Inconclusiveness of Chytridiomycosis as the Agent in Widespread Frog Declines

Abstract:  Although there is considerable evidence to support the hypothesis that the chytrid fungus Batrachochytrium dendrobatidis is the primary agent responsible for widespread declines in amphibian populations, particularly rainforest frog populations in Australia and Central America, I argue the case has not yet been made conclusively. Few specimens were collected at the time of population declines, so it may never be possible to conclusively determine their cause. It remains unclear whether the pathogen is novel where declines have occurred. Although it is not necessary that the infection be novel for it to be implicated in declines, if a preexisting pathogen has only recently caused extinctions, cofactors must be important. Whether the pattern of outbreaks represents a "wave" of extinctions is unclear, but if it does, the rate of spread in Australia is implausibly high for a waterborne pathogen, given the most likely estimates of epidemiological parameters. Although B. dendrobatidis is an amphibian pathogen according to Koch's postulates, the postulates are neither necessary nor sufficient criteria to identify a pathogen. The following key pieces of information are necessary to better understand the impact of this fungus on frog communities: better knowledge of the means and rate of transmission under field conditions, prevalence of infection among frog populations, as distinct from morbid individuals, and the effect of the fungus on frogs in the wild. It is crucial to determine whether there are strains of the fungus with differing pathogenicity to particular frog species and whether host-pathogen coevolution has occurred or is occurring. Recently developed diagnostic tools bring into reach the possibility of addressing these questions and thus developing appropriate strategies to manage frog communities that may be affected by this fungus.     

Emerging infectious disease as a proximate cause of amphibian mass mortality

A newly discovered infectious disease of amphibians, chytridiomycosis, caused by the fungal pathogen Batrachochytrium dendrobatidis, is implicated in population declines and possible extinctions throughout the world. The purpose of our study was to examine the effects of B. dendrobatidis on the mountain yellow-legged frog (Rana muscosa) in the Sierra Nevada of California (USA). We (1) quantified the prevalence and incidence of B. dendrobatidis through repeat surveys of several hundred R. muscosa populations in the southern Sierra Nevada; (2) described the population-level effects of B. dendrobatidis on R. muscosa population abundance; and (3) compared the mortality rates of infected and uninfected R. muscosa individuals from pre- through post-metamorphosis using both laboratory and field experiments. Mouthpart inspections conducted in 144 and 132 R. muscosa populations in 2003 and 2004, respectively, indicated that 19% of R. muscosa populations in both years showed indications of chytridiomycosis. Sixteen percent of populations that were uninfected in 2003 became infected by 2004. Rana muscosa population sizes were reduced by an average of 88% following B. dendrobatidis outbreaks at six sites, but at seven B. dendrobatidis-negative sites, R. muscosa population sizes increased by an average of 45% over the same time period. In the laboratory, all infected R. muscosa developed fatal chytridiomycosis after metamorphosis, while all uninfected individuals remained healthy. In the field experiment in which R. muscosa tadpoles were caged at infected and uninfected sites, 96% of the individuals that metamorphosed at infected sites died vs. 5% at the uninfected sites. These studies indicate that chytridiomycosis causes high mortality in post-metamorphic R. muscosa, that this emerging disease is the proximate cause of numerous observed R. muscosa population declines, and that the disease threatens this species with extirpation at numerous sites in California's Sierra Nevada.     

Using a Bayesian network to clarify areas requiring research in a host–pathogen system

