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Disease Reveals the Predator: Sarcoptic Mange, Red Fox Predation, and Prey Populations
Ecology
Abstract
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 (10^1-10^2 km^2), a regional (10^4 km^2), 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.
... Brown hares are also exposed to contamination from specific environmental pollutants, such as heavy metals, which accumulate in the organisms of hares at a higher rate than in other animals (Beuković et al. 2022(Beuković et al. , 2023. Predators, especially the red fox Vulpes vulpes (Linnaeus, 1758), collisions with vehicles and infectious diseases are the main reasons given for the mortality of European brown hares (Lindström et al. 1994;Lamarque et al. 1996;Haerer et al. 2001). Lamarque et al. 1996 found that more than 50% of hares found dead in France between 1986 and 1994 had died on infectious diseases, primarily EBHSV infection, then pseudotuberculosis, pasteurellosis and coccidiosis. ...
Serological tests for the presence of antibodies to European brown hare syndrome virus and rabbit hemorrhagic disease virus type a and type 2 were performed on 275 samples of blood serum from the European brown hare by hemagglutination inhibition test and enzyme-linked immunosorbent assay. The presence of antibodies against European brown hare syndrome virus was 28% in the Czech Republic while in the Slovak Republic between 9-33%. Furthermore, the results showed the possibility of interspecies transmission, both rabbit hemorrhagic disease virus type a and rabbit hemorrhagic disease virus type 2 on the European brown hare. In case of RHDVa it is the first documented interspecies transmission, which has not yet been described. This study improved our knowledge about circulation of RHDV in Central European ecosystems and its possible ability to cross interspecies barriers. However, from an epizootiological point of view, it is likely European brown hare is not a significant source of RHD infection for domesticated rabbits.
... In the APH, the red fox (Vulpes vulpes) and the pine marten (Martes martes) have been regarded as the most important predators, but the effect of each could not be disentangled in predator removal experiments (Marcström et al., 1988(Marcström et al., , 1989; see also Lindström et al., 1987;Kurki et al., 1997). However, the decline of the red fox population caused by an irruption of the sarcoptic mange (Sarcoptes scabei) in Sweden and Norway in the 1970s revealed that the effect of the red fox on alternative prey was according to the APH (Lindström et al., 1994), and also that the red fox limited the pine marten population Smedshaug et al., 1999). ...
According to the alternative prey hypothesis (APH), the temporal synchrony in population fluctuations of microtine rodents and other small herbivores in boreal areas is caused by generalist predators with numerical and functional response to microtines, leading to an increased predation of prey alternative to microtines in the low phase of the microtine population fluctuations. The tree-climbing pine marten (Martes martes) is a food generalist that includes bird eggs among its alternative prey, also eggs of the cavity-nesting common goldeneye (Bucephala clangula). We used long-term data to test whether pine marten predation of goldeneye eggs in nest boxes varied as predicted by the APH. As a measure of microtine abundance at the time of nesting, we applied two measures. First, for goldeneye nests located <40 km from our microtine trapping site, we applied the trapping index of microtine rodents. Second, to also use data from nests located >40 km from our microtine trapping site, and from nests in years when trapping was not conducted, we used two proxies for the microtine abundance: whether boreal owls (Aegolius funereus) nested in any of our boxes <40 km from each goldeneye nest and the average clutch size of these boreal owls. The probability of predation of a goldeneye nest was independent of the microtine trapping index and independent of the proxies for microtine abundance. However, it increased with cavity age, taken as the number of nesting seasons elapsed since the actual nest box was installed, and declined with distance from habitat with forest canopy. The effect of cavity age confirms that the long-term spatial memory of pine marten is an important factor in the pattern of its predation on nests in tree cavities. K E Y W O R D S alternative prey hypothesis, cavity age, forest edge, long-term spatial memory, microtine rodents, nest box, nest predation
... The models for densities of prey species consisted of habitat components (PC1 and PC2), year and the abundance of the red fox. The red fox was chosen to the models because it is an important predator limiting the numbers of hare and grouse (Lindström et al. 1994). All the statistical analyses were conducted with the SPSS 9.05 for Windows. ...
