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Potential spread of highly pathogenic avian influenza H5N1 by wildfowl: dispersal ranges and rates determined from large-scale satellite telemetry

1. Migratory birds are major candidates for long-distance dispersal of zoonotic pathogens. In recent years, wildfowl have been suspected of contributing to the rapid geographic spread of the highly pathogenic avian influenza (HPAI) H5N1 virus. Experimental infection studies reveal that some wild ducks, geese and swans shed this virus asymptomatically and hence have the potential to spread it as they move. 2. We evaluate the dispersive potential of HPAI H5N1 viruses by wildfowl through an analysis of the movement range and movement rate of birds monitored by satellite telemetry in relation to the apparent asymptomatic infection duration (AID) measured in experimental studies. We analysed the first large-scale data set of wildfowl movements, including 228 birds from 19 species monitored by satellite telemetry in 2006–2009, over HPAI H5N1 affected regions of Asia, Europe and Africa. 3. Our results indicate that individual migratory wildfowl have the potential to disperse HPAI H5N1 over extensive distances, being able to perform movements of up to 2900 km within timeframes compatible with the duration of asymptomatic infection. 4. However, the likelihood of such virus dispersal over long distances by individual wildfowl is low: we estimate that for an individual migratory bird there are, on average, only 5–15 days per year when infection could result in the dispersal of HPAI H5N1 virus over 500 km. 5. Staging at stopover sites during migration is typically longer than the period of infection and viral shedding, preventing birds from dispersing a virus over several consecutive but interrupted long-distance movements. Intercontinental virus dispersion would therefore probably require relay transmission between a series of successively infected migratory birds. 6. Synthesis and applications . Our results provide a detailed quantitative assessment of the dispersive potential of HPAI H5N1 virus by selected migratory birds. Such dispersive potential rests on the assumption that free-living wildfowl will respond analogously to captive, experimentally-infected birds, and that asymptomatic infection will not alter their movement abilities. Our approach of combining experimental exposure data and telemetry information provides an analytical framework for quantifying the risk of spread of avian-borne diseases.

Journal of Applied Ecology

Control of avian influenza: Philosophy and perspectives on behalf of migratory birds

Aquatic birds are considered the primary reservoir for influenza A viruses (Nettles et al., 1987). However, there is little concern about avian influenza among conservation agencies responsible for the welfare of those species. IN contrast, the poultry industry has great concern about avian influenza and view aquatic birds as a source for infection of poultry flocks. In some instances, differences in these perspectives created conflict between conservation agencies and the poultry industry. I speak on behalf of migratory birds, but philosophy and perspectives offered are intended to be helpful to the poultry industry in their efforts to combat avian influenza.

Avian Diseases

Causes of mortality in common loons

Summarized are necropsy results from 222 carcasses of Common Loons ( Gavia immer ) submitted to the National Wildlife Health Research Center from 1976 through 1991. The carcasses were from 18 states, and 10 or more birds each were from Minnesota, Florida, Virginia, Michigan, Wisconsin, Maine, and North Carolina. Seventy-three (33%) carcasses were emaciated, and in some of these birds emaciation was thought to be related to exposure to mercury. OVer 40% of these emaciated birds were from Florida. Trauma, including blunt trauma of unknown origin, outboard motor propeller wounds, and shooting caused the deaths of 49 (22%) loons, 30 of which were from Minnesota. Diseases, primarily avian botulism type E and aspergillosis, account for 39 (18%) moralities and lead poisoning for 14 (6%), 11 of which had fishing sinkers in their stomachs. Most of the avian botulism type E cases occurred during two outbreaks on Lake Michigan. Seven of the 14 lead-poisoned birds were from Minnesota. Nine (4%) birds died of miscellaneous causes and 9 (4%) of drowning, primarily from entanglement in nets. No diagnosis could be reached for 29 (13%) carcasses. Sample bias precludes interpretation of these data to represent actual proportional causes of mortality in the loon population. However, the sample size is sufficient to clearly identify major causes of mortality.

