Factors related to the occurrence of hybrids between brown hares Lepus europaeus and mountain hares L. timidus in Sweden

Hybridization occurs among many species, and may have implications for conservation as well as for evolution. Interspecific gene flow between brown hares Lepus europaeus and mountain hares L. timidus has been documented in Sweden and in continental Europe, and has probably to some extent occurred throughout history in sympatric areas. What local factors or ecological relationships that correlate with or trigger hybridization between these species has however been unclear. We studied spatial distribution of hybrids between brown hares and mountain hares in Sweden in relation to characteristics of the sampled localities (hunting grounds). In a sample of 70 brown hares collected from 39 populations in south‐central Sweden during 2003–2005, 11 (16%) showed introgressed mtDNA from mountain hares. Among the brown hares from their northern range, i.e. in general the most recent establishments, the corresponding figure was 75% (9/12). The frequency of samples with hybrid ancestry increased significantly with latitude, altitude and hilliness, and were higher (p<0.1) in recently established populations and/or where the proportion of arable land was low. Several site‐specific parameters were correlated, e.g. latitude as expected to hilliness, and no parameter explained the occurrence of hybrids exclusively. Instead, the appearance of mountain hare mtDNA among brown hares was associated with a conglomerate of parameters reflecting landscapes atypical for the brown hare, e.g. forest dominated and steep areas where the species quite recently was established. We suggest that these abiotic factors mirror the main aspect influencing hybridization frequency, namely the density or relative frequency of the two species. In atypical brown hare landscapes with recent establishment, mountain hares are probably relatively more common. When one species dominate in numbers, or when both species display low densities, increased frequency of hybridization is expected due to low availability of conspecific partners, a phenomenon referred to as Hubbs’ principle.     

The recent expansion of the brown hare (<Emphasis Type="Italic">Lepus europaeus</Emphasis>) in Sweden with possible implications to the mountain hare (<Emphasis Type="Italic">L. timidus</Emphasis>)

The brown hare (Lepus europaeus) expanded its Swedish distribution since the 1980s northwards and locally to new areas within its former range. Of 115 brown hare populations within the former range reported in a hunter enquiry, those established after 1980 were situated higher above the sea level than older ones and higher than neighbouring (<50 km) older populations. Reports on increased use of forest habitats by brown hares were equally frequent among recent and older populations, suggesting a process promoted solely by less harsh winters. Supposed hare hybrids were more often reported from hunting grounds with recent brown hare establishment, i.e. where the species expands in time and in space. In a 27-year dataset on brown hare observations, the recent increased use of forest habitats was supported in that maximum distances to agricultural land for brown hare sightings were higher in mild winters, whereas the proportions of the annual observations made during winter were lower. In 40-year bag records from two Swedish counties, the dynamics of the mountain hare (Lepus timidus) responded positively to snow parameters, whereas brown hares responded negatively. We suggest that the state of mountain hare populations primarily depends on winter conditions and predation pressure, whereas possible effects of hybridization are unclear. If winter conditions remain as in the last 15 years, mountain hare numbers are not likely to increase in southern Sweden, whereas the brown hare may expand even further. In either case, hybrids will occur in sympatric areas in frequencies probably related to the density of the respective true species.     

Winter browsing of brown hares: evidence for diet breadth expansion

Foraging theory predicts that diet breadth should expand as food availability decreases. We tested this by looking at the winter browsing behaviour of the brown hare Lepus europaeus. We predicted selective feeding on different woody plant species, diet generalisation under increasingly severe winter conditions and a rank preference between the different food items. Following a period of severe winter conditions, we censused browsing marks of brown hares on woody plants at six sites situated at different altitudes (340 – 600 m a. s. l.) in Upper Franconia, Germany. We assumed that access to ground vegetation, which is the general diet of brown hares, was more restricted at sites with higher snow cover. The results provided support for all of our predictions: Feeding intensity varied strongly between the different plant species indicating selectivity of feeding. The number and also the percentage of browsed woody plant species was positively correlated with the altitude of the study site indicating a wider diet breadth in situations where less food was available. On the basis of a rank model on the food choice of brown hares, which was evaluated by an independent data set, we conclude that brown hares show a rank preference with regard to different groups of woody plant species. Our findings support the assumption that food restricted hares increasingly include unfavourable, low quality items into the diet.     

