Defense of winter-dormant Alaska paper birch against snowshoe hares

Summary Mature growth-phase internodes of Alaska paper birch (Betula resinifera) are preferred by the snowshoe hare (Lepus americanus) over juvenile growth-phase internodes due to the low food value of the latter. While the mature over juvenile preferencec cannot be explained by the levels of inorganic nutrients or gross chemical fractions (resins or phenols), it can be explained by the striking differences in secondary metabolites of the two growth phases. The principle compound which renders the juvenile phase internodes unpalatable is papyriferic acid, a triterpene which is a demonstrated feeding deterrent to snowshoe hares and which is present in juvenile internodes at concentrations 25 times greater than those in mature internodes.     

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.     

Do plant secondary compounds determine feeding preferences of snowshoe hares?

Summary We investigated the food preferences of captive snowshoc hares (Lepus americanus) in winter to test three hypotheses proposed to explain food choices by hares: (1) that food choice is related to the protein content of twigs; 92) that defensive chemicals present in twigs are negatively correlated with hare food preferences; and (3) that hares eat less-preferred but protein-rich twigs when their diet is buffered by large amounts of palatable food. Hares exhibited striking and consistent preferences for different species and, in general, preferred mature twigs to juvenile growth stages. Preferences across species among mature twigs were not, however, the same as preferences for juvenile growth stages across species. None of the three hypotheses adequately explained food choice by hares. Hares did not (1) select twigs that were high in protein content. They also did not (2) consistently select twigs that were low in resins or phenols. Finally (3), hares generally ate less, not more of non-preferred twigs in the presence of a protein and energy rich alternative food, commercial rabbit chow. Food preferences of hares must presumably have some chemical basis, but no simple theory has yet explained what this is. We suggest that hares may not be under severe dietary constraints imposed by chemical defenses in winter.     

Winter browsing on Alaska feltleaf willow twigs improves leaf nutritional value for snowshoe hares in summer

In boreal forests, browsing by mammals on winter-dormant twigs increases leaf nitrogen, leaf greenness, and leaf size. This suggests browsing reduces competition among meristems for mineral nutrients, and in particular, competition for nitrogen. Winter browsing also reduces the shoot carbohydrate reserves used by leaves to produce condensed tannin. These effects of winter browsing are predicted to improve the nutritional value of leaves for mammals because they increase the mass of digestible nitrogen in leaves. This hypothesis was tested using Alaska feltleaf willow and the snowshoe hare as the experimental system. Six in vivo indicators of leaf nutritional quality were used to compare leaves from winter-browsed plants with leaves from unbrowsed plants. The indicators used were dry matter intake, nitrogen intake, condensed tannin intake, dry matter digestibility, apparent digestibility of nitrogen and nitrogen retention. The results obtained were in agreement with the above hypothesis. In early summer, at the time snowshoe hares and other northern herbivores reproduce, hares fed leaves from browsed plants consumed more nitrogen, digested more of the nitrogen they consumed, and retained more of the nitrogen they digested than did hares fed leaves from unbrowsed plants. The high nitrogen content and low tannin content of leaves from browsed plants may explain this browsing caused increase in leaf nutritional value. How these positive effects of winter browsing on snowshoe hare nutrition at the time of reproduction might affect hare population dynamics are briefly discussed.     

Variation in quality of mountain birch and tea-leaved willow for mammal and insect herbivores: differences among trees, among sites and between tree species

