The role of wild birds in the transmission of avian influenza for Australia : an ecological perspective

Waterbirds, particularly Anatidae, are natural reservoirs for low-pathogenic avian influenza and have been implicated as the primary source of infection in outbreaks of highly pathogenic avian influenza. An understanding of the movements of birds and the ecology of avian influenza viruses within the wild bird population is essential in assessing the risks to human health and production industries. Marked differences in the movements of Australian birds from those of the Northern Hemisphere emphasises the danger of generalising trends of disease prevalence to Australian conditions. Populations of Anatidae in Australia are not migratory, as they are in the Northern Hemisphere, but rather display typical nomadic traits, sometimes moving large distances across continental Australia in response to flooding or drought. There is little known regular interchange of anatids between Australia and Asia. In contrast, species such as shorebirds and some seabirds are annual migrants to Australia along recognised flyways from breeding grounds in the Northern Hemisphere. Movement into Australia by these species mainly occurs into the north-west and along the east coast over the Pacific Ocean. These species primarily arrive during the Australian spring and form large aggregations along the coastline and on inland wetlands. Other Australian migratory species (passerines, bee-eaters, dollar-birds, cuckoos, doves) regularly move to and from Asia through the Torres Strait Islands. The disease status of these birds is unknown. The movements of some species, particularly anatids and ardeids, which have ranges including Australia and regions where the virus is known to occur, have been poorly studied and there is potential for introduction of avian influenza subtypes via this route. Avian influenza viruses are highly unpredictable and can undergo reassortment to more pathogenic forms. There is insufficient knowledge of the epidemiology and transmission of these viruses in Australia and broad-scale surveillance of wild birds is logistically difficult. Long-term studies of anatids that co-habit with Charadriiformes are recommended. This would provide an indication of the spatial and temporal patterns of subtypes entering Australia and improve our understanding of the ecology of endemic viruses. Until such time as these data become available, Australia's preparedness for avian influenza must focus on biosecurity at the wild bird–poultry interface.

Surveillance of wild birds for avian influenza virus

Recent demand for increased understanding of avian influenza virus in its natural hosts, together with the development of high-throughput diagnostics, has heralded a new era in wildlife disease surveillance. However, survey design, sampling, and interpretation in the context of host populations still present major challenges. We critically reviewed current surveillance to distill a series of considerations pertinent to avian influenza virus surveillance in wild birds, including consideration of what, when, where, and how many to sample in the context of survey objectives. Recognizing that wildlife disease surveillance is logistically and financially constrained, we discuss pragmatic alternatives for achieving probability-based sampling schemes that capture this host-pathogen system. We recommend hypothesis-driven surveillance through standardized, local surveys that are, in turn, strategically compiled over broad geographic areas. Rethinking the use of existing surveillance infrastructure can thereby greatly enhance our global understanding of avian influenza and other zoonotic diseases.

Feeding wild birds in gardens: a test of water versus food

Bird feeding in residential gardens is an increasingly popular human-wildlife interaction. In Australia, the practice is discouraged by most government and nongovernment wildlife conservation agencies, although advice varies and the most common recommendation is to provide water and habitat for birds rather than supplementary food. This study compares bird abundance and diversity when residents in a Melbourne municipality provide water for birds versus food. Bird abundance was greater when food was provided compared with water, but avian assemblages did not differ.

Avian influenza virus dynamics in Australian wild birds

Understanding avian influenza infection dynamics in wildlife is crucial because of the possibility of virus spill over to livestock and humans. There are still knowledge gaps how different ecological and environmental factors influence infection dynamics in birds. My study highlights the importance of investigating disease dynamics in Australia.

A study of seed viability following consumption by birds

This project aimed to quantify the potential for wild birds to spread genetically modified seeds