Role of predation in short-term population fluctuations of some birds and mammals in Fennoscandia

Summary We tested the hypothesis that synchronous fluctuations in small game species in boreal Fennoscandia are caused by varying predation pressure. The main prey of predators are the cyclically superabundant voles. Small game species (alternative prey) are rare compared to voles. The following 4 predictions were checked: (1) Predators should shift their diet from main prey to alternative prey as main prey decline. — This was confirmed using data on red fox (Vulpes vulpes L.) diet.; (2) The mortality rate of alternative prey should be inversely correlated to the abundance of main prey. — This was true for mountain hare (Lepus timidus L.) mortality rates and the rate of nest predation on black grouse (Tetrao tetrix L.).; (3) The total consumption of prey by all the predators should at least equal the critical losses in alternative prey during a decline year. — A tentative estimate of predator consumption amounted to 10 times the losses in grouse and hare.; and (4) The absence of synchrony between the species in the boreonemoral region should be associated with a more diverse diet of predators. — This was the case for red fox diets throughout Sweden. Although all 4 predictions were confirmed, we could not necessarily exclude other hypotheses involving changes in quality or quantity of plant food.     

Synchronous short-term population fluctuations of some birds and mammals in Fennoscandia - occurrence and distribution

We examined population fluctuations of the voles Microtus agrestis L. and Clethrionomys glareolus Schreb. by biannual trapping; black grouse Tetrao tetrix L., mountain hare Lepus timidus L., and red fox Vulpes vulpes L. by using bag records from all over Sweden, questionnaires from south-central Sweden, and population indices from Grimsö Wildlife Research Area in south-central Sweden. Synchronous population fluctuations between voles as a group and the other species conformed to a 3–4 year periodic pattern in both autumn and spring populations only in northern and central Sweden (the boreal forest region). Spring populations of boreal forest grouse, hare, and probably also fox, lagged one year behind the voles. The northerly areas also formed geographical units of co-fluctuation within each game species. Using our own data as well as reviewing previous studies in Fennoscandia, we conclude that synchronized 3–4 year population fluctuations of voles and medium-sized herbivores are confined to the central and northern part of Fennoscandia, although voles may exhibit short-term population fluctuations further south. The synchronizing link between the herbivores could be (1) food plant quality and/or quantity and/or (2) predation. We could not reject either of these two plausible mechanisms as a cause of interspecifically synchronous fluctuations.     

Vulnerability of black grouse hens to goshawk predation: result of food supply or predation facilitation?

The plant cycle hypothesis says that poor-quality food affects both herbivorous voles (Microtinae spp.) and grouse (Tetraonidae spp.) in vole decline years, leading to increased foraging effort in female grouse and thus a higher risk of predation by the goshawk Accipiter gentilis. Poor-quality food (mainly the bilberry Vaccinium myrtillus) for these herbivores is induced by seed masting failure in the previous year, when the bilberry is able to allocate resources for chemical defence (the mast depression hypothesis; MDH). The predation facilitation hypothesis (PFH) in turn states that increased searching activity of vole-eating predators during or after the decline year of voles disturbs incubating and brooding grouse females. The behaviours used by grouse to avoid these terrestrial predators make them more vulnerable to predation by goshawks. We tested the main predictions of the MDH and PFH by collecting long-term (21-year) data from black grouse Tetrao tetrix hens and cocks killed by breeding goshawks supplemented with indices of bilberry crop, vole abundance and small carnivores in the vicinity of Oulu, northern Finland. We did not find obvious support for the prediction of the MDH that there is a negative correlation of bilberry crop in year t with vole abundance and with predation index of black grouse hens in year t + 1. We did find obvious support for the prediction of the PFH that there is a positive correlation between predator abundance and predation index of grouse hens, because the stoat Mustela erminea abundance index was positively related to the predation index of black grouse hens. We suggest that changes in vulnerability of grouse hens may mainly be caused by the guild of vole-eating predators, who shift to alternative prey in the decline phase of the vole cycle, and thus chase grouse hens and chicks to the talons of goshawks and other avian predators.     

