Initiation of Batrachochytrium dendrobatidis infection in the absence of physical contact with infected hosts – a field study in a high altitude lake

Understanding transmission is a critical prerequisite for predicting disease dynamics and impacts on host populations. It is well established that Batrachochytrium dendrobatidis (Bd), the amphibian fungal pathogen responsible for chytridiomycosis, can be transmitted directly, through physical contact with an infected host. However, indirect pathways of transmission remain poorly investigated. We conducted a five‐week long field infection experiment at a high altitude mountain lake in the French Pyrenees to investigate Bd transmission pathways in larval midwife toads Alytes obstetricans. Uninfected naïve tadpoles were co‐housed either with infected tadpoles (direct and indirect transmission) or with uninfected ones (indirect transmission only). We found that physical contact with an infected host is not necessary for initial infection with Bd and that all tadpoles became infected after only four weeks. However, physical contact with infected tadpoles led to a faster spread within a tadpole group and resulted in higher Bd loads and subsequently higher mortality. Our findings clearly demonstrate that in A. obstetricans, Bd can quickly spread in a population even without physical contact. Our experiment therefore stresses the importance of indirect transmission of Bd zoospores in infected lakes for disease dynamics, especially when a reservoir species such as A. obstetricans is present.     

Demonstrating frequency-dependent transmission of sarcoptic mange in red foxes

Understanding the relationship between disease transmission and host density is essential for predicting disease spread and control. Using long-term data on sarcoptic mange in a red fox Vulpes vulpes population, we tested long-held assumptions of density- and frequency-dependent direct disease transmission. We also assessed the role of indirect transmission. Contrary to assumptions typical of epidemiological models, mange dynamics are better explained by frequency-dependent disease transmission than by density-dependent transmission in this canid. We found no support for indirect transmission. We present the first estimates of R₀ and age-specific transmission coefficients for mange in foxes. These parameters are important for managing this poorly understood but highly contagious and economically damaging disease.     

Multiple Transmission Pathways and Disease Dynamics in a Waterborne Pathogen Model

Multiple transmission pathways exist for many waterborne diseases, including cholera, Giardia, Cryptosporidium, and Campylobacter. Theoretical work exploring the effects of multiple transmission pathways on disease dynamics is incomplete. Here, we consider a simple ODE model that extends the classical SIR framework by adding a compartment (W) that tracks pathogen concentration in the water. Infected individuals shed pathogen into the water compartment, and new infections arise both through exposure to contaminated water, as well as by the classical SIR person–person transmission pathway. We compute the basic reproductive number (ℛ₀), epidemic growth rate, and final outbreak size for the resulting “SIWR” model, and examine how these fundamental quantities depend upon the transmission parameters for the different pathways. We prove that the endemic disease equilibrium for the SIWR model is globally stable. We identify the pathogen decay rate in the water compartment as a key parameter determining when the distinction between the different transmission routes in the SIWR model is important. When the decay rate is slow, using an SIR model rather than the SIWR model can lead to under-estimates of the basic reproductive number and over-estimates of the infectious period.     

Alternative Feeding Strategies and Potential Disease Transmission in Wisconsin White-Tailed Deer

ABSTRACT We conducted experimental feeding using 3 feeding methods (pile, spread, trough) and 2 quantities (rationed, ad libitum) of shelled corn to compare deer activity and behavior with control sites and evaluate potential direct and indirect transmission of infectious disease in white-tailed deer (Odocoileus virginianus) in central Wisconsin, USA. Deer use was higher at 2 of the feeding sites than at natural feeding areas (P ≤ 0.02). Deer spent a higher proportion of time (P < 0.01) feeding at pile (49%) and spread (61%) treatments than at natural feeding areas (36%). We found higher deer use for rationed than ad libitum feeding quantities and feeding intensity was greatest at rationed piles and lowest at ad libitum spreads. We also observed closer pairwise distances (≤0.3 m) among deer when corn was provided in a trough relative to spread (P=0.03). Supplemental feeding poses risks for both direct and indirect disease transmission due to higher deer concentration and more intensive use relative to control areas. Concentrated feeding and contact among deer at feeding sites can also increase risk for disease transmission. Our results indicated that restrictions on feeding quantity would not mitigate the potential for disease transmission. None of the feeding strategies we evaluated substantially reduced the potential risk for disease transmission and banning supplemental feeding to reduce transmission is warranted.     

