Lloyd B. Keith

Interactive effects of sublethal nematodes and nutritional status on snowshoe hare vulnerability to predation

1. We studied the effect of parasitism on snowshoe hare (Lepus americanus) survival through a field experiment that reduced natural burdens of sublethal nematodes in a free-ranging hare population. We treated half the hares on each of six study areas year-round with an anthelminthic drug, and the other half with a placebo. Potential interactive effects of parasitism and nutrition were examined by supplementing the natural food supply on three of the six study areas during two winters. Survival was measured by radio-collaring a total of 612 hares with mortality-sensitive transmitters and monitoring survival daily between April 1991 and June 1993. 2. Overall, nematode burdens in hares were highest between March and October, and Obeliscoides cuniculi was the most abundant of the five species present. The proximate cause of 95% of mortalities (n = 318) during the study was predation. Predators killed hares with heavy burdens of O. cuniculi disporportionately during May-June, but burdens of the four other species (Nematodirus triangularis, Trichuris leporis, Dirofilaria scapiceps, Protostrongylus boughtoni) were similar between predator-killed hares and the live population. 3. During May-October 1991, the anthelminthic treatment did not affect hare survival, but during May-October 1992 survival of parasite-reduced hares was 2.4-times higher than that of controls. During November 1991-April 1992 survival of food supplemented hares was 21% higher than food-normal animals, but survival was similar during November 1992-April 1993. 4. The effect of parasite-reduction on hare survival was apparently contingent on overwinter food supplies between November 1991 and April 1992, with survival being highest in hares subjected to both treatments, intermediate in those receiving only food supplementation, and lowest in unfed hares. We conclude that the effect of sublethal nematode parasitism on hare survival can be important if interactive with predation, and that synergistic effects of parasitism and nutrition may affect hares if food availability is limited.

Survival of snowshoe hares at a geographic range boundary

The southern limit of snowshoe hare (Lepus americanus) distribution passes through central Wisconsin. Reproduction does not decline at this range boundary, hence lower survival must prevent addi- tional dispersal and colonization. During February 1982-January 1983 we monitored survival of radio- collared hares to test the hypothesis that predation is the major immediate cause of death and is heaviest on dispersers and individuals within habitats having little understory cover. We simulated dispersal by trans- planting snowshoes throughout the year onto study areas with and without good understory cover, inside and outside currently occupied range. A control cohort of residents (not transplanted) was also monitored year-round. Predators killed 87% of the 67 radio-collared hares that died. Decreased survival was strongly associated with hare movements and factors tending to increase movement: viz., dispersal, poor understory cover, presence of resident hares, and fragmented habitat. Survival was apparently enhanced by cover that concealed hares or obstructed predators. Poor physical condition and small body size were linked to increased rates of loss from predation. This study supports the view that predator-caused mortality determines the geographic limit of snowshoe hare distribution in Wisconsin, and losses are most markedly influenced by factors which induce movement. Dispersal beyond established home ranges may be relatively uncommon in these marginal populations due to heavy predation on individuals moving between patches of suitable habitat within relatively large home ranges. The high incidence of trap deaths among hares captured in bogs and the frequency of low bone marrow fat in live-trapped and predator-killed samples suggest that these snowshoes may compromise their access to an adequate food supply by seeking protection from predators in dense conifer cover.

DO PARASITISM AND NUTRITIONAL STATUS INTERACT TO AFFECT PRODUCTION IN SNOWSHOE HARES

We evaluated the hypothesis that the effects of parasitism on animal body condition are accentuated when host nutritional status is compromised. In a field experiment we manipulated natural burdens of five nematode species via anthelmintic treatment in one- half the free-ranging snowshoe hares (Lepus americanus) on each of six study areas and supplemented overwinter food level on three areas, to assess whether treatments interacted synergistically. We predicted that the effects of parasitism would be aggravated in mal- nourished hares (i.e., hares not administered supplemental food), and that animals receiving both treatments would have (1) lower parasite burdens, and (2) higher body mass, fat storage, and reproduction, than those receiving only one or no treatments. Mean numbers of Trichuris leporis were lower in hares subjected to food supplementation, suggesting that nutritional status affected immunity to that species. Obeliscoides cuniculi, Nematodirus triangularis, Dirofilaria scapiceps, and Protostrongylus boughtoni numbers were not directly affected by supplementation. Body mass of parasite-normal controls (i.e., not administered the anthelmintic treatment) was negatively correlated to nematode abundance during May- June, implying that parasitism had a deleterious effect on hare mass at that time. However, the anthelmintic treatment failed to directly affect hare body mass, fat storage, or repro- duction. Food supplementation had a positive effect on body mass, fat storage, and repro- duction, although effects of food were neither strong nor consistent among study areas and body condition parameters being measured. Only 2 of 22 analyses of hare production yielded marginally significant (i.e., 0.05 < P < 0.10) interactions between food and parasitism; therefore, we concluded that the two factors were not strongly linked. However, because our snowshoe hare population was at low densities and likely exposed to neither severe food shortage nor high rates of nematode parasitism, failure to detect an interaction between treatments may not comprise a general refutation of the hypothesis. Rather, hare populations subject to more serious food limitation (i.e., during a cyclic peak in numbers) may be apt to display stronger interactions between nutrition and parasitism.