Bayesian network analyses can be used to interactively change the strength of effect of variables in a model to explore complex relationships in new ways. In doing so, they allow one to identify influential nodes that are not well studied empirically so that future research can be prioritized. We identified relationships in host and pathogen biology to examine disease‐driven declines of amphibians associated with amphibian chytrid fungus (Batrachochytrium dendrobatidis). We constructed a Bayesian network consisting of behavioral, genetic, physiological, and environmental variables that influence disease and used them to predict host population trends. We varied the impacts of specific variables in the model to reveal factors with the most influence on host population trend. The behavior of the nodes (the way in which the variables probabilistically responded to changes in states of the parents, which are the nodes or variables that directly influenced them in the graphical model) was consistent with published results. The frog population had a 49% probability of decline when all states were set at their original values, and this probability increased when body temperatures were cold, the immune system was not suppressing infection, and the ambient environment was conducive to growth of B. dendrobatidis. These findings suggest the construction of our model reflected the complex relationships characteristic of host–pathogen interactions. Changes to climatic variables alone did not strongly influence the probability of population decline, which suggests that climate interacts with other factors such as the capacity of the frog immune system to suppress disease. Changes to the adaptive immune system and disease reservoirs had a large effect on the population trend, but there was little empirical information available for model construction. Our model inputs can be used as a base to examine other systems, and our results show that such analyses are useful tools for reviewing existing literature, identifying links poorly supported by evidence, and understanding complexities in emerging infectious‐disease systems.     

Ecology of Chytridiomycosis in Rainforest Stream Frog Assemblages of Tropical Queensland

Abstract:  In the wet tropics of Queensland, Australia, eight species of stream-dwelling frogs have experienced population declines. Some declines were associated with an emerging infectious disease of amphibians (chytridiomycosis) caused by the fungus Batrachochytrium dendrobatidis. We examined the spatial and temporal pattern of infection prevalence in a sample of frog populations. Infected adults and tadpoles of all species were found, and infections occurred at every site. Infection prevalence varied among species and was always < 10.0% in adults but ranged from 0.75 to 76.0% in tadpoles. In this system tadpoles and adults of some species may act as disease reservoirs, experiencing avirulent infections, whereas other hosts (declining species) experience virulent infections. Infection prevalence was higher during the cool, dry winter season (May to September) and at high elevations (600–800 m), suggesting regulation by environmental conditions, including temperature and precipitation. We found no relationships between infection prevalence and mean body condition, fluctuating asymmetry of hind limbs, population density, or the presence of metamorphosing tadpoles and juvenile frogs. Although it is not certain whether chytridiomycosis was responsible for past frog population declines in the wet tropics of Queensland, the pathogen is now endemic. Our data indicate that at the landscape level, environmental conditions have strong effects on host-pathogen dynamics. These effects interact with species-specific behavior or immune function and may be important underlying determinants of chytridiomycosis epizootics and emergence.     

Effects of chytrid fungus and a glyphosate-based herbicide on survival and growth of wood frogs (Lithobates sylvaticus)

Anthropogenic-derived stressors in the environment, such as contaminants, are increasingly considered important cofactors that may decrease the immune response of amphibians to pathogens. Few studies, however, have integrated amphibian disease and contaminants to test this multiple-stressor hypothesis for amphibian declines. We examined whether exposure to sublethal concentrations of a glyphosate-based herbicide and two strains of the pathogenic chytrid fungus, Batrachochrytrium dendrobatidis (Bd) could: (1) sublethally affect wood frogs (Lithobates sylvaticus) by altering the time to and size at metamorphosis, and (2) directly affect survivability of wood frogs after metamorphosis. Neither Bd strain nor herbicide exposure alone significantly altered growth or time to metamorphosis. The two Bd strains did not differ in their pathogenicity, and both caused mortality in post-metamorphic wood frogs. There was no evidence of an interaction between treatments, indicating a lack of herbicide-induced susceptibility to Bd. However, the trends in our data suggest that exposure of wood frogs to a high concentration of glyphosate-based herbicide may reduce Bd-caused mortality compared to animals exposed to Bd alone. These results exemplify the complexities inherent when populations are coping with multiple stressors. In this case, the perceived stressor, glyphosate-based herbicide, appeared to affect the pathogen more than the host's immune system, relieving the host from disease-caused effects. This suggests caution when invoking multiple stressors as a cause for increased disease susceptibility and indicates that the effects of multiple stressors on disease outcome depend on the interrelationships of stressors to both the pathogen and the host.     