Spring and autumn habitat preferences of active European hares (Lepus europaeus) in an agricultural area with low hare density

The number of European brown hares (Lepus europaeus) has been declining throughout much of Europe since the 1960s. Consequently, many studies have focused on analysing habitat selection of European hares in order to improve the suitability of the habitat for this species. Habitat preferences of European hares are known to be affected by hare density, but most studies have been conducted in agricultural areas where hare densities were medium to high. Finding habitat preferences at high densities is difficult as most available habitats are occupied. In addition, in agricultural areas, field size might influence the hares’ habitat selection because it affects the distribution and availability of certain habitat types. However, most studies relate to areas with large field sizes. In this study, we analysed the habitat preferences of European hares in spring and autumn during the activity period, in the early hours of the night, in an agricultural area with low hare density and small average field size using Chesson’s electivity index. Moreover, we focused on the question whether two different habitat classifications varying in their specificity might cause contradictory results regarding European hares’ habitat preferences. Our results show that in this agricultural area with low hare density, European hares avoided several habitat types which were preferred in other study areas with higher hare densities. Therefore, we assume that hare density has an influence on the species’ habitat selection. In contrast, the small average field size of our study area seemed not to have an effect on hare habitat preference. Furthermore, by pooling habitat types into broader groups, substantial information was lost in some categories. Hence, for some categories, e.g. grassland or agricultural crop land, more detail might be needed than for others, such as urban areas, when analysing hares’ habitat selection. In conclusion, our results imply that studies on habitat preferences have to be conducted in areas with low hare density to be able to gain knowledge on the species’ habitat requirement and hereinafter improve the suitability of the habitat for this species.     

The distribution of mountain hares Lepus timidus in Europe: a challenge from brown hares L. europaeus?

1. Throughout the most recent glacial period (Weichsel), the mountain hare Lepus timidus had a continuous distribution in the tundra habitat south of the ice‐rim. When the ice retreated, mountain hares colonized deglaciated land, and spread over northern Europe. 2. Since the Weichsel, the mountain hare's distribution in Europe has been gradually reduced and at present comprises Ireland and the Scottish Highlands, high altitudes in the Alps, isolated forests in eastern Poland, most of Fennoscandia and from the Baltic countries eastwards through Russia. Declines during the last century have been observed in Sweden and Russia. 3. This review defines and evaluates causes for this gradual reduction and fragmentation of the mountain hare's distribution, with special focus on interactions with brown hares Lepus europaeus. The relative importance of diseases, predation, cultivation and interactions with other herbivores than brown hares are discussed. 4. A plausible cause of the possible permanent disappearance of mountain hares in Europe appears to be exclusion by interspecific competition and hybridization with, and/or epidemic diseases mediated by, the congeneric brown hare.     

The occurrence of mountain hare mitochondrial DNA in wild brown hares

If interspecific hybrids are fertile and backcross to either parental species, transmission of mitochondrial DNA over the species barrier can occur. To investigate if such transmission has occurred between the brown hare Lepus europeus Pall and the mountain hare L. timidus L. in Scandinavia, an analysis of genetic variation in mitochondrial DNA from 36 hares, collected from 15 localities, was performed. Sequence divergence of mtDNA between species was estimated at 8 ± 1% (SD). Intraspecific mtDNA sequence divergence varied between 0.09 and 0.38% in brown hares and 0.10 and 1.44% in mountain hares. In six out of 18 brown hares examined, two different haplotypes of mountain hare origin were detected, demonstrating a transmission of mtDNA haplotypes from mountain hares to brown hares. The results indicate that interspecific hybridization between the two species occurs in wild populations.     

