Global amphibian declines have often been attributed to disease, but ignorance of the relative importance and mode of action of potential drivers of infection has made it difficult to develop effective remediation. In a field study, here we show that the widely used herbicide, atrazine, was the best predictor (out of more than 240 plausible candidates) of the abundance of larval trematodes (parasitic flatworms) in the declining northern leopard frog Rana pipiens. The effects of atrazine were consistent across trematode taxa. The combination of atrazine and phosphate--principal agrochemicals in global corn and sorghum production--accounted for 74% of the variation in the abundance of these often debilitating larval trematodes (atrazine alone accounted for 51%). Analysis of field data supported a causal mechanism whereby both agrochemicals increase exposure and susceptibility to larval trematodes by augmenting snail intermediate hosts and suppressing amphibian immunity. A mesocosm experiment demonstrated that, relative to control tanks, atrazine tanks had immunosuppressed tadpoles, had significantly more attached algae and snails, and had tadpoles with elevated trematode loads, further supporting a causal relationship between atrazine and elevated trematode infections in amphibians. These results raise concerns about the role of atrazine and phosphate in amphibian declines, and illustrate the value of quantifying the relative importance of several possible drivers of disease risk while determining the mechanisms by which they facilitate disease emergence.
The effect of echinostome infections on the survival of Rana pipiens tadpoles was examined in relation to developmental stage of tadpoles. Individual tadpoles of Gosner stages 25, 27, 32-33, and 37-39 were exposed to 1 of 4 levels of cercariae (0, 20, 50, or 100). Only tadpoles at stage 25, the earliest stage infected, died within a 5-day experimental period. This stage-specific mortality rate could be explained, in part, by the stage-specific location of encystment of cercariae, which was documented in a separate experiment. In accordance with kidney development, cercariae predominately encysted in the pronephroi during early stages of tadpole development (stages 25 through 31-32) and only in the mesonephroi and associated ducts at later stages (stages 37 through 46). As the mesonephros develops, renal capacity presumably increases. Thus, tadpoles died only when metacercariae concentrated in the functional portion of the kidney with the most limited renal capacity. As tadpoles aged, they also became less susceptible to infections. On average, 69.5% of cercariae that were exposed to stage 25-26 tadpoles successfully encysted. compared with only 8.4% of cercariae exposed to stage 37-38 tadpoles. Exposures of metamorphic frogs (poststage 46) to cercariae revealed that these individuals can become infected with echinostomes. Collectively, our data highlight the host stage-dependent dynamics of tadpole-echinostome interactions.
Humans are altering biodiversity globally and infectious diseases are on the rise; thus, there is interest in understanding how changes to biodiversity affect disease. Here, we explore how predator diversity shapes parasite transmission. In a mesocosm experiment that manipulated predator (larval dragonflies and damselflies) density and diversity, non-intraguild (non-IG) predators that only consume free-living cercariae (parasitic trematodes) reduced metacercarial infections in tadpoles, whereas intraguild (IG) predators that consume both parasites and tadpole hosts did not. This likely occurred because IG predators reduced tadpole densities and anticercarial behaviors, increasing per capita exposure rates of the surviving tadpoles (i.e., via density-and trait-mediated effects) despite the consumption of parasites. A mathematical model demonstrated that non-IG predators reduce macroparasite infections, but IG predation weakens this "dilution effect" and can even amplify parasite burdens. Consistent with the experiment and model, a wetland survey revealed that the diversity of IG predators was unrelated to metacercarial burdens in amphibians, but the diversity of non-IG predators was negatively correlated with infections. These results are strikingly similar to generalities that have emerged from the predator diversity-pest biocontrol literature, suggesting that there may be general mechanisms for pest control and that biocontrol research might inform disease management and vice versa. In summary, we identified a general trait of predators-where they fall on an IG predation continuum-that predicts their ability to reduce infections and possibly pests in general. Consequently, managing assemblages of predators represents an underused tool for the management of human and wildlife diseases and pest populations.biodiversity-ecosystem function | dilution effect | schistosomiasis | snail | trophic cascade