Lynx-Prey Interactions in Central Alberta

A lynx (Lynx canadensis) study was conducted in central Alberta in 1964-68. Population densities on 57 square miles in winter decreased from 11 in 196>6S to 3 in 1966-67, then increased to 9 in 1967-68. The winter diet was comprised of 76 percent snowshoe hare ( Lepus americanus), 9 percent ruffed grouse (Bonasa umbellus), 3 percent red squirrel ( Tamiasciutus hudsonicus), 10 percent carrion, and other less important items. The relative importance of the major food items did not change significantly between years, but use of carrion was higher in 196S67 than in the previous two winters. Daily food requirements in winter were 600 and 400 grams for adult and juvenile lynxes, respeotively. From December through MarcAh, lynxes removed six, six, two, and three percent of the December hare population; they accounted for 10, 24, 8, and 37 percent of the December to April decline in hare numbers in 196465 through 1967-68, respectively. Lynxes removed less than six, two, one, and two percent of the fall ruffed grouse population during these same winters. Between one and two percent of the fall red squirrel population was taken by lynxes over winter. Kittens were produced in all years, but only those born in 1967 survived through their first winter. Ages of autopsied lynxes also indicated that no young were added to the population in 196>66-the years of lowest hare numbers. Thus, annual productivity of lynxes appears to be direcKy related to abundance of snowshoe hares. We believe that some critical minimum density of hares is necessary for female lynxes to raise kittens. 320 Journal of Wildlife Management, Vol. 36, No. 2, April 1972 ogy and control of the Engelmann spruce beetle in Colorado. U. S. Dept. Agr. Circ. 944. 35pp. MITCHELL, H. H. 1964. Comparative nutrition of man and domestic animals. Vol. a. Academic Press, New York and London. 840pp. OTVOS, I. S. 1965. Studies on avian predators of Dendroctonus brevicomis LeConte ( Coleoptera: Scolytidae ) with special reference to picidae. Canadian Entomol. 97(11 ) :11841199. PORTER, W. P., AND D. M. GA12;S. 1969. TheImodynamic equilibria of animals with environment. Ecol. Monographs 39 ( 3 ): 227-244. VAN DYNE, G. M. 1962. Micro-methods for nutritive evaluation of range forages. J. Range Mgmt. 15 ( 6 ): 303-314. YEAGER, L. E. 1955. TWO woodpecker populations in reladon to environmental change. Condor 57 ( 3 ): 148-153. Received for p2Iblication April 30, 1971. Lynx populations exhibit marked fluctuations that are associated with the well1 A contribution of the Department of Wildlife Ecology, College of Agriculture and Life Sciences, and Research Committee of the Graduate School, University of Wisconsin; the Research Council of Alberta; the Alberta Departnent of Lands and Forests, Fish and Wildlife Division; the Alberta Department of Agriculture, Veterinary Services Branch; the National Science Foundation (Grants GB-6156 and GB-7744); and the Wildlife Management Institute. 2Present address: College of Forest Resources, University of Washington, Seatt]e. 3 Present address: P. O. Box lS9, Happy Valley, Labrador. known 10-year cycle of snowshoe hares as reviewed by Keith ( 1963:6) . The present paper examines some relationships between the lynx and its chief winter prey during a trough (1964 to 1968) in the hare cycle in central Alberta. We thank H. O. Johnson, D. H. Wood, and the late C. H. Browning for assistance with fieldwork. Other students at Rochester were also helpful, especially E. C. Meslow and D. H. Rusch. We are also grateful to H. W. Mossman for help in reading reproductive tracts and to R. D. Taber for reading the manuscript. This content downloaded from 157.55.39.162 on Thu, 11 Aug 2016 06:09:26 UTC All use subject to http://about.jstor.org/terms LYNX-PREY INTERACTIONS * Nellis et al. 321 METHODS AND MATERIALS The main study area was a 57-squaremile block located at Rochester, 60 miles north of Edmonton, Alberta. In 1964, the area was approximately 31 percent open farmland, 34 percent aspen ( Populus tremuZoides ) -dominated upland forest, 16 percent spruce (Picea mariarla and P. glst4ca) forest, 13 percent bog with bog birch ( Betula glandulosa) and willow (Salix spp.) predominating, 2 percent marsh, 2 percent open water, and 3 percent scattered brush on burned-over land. Jack pine ( Pinus banksiana ) was scattered throughout the forested uplands and, on some light soils, formed nearly pure stands. Nine lynx carcasses were also collected from other localities, where the habitat varied from 90 percent cultivated farmland to undisturbed forest. Lynxes were captured in steel traps, immobilized with Sernylan (a phencyclidine hydrochloride from Parke, Davis and Company), marked, and released. Marking devices used were ear tattoos, ear tags, springbronze collars, and Nyanzol D dye in patterns that allowed recognition of individuals. Ear tags and collars were engraved with a number, our address, and notice of a

