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Population and Movement Characteristics of Radio-Collared Striped Skunks in North Dakota During an Epizootic of Rabies

Discussion


Rabies is enzootic in striped skunks in North Dakota, where in some years, skunks may account for all of the submitted rabies-positive cases (Charlton et al. 1991). In 1992, however, the epizootic we observed in Stutsman County likely would have been undetected without our study. None of the residents of our study area was aware of the rabies epizootic until we informed them of it in mid-May. Few skunks that died of rabies during March through July 1992 were visible to the public; nearly one-third of the carcasses or remains were below ground (Table 3). Most carcasses above ground were concealed in vegetation and, had we not retrieved them, would have decomposed within a few days.

In 1992, 115 cases of rabies in striped skunks were reported in North Dakota (Krebs et al., 1993). Of 40 cases reported from Stutsman County, 36 were from our study. Our estimate is a minimum; four skunks died or were released before we decided to test for rabies, two decomposed before we recovered their remains, and two others were not recovered. One of the decomposed skunks contained numerous porcupine (Erethizon dorsatum) quills, suggesting it may have been rabid (MacInnes 1987). Without our sample, cases of rabies in 1992 would have been underestimated by a minimum of 31% in the state and by 90% in the county. Considering the above factors and relatively small area from which we obtained animals, the magnitude of underestimating of rabies deaths in striped skunks probably was greater than that. Overestimation may be more common, however, because high proportions of skunks submitted for necropsy are rabid, thus inflating estimates of proportions of rabid animals in populations (Gunson et al., 1978).

We cannot explain the etiology of lymphocytic meningitis in the four skunks that were negative for rabies and canine distemper. Two were found dead in May and the two other were euthanized in July and appeared to be healthy. None of the four showed evidence of fighting or clinical signs of rabies. Based on these observations, we believe another virus or other unknown agent may have affected these animals.

In 1992, only 22% of skunks we captured were age class 1 (Table 1). In 1991, however, 66% of the skunks were age class 1. Greenwood and Sargeant (1994), likewise, found a high proportion (74%) of age class 1 animals among skunks examined from eastern North Dakota and western Minnesota between 1979 and 1990. First year animals usually compose about 45 to 50% of populations of healthy striped skunks (Casey and Webster, 1975; Schowalter and Gunson, 1982). Based on the disparity in age structure in 1992, we believe disease or other notable factor affected the first year animals, as suggested by Fuller and Kuehn (1985).

We suspect that rabies in 1991 may have affected productivity of females in the vicinity of our study area and consequently, reduced numbers of juveniles available to disperse to our area. In 1991, we confirmed rabies in one radio-collared skunk on the extreme north edge of our study area and had an unconfirmed report of another rabid skunk approximately 3.2 km northwest of there.

That rabies may have affected productivity was supported by our finding that only 72% of females we observed in 1992 were pregnant or parous. Pregnancy rates usually are considerably higher (Bjorge et al., 1981; Schowalter and Gunson, 1982). Greenwood and Sargeant (1994) reported a pregnancy rate of 95% in striped skunks from eastern North Dakota and western Minnesota during 1979 through 1991.

Although rabies is not known to affect implantation rate or embryo mortality, there are several other ways in which rabies may affect productivity. At northern latitudes, striped skunks breed in February and March (Greenwood and Sargeant, 1994), when they frequently occupy communal dens (Gunson and Bjorge, 1979). Although males seldom den together, individual males commonly den concurrently with several females (Houseknecht and Tester, 1978). Communal dens provide a focus for rabies transmission (Rosatte, 1984). Aggressive behavior that is characteristic of skunks with rabies (Charlton et al., 1991) might affect breeding success (Verts, 1967).

The influence of rabies on productivity likely would be additive to other factors that affect skunk populations. Adult skunks and American badgers prey on young skunks in natal dens (Sargeant et al., 1982) and juvenile skunks at northern latitudes may suffer high mortality due to stress and starvation during winter (Schowalter and Gunson, 1982; Fuller and Kuehn, 1985). Based on our findings, we believe that juvenile skunks also are more vulnerable to disease, in this instance rabies, and to predation, than are older skunks (Table 5). At northern latitudes, juvenile skunks commonly disperse from natal areas in fall (Bjorge et al. 1981) when incidence of rabies in skunk populations is high (Hayles and Dryden, 1970), compounding risks to juveniles.

