. abortus have been established (Rhyan et al. 1994). Isolates of B. abortus obtained from bison have been shown to be pathogenic in cattle; for example, biovar 1 isolates from a Wood Buffalo National Park bison in Canada were virulent when inoculated into cattle (Forbes et al. 1996), even though the bison had been segregated from cattle for more than 60 years. The current risk of transmission from YNP bison to cattle is low. Furthermore,

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domestic cattle adjacent to the park are vaccinated, cattle are monitored by federal agencies, and ranchers are vigilant. Elk to Cattle Transmission of B. abortus from elk to cattle is unlikely in a natural setting. The ability of brucellae to be transmitted from elk to cattle under experimental conditions has been proved (Thorne et al. 1979), however, and cattle mingling with aborting elk on feeding grounds would be at high risk for infection. Elk densities in YNP reach those of the winter feeding grounds (p. 76, ''Other Elk Herds in the GYA") for short periods during some times of the year; although the incidence of brucellosis in these elk is very low, that might present another risk factor. Data on the incidence of elk-to-cattle transmissions might be skewed if ranchers are not forthright in admitting when cattle might have been exposed by commingling with infected elk. Elk to Bison Elk can transmit B. abortus to bison. Transmission is probably limited to aborting and parturition of infected elk with release of fetal membranes and genital exudates that contain large numbers of B. abortus . That has occurred during mixing of bison with infected elk on feeding grounds of the National Elk Refuge. M. Meyer (U. Calif., pers. commun., 1997) claims that the Jackson (GTNP) bison herd was brucellosis-free until it discovered the elk feed lines. The Jackson herd, which for 20 years was confined in a wildlife park and allegedly was brucellosis-free, escaped in 1968 and commingled with infected feeding-ground elk around 1980. The herd became infected (the seroprevalence in 35 bison collected in 1989-1990 was 77%) either by elk on the National Elk Refuge (NER) or by bison that were infected (although seronegative) when they escaped. Transmission from elk to bison might have occurred under natural conditions in the GYA (Williams et al. 1993). If low infection rates are attained through management of bison, the population of bison will remain uninfected for quite some time before a low-probability elk-bison or bison-elk transmission would occur. During the brucellosis-eradication program in Custer State Park in South Dakota, elk, deer, and antelope mingled with infected bison; there is no evidence that bison from which brucellosis was eliminated were reinfected by B. abortus from elk (Gilsdorf 1997).

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Bison to Elk Whether and at what rate B. abortus is transmitted from bison to elk are unknown (S. Olsen, USDA, pers. commun., 1997). One group states that "although controlled or field studies have not been done to establish transmission between bison and elk, it certainly is possible" (T. Kreeger, Wyo. Game and Fish, pers. commun., 1997). Evidence of transmission of brucellosis among wildlife species comes from Elk Island, a fenced national park in Alberta, Canada, where bison were believed to have been the source of B. abortus infection in elk and probably moose (Corner and Connell 1958). Elk as a Reinfection Pathway for Bison Bison can contract B. abortus from elk, as demonstrated by the case cited above in which a clean herd of bison was introduced in 1970 to GTNP, later wintered on the elk feeding grounds of the NER, and tested positive for B. abortus in 1989. The risk of transmission to bison will depend on the success of efforts to reduce the infection rate in elk by vaccinating elk on feeding grounds and dispersing them over a larger wintering area in the southern GYA. If infection rates are not substantially reduced in elk, it seems inevitable that reinfection of bison will occur, just as bison are a continuing reinfection source for elk (Thorne et al. 1997). It must be remembered that low-probability events multiplied by large-enough animal contacts over a long-enough time become inevitable events. Apparent multiple transmissions between some combination of cattle, bison, and elk with the arrival of B. abortus in the GYA (Meagher and Meyer 1994; Thorne et al. 1997) should be a cautionary note, as should the occurrence of a case of undulant fever in an elk hunter in the northern range (where seropositive rates of elk are low), whereas no cases in hunters in the southern range (where seropositive rates are high) are known. Early work with vaccination of elk at Greys River winter feeding ground resulted in promising reductions in seropositive rates (67% to 12%). In the winter of 1996-1997, however, the rate rebounded to 26%. The cause of the increase is unknown, but it could be related to the hard winter of 1996-1997, which would indicate that environmental stress, as well as pregnancy stress, can contribute to B. abortus infection rates. The reduction from 67% (1976) to 12% (1996) is significant, but inclusion of the 1996-1997 point results in lack of significance (P = 0.11). It is problematic that the first year in the time series (1976) was 17 years before the first of the consecutive data points