Food competition between a large ruminant and a small hindgut fermentor: the case of the roe deer and mountain hare

In this study, we demonstrate that the mountain hare and roe deer compete with each other. This was determined using "natural experiments" of populations found in sympatry and allopatry on the islands along the west coast of Norway. We demonstrate that both species occupy the same habitats, share the same food resources and that food availability is limited. Two browsing species as different in size as roe deer and mountain hare might be expected to partition the available vegetation (e.g. woody scrub) in terms of height above ground level. However, from the evidence collected, the feeding-height-separation hypothesis must be rejected as an explanation for ecological separation between roe deer and mountain hares because there was extensive height overlap in resource utilisation by both species and neither species changed its feeding height in response to the presence of the other. Total browse utilisation did not increase when both species were together; rather, species-specific browse utilisation declined when the other species was present. However, the foraging behaviour of each herbivore varied significantly between the allopatric and sympatric sites. When both herbivores were present, the clip diameter of shoots browsed by mountain hares declined to match those selected by roe deer, while roe deer switched from a browse-dominated diet to a diet dominated by winter-green gramineae. The change to smaller-diameter shoots likely resulted in the hare increasing its intake of digestion-inhibiting or toxic secondary metabolites, while the alternative choice of digging through the snow like roe deer to reach the winter-green gramineae is a practice considered energetically too costly for hares. On this basis, we conclude that the enforced switch to a nutritionally inferior diet by mountain hares at the sympatric sites may result in changes to growth rate and body size which consequently impact on mortality and may explain the competitive superiority of the roe deer.     

Unstable dynamics and population limitation in mountain hares

The regular large-scale population fluctuations that characterize many species of northern vertebrates have fascinated ecologists since the time of Charles Elton. There is still, however, no clear consensus on what drives these fluctuations. Throughout their circumpolar distribution, mountain hares Lepus timidus show regular and at times dramatic changes in density. There are distinct differences in the nature, amplitude and periodicity of these fluctuations between regions and the reasons for these population fluctuations and the geographic differences remain largely unknown. In this review we synthesize knowledge on the factors that limit or regulate mountain hare populations across their range in an attempt to identify the drivers of unstable dynamics. Current knowledge of mountain hare population dynamics indicates that trophic interactions--either predator-prey or host-parasite--appear to be the major factor limiting populations and these interactions may contribute to the observed unstable dynamics. There is correlative and experimental evidence that some mountain hare populations in Fennoscandia are limited by predation and that predation may link hare and grouse cycles to microtine cycles. Predation is unlikely to be important in mountain hare populations in Scotland as most hares occur on sporting estates where predators are controlled, but this hypothesis remains to be experimentally tested. There is, however, emerging experimental evidence that some Scottish mountain hare populations are limited by parasites and that host-parasite interactions contribute to unstable dynamics. By contrast, there is little evidence from Fennoscandia that parasitism is of any importance to mountain hare population dynamics, although disease may cause periodic declines. Although severe weather and food limitation may interact to cause periodic high winter mortality there is little evidence that food availability limits mountain hare populations. There is a paucity of information concerning the factors limiting or regulating mountain hare populations in the Alps of Central Europe or in the tundra and taiga belts of Russia. Future research on mountain hare population dynamics should focus on the interactions between predation, parasitism and nutrition with stochastic factors such as climate and anthropogenic management including harvesting.     

Effects of roads on spatial distribution,abundance and mortality of brown hare (<Emphasis Type="Italic">Lepus europaeus</Emphasis>) in Switzerland