Minnesota, Florida, Virginia, Michigan, Wisconsin,

Gene expression reveals immune response strategies of naïve Hawaiian honeycreepers experimentally infected with introduced avian malaria

The unprecedented rise in the number of new and emerging infectious diseases in the last quarter century poses direct threats to human and wildlife health. The introduction to the Hawaiian archipelago of Plasmodium relictum and the mosquito vector that transmits the parasite has led to dramatic losses in endemic Hawaiian forest bird species. Understanding how mechanisms of disease immunity to avian malaria may evolve is critical as climate change facilitates increased disease transmission to high elevation habitats where malaria transmission has historically been low and the majority of the remaining extant Hawaiian forest bird species now reside. Here, we compare the transcriptomic profiles of highly susceptible Hawai‘i ‘amakihi ( Chlorodrepanis virens ) experimentally infected with P. relictum to those of uninfected control birds from a naïve high elevation population. We examined changes in gene expression profiles at different stages of infection to provide an in-depth characterization of the molecular pathways contributing to survival or mortality in these birds. We show that the timing and magnitude of the innate and adaptive immune response differed substantially between individuals that survived and those that succumbed to infection, and likely contributed to the observed variation in survival. These results lay the foundation for developing gene-based conservation strategies for Hawaiian honeycreepers by identifying candidate genes and cellular pathways involved in the pathogen response that correlate with a bird’s ability to recover from malaria infection.

Hawaii

Can lowland dry forests represent a refuge from avian malaria for native Hawaiian birds?

Hawaii's native birds have become increasingly threatened over the past century. Introduced mosquito borne diseases such as avian malaria may be responsible for the near absence of endemic Hawaiian forest birds in low-elevation habitats. The recent recognition that some native Hawaiian forest birds may be repopulating moist lowland habitats as a result of evolved resistance to this disease has increased the conservation value of these areas. Here, we investigate whether remnant low elevation dry forests on Hawaii Island provide natural 'refuges' from mosquito-transmitted malaria by nature of their low rainfall and absence of suitable natural sources of water for mosquito breeding. Unlike lowland wet forests where high rates of disease transmission may be selecting for disease resistance, lowland dry forests may provide some refuge for native forest birds without natural resistance to malaria. We mistnetted forest birds in two lowland dry forests and tested all native birds by microscopy and serology for avian malaria caused by the Plasmodium relictum parasite. We also conducted surveys for standing water and mosquito larvae. Overall prevalence of infections with Plasmodium relictum in the Hawaii Amakihi Hemignathus virens virens was 15%. Most infected birds had lowlevel parasitemias, suggesting chronic infections. Although avian malaria is present in these lowland dry forest Amakihi populations, infection rates are significantly lower than in wet forest populations at similar elevations. Sources of breeding mosquitoes in these forests appeared to be largely anthropogenic; thus, there is potential to manage dry forests as mosquito-free habitat for Hawaii Amakihi and other Hawaiian forest birds.

Hawai'i

Avian influenza in wild birds

Influenza A viruses (IAVs)maintained among wild waterfowl, gulls, shorebirds, and some seabirds, and typically do not cause disease. Some avian-origin IAVs that have previously spilled over into domestic poultry have developed a highly pathogenic phenotype and have become important pathogens affecting both wild birds and poultry. These avian-origin IAVs have important implications to the production and trade of domestic birds, conservation and management of wild birds, and the risk of spillover of zoonotic influenza to humans handling infected birds.