Differences in sensitivity to the fungal pathogen Batrachochytrium dendrobatidis among amphibian populations

Contributing to the worldwide biodiversity crisis are emerging infectious diseases, which can lead to extirpations and extinctions of hosts. For example, the infectious fungal pathogen Batrachochytrium dendrobatidis (Bd) is associated with worldwide amphibian population declines and extinctions. Sensitivity to Bd varies with species, season, and life stage. However, there is little information on whether sensitivity to Bd differs among populations, which is essential for understanding Bd‐infection dynamics and for formulating conservation strategies. We experimentally investigated intraspecific differences in host sensitivity to Bd across 10 populations of wood frogs (Lithobates sylvaticus) raised from eggs to metamorphosis. We exposed the post‐metamorphic wood frogs to Bd and monitored survival for 30 days under controlled laboratory conditions. Populations differed in overall survival and mortality rate. Infection load also differed among populations but was not correlated with population differences in risk of mortality. Such population‐level variation in sensitivity to Bd may result in reservoir populations that may be a source for the transmission of Bd to other sensitive populations or species. Alternatively, remnant populations that are less sensitive to Bd could serve as sources for recolonization after epidemic events.     

Ambient Ultraviolet B Radiation and Prevalence of Infection by Batrachochytrium dendrobatidis in Two Amphibian Species

Abstract: Chytridiomycosis, the emerging disease caused by the chytrid fungus Batrachochytrium dendrobatidis (Bd) is responsible for declines and extirpations of amphibian populations worldwide. Environmental covariates modify the host‐Bd interaction and thus affect the ongoing spread of the pathogen. One such covariate may be the intensity of ultraviolet B (UV‐B) radiation. In a field experiment conducted in Laguna Grande de Peñalara (central Spain), a mountainous region where the presence of Bd has been documented since 1997, we analyzed the potential effect of environmental UV‐B (daily maximum 2.5–3.9 W/m²) on the susceptibility of larvae of the common toad (Bufo bufo) to Bd. The proportion of infected individuals increased as tadpoles developed. The prevalence of Bd was significantly lower in tadpoles exposed to environmental UV‐B intensities (2.94%) than in tadpoles not exposed to the radiation (9.72%). This finding mirrors that seen for a second amphibian species, the European midwife toad (Alytes obstetricans), for which conditional prevalence (i.e., prevalence of infection conditioned on the probability of a site being infected) across the Iberian Peninsula was inversely correlated with the intensity of UV‐B.     

Selecting for Tolerance against Pathogens and Herbivores to Enhance Success of Reintroduction and Translocation

Abstract: Some species have insufficient defenses against climate change, emerging infectious diseases, and non‐native species because they have not been exposed to these factors over their evolutionary history, and this can decrease their likelihood of persistence. Captive breeding programs are sometimes used to reintroduce individuals back into the wild; however, successful captive breeding and reintroduction can be difficult because species or populations often cannot coexist with non‐native pathogens and herbivores without artificial selection. In captive breeding programs, breeders can select for host defenses that prevent or reduce pathogen or herbivore burden (i.e., resistance) or traits that limit the effects of parasitism or herbivory on host fitness (i.e., tolerance). We propose that selection for host tolerance may enhance the success of reintroduction or translocation because tolerant hosts generally have neutral effects on introduced pathogens and herbivores. The release of resistant hosts would have detrimental effects on their natural enemies, promoting rapid evolution to circumvent the host resistance that may reduce the long‐term probability of persistence of the reintroduced or translocated species. We examined 2 case studies, one on the pathogenic amphibian chytrid fungus ( Batrachochytrium dendrobatidis [Bd]) and the other on the herbivorous cactus moth ( Cactoblastis cactorum) in the United States, where it is not native. In each case study, we provide recommendations for how captive breeders and managers could go about selecting for host tolerance. Selecting for tolerance may offer a promising tool to rescue hosts species from invasive natural enemies as well as new natural enemies associated with climate change‐induced range shifts.     