Characteristics of winter feeding aggregations of ruffed grouse in Alberta

2 reward for return of the tag and

Seasonal and Annual Trends in Numbers of Alberta Ruffed Grouse

4 for both tag and carcass. Trailing three lynxes in winter provided estimates of home range size. Activity centers-separate areas containing lynx sign immediately after fresh snows were located by winter tracks and yielded estimates of lynx densities on the study area. Food habits were determined from analysis of 35 digestive tracts and 123 scats and from records of 261 miles of winter trailing. The data from winter trailing were previously reported (Nellis and Keith 1968). The food from the stomachs was stored in 10 percent formalin until examined; the total volume was determined by water displacement. Food items were separated by species, and the volume and number of individuals of each species were determined. For the number of individuals, the characteristic (teeth, bones, feet, tails) that gave the highest count was utilized.

PARASITISM IN A DECLINING POPULATION OF SNOWSHOE HARES

Winter feeding aggregations of ruffed grouse (Bonasa umbellus) were studied near Roch- ester, Alberta. The annual onset of budding by grouse in fall commenced with the first snow cover. During two winters, aggregation size increased through mid-January, after which there was a significant linear decrease averaging nearly 50 percent by early April. The decrease in group size after mid-January was probably effected chiefly by fragmentation resulting from increasing intragroup strife. Sex and age structure of aggregations was not significantly different from that expected by random combinations. Ruffed grouse fed in male aspen (Populus tremuloides) or in willow (Salix spp.) for an average of 16 minutes during morning, usually leaving at sunrise. Feeding began in evening about 52 minutes after sunset, and lasted an average of 24 minutes. The mean age of 100 male aspen utilized by grouse near Rochester was 36 years. Tree densities at 12 feeding sites were significantly higher than those at systematic-grid stations, drumming logs, and kill sites within aspen stands at Rochester. Buds and twigs of aspen and willow comprised about 80 percent (by volume) of crop contents of 148 grouse shot while budding. Nutrient analyses of male aspen buds indicated that ruffed grouse ingested those buds having the highest protein and potassium contents. Willow buds from grouse crops contained more protein (14.0 percent) than aspen buds from two other groups of crops (12.9 and 11.7 percent).