Epizootic transmission of West Nile virus (WNV) often intensifies rapidly leading to increasing risk of human infection, but the processes underlying amplification remain poorly understood. We quantified epizootic WNV transmission in communities of mosquitoes and birds in the Chicago, Illinois (USA) region during 2005 and 2006. Using quantitative polymerase chain reaction (PCR) methods, we detected WNV in 227 of 1195 mosquito pools (19%) in 2005 and 205 of 1685 (12%) in 2006; nearly all were Culex pipiens. In both years, mosquito infection rates increased rapidly in the second half of July to a peak of 59/1000 mosquitoes in 2005 and 33/1000 in 2006, and then declined slowly. Viral RNA was detected in 11 of 998 bird sera (1.1%) in 2005 and 3 of 1285 bird sera (<1%) in 2006; 11 of the 14 virus-positive birds were hatch-year birds. Of 540 hatch-year birds, 100 (18.5%) were seropositive in 2005, but only 2.8% (14/493) tested seropositive in 2006 for WNV antibodies using inhibition enzyme-linked immunosorbent assay (ELISA). We observed significant time series cross-correlations between mosquito infection rate and proportion of virus-positive birds, proportion of hatch-year birds captured in mist nets (significant in 2006 only), seroprevalence of hatch-year birds, and number of human cases in both seasons. These associations, coupled with the predominance of WNV infection and seropositivity in hatch-year birds, indicate a key role for hatch-year birds in the amplification of epizootic transmission of WNV, and in increasing human infection risk by facilitating local viral amplification.
Recent evidence suggests that infection by larvae of the trematode Ribeiroia ondatrae accounts for a significant proportion of limb malformations currently observed in amphibian populations of North America. However, the effects of R. ondatrae infection on northern leopard frogs (Rana pipiens), one of the species most frequently reported with malformations, have not been adequately explored. Moreover, the risk factors associated with R. ondatrae-induced malformations have not been clearly identified. We examined the effects of timing of infection on tadpole survival and limb development. Rana pipiens tadpoles were individually exposed to R. ondatrae cercariae at the pre-limb-bud (Gosner stages 24 and 25), limb-bud (Gosner stages 27 and 28), or paddle (Gosner stages 31-33) stages of development and monitored through metamorphosis. The effects of infection were stage-specific. Infections acquired at the pre-limbbud stage resulted in a high mortality rate (47.5-97.5%), whereas tadpoles infected at the limb-bud stage displayed a high malformation rate (16% overall), and the magnitude of effects increased with the level of exposure to cercariae. In contrast, infections acquired at the paddle stage had no effect on limb development or tadpole survival, which suggests that the timing of R. ondatrae infection in relation to the stage structure of tadpole populations in the wild is an important determinant of the degree to which populations are affected by R. ondatrae.Résumé : Des indications récentes font croire que des infections par les larves du trématode Ribeiroia ondatrae pourraient expliquer une partie importante des malformations des membres que l'on observe actuellement chez les populations d'amphibiens d'Amérique du Nord. Cependant, les effets des infections à R. ondatrae sur les grenouilles léopards (Rana pipiens), une des espèces le plus fréquemment signalées avec des malformations, n'ont pas été étudiés adéquatement. De plus, les facteurs de risque associés aux malformations causées par R. ondatrae ne sont pas clairement identifiés. Nous avons étudié les effets du moment de l'infection sur la survie et le développement des membres chez le têtard. Nous avons exposé des têtards de R. pipiens individuellement à des cercaires de R. ondatrae au stade de développement précédant l'apparition des bourgeons des membres (stades 24 et 25 de Gosner), au stade des bourgeons des membres (stades 27 et 28 de Gosner) et au stade des membres en palettes (stades 31-33 de Gosner) et les avons suivi jusqu'après la métamorphose. Les effets de l'infection dépendent du stade. Les infections acquises avant l'apparition des bourgeons des membres entraînent une forte mortalité (47,5-97,5 %), alors que les têtards infectés lorsque les bourgeons sont présents ont un taux élevé de malformations (en tout 16 %); l'importance des effets augmente avec le degré d'exposition aux métacercaires. En revanche, les infections acquises lorsque les membres ont la forme de palettes restent sans effet sur le développement des membres et la survie des tê...
