Birger Hörnfeldt

Disease Reveals the Predator: Sarcoptic Mange, Red Fox Predation, and Prey Populations

An epizootic of sarcoptic mange was prevalent among Scandinavian red foxes (Vulpes vulpes) during the late 1970s and 1980s. By substantially reducing the population density of foxes, the epizootic created a natural experiment on the importance of fox predation for prey density. The fox population started to recover during the late 1980s. We monitored the populations of the fox and its prey [voles (Cricetidae), mountain hare (Lepus timidus), European hare (L. europaeus), Capercaillie (Tetrao urogallus), Black Grouse (T. tetrix), Hazel Grouse (Bonasa bonasia), and roe deer (Capreolus capreolus)] throughout the event, on a local (101—102 km2), a regional (104 km2), and a national scale. Methods included den counts, snap—trapping, pellet/dropping counts, counts of displaying birds, young/adult ratio from incidental observations of deer, regional questionnaires, and national hunting records. The study revealed red fox predation as a crucial factor in limiting the numbers of hares and grouse as well as fawns per doe of roe deer in autumn, and in conveying the 3—4 yr cyclic fluctuation pattern of voles to small game. The classical view, that predators take but a doomed surplus of their prey, was false for these species in Scandinavia.

Delayed Density Dependence as a Determinant of Vole Cycles

Largely synchronous population fluctuations of Clethrionomys glareolus, C. rufocanus, and Microtus agrestis were monitored by snap-trapping in spring and autumn in 1971-1988 in a strongly seasonal environment near Umea, northern Sweden. All species were cyclic in the sense that they showed fairly regular (3-4 yr) fluctuations, but amplitudes (nma,/nmin) varied, averaging - 200-fold in each species. This conclusion was supported by autocorrelation and spectral analysis, and by fitting time series data to a model for phase-forgetting cycles. By contrast, data did not conform to a model for phase-remem- bering cycles (with fixed period and amplitude). The transition between cycles, i.e., from the low to increase phase, was characterized by a distinct shift in rate of change in numbers from low to high or markedly higher values both in summer and winter. Generally, rate of change in summer declined continuously from the increase phase through each cycle. Moreover, there was a similar decrease of rate of change in winter, although rate of change (mainly in C. rufocanus and M. agrestis) first frequently increased early in the cycle. Rate of change was delayed density dependent in all species both in summer and winter, as revealed by high negative correlations with density in previous autumn and spring for summer and winter changes, respectively. These new findings of delayed density dependence (DDD) support the suggestion that vole cycles are generated by a time-lag mechanism. Possible mechanisms of the DDD are discussed. Regression analyses of rate of change in the different voles suggest that, besides the strong dependence on previous density, rate of change in numbers was also affected by current seed supply (in C. glareolus) and/or weather variables (temperature and precipi- tation sums) that may have affected the quantity or quality of food.

Synchronous population fluctuations in voles, small game, owls, and tularemia in northern Sweden

Summary1.The population fluctuations in time in northern Sweden are examined for the following species: voles, mountain hare, willow grouse, black grouse, capercaillie, hazel hen, red fox, long-eared owl, Tengmalms owl, and tularemia. Necessary population data have been obtained from the period 1963–1975/76 as revealed by catches, literature survey, hunting statistics, bird ringing, and obligatory reporting of tularemia in man.2.The populations of the species under consideration are found to fluctuate synchronously in time and show a 3- or 4-year cycle for the period 1963–1975. Population peaks have occurred in connection with the peak densities of voles in the winters 1963–1964, 1966–1967, 1969–1970 and 1973–1974.3.Voles caused extensive forest damage (mainly bark-eating) in at least the latter three peak winters. From consideration of the available literature it is apparent that bark is a marginal food. Thus, increased bark-eating during peak densities of voles in winter should be interpreted as a shortage of preferred food.4.The species studied appear to form a unit (subsystem) within the boreal forest ecosystem. This idea is supported by the connecting predatorprey relationships and the demonstrated synchronous population fluctuations. The subsystem contains herbivores, their food vegetation, and predators. Tularemia is regarded as only one among other predators on voles and mountain hares.5.It is postulated that voles play a central role in causing the overall synchronism in the population fluctuations of the subsystem.6.The synchronous population fluctuations described can be explained by the following model for their regulation:a)An initial decline in vole numbers is brought about by food shortage at winter peak densities.b)Predator populations (built up with the help of the rich supply of voles) cooperate with food shortage and at some critical point predators alone are able to fulfil the decrease in vole numbers.c)Because of the decrease in vole numbers the predators are forced into a decline themselves and must turn to alternative prey species. Mountain hare and gamebird populations represent a low biomass compared with vole populations and predation thus causes the decline in numbers of these small game.d)Low numbers of predators and excessive food supply then allow voles, mountain hares, and gamebirds to increase again.e)The building up of vole populations sets the stage for another increase in the number of predators and a new cycle is started.