Spatial spread of an emerging infectious disease: conjunctivitis in House Finches

In this paper we quantify the rate of spread of the newly emerged pathogen Mycoplasma gallisepticum of the House Finch, Carpodacus mexicanus, in its introduced range. We compare and contrast the rapid, yet decelerating, rate of spread of the pathogen with the slower, yet accelerating rate of spread of the introduced host. Comparing the rate of spread of this pathogen to pathogens in terrestrial mammalian hosts, we see that elevation and factors relating to host abundance restrict disease spread, rather than finding any major effects of discrete barriers or anthropogenic movement. We examine the role of seasonality in the rate of spread, finding that the rate and direction of disease spread relates more to seasonality in host movement than to seasonality in disease prevalence. We conclude that asymptomatic carriers are major transmitters of Mycoplasma gallisepticum into novel locations, a finding which may also be true for many other diseases, such as West Nile Virus and avian influenza.     

Life-history trade-offs influence disease in changing climates: strategies of an amphibian pathogen

Life-history trade-offs allow many animals to maintain reproductive fitness across a range of climatic conditions. When used by parasites and pathogens, these strategies may influence patterns of disease in changing climates. The chytrid fungus, Batrachochytrium dendrobatidis, is linked to global declines of amphibian populations. Short-term growth in culture is maximal at 17 degrees-25 degrees C. This has been used in an argument that global warming, which increases the time that amphibians spend at these temperatures in cloud-covered montane environments, has led to extinctions. Here we show that the amphibian chytrid responds to decreasing temperatures with trade-offs that increase fecundity as maturation rate slows and increase infectivity as growth decreases. At 17 degrees-25 degrees C, infectious zoospores encyst (settle and develop a cell wall) and develop into the zoospore-producing stage (zoosporangium) faster, while at 7 degrees-10 degrees C, greater numbers of zoospores are produced per zoosporangium; these remain infectious for a longer period of time. We modeled the population growth of B. dendrobatidis through time at various temperatures using delayed differential equations and observational data for four parameters: developmental rate of thalli, fecundity, rate of zoospore encystment, and rate of zoospore survival. From the models, it is clear that life-history trade-offs allow B. dendrobatidis to maintain a relatively high long-term growth rate at low temperatures, so that it maintains high fitness across a range of temperatures. When a seven-day cold shock is simulated, the outcome is intermediate between the two constant temperature regimes, and in culture, a sudden drop in temperature induces zoospore release. These trade-offs can be ecologically important for a variety of organisms with complex life histories, including pathogenic microorganisms. The effect of temperature on amphibian mortality will depend on the interaction between fungal growth and host immune function and will be modified by host ecology, behavior, and life history. These results demonstrate that B. dendrobatidis populations can grow at high rates across a broad range of environmental temperatures and help to explain why it is so successful in cold montane environments.     

Heterogeneity shapes invasion: host size and environment influence susceptibility to a nonnative pathogen.

Theoretical study of invasion dynamics has suggested that spatial heterogeneity should strongly influence the rate and extent of spreading organisms. However, empirical support for this prediction is scant, and the importance of understanding heterogeneity for real-world systems has remained ambiguous. This study quantified the influence of host and environmental heterogeneity on the dynamics of a 19-year disease invasion by the exotic and fatal pathogen, Phytophthora lateralis, within a stream population of its host tree, Port Orford cedar (Chamaecyparis lawsoniana). Using dendrochronology, we reconstructed the invasion history along a 1350-m length of infected stream, which serves as the only route of pathogen dispersal. Contrary to theoretical predictions, the temporal progression of the disease invasion was not related to a host's downstream spatial position, but instead was determined by two sources of heterogeneity: host size and proximity to the stream channel. These sources of heterogeneity influenced both the epidemic and endemic dynamics of this pathogen invasion. This analysis provides empirical support for the influence of heterogeneity on the invasion dynamics of a commercially important forest pathogen and highlights the need to incorporate such natural variability into both invasion theory and methods aimed at controlling future spread.     