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(1993-1997). Also, Smith and Roffe (1997) have questioned the validity of conclusions from the vaccination experiments on which the program is based. Alternatively, the field-vaccination program might be reaching the limits of its efficiency. For example, modeling of vaccination in bison (Peterson et al. 1991a) and cattle shows that reduction in seropositive rates amount to only 60-80% of baseline prevalence. That would predict that elk vaccinated on the feeding grounds would show a reduction in seroprevalence from 67% to about 13-27%, the approximate range observed in recent years. Further work will be necessary to evaluate the success of the program. The source of the 1-2% seropositive rate in elk in the YNP northern range is potentially important. That seroprevalence might be, as has been proposed, the result of movement of elk from southern to northern ranges. But alternative explanations need to be considered, such as the infection of northern-range elk by contact with infected southern-range elk or YNP bison. The calving areas of southern-range elk, where birth and abortion increase the likelihood of transmission, are well south of YNP (Boyce 1989), and this casts doubt on that source of infection. If movement of southern-range elk to the northern range is not responsible for the seropositive rate in northern elk and if northern-range elk are not in close contact with southern-range elk, then the rate would seem to be natural infection due to contact of elk with infected bison. Because the potential of such transmission—either between bison and elk or between elk away from the winter feeding grounds, a key issue in sustainability of B. abortus in non-feeding-ground elk—is of particular interest, it is important to determine whether the seropositive elk in the northern range have moved from the southern range by marking them on the feeding grounds through feed or vaccination. Several factors contribute to the likelihood of potentially infective contact of bison with elk. First, the distributions of the two species overlap broadly in the GYA on the summer range, where they are more dispersed, and on the winter range, where they are concentrated (Meagher 1973). Bison and elk are often seen near each other. Second, their habitat requirements overlap broadly. In YNP, Singer and Norland (1996) found overlap of diet (1 = complete overlap, 0 = no overlap) to be 0.47 and 0.63, and use of vegetation 0.43 and 0.75, slope/aspect 0.45 and 0.57, and snow 0.59 and 0.89 for early and late periods. Those overlap values are high, and that they invariably were higher in the later years suggests that increases in density in both species are increasing the overlap of their use of the environment. Similar overlap between bison and elk was reported by McCullough (1980) for the National Bison Range in northwestern Montana and by Telfer and Cairns (1979) for Elk Island National Park, Alberta.