Brown hare populations (Lepus europaeus) are in decline throughout Europe since the 1960s, and numerous impact factors have been discussed in the literature. Although landscape fragmentation by roads is assumed to be one potential factor, the effects of roads on brown hare populations are poorly understood. We studied three potential effects of roads on brown hares asking: (1) Do roads affect the spatial distribution of hares due to disturbance effects? (2) Does road network density affect hare abundance due to barrier effects? (3) Does road network density affect road mortality rates in hare populations? The study is based on harvest statistics and spotlight taxations in Canton Aargau, Switzerland and was conducted at three different spatial scales. Spatial distribution was studied in plots established in varying distances parallel to roads, effects on abundance were analysed on the basis of raster grids, and road mortality was studied on the level of hunting districts. We show that (1) hares avoid the proximity to roads and prefer large non-fragmented areas over small isolated patches. (2) The density of freeways, federal and main roads has a negative effect on hare abundance. The density of unpaved field tracks has a positive effect probably because vegetation at field tracks contributes to the diet spectrum. (3) Effects of road network density on road mortality rates could not be shown, although road mortality has increased since the 1990s. We conclude that in debilitated populations, roads act as threatening factor for brown hare. We recommend establishing large un-dissected areas as a new category of wildlife refuge and to protect these areas from being further fragmented.     

European brown hare syndrome in free-ranging European brown and mountain hares from Switzerland.

From 1997 to 2000, complete necropsy and histopathologic investigations were performed on 157 free-ranging European brown hares (Lepus europaeus) found dead throughout Switzerland. Organ samples of all these individuals (157 livers and 107 spleens available) were tested for European brown hare syndrome virus (EBHSV)-antigen by enzyme-linked immunosorbent assay (ELISA) test kit. Furthermore, 60 additional blood samples were tested for antibodies against EBHSV by ELISA. In addition, liver samples of 87 free-ranging mountain hares (Lepus timidus) hunted in 1996 were tested for EBHSV-antigen. In two European brown hares from southern Switzerland lesions suggestive of changes induced by EBHSV were present, and high titers of EBHSV-antigen were detected in both liver and spleen samples of these animals. Based on negative staining electron microscopy investigations of liver and spleen homogenates, we observed calicivirus in one antigen-positive hare. Low EBHSV-antigen titers were found in three additional European brown hares from central and western Switzerland, but EBHS-lesions were absent. Antibodies against EBHSV were not detected in any of the sera of European brown hares, and EBHSV-antigen was not found in the samples of mountain hares. This is the first report of EBHS in European brown hares from Switzerland.     

Diet of the brown hare (Lepus europaeus) and food availability in northern Patagonia (Mendoza, Argentina)

The brown hare, a Leporid widespread in the world, is now dispersed across Argentina after its introduction at the end of the 19th century. Studies on hare feeding ecology are important to evaluate a potential competition with domestic and native wild herbivores. This study analyses the brown hare diet in relation to food availability, and dietary overlaps with several herbivores in northern Patagonia. Food availability was estimated by point-quadrat transects, and hare diet by microhistological analysis of faeces, carried out in five habitats in five seasonal samplings. Significant differences were detected by Kruskall–Wallis ANOVA with multiple comparisons by Tukey test. Feeding selection was detected by χ² test, and dietary preferences by the confidence interval of Bailey. Grasses and chamaephytes were the most available plant categories, with Stipa, Panicum and Acantholippia as main species. Grasses and phanerophytes were the main dietary categories, including Poa, Panicum, Bromus, Adesmia and Prosopidastrum. The phanerophytes Prosopidastrum and Ephedra were more eaten in winter, when the main food item (Poa) presented lower availability. A higher dietary proportion of the chamaephyte Acantholippia occurred in rocky habitats, where the coarse dominant grasses were always avoided. Hares shared most food items with several wild and domestic herbivores in northern Patagonia. The lack of preference for forbs differentiates brown hares from other herbivores. However, hares exhibited important dietary similarities with plain and mountain vizcachas, goats and horses, and an interspecific competition for food is highly probable.     

Winter diet, habitat selection and fluctuation of a mountain hare Lepus timidus population in Finnish Forest Lapland

Composition of the winter diet, habitat selection and population fluctuations in the mountain hare Lepus timidus were studied in the Värriötunturi fell area, Eastern Finnish Forest Lapland, during the winters 1968/69–1984/85. The three population lows recorded during this 17-year period followed each other at intervals of 4 and 8 years. During the lows the hares occurred only in the most favoured (forest-covered) habitats and in two of them they behaved according to the concept of the refuge theory. The mountain birch Betula pubescens ssp. tortuosa appeared to be the most important, but not the most favoured winter food item. When the population crashed, the proportion of birch in the diet decreased, and was replaced especially by juniper which is one of the secondary food items (and is for this reason often discarded although cut). It is suggested that the quality and/or quantity of the winter food (i.e. winter pastures) are one of the driving forces in the population fluctuation of the mountain hare in this area.     