Early-phase transmission (EPT) is a recently described model of plague transmission that explains the rapid spread of disease from flea to mammal host during an epizootic. Unlike the traditional blockage-dependent model of plague transmission, EPT can occur when a flea takes its first blood meal after initially becoming infected by feeding on a bacteraemic host. Blockage of the flea gut results from biofilm formation in the proventriculus, mediated by the gene products found in the haemin storage (hms) locus of the Yersinia pestis chromosome. Although biofilms are required for blockage-dependent transmission, the role of biofilms in EPT has yet to be determined. An artificial feeding system was used to feed Xenopsylla cheopis and Oropsylla montana rat blood spiked with the parental Y. pestis strain KIM5(pCD1)+, two different biofilm-deficient mutants (ΔhmsT, ΔhmsR), or a biofilm-overproducer mutant (ΔhmsP). Infected fleas were then allowed to feed on naïve Swiss Webster mice for 1–4 days after infection, and the mice were monitored for signs of infection. We also determined the bacterial loads of each flea that fed upon naïve mice. Biofilm-defective mutants transmitted from X. cheopis and O. montana as efficiently as the parent strain, whereas the EPT efficiency of fleas fed the biofilm-overproducing strain was significantly less than that of fleas fed either the parent or a biofilm-deficient strain. Fleas infected with a biofilm-deficient strain harboured lower bacterial loads 4 days post-infection than fleas infected with the parent strain. Thus, defects in biofilm formation did not prevent flea-borne transmission of Y. pestis in our EPT model, although biofilm overproduction inhibited efficient EPT. Our results also indicate, however, that biofilms may play a role in infection persistence in the flea.
Factors potentially contributing to the lower incidence of Lyme borreliosis (LB) in the far-western than in the northeastern United States include tick host-seeking behavior resulting in fewer human tick encounters, lower densities of Borrelia burgdorferi-infected vector ticks in peridomestic environments, and genetic variation among B. burgdorferi spirochetes to which humans are exposed. We determined the population structure of B. burgdorferi in over 200 infected nymphs of the primary bridging vector to humans, Ixodes pacificus, collected in Mendocino County, CA. This was accomplished by sequence typing the spirochete lipoprotein ospC and the 16S-23S rRNA intergenic spacer (IGS). Thirteen ospC alleles belonging to 12 genotypes were found in California, and the two most abundant, ospC genotypes H3 and E3, have not been detected in ticks in the Northeast. The most prevalent ospC and IGS biallelic profile in the population, found in about 22% of ticks, was a new B. burgdorferi strain defined by ospC genotype H3. Eight of the most common ospC genotypes in the northeastern United States, including genotypes I and K that are associated with disseminated human infections, were absent in Mendocino County nymphs. ospC H3 was associated with hardwood-dominated habitats where western gray squirrels, the reservoir host, are commonly infected with LB spirochetes. The differences in B. burgdorferi population structure in California ticks compared to the Northeast emphasize the need for a greater understanding of the genetic diversity of spirochetes infecting California LB patients.In the United States, Lyme borreliosis (LB) is the most commonly reported vector-borne illness and is caused by infection with the spirochete Borrelia burgdorferi (3, 9, 52). The signs and symptoms of LB can include a rash, erythema migrans, fever, fatigue, arthritis, carditis, and neurological manifestations (50, 51). The black-legged tick, Ixodes scapularis, and the western black-legged tick, Ixodes pacificus, are the primary vectors of B. burgdorferi to humans in the United States, with the former in the northeastern and north-central parts of the country and the latter in the Far West (9, 10). These ticks perpetuate enzootic transmission cycles together with a vertebrate reservoir host such as the white-footed mouse, Peromyscus leucopus, in the Northeast and Midwest (24, 35), or the western gray squirrel, Sciurus griseus, in California (31, 46). B. burgdorferi is a spirochete species with a largely clonal population structure (14, 16) comprising several different strains or lineages (8). The polymorphic ospC gene of B. burgdorferi encodes a surface lipoprotein that increases expression within the tick during blood feeding (47) and is required for initial infection of mammalian hosts (25, 55). To date, approximately 20 North American ospC genotypes have been described (40,45,49,56). At least four, and possibly up to nine, of these genotypes are associated with B. burgdorferi invasiveness in humans (1,15,17,49,57). Restriction fragment length po...
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