Book chapter

Disease emergence and resurgence—the wildlife-human connection

In 2000, the Global Outbreak Alert and Response Network (GOARN) was organized as a global disease watchdog group to coordinate disease outbreak information and health crisis response. The World Health Organization (WHO) is the headquarters for this network. Understandably, the primary focus for WHO is human health. However, diseases such as the H5N1 avian influenza epizootic in Asian bird populations demonstrate the need for integrating knowledge about disease emergence in animals and in humans. Aside from human disease concerns, H5N1 avian influenza has major economic consequences for the poultry industry worldwide. Many other emerging diseases, such as severe acute respiratory syndrome (SARS), monkeypox, Ebola fever, and West Nile fever, also have an important wildlife component. Despite these wildlife associations, the true integration of the wildlife component in approaches towards disease emergence remains elusive. This separation between wildlife and other species’ interests is counterproductive because the emergence of zoonotic viruses and other pathogens maintained by wildlife reservoir hosts is poorly understood. This book is about the wildlife component of emerging diseases. It is intended to enhance the reader’s awareness of the role of wildlife in disease emergence. By doing so, perhaps a more holistic approach to disease prevention and control will emerge for the benefit of human, domestic animal, and free-ranging wildlife populations alike. The perspectives offered are influenced by more than four decades of my experiences as a wildlife disease practitioner. Although wildlife are victims to many of the same disease agents affecting humans and domestic animals, many aspects of disease in free-ranging wildlife require different approaches than those commonly applied to address disease in humans or domestic animals. Nevertheless, the broader community of disease investigators and health care professionals has largely pursued a separatist approach for human, domestic animal, and wildlife rather than embracing the periodically proposed concept of “one medicine.” We especially need to embrace this concept as the human population increases because there will be more contact, direct and indirect, among humans, domestic animals, and wildlife. An “Ecology for a Crowded Planet” will be an even more pressing concern, and that includes increasing our understanding of disease ecology, especially that of the zoonoses.

Circular

Infectious diseases, parasites, and biological toxins in sea ducks

This chapter addresses disease agents in the broad sense, including viruses, bacteria, fungi, protozoan and helminth parasites, and biological toxins. Some of these agents are known to cause mortality in sea ducks, some are thought to be incidental findings, and the significance of others is yet poorly understood. Although the focus of the chapter is on free-living sea ducks, the study of disease in this taxonomic group has been relatively limited and examples from captive sea ducks and other wild waterfowl are used to illustrate the pathogenicity of certain diseases. Much of the early work in sea ducks consisted of anecdotal and descriptive reports of parasites, but it was soon recognized that diseases such as avian cholera, renal coccidiosis, and intestinal infections with acanthocephalans were causes of mortality in wild populations. More recently, adenoviruses, reoviruses, and the newly emergent Wellfleet Bay virus, for example, also have been linked to die-offs of sea ducks. Declining populations of animals are particularly vulnerable to the threats posed by disease and it is important that we improve our understanding of the significance of disease in sea ducks. To conclude, we offer our recommendations for future directions in this field.

Book chapter

Chapter 5: Health and diseases

Health and diseases are integral parts of the life of seabirds that merit attention if we expect to truly understand, protect, and conserve them. Diseases such as avian influenza, avian pox, pasteurellosis, and paralytic shellfish poisoning have a proven history of decreasing the survival or breeding success of seabirds. However, each host-pathogen-environment system is unique, and our current knowledge about seabird health is limited and subject to biases. Thus, an exploratory mindset should be maintained, always considering that new or previously undiagnosed diseases could have substantial effects on a given seabird population. Therefore, incorporating a health monitoring component in seabird population monitoring programs, wherein data and biological samples are routinely collected for long-term pathogen surveillance and physiological analyses, would help us understand factors that limit seabird populations. Finally, the implementation of biosecurity best practices at seabird aggregations is imperative to avoid the accidental introduction or spread of pathogens.

