Threshold Host Density Research Articles

Stochasticity and Infectious Disease Dynamics: Density and Weather Effects on a Fungal Insect Pathogen.

In deterministic models of epidemics, there is a host abundance threshold above which the introduction of a few infected individuals leads to a severe epidemic. Studies of weather-driven animal pathogens often assume that abundance thresholds will be overwhelmed by weather-driven stochasticity, but tests of this assumption are lacking. We collected observational and experimental data for a fungal pathogen, Entomophaga maimaiga, that infects the gypsy moth, Lymantria dispar. We used an advanced statistical-computing algorithm to fit mechanistic models to our data, such that different models made different assumptions about the effects of host density and weather on E. maimaiga epizootics (epidemics in animals). We then used Akaike information criterion analysis to choose the best model. In the best model, epizootics are driven by a combination of weather and host density, and the model does an excellent job of explaining the data, whereas models that allow only for weather effects or only for density-dependent effects do a poor job of explaining the data. Density-dependent transmission in our best model produces a host density threshold, but this threshold is strongly blurred by the stochastic effects of weather. Our work shows that host-abundance thresholds may be important even if weather strongly affects transmission, suggesting that epidemiological models that allow for weather have an important role to play in understanding animal pathogens. The success of our model means that it could be useful for managing the gypsy moth, an important pest of hardwood forests in North America.

Experimental evidence of a pathogen invasion threshold.

Host density thresholds to pathogen invasion separate regions of parameter space corresponding to endemic and disease-free states. The host density threshold is a central concept in theoretical epidemiology and a common target of human and wildlife disease control programmes, but there is mixed evidence supporting the existence of thresholds, especially in wildlife populations or for pathogens with complex transmission modes (e.g. environmental transmission). Here, we demonstrate the existence of a host density threshold for an environmentally transmitted pathogen by combining an epidemiological model with a microcosm experiment. Experimental epidemics consisted of replicate populations of naive crustacean zooplankton (Daphnia dentifera) hosts across a range of host densities (20–640 hosts l−1) that were exposed to an environmentally transmitted fungal pathogen (Metschnikowia bicuspidata). Epidemiological model simulations, parametrized independently of the experiment, qualitatively predicted experimental pathogen invasion thresholds. Variability in parameter estimates did not strongly influence outcomes, though systematic changes to key parameters have the potential to shift pathogen invasion thresholds. In summary, we provide one of the first clear experimental demonstrations of pathogen invasion thresholds in a replicated experimental system, and provide evidence that such thresholds may be predictable using independently constructed epidemiological models.

Paradigms for parasite conservation.

Parasitic species, which depend directly on host species for their survival, represent a major regulatory force in ecosystems and a significant component of Earth's biodiversity. Yet the negative impacts of parasites observed at the host level have motivated a conservation paradigm of eradication, moving us farther from attainment of taxonomically unbiased conservation goals. Despite a growing body of literature highlighting the importance of parasite-inclusive conservation, most parasite species remain understudied, underfunded, and underappreciated. We argue the protection of parasitic biodiversity requires a paradigm shift in the perception and valuation of their role as consumer species, similar to that of apex predators in the mid-20th century. Beyond recognizing parasites as vital trophic regulators, existing tools available to conservation practitioners should explicitly account for the unique threats facing dependent species. We built upon concepts from epidemiology and economics (e.g., host-density threshold and cost-benefit analysis) to devise novel metrics of margin of error and minimum investment for parasite conservation. We define margin of error as the risk of accidental host extinction from misestimating equilibrium population sizes and predicted oscillations, while minimum investment represents the cost associated with conserving the additional hosts required to maintain viable parasite populations. This framework will aid in the identification of readily conserved parasites that present minimal health risks. To establish parasite conservation, we propose an extension of population viability analysis for host-parasite assemblages to assess extinction risk. In the direst cases, ex situ breeding programs for parasites should be evaluated to maximize success without undermining host protection. Though parasitic species pose a considerable conservation challenge, adaptations to conservation tools will help protect parasite biodiversity in the face of an uncertain environmental future.

