Seasonal host dynamics drive the timing of recurrent epidemics in a wildlife population (original) (raw)
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Seasonal host dynamics drive the timing of recurrent epidemics in a wildlife
2009
The seasonality of recurrent epidemics has been largely neglected, especially where patterns are not driven by forces external to the population. Here, we use data on cowpox virus in field voles to explore the seasonal patterns in wildlife (variable abundance) populations and compare these with patterns previously found in humans. Timing in our system was associated with both the number and the rate of recruitment of susceptible hosts. A plentiful and sustained supply of susceptible hosts throughout the summer gave rise to a steady rise in infected hosts and a late peak. A meagre supply more limited in time was often insufficient to sustain an increase in infected hosts, leading to an early peak followed by a decline. These seasonal patterns differed from those found in humans, but the underlying association found between the timing and the supply of susceptible hosts was similar to that in humans. We also combine our data with a model to explore these differences between humans and wildlife. Model results emphasize the importance of the interplay between seasonal infection and recruitment and suggest that our empirical patterns have a relevance extending beyond our own system.
Proceedings of The National Academy of Sciences, 2009
A key aim in epidemiology is to understand how pathogens spread within their host populations. Central to this is an elucidation of a pathogen's transmission dynamics. Mathematical models have generally assumed that either contact rate between hosts is linearly related to host density (density-dependent) or that contact rate is independent of density (frequency-dependent), but attempts to confirm either these or alternative transmission functions have been rare. Here, we fit infection equations to 6 years of data on cowpox virus infection (a zoonotic pathogen) for 4 natural populations to investigate which of these transmission functions is best supported by the data. We utilize a simple reformulation of the traditional transmission equations that greatly aids the estimation of the relationship between density and host contact rate. Our results provide support for an infection rate that is a saturating function of host density. Moreover, we find strong support for seasonality in both the transmission coefficient and the relationship between host contact rate and host density, probably reflecting seasonal variations in social behavior and/or host susceptibility to infection. We find, too, that the identification of an appropriate loss term is a key component in inferring the transmission mechanism. Our study illustrates how time series data of the hostpathogen dynamics, especially of the number of susceptible individuals, can greatly facilitate the fitting of mechanistic disease models.
Epidemiology and Infection, 2009
SUMMARYRecent studies have provided evidence that endemic pathogens may affect dynamics in animals. However, such studies have not typically considered that infected individuals might have a preceding underlying poor condition. We examined whether individuals in poor condition are more likely to become infected by an endemic pathogen, using as a system the dynamics of cowpox virus in field voles. With data from monthly sampled vole populations, a nested case-control study evaluated whether susceptible individuals with poorer condition had higher probabilities of contracting cowpox. The influence of condition was found to be considerable, especially for males. At times when a susceptible male with good body condition had a relatively low probability of becoming infected, a susceptible male with poor body condition was twice as likely to contract cowpox; if this male was also anaemic, the chances were almost quadrupled. We discuss the care needed when interpreting the findings of wild...
Disease effects on reproduction can cause population cycles in seasonal environments
Journal of Animal Ecology, 2008
1. Recent studies of rodent populations have demonstrated that certain parasites can cause juveniles to delay maturation until the next reproductive season. Furthermore, a variety of parasites may share the same host, and evidence is beginning to accumulate showing nonindependent effects of different infections. 2. We investigated the consequences for host population dynamics of a disease-induced period of no reproduction, and a chronic reduction in fecundity following recovery from infection (such as may be induced by secondary infections) using a modified SIR (susceptible, infected, recovered) model. We also included a seasonally varying birth rate as recent studies have demonstrated that seasonally varying parameters can have important effects on long-term host-parasite dynamics. We investigated the model predictions using parameters derived from five different cyclic rodent populations. 3. Delayed and reduced fecundity following recovery from infection have no effect on the ability of the disease to regulate the host population in the model as they have no effect on the basic reproductive rate. However, these factors can influence the long-term dynamics including whether or not they exhibit multiyear cycles. 4. The model predicts disease-induced multiyear cycles for a wide range of realistic parameter values. Host populations that recover relatively slowly following a disease-induced population crash are more likely to show multiyear cycles. Diseases for which the period of infection is brief, but full recovery of reproductive function is relatively slow, could generate large amplitude multiyear cycles of several years in length. Chronically reduced fecundity following recovery can also induce multiyear cycles, in support of previous theoretical studies. 5. When parameterized for cowpox virus in the cyclic field vole populations (Microtus agrestis) of Kielder Forest (northern England), the model predicts that the disease must chronically reduce host fecundity by more than 70%, following recovery from infection, for it to induce multiyear cycles. When the model predicts quasi-periodic multiyear cycles it also predicts that seroprevalence and the effective date of onset of the reproductive season are delayed density-dependent, two phenomena that have been recorded in the field.