Book chapter

Comparative genomics analyses support the reclassification of Bisgaard taxon 40 as Mergibacter gen. nov., with Mergibacter septicus sp. nov. as type species: Novel insights into the phylogeny and virulence factors of a Pasteurellaceae family member associated with mortality events in seabirds

The Pasteurellaceae family has been associated with fatal diseases in numerous avian species. Several new taxa within this family, including Bisgaard taxon 40, have been recently described in wild birds, but their genomic characteristics and pathogenicity are not well understood. We isolated Bisgaard taxon 40 from four species of seabirds, including one sampled during a mass, multi-species mortality event in Florida, United States. Here, we present a comprehensive phenotypic and genetic characterization of Bisgaard taxon 40 and comparative genomic analysis with reference strains from the Pasteurellaceae family, aiming at determining its phylogenetic position, antimicrobial susceptibility profile, and identifying putative virulence factors. In silico multilocus sequence-based and whole-genome-based phylogenetic analysis clustered all Bisgaard taxon 40 strains together on a distinct branch separated from the other members of the Pasteurellaceae family, indicating that Bisgaard taxon 40 could represent a new genus. These findings were further supported by protein similarity analyses using the concatenation of 31 conserved proteins and other taxonomic approaches such as the percentage of conserved protein test. Additionally, several putative virulence factors were identified, including those associated with adhesion (capsule, ompA , ompH ) and colonization ( exbD , fur , galU , galE , lpxA , lpxC , and kdsA ) of the host and a cytolethal distending toxin ( cdt ), which may have played a role in disease development leading to the mortality event. Considerably low minimum inhibitory concentrations (MICs) were found for all the drugs tested, in concordance with the absence of antimicrobial resistance genes in these genomes. The novel findings of this study highlight genomic and phenotypic characteristics of this bacterium, providing insights into genome evolution and pathogenicity. We propose a reclassification of these organisms within the Pasteurellaceae family, designated as Mergibacter gen. nov., with Mergibacter septicus sp. nov. as the type species. The type strain is Mergibacter septicus A25201 T (=DSM 112696).

Frontiers in Microbiology

Wetland environmental conditions associated with the risk of avian cholera outbreaks and the abundance of Pasteurella multocida

Avian cholera is a significant infectious disease affecting waterfowl across North America and occurs worldwide among various avian species. Despite the importance of this disease, little is known about the factors that cause avian cholera outbreaks and what management strategies might be used to reduce disease mortality. Previous studies indicated that wetland water conditions may affect survival and transmission of Pasteurella multocida, the agent that causes avian cholera. These studies hypothesized that water conditions affect the likelihood that avian cholera outbreaks will occur in specific wetlands. To test these predictions, we collected data from avian cholera outbreak and non-outbreak (control) wetlands throughout North America (wintera??spring 1995a??1996 to 1998a??1999) to evaluate whether water conditions were associated with outbreaks. Conditional logistic regression analysis on paired outbreak and non-outbreak wetlands indicated no significant association between water conditions and the risk of avian cholera outbreaks. For wetlands where avian cholera outbreaks occurred, linear regression showed that increased eutrophic nutrient concentrations (Potassium [K], nitrate [NO3], phosphorus [P], and phosphate [PO3]) were positively related to the abundance of P. multocida recovered from water and sediment samples. Wetland protein concentration and an El Ni??o event were also associated with P. multocida abundance. Our results indicate that wetland water conditions are not strongly associated with the risk of avian cholera outbreaks; however, some variables may play a role in the abundance of P. multocida bacteria and might be important in reducing the severity of avian cholera outbreaks.

Journal of Wildlife Management

Blood parasites in Owls with conservation implications for the Spotted Owl (Strix occidentalis)