Density thresholds for Mopeia virus invasion and persistence in its host Mastomys natalensis

Well-established theoretical models predict host density thresholds for invasion and persistence of parasites with a density-dependent transmission. Studying such thresholds in reality, however, is not obvious because it requires long-term data for several fluctuating populations of different size. We developed a spatially explicit and individual-based SEIR model of Mopeia virus in multimammate mice Mastomys natalensis. This is an interesting model system for studying abundance thresholds because the host is the most common African rodent, populations fluctuate considerably and the virus is closely related to Lassa virus but non-pathogenic to humans so can be studied safely in the field. The simulations show that, while host density clearly is important, sharp thresholds are only to be expected for persistence (and not for invasion), since at short time-spans (as during invasion), stochasticity is determining. Besides host density, also the spatial extent of the host population is important. We observe the repeated local occurrence of herd immunity, leading to a decrease in transmission of the virus, while even a limited amount of dispersal can have a strong influence in spreading and re-igniting the transmission. The model is most sensitive to the duration of the infectious stage, the size of the home range and the transmission coefficient, so these are important factors to determine experimentally in the future.

Critical thresholds in sea lice epidemics: evidence, sensitivity and subcritical estimation

Host density thresholds are a fundamental component of the population dynamics of pathogens, but empirical evidence and estimates are lacking. We studied host density thresholds in the dynamics of ectoparasitic sea lice (Lepeophtheirus salmonis) on salmon farms. Empirical examples include a 1994 epidemic in Atlantic Canada and a 2001 epidemic in Pacific Canada. A mathematical model suggests dynamics of lice are governed by a stable endemic equilibrium until the critical host density threshold drops owing to environmental change, or is exceeded by stocking, causing epidemics that require rapid harvest or treatment. Sensitivity analysis of the critical threshold suggests variation in dependence on biotic parameters and high sensitivity to temperature and salinity. We provide a method for estimating the critical threshold from parasite abundances at subcritical host densities and estimate the critical threshold and transmission coefficient for the two epidemics. Host density thresholds may be a fundamental component of disease dynamics in coastal seas where salmon farming occurs.

Predicting outbreaks of a climate-driven coral disease in the Great Barrier Reef

Links between anomalously high sea temperatures and outbreaks of coral diseases known as White Syndromes (WS) represent a threat to Indo-Pacific reefs that is expected to escalate in a changing climate. Further advances in understanding disease aetiologies, determining the relative importance of potential risk factors for outbreaks and in trialing management actions are hampered by not knowing where or when outbreaks will occur. Here, we develop a tool to target research and monitoring of WS outbreaks in the Great Barrier Reef (GBR). The tool is based on an empirical regression model and takes the form of user-friendly interactive ~1.5-km resolution maps. The maps denote locations where long-term monitoring suggests that coral cover exceeds 26% and summer temperature stress (measured by a temperature metric termed the mean positive summer anomaly) is equal to or exceeds that experienced at sites in 2002 where the only severe WS outbreaks documented on the GBR to date were observed. No WS outbreaks were subsequently documented at 45 routinely surveyed sites from 2003 to 2008, and model hindcasts for this period indicate that outbreak likelihood was never high. In 2009, the model indicated that outbreak likelihood was high at north-central GBR sites. The results of the regression model and targeted surveys in 2009 revealed that the threshold host density for an outbreak decreases as thermal stress increases, suggesting that bleaching could be a more important precursor to WS outbreaks than previously anticipated, given that bleaching was severe at outbreak sites in 2002 but not at any of the surveyed sites in 2009. The iterative approach used here has led to an improved understanding of disease causation, will facilitate management responses and can be applied to other coral diseases and/or other regions.

Host density thresholds and disease control for fisheries and aquaculture

The outbreak, persistence, and eradication of infectious diseases often depend on the density of hosts. In coastal seas, many fisheries are fully or over-exploited; meanwhile, farmed popu- lations are increasing rapidly with aquaculture growth. Marine aquaculture facilities are typically open to the surrounding ecosystem and, therefore, wild and farmed populations are connected by their shared parasites. At the core of epidemiological theory are host density thresholds, above which diseases can persist or invade and below which diseases can be eradicated. Host density thresholds in aquaculture-fishery interactions likely function at regional scales that encompass multiple farms, which are connected by pathogen dispersal and the movement of wild hosts. Sudden outbreaks of parasitic copepods in wild-farmed salmon systems may be linked to aquaculture growth exceeding host density thresholds. Abiotic (e.g. temperature and salinity), management (e.g. husbandry and farm siting), and biotic factors (e.g. migrations of wild hosts) likely affect threshold values. A con- nected wild-farmed host population can exceed a host density threshold due to an influx of wild hosts via migration, increases in aquaculture production, or environmental change such as climate warm- ing. Coastal management and policy should heed the disease implications of climate warming, aqua- culture growth, and fisheries restoration that suggest increasing host densities and decreasing threshold values.