We evaluated palatability of winter dormant tree twigs to the mountain hare Lepus tunidus and the grey-sided vote Clethrionomys rufocanus with captive animals We tested differences among trees within sites, among sites, and between two tree species (the mountain birch Betula pubescens ssp czerepanovii and the tea-leaved willow Salix phylicifolia ) In one of the sites, we also measured growth rates of autumnal moth Epirrita autumnata larvae on the same trees that were used m preference trials with the hares and voles The differences m palatability to hares and voles were greatest at the level of tree Species, both hares and voles preferred birches over willows, but with the hare there was some overlap in palatability between the tree species There were also large and significant differences among sites and among trees within sites Within sites, variation in tree palatability seemed to be larger among willows than among birches Hares and voles may select willows at least partly on the same basis, but there was no correlation between palatability of the trees to the mammals and the growth rate of the larvae of the autumnal moth on the same trees Variation in twig palatability to the hares and voles was so large at all levels (among trees within sites, among sites and between tree species) that we suggest it also has implications for food selection of these mammalian herbivores under natural conditions     

The effects of elevated CO2 and temperature on the resistance of winter-dormant birch seedlings (Betula pendula) to hares and voles

The effects of elevated CO₂ and temperature on the resource allocation pattern and resistance against mammalian herbivores of silver birch (Betula pendula Roth) were studied. Birch seedlings were grown through two growing seasons in closed‐top chambers exposed to four different treatments: ambient CO₂ and temperature, elevated atmospheric CO₂ (700 ppm) and ambient temperature, elevated temperature (+3°C above ambient) and ambient CO₂, and a combination of elevated CO₂ and temperature. After winter hardening of the seedlings, the growth of the seedlings was measured and the concentration of secondary compounds such as phenolics and papyriferic acid determined. The top parts of the stem were fed to hares, and the basal parts of the same stems were offered to voles. Elevated CO₂ increased the height and basal diameter of the shoots, shoot biomass and total biomass of the seedlings but did not have any effect on secondary chemistry. Elevated temperature increased the height and shoot biomass, but did not have a significant effect on the total biomass of the seedlings. Elevated temperature decreased the concentration of condensed tannins and their precursor, (+)‐catechin, in the top part of the stems, but only the concentration of (+)‐catechin in the basal part of the stems. There were no significant interactive effects between CO₂ and temperature on phenolics in the stems, while the concentration of papyriferic acid showed significant interaction in the top part of the stems. This indicates high accumulation of papyriferic acid in ambient CO₂ under increased temperature. Consequently, elevated temperature increased the resistance of birch against hares, but did not affect the resistance of the basal parts of the same birches to voles. Our results indicate that the predicted climatic change will not necessarily lead to increased browsing damage by the mountain hare and the field vole to silver birch.     

Owl predation on snowshoe hares: consequences of antipredator behaviour

We show evidence of differential predation on snowshoe hares (Lepus americanus) by great horned owls (Bubo virginianus) and ask whether predation mortality is related to antipredator behaviour in prey. We predicted higher predation on (1) young and inexperienced hares, (2) hares in open habitats lacking cover to protect from owl predation, and (3) hares in above average condition assuming that rich food patches are under highest risk of predation. Information on killed hares was obtained at nest sites of owls and by monitoring hares using radio-telemetry. The availability of age classes within the hare population was established from live-trapping and field data on reproduction and survival. Great horned owls preferred juvenile over adult hares. Juveniles were more vulnerable to owl predation before rather than after dispersal, suggesting that displacement or increased mobility were not causes for this increased mortality. Owls killed ratio-collared hares more often in open than in closed forest types, and they avoided or had less hunting success in habitats with dense shrub cover. Also, owls took hares in above average condition, although it is unclear whether samples from early spring are representative for other seasons. In conclusion, these results are consistent with the hypothesis that variation in antipredator behaviours of snowshoe hares leads to differential predation by great horned owls.     