Begging behavior and food acquisition by brown-headed cowbird nestlings

Understanding the selective forces that limit the exaggeration of begging signals is a critical issue in understanding the evolution of begging behavior. I studied the begging behavior of nestlings of the brown-headed cowbird (Molothrus ater), a brood parasite. In the nests of indigo buntings (Passerina cyanea), brown-headed cowbird nestlings received approximately twice as much food per hour than their host nestmates. I tested three hypotheses for the mechanism by which cowbirds acquired more food than their bunting nestmates: the size advantage hypothesis, the signal exaggeration hypothesis, and the novel begging behavior hypothesis. I found support for the hypotheses that cowbirds acquire more food as a result of their larger body size, and due to the exaggeration of begging signals that are not dependent on body size. I did not find support for the role of novel begging behaviors in cowbird food acquisition. These results suggest that food acquisition by host chicks in unparasitized nests could be increased by the exaggeration of begging signals. Recent work suggests that such exaggeration may be limited by the risk of nest predation, but further studies are needed. Received: 12 December 1997 / Accepted after revision: 29 December 1997     

Batrachochytrium dendrobatidis and the Collapse of Anuran Species Richness and Abundance in the Upper Manu National Park,Southeastern Peru

Abstract: Amphibians are declining worldwide, but these declines have been particularly dramatic in tropical mountains, where high endemism and vulnerability to an introduced fungal pathogen, Batrachochytrium dendrobatidis (Bd), is associated with amphibian extinctions. We surveyed frogs in the Peruvian Andes in montane forests along a steep elevational gradient (1200–3700 m). We used visual encounter surveys to sample stream‐dwelling and arboreal species and leaf‐litter plots to sample terrestrial‐breeding species. We compared species richness and abundance among the wet seasons of 1999, 2008, and 2009. Despite similar sampling effort among years, the number of species (46 in 1999) declined by 47% between 1999 and 2008 and by 38% between 1999 and 2009. When we combined the number of species we found in 2008 and 2009, the decline from 1999 was 36%. Declines of stream‐dwelling and arboreal species (a reduction in species richness of 55%) were much greater than declines of terrestrial‐breeding species (reduction of 20% in 2008 and 24% in 2009). Similarly, abundances of stream‐dwelling and arboreal frogs were lower in the combined 2008–2009 period than in 1999, whereas densities of frogs in leaf‐litter plots did not differ among survey years. These declines may be associated with the infection of frogs with Bd. B. dendrobatidis prevalence correlated significantly with the proportion of species that were absent from the 2008 and 2009 surveys along the elevational gradient. Our results suggest Bd may have arrived at the site between 1999 and 2007, which is consistent with the hypothesis that this pathogen is spreading in epidemic waves along the Andean cordilleras. Our results also indicate a rapid decline of frog species richness and abundance in our study area, a national park that contains many endemic amphibian species and is high in amphibian species richness.     

Cover Caption

Cover : Little brown bats (Myotis lucifugus) hibernating in Aeolis Cave, Bennington County, Vermont (U.S.A.), March 2009. The probability of persistence of many species of hibernating bats in the eastern United States and Canada is greatly decreased by white‐nose syndrome, a rapidly emerging infectious disease that is causing mass mortality. Culling of bats in hibernacula has been proposed as a mechanism to control the disease. On pages 189‐194, Hallam and McCracken present a simulation model that suggests culling is unlikely to reduce spread of white‐nose syndrome.     

Using a common commensal bacterium in endangered Takahe as a model to explore pathogen dynamics in isolated wildlife populations

Predicting and preventing outbreaks of infectious disease in endangered wildlife is problematic without an understanding of the biotic and abiotic factors that influence pathogen transmission and the genetic variation of microorganisms within and between these highly modified host communities. We used a common commensal bacterium, Campylobacter spp., in endangered Takahe (Porphyrio hochstetteri) populations to develop a model with which to study pathogen dynamics in isolated wildlife populations connected through ongoing translocations. Takahe are endemic to New Zealand, where their total population is approximately 230 individuals. Takahe were translocated from a single remnant wild population to multiple offshore and mainland reserves. Several fragmented subpopulations are maintained and connected through regular translocations. We tested 118 Takahe from 8 locations for fecal Campylobacter spp. via culture and DNA extraction and used PCR for species assignment. Factors relating to population connectivity and host life history were explored using multivariate analytical methods to determine associations between host variables and bacterial prevalence. The apparent prevalence of Campylobacter spp. in Takahe was 99%, one of the highest reported in avian populations. Variation in prevalence was evident among Campylobacter species identified. C. sp. nova 1 (90%) colonized the majority of Takahe tested. Prevalence of C. jejuni (38%) and C. coli (24%) was different between Takahe subpopulations, and this difference was associated with factors related to population management, captivity, rearing environment, and the presence of agricultural practices in the location in which birds were sampled. Modeling results of Campylobacter spp. in Takahe metapopulations suggest that anthropogenic management of endangered species within altered environments may have unforeseen effects on microbial exposure, carriage, and disease risk. Translocation of wildlife between locations could have unpredictable consequences including the spread of novel microbes between isolated populations.     

