Isabella M. Cattadori

Parasites and climate synchronize red grouse populations

There is circumstantial evidence that correlated climatic conditions can drive animal populations into synchronous fluctuations in abundance. However, it is unclear whether climate directly affects the survival and fecundity of individuals, or indirectly, by influencing food and natural enemies. Here we propose that climate affects trophic interactions and could be an important mechanism for synchronizing spatially distributed populations. We show that in specific years the size of red grouse populations in northern England either increases or decreases in synchrony. In these years, widespread and correlated climatic conditions during May and July affect populations regionally and influence the density-dependent transmission of the gastrointestinal nematode Trichostrongylus tenuis, a parasite that reduces grouse fecundity. This in turn forces grouse populations into synchrony. We conclude that specific climatic events may lead to outbreaks of infectious diseases or pests that may cause dramatic, synchronized changes in the abundance of their hosts.

Sacred Cows and Sympathetic Squirrels: The Importance of Biological Diversity to Human Health

Dobson and colleagues describe how some host species act to reduce the risk of transmission of virulent zoonotic pathogens to humans.

Peak shift and epidemiology in a seasonal host–nematode system

Insight into the dynamics of parasite–host relationships of higher vertebrates requires an understanding of two important features: the nature of transmission and the development of acquired immunity in the host. A dominant hypothesis proposes that acquired immunity develops with the cumulative exposure to infection, and consequently predicts a negative relationship between peak intensity of infection and host age at this peak. Although previous studies have found evidence to support this hypothesis through between-population comparisons, these results are confounded by spatial effects. In this study, we examined the dynamics of infection of the nematode Trichostrongylus retortaeformis within a natural population of rabbits sampled monthly for 26 years. The rabbit age structure was reconstructed using body mass as a proxy for age, and the host age–parasite intensity relationship was examined for each rabbit cohort born from February to August. The age–intensity curves exhibited a typical concave shape, and a significant negative relationship was found between peak intensity of infection and host age at this peak. Adult females showed a distinct periparturient rise in T. retortaeformis infection, with higher intensities in breeding adult females than adult males and non-breeding females. These findings are consistent with the hypothesis of an acquired immune response of the host to a parasite infection, supporting the principle that acquired immunity can be modelled using the cumulative exposure to infection. These findings also show that seasonality can be an important driver of host–parasite interactions.

Localized deer absence leads to tick amplification

Deer support high tick intensities, perpetuating tick populations, but they do not support tick-borne pathogen transmission, so are dilution hosts. We test the hypothesis that absence of deer (loss of a dilution host) will result in either an increase or a reduction in tick density, and that the outcome is scale dependent. We use a complementary methodological approach starting with meta-analysis, followed up by a field experiment. Meta-analysis indicated that larger deer exclosures reduce questing (host-seeking) tick density, but as the exclosure becomes smaller (<2.5 ha) the questing tick density is increased (amplified). To determine the consequences for tick-borne pathogen transmission we carried out a field experiment, comparing the intensity of ticks that fed on hosts competent for tickborne pathogen transmission (rodents) in two small (<1 ha) deer exclosures and their replicated controls. Intensity of larval ticks on rodents was not significantly different between treatments, but nymph intensity, the tick stage responsible for tick-borne encephalitis (TBE) transmission, was higher in deer exclosures. TBE seropositive rodents were found in a deer exclosure but not in the controls. We propose that localized absence of deer (loss of a dilution host) increases tick feeding on rodents, leading to the potential for tick-borne disease hotspots.

Climate disruption and parasite-host dynamics: patterns and processes associated with warming and the frequency of extreme climatic events

Levels of parasitism and the dynamics of helminth systems is subject to the impact of environmental conditions such that we may expect long term increases in temperature will increase the force of infection and the parasites basic reproduction number, R0. We postulate that an increase in the force of infection will only lead to an increase in mean intensity of adults when adult parasite mortality is not determined by acquired immunity. Preliminary examination of long term trends of parasites of rabbits and grouse confirm these predictions. Parasite development rate increases with temperature and while laboratory studies indicate this is linear some recent studies indicate that this may be non-linear and would have an important impact on R0. Warming would also reduce the selective pressure for the development of arrestment and this would increase R0 so that in systems like the grouse and Trichostrongylus tenuis this would increase the instability and lead to larger disease outbreaks. Extreme climatic events that act across populations appear important in synchronizing transmission and disease outbreaks, so it is speculated that climate disruption will lead to increased frequency and intensity of disease outbreaks in parasite populations not regulated by acquired immunity.

Variation in host susceptibility and infectiousness generated by co-infection: the myxoma–Trichostrongylus retortaeformis case in wild rabbits

One of the conditions that can affect host susceptibility and parasite transmission is the occurrence of concomitant infections. Parasites interact directly or indirectly within an individual host and often these interactions are modulated by the host immune response. We used a free-living rabbit population co-infected with the nematode Trichostrongylus retortaeformis, which appears to stimulate an acquired immune response, and the immunosuppressive poxvirus myxoma. Modelling was used to examine how myxoma infection alters the immune-mediated establishment and death/expulsion of T. retortaeformis, and consequently affects parasite intensity and duration of the infection. Simulations were based on the general TH1–TH2 immunological paradigm that proposes the polarization of the host immune response towards one of the two subsets of T helper cells. Our findings suggest that myxoma infections contribute to alter host susceptibility to the nematode, as co-infected rabbits showed higher worm intensity compared with virus negative hosts. Results also suggest that myxoma disrupts the ability of the host to clear T. retortaeformis as worm intensities were consistently high and remained high in old rabbits. However, the co-infection model has to include some immune-mediated nematode regulation to be consistent with field data, indicating that the TH1–TH2 dichotomy is not complete. We conclude that seasonal myxoma outbreaks enhance host susceptibility to the nematode and generate highly infected hosts that remain infectious for a longer time. Finally, the virus–nematode co-infection increases heterogeneities among individuals and potentially has a large effect on parasite transmission.

