Disease dynamics in cyclic populations of field voles (Microtus agrestis): cowpox virus and vole tuberculosis (Mycobacterium microti)

The possible role of pathogens in rodent population cycles has been largely neglected since Elton's 'epidemic hypothesis' of 1931. To revisit this question, 12 adjacent, cyclic but out-of-phase populations of field voles (Microtus agrestis) in North East England were studied and the initial results are presented here. The prevalences of antibodies to cowpox virus and of clinical signs of Mycobacterium microti infection (vole tuberculosis) showed delayed (not direct) density dependence (with a lag of three to six months). This did not result from changes in population structure, even though there were such changes associated with the different phases of the cycle. The prevalences rose as vole numbers rose, and peaked as numbers declined. The apparent lag in the numerical response of infection prevalence to changes in host abundance is consistent with the hypothesis that diseases, singly or in combination, play a hitherto underestimated role in the dynamics of cyclic populations.     

The dynamics of health in wild field vole populations: a haematological perspective

1. Pathogens have been proposed as potentially important drivers of population dynamics, but while a few studies have investigated the impact of specific pathogens, the wealth of information provided by general indices of health has hardly been exploited. By evaluating haematological parameters in wild populations, our knowledge of the dynamics of health and infection may be better understood. 2. Here, haematological dynamics in natural populations of field voles are investigated to determine environmental and host factors associated with indicators of inflammatory response (counts of monocytes and neutrophils) and of condition: measures of immunological investment (lymphocyte counts) and aerobic capacity (red blood cell counts). 3. Individuals from three field vole populations were sampled monthly for 2 years. Comparisons with individuals kept under controlled conditions facilitated interpretation of field data. Mixed effects models were developed for each cell type to evaluate separately the effects of various factors on post-juvenile voles and mature breeding females. 4. There were three well-characterized 'physiological' seasons. The immunological investment appeared lowest in winter (lowest lymphocyte counts), but red blood cells were at their highest levels and indices of inflammatory response at their lowest. Spring was characterized by a fall in red blood cell counts and peaks in indicators of inflammatory response. During the course of summer-autumn, red blood cell counts recovered, the immunological investment increased and the indicators of inflammatory response decreased. 5. Poor body condition appeared to affect the inflammatory response (lower neutrophil and monocyte peaks) and the immunological investment (lower lymphocyte counts), providing evidence that the capacity to fight infection is dependent upon host condition. 6. Breeding early in the year was most likely in females in better condition (high lymphocyte and red blood cell counts). 7. All the haematological parameters were affected adversely by high population densities.     

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.     

Splenomegaly and reticulocytosis caused by Babesia microti infections in natural populations of the montane vole, Microtus montanus.

A survey for Babesia microti in rodents was conducted at six sites within Grand Teton National Park, Wyoming. Blood and spleen smears, hematocrits, and reticulocyte counts were made on all of the animals to evaluate parameters for the diagnosis of babesiosis. Ticks were removed for identification. Of 257 Microtus montanus, 103 were infected with B. microti. In addition, five of 12 Microtus pennsylvanicus and one of three Arvicola richardsoni were parasitized by B. microti. Peromyscus maniculatus (n = 40) were not infected. Concurrent infections by Hepatozoon sp., Trypanosoma sp., and the bacterium, Grahamella sp., were noted in blood smears from a number of M. montanus. Splenomegaly and reticulocytosis were significant parameters associated with babesiosis while decreased hematocrit was not. Ticks removed from the voles were identified as Ixodes eastoni and were the probable vectors of the B. microti.     

Tuberculosis (Mycobacterium tuberculosis) in a pregnant baboon (Papio cynocephalus)

BACKGROUND: Old World monkeys are considered more susceptible to tuberculosis (TB) than New World monkeys. Several cases of TB in baboons are described in the literature. The data regarding baboon reaction to the tuberculin skin test (TST) are controversial. Some authors described anergy in this species, while the others documented a positive reaction. CASE REPORT: An 8-year-old clinically healthy pregnant female baboon (Papio cynocephalus anubis) developed positive TST after 3 years of negative tests in captivity while not pregnant. Thoracic radiographs demonstrated three nodular densities in the lung. RESULTS: Histological examination of tracheobronchial lymph nodes revealed multiple coalescing pyogranulomas filled with caseonecrotic debris and mineralized foci with numerous large foreign body-type and Langhans-type multinucleated giant cells. The bacterial culture contained a slow growing Mycobacterium tuberculosis complex. CONCLUSIONS: We describe, to the best of our knowledge, the first case of a positive TST in a wild caught, pregnant baboon with latent infection after 3 years in captivity.     