Variation in the diet composition of a generalist predator, the red fox, in relation to season and density of main prey

Diet composition of a generalist predator, the red fox (Vulpes vulpes) in relation to season (winter or summer) and abundance of multi-annually cyclic voles was studied in western Finland from 1983 to 1995. The proportion of scats (PS; a total of 58 scats) including each food category was calculated for each prey group. Microtus voles (the field vole M. agrestis and the sibling vole M. rossiaemeridionalis) were the main prey group of foxes (PS = 0.55) and they frequently occurred in the scats both in the winter and summer (PSs 0.50 and 0.62, respectively). There was a positive correlation between the PSs of Microtus voles in the winter diet of foxes and the density indices of these voles in the previous autumn. Other microtine rodents (the bank vole Clethrionomys glareolus, the water vole Arvicola terrestris and the muskrat Ondatra zibethicus) were consumed more in winter than in summer. The unusually high small mustelid predation by red foxes (PS = approx. 0.10) in our study area gives qualitative support for the hypothesis on the limiting impact of mammalian predators on least weasel and stoat populations. None of the important prey groups was preyed upon more at low than at high densities of main prey (Microtus voles). This is consistent with the notion that red foxes are generalist predators that tend to opportunistically subsist on many prey groups. Among these prey groups, particularly hares and birds (including grouse), were frequently used as food by foxes.     

Mountain hare populations on islands: effects of predation by red fox

Summary On islands off the west coast of Sweden the density of mountain hares (Lepus timidus L.) is very high. One of the main predators on hares, the red fox (Vulpes vulpes L.), is only present during short periods. Data on hare density and predation by red fox and eagle owl (Bubo bubo (L.)) has been analyzed from five islands over several years. Winter mortality in years with low predation pressure was independent of hare density. But when red fox or eagle owl were present on islands (i.e., high predation pressure) winter mortality became density dependent. Thus, at low density, winter mortality did not increase through red fox predation. But at densities up to two hares/ha, predation pressure was increasing and could be limiting for these populations. At still higher hare density predation pressure became less intensive. The functional response for foxes preying on hares showed a type II or a sigmoid type III response pattern. In normal summers, the population increase due to reproduction was at least two-fold. When a fox was present there was instead a sharp decrease in hare numbers. Fox predation had a stronger effect in summer than in winter. By switching between islands and mainland areas from winter to summer, a fox can stabilize fluctuations in hare numbers on the islands. This is dependent on how often the ice permits a fox to reach an island and the lack of numerical response by predators.     

Snow tracking reveals different foraging patterns of red foxes and pine martens

Red fox (Vulpes vulpes) shares similar prey preferences and co-occurs with several other carnivores, and is together with pine marten (Martes martes), the most common mesocarnivore in the northern boreal forest. Voles are important prey for both species, but it is unclear to what extent they compete for the same food resources in winter. Here, we use 2139 km and 533 km of meticulous snow tracking of red foxes and pine martens to evaluate their food niches. We measured hunting and digging behaviour, whether successful or not, and the effect of snow depth and temperature. Pine martens were restricted to forested habitats, whereas red foxes used a wide range of habitats. Red foxes were found to dig more often than pine martens, 0.67 vs. 0.39 digging events per kilometre. Hunting was less common and similar in both species, about 0.1 hunting event per kilometre. Pine martens were more efficient in hunting and finding food remains compared to red foxes. Increasing snow depth reduced hunting success and also reduced dig success of red foxes. Food niche overlap was small. Red foxes used mostly voles and carrion remains of ungulates, whereas pine martens used cached eggs and small birds. We suggest that caching eggs is an important strategy for pine martens to survive winter in northern latitudes. Snow depth was important for capturing voles, and thick snow cover appeared to mask the effect of vole peaks. Intensified land use, as clear-cutting and leaving slaughter remains from harvest, will benefit red foxes on the expense of pine martens. The ongoing climate change with warmer winters and less snow will likely further benefit the red fox.     