Success,failure and ambiguity of the dilution effect among competitors

It remains challenging to predict variation in the magnitude of disease outbreaks. The dilution effect seeks to explain this variation by linking multiple host species to disease transmission. It predicts that disease risk increases for a focal host when host species diversity declines. However, when an increase in species diversity does not reduce disease, we are often unable to diagnose why. Here, we increase mechanistic and predictive clarity of the dilution effect with a general trait‐based model of disease transmission in multi‐host communities. Then, we parameterise and empirically test our model with a multi‐generational case study of planktonic disease. The model‐experiment combination shows that hosts that vary in competitive ability (R*) and potential to spread disease (R₀) can produce three qualitatively disparate outcomes of dilution on disease: the dilution effect can succeed, fail, or be ambiguous/irrelevant.     

The effect of transmission route on plant virus epidemic development and disease control

A model for indirect vector transmission and epidemic development of plant viruses is extended to consider direct transmission through vector mating. A basic reproduction number is derived which is the sum of the R₀ values specific for three transmission routes. We analyse the model to determine the effect of direct transmission on plant disease control directed against indirect transmission. Increasing the rate of horizontal sexual transmission means that vector control rate or indirect transmission rate must be increased/decreased substantially to maintain R₀ at a value less than 1. By contrast, proportionately increasing the probability of transovarial transmission has little effect. Expressions are derived for the steady-state values of the viruliferous vector population. There is clear advantage for an insect virus in indirect transmission to plants, especially where the sexual and transovarial transmission rates are low; however information on virulence-transmissibility relationships is required to explain the evolution of a plant virus from an insect virus.     

Hantavirus Transmission in Sylvan and Peridomestic Environments

We developed a compartmental model for hantavirus infection in deer mice (Peromyscus maniculatus) with the goal of comparing relative importance of direct and indirect transmission in sylvan and peridomestic environments. A direct transmission occurs when the infection is mediated by the contact of an infected and an uninfected mouse, while an indirect transmission occurs when the infection is mediated by the contact of an uninfected mouse with, for instance, infected soil. Based on population dynamics data and estimates of hantavirus decay in the two types of environments, our model predicts that direct transmission dominates in the sylvan environment, while both pathways are important in peridomestic environments. The model allows us to compute a basic reproduction number R ₀, which indicates whether the virus will be endemic or eradicated from the mouse population, in both an autonomous and a time-periodic model. Our analysis can be used to evaluate various eradication strategies.     

Global dynamics of cholera models with differential infectivity

A general compartmental model for cholera is formulated that incorporates two pathways of transmission, namely direct and indirect via contaminated water. Non-linear incidence, multiple stages of infection and multiple states of the pathogen are included, thus the model includes and extends cholera models in the literature. The model is analyzed by determining a basic reproduction number R₀ and proving, by using Lyapunov functions and a graph-theoretic result based on Kirchhoff’s Matrix Tree Theorem, that it determines a sharp threshold. If R₀?1, then cholera dies out; whereas if R₀>1, then the disease tends to a unique endemic equilibrium. When input and death are neglected, the model is used to determine a final size equation or inequality, and simulations illustrate how assumptions on cholera transmission affect the final size of an epidemic.     

Analytic approximation of spatial epidemic models of foot and mouth disease

The effect of spatial heterogeneity in epidemic models has improved with computational advances, yet far less progress has been made in developing analytical tools for understanding such systems. Here, we develop two classes of second-order moment closure methods for approximating the dynamics of a stochastic spatial model of the spread of foot and mouth disease. We consider the performance of such ‘pseudo-spatial’ models as a function of R₀, the locality in disease transmission, farm distribution and geographically-targeted control when an arbitrary number of spatial kernels are incorporated. One advantage of mapping complex spatial models onto simpler deterministic approximations lies in the ability to potentially obtain a better analytical understanding of disease dynamics and the effects of control. We exploit this tractability by deriving analytical results in the invasion stages of an FMD outbreak, highlighting key principles underlying epidemic spread on contact networks and the effect of spatial correlations.     