Spatial dynamics in fluctuating vole populations

Summary Patterns and consistency of distribution, spatial and temporal components, and the extent of spatial density-dependence were compared between semi-cyclic and cyclic populations of the vole species Clethrionomys glareolus and Microtus agrestis in south-central and north Sweden. Cyclic populations were less clumped and only C. glareolus showed a consistency in distribution between years. Spatial variation contributed little to the distributions in cyclic populations while the spatial and temporal variations were of the same magnitude in the semi-cyclic populations. The latter populations could be subdivided into areas with different spatial and temporal components. The spatial density-dependence increased from increase to decline years in C. glareolus but not in M. agrestis, which differed conspicuously between reregions in population development. The data imply that spatial dynamics should be considered as much as temporal ones for non-cyclic populations, that the same regulating or limiting factors may be at work in both spatial and temporal components and that, in addition, social behaviour may be important in explaining spatial dynamics. However, the latter effects may be fairly species-specific.     

Mycobacterium microti infection in a cat and some pigs

A case of tuberculosis in a cat, probably caused by the vole-type tubercle bacterium (M. microti) and 3 cases of vole tuberculosis in pigs are described. Contrary to what had been found earlier in ferrets and a calf, the vole bacillus was to some extent pathogenic to pigs, causing gross lesions in several lymph nodes and in one case in the spleen. The possibility that the vole bacillus causes pseudo-specificity to bovine tuberculin in cattle is discussed.     

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.     

Fine structure of the mandibular gland in Japanese field vole (Microtus montebelli)

The mandibular glands of the Japanese field vole were examined by light microscopy, and transmission and scanning electron microscopies. The acinar cells contained light and coarse secretory granules, and reacted with PAS and stained slightly with AB; they were considered to be seromucous in nature. The acinar epithelium was composed of light and dark cells containing many secretory granules. The intercalated duct cells consisted of light cells possessing a few dense granules. A few cytoplasmic crystalloides of moderate density were observed in occasional light cells. The striated ducts were comprized of two distinct portions, a secretory portion and a typical striated portion without secretory granules. The epithelium secretory portion consisted of light and dark cells containing acidophilic granules and exhibited a sexual dimorphism in these granules: The male epithelia contained the granules of low to high densities, while the female epithelia had only dense granules being smaller than those in the males. The epithelium of typical striated portion was composed of light and dark cells containing fine vacuoles and vesicles.     

Experimental fluoride accumulation and toxicity in the short-tailed field vole (Micvotus agrestis)

Vegetation established naturally on three industrial sites contaminated by either airborne or soilborne fluorides was used to formulate dietary feed for a laboratory-reared population of field voles ( Microtus ugrestis L.), an herbivorous species indigenous to all three locations. Animals exposed to laboratory diets containing 100–300 mg F kg^-1 derived from vegetation from around the aluminium smelter and fluorochemical works showed reduced live weight gain, between 40 and 100% mortality and developed marked dental lesions. These comprised banding of the enamel, loss of colour and erosion of the cutting surfaces of the incisors, and dentine cavitation and erosion of the grinding faces of the molar teeth. These morphological changes were accompanied by excessive accumulation of fluoride in the teeth. Voles consuming a diet of vegetation from the mine tailings site with a similar level of fluoride (100 mg kg^-1) as for the other industrial locations, showed only slight dental changes and no weight loss or early mortality. This pattern for laboratory-bred voles is similar to that experienced in populations of this species in the wild, and the contrast in the severity of the dental lesions is ascribed to intersite differences in the chemical speciation and bioavailability of fluoride.     

Mycobacterium microti (Vole Bacillus): a Method for Viable Counts Within 21 Days of Culture

A method is described for counting viable units of Mycobacterium microti (vole bacillus) suspensions after 21 days of culture on an oleic-albumin agar medium containing 5% defibrinated horse blood, with a tight seal to maintain humidity. This method is important because vole bacillus is an alternative to BCG in the prevention of tuberculosis.     

Phytosterols affect endocrinology and metabolism of the field vole (Microtus agrestis)

Phytosterols or plant sterols (PS) enter the ecosystem via pulp mill effluents. They are also consumed by the general population of developed countries in natural remedies and margarines to lower elevated serum cholesterol levels. This study screened the endocrine and enzymatic parameters of the field vole (Microtus agrestis) for the effects of subchronic PS exposure at three doses (0, 5, or 50 mg of PS kg(-1) day(-1)). PS at 5 or 50 mg kg(-1) day(-1) decreased the relative liver weight of the voles. The kidney glycogen phosphorylase activity decreased at 5 or 50 mg kg(-1) day(-1), but the liver glycogen phosphorylase activity increased at 5 mg kg(-1) day(-1). The plasma estradiol and testosterone concentrations of males were higher due to PS supplement at 5 mg kg(-1) day(-1). This can be due to increased sex steroid synthesis from PS precursors. Biotransformation enzyme activities were not affected. PS caused multiple, previously unreported effects that were more pronounced at a low dose. As 5 mg PS kg(-1) day(-1) is the recommended dose for various health products, a thorough risk assessment of the effects and interactions of PS is warranted.     