Europe-Wide Dampening of Population Cycles in Keystone Herbivores

Cycling in Unison Many small mammals, especially voles, display semi-regular cycles of population boom and bust. Given the fundamental importance of small mammals as basal consumers and prey, such cycles can have cascading effects in trophic food webs. Cornulier et al. (p. 63) collated raw data from vole populations across Europe collected over the past 18 years. Reduction in winter growth rate was common across a wide variety of habitats with very different local climates, suggesting the presence of a continental-scale climatic driver of vole populations. Synchronicity in vole population fluctuation across Europe suggests a common climatic driver. Suggestions of collapse in small herbivore cycles since the 1980s have raised concerns about the loss of essential ecosystem functions. Whether such phenomena are general and result from extrinsic environmental changes or from intrinsic process stochasticity is currently unknown. Using a large compilation of time series of vole abundances, we demonstrate consistent cycle amplitude dampening associated with a reduction in winter population growth, although regulatory processes responsible for cyclicity have not been lost. The underlying syndrome of change throughout Europe and grass-eating vole species suggests a common climatic driver. Increasing intervals of low-amplitude small herbivore population fluctuations are expected in the future, and these may have cascading impacts on trophic webs across ecosystems.

Human Hantavirus Infections, Sweden

The prevalent human hantavirus disease in Sweden is nephropathia epidemica, which is caused by Puumala virus and shed by infected bank voles (Clethrionomys glareolus). To evaluate temporal and spatial patterns of this disease, we studied 2,468 reported cases from a highly disease-endemic region in northern Sweden. We found that, in particular, middle-aged men living in rural dwellings near coastal areas were overrepresented. The case-patients were most often infected in late autumn, when engaged in activities near or within manmade rodent refuges. Of 862 case-patients confident about the site of virus exposure, 50% were concentrated within 5% of the study area. The incidence of nephropathia epidemica was significantly correlated with bank vole numbers within monitored rodent populations in part of the region. Understanding this relationship may help forestall future human hantavirus outbreaks.

Cycles in voles and small game in relation to variations in plant production indices in Northern Sweden

Population dynamics for voles (Cricetidae), Tengmalms owl (Aegolius funereus (L.)), red fox (Vulpes vulpes (L.)) willow grouse (Lagopus lagopus (L.)), black grouse (Lyrurus tetrix (L.)), capercaillie (Tetrao urogallus L.), hazel hen (Tetrastes bonasia (L.)), mountain hare (Lepus timidus L.) and tularemia (Francisella tularensis (McCoy & Chapin)) and game bird recruitment were studied by index methods in northern Sweden. In addition contemporary temperature records and spruce (Picea abies (L.) Karst.) and pine (Pinus silvestris L.) cone crops (as indices for plant production) and the occurrence of forest damage, caused by voles eating bark, were studied.During 1970–80 two synchronous 4-year cycles were observed for voles, predators (Tengmalms owl and red fox) and their alternative prey species (grouse and mountain hare). In grouse the change of numbers was correlated with that of recruitment. Autumn vole numbers peaked about a year before the other species and extensive forest damage occurred at winter peak densities of voles. These population fluctuations are consistent with a predator-prey model for their regulation. In short the model suggests that vole-food plant interactions trigger the cycle of voles, that voles generate the cycle of predators and that these in turn synchronize alternative prey populations to the others at vole declines.For voles, grouse and red fox the amplitude was higher in the first cycle compared to the second one whilst the opposite was true for the mountain hare. Although temperature and cone crops showed large interannual variations they still implied that herbivore food conditions were ‘better’ during the former cycle. Hence, the reduction of the amplitude of the vole cycle may be explained by inter-cyclic differences in plant food conditions, implying food shortage (as indicated by bark-eating) at different population levels. The similar decrease of grouse and red fox populations may also be explained by deteriorated food conditions and/or for the fox by an outbreak of sarcoptic mange (Sarcoptes scabiae var. vulpes). The increased amplitude of the mountain hare cycle was part of a long-term rise in numbers after a tularemia epidemic in 1967. This is interpreted as a recovery, probably towards the generally higher pre-epidemic population level.