Vole fluctuations,red fox responses,predation on fawns,and roe deer dynamics in a temperate latitude

The alternative prey hypothesis predicts that predators respond both functionally and numerically (with a time lag) to fluctuations in the main prey abundance, which affects the survival of alternative prey. This pattern was found in northern Europe in the community formed by voles (Microtidae), red foxes (Vulpes vulpes) and roe deer (Capreolus capreolus). We studied the same predator—prey community in a temperate latitude where, according to the predation hypothesis, only the functional response of predators to changes in main prey availability should occur. In the years 1997–2007, in western Poland, we estimated the index of common vole (Microtus arvalis) abundance (burrow counts), the density of foxes (spotlight counts), the young production in foxes (young/adult ratio), the index of fox predation on fawns (prey remains near dens) as well as the reproduction index (fawn/female ratio) and density of roe deer (total counts). The vole abundance fluctuated considerably, the young production in foxes did not correlate with the main prey availability, but the density of foxes showed direct numerical response. The index of fox predation on fawns decreased with the vole abundance and negatively affected the fawn/female ratio in roe deer. Thus, the relationships between voles and foxes were not fully consistent with the predation hypothesis. The direct numerical response of foxes should tend to stabilize this predator—prey community. It is suggested, however, that responses showed by vole-eating predators in temperate latitudes may sometimes affect their alternative prey, including animals with unfavourable conservation status.     

Fox predation on cyclic field vole populations in Britain

The diet of the red fox Vulpes vulpes L. was studied during three winter periods in spruce pklantations in Britain, during which time the cyclic field vole Microtus agrestis L. populations varied in abundance. Field voles and roe deer Capreolus capreolus L. were the two main prey species in the diet of the red fox. The contribution of lagomorphs to fox diet never exceeded 35% and species of small mammal other than field voles were of minor importance. The contribution of field voles was dependent on vole density. The non-linear density dependent relationship with a rather abrupt increase of field voles in fox did when vole density exceeded ca 100 voles ha⁻¹ was consistent with a prey-switching response. The contribution of field voles to fox diet during the low phase of population cycles was lower in Kielder Forest than in other ecosystems with cyclic vole populations. The number of foxes killed annually by forestry rangers was consistent with the evidence from other studies that foxes preying on cyclic small rodents might show a delayed numerical response to changes in vole abundance. Estimates of the maximum predation rate of the fox alone (200–290 voles ha⁻¹ of vole habitat year⁻¹) was well above a previously predicted value for the whole generalist predator community in Kielder Forest. Our data on the functional response of red foxes and estimates of their predation rates suggest that foxes should have a strong stabilising impact on vole populations, yet voles show characteristic 3-4 yr cycles.     

Contrasting phenotypic correlations in food provision of male Tengmalm's owls (Aegolius funereus) in a temporally heterogenous environment

Summary We examined the food provision rate of male Tengmalm's owls,Aegolius funereus, during one 3 year vole cycle consisting of consecutive low, increase and peake vole years. The data were collected in the midnestling period when males provisioned the whole family. In the low vole year, males with a low loading index (g/cm²) of flying area fed their offspring more often than did males with a high loading index, whereas in the peak vole year the opposite trend was evident. Similar relationships were found in the food mass provisioned to the nest. In the increase vole year, male body size had no effect on feeding efficiency. In the peak vole year, when large voles are abundant, heavy males preyed on larger voles than were generally available in their territories, indicating that largeness may increase strike power in hunting attempts. In the low vole year, when breeding is costly due to food scarcity and extensive hunting area, small males are more economical fliers and efficient hunters than large males. The contrasting trends in correlations between male size and feeding efficiency in years of vole abundance versus scarcity suggest that no fixed phenotype may most efficiently cope with variable food supply.     

Effect of felling on red fox (Vulpes vulpes) and pine marten (Martes martes) diets in transitional mixed forest in Belarus

In transitional mixed forests in northern and central Belarus the influence of intensified felling on the diets of red foxes Vulpes vulpes L. and pine martens Martes martes L. was investigated in two model forested terrains with sandy and clay top-grounds. A total of 1904 scats of red foxes and 1624 scats of pine martens were analysed over two periods differed by logging rate. When logging rate was conservative, red fox and pine marten diets were found to be similar, but under heavy logging feeding of the predator species shifted. In both model woodlands we found the same pronounced dietary trend of higher consumption of rodents, first of all, Microtus voles. The dietary changes were well related to the registered increase in Microtus vole numbers and total number of rodents in felling areas. The increased preying on rodents caused lower consumption of other food items, particularly medium-sized mammals (year-round) or/and birds or/and fruits (in the warm season) or/and mammalian carrion (in the cold season). In the conditions of intensified felling the food niches of the red fox and pine marten diverged mostly because of the great difference in the species structure of rodents consumed. Red foxes turned to preying on Microtus voles more frequently, but less on bank voles Myodes glareolus; while pine martens increased their taking of Microtus voles, continued foraging for bank voles and began taking slightly more of Apodemus mice. Before heavy logging dietary similarity between the red fox and pine marten was high and did not vary considerably through seasons and study areas, whereas after felling was intensified their diet overlap became lower.     