Novel wildlife in the Arctic: the influence of changing riparian ecosystems and shrub habitat expansion on snowshoe hares

Warming during the 20th century has changed the arctic landscape, including aspects of the hydrology, vegetation, permafrost, and glaciers, but effects on wildlife have been difficult to detect. The primary aim of this study is to examine the physical and biological processes contributing to the expanded riparian habitat and range of snowshoe hares (Lepus americanus) in northern Alaska. We explore linkages between components of the riparian ecosystem in Arctic Alaska since the 1960s, including seasonality of stream flow, air temperature, floodplain shrub habitat, and snowshoe hare distributions. Our analyses show that the peak discharge during spring snowmelt has occurred on average 3.4 days per decade earlier over the last 30 years and has contributed to a longer growing season in floodplain ecosystems. We use empirical correlations between cumulative summer warmth and riparian shrub height to reconstruct annual changes in shrub height from the 1960s to the present. The effects of longer and warmer growing seasons are estimated to have stimulated a 78% increase in the height of riparian shrubs. Earlier spring discharge and the estimated increase in riparian shrub height are consistent with observed riparian shrub expansion in the region. Our browsing measurements show that snowshoe hares require a mean riparian shrub height of at least 1.24–1.36 m, a threshold which our hindcasting indicates was met between 1964 and 1989. This generally coincides with observational evidence we present suggesting that snowshoe hares became established in 1977 or 1978. Warming and expanded shrub habitat is the most plausible reason for recent snowshoe hare establishment in Arctic Alaska. The establishment of snowshoe hares and other shrub herbivores in the Arctic in response to increasing shrub habitat is a contrasting terrestrial counterpart to the decline in marine mammals reliant on decreasing sea ice.     

Survival of dispersing versus philopatric juvenile snowshoe hares: do dispersers die?

We used radio-telemetry to monitor the survival of dispersing and philopatric juvenile snowshoe hares ( Lepus americanus ) in southwestern Yukon Territory, Canada, during a cyclic population increase. Neither 28-d survival nor the proportion of hares surviving to breed differed significantly between juvenile hares that dispersed and those that did not, nor was there a significant relationship between dispersal distance and fate (dead or alive). Our results indicate that the overall survival cost associated with natal dispersal is low for snowshoe hares during the early increase of the hare cycle.     

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.     

Effects on heather of heavy grazing by mountain hares

Continual heavy grazing of small patches of heather by mountain hares produces conspicuous, short, lawn-like bushes. Their probable development is described. The shoots of such heather bushes maintained a juvenile appearance, contained more nitrogen and phosphorus than the surrounding heather and, to judge from their chemical composition, were more digestible. The generalization that tree and shrub twigs of juvenile growth form are more unpalatable to hares than twigs of mature growth form did not apply in this case.     

An antifeedant in balsam poplar inhibits browsing by snowshoe hares

Summary The plant defense guild hypothesis for the evolution of plant secondary chemicals predicts that plant species defend themselves against generalist herbivores such as the snowshoe hare (Lepus americanus) in the Canadian boreal forest by evolving unique antifeedant chemicals. Plant species may coevolve in an ecosystem by presenting an array of chemicals to herbivores. We report further evidence for this idea from the presence of 2,4,6-trihydroxydihydrochalcone in the CH₂Cl₂ extracts of Populus balsamifera juvenile twigs. These extracts, added to rabbit chow, were offered to hares in choice tests. The bioassay established that the chemical acted as an antifeedant for hares.     

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.     