Variation in wild populations of annual beet (Beta,Chenopodiaceae)

Among the morphological variation in wild annual populations of sect.Beta only tepal characters show a geographic pattern, and hence can be used to distinguish different taxa. Two morphological types correspond with taxa already described:B. macrocarpa (incl.B. bourgaei) has a Macaronesian and W. to E. Mediterranean andB. adanensis an E. Mediterranean distribution area. A third type in the Aegean region is not well known yet and possibly has to be included inB. macrocarpa. Both diploid and tetraploid (x = 9) cytotypes are found withinB. macrocarpa, the latter exclusively on the Canary Islands.     

Cowpox virus infection in natural field vole Microtus agrestis populations: significant negative impacts on survival

1. Cowpox virus is an endemic virus circulating in populations of wild rodents. It has been implicated as a potential cause of population cycles in field voles Microtus agrestis L., in Britain, owing to a delayed density-dependent pattern in prevalence, but its impact on field vole demographic parameters is unknown. This study tests the hypothesis that wild field voles infected with cowpox virus have a lower probability of survival than uninfected individuals. 2. The effect of cowpox virus infection on the probability of an individual surviving to the next month was investigated using longitudinal data collected over 2 years from four grassland sites in Kielder Forest, UK. This effect was also investigated at the population level, by examining whether infection prevalence explained temporal variation in survival rates, once other factors influencing survival had been controlled for. 3. Individuals with a probability of infection, P(I), of 1 at a time when base survival rate was at median levels had a 22.4% lower estimated probability of survival than uninfected individuals, whereas those with a P(I) of 0.5 had a 10.4% lower survival. 4. At the population level, survival rates also decreased with increasing cowpox prevalence, with lower survival rates in months of higher cowpox prevalence. 5. Simple matrix projection models with 28 day time steps and two stages, with 71% of voles experiencing cowpox infection in their second month of life (the average observed seroprevalence at the end of the breeding season) predict a reduction in 28-day population growth rate during the breeding season from lambda = 1.62 to 1.53 for populations with no cowpox infection compared with infected populations. 6. This negative correlation between cowpox virus infection and field vole survival, with its potentially significant effect on population growth rate, is the first for an endemic pathogen in a cyclic population of wild rodents.     

Individual growth rates in natural field vole, Microtus agrestis, populations exhibiting cyclic population dynamics

Rodents that have multi-annual cycles of density are known to have flexible growth strategies, and the “Chitty effect”, whereby adults in the high-density phase of the cycle exhibit larger average body mass than during the low phase, is a well-documented feature of cyclic populations. Despite this, there have been no studies that have repeatedly monitored individual vole growth over time from all phases of a density cycle, in order to evaluate whether such variation in body size is due to differences in juvenile growth rates, differences in growth periods, or differential survival of particularly large or small voles. This study compares growth trajectories from voles during the peak, increase and crash phases of the cycle in order to evaluate whether voles are exhibiting fast or slow growth strategies. We found that although voles reach highest asymptotic weights in the peak phase and lowest asymptotes during the crash, initial growth rates were not significantly different. This suggests that voles attain larger body size during the peak phase as a result of growing for longer.     

AFLP genetic polymorphism in wild barley (Hordeum spontaneum) populations in Israel

The genetic diversity produced by the amplified fragment length polymorphism (AFLP) method was studied in 94 genotypes of wild barley, Hordeum spontaneum (C. Koch) Thell., originating from ten ecologically and geographically different locations in Israel. Eight primer pairs produced 204 discernible loci of which 189 (93%) were polymorphic. Each genotype had a unique banding profile and the genetic similarity coefficient varied between 0.74 and 0.98. The phenogram generated from these similarities by the UPGMA method did not group genotypes strictly according to their geographical origin, which pattern was also seen in the principal coordinate (PCO) plot. Genetic diversity was larger within (69%) than among (31%) populations. Associations between ecogeographical variables and the mean gene diversity were found at one primer pair. The results are discussed and compared with data obtained by the simple sequence repeat (SSR) method.