Northern Prairie Wildlife Research Center
In the Denali system, numbers of moose, caribou, sheep, and wolves have been interacting and fluctuating naturally for many years. During our study, caribou increased (Adams et al. 1993). This finding may represent one of the exceptions implied by Seip (1991:51), when he concluded that, "Caribou generally appear unable to survive in areas where there is extensive overlap with wolves and alternate prey species."
We do not know the trend in populations of moose and sheep. No drastic decline was not discernible in either, and both species remained about as widely distributed as they have been for decades (Haber 1977). Wolves consumed their prey as completely as possible, leaving only hair, rumen contents, and bones, most of them chewed. Thus, there was no indication, such as incomplete consumption of kills (Pimlott et al. 1969, Mech and Frenzel 1971a, Peterson 1977), that conditions were especially extreme for prolonged periods during most of the study.
Under these circumstances, the Denali wolves found enough prey not only to survive and reproduce, but to double in numbers (Meier et al. 1993) during a period of widely variable snowfall. They showed a high degree of selectivity in their predation patterns over different dimensions in their relationships with prey. The commonality of each dimension, however, was prey vulnerability.
Vulnerability took the form of youth, old age, poor condition, and hindrance by snow, and it varied by species, sex, time of year, and snow depth. Calves were especially important prey during summer when they are weakest, bulls before, during and after their autumn rut when they are most vulnerable, and cows in late winter when snow depth, negative energy-balance, and the drain of pregnancy reduce nutritional state. Probably the poor nutritional condition of caribou bulls during and after the rut (Table 5) explains why wolves took proportionately more bulls than cows. Although cows and calves become more vulnerable primarily during or after winters of above-average snowfall, bulls must rut every year. Rutting ungulates are generally in poor nutritional condition due to fighting and chasing females rather than feeding (Bergerud 1973, Geist 1974, Clutton-Brock et al. 1982). The reason for caribou bull vulnerability before the rut is currently under investigation (Adams et al. in preparation).
Our sample of sheep kills was small and biased. Nevertheless, it is clear that wolves kill sheep year around, apparently more during late fall, possibly a result of the vulnerability of rutting males. Murie (1944) and Haber (1977) also found that sheep were important to wolves in Denali.
|Denali National Park, formerly known as Mt. McKinley National Park, has been an important area for extensive, long-term wolf/ungulate studies dating back to 1944. Adolf Murie was the first to conduct a study. Dall sheep (top photo) are an important prey species. Current research (right photo) involves radio-collaring of wolves and subsidiary studies of prey species.|
Skeletal abnormalities and other possibly-debilitating factors were found among prey remains. The incidence of these conditions in the general prey population is unknown, and to what degree they contribute to prey vulnerability is open to conjecture. Jaw necrosis can result in abnormal occlusion and tooth loss, and was common in adult moose and sheep taken by wolves. Arthritis of the lumbosacral joint (between the sacrum and sixth lumbar vertebra) appears to be related to age in moose, with severe arthritis common in animals ≥15 years. Few skeletal abnormalities have been found among the remains of caribou eaten by wolves.
The mean ages of female prey animals taken were older than those of males. Because arthritis did not afflict cow moose until much older than bulls, this suggests that the arthritis may have helped predispose older individuals to predation.
Although Denali wolves were able to survive and increase during periods of below-average snowfall, above-average snowfall in Denali helped predispose prey to wolf predation. Deep snow had a direct effect on reducing prey condition and mobility and thus increasing predation by wolves (Mech and Frenzel 1971a, Mech and Karns 1977, Peterson 1977, Haber 1977, Nelson and Mech 1986b). We also found evidence of an indirect effect of snow depth on caribou calves that had been in utero and thus were predisposed to wolf predation during the next summer (Adams et al. 1993) and winter (Table 2), similar to findings in other wolf-prey systems (Mech and Karns 1977, Peterson 1977, Mech et al. 1987, 1991b). The most important common denominator in predisposing Denali prey to wolves was probably nutritional condition indicated by the low marrow fat content in all of the prey species, ages, and sexes of our wolf-kill sample (Table 4). Considering that some individuals must have been predisposed by physical frailties not apparent in the bones, which were usually all that could be examined for most kills (Mech 1970), and that such animals would not necessarily show low marrow fat (Mech and DelGuidice 1985), the low average percent fat we found is striking. This is especially true given that our values are probably artificially high (see Methods).