The role of vole populations in prevalence of the parasite (Echinococcus multilocularis) in foxes

Effects of population fluctuation of the gray-sided vole(Clethrionomys rufocanus) on the prevalence (infection rates) of the parasiteEchinococcus multilocularis in red fox(Vulpes vulpes) populations was investigated from 1985 to 1992 in eastern Hokkaido (Abashiri, Nemuro, and Kushiro area), Japan. This parasite needs two hosts to complete its life cycle; the gray-sided vole as its intermediate host and the red fox as its final host. We found that: (1) Infection rates in foxes depended on the current-year abundance of voles in all three study areas, particularly in Abashiri. (2) In addition to this direct density-dependence, delayed density-dependence between the infection rate and the prior-year abundance of voles was detected in Nemuro and in Kushiro. (3) The regional differences in density-dependence pattern were related to regional differences in the winter food habits of red foxes: in Abashiri the proportion of voles in the fox’s diet greatly decreases in winter, while the proportion remains high in winter in Nemuro and in Kushiro, probably because of shallower snowpack. These results suggest that infection rates in foxes in Abashiri were less influenced by the prior-year prevalence, since the infection cycle might be interrupted in winter, when voles became less important in fox’s diet. In contrast, the state of the prevalence may carry over from year to year in Nemuro and in Kushiro, because red foxes continue to eat a considerable amount of voles throughout year. The regionally contrasted results for the relationship between infection rate in foxes and vole abundance were parallel to the regional difference in fluctuation pattern of vole populations, which are highly variable in Abashiri area, but less variable in Kushiro-Nemuro area. Drastic change in vole populations appears to affect the host-parasite system.     

Synchronous and nonsynchronous population fluctuations of some predators and their prey in central Sweden

To test the alternative prey hypothesis (APH), we examined 29-yr time series of bank voles (indexed by snap-trapping) and 6 game species (indexed by bag records) from Gavleborg county, central Sweden, for the occurrence of synchronous population fluctuations Only voles and the 3 grouse species exhibited cyclic fluctuations, grouse fluctuations were highly synchronous, and positively correlated with vole fluctuations Although hares were positively correlated with grouse, they were negatively correlated with voles Fox were positively correlated with voles and grouse, however, a strong negative relationship was observed between fox and hares During a sharp decline in fox numbers during the early 1980's due to sarcoptic mange, both grouse and hares exhibited a strong positive numerical response, but, not in synchrony In addition, grouse exhibited large fluctuations during the fox decrease whereas hares did not Due to the contradictory predator-prey interactions observed, these results provide only partial support for APH     

Hare and vole browsing preferences during winter

The aim with this study was to, under controlled conditions, determine the food preference of mountain haresLepus timidus Linnaeus, 1758 and bank volesClethrionomys glareolus (Schreber, 1780) for a substantial part of the woody plants potentially available for these herbivores during winter. In addition, we compared hare and vole preference patterns. Thirteen woody plant species were simultaneously presented to 9 captive voles and 9 captive hares in preference tests during winter. Consumption by hares from 50 g bundles (one per species) was measured after 3 h, whereas shoot consumption by voles was measured after 12 h. Both hares and voles preferred deciduous species to conifers,Populus tremula, andVaccinium myrtillus being the most preferred species. However, there was considerable variation in palatability among deciduous plant species and only a marginally significant correlation was found between hare and vole preference. One striking differences between hares and voles was that Sorbusaucuparia was the most utilised by voles but the least preferred by hares. In conclusion, deciduous plant species were generally considerably more palatable to hares and voles than conifers, which is consistent with current theories. Nevertheless, the high variation in palatability among deciduous trees and the difference in preference between hares and voles indicate more complex and species-specific patterns with regard to plant— animal interactions. The latter also suggests that hares and voles differ in their dietary adaptations and have different dietary constrains.     