Elevated CO2 alters birch resistance to Lagomorpha herbivores

We studied the three‐way interaction of elevated CO₂, nitrogen (N), and temperature (T), and the two‐way interaction of elevated CO₂ and early‐season defoliation on the secondary chemistry and resistance of Eurasian silver birch (Betula pendula) and North American paper birch (B. papyrifera) against the Eurasian hare (Lepus timidus) and the North American eastern cottontail rabbit (Sylvilagus floridanus), respectively. Elevated CO₂ decreased the palatability of winter‐dormant silver and paper birch stems to both hares and rabbits, respectively. But the effect on hares was only apparent at intermediate levels of N fertilization. Elevated T had no effect on palatability. The effects of elevated CO₂, N, and T on levels of silver birch bark phenolics and terpenoids were dominated by two‐way interactions between N and CO₂, and N and T. Generally, however, N amendments elicited a parabolic response in carbon partitioning to most biosynthetic classes of silver birch phenolics (i.e. highest concentrations occurring at intermediate N). CO₂ elevation was most enhancing at highest levels of N. On the other hand, T increases, more often than not, elicited reductions in phenolics, but especially so at the highest N level. In the case of B. papyrifera, elevated CO₂ increased carbon partitioning to Folin‐Denis stem and branch phenolics and condensed tannins. Early‐season defoliation, on the other hand, had no effect on phenolics and tannins but lowered both N and energy levels of branches. Elevated CO₂ substantially ameliorated the negative effects of severe defoliation on tree growth. These results support the hypothesis that continuing anthropogenic alterations of the atmosphere may trigger significant changes in plant phenotypic resistance to mammalian herbivores owing to an increasing net carbon balance between the highly vagile supply and demand capacities of plant carbon sources and sinks.     

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.     

Age-related changes in defensive traits of Acacia tortilis Hayne

The theory of plant defences proposes that investments in physical and chemical defences are driven by the risk of herbivore damage, and limited by the cost of producing the particular defensive trait in terms of resources that could be directed to other sinks, such as growth and reproduction. We sampled twigs of 18 mature Acacia tortilis trees and their cohort of juveniles to test some predictions of this hypothesis. We expected a higher allocation of defensive traits to leaves and twigs in the young plants than in the mature ones as a result of a higher risk of damage by ungulates at the juvenile stage. Our results show that the juvenile plants produce more spines along their twigs, but have lower concentrations of phenolic compounds in their leaves than in the mature ones. We also expected a negative relation between the concentration of foliar nutrients and phenolic compounds, as predicted by the carbon/nutrient hypothesis. Only mature plants showed this pattern. Reproduction (in mature plants) and water stress (in juvenile plants) did not relate to allocation to secondary compounds as predicted by current hypotheses of plant defence.     

Multiscale habitat relationships of snowshoe hares (Lepus americanus) in the mixed conifer landscape of the Northern Rockies,USA: Cross‐scale effects of horizontal cover with implications for forest management

Snowshoe hares (Lepus americanus) are an ecologically important herbivore because they modify vegetation through browsing and serve as a prey resource for multiple predators. We implemented a multiscale approach to characterize habitat relationships for snowshoe hares across the mixed conifer landscape of the northern Rocky Mountains, USA. Our objectives were to (1) assess the relationship between horizontal cover and snowshoe hares, (2) estimate how forest metrics vary across the gradient of snowshoe hare use and horizontal cover, and (3) model and map snowshoe hare occupancy and intensity of use. Results indicated that both occupancy and intensity of use by snowshoe hares increased with horizontal cover and that the effect became stronger as intensity of use increased. This underscores the importance of dense horizontal cover to achieve high use, and likely density, of snowshoe hares. Forest structure in areas with high snowshoe hare use and horizontal cover was characterized as multistoried with dense canopy cover and medium‐sized trees (e.g., 12.7–24.4 cm). The abundance of lodgepole pine (Pinus contorta) was associated with snowshoe hare use within a mixed conifer context, and the only species to increase in abundance with horizontal cover was Engelmann spruce (Picea engelmannii) and subalpine fir (Abies lasiocarpa). Our landscape‐level modeling produced similar patterns in that we observed a positive effect of lodgepole pine and horizontal cover on both occupancy and use by snowshoe hares, but we also observed a positive yet parabolic effect of snow depth on snowshoe hare occupancy. This work is among the first to characterize the multiscale habitat relationships of snowshoe hares across a mixed conifer landscape as well as to map their occupancy and intensity of use. Moreover, our results provide stand‐ and landscape‐level insights that directly relate to management agencies, which aids in conservation efforts of snowshoe hares and their associated predators.     