Host density thresholds and disease control for fisheries and aquaculture

Host density thresholds and disease control for fisheries and aquaculture

Testing a key assumption of host‐pathogen theory: density and disease transmission

Conventional disease theory suggests that extinction with density‐dependent transmission is unlikely as the threshold host density (KT) is greater than zero. Extinction may result if transmission is frequency dependent or the pathogen has an environmental reservoir. Given the importance of understanding how pathogens affect species richness and diversity there are few empirical tests of these conclusions. We used anAmbystoma tigrinum–Ambystoma tigrinumvirus (ATV) model system in the laboratory to examine disease transmission dynamics. SusceptibleA. tigrinumlarvae were exposed to three different densities and proportions of infected larvae for 24 h. We then housed susceptible hosts individually for 28 days and monitored them for infection. The density of infected hosts to which susceptible hosts were exposed was the best predictor of infection (p=0.037). There was no effect of host clutch on the probability of becoming infected (p=0.67). Larvae in the highest density treatments died sooner than larvae in lower density treatments (p<0.001). Asymptomatic but infected hosts shed sufficient virus into the water in a 24‐h period to infect susceptible hosts without any direct contact between individuals. ATV transmission was best described by a power function, leading to the prediction that extinction ofA. tigrinumas a result of this pathogen is unlikely. Indeed, field observations show that larval salamander populations that experience ATV‐driven epidemics may decrease, but not to extinction, and then recover. Disease is proposed as a possible explanation for the global decline of amphibians. Ranaviruses infect many amphibian populations, but based on our results may not be a general cause of declines to extinction. In contrast, frequency dependent transmission, environmental reservoirs and alternative hosts may be the most likely explanation for the enigmatic decline, at times to extinction, of some amphibian populations as a result of emerging infectious diseases, like the chytrid fungusBatrachochytrium dendrobatidis.

Seasonal, demographic and density‐related patterns of contact between Tasmanian devils (Sarcophilus harrisii): Implications for transmission of devil facial tumour disease

Abstract Devil facial tumour disease (DFTD), is an emerging infectious cancer thought to be spread by biting. It is causing ongoing, severe population decline of the Tasmanian devil (Sarcophilus harrisii), the largest surviving marsupial carnivore and there are concerns that DFTD may lead to extinction of the devil. Whether extinction is likely depends on contact rates and their relationship to host density. We investigated contact rates using two different datasets. The first consisted of field observations of contact and biting behaviour around prey carcasses and, the second was a 3‐year longitudinal series of injuries in a marked devil population. During feeding interactions at carcasses, contact rates were significantly positively associated with population density and subadults delivered more bites than adult males and females. Injuries from the marked devil population did not differ between adult males and females. In two of the three years, penetrating biting (resulting in injury) increased markedly during the mating season and was more frequent in adults than in subadults. Among injured devils with wounds penetrating the dermal layer, adults were more frequently bitten in the head (the location of primary tumours) in the mating season than in other seasons, and had more head bites than subadults. Our results suggest that the mating season may be the key period for disease transmission. If most penetrating bites occur during mating interactions, DFTD transmission is likely to be frequency dependent, which means that there would be no threshold host density for disease persistence, and disease‐induced extinction is possible.