Increased Infectious Disease Susceptibility Resulting from Outbreeding Depression

Abstract:  The mechanisms by which outbreeding depression leads to reduced fitness are poorly understood. We considered the hypothesis that outbreeding can depress fitness by increasing the susceptibility of hybrid individuals and populations to infectious disease. Competitive breeding trials in experimental ponds indicated that outbred largemouth bass (  Micropterus salmoides ) crossed from two geographically and genetically distinct populations suffered a reduction in fitness of approximately 14% relative to parental stocks. We measured the comparative susceptibility of these same outbred stocks to a novel viral pathogen, largemouth bass virus. Following experimental inoculation, F2 generation hybrids suffered mortality at a rate 3.6 times higher than either F1 generation hybrids or wild-type parental fish. Analysis of viral loads indicated that viral replication was more rapid in F2 fish than in F1 hybrids or wild-type parental fish. We attribute these results to the disruption of coadapted gene complexes in the immune systems of outbred fish in the F2 generation. Increased susceptibility to infectious disease may be an important but underappreciated mechanism by which outbreeding reduces the fitness of individuals and populations and by which novel infectious diseases emerge in populations of hybrid organisms.     

Edge effects, not connectivity, determine the incidence and development of a foliar fungal plant disease

Using a model plant-pathogen system in a large-scale habitat corridor experiment, we found that corridors do not facilitate the movement of wind-dispersed plant pathogens, that connectivity of patches does not enhance levels of foliar fungal plant disease, and that edge effects are the key drivers of plant disease dynamics. Increased spread of infectious disease is often cited as a potential negative effect of habitat corridors used in conservation, but the impacts of corridors on pathogen movement have never been tested empirically. Using sweet corn (Zea mays) and southern corn leaf blight (Cochliobolus heterostrophus) as a model plant-pathogen system, we tested the impacts of connectivity and habitat fragmentation on pathogen movement and disease development at the Savannah River Site, South Carolina, USA. Over time, less edgy patches had higher proportions of diseased plants, and distance of host plants to habitat edges was the greatest determinant of disease development. Variation in average daytime temperatures provided a possible mechanism for these disease patterns. Our results show that worries over the potentially harmful effects of conservation corridors on disease dynamics are misplaced, and that, in a conservation context, many diseases can be better managed by mitigating edge effects.     

Ancient behaviors of larval amphibians in response to an emerging fungal pathogen, <Emphasis Type="Italic">Batrachochytrium dendrobatidis</Emphasis>

Behaviors have evolved in response to various selection pressures over evolutionary time. However, not all behaviors are adaptive. Some presumably “ancient” behaviors, persistent for millions of years, may be detrimental in the face of novel selection pressures in modern times. These pressures include a multitude of emerging infectious diseases which may be stimulated by environmental changes. We examined how a globally emerging amphibian pathogen, Batrachochytrium dendrobatidis (BD), affected two key evolutionarily persistent behaviors displayed by amphibian larvae: aggregation and thermoregulation. Larval aggregation behavior is often essential for foraging, thermoregulation, and antipredator defense, but varies among species. Thermoregulatory behavior speeds larval development in ephemeral habitats. Specifically, we examined whether aggregation and thermoregulatory behaviors changed when exposed to the BD pathogen in two species (Bufo boreas and Rana cascadae) whose larvae aggregate in nature. In laboratory choice tests, larvae of neither species avoided infected conspecifics. BD-exposed B. boreas larvae aggregated, while unexposed R. cascadae larvae associated more frequently with BD-exposed conspecifics. There was no evidence of behavioral fever or altered thermoregulation in larvae of four species we examined (Pseudacris regilla, Rana aurora, B. boreas, R. cascadae). The absence of behavioral fever may suggest an inability of the larvae of some host species to mediate infection risk by this pathogen. Thermoregulatory behaviors may exhibit a high degree of evolutionary inertia in amphibian hosts because they are linked with host physiology and developmental rates, while altered aggregation behaviors could potentially elevate pathogen transmission rates, leading to increased infection risk in social amphibian species.     