Modeling the dynamics of woody plant–herbivore interactions with age-dependent toxicity

In this paper we study the effects that woody plant chemical defenses may have on interactions between boreal hares that in winter feed almost entirely on twigs. We focus particularly on the fact that toxin concentration often varies with the age of twig segments. The model incorporates the fact that the woody internodes of the youngest segments of the twigs of the deciduous angiosperm species that these hares prefer to eat are more defended by toxins than the woody internodes of the older segments that subtend and support the younger segments. Thus, the per capita daily intake of the biomass of the older segments of twigs by hares is much higher than their intake of the biomass of the younger segments of twigs. This age-dependent toxicity of twig segments is modeled using age-structured model equations which are reduced to a system of delay differential equations involving multiple delays in the woody plant-hare dynamics. A novel aspect of the modeling was that it had to account for mortality of non-consumed younger twig segment biomass when older twig biomass was bitten off and consumed. Basic mathematical properties of the model are established together with upper and lower bounds on the solutions. Necessary and sufficient conditions are found for the linear stability of the equilibrium in which the hare is extinct, and sufficient conditions are found for the global stability of this equilibrium. Numerical simulations confirmed the analytical results and demonstrated the existence of limit cycles over ranges of parameters reasonable for hares browsing on woody vegetation in boreal ecosystems. This showed that age dependence in plant chemical defenses has the capacity to cause hare-plant population cycles, a new result.     

Palatability of transgenic birch and aspen to roe deer and mountain hare

Genetic engineering of plant resistance characteristics against fungi may unintentionally influence traits that are important for plant–herbivore interactions. We studied the palatability of transgenic birch (Betula pendula), aspen (Populus tremula) and hybrid aspen (P. tremula x tremuloides) genetically modified with the aim to improve fungal disease resistance, to selective mammalian herbivores in cafeteria tests. Roe deer (Capreolus capreolus) were fed with transgenic birch carrying a sugar beet chitinase IV gene. In the experiment with roe deer, none of the six transgenic birch lines differed significantly from the wild-type control in the proportion of consumed plant biomass. Correlation analyses suggested that sugar content did not guide the feeding preferences of roe deer but revealed a positive correlation between starch content and proportion of mass consumed. However, the variation in starch content could not be related to the level of transgene expression. Mountain hares (Lepus timidus) were fed with plant material from chitinase transgenic birch and aspen and hybrid aspen that carried a pinosylvin synthase gene from Scots pine. One transgenic birch line was significantly less palatable to hares than the wild-type control. The results of this study suggest that plant genotype may be related to the palatability of plant material when transgenic and wild-type woody plant material is used as winter food for hares. The results of this case study did not reveal changes in the palatability of the studied transgenic lines that could be readily related to the functioning of the used transgenes.     

Interaction of growth retardants,daylength, and gibberellins A19, A20, and A1 on shoot elongation in birch and alder

Gibberellins A₁₉, A₂₀, and A₁ were applied to seedlings of birch (Betula pubescens Ehrh.) and alder (Alnus glutinosa (L.) Gaertn.) in order to test their ability to counteract growth inhibition induced by growth retardants (ancymidol and BX-112) or short day (SD, 12 h) photoperiod. Ancymidol inhibits early and BX-112 inhibits late steps in gibberellin biosynthesis. BX-112 inhibited stem elongation in both species while ancymidol, applied as a soil drench, was effective in alder only. Growth retardants affected stem elongation mainly by inhibiting elongation of internodes. All three gibberellins were equally active when applied to seedlings treated with ancymidol; however, only GA₁ was able to counteract the growth inhibition induced by BX-112. SD-induced cessation of elongation growth in birch was counteracted by GA₁, and to some degree, by GA₂₀, while GA₁₉ was inactive. SD treatment did not induce cessation of apical growth in alder. These results are consistent with the hypothesis that of gibberellins belonging to the early C-13 hydroxylation pathway, GA₁ is the only active gibberellin for stem elongation.