The sprawl of tourism to natural areas may have many kinds of effects on wildlife species due to urban development, landscape fragmentation and increased disturbance. I examined potential effects of tourist destinations on four forest grouse and five mammalian species in northern Finland. I used density data coming from the late-summer and mid-winter wildlife counts. The data was collected in 88 wildlife triangles (length of 12 km each) within a radius of 40 km around ten tourist destinations in northern Finland conducted during 1989–2006 by hunters. The densities of the mountain hare ( Lepidus timidus ) and the mustelid species correlated negatively with the distance to a tourist destination. The density of adult grouse, juvenile grouse, mountain hare, and mustelids were positively correlated with the area of mixed forests surroundings of destinations. The densities of adult and juvenile grouses were positively and the density of pine marten and mustelids were negatively correlated with the area of agricultural land surroundings of destinations. The density of studied wildlife species varied between the destinations and the years. The results of the study suggest that the current recreation pressure has not caused substantial changes in the wildlife fauna in the surroundings of tourist destinations studied. The location of a destination, predator densities, and a landscape structure around destinations affected most the density of wildlife species.
... A notable aspect of the literature in this study is the occurrence of research themes in pathogen impacts assessed among host species, especially for well-studied host species. For example, red foxes were commonly used to assess population and community-level efects of infection [60][61][62]. In contrast, studies on bare-nosed wombats, Iberian ibexes, and Japanese raccoon dogs were often used to assess the immunological and physiological efects given infection [38,[63][64][65][66][67][68][69], whereas coyotes and grey wolves were more frequently used to assess the behavioural and social efects of infection [70][71][72][73]. ...
Most pathogens infect more than one host species, and given infection, the individual-level impact they have varies among host species. Nevertheless, variation in individual-level impacts of infection remains poorly characterised. Using the impactful and host-generalist ectoparasitic mite Sarcoptes scabiei (causing sarcoptic mange), we assessed individual-level variation in pathogen impacts by (1) compiling all documented individual-level impacts of S. scabiei across free-living host species, (2) quantifying and ranking S. scabiei impacts among host species, and (3) evaluating factors associated with S. scabiei impacts. We compiled individual-level impacts of S. scabiei infection from 77 host species, spanning 31 different impacts, and totalling 683 individual-level impact descriptions. The most common impacts were those affecting the skin, alopecia (130 descriptions), and hyperkeratosis coverage (106). From these impacts, a standardised metric was generated for each species (average impact score (AIS) with a 0-1 range), as a proxy of pathogen virulence allowing quantitative comparison of S. scabiei impacts among host species while accounting for the variation in the number and types of impacts assessed. The Japanese raccoon dog (Nyctereutes viverrinus) was found to be the most impacted host (AIS 0.899). We applied species inclusion criteria for ranking and found more well-studied species tended to be those impacted more by S. scabiei (26/27 species AIS < 0.5). AIS had relatively weak relationships with predictor variables (methodological, phylogenetic, and geographic). There was a tendency for Diprotodontia, Artiodactyla, and Carnivora to be the most impacted taxa and for research to be focussed in developed regions of the world. This study is the first quantitative assessment of individual-level pathogen impacts of a multihost parasite. The proposed methodology can be applied to other multihost pathogens of public health, animal welfare, and conservation concern and enables further research to address likely causes of variation in pathogen virulence among host species.
... Predicting outcomes under uncertainty is one thing, predictions without understanding uncertainty can result in unexpected surprises (Allen and Gunderson 2011, Seville et al. 2015). For example, the effects of the sarcoptic mange on the fox population and many of its prey populations when it first entered Sweden came as a surprise (Lindström et al. 1994, Willebrand et al. 2021. I think we need more emphasize on explaining knowledge, uncertainty and surprise to stakeholders and students (Tobias and Everson 2002). ...
THIS IS NOT AN ABSTRACT This is not a traditional manuscript and is a result of my thoughts on wildlife research since NKV decided to start Wildlife Biology to replace the national journals 30 years ago. I am not sure that this is a format suitable for Wildlife Biology but it would be interesting to know what you think. Best wishes, Tomas Willebrand
... While variation in opening day of hunting is likely to have some effect, variation in CPUE of this magnitude is most likely dominated by changes in true population size. Harvest and population census data often gives a reasonable match (Small et al. 1993, Lindstrom et al. 1994, Cattadori et al. 2003, Ranta et al. 2008, Lampila et al. 2011, Soininen et al. 2016, especially when the annual variation in hunting bags as well as true populations size is large (Willebrand et al. 2011). We argue that this is the case for our willow ptarmigan time series. ...