Spatially mixed crops to control the stratified dispersal of airborne fungal diseases

Intraspecific crop diversification is thought to be a possible solution to the disease susceptibility of monocultured crops. We modelled the stratified dispersal of an airborne pathogen population in order to identify the spatial patterns of cultivar mixtures that could slow epidemic spread driven by dual dispersal mechanisms acting over both short and long distances. We developed a model to simulate the propagation of a fungal disease in a 2D field, including a reaction-diffusion model for short-distance disease dispersal, and a stochastic model for long-distance dispersal. The model was fitted to data for the spatio-temporal spread of faba bean rust (caused by Uromyces viciae-fabae) through a discontinuous field. The model was used to compare the effectiveness of eight different planting patterns of cultivar mixtures against a disease spread by short-distance and stratified dispersal. Our combined modelling approach provides a reasonably good fit with the observed data for the spread of faba bean rust. Similar predictive power could be expected for the management of resource-mediated invasions by other airborne fungi. If a disease spreads by short-distance dispersal, random mixtures can be used to slow the epidemic spread, since their spatial irregularity creates a natural barrier to the progression of a smooth epidemic wave. In the context of stratified dispersal, heterogeneous patterns should be used that include a minimum distance between susceptible units, which decreases the probability of infection by long-distance spore dispersal. We provide a simple framework for modelling the stratified dispersal of disease in a diversified crop. The model suggests that the spatial arrangement of components in cultivar mixtures has to accord with the dispersal characteristics of the pathogen in order to increase the efficiency of diversification strategies in agro-ecosystems and forestry. It can be applied in low input agriculture to manage pathogen invasion by intercropping and cultivar mixtures, and to design sustainable systems of land use.     

Variation with Land Use of Immune Function and Prevalence of Avian Pox in Galapagos Finches

Introduced disease has been implicated in recent wildlife extinctions and population declines worldwide. Both anthropogenic‐induced change and natural environmental features can affect pathogen spread. Furthermore, environmental disturbance can result in changes in stress physiology, nutrition, and social structure, which in turn can suppress immune system function. However, it remains unknown whether landscape variation results in heterogeneity in host resistance to pathogens. Avian pox virus, a pathogen implicated in avian declines and extinctions in Hawaii, was introduced to the Galapagos in the 1890s, and prevalence (total number of current infections) has increased recently in finches. We tested whether prevalence and recovery trends in 7 species of Galapagos finches varied by elevation or human land use. To do so, we used infection data obtained from 545 wild‐caught birds. In addition, we determined whether annual changes in 4 aspects of innate immune function (complement protein activity, natural antibody activity, concentration of PIT54 protein, and heterophil:lymphocyte ratio) varied by elevation or land use. Prevalence and recovery rates did not vary by elevation from 2008 to 2009. Avian pox prevalence and proportion of recovered individuals in undeveloped and urban areas did not change from 2008 to 2009. In agricultural areas, avian pox prevalence increased 8‐fold (from 2% to 17% of 234 individuals sampled) and proportion of recovered individuals increased (11% to 19%) from 2008 to 2009. These results suggest high disease‐related mortality. Variation in immune function across human land‐use types correlated with variation in both increased prevalence and susceptibility, which indicates changes in innate immune function may underlie changes in disease susceptibility. Our results suggest anthropogenic disturbance, in particular agricultural practices, may underlie immunological changes in host species that themselves contribute to pathogen emergence. Variación con el Uso de Suelo de la Función Inmune y la Prevalencia de la Varicela Aviar en Pinzones de las Galápagos