Population genetic structure of the cyclic snowshoe hare (Lepus americanus) in southwestern Yukon,Canada

Spatial population structure has important ecological and evolutionary consequences. Little is known about the population structure of snowshoe hares (Lepus americanus), despite their ecological importance in North American boreal forests. We used seven variable microsatellite DNA loci to determine the spatial genetic structure of snowshoe hares near Kluane Lake, Yukon during a cyclic population peak. We sampled 317 hares at 12 sites separated by distances ranging from 3 to 140 km, and used 46 additional samples from Alaska and Montana. The level of genetic variation was high (13.4 alleles/locus, 0.67 expected heterozygosity) and the distribution of alleles and genotypes was not homogeneous across the sites. The degree of differentiation was low among Yukon sites (FST = 0.015) and between Yukon and Alaska (FST = 0.012), but the Montana site was highly differentiated (FST = 0.20). A weak pattern of isolation by distance was found over the Yukon study area, with an indication that local genetic drift may be important in shaping the regional genetic structure. Landscape barriers expected to influence gene flow did not consistently affect genetic structure, although there was evidence for a partial barrier effect of Kluane Lake. The high level of inferred gene flow confirms that snowshoe hare dispersal is widespread, successful and equal between the sexes. A stepping-stone model of gene flow, potentially influenced by the synchronous density cycle, appears to best explain the observed genetic structure. Our results suggest that despite their dramatic fluctuations in density, snowshoe hares in the northern boreal forest have a large evolutionary effective population size and are not strongly subdivided by either physical or social barriers to gene flow.     

Prevalence of helminths in a cyclic snowshoe hare population

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 defined 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 gonadotrophins, 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 lage between this "10-yr" cycle in hare density and the cycles of parasite prevalence among juveniles (less than 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 1950's, and its continued scarcity thereafter, paralleled a major change in numbers of one important definitive host--the red fox (Vulpes vulpes).(ABSTRACT TRUNCATED AT 400 WORDS)     

Powassan virus infection in snowshoe hares (Lepus americanus)

Sera from snowshoe hares (Lepus americanus) trapped near Rochester, Alberta, Canada were tested for Powassan virus antibody by the constant virus/serum dilution neutralization test. Of 1264 serum samples tested, 137 had an antibody titer of at least 1:4 for Powassan virus. Ten hares were inoculated with Powassan virus in the laboratory. Viremia lasted 4-5 days and ceased with the appearance of Powassan antibody in the serum. Neutralizing antibody reached a peak titer of 1:119 on day 15 post-inoculation and was still detectable 13 months post-inoculation.     

Actinobacillosis in free-ranging snowshoe hares (Lepus americanus) from Alaska

Actinobacillus capsulatus was isolated from lung, liver, and/or spleen tissue of three snowshoe hares (Lepus americanus) in Alaska. This is the first report of the isolation of this bacterium from free-ranging hares. Actinobacillus capsulatus may have a negative impact on the population density of hares.     

The hidden history of the snowshoe hare,Lepus americanus: extensive mitochondrial DNA introgression inferred from multilocus genetic variation

Hybridization drives the evolutionary trajectory of many species or local populations, and assessing the geographic extent and genetic impact of interspecific gene flow may provide invaluable clues to understand population divergence or the adaptive relevance of admixture. In North America, hares (Lepus spp.) are key species for ecosystem dynamics and their evolutionary history may have been affected by hybridization. Here we reconstructed the speciation history of the three most widespread hares in North America – the snowshoe hare (Lepus americanus), the white‐tailed jackrabbit (L. townsendii) and the black‐tailed jackrabbit (L. californicus) – by analysing sequence variation at eight nuclear markers and one mitochondrial DNA (mtDNA) locus (6240 bp; 94 specimens). A multilocus–multispecies coalescent‐based phylogeny suggests that L. americanus diverged ~2.7 Ma and that L. californicus and L. townsendii split more recently (~1.2 Ma). Within L. americanus, a deep history of cryptic divergence (~2.0 Ma) was inferred, which coincides with major speciation events in other North American species. While the isolation‐with‐migration model suggested that nuclear gene flow was generally rare or absent among species or major genetic groups, coalescent simulations of mtDNA divergence revealed historical mtDNA introgression from L. californicus into the Pacific Northwest populations of L. americanus. This finding marks a history of past reticulation between these species, which may have affected other parts of the genome and influence the adaptive potential of hares during climate change.     