Effect of fox hunting with small hound packs on spatial behaviour of brown hares

Control of red fox Vulpes vulpes populations is a fundamental game management tool used by hunters interested in increasing prey populations. In Italy, a popular method to control fox populations is hunting with small hound packs. The effects of this hunting technique on non-target species such as the brown hare Lepus europaeus, are unknown. In this study, we analysed for the first time the effects of fox hunting with hound packs on brown hares tagged with VHF collars. Our results showed that hunting with four trained hounds did not significantly modify the spatial behaviour of the brown hare.     

Experimental evidence that livestock grazing intensity affects the activity of a generalist predator

Grazing by domestic ungulates has substantial impacts on ecosystem structure and composition. In grasslands of the northern hemisphere, livestock grazing limits populations of small mammals, which are a main food source for a variety of vertebrate predators. However, no experimental studies have described the impact of livestock grazing on vertebrate predators. We experimentally manipulated sheep and cattle grazing intensity in the Scottish uplands to test its impact on a relatively abundant small mammal, the field vole (Microtus agrestis), and its archetypal generalist predator, the red fox (Vulpes vulpes). We demonstrate that ungulate grazing had a strong consistent negative impact on both vole densities and indices of fox activity. Ungulate grazing did not substantially affect the relationship between fox activity and vole densities. However, the data suggested that, as grazing intensity increased i) fox activity indices tended to be higher when vole densities were low, and ii) the relationship between fox activity and vole density was weaker. All these patterns are surprising given the relative small scale of our experiment compared to large red fox territories in upland habitats of Britain, and suggest that domestic grazing intensity causes a strong response in the activity of generalist predators important for their conservation in grassland ecosystems.     

Long-term data on invaders: when the fox is away, the mink will play

Studies of the effects and population dynamics of invasive species typically cover only short time periods. However, populations of invasive species interact with native species, and these interactions may have strong effects on invaders’ populations and effects over time. We present and analyze long-term data on invasive American mink (Neovison vison), native red fox (Vulpes vulpes), and mountain hare (Lepus timidus) in Sweden. The mink’s population dynamics followed a pattern of logistic growth from the late 1930s to the late 1970s. In the early 1980s, however, the population tripled, then declined sharply. We suggest that the mink’s population tripling was caused by a drastic decline in red fox populations, which caused terrestrial prey to increase. Later recovery of the fox population reversed the trend and caused the mink population’s recent decline. Our study shows that species interactions between native and invasive species, and therefore biotic resistance, can change dramatically over time.     

Environmental,parental and adaptive variation in egg size of Tengmalm's owls under fluctuating food conditions

We studied egg size variation of Tengmalm's owls in western Finland during 1981–1990. The owls fed on voles whose population fluctuated in a predictable manner: low (1981, 1984, 1987, 1990), increase (1982, 1985, 1988) and peak (1983, 1986, 1986) phases of the cycle occurred every third year. Eggs were largest in the increase phase of the vole cycle, even though that voles were more abundant and egg-laying started earlier in the peak phase than in the increase phase. This suggests that owls invest mostly in egg size when vole abundance increases along with survival chances of offspring. Territory quality and female age had no effects on egg size, but egg size decreased with laying data in the increase phase of the vole cycle. Egg size was significantly positively related to the male age in the increase phase, but the opposite relationship was significant in the peak phase of the vole cycle. The partners of adult males also decreased their egg volume from the increase to the peak phase, whereas the partners of yearling males produced their largest eggs in the peak phase of the vole cycle. This suggests the importance of experience in prevailing food fluctuations. Possibly male Tengmalm's owls can adjust the intensity of courtship feeding not only in relation to the food abundance on their territories at the time of egg laying, but also to the survival prospects of their offspring. Phenotypic plasticity seems to play a substantial role, as the egg size repeatabilities of individual females and partners of individual males were low. Obviously, under cyclic food conditions, predictability and inter-generational trade-offs are important to life history traits.     