Bioenergy crops and farmland biodiversity: benefits and limitations are scale-dependant for a declining mammal,the brown hare

Biomass energy crops are prompting major land-use changes in agricultural and marginal land in an effort to reduce dependency on fossil fuels. Miscanthus × giganteus, a perennial giant grass, is one of the main such crops in Europe but few studies exist of its interaction with farmland wildlife, particularly mammals. Understanding ecological impacts of bioenergy planting schemes is vital for mitigating potential negative effects on already declining farmland biodiversity and for maximising any benefits from these low-management, structurally diverse crops. We assessed in a mixed farming area in the UK the impact of Miscanthus crops on the brown hare (Lepus europaeus), a widespread but declining farmland species of conservation concern. We intensively radio-tracked hares in Miscanthus blocks of contrasting size and analysed hare diet for evidence of the consumption of Miscanthus. Home ranges differed starkly averaging 10.5 versus 49.6 ha in the small and the large Miscanthus blocks, respectively. Despite entirely avoiding the crop as food, hares appeared able to exist and even thrive in areas planted with Miscanthus though their populations may be significantly limited by reduced food availability and increased energy use where dense Miscanthus is planted over a wide area. As a component of a mixed farming landscape, Miscanthus may provide biodiversity benefits by increasing spatial heterogeneity and refuge areas for declining farmland species like brown hares but any effect is likely to be strongly scale-dependant.     

Long-term changes in the feeding pattern of red foxes Vulpes vulpes and their predation on brown hares Lepus europaeus in western Poland

The aim of this study was to estimate long-term changes in the winter feeding pattern of red foxes Vulpes vulpes and in their predation on brown hares Lepus europaeus in relation to the decreasing abundance of hares in western Poland in 1965/1966–2006/2007. The frequencies of occurrence in the stomachs of culled foxes (N?=?726) were used as indices of prey capture rates. The average autumn density of brown hares in the study area decreased from 48 individuals/km² at the turn of the 1960s and 1970s to seven individuals/km² in 1999–2006. Hares and small rodents were the main food classes of foxes in western Poland at the turn of the 1960s and 1970s; however, the occurrence of hares in the fox diet subsequently decreased, and they were replaced by livestock carrion. The relationship between the occurrence frequency of hares in the fox diet and the hare density was best described by sigmoid equation. It indicates that the red fox showed a type III functional response to long-term changes in hare abundance. When predation rate index was estimated on the basis of functional response, the potential fox predation was density-dependent at low to intermediate hare densities (<25 individuals/km²). This finding suggests that the increase in the number of low-density hare populations may require intensive management measures, e.g. simultaneous use of fox control and habitat improvement.     

The consequences of predator control for brown hares (<Emphasis Type="Italic">Lepus europaeus</Emphasis>) on UK farmland

The brown hare Lepus europaeus is a valued game species but also a species of conservation concern owing to its severe decline in abundance on farmland throughout Europe during the twentieth century. Changes in the farmland habitat and predation have both been cited as causative factors. Their relative roles have been unclear, but most conservation action has focused on improving habitat. We analyse data from a sequence of three unique studies (one experiment and two demonstrations) covering the period 1985–2006 in which control of several common predator species was undertaken to increase densities of wild game on farmland in England. Across the three studies, regression modelling of the proportional change in hare numbers between successive years showed that—after site, year differences and harvesting were accounted for—predator control was a significant determinant of hare population change. Where habitat improvement also took place, hares reached autumn densities that were exceptional for the UK and which could sustain substantial harvests. When predation control was stopped, hare densities fell, even where habitat improvements remained in place. This analysis demonstrates that even where farmland habitat is greatly improved, uncontrolled predation prevents hares making full use of its carrying capacity. This helps explain the mixed—and at best modest—success of agri-environment schemes in the UK and elsewhere in Europe to increase hare densities. Game-shooting estates, on which effective predator control takes place, probably have a special significance within the landscape as source areas for brown hares.     