In caribou, femur fat <70% indicates that the animal's body weight has declined about to its limit (Dauphine 1971), with total body fat <5% (Huot and Goudreault 1985). Adult caribou cows in good condition possess 11-14% body fat (Dauphine 1971, Huot and Goudreault 1985), and bulls ≥31% (Dauphine 1971), with marrow fat ≥70%. Starvation has been documented in adult moose at a mean marrow fat level of 52% (S.E.= 15.3) (Ballard et al. 1987).
However, several workers believe that marrow fat must reach much lower levels before indicating that an animal is near death. Stephenson and Johnson (1972), Franzmann and Arneson (1976), Peterson et al. (1984) and Hayes et al. (1991) used 20% marrow fat in adults and 10% in calves as indicators of starvation. Although there is value in being conservative, using such low levels ignores starvation physiology and risks reaching erroneous conclusions.
Ungulate marrow fat ≤70-87%, depending on species, is a direct indicator of total body fat, but by the time the marrow fat is as low as this threshold, the greater majority of body fat has already been lost (Dauphine 1971, Huot and Goodreault 1985, Watkins et al. 1991, Holand 1992). As ungulates lose fat stores, they also lose protein, or muscle mass (Leibholz 1970, Paquay et al. 1972, Hovell et al. 1987, Torbit et al. 1985, DelGuidice et al. 1990). In adult white-tailed deer (Odocoileus virginianus), for example, the R2 between weight loss and protein (muscle) loss was 0.91 (DelGuidice et al. 1990). At maximal work loads, such as when running from wolves, it is muscle glycogen that forms the major source of fuel (Froberg et al. 1971, Hultman and Nilsson 1971). Furthermore, blood glucose which also is important to a running animal, in starved individuals falls to about a third of its level in fed animals, and insulin which fosters glucose use, drops to one-tenth (Smith et al. 1983:542).
Thus, marrow-fat percentage should be viewed not so much in terms of a fat indicator, but as an indicator of fat, muscle, and energy depletion, and any level below the threshold indicates an animal in marginal condition. While it certainly is true that some individuals do not actually die until their marrow fat is almost depleted, loss of vigor and vitality is a matter of degree rather than an all-or-none phenomenon. Additional stressors such as fighting, plowing through snow, or being chased by wolves probably would raise the marrow-fat threshold at which individuals in marginal condition would perish. This relationship could explain Ballard's et al. (1987) starved moose with a mean of 52% marrow fat.
Given the above considerations, we believe that most of our wolf-killed moose and caribou were in poor condition. Because such individuals would have lost considerable muscle mass as well as fat, these animals would have had little energy left to withstand chases by wolves.
The marrow fat content of Denali wolf-killed prey was consistently low despite relatively low snow depths in some years. There seemed to be no relationship between percentage marrow fat in our wolf kills and the snowfall, except that marrow fat of our moose kills was lowest during the winter of deepest snow (Table 1, Table 4).
The preponderance of low marrow fat despite low snow depth during three of the seven years of the study indicates that the unharvested Denali prey herds must include a certain proportion of individuals that are unable to secure sufficient food, even under average environmental conditions. Our data indicate that such individuals are among the oldest, youngest, and the bulls during the rut. This situation probably is typical of natural ungulate populations unharvested by humans. Wolves could depend on such vulnerable members of natural prey populations, along with the young which are generally more vulnerable, to sustain their own numbers during most years. When snowfall, or other weather factors become extreme and increase prey vulnerability, wolf populations can increase (Mech 1977b, Peterson 1977) to make use of the sudden increase in resources, such as the caribou in our study.