Fluctuating food supply affects the clutch size of Tengmalm's owl independent of laying date

Summary In western Finland, yearly median laying dates of Tengmalm's owls varied from 14 March to 27 April during 1973–1989 and were negatively correlated with the winter densities of voles. Yearly mean clutch sizes varied from 4.0 to 6.7 and were more closely related to the spring than to the winter densities of voles. The yearly mean clutch size decreased with yearly median laying date. The 3-year vole population cycle is typical of the study area. The start of egg-laying was earliest in the peak phase of the cycle (median laying date 22 March), when vole numbers are high during egg-laying, but decline rapidly to low numbers in the next autumn or winter. In the increase phase (1 April) vole abundances are moderate at the time of laying, but increase to a peak in the next autumn or winter. In the low phase (15 April) voles are scarce in spring and in the preceding winter, starting to increase in late summer. Clutch size and female body mass were independent of laying date in the low phase, decreased slowly but significantly in the increase phase, and declined abruptly in the peak phase. These trends also held when the effects of territory quality, female age and male age were ruled out. When comparing the same laying periods, clutch sizes were significantly larger in the increase than in other phases of the cycle, but there was no difference between the peak and low phases. Supplementary feeding prior to and during egg-laying increased clutch size independent of laying date. These results agreed with the income model (the rate of energy supply during laying determines clutch size). Tengmalm's owls invest most in a clutch in the increase phase, as the reproductive value of eggs is largest because of high survival of yearlings. A high reproductive effort may be adaptive during this phase, because the availability of voles is predictable during the laying period.     

The effects of sex,age, season and habitat on diet of the red fox <Emphasis Type="Italic">Vulpes vulpes</Emphasis> in northeastern Poland

The diet of the red fox Vulpes vulpes was investigated in five regions of northeastern Poland by stomach content analysis of 224 foxes collected from hunters. The red fox is expected to show the opportunistic feeding habits. Our study showed that foxes preyed mainly on wild prey, with strong domination of Microtus rodents, regardless of sex, age, month and habitat. Voles Microtus spp. were found in 73% of stomachs and constituted 47% of food volume consumed. Other food items were ungulate carrion (27% of volume), other mammals (11%), birds (9%), and plant material (4%). Sex- and age-specific differences in dietary diversity were found. Adult males and juvenile foxes had larger food niche breadths than adult females and their diets highly overlapped. Proportion of Microtus voles increased from autumn to late winter. Significant habitat differences between studied regions were found. There was a tendency among foxes to decrease consumption of voles with increasing percentage of forest cover. Based on our findings, red foxes in northeastern Poland can be recognized as a generalist predators, consuming easily accessible and abundant prey. However, high percentage of voles consumed regardless of age, sex, month, or habitats may indicate red fox specialization in preying on Microtus rodents.     

Guardian or threat: does golden eagle predation risk have cascading effects on forest grouse?

Previous studies on intraguild predation have mainly focused on within-class assemblages, even though avian top predators may also influence mammalian mesopredator prey. By using nation-wide long-term data from Finland, northern Europe, we examined the impacts of golden eagles (Aquila chrysaetos) together with red foxes (Vulpes vulpes) and pine martens (Martes martes) on forest-dwelling herbivores, black grouse (Tetrao tetrix) and hazel grouse (Tetrastes bonasia). We hypothesized that eagles may alleviate the overall predation pressure on grouse by imposing intraguild predation risk on mesopredators. The predation impact of eagle was modelled using eagle density estimates and distance to eagle nest. Wildlife triangle counts were used as predation impact proxies of mammalian mesopredators and as measures of response in grouse. Our results show that eagle density correlated negatively with black grouse abundance indices while being positively associated with the proportion of juveniles in both grouse species, irrespective of the abundance of mesopredators. Yet, foxes and martens alone had a negative effect on the abundance indices and the proportion of young in the two grouse species. This suggests that the possible cascading effects of eagles are not mediated by decreased mesopredator numbers, but instead by fear effects. Alternatively, they may be mediated by other species than fox or marten studied here. In conclusion, we found support for the hypothesis that eagles provide protection for juvenile black and hazel grouse, whereas they are a threat for adult grouse. This important information helps us to better understand the role of avian top predators in terrestrial ecosystems.