JOINTLY‐DETERMINED ECOLOGICAL THRESHOLDS AND ECONOMIC TRADE‐OFFS IN WILDLIFE DISEASE MANAGEMENT

ABSTRACT. We investigate wildlife disease management, in a bioeconomic framework, when the wildlife host is valuable and disease transmission is density‐dependent. Disease prevalence is reduced in density‐dependent models whenever the population is harvested below a host‐density threshold a threshold population density below which disease prevalence declines and above which a disease becomes epidemic. In conventional models, the threshold is an exogenous function of disease parameters. We consider this case and find a steady state with positive disease prevalence to be optimal. Next, we consider a case in which disease dynamics are affected by both population controls and changes in human‐environmental interactions. The host‐density threshold is endogenous in this case. That is, the manager does not simply manage the population relative to the threshold, but rather manages both the population and the threshold. The optimal threshold depends on the economic and ecological trade‐offs arising from the jointly‐determined system. Accounting for this endogene‐ity can lead to reduced disease prevalence rates and higher population levels. Additionally, we show that ecological parameters that may be unimportant in conventional models that do not account for the endogeneity of the host‐density threshold are potentially important when host density threshold is recognized as endogenous.

A Simulation Model for Low-Pathogenicity Avian Influenza Viruses in Dabbling Ducks in Europe

Anseriformes are the reservoir of low-pathogenicity avian influenza viruses (LPAIV). Studies have shown a high LPAIV prevalence associated with low antibody detection in a wild duck population in northern European countries, whereas in winter areas (Mediterranean basin), low viral detection and high seroprevalence were observed. In order to gain insight into the role played by both population recruitment and migration on AIV persistence, an epidemiological model was developed. A susceptible, infectious and removed (immune or dead)-individuals model coupling population and infection dynamics was developed to simulate LPAIV circulation in dabbling ducks throughout the entire year. The transmission coefficient (beta) was calculated using the original dataset of published works, whereas dabbling duck demographic parameters were obtained from the literature. The estimated host density threshold for virus persistence is 380 susceptible individuals per day whereas the critical community size needed for maintaining the virus throughout the winter has been estimated to be about 1200 individuals. The model showed peaks of viral prevalence after nesting and during the moult period because of population recruitment and high host density, respectively. During the winter and spring periods, the viruses reach the minimal endemic level and local extinction is highly probable because of stochastic phenomena, respectively 80% and 90% of probabilities. The most sensitive parameters of the model are the recruitment rate of young susceptible animals and the duration of virus shedding.

Parasite establishment in host communities

AbstractMany pathogens and parasites attack multiple host species, so their ability to invade a host community can depend on host community composition. We present a graphical isocline framework for studying disease establishment in systems with two host species, based on treating host species as resources. The isocline approach provides a natural generalization to multi‐host systems of two related concepts in disease ecology – the basic reproductive rate of a parasite, and threshold host density. Qualitative isocline shape characterizes the threshold community configurations that permit parasite establishment. In general, isocline shape reflects the relative forces of inter‐ and intraspecific transmission of shared parasites. We discuss the qualitative implications of parasite isocline shape for issues of mounting concern in conservation ecology.

Non‐linear transmission and simple models for bovine tuberculosis

1. A new model is presented for a possum–tuberculosis (TB) system (Trichosurus vulpecula–Mycobacterium bovis) that is both realistic and parsimonious. The model includes a phenomenological treatment of heterogeneity of risk for susceptible hosts, similar to that used in insect host–parasitoid systems. 2. Parameter values for the model reflect current knowledge and differ significantly from those in other recent models of this system. Associated with these structural and parametric changes are substantially different predictions for the dynamics and control of TB in possums. 3. The model predictions include (i) only limited host suppression due to the disease (< 10%, cf. several earlier simple models for TB in both possums and badgers); (ii) asymptotically stable disease dynamics (cf. homogeneous‐mixing models that predict either extremely weak stability such that disease fails to recover when host density is temporarily reduced, or oscillatory behaviour and potential elimination of disease following such a perturbation); (iii) TB that is harder to control than in the homogeneous‐mixing model equivalents, in line with practical experience; and (iv) a threshold host density for disease elimination that differs substantially from the host equilibrium density in the presence of disease. 4. Homogeneous‐mixing models are unable to reproduce this behaviour, whatever parameter values are chosen. Heterogeneous‐mixing models with non‐linear transmission may therefore be worth consideration in other endemic wildlife disease systems, as is now commonplace for insect–parasitoid and insect–pathogen ones.

