Guide Emerging Avian Disease: Published for the Cooper Ornithological Society (Studies in Avian Biology)

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Our study population comprises a large population of mute swans Cygnus olor that have been naturally infected by three different HPAIV viruses belonging to two genetic clades 2. Importantly, these birds have been the subject of ornithological study for more than 60 years, and therefore detailed demographic information is available for the population and the individual birds within it. The population is therefore particularly suitable for exploring the natural epidemiology, evolution and ecology of HPAIV in wild birds at a high degree of precision and certainty.

We show that key epidemiological features are consistent and predictable across multiple outbreaks in a complex natural population and we discuss the implications of these findings for HPAIV transmission in wild birds. The population size changes seasonally and between years, but typically ranges between and birds. Swans hatched at the site are tagged with unique ID markers approximately 24 h after hatching that are replaced with adult rings at approximately four months of age.

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Relatively few birds that hatch locally move away from the Fleet [ 13 ]. As a consequence, detailed data about the date of hatching and sex are known for most swans on the Fleet Lagoon. Individual birds can be identified by unique IDs that they carry on two different leg rings one metal ring, supplied by the British Trust for Ornithology, and one Darvic ring, which allows long-range visual identification. Birds thought to have been in the population at the time of each outbreak were estimated from census data, according to details in the electronic supplementary material.

A cloacal swab and an oropharyngeal swab were also taken from every bird that was blood sampled. HI assays were conducted according to standard methods [ 14 ] further details are provided in the electronic supplementary material. Following detection of HPAIV H5 at the site in December , December and December , oropharyngeal and cloacal swabs were collected from all dead birds of any species, where possible, and processed at APHA further details of site surveillance across outbreak years are provided in the electronic supplementary material.

The epidemiological analyses for the H5N8 outbreak undertaken here see below therefore assume that untested dead birds found during the H5N8 outbreak were HPAIV-positive see electronic supplementary material, figure S1 for details of which birds were tested.

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The typical age-adjusted mortality rate of birds in the same weeks during non-epidemic years is dramatically lower approx. H5N8-positive samples from January were reverse transcribed, amplified using a multiplex PCR method and sequenced using the Oxford Nanopore Technologies MinION device, following an adaptation of previous methods [ 18 ].

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H5N6-positive samples from January were sequenced on an Illumina MiSeq using a non-specific metagenomic approach see electronic supplementary material for more details of sequencing approaches. Appropriate temporal signal for molecular clock analysis was confirmed using TempEst [ 22 ]. Two independent MCMC runs of steps were computed under a strict molecular clock model, an SRD06 nucleotide substitution model, and a constant population size coalescent prior. Convergence of the MCMC runs were checked using Tracer [ 23 ] and maximum clade credibility trees were computed using TreeAnnotator [ 24 ].

For the other seven segments, a preliminary phylogenetic tree was estimated using neighbour-joining, with Jukes—Cantor genetic distances.

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If several genetically distinct large clades were observed typically representing reassorted internal genes , then the clade that contained the sequences from this study was extracted. These extracted sequences were then used to estimate maximum-likelihood ML phylogenies using PhyML [ 25 ], including ML bootstrap replicates to evaluate statistical support. R 0 was not estimated for the H5N1 outbreak because very few cases were observed during that outbreak. Numbers of observed swan carcasses were used as a proxy for HPAI case counts. A distribution was specified for the epidemic generation time, obtained from laboratory studies that observed the time between experimental inoculation of geese or ducks with H5N8 and the time to subsequent infection of contact birds [ 28 — 32 ].

The majority of deaths occurred in juvenile birds less than 1 year old. We tested for possible effects of the last known weight or exact age on the probability of death of juvenile birds. Exact hatch dates are known for almost all birds born into the population, and all juveniles are weighed in September or October of their hatch year.

For all ringed juveniles, exact age in days was calculated for the day on which they were weighed, and a generalized linear model was fitted to calculate the expected weight of a bird of that age and sex. The difference between the weight of the bird at ringing and its expected weight was calculated. The case fatality rate the proportion of individuals that died among all individuals that were infected was crudely estimated for juvenile birds in both outbreaks.

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Estimates were not calculated for adult birds because the protective effect of primary exposure to H5N8 upon subsequent exposure with H5N6 would prevent direct comparisons of viral virulence. As no blood samples were collected prior to the H5N8 outbreak, we assume that juvenile birds were seronegative for H5N8 prior to the outbreak and that the presence of an H5N8 response therefore represents seroconversion following infection. However, we stress that these assumptions make our estimates of the case fatality rate relatively crude.