PREVALENCE OF HELMINTHS IN A CYCLIC SNOWSHOE HARE POPULATION

Estimates of spring populations of ruffed grouse (Bonasa umbellus) on a 4-square-mile area (Main Area) near Rochester, Alberta, increased from 112 grouse in 1966 to 124 in 1967 and to 164 in 1968. Data from smaller study areas and provincewide questionnaires showed similar trends. In 1966 and 1967, grouse populations declined rapidly throughout November, but numbers were stationary between December and the following spring. Approximately 36, 42, and 23 percent of the males present in 1966-68 did not establish territories. The numbers of grouse produced (308 and 330) were similar in 1966 and 1967, and survival of juveniles ( 12 months of age). Predation on grouse, mainly by great horned owls (Bubo ?irginianus), lynxes (Lynx canaderesis), and goshawks (Accipiter gentilis) accounted for more than 25 percent of the annual mortality and for more than 80 percent of fall-to-spring mortality each year. In the fall, predation was selective toward males and young but not toward smaller versus larger grouse. As populations of snowshoe hares (Lepus amertcanus) increased rapidly between 1966 and 1969, great horned owls consumed relatively more snowshoe hares and relatively fewer ruffed grouse. It was this shift in predator food habits that allowed higher survival of young ruffed grouse and was thus responsible for increased numbers of grouse in the spring. Marshall and Gullion 1963, Gullion and Marshall 1968, and others ) have implicated predation as an important proximate source of mortality, but the limiting or regulatory effects of predation on these grouse populations were not clear. In western Canada, where the 10-yearcycle is best known and most pronounced ( Keith 1963), little is known of population dynamics of ruffed grouse and the role of predation in the grouse cycle. IThis paper documents the dynamics of an increasing ruffed grouse population at Rochester, A1berta, during 196S68 and quantifies and evaluates the impact of predation upon numbers of ruffed grouse. We acknowledge D. H. Wood, C. Bitzer, G. Saunders, N. Saunders, R. Saunders, S. Saunders, E. C. Meslow, P. D. Doerr, and C. Cameron for field assistance and thank 803 Islany past studies of ruffed grouse were concerned with periodic or cyclic fluctuations in numbers, and hypotheses concerning these fluctuations are legion (Keith 1963). Two long-term population studies, the ruffed grouse investigation in New York ( Bump et al. 1947 ) and the Minnesota studies at Cloquet (King 1937, Eng 1959, 1 This paper is a contribution of the Department of Wildlife Ecology, University of Wisconsin, and the Research Council of Alberta. The study was supported by the Research Council of Alberta; the University of Wisconsin, College of Agricultural and Life Sciences, and Research Committee of the Graduate School; the Alberta Department of Lands and Forests, Fish and Wildlife Division; the A1berta Department of Agriculture, Veterinaxy Services Branch; the National Science Foundation (Grants GB-615(3 and GB-7744); and the Wildlife Management Institute. 2 Present address: Manitoba Department of Mines, Resollrces and Environmental Management, NVinnipeg. This content downloaded from 157.55.39.223 on Wed, 24 Aug 2016 05:33:10 UTC All use subject to http://about.jstor.org/terms 804 Journal of Wildlife Management, Vol. 35, No. 4, October 1971 was comprised of 9 percent open farmland, 20 percent burn, 27 percent aspen woods, 11 percent spruce woods, and 33 percent open bog. These cover types are largely self-descriptive, but plant communities and history of recent fires on the Main Area are also described in detail by Rusch et al. 1971. A 330x 660-fo+at grid was surveyed and marked on this area, and the grid intersections served as reference points for locations of traps and grouse. Drumming males were trapped on four smaller areas in the springs of 1966-68. The Landing-trail ( 69 acres ), Moores-pinewoods ( 85 acres ), and Halls ( 63 acres ) areas (Fig. 1), also used as study plots for snowshoe hares, are described by Meslow and Keith (1968:813). Upland forest, the primary grouse habitat near Rochester ( Rusch and Keith 1971), covered all of the Landing-trail and Moores-pinewoods areas, and about 40 percent of the Halls Area. The Camp Area (Fig. 1) consisted of 37 acres of mature aspen woods on a northfacing slope of the Tawatinaw River Valley. This area had probably not been burned for 30 years or more, and many aspen, balsam poplar, and scattered white spruce had attained 13 inches or more in diameter. Alder (Alnus crispa and A. rugosa) and willow (Salix spp.) were the dominant shrubs on the Main, Moores-pinewoods, and Halls areas, but beaked hazel (Corylus cornufa) and s askato on ( Ame lanc hi er alnifolia ) were more abundant on the Camp and Landingtrail areas. Drumming males were experimentally removed from Schmidts Area in 1967 and Revols Area in 1968 ( Fig. 1). These areas consisted of 640 acres and 634 acres of predominantly aspen woods. Both were Oll west-facing slopes of the Tawatinaw River Valley, and both had vegetation similar to that on the Camp Area. 9tG STRE M 2 -n g ---O D