On the Capacity of Macroparasites to Control Insect Populations

A graphical model of the population dynamics of macroparasites and their hosts is developed. Three principal means by which the parasites can be regulated are considered: reduction in host density as a result of parasite-induced host mortality, reduction in host density as a result of parasite-induced host sterility, and competition among parasites within multiply-infected hosts. The means by which parasites are regulated has a major effect on the degree to which they can depress host population densities. In particular, a parasite that sterilizes its host is expected to reduce host density more than one that causes an equivalent decline in host fitness through increased mortality. A special case of the model is developed for herbivorous insects that, in the absence of parasites, are limited by larval food resources. Parasites that are regulated via parasite-induced host sterility will control the insect populations below the level set by larval resources if the threshold host density for the parasites (N(T)) is less than the ratio of carrying capacity to net reproductive rate of the insects (K/R). Data are presented showing that all three means of parasite regulation, but especially parasite-induced host sterility, can operate in Howardula aoronymphium, a nematode parasite of mycophagous Drosophila flies. Data from a field cage experiment show that, if these nematodes are regulated primarily via reductions in host density due to this sterility, the parameters N(T), K, and R are such that Howardula is likely to play an important role in controlling Drosophila populations. However, this conclusion must be tempered by the fact that these nematodes also cause increased host mortality and experience within-host competition, making the conditions for parasite control of the flies more stringent.

On the Capacity of Macroparasites to Control Insect Populations

A graphical model of the population dynamics of macroparasites and their hosts is developed. Three principal means by which the parasites can be regulated are considered: reduction in host density as a result of parasite‐induced host mortality, reduction in host density as a result of parasite‐induced host sterility, and competition among parasites within multiply‐infected hosts. The means by which parasites are regulated has a major effect on the degree to which they can depress host population densities. In particular, a parasite that sterilizes its host is expected to reduce host density more than one that causes an equivalent decline in host fitness through increased mortality. A special case of the model is developed for herbivorous insects that, in the absence of parasites, are limited by larval food resources. Parasites that are regulated via parasite‐induced host sterility will control the insect poppopulations below the level set by larval resources if the threshold host density for the parasites (NT) is less than the ratio of carrying capacity to net reproductive rate of the insects (K/R). Data are presented showing that all three means of parasite regulation, but especially parasite‐induced host sterility, can operate in Howardula aoronymphium, a nematode parasite of mycophagous Drosophila flies. Data from a field cage experiment show that, if these nematodes are regulated primarily via reductions in host density due to this sterility, the parameters NT, K, and R are such that Howardula is likely to play an important role in controlling Drosophila populations. However, this conclusion must be tempered by the fact that these nematodes also cause increased host mortality and experience within‐host competition, making the conditions for parasite control of the flies more stringent.

Modeling the Dynamics of Entomophaga maimaiga (Zygomycetes: Entomophthorales) Epizootics in Gypsy Moth (Lepidoptera: Lymantriidae) Populations

A virulent fungal pathogen, Entomophaga maimaiga Humber, Shimazu & Soper, was discovered in gypsy moth, Lymantria dispar (L.), populations across northeastern North America in 1989. It had never before been reported from North America, but many reports have documented the importance of this natural enemy in Japanese gypsy moth populations. We conducted experiments to estimate parameters for several components of the E. maimaiga/L. dispar system, and an object-oriented simulation model was used to evaluate the dynamics of this system. Studies conducted with a 1984 Japanese isolate of E. maimaiga formed the basis for this model. Successful infection by conidia required a median time of 8.69 h at 25°C. Data for period of lethal infection demonstrated that this pathogen cannot develop at 30°C, and that mortality is high across all instars. Transmission experiments using caged saplings in the field were used to estimate a value for the proportion of conidia that successfully reach hosts and cause infection. Experiments with the model demonstrated results consistent with the existence of a host density threshold below which the rapid increase in secondary infection characteristic of epizootics does not occur. Primary infections throughout the field season were important in producing an adequate level of secondary inoculum for development of epizootics. Instar-specific larval behaviors were hypothesized as resulting in differential instar exposure to primary inoculum; inclusion of behavior-specific coefficients resulted in disease phenology more similar to observed patterns in the field. The model was also successfully tested using weather data from sites and dates when epizootics caused by E. maimaiga were known either to occur or not to occur. Variability in weather conditions across a larger geographic area caused heterogeneity in development of epizootics.