Long time series are important because they extend back to an era when animal populations were less influenced by habitat loss and climate change. Annual fluctuations in harvest yields are good proxies for large changes in population size and may reveal underlying ecological processes. From a variety of sources, we built a 142‐year long time series representing the mean daily catch (CPUE) of willow ptarmigan Lagopus lagopus in southeastern Norway. CPUE decreased over the 142 years, from approximately 35 birds shot per day in early years to around two in the last years. There were three periods in the time series: a first period with 3–5 year cycles of high peaks and low troughs (1872–1900), a short second period with similarly high peaks, variable depth of troughs and variable cyclicity (1901–1916), and a third long period with much lower peaks and faded cycles (1917–2013). Yearly variation in CPUE was best explained by an interacting effect of small rodent peak years and period, with a reduced positive effect of rodents in the last period, and a positive effect of the North Atlantic Oscillation index in spring and early summer. None of the weather variables with significant time trends explained any variation in CPUE and we could therefore not attribute the decline in CPUE directly to climate change. We postulate that a long‐term dampening of the amplitude in small rodent cycles combined with an increase in red fox numbers, have increased predation on alternative prey like ptarmigan, and prevented the populations from reaching their earlier peaks. Even though the present population of willow ptarmigan is only a fraction of what it was in former days, we recommend light hunting to motivate for monitoring and to keep public attention on the bird.
The aim of the current study is to determine the
habitat usage of brown hare (Lepus europaeus L.)
which is spread in Isparta Gölcük Nature Park. The
study was carried out in 2011 and 2012. In order to
determine the habitat use and habitat preference,
the presence-absence method was applied. It has
been determined that brown hare use more
coniferous forest and forested openings according
to the relative frequencies found at the end of
counts performed on a total of 106 lines and 2655
plots. It has been seen that brown hare prefers the
west and south aspect. It would be useful to use the
data obtained in the sustainable management of
interest by interest groups.
In conclusion, Western Hazel Grouse is most probably doomed to extinction
in the southern Vosges Mountains which means also globally.
Unlabelled:
Since 2017, a reinforcement programme was developed to save the last, endangered, Belgian population of black grouse (Lyrurus tetrix), in the High Fens Natural Park. To improve the success of this programme, an analysis of past data of this population was undertaken to understand the causes of its past decline. A time series analysis was applied, using annual spring male census data recorded between 1967 and 2016. In the period 1967-1993, there was a fluctuation around an equilibrium of a population of ca. 40-45 males. The peak of 85 males observed in 1971 was probably due to a succession of several favourable years in terms of environmental conditions, albeit without an exceptional annual growth rate. It seems that fox density, by using the occurrence of rabies as a proxy, has an impact on the black grouse population. After 1993, the population dynamic changed drastically, decreasing continuously until finally reaching quasi-extinction. On average, the population lost 15.4% of its size each year. Climate models, applied in previous studies to explain these population trends in the High Fens, failed to describe this major modification in this population's dynamic and its recent decline. We suggest that this negative effect was mainly induced by a significant increase in predation by red fox (Vulpes vulpes), whose abundance has increased considerably since the 1990s, in particular, as a consequence of the eradication of fox rabies. We also discuss alternative hypotheses, such as the impact of other predator species, modification of the natural environment and climatic modifications.
Supplementary information:
The online version contains supplementary material available at 10.1007/s10344-023-01642-w.
Danell K. 1985: Population fluctuations of the muskrat in coastal northern Sweden. Acta theriol., 30, 12: 219—227 [With 1 Table & 3 Figs.] The fluctuations of five muskrat populations in coastal northern Sweden are described over periods of 7—14 years. The population in Sladan was studied more intensively since it colonized this area around 1963. During the last 14 years it fluctuated with a periodicity of 4 years. This time length is identical to the vole cycle length in the area. However, the muskrat population reached their peaks one year after the vole peaks. In the above population the predation pressure by foxes upon muskrats was recorded yearly for 9 years. The predation pressure was negatively correlated with vole density. Two other muskrat populations which settled in 1955 and 1963, respectively, displayed fluctuations similar to those of the voles, and the muskrat peaked with a one year dephasing. Two muskrat populations which had colonized their localities more recently (in 1970 and 1975) remained for some years at low levels and then steadily increased. The population fluctuations were not directly related to the changes in the vole populations.
Population dynamics of sympatric microtines and shrews in Finnish Lapland are compared on the basis of a long-term data set. Hansson's (1984) observation of the simultaneous crash in shrews and cyclic microtines seems to be a general pattern in northern Fennoscandian taiga, probably best explained by predation by small mustelids.
Synchronized fluctuations in vole and grouse populations in boreal Fennoscandia have been explained as the result of shifting predation pressure: the alternative prey hypothesis. We tested this hypothesis by supplying additional food to predators in only one of two 615 ha areas during the crash in vole density in 1985. As predicted from the hypothesis the proportion of young grouse in autumn was higher in the experimental area than in the control area. Moreover, the proportion decreased in the control area in comparison with the year before, but did not do so in the experimental area. Thus, with respect to synchronized short-term population fluctuations of voles and grouse, we find the hypothesis that predators take only a doomed surplus less probable. However, we cannot discard the hypothesis that grouse decline during years of strong vole decline for example because a poor quality or low quantity of food makes them more vulnerable to predators. Hence, predation is a necessary but perhaps not a sufficient factor in mediating short-term fluctuations from voles to grouse in boreal Fennoscandia.