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Thus, increases in potential contacts are not a simple function of numbers, but a function of the increased forcing of overlap of niche space as well. Third, the probability of transmission of B. abortus needs to take into account a behavioral component. The movements of the two species are essentially independent. If encountering a site (such as a birth or abortion site) at which B. abortus might occur in the environment were random, the probability of transmission would be low by chance. However, birth and abortion sites are likely to attract both species. Bison and elk are highly olfactorily oriented. The observation of W. Cook (U. Wyoming, pers. commun., 1997) of attraction of elk and bison to noninfective bovine fetuses placed in the environment illustrates the point. Such attraction might occur across species as well. Reproductive fitness is a major component of natural selection (Fisher 1930), so it behooves individuals to be cognizant of each other's reproductive state. Bison—especially males—show substantial interest in matters associated with reproduction. Berger and Cunningham (1994) discuss these aspects in detail for bison. Elk and bison engage in flehman , a behavior most commonly associated with males testing the estrus state of females by licking the vulva or urine and exposing the molecules therein to the vomeronasal organ in the palate. Bison males have been reported as displaying "very aggressive behavior towards cows in estrus, or any blood discharge, death or injury" (S. Holland, as cited by Kearley 1996). They are especially animated by the occurrence of aseasonal estrus (S. Holland, state vet., S.D., pers. commun., 1997) or by blood at any time (J. Rhyan, APHIS, pers. commun., 1997), and the aseasonality of abortion might evoke similar interest. Behavioral attraction to sites of abortion or birth, therefore, is likely to bring individuals into contact with potentially infective materials at a rate far greater than expected from random movements. That behavior is most prevalent in bulls, but it occurs to some extent in cows. That would increase the probability that bison, especially males with greater movements and sexual curiosity, would be infected by B. abortus shed by elk. In fact, in the bison herd observed by Holland, bulls were more likely than cows to become infected by cows. That also is true of the GYA. Bulls tested in the winterkilled sample leaving YNP had a 57% culture-positive rate compared with 24% for cows; for GTNP, bulls had an 84% seropositive rate compared with 69% for cows. Furthermore, the difference is already present in subadult males (Meyer and Meagher 1997). The higher prevalence of brucellosis in bison bulls than cows is puzzling. The difference might arise from differential survival of offspring by sex. If birth to infected mothers or acquisition of B. abortus through the milk (see p.

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23, "Shedding in Mammary Glands and Milk") were the source of infection, calves of both sexes would have similar infection rates unless there were differential abortion or calf mortality by sex. We assume that mortality is more likely among infected fetuses or calves than among uninfected ones. Abortion would have to be more prevalent for female than male fetuses to account for the differences. Ordinarily the reverse would be expected—the male is larger and places greater stress on the mother. Furthermore, abortion is thought to be relatively uncommon in YNP bison, so differential abortion by sex is not an expected source of the different infection rates. Differential mortality of male calves is not likely the cause, in that uninfected calves would have to have a higher mortality. The difference could be due to differential mortality of infected female calves, but this would invert the logic in explaining why female infective rates were low rather than why male rates were high. Although possible, this explanation seems at odds with the typical higher male calf mortality that results in a prevalence of females among adult bison. Higher seropositive rates in bison males are unlikely to be due to differential mortality by sex in calves. A more likely possibility is that higher infection rates in males arise from differential behavior of males later in life. Male behavior that might contribute to infection includes naso-oral contact with genital exudates and urine during flehman to ascertain estrus, greater inclination to smell or lick afterbirth or aborted materials (even subadult males would be subject to this route of infection), and venereal transmission during coitus or contact in tending bonds, which because of the polygynous breeding behavior of bison brings each male into contact with multiple females. It is notable that elk show the reverse condition: females have higher seropositive rates than males. Ordinarily, elk bulls are spatially segregated from females except during rut (McCullough 1969; Geist 1982). Like bison, elk bulls perform flehman during rut and mate with multiple females. They do not form tending bonds but instead guard harems; this lessens the period of close contact and reduces the number of males involved in copulation. For example, McCullough (1969) found that only 12% of male elk were important contributors to reproduction, whereas in Badlands National Park, 51% of 37 bison males 4-9 years old mated (J. Berger, U. Nev., pers. commun., 1997). In general, elk seem less alert to strange odors outside of rut than do bison. That means that male elk on the winter feeding grounds are less likely to be curious about abortions in the winter time than are females. All those factors suggest that bison bulls are more instrumental in transmission of B. abortus than are elk bulls. As noted earlier, the role of bison bulls in transmission of B. abortus presents an important gap in our knowledge.