The three subspecies of Spotted Owl (Northern, Strix occidentalis courina; California, S. o. occidentalis; and Mexican, S. o. lucida) are all threatened by habitat loss and range expansion of the Barred Owl (S. varia). An unaddressed threat is whether Barred Owls could be a source of novel strains of disease such as avian malaria (Plasmodium spp.) or other blood parasites potentially harmful for Spotted Owls. Although Barred Owls commonly harbor Plasmodium infections, these parasites have not been documented in the Spotted Owl. We screened 111 Spotted Owls, 44 Barred Owls, and 387 owls of nine other species for haemosporidian parasites (Leucocytozoon, Plasmodium, and Haemoproteus spp.). California Spotted Owls had the greatest number of simultaneous multi-species infections (44%). Additionally, sequencing results revealed that the Northern and California Spotted Owl subspecies together had the highest number of Leucocytozoon parasite lineages (n=17) and unique lineages (n=12). This high level of sequence diversity is significant because only one leucocytozoon species (L. danilewskyi) has been accepted as valid among all owls, suggesting that L. danilewskyi is a cryptic species. Furthermore, a Plasmodium parasite was documented in a Northern Spotted Owl for the first time. West Coast Barred Owls had a lower prevalence of infection (15%) when compared to sympatric Spotted Owls (S. o. caurina 52%, S. o. occidentalis 79%) and Barred Owls from the historic range (61%). Consequently, Barred Owls on the West Coast may have a competitive advantage over the potentially immune compromised Spotted Owls. ?? 2008 Ishak et al.

PLoS ONE

Avian vacuolar myelinopathy: a newly recognized fatal neurologic disease of eagles, waterfowl, and other birds

Wildlife biologists and health specialists have been frustrated by a long list of negative findings in their AVM investigations, however studies continue to provide pieces of information to aid the determination of the cause and its source. Available data indicated that AVM may have been present since at least 1990, occurs in at least five states, has been documented during October through April at sites of wintering populations of birds where the exposure apparently occurs, and has killed at least 90 bald eagles. Birds with AVM have difficulty or inability to fly, swim, walk, or perch, but there has been resolution of clinical signs in some affected coots. The list of affected species continues to grow, but remains confined to wild avians, including bald eagle, American coot, great horned owl, killdeer, Canada goose, mallard, ring-necked duck and bufflehead. The effects of the AVM agent on mammals, including human beings, are unknown. A neurotoxicant of manmade or natural origin is the suspected cause of AVM because no infectious disease agents, such as viruses, bacteria, parasites and prions, have been found, and the lesion and epizootiology of AVM resemble those of toxicoses. Additionally it is documented, experimentally, that exposure to raptors can occur through ingestion of infected coots. Collaborative studies will continue in the effort to identify the cause of AVM, its geographic distribution, and the range of species susceptibility. Hopefully, this information can be used to identify measures that might be taken to reduce the impact of AVM on the wildlife resource. Multiple agencies, institutions, and individuals must rely on each other's expertise in the multidisciplinary approach to this problem, persevere in their efforts and take advantage of serendipity that presents itself during investigations of this newly recognized cause of wild bird mortality.

Arkansas, Georgia, North Carolina, South Carolina

Avian influenza shedding patterns in waterfowl: implications for surveillance, environmental transmission, and disease spread

Despite the recognized importance of fecal/oral transmission of low pathogenic avian influenza (LPAI) via contaminated wetlands, little is known about the length, quantity, or route of AI virus shed by wild waterfowl. We used published laboratory challenge studies to evaluate the length and quantity of low pathogenic (LP) and highly pathogenic (HP) virus shed via oral and cloacal routes by AI-infected ducks and geese, and how these factors might influence AI epidemiology and virus detection. We used survival analysis to estimate the duration of infection (from virus inoculation to the last day virus was shed) and nonlinear models to evaluate temporal patterns in virus shedding. We found higher mean virus titer and longer median infectious period for LPAI-infected ducks (10–11.5 days in oral and cloacal swabs) than HPAI-infected ducks (5 days) and geese (7.5 days). Based on the median bird infectious dose, we found that environmental contamination is two times higher for LPAI- than HPAI-infectious ducks, which implies that susceptible birds may have a higher probability of infection during LPAI than HPAI outbreaks. Less environmental contamination during the course of infection and previously documented shorter environmental persistence for HPAI than LPAI suggest that the environment is a less favorable reservoir for HPAI. The longer infectious period, higher virus titers, and subclinical infections with LPAI viruses favor the spread of these viruses by migratory birds in comparison to HPAI. Given the lack of detection of HPAI viruses through worldwide surveillance, we suggest monitoring for AI should aim at improving our understanding of AI dynamics (in particular, the role of the environment and immunity) using long-term comprehensive live bird, serologic, and environmental sampling at targeted areas. Our findings on LPAI and HPAI shedding patterns over time provide essential information to parameterize environmental transmission and virus spread in predictive epizootiologic models of disease risks.