Evolutionary history and attenuation of myxoma virus on two continents.

The attenuation of myxoma virus (MYXV) following its introduction as a biological control into the European rabbit populations of Australia and Europe is the canonical study of the evolution of virulence. However, the evolutionary genetics of this profound change in host-pathogen relationship is unknown. We describe the genome-scale evolution of MYXV covering a range of virulence grades sampled over 49 years from the parallel Australian and European epidemics, including the high-virulence progenitor strains released in the early 1950s. MYXV evolved rapidly over the sampling period, exhibiting one of the highest nucleotide substitution rates ever reported for a double-stranded DNA virus, and indicative of a relatively high mutation rate and/or a continually changing selective environment. Our comparative sequence data reveal that changes in virulence involved multiple genes, likely losses of gene function due to insertion-deletion events, and no mutations common to specific virulence grades. Hence, despite the similarity in selection pressures there are multiple genetic routes to attain either highly virulent or attenuated phenotypes in MYXV, resulting in convergence for phenotype but not genotype.

Hantavirus and arenavirus antibody prevalence in rodents and humans in Trentino, Northern Italy

The spatial and temporal distribution of hantavirus and arenavirus antibody-positive wild rodents in Trentino, Italy, was studied using immunofluorescence assays (IFA) in two long-term sites trapped in 2000-2003, and six other sites trapped in 2002. The overall hantavirus seroprevalence in the bank voles, Clethrionomys glareolus (n=229) screened for Puumala virus (PUUV) antibodies was 0.4%, and that for Apodemus flavicollis mice (n=1416) screened for Dobrava virus (DOBV) antibodies was 0.2%. Antibodies against lymphocytic choriomeningitis virus (LCMV) were found in 82 (5.6%) of the 1472 tested rodents; the seroprevalence being 6.1% in A. flavicollis (n=1181), 3.3% in C. glareolus (n=276), and 14.3% in Microtus arvalis (n=7). Of the serum samples of 488 forestry workers studied by IFA, 12 were LCMV-IgG positive (2.5%) and one DOBV-IgG positive (0.2%), however, the latter could not be confirmed DOBV-specific with a neutralization assay. Our results show a widespread distribution but low prevalence of DOBV in Trentino, and demonstrate that the arenavirus antibodies are a common finding in several other rodent species besides the house mouse.

Analysing noisy time-series: describing regional variation in the cyclic dynamics of red grouse

We develop a method for describing the periodicity of noisy ‘quasi–cyclic’ time–series based on integrals of their power spectra corresponding to different frequency intervals that we use to classify time–series as ‘strongly cycli’,‘weakly cycli’ or‘non–cycli’. We apply this analysis to over 300 time–series of shooting records of red grouse from 289 moors located in 20 regions of the UK. Time–series from 63 of these populations were not distinguishable from white noise, but significant evidence of cyclic behaviour in the 2–15 year range was detected in time–series from 183 other populations. Time–series from the remaining 43 populations, though distinguishable from white noise, did not exhibit consistently recognizable cyclic behaviour in the same period range. Cyclic populations exhibit an average periodicity of 8.3 years, but only 20% of these populations cycle with a period of four to six years. Geographically, grouse populations are remarkable more for their dynamic heterogeneity than for any observable regularity. The relationship between the location of populations and their dynamical behaviour is weak. The prevalence of cyclic time–series within a region did not significantly differ from the overall average value. Moor region explained 22% of the variation in periodicity, differing from the overall mean in three regions. Average periodicity increases significantly from 6.8 to 8.9 years from the most southerly to most northerly populations. However, latitude explains only 5.3% of the variation in periodicity of the cycles.

Genetic variation in resistance to mixed, predominantly Teladorsagia circumcincta nematode infections of sheep: from heritabilities to gene identification

In cool temperate areas, such as Scotland, sheep are infected by a variety of nematodes but the dominant nematode is Teladorsagia circumcincta. Resistant animals have one or more of the following features: fewer adult nematodes, more inhibited larvae, shorter adult nematodes and decreased production of nematode eggs. In lambs at the end of the first grazing season, the heritability of adult worm length is very strong, whereas the heritability of egg production is moderate. The heritability of worm number is low while there is no detectable genetic variation in the number of inhibited larvae. The major mechanisms underlying resistance to T. circumcincta appear to be the IgA mediated suppression of worm growth and the mast cell mediated regulation of worm number. Mast cell responses are slow to develop, possibly because they are responsible for protein loss and reduced growth of the host. Two genes have been repeatedly associated with resistance to T. Circumcincta: the MHC class II DRB1 locus on chromosome 20 and the interferon‐γ locus on chromosome 3. Although the causative mutations are still unknown both genes are plausible candidates.