High mtDNA haplotype diversity among introduced Swedish brown haresLepus europaeus

The brown hareLepus europaeus Pallas, 1778 occurs naturally in central Eurasia, but has been introduced to parts of northern Europe, South- and North America, Australia and New Zealand. Brown hares were introduced to Sweden from central Europe for hunting purposes during the 19th century. We investigated how the human--mediated brown hare colonisation of Sweden is reflected in the amount of genetic variation present by assessing variation and composition of mitochondrial DNA (mtDNA) lineages among Swedish brown hares. MtDNA from a total of 40 brown hare specimens from 15 localities were analysed for Restriction Fragment Length Polymorphisms. The haplotype diversity is surprisingly high (0.893 ± 0.002) when compared to the mtDNA diversity among brown hares on the European continent as well as to other mammalian species. Admixture of haplotypes from different source populations combined with a reduced effect of random genetic drift and a relaxed selection pressure due to rapid population growth after introduction are mechanisms that are likely to account for the observed high mtDNA haplotype diversity.     

Temporal dynamics of European brown hare syndrome infection in Northern Italian brown hares (Lepus europaeus)

The progressive decline in the hare population across Europe has been associated with the occurrence of European brown hare syndrome (EBHS), a highly contagious disease considered endemic in all European countries. This study aimed to evaluate the in-field temporal dynamics of European brown hare syndrome virus (EBHSV) infection in wild European brown hares (Lepus europaeus) and to test the influence of population density on EBHS seroprevalence. A total of 512 blood samples were collected from free ranging hares captured for restocking in seven different areas of the province of Brescia (Northern Italy) during seven consecutive years (2006–2013) and tested using a competitive ELISA. A generalized linear mixed model estimated the yearly effects of population density on EBHS prevalence. Of the 512 tested, 344 (67.2 %) tested positive for EBHSV antibodies, with the annual seroprevalence ranging from 94.3 to 35.8 %. The prevalence was 3.303 times higher in areas with a density of over 15 hares/km² and declined over the years. The results indicate the ongoing transmission of the virus in the tested brown hare population. Since the eradication of EBHS in a wild population is not feasible, a strategy aimed at promoting the endemic stability of the virus through density-dependent mechanisms could be applied; however, this seems more difficult in practice than in theory and would most likely require a very high density of brown hares.     

Detectability counts when assessing populations for biodiversity targets

Efficient, practical and accurate estimates of population parameters are a necessary basis for effective conservation action to meet biodiversity targets. The brown hare is representative of many European farmland species: historically widespread and abundant but having undergone rapid declines as a result of agricultural intensification. As a priority species in the UK Biodiversity Action Plan, it has national targets for population increase that are part of wider national environmental indicators. Previous research has indicated that brown hare declines have been greatest in pastural landscapes and that gains might be made by focussing conservation effort there. We therefore used hares in pastural landscapes to examine how basic changes in survey methodology can affect the precision of population density estimates and related these to national targets for biodiversity conservation in the UK. Line transects for hares carried out at night resulted in higher numbers of detections, had better-fitting detection functions and provided more robust density estimates with lower effort than those during the day, due primarily to the increased probability of detection of hares at night and the nature of hare responses to the observer. Hare spring densities varied widely within a single region, with a pooled mean of 20.6 hares km(-2), significantly higher than the reported national average of hares in pastures of 3.3 hares km(-2). The high number of encounters allowed us to resolve hare densities at site, season and year scales. We demonstrate how survey conduct can impact on data quantity and quality with implications for setting and monitoring biodiversity targets. Our case study of the brown hare provides evidence that for wildlife species with low detectability, large scale volunteer-based monitoring programmes, either species specific or generalist, might be more successfully and efficiently carried out by a small number of trained personnel able to employ methods that maximise detectability.