An assessment of overwinter food limitation in a snowshoe hare population at a cyclic low

Snowshoe hares (Lepus americanus) undergo 8- to 11-year population cycles caused by direct and/or interactive effects of overwinter food shortage and predation. However, the demographic significance of food shortage during cyclic population lows remains unclear. I evaluated the importance of overwinter food limitation to the demography (numbers, age and sex ratios) of low-density hare populations during two winters in Manitoba. Also, I examined whether the hypothesized differences in demography of fed and unfed hare populations could be explained by altered movement patterns or social dynamics. Bimonthly live-trapping revealed that food failed to have a direct long-term effect on the number, or change in number, of hares estimated to be on the three supplemented areas, relative to three control areas. Modest numerical responses to supplementation tended to be short-term (i.e., restricted to winter) and related to pre-supplementation densities, with the study area characterized by the highest hare density displaying the strongest and most consistent response to added food. During winter the percentage of females was remarkably variable among study areas and time periods, but added food may have augmented slightly the proportion of females captured in traps. There tended to be slightly more juveniles on supplemented areas during winter periods, and this effect was strongest during the first winter (1991–1992). I found that immigration rates and percentage of hares that were considered to be transient animals were similar on supplemented and control areas, and that spatial distribution of radio-collared animals on versus off of study areas also was similar. Because the overall effect of food on hare populations was small and short-lived, and could be explained largely by small increases in survival and reproduction, I conclude that the study population was not subject to overwinter food limitation. Received: 22 February 1998 / Accepted: 12 February 1999     

Patterns and potential drivers of intraspecific variability in the body C,N, and P composition of a terrestrial consumer,the snowshoe hare (Lepus americanus)

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Serologic survey for Actinobacillus capsulatus in free-ranging snowshoe hares (Lepus americanus) from Alaska and Alberta

A plate agglutination method was developed to test sera from free-ranging snowshoe hares (Lepus americanus) captured in Alaska (USA) or Alberta (Canada) for antibody against Actinobacillus capsulatus. Antiserum against A. capsulatus was prepared in a domestic rabbit. A concentrated suspension of formalin-killed A. capsulatus was prepared for use as an antigen. Serum antibody prevalence for hares was 98 of 239 (41%) in Alaska and 51 of 111 (46%) in Alberta. Prevalence in Alaska peaked in 1981 corresponding to a peak in hare population density. Seasonal prevalence peaked in May in Alaska. Prevalence at one capture site in Alaska was significantly higher than at four other sites. There was no difference in sex-specific prevalence for either Alaska or Alberta.     

Helminth communities of an introduced hare (Lepus granatensis) and a native hare (Lepus europaeus) in southern France

We investigated the parasite communities of introduced Iberian hares (Lepus granatensis) and native European hares (Lepus europaeus) in southern France, where Iberian hares were introduced locally 20 yr ago as a game animal. Parasite communities of sympatric populations of the two hare species and of allopatric populations of European hares were compared. Iberian hares in France harbored a depauperate community of parasites relative to the population in its native habitat in Spain. European hares in areas of sympatry also were infected by Nematodiroides zembrae, which normally infects Iberian hares on their native range.     

Critical temperature and changes in cuticular lipids in the rabbit tick, Haemaphysalis leporispalustris

The epicuticle in the rabbit tick, Haemaphysalis leporispalustris, appeared to be continuously changing, with deposition and removal of lipids during and after engorgement. These changes were accompanied by corresponding changes in critical temperature. The correlation between changes in critical temperature and composition of cuticular lipids (i.e. changes in the number, types, and relative concentration of lipid classes) suggested that changes in lipid composition could be responsible for changes in critical temperature.A hypothesis, alternative to those of Beament and Locke, is proposed to explain the phenomenon of critical temperature. At critical temperature, certain lipids probably change phase from crystal to liquid crystal, with hydrocarbon chains in a highly mobile condition. The hypothesis is not based on the presence of a water-proofing monolayer, and is supported by transition phenomena known in many lipids.     