Site tenacity and nomadism in Tengmalm's owl (Aegolius funereus (L.)) in relation to cyclic food production

In northern Sweden breeding males of Tengmalms owls (Aegolius funereus (L.)) were site tenacious during and between the peaks of the vole (staple food) cycles, but females only during the peaks. Most of these adults shifted nest boxes between successive years. They selected nest boxes randomly in a radius of 3 km. Juveniles, in contrast to site tenacious adults, dispersed outside their natal area. The females moved longer than the males prior to their first breeding. Five adult females were found to be nomadic. One of these nomadic females previously bred site tenaciously as long as food was abundant. Juveniles and adult males were not found to be nomadic. Emigration of adult females and juveniles occurred most frequently when vole populations declined. The breeding population increased sharply and received immigrants suggesting that nomadism may be essential in the population dynamics. Site tenacity and nomadism are discussed in terms of costbenefit to males and females, respectively. Emphasis is on the main functional roles of males (feeding femle and young) and females (incubation).

Predicting High Risk for Human Hantavirus Infections, Sweden

An increased risk for hemorrhagic fever with renal syndrome caused by Puumala hantavirus was forecast for Sweden in 2007. The forecast was based on a predicted increase in the number of Myodes glareolus rodents (reservoir hosts). Despite raised awareness and preparedness, the number of human cases during July 2007–June 2008 was 1,483, a new high.

Distribution and genetic heterogeneity of Puumala virus in Sweden

Small mammals trapped in Sweden were analysed for specific antibody responses against three hantavirus serotypes and for the presence of viral antigen. To determine the genetic identity of viral RNA in lungs of seropositive bank voles (Clethrionomys glareolus), polymerase chain reactions and subsequent partial sequencing of both the M and S segments were employed. The sequences obtained were all identified as Puumala (PUU) virus, with a high degree of heterogeneity between the different geographical localities. Alignment of nucleotide and deduced amino acid sequences, together with phylogenetic analysis, showed that PUU viruses circulating in central Sweden were distinct from those in the northern region. The localization of the two distinct PUU virus genotypes was shown to correlate with the postglacial recolonization of Sweden by bank voles.

Numerical responses by populations of red fox and mountain hare during an outbreak of sarcoptic mange

SummaryDuring a severe outbreak of sarcoptic mange (Sarcoptes scabiei vulpes) starting among red foxes (Vulpes vulpes) in Sweden in the 1970s, we studied: 1) the establishment and spread of the disease in northernmost Sweden (by inquiries), and 2) the 1970–84 bag records for foxes and mountain hares (Lepus timidus) (an alternative prey to the foxs main prey, voles). Since the first case of sarcoptic mange in 1975 the disease spread rapidly, with >50% of the hunting organizations having reported the disease in 1981 and >75% in 1983. Also the disease became more abundant within the areas affected. In areas with a low mange infection rate (index) the number of foxes killed in the 1980s did not deviate markedly from the average level in the 1970s. However, there was a slight tendency towards a decline in areas with a medium index and numbers declined markedly where the index was high. Hare harvests initially were low (after a tularemia epidemic) in the 1970s. In that decade harvests increased dramatically and stabilized, increased gradually or changed little, respectively, where mange infection rates were low, medium or high in the early 1980s. In areas with a low mange index hare harvests remained cyclical and at the same level in the 1980s as in most of the 1970s. However, in areas with a medium index harvests increased and seemed to begin to lose their cyclicity, and where the index was high the low and relatively stable hare harvests increased annually. A predator-prey hypothesis, assuming predators to synchronize alternative prey declines to those of the cyclic main prey, predicts that a predator reduction would cause a gradual disappearance of the cyclicity and increasing numbers among alternative prey. Our hare data are partially consistent with this prediction.