Seasonality and the dynamics of infectious diseases
Ecology Letters, 2006
Seasonal variations in temperature, rainfall and resource availability are ubiquitous and can exert strong pressures on population dynamics. Infectious diseases provide some of the best-studied examples of the role of seasonality in shaping population fluctuations. In this paper, we review examples from human and wildlife disease systems to illustrate the challenges inherent in understanding the mechanisms and impacts of seasonal environmental drivers. Empirical evidence points to several biologically distinct mechanisms by which seasonality can impact host-pathogen interactions, including seasonal changes in host social behaviour and contact rates, variation in encounters with infective stages in the environment, annual pulses of host births and deaths and changes in host immune defences. Mathematical models and field observations show that the strength and mechanisms of seasonality can alter the spread and persistence of infectious diseases, and that population-level responses can range from simple annual cycles to more complex multiyear fluctuations. From an applied perspective, understanding the timing and causes of seasonality offers important insights into how parasite-host systems operate, how and when parasite control measures should be applied, and how disease risks will respond to anthropogenic climate change and altered patterns of seasonality. Finally, by focusing on well-studied examples of infectious diseases, we hope to highlight general insights that are relevant to other ecological interactions.
REVIEWS AND SYNTHESES Seasonality and the dynamics of infectious diseases
Seasonal variations in temperature, rainfall and resource availability are ubiquitous and can exert strong pressures on population dynamics. Infectious diseases provide some of the best-studied examples of the role of seasonality in shaping population fluctuations. In this paper, we review examples from human and wildlife disease systems to illustrate the challenges inherent in understanding the mechanisms and impacts of seasonal environmental drivers. Empirical evidence points to several biologically distinct mechanisms by which seasonality can impact host–pathogen interactions, including seasonal changes in host social behaviour and contact rates, variation in encounters with infective stages in the environment, annual pulses of host births and deaths and changes in host immune defences. Mathematical models and field observations show that the strength and mechanisms of seasonality can alter the spread and persistence of infectious diseases, and that population-level responses can...
Transmission dynamics of a zoonotic pathogen within and between wildlife host species
Proceedings of the Royal Society B: Biological Sciences, 1999
The transmission dynamics of the cowpox virus infection have been quanti¢ed in two mixed populations of bank voles (Clethrionomys glareolus) and wood mice (Apodemus sylvaticus), through analyses of detailed time-series of the numbers of susceptible, infectious and newly infected individuals. The cowpox virus is a zoonosis which circulates in these rodent hosts and has been shown to have an adverse e¡ect on reproductive output. The transmission dynamics within species is best described as frequency dependent rather than density dependent, contrary to the`mass action' assumption of most previous studies, both theoretical and empirical. Estimation of a transmission coe¤cient for each species in each population also allows annual and seasonal variations in transmission dynamics to be investigated through an analysis of regression residuals. Transmission between host species is found to be negligible despite their close cohabitation. The consequences of this for the combining ability of hosts as zoonotic reservoirs, and for apparent competition between hosts, are discussed.
Journal of Animal Ecology, 2008
1Cowpox 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.2The 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.3Individuals 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.4At the population level, survival rates also decreased with increasing cowpox prevalence, with lower survival rates in months of higher cowpox prevalence.5Simple 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 λ = 1·62 to 1·53 for populations with no cowpox infection compared with infected populations.6This 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.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.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.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.At the population level, survival rates also decreased with increasing cowpox prevalence, with lower survival rates in months of higher cowpox prevalence.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 λ = 1·62 to 1·53 for populations with no cowpox infection compared with infected populations.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.
Seasonal dynamics of recurrent epidemics
Nature, 2007
Seasonality is a driving force that has a major effect on the spatiotemporal dynamics of natural systems and their populations 1-5 . This is especially true for the transmission of common infectious diseases (such as influenza, measles, chickenpox and pertussis), and is of great relevance for host-parasite relationships in general 1-23 . Here we gain further insights into the nonlinear dynamics of recurrent diseases through the analysis of the classical seasonally forced SIR (susceptible, infectious or recovered) epidemic model 6,7 . Our analysis differs from other modelling studies in that the focus is more on post-epidemic dynamics than the outbreak itself. Despite the mathematical intractability of the forced SIR model, we identify a new threshold effect and give clear analytical conditions for predicting the occurrence of either a future epidemic outbreak, or a 'skip'-a year in which an epidemic fails to initiate. The threshold is determined by the population's susceptibility measured after the last outbreak and the rate at which new susceptible individuals are recruited into the population. Moreover, the time of occurrence (that is, the phase) of an outbreak proves to be a useful parameter that carries important epidemiological information. In forced systems, seasonal changes can prevent late-peaking diseases (that is, those having high phase) from spreading widely, thereby increasing population susceptibility, and controlling the triggering and intensity of future epidemics. These principles yield forecasting tools that should have relevance for the study of newly emerging and re-emerging diseases controlled by seasonal vectors.