Distributions of the mortality rate among infected individuals were estimated in order to accommodate the effects of sampling and to allow for some uncertainty in the exact number of juvenile birds present in the population in December of each year electronic supplementary material, figure S2. The time between the first and last confirmed positive cases in swans at the site hereafter referred to as the outbreak period was 33 days for H5N1, 32 days for H5N8 and 31 days for H5N6.

Figure 1. Mortality among swans on the Fleet Lagoon. Brightly coloured bars include all mortality observed during the outbreak period, regardless of whether the carcasses were tested for AIV or AIV positivity. Pale-coloured bars indicate the mortality observed among birds on the Fleet Lagoon in periods when HPAIV was not detected, and therefore indicate the typical level of mortality observed among swans on the Fleet Lagoon. Colours indicate the respective outbreaks. During each of the outbreaks, several swans were observed to be compulsively spinning on the water.

Multiple birds, including one bird that was found to be positive for H5N6, were observed to be lethargic or to have very poor coordination. In the months following all three outbreaks, unusually high numbers of swans with severe torticollis abnormally twisted necks were observed. The four remaining birds were not tested, typically because carcasses were incomplete electronic supplementary material, figure S1.

Most of the remaining birds could not be tested because, owing to the scale of the outbreak, it became necessary to dispose of bird carcasses before testing could be conducted. The lower ratio of AIV-positive-to-negative birds in the H5N8 outbreak compared with the H5N6 outbreak is likely because AIV testing took place only at the start and end of the former electronic supplementary material, figure S1 ; if testing had occurred during the peak of mortality then a higher proportion of total deaths would have been attributable to AIV.

The basic reproductive number R 0 was estimated for the H5N8 and H5N6 epidemics from time series of the number of recovered carcasses at the site and an estimated epidemic generation time distribution; the latter was obtained from published experimental data for H5N8 viruses. The best-fitting distribution for this parameter was a Weibull distribution with a mean generation time of 2. Preliminary ML phylogenetic trees estimated for each segment showed that, for H5N8, all samples from the Fleet Lagoon formed a single, well-supported clade, consistent with a single introduction to the site.


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For H5N6, all sequences from the Fleet Lagoon clustered together, but monophyly of this grouping was less robust. For each outbreak, marginal posterior estimates of the date of the most recent common ancestor MRCA of the outbreak clade were obtained from the HA alignment.

Figure 2. Bayesian phylogenetic trees of HA sequences. Colours at tips indicate the location of sampling Asia: red, Europe including Russia : dark blue, Fleet Lagoon: bright blue. The location of this clade within the larger phylogeny is indicated by the linked vertical grey line in a. Nodes with posterior support values greater than 0. However, branch order within this clade is poorly resolved owing to the high genetic similarity of the outbreak sequences. The divergence date of the H5N8 outbreak clade with the most closely related non-outbreak viruses is estimated to be nearly 1 year prior to the MRCA of the H5N8 outbreak on the Fleet Lagoon.


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  8. We therefore cannot identify a likely source location for the H5N8 virus that was introduced to the Fleet Lagoon. Although we cannot rule out that possibility that the H5N6 outbreak strain originated from an unsampled location, the spatio-temporal proximity and genetic similarity of the UK and The Netherlands strains means that it is plausible that the H5N6 outbreak was introduced to the UK by migrating birds from The Netherlands.

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    The mute swan was known to be resident at the Fleet Lagoon. Given that infections in the mute swans were likely acquired locally, and the MRCA of the pochard and goose sequences is more recent than that of the swan, the pochard and goose may also have been infected locally.

    We tested the significance of the difference in mortality between juvenile less than 1 year and older birds for each outbreak using two-sided Fisher's exact tests. Juvenile birds died By contrast, during the same winter period of previous non-epidemic years — , juvenile birds were not significantly more likely to die than adult birds odds ratio 1. At the start of the H5N8 and H5N6 outbreaks December and , juvenile birds varied between and days old and and days old, respectively.

    Their last known weights, measured in September and October of their respective year of hatching, varied between 4. Generalized linear models were constructed to test whether juvenile birds that died during the H5N8 and H5N6 outbreaks had, on average, different ages or weights from juvenile birds that survived.

    When analysing the outbreaks both together and separately, there was a trend towards older juveniles and those that were below average weight upon ringing being more likely to survive the outbreak, but neither difference was significant p -value greater than 0. In order to investigate why mortality was significantly higher in juveniles than in older birds during the three HPAIV outbreaks, we conducted serological assays on blood collected from swans in our study population at multiple times during — When this cohort i.

    Figure 3. Seropositivity of swans. Colours represent birds hatched in different years. Birds that were sampled on more than one occasion have been removed. Samples were collected during June, July and November , but birds are grouped by hatch year only as no seasonal trend in change in titre was observed in these data.