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Other GYA Wildlife to Cattle Infection with B. abortus is self-limiting in many wild mammals. Brucellosis occurs rarely in deer, pronghorn antelope, and mountain sheep. Brucellosis has not been documented in those species in the GYA, and any infection in them would be inconsequential for the control of brucellosis in bison and elk populations. Natural infection with B. abortus in avian species has been reported (Angus et al. 1971) but plays no role in transmission to mammals. Transmission to Humans in the GYA Human infection with B. abortus in the GYA has been reported, and a woman elsewhere was reported as having aborted due to Brucella spp. Hunters consume bison meat from areas outside YNP, and some bison meat is given to tribal peoples and soup kitchens for needy people. Meyer reports that "in December 1991-February 1992 over 500 bison were shot and carcasses were eviscerated, largely by Indians who literally just mucked through the guts" (M. Meyer, pers. commun., 1997). However, no evidence that B. abortus infected those Indian populations has been reported. The U.S. Centers for Disease Control and Prevention no longer requires reporting of undulant fever. The World Health Organization Laboratory Biosafety Manual places B. abortus in risk group III, indicating a high risk to persons involved in handling infected animals or tissues. All personnel involved in sampling should be formally advised of the risk of infection and trained in the handling of infectious tissue and the use of masks and equipment. Face masks, gloves, and protective clothing should be used in high-risk situations that involve female bison that have placental lesions of brucellosis or that have aborted. The greatest risk of human infection lies in body contact with infectious material and transmission of microorganisms from hands to body orifices. B. abortus is typically present in low numbers in blood and lymphoid tissues of animals. Although most genital tissues in males and nonpregnant females have only low numbers of organisms, the infected placenta and its fluids are extremely hazardous and can contain up to 1013 bacteria per gram, a concentration that makes aerosol transmission possible. Blood and milk are hazardous, but infection from them is unlikely if reasonable means are used to prevent contamination of hands and face and thereby controlling the potential to spread microorganisms to body orifices. Pasteurization of milk eliminates the risk of infection from milk consumption. Human brucellosis caused by B. suis has been well documented in people

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who eat rangiferine animals (reindeer and caribou) in North America (Ferguson 1997), but no systematic study of brucellosis in American Indians has been done. Brucellosis was identified in Eskimos in Canada (Toshach 1963). In Alaska, 49 cases have been reported. It was suggested that rangiferine brucellosis is widely underreported because mild cases are not brought to medical attention and that chronic human cases might be undetected by small medical clinics. Treatment of human brucellosis involves 4-6 weeks of antibiotic therapy, which carries the possibility of toxicity in some patients. Cure is not ensured, especially in chronic disease, which can be lifelong. OTHER SPECIES OF BRUCELLA AND BRUCELLOSIS IN WILDLIFE Species of Brucella other than B. abortus are associated with brucellosis in wildlife (Table II-1). Rangiferine brucellosis in commercial herds of reindeer TABLE II-1. Species of Brucella Bacterium Primary Hosts Wildlife Hosts Pathogenicity in Humans B. abortus Cow Bison, elk, wolf, coyote ++ B. melitensis Goat, sheep Camel, wild ruminants +++ B. suis Biogroups 1 and 3: Pig; Biogroup 2: Pig and hare; Biogroup 4: Reindeer and caribou; Biogroup 5: Rodents Reindeer, pig, caribou +++ B. ovis Sheep Mountain goat – B. canis Dog ? + B. neotomae Woodrat Desert woodrat – B. sp (unnamed) Dolphin, seal Many marine mammals +

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and in caribou (Rangifer tarandus) throughout North America is caused by B. suis biovar 4. B. suis in these animals has been shown to infect cattle. In one study, four of eight cattle penned with 14 naturally infected reindeer became infected with B. suis and were seropositive (Forbes and Tesaro 1993). Although it has not been reported, reindeer likely can transmit brucellosis to other wild mammals, and this could cause confusing serologic responses in bison (Forbes and Tessaro 1993). A variety of rodents have been reported to be susceptible to infection and to develop disease (Moore and Schnurrenberger 1981), but rodents have not been implicated in the spread of brucellosis in the GYA, perhaps because of inadequate investigation.