A natural feeding experiment on a declining snowshoe hare population

Summary A snowshoe hare (Lepus americanus) population on a 9-ha area was supplied with extra natural food by chopping down large white spruce (Picea glauca) and aspen (Populus tremuloides) trees throughout 3 winters from 1981 to 1984. Hares fed vigorously on the downed trees, but the phase of decline of the ten-year cycle occurred equally on control and experimental grids from 1981–1983, and we could detect no improvement in survival or reproduction on the food area. Growth rates were improved on the food grid during the first winter of the decline (1981–82). We concluded that food shortage is not necessary for the cyclic decline of snowshoe hares in the southern Yukon.     

A plant toxin mediated mechanism for the lag in snowshoe hare population recovery following cyclic declines

A necessary condition for a snowshoe hare population to cycle is reduced reproduction after the population declines. But the cause of a cyclic snowshoe hare population's reduced reproduction during the low phase of the cycle, when predator density collapses, is not completely understood. We propose that moderate‐severe browsing by snowshoe hares upon preferred winter‐foods could increase the toxicity of some of the hare's best winter‐foods during the following hare low, with the result being a decline in hare nutrition that could reduce hare reproduction. We used a combination of modeling and experiments to explore this hypothesis. Using the shrub birch Betula glandulosa as the plant of interest, the model predicted that browsing by hares during a hare cycle peak, by increasing the toxicity B. glandulosa twigs during the following hare low, could cause a hare population to cycle. The model's assumptions were verified with assays of dammarane triterpenes in segments of B. glandulosa twigs and captive hare feeding experiments conducted in Alaska during February and March 1986. The model's predictions were tested with estimates of hare density and measurements of B. glandulosa twig growth made at Kluane, Yukon from 1988–2008. The empirical tests supported the model's predictions. Thus, we have concluded that a browsing‐caused increase in twig toxicity that occurs during the hare cycle's low phase could reduce hare reproduction during the low phase of the hare cycle.     

Biases in the estimation of the demographic parameters of a snowshoe hare population

1. Survival rates and natalities for a population of snowshoe hares in the Yukon were estimated independently of and simultaneously with estimates of population change during the increase phase of a hare cycle.
2. Simple demographic models are used to show that even though the estimated survival rates and natalities were high relative to previously published estimates, the observed demographic parameters are unable to explain the extent of population increase, and we conclude that some of these parameters must be underestimates.
3. A sensitivity analysis is used to examine the potential influence of changes in these demographic parameters on the population growth rate. During most years of the hare cycle the population growth rate is potentially most sensitive to changes in juvenile postweaning survival. Only during crash years is adult survivorship likely to be a more important determinant of the rate of population change.
4. Examination of previously published data sets on two full population cycles suggests that while survival rates are positively correlated with population growth rates, their incorporation into demographic models results in frequent underestimation of the rate of population increase.     

European hare (Lepus europaeus) invasion ecology: implication for the conservation of the endemic Irish hare (Lepus timidus hibernicus)

European hare Lepus europaeus populations have undergone recent declines but the species has successfully naturalised in many countries outside its native range. It was introduced to Ireland during the mid-late nineteenth century for field sport and is now well established in Northern Ireland. The native Irish hare Lepus timidus hibernicus is an endemic subspecies of mountain hare L. timidus and has attracted major conservation concern following a long-term population decline during the twentieth century and is one of the highest priority species for conservation action in Ireland. Little is known about the European hare in Ireland or whether it poses a significant threat to the native mountain hare subspecies by compromising its ecological security or genetic integrity. We review the invasion ecology of the European hare and examine evidence for interspecific competition with the mountain hare for habitat space and food resources, interspecific hybridisation, disease and parasite transmission and possible impacts of climate change. We also examine the impact that introduced hares can have on native non-lagomorph species. We conclude that the European hare is an emerging and significant threat to the conservation status of the native Irish hare. Invasive mammal species have been successfully eradicated from Ireland before and immediate action is often the only opportunity for cost-effective eradication. An urgent call is issued for further research whilst the need for a European hare invasive Species Action Plan (iSAP) and Eradication strategy are discussed.