After a reduction in red fox Vulpes vulpes Linnaeus, 1758 density in south-central Sweden due to an epizootic of sarcoptic mange, which reached the study area in 1982, pine martens Martes martes Linnaeus. 1758 became more abundant. By scat analysis and by snow-tracking we compared winter diet and habitat selection of martens before (1979-80) and after (1987) the decline in foxes to test potential effects of relieved competition on martens. We also used radiotelemetry to study habitat selection after the fox decline in winter and in summer. We were able to show that, at least in the winter situation, martens and foxes do not compete over field voles Microtus agrestis which are a favoured prey of foxes. Probably snow conditions rather than competition limited the consumption of voles by martens in winter. The avoidance of clearcuts by martens seemed to be related to the martens' escape behaviour and had not changed after the decline in foxes. Our data did not contradict relieved interferenceand resource-competition as causes of the increase in the marten population. Our study confirmed the role of the pine marten in the boreal forest as an opportunistic generalist predator which is largely bound to old successional stages.
Predation impact has recently been considered generally important but in experiments has only been measured in the optimal habitat of the prey species, while predators usually forage over much larger areas. Arguments are presented that such optimum habitats are often not the very best test objects, that dispersal may confuse the results and that suboptimal and marginal habitats of prey are more important for generalized predators. Experimental studies should thus cover entire landscapes, which is not easily achieved. Natural experiments, therefore, should not be disregarded in this type of research.
(1) Predators were removed in an experiment to study the impact of mammal predation on woodland tetraonid populations during vole cycles. Foxes and martens were killed from 1976 to 1980 on one of two similar islands in the northern Baltic. The treatment was then reversed until 1984. (2) When predators were killed, tetraonid brood sizes averaged 5.52 in August, and 77% of hens had chicks. When predator were not killed, broods averaged 3.29 chicks and 59% of hens had chicks. (3) Counts of adult capercaillie and black grouse during July and August increased by 56-80% after 2 years of predator removal. Counts at leks increased by 166-174%. (4) Removing foxes and martens had no significant effect on vole abundance during two 4-year cycles. (5) When predators were not removed, tetraonid brood sizes and the proportion of females that bred successfully were each positively correlated with vole abundance in summer. There were most chicks per adult hen when vole numbers were high and increasing slowly from summer to autumn. When foxes and martens were killed, neither brood size nor subsequent adult numbers were significantly correlated with vole abundance in summer, although losses of whole broods increased slightly when vole numbers grew most rapidly from summer to autumn. We conclude that large vole populations resulted in large autumn grouse populations mainly because they reduced predation on breeding grouse. (6) The vole numbers and increase rates that were asociated with high grouse breeding success in one summer were also associated with low counts of adult grouse the next year, and thus with an increase in grouse losses from one summer to the next.
Cederlund G. & Lindstrom E., 1983 : Effects of severe winter and fox predation on roe deer mortality. Acta theriol., 28, 7 : 129—145 [With 7 Tables & 5 Figs.] This is a study of the mutual impact of roe deer, Capreolus capreolus (Linnaeus, 1758) and red foxes, Vulpes vulpes (Linnaeus, 1758) ; deer mortality and food supply needed for fox reproduction. Density of roe deer was reported via questionnaires to increase during the study except an interruption after the severe winter 1976/77. The interruption was more pronounced in a northern forested area with deeper snow cover than in a southern mixed agricultural area. Mortality rate of roe deer as measured by radio-telemetry was high (0.31 in adults and 0.66 in juveniles) during the severe winter compared to the other winters (0.02 for pooled sample). Individual foxes consumed more roe deer (1) during the severe winter than during any other winter, (2) in the northern area than in the southern area during the winter 1976/77, and (3) the more snow-depth increased during 1976/77 (scat and stomach analyses). The ultimate cause of deer death during 1976/77 was most probably malnutrition. 1976/77 was of increasing vole densities and it was not possible to detect any impact of roe deer availability on reproductive success of foxes. If the severe winter had occurred during a vole low, the availability of weakened and dead roe deer would probably have prevented an expected reproductive failure among foxes. Summer mortality of fawns was indirectly attributable to fox predation. Occurrence of roe deer remains in scats of juvenile foxes was inversely related to vole abundance. We suggest that the effect of fox predation on roe deer fawns may be conspicuous in the summer after a severe winter coinciding with a vole low. [The National Swedish Environment Protection Board, Grimso Wildlife Research Station, S-770 31 Riddarhyttan, Sweden].