Journal of Wildlife Diseases

Prevalence and diversity of avian blood parasites in a resident northern passerine

Background: Climate-related changes are expected to influence the prevalence and distribution of vector-borne haemosporidian parasites at northern latitudes, although baseline information about resident birds is still lacking. In this study, we investigated prevalence and genetic diversity of Plasmodium, Haemoproteus, and Leucocytozoon parasites infecting the Northwestern Crow (Corvus caurinus), a non-migratory passerine with unique life-history characteristics. This species occupies both intertidal and forested habitats and is subject to high prevalence of avian keratin disorder (AKD), a disease that causes gross beak deformities. Investigation of avian blood parasites in Northwestern Crows at sites broadly distributed across coastal Alaska provided an opportunity to evaluate specific host factors related to parasite infection status and assess geographic patterns of prevalence. Results: We used molecular methods to screen for haemosporidian parasites in Northwestern Crows and estimated genus-specific parasite prevalence with occupancy modeling that accounts for imperfect detection of parasite infection. We observed considerable geographic and annual variation in prevalence of Plasmodium, Haemoproteus, and Leucocytozoon , but these patterns were not correlated with indices of local climatic conditions. Our models also did not provide support for relationships between the probability of parasite infection and body condition or the occurrence of co-infections with other parasite genera or clinical signs of AKD. In our phylogenetic analyses, we identified multiple lineages of each parasite genus, with Leucocytozoon showing greater diversity than Plasmodium or Haemoproteus. Conclusions: Results from this study expand our knowledge about the prevalence and diversity of avian blood parasites in northern resident birds as well as corvids worldwide. We detected all three genera of avian haemosporidians in Northwestern Crows in Alaska, although only Leucocytozoon occurred at all sites in both years. Given the strong geographic and interannual variation in parasite prevalence and apparent lack of correlation with climatic variables, it appears that there are other key factors responsible for driving transmission dynamics in this region. Thus, caution is warranted when using standard climatic or geographic attributes in a predictive framework. Our phylogenetic results demonstrate lower host specificity for some lineages of Leucocytozoon than is typically reported and provide insights about genetic diversity of local haemosporidian parasites in Alaska.

Parasites & Vectors

Thermal constraints to the sporogonic development and altitudinal distribution of avian malaria Plasmodium relictum in Hawai'i

More than half of the Hawaiian honeycreepers (Drepanidinae) known from historical records are now extinct. Introduced mosquito-borne disease, in particular the avian malaria Plasmodium relictum , has been incriminated as a leading cause of extinction during the 20th century and a major limiting factor in the recovery of remaining species populations. Today, most native Hawaiian bird species reach their highest densities and diversity in high elevation (>1,800 m above sea level) forests. We determined the thermal requirements for sporogonic development of P. relictum in the natural vector, Culex quinquefasciatus , and assessed the current distribution of native bird species in light of this information. Sporogonic development was completed at constant laboratory and mean field temperatures between 30 and 17 C, but development, prevalence, and intensity decreased significantly below 21 C. Using a degree-day (DD) model, we estimated a minimum threshold temperature of 12.97 C and a thermal requirement of 86.2 DD as necessary to complete development. Predicted (adiabatic lapse-rate) and observed summer threshold isotherm (13 C) correspond to the elevation of high forest refuges on the islands of Maui and Hawai'i. Our data support the hypothesis that avian malaria currently restricts the altitudinal distribution of Hawaiian honeycreeper populations and provide an ecological explanation for the absence of disease at high elevation.

Hawaii