Ecology of Red-Tailed Hawk Predation in Alberta

Prevalence and intensity of six endoparasites were determined in 346 snowshoe hares (Lepus americanus) obtained at Rochester, Alberta, during December–April 1981–1982, the second winter of a cyclic population decline. The data were analyzed for (1) differences among host sex and age classes, and among months and sample sources, and (2) evidence that parasitism was of demographic significance to the hare population. Prevalence and intensity of Obeliscoides cuniculi were consistently highest among adult hares, but rose most sharply from February to March among juveniles. In contrast, prevalence and intensity of Nematodirus triangularis were highest among juveniles; prevalence reached 90–100% by January, whereas intensity continued to rise through April. Prevalence and intensity of both Trichuris leporis and Protostrongylus boughtoni were highest also among juvenile hares; neither parameter exhibited a definite trend over time. Prevalences of Taenia pisiformis (cysticerci) and Eimeria spp. were unrelated to sex, age or month; but Taenia intensity was highest among juveniles, and Eimeria intensity tended to decrease from December to April. Intensities of Nematodirus, Protostrongylus and Eimeria were higher in male hares than in females. Prevalence and intensity were correlated directly in Obeliscoides, Nematodirus, Trichuris and Eimeria. Hares that died during trapping and handling, or from natural predation, had greater intensities of Obeliscoides than did animals killed on purpose. There was no indication, however, that risk of death was increased by the other parasitic infections. Age-related immune responses to parasitism (except Obeliscoides) were evidenced by reduced or stabilized prevalence and/or intensity among older hares. A multiple-regression model predicted depressed body weight with increasing intensities of Nematodirus, Trichuris or Protostrongylus. Other body-condition and reproductive indices were unassociated with parasite intensities. Within the hare population, Obeliscoides, Trichuris, Protostrongylus and Taenia had overdispersed distributions (typical of many endoparasites) that did not differ from a negative binomial. The frequency with which each possible combination of helminth species occurred within individual hares was consistent with the assumption that such infections occurred independently. There was no compelling reason to believe parasitism was a significant factor in the overwinter decline of this population of snowshoe hares.

A Correlation Analysis of Weather versus Snowshoe Hare Population Parameters

Five species of helminths were monitored in a population of snowshoe hares (Lepus americanus) near Rochester, Alberta, during 1961-1977. Prevalence of both Obeliscoides cuniculi and Protostrongylus boughtoni among young hares averaged about 50% by age 2 mo, then tended to level off. Prevalence of Taenia pisiformis (cysticerci) and Dirofilaria scapiceps rose more slowly, but continued to increase steadily beyond their mean levels of 8% and 1% at age 2 mo. There were well denned seasonal (within-year) cycles in prevalence of O. cuniculi and P. boughtoni that were generated evidently to a major degree by arrested development of larvae in fall and renewed development in late winter. It was hypothesized that renewed larval development was triggered (in February) in O. cuniculi by the seasonal rise of circulating pituitary gonadotropins, and (in April) in P. boughtoni by the seasonal rise of gonadal androgens and estrogens. Indices to gonadal hormone levels in hares indicated that these increased most rapidly among males, and may have accounted for the higher prevalences of P. boughtoni in males during April-May. Neither T. pisiformis nor D. scapiceps exhibited conspicuous seasonal changes in prevalence. Maximum prevalence of T. pisiformis was attained at about 1 yr of age, whereas D. scapiceps increased among adult snowshoes through age 2 yr before stabilizing. Long-term (between-year) changes in prevalence of O. cuniculi, T. pisiformis, and D. scapiceps were correlated significantly with the cyclic hare population which declined from a peak in fall 1961 to a low in 1965–1966, rose to another peak by fall 1970, and declined again to a low in 1975. There was no detectable time lag between this “10-yr” cycle in hare density and the cycles of parasite prevalence among juveniles (<1 yr of age). Among adult hares, the cycle of O. cuniculi prevalence was likewise synchronous with that of the hare population, but the cycles of D. scapiceps and T. pisiformis lagged by approximately 1 and 2 yr, respectively. This lag in T. pisiformis prevalence was largely inexplicable to us. Our data on P. boughtoni were not suitable for analyses of between-year trends; nor were those for the fifth helminth, Taenia serialis (coenuri), because mean prevalence was less than 1% among both juveniles and adults. An apparent decline in T. serialis after the early 1950s, and its continued scarcity thereafter, paralleled a major change in numbers of one important definitive host—the red fox (Vulpes vulpes). Lighter weights of young hares at age 37–96 days, and of adults and fully grown juveniles, were associated with P. boughtoni infections. There was no demonstrable relationship between snowshoe hare reproductive parameters and helminth parasitism.