Population Dynamics of Bacteriophage and Bacillus Subtilis in Soil

The dynamics of the interaction of populations of Bacillus subtilis and a temperate bacteriophage in soil microorganisms were examined. The purpose of the study was to investigate these dynamics in a structured habitat approaching that of their natural habitat in soil, in contrast to previous investigations in broth or chemostats. We addressed three main questions. What are the population dynamics of a phage—bacteria interaction in soil? What role might the heterogeneity of the soil play in shaping the interaction? Are the dynamics controlled more by the population biology of the phage or of the bacteria? The phage used was isolated from Arizona desert soil in which B. subtilis is common. Phage and bacteria were grown separately or together in sterile soil microcosms consisting of autoclaved soil rich in organic material. Densities of phage and bacteria were estimated through repeated sterile sampling of the microcosms by spreading precise dilutions of sampled soil suspensions onto plates of microbiological media. The plates for estimation of phage densities contained in addition a lawn of host bacteria. While the principal focus is on temperate phage ecology, the dynamics of a single example of interaction between B. subtilis and virulent phage is also presented. In all cases an initial epidemic of phage occurred, followed by stable equilibria lasting weeks to months. A threshold host density for phage outbreak occurs at °5 x 106 colony—forming units per gram of soil. At equilibrium the phage, both temperate and virulent, were much less abundant than the bacteria. The temperate phage did not depress the equilibrium host density, while the virulent phage lowered it by a factor of ten. The acidic soil of these experiments caused rapid and permanent inactivation of free phage, making the continuous interaction of phage and host essential for persistence of phage. Low levels of phage resistance (superimmunity or genetic) were typical of host populations. Most properties of the interaction between B. subtilis and phage in soil are quite different from those observed with chemostat populations of Escherichia coli and virulent phages. Potential doubling times and rates of increase in soil for phage and B. subtilis were calculated. At equilibrium, soil slows the interaction of phage and host relative to population growth in broth culture, and possibly also makes it heterogeneous in space and time. The life—history features of B. subtilis and temperate phage are considerably more complex than those of non—sporeforming bacteria and virulent phage. The biotic relationship of temperate phage and host may be distinct from predation or parasitism. Patterns in the ecology and evolution of temperate and virulent phage were explored, leading to the expectation that temperate forms will be more common among the phages of soil bacteria.

Effects of phosphorus limitation on the epidemiology of a chytrid phytoplankton parasite

SUMMARY 1. The effect of phosphorus limitation of the diatom Asterionella formosa Hass. on growth, survival and epidemic development of its fungal parasite Rhizophydium planktonicum Canter emend. was estimated, using measurements of production and infectivity of the zoospores of the chytrid grown on host cultures with different phosphorus‐limited growth rates.2. Phosphorus‐limited host cells were less susceptible to infection with zoospores of the parasite than non‐limited host cells.3. The sporangia on phosphorus‐limited algae produced substantially less zoospores, but the development time of these sporangia was only slightly reduced.4. As a result of these effects, Rhizophydium will reach lower growth rates at a given host density, and survival of the parasite will require higher host densities when Asterionella is phosphorus‐limited.5. The zoospore production remained high enough to enable the parasite to grow faster than the alga at sufficiently high host densities, both at limiting and non‐limiting phosphorus levels.6. In spite of the reduced growth rate of the parasite, phosphorus limitation of Asterionella was found to facilitate the development of a Rhizophydium epidemic. This was a consequence of the reduced algal growth rate at phosphorus limitation, which makes the host population more easily outgrown by the parasite.7. Phosphorus limitation of the host could reduce the threshold host density required for the development of an epidemic by a factor of 2.5.

Spatial and temporal dynamics of animals and the host-density threshold in epizootiology

The concept of a host-density threshold, commonly discussed in theoretical epidemiology and epizootiology, is based on simple theoretical models and several vague definitions. We computed a more complex model on a supercomputer to study the temporal and spatial dynamics of an insect population and its microsporidian disease. Results demonstrated that the threshold is sensitive to initial prevalence of the disease, intragenerational temporal dynamics, and spatial dynamics of the host. The threshold also depends on whether pathogen persistence, an increase in prevalence, an increase in density of infected hosts, or an epidemic is being predicted. To improve epizootiological theory, models with greater realism must be studied and the concept must include general temporal and spatial scales.