We could not distinguish effects of disease from predation. Seven of the nine skunks whose deaths we attributed to predation were rabid. They may have been predisposed to predation because of changes in behavior or could have been scavenged by a predator after death from rabies. Regardless of the proximate cause of death, however, the ultimate cause of death would have been rabies.

We observed relatively consistent patterns of variation in rates of travel within groups of healthy and rabid skunks. Healthy animals tended to follow a nightly pattern of rapid movement, punctuated periodically with periods of slow movement, possibly while animals foraged. Among rabid skunks, however, rates of travel were erratic within nights, especially during the clinical period when we observed prolonged periods of inactivity on some nights. Some rabid skunks became virtually immobile 2 to 3 days before death. The five skunks we euthanized in the late clinical stage of rabies moved less than 100 m in their final 2 to 3 days.

Our estimates for healthy skunks of average distance traveled in a night and of home range size were slightly lower than reported by Greenwood et al. (1985), who monitored striped skunks in east-central North Dakota during 1977 and 1978. Those authors reported that females traveled 2650 and males 3300 m/night during late April. They estimated home range sizes during the same period of 2.4 km2 for females and 3.1 km2 for males.

We detected no evidence of heightened activity by males or females during the 14-day period before death, which we attributed to the clinical stage of rabies. Rates of travel and distances traveled in a night decreased markedly during the clinical period for both sexes, as did home range size of males. Storm and Verts (1966) concluded that movements of a radio-collared female striped skunk with rabies during the week before her death were not notably different from other female skunks they monitored at that time of year. Andral et al. (1982) likewise detected no change in home range of three radio-collared red foxes with rabies between the pre-clinical and clinical period. However, they reported a change in use of habitat and in diel activity patterns of foxes during the clinical period of rabies. Our sampling scheme was not designed to monitor daytime activity. However, the first radio-collared skunk we found in 1992 with rabies was observed staggering along a roadside at about 1300 on 10 April, 3 days before we found it dead of rabies only 60 m away. Healthy skunks seldom ventured far from their retreats during daytime in April and May in North Dakota (Greenwood et al., 1985). Parker (1962) suggested that skunks observed to be active during daytime are likely to be rabid.

Among skunks we monitored in 1992, rabies appeared to spread first between animals in the center of the radio-collared population. After the first eight or nine animals died, however, there was little consistency to the pattern of deaths of the animals that remained. We do not know when individual animals became infected. Based on dates of death of the skunks that we first found dead of rabies, infection easily could have occurred in winter dens. The incubation period of rabies in striped skunks may vary from 18 to 41 days (Gough and Niemeyer, 1975), but can be considerably longer (Charlton et al., 1991), thus some skunks we monitored may have been infected for several months before we captured them.

Our feeding sites provided a continuous source of food, but we believe they probably did not influence movements or interspecific contact of skunks more than farm middens where skunks are known to forage (R. J. Greenwood, Unpubl.). Although Seidensticker et al. (1988) suggested that radio-collared raccoons, some of which were rabid, moved their dens closer to sites where food was provided, we had no direct evidence that our food manipulations affected rates of travel, distances traveled, or home range sizes of skunks. We cannot explain differences in visitation rates to feeding sites by male and female skunks in relation to rabies status.

Rabies virus typically is transmitted in saliva by biting (Charlton et al., 1991) and we had strong evidence of biting among skunks, as well as among skunks and other carnivores, possibly including coyotes, red foxes, American badgers, raccoons, dogs, and cats. We also detected three cached heads of skunks, which is evidence that carcasses had been eaten. Transmission by eating tissue of a rabid animal is possible (Ramsden and Johnston, 1975). In spite of these interspecific contacts, however, we are not aware of spillover into other species, wild or domestic, during the rabies epizootic we observed. Other than striped skunks, we know of only one animal diagnosed with rabies in the locality of our study area in 1992. That was a red fox about 16 km southwest of our study area. Thus, although the behavior and timing of movements of striped skunks at northern latitudes are conducive to spread of rabies (Sargeant et al., 1982), this epizootic apparently was confined to skunks, and probably would have been undetected without our monitoring.


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