Tinea cruris in female prostitutes

Tinea cruris is a dermatophytosis that mainly affects males. Infections in females are rare, and there are no known data on the frequency of tinea cruris in female prostitutes. We describe seven female prostitutes with tinea cruris with on age range of between 19–34 years (mean 25.3). Each prostitute had a mean of 50 sexual partners per month. Four Trichophyton mentagrophytes (57.1%),2 T. rubrum (28.6%), and 1 Epidermophyton floccosum (14.3%) isolates were cultered. Tinea cruris transmission is mainly indirect, but direct contact may serve to transmit the disease in some cases, and the spread of active lesions in prostitutes through multiple contacts among with their clients is possible. This revised version was published online in June 2006 with corrections to the Cover Date.     

Anthropogenic disturbance and streams: land use and land‐use change affect stream ecosystems via multiple pathways

1. Ecosystems are strongly influenced by land use practices. However, identifying the mechanisms behind these influences is complicated by the many potential pathways (often indirect) between land use and ecosystems and by the long‐lasting effects of past land use. To support ecosystem restoration and conservation efforts, we need to better understand these indirect and lasting effects. 2. We constructed structural equation models (SEM) to evaluate the direct and indirect effects of contemporary (2002) land use (agriculture and development) and change in land use from 1952 to 2002 on present‐day streams (n = 190) in Maryland, U.S.A. Additional variables examined included site location, system size, altitude, per cent sand in soils, riparian condition, habitat quality, stream water NO₃‐N and benthic macroinvertebrate and fish measures of stream condition. Our first SEM (2002 Land Use) included the proportions of contemporary agriculture and development in catchments in the model. The second SEM (Land Use Change) included five measures of land use change (proportion agricultural in both times, developed in both times, agricultural in 1952 and developed in 2002, forested in 1952 and developed in 2002 and agricultural in 1952 and forested in 2002). 3. The data set fit both SEMs well. The 2002 Land Use model explained 71% of variation in NO₃‐N and 55%, 42% and 38% of variation in riffle quality, macroinvertebrate condition and fish condition, respectively. The Land Use Change model explained similar amounts of variation in NO₃‐N (R² = 0.72), riffle quality (R² = 0.57) and macroinvertebrate condition (R² = 0.44) but slightly more variation in fish condition (R² = 0.43). 4. Both models identified pathways through which landscape variables affect stream responses, including negative direct effects of latitude on macroinvertebrate and fish conditions and positive direct and indirect effects of altitude on NO₃‐N, riffle quality and macroinvertebrate and fish conditions. The 2002 Land Use model showed contemporary development and agriculture had positive total effects on NO₃‐N (both through direct pathways); contemporary development had negative effects on macroinvertebrate condition. The Land Use Change model showed that contemporary developed land that was forested in 1952 had no effects on NO₃‐N; current developed land that was developed or agricultural in 1952 showed positive effects on NO₃‐N. Forests that were agricultural in 1952 had negative effects on NO₃‐N, suggesting reduced NO₃‐N export with reforestation. The Land Use Change model also showed negative total effects of all types of contemporary developed land (developed, agricultural or forested in 1952) on benthic condition. Developed land that was forested in 1952 had negative effects on fish condition. Forest sites that were agricultural in 1952 had negative effects on fish and macroinvertebrate conditions, suggesting a long‐term imprint of abandoned agriculture in stream communities. 5. Our analyses (i) identified multiple indirect effects of contemporary land use on streams, (ii) showed that current land uses with different land use histories can exhibit different effects on streams and (iii) demonstrated an imprint of land use lasting >50 years. Knowledge of these indirect and long‐term effects of land use will help to conserve and restore streams.     

Spatial environmental complexity mediates sexual conflict and sexual selection in Drosophila melanogaster

Sexual selection is an important agent of evolutionary change, but the strength and direction of selection often vary over space and time. One potential source of heterogeneity may lie in the opportunity for male–male and/or male–female interactions imposed by the spatial environment. It has been suggested that increased spatial complexity permits sexual selection to act in a complementary fashion with natural selection (hastening the loss of deleterious alleles and/or promoting the spread of beneficial alleles) via two (not mutually exclusive) pathways. In the first scenario, sexual selection potentially acts more strongly on males in complex environments, allowing males of greater genetic “quality” a greater chance of outcompeting rivals, with benefits manifested indirectly in offspring. In the second scenario, increased spatial complexity reduces opportunities for males to antagonistically harm females, allowing females (especially those of greater potential fecundities) to achieve greater reproductive success (direct fitness benefits). Here, using Drosophila melanogaster, we explore the importance of these mechanisms by measuring direct and indirect fitness of females housed in simple vial environments or in vials in which spatial complexity has been increased. We find strong evidence in favor of the female conflict‐mediated pathway as individuals in complex environments remated less frequently and produced more offspring than those housed in a simpler spatial environment, but no difference in the fitness of sons or daughters. We discuss these results in the context of other recent studies and what they mean for our understanding of how sexual selection operates.     

Disease risk and inter‐institutional transfer of specimens in cooperative breeding programs: Herpes and the elephant species survival plans

Managers of cooperative breeding programs and re‐introduction projects are increasingly concerned with the risk of disease transmission when specimens are transferred among facilities or between facilities and the natural environment. We used data maintained in North American studbooks to estimate the potential risks of disease transmission by direct and indirect contact of specimens in the American Zoo and Aquarium Association’s Elephant Species Survival Plan. Histological evidence for a novel herpesvirus disease transmitted between and within elephant species housed in North American facilities prompted an examination of the scope of possible transmission routes within the captive population. We found that, compared with other species managed through Species Survival Plans, elephants experience relatively few transfers between zoos. Nevertheless, the number of direct contacts with other elephants born during the study period of 1983–1996 (excluding stillbirths) was much higher than we had anticipated (μ = 25 ± 27; N = 59) and the number of potential indirect contacts was surprisingly large (μ = 143 ± 92; N = 59). Although these high rates of potential contacts complicate exact identification of infection pathways for herpesvirus, we were able to propose potential routes of transmission for the histologically identified cases. Furthermore, the extraction of data from studbooks allowed us to readily identify other specimens that did not succumb to the disease despite similar exposure. Moreover, we were able to identify other possible cases to recommend for histological examination. Herein we reveal the possibilities of multiple disease transmission pathways and demonstrate how complex the patterns of transmission can be, confounded by the unknown latency of this novel herpesvirus. This emphasizes the need for zoo veterinarians and cooperative breeding programs to consider the full potential for disease transmission associated with each and every inter‐zoo transfer of specimens. Zoo Biol 20:89–101, 2001. © 2001 Wiley‐Liss, Inc.     

The direct and indirect effects of fire on the assembly of insect herbivore communities: examples from the Florida scrub habitat

Disturbance is a major source of spatial and temporal heterogeneity. In fire-maintained systems, disturbance by fire is often used as a management tool to increase biological diversity, restore degraded habitats, and reduce pest outbreaks. Much attention has been given to how plant communities recover from fire, but relatively few studies have examined post-fire responses of higher order species, such as insect herbivores. Because dynamic feedbacks occur between plants and their consumers, which can in turn influence the response of the entire ecosystem, incorporating higher trophic level responses into our understanding of the effects of fire is essential. In this study, we used structural equation modeling (SEM) to tease apart the direct and indirect effects of fire on insect herbivore assemblages found on three common oak species in the Florida scrub (Quercus inopina, Q. chapmanii, and Q. geminata). We investigated how fire affected herbivore abundance, richness, and community composition both directly and indirectly through environmental heterogeneity at different spatial scales (e.g., leaf quality, plant architecture, and habitat structure). We also investigated how seasonality and landscape heterogeneity influenced post-fire responses of insect herbivores and whether fire effects on herbivore assemblages varied among different host plants. Our general findings were that fire effects were (1) largely indirect, mediated through habitat structure (although direct fire effects were observed on Q. inopina herbivores), (2) non-linear through time due to self-thinning processes occurring in the scrub habitat, and (3) varied according to herbivore assemblage as a result of differences in the composition of species in each herbivore community. To the best of our knowledge, this is the first comprehensive study to examine how fire influences the assembly of insect herbivore communities through both direct and indirect pathways and at multiple spatial scales.     

Differential impacts of habitat heterogeneity on male and female connectivity in a spatially structured pest system

In a previous study, a model of landscape heterogeneity was developed and applied to a spatially structured wild rabbit (Oryctolagus cuniculus) population. That study showed clearly the influence of resource heterogeneity on connectivity levels. The simulation study was based on female movements and used population genetic validation data appropriate for a female study. Most models assume that males and females will exhibit similar patterns, although this has rarely been tested. In the current study we extend the analysis to consider differences between female and male connectivity in the same spatially structured pest system. Amplified fragment length polymorphism (AFLP) markers were screened on the same samples used previously for mtDNA analysis. The mtDNA data were used to validate female results, and AFLP data were used to validate combined male and female results. Connectivity patterns from the two simulations (female, and combined male and female) connectivity patterns showed no association. However, each was concordant with appropriate validation data, showing highly significant associations between pairwise population connectivity and the genetic data. A relative connectivity metric for the combined simulation was regressed against the mean of pairwise Φ_ST values, with almost 70% of the variation explained by a linear model. Demonstrating differential effects of habitat heterogeneity on male and female connectivity provides further evidence that spatial resource heterogeneity impacts on connectivity. Understanding differences in population connectivity will allow improved predictions of disease spread, local extinctions and recolonizations. Furthermore, modelling such differences in pest systems will allow management plans to be better targeted, for example by strategically introducing diseases for control purposes into populations which exhibit high male connectivity to aid spread, but low female connectivity to inhibit recolonization potential after control.     

Plant intraspecific functional trait variation is related to within‐habitat heterogeneity and genetic diversity in Trifolium montanum L.

Intraspecific trait variation (ITV), based on available genetic diversity, is one of the major means plant populations can respond to environmental variability. The study of functional trait variation and diversity has become popular in ecological research, for example, as a proxy for plant performance influencing fitness. Up to now, it is unclear which aspects of intraspecific functional trait variation (iFD_CV) can be attributed to the environment or genetics under natural conditions. Here, we examined 260 individuals from 13 locations of the rare (semi‐)dry calcareous grassland species Trifolium montanum L. in terms of iFD_CV, within‐habitat heterogeneity, and genetic diversity. The iFD_CV was assessed by measuring functional traits (releasing height, biomass, leaf area, specific leaf area, leaf dry matter content, F_v/F_m, performance index, stomatal pore surface, and stomatal pore area index). Abiotic within‐habitat heterogeneity was derived from altitude, slope exposure, slope, leaf area index, soil depth, and further soil factors. Based on microsatellites, we calculated expected heterozygosity (H_e) because it best‐explained, among other indices, iFD_CV. We performed multiple linear regression models quantifying relationships among iFD_CV, abiotic within‐habitat heterogeneity and genetic diversity, and also between separate functional traits and abiotic within‐habitat heterogeneity or genetic diversity. We found that abiotic within‐habitat heterogeneity influenced iFD_CV twice as strong compared to genetic diversity. Both aspects together explained 77% of variation in iFD_CV ( = .77, F_{2, 10} = 21.66, p < .001). The majority of functional traits (releasing height, biomass, specific leaf area, leaf dry matter content, F_v/F_m, and performance index) were related to abiotic habitat conditions indicating responses to environmental heterogeneity. In contrast, only morphology‐related functional traits (releasing height, biomass, and leaf area) were related to genetics. Our results suggest that both within‐habitat heterogeneity and genetic diversity affect iFD_CV and are thus crucial to consider when aiming to understand or predict changes of plant species performance under changing environmental conditions.     

Soil resource availability is much more important than soil resource heterogeneity in determining the species diversity and abundance of karst plant communities

Resource availability and heterogeneity are recognized as two essential environmental aspects to determine species diversity and community abundance. However, how soil resource availability and heterogeneity determine species diversity and community abundance in highly heterogeneous and most fragile karst landscapes is largely unknown. We examined the effects of soil resource availability and heterogeneity on plant community composition and quantified their relative contribution by variation partitioning. Then, a structural equation model (SEM) was used to further disentangle the multiple direct and indirect effects of soil resource availability on plant community composition. Species diversity was significantly influenced by the soil resource availability in shrubland and woodland but not by the heterogeneity in woodland. Abundance was significantly affected by both soil resource availability and heterogeneity, whereas variation partitioning results showed that soil resource availability explained the majority of the variance in abundance, and the contribution of soil resource heterogeneity was marginal. These results indicated that soil resource availability plays a more important role in determining karst plant community composition than soil resource heterogeneity. Our SEMs further found that the multiple direct and indirect processes of soil resource availability in determining karst species diversity and abundance were different in different vegetation types. Soil resource availability and heterogeneity both played a certain role in determining karst plant community composition, while the importance of soil resource availability far exceeded soil resource heterogeneity. We propose that steering community restoration and reconstruction should be highly dependent on soil resource availability, and multiple direct and indirect pathways of soil resource availability for structuring karst plant communities need to be taken into account.     

A dynamic model of motor basal ganglia functions

 Fast aiming movements were measured in a choice reaction paradigm in a healthy control group and in Parkinsonian patients. The patients were tested without (‘off ’) and with 3,4-dihydroxyphenylalanine (‘on’) (L-dopa) medication. The movement trajectories were used to estimate the parameters of a dynamic linear model. The model is based on the functional structure of the basal ganglia-thalamocortical circuit with direct and indirect pathways linking the putamen to the basal ganglia output nuclei (Albin et al. 1989). The output of the circuit is connected to a model for the motor neuron-musculo-skeletal system. The gain k _d for the direct pathway and the gain k _i for the indirect pathway were estimated. They were found to be significantly decreased for Parkinsonian patients in ‘off ’ compared with the control group. L-dopa therapy in Parkinsonian patients increased the gains of the direct and the indirect pathway almost to normal values which implies that the long-term dopamine level in the striatum was excitatory for the direct and for the indirect pathway. This result is restricted to movements of correct size. For movements of diminished size, which are typical for Parkinsonian patients, the model predicts that the dopamine level in the striatum is excitatory for the direct pathway but inhibitory for the indirect pathway. The simulated values for neuronal activities are in agreement with expected values according to the experimental data. The proposed model of the ‘motor’ basal ganglia thalamocortical circuit implies that information about biomechanical properties of the musculo-skeletal system is stored in the ‘motor’ basal ganglia-thalamocortical circuit, and that the basal ganglia are involved in computation of the desired movement amplitude. Received: 24 April 1996/Accepted in revised form: 25 February 1997     

N2-Fixing Red Alder Indirectly Accelerates Ecosystem Nitrogen Cycling

Symbiotic N₂-fixing tree species can accelerate ecosystem N dynamics through decomposition feedbacks via both direct and indirect pathways. Direct pathways include the production of readily decomposed leaf litter and increased N supply to decomposers, whereas indirect pathways include increased tissue N and altered detrital dynamics of non-fixing vegetation. To evaluate the relative importance of direct and indirect pathways, we compared 3-year decomposition and N dynamics of N₂-fixing red alder leaf litter (2.34% N) to both low-N (0.68% N) and high-N (1.21% N) litter of non-fixing Douglas-fir, and decomposed each litter source in four forests dominated by either red alder or Douglas-fir. We also used experimental N fertilization of decomposition plots to assess elevated N availability as a potential mechanism of N₂-fixer effects on litter mass loss and N dynamics. Direct effects of N₂-fixing red alder on decomposition occurred primarily as faster N release from red alder than Douglas-fir litter. Direct increases in N supply to decomposers via experimental N fertilization did not stimulate decomposition of either species litter. Fixed N indirectly influenced detrital dynamics by increasing Douglas-fir tissue and litter N concentrations, which accelerated litter N release without accelerating mass loss. By increasing soil N, tissue N, and the rate of N release from litter of non-fixers, we conclude that N₂-fixing vegetation can indirectly foster plant–soil feedbacks that contribute to the persistence of elevated N availability in terrestrial ecosystems.     

Disease spread in age structured populations with maternal age effects

Fundamental ecological processes, such as extrinsic mortality, determine population age structure. This influences disease spread when individuals of different ages differ in susceptibility or when maternal age determines offspring susceptibility. We show that Daphnia magna offspring born to young mothers are more susceptible than those born to older mothers, and consider this alongside previous observations that susceptibility declines with age in this system. We used a susceptible‐infected compartmental model to investigate how age‐specific susceptibility and maternal age effects on offspring susceptibility interact with demographic factors affecting disease spread. Our results show a scenario where an increase in extrinsic mortality drives an increase in transmission potential. Thus, we identify a realistic context in which age effects and maternal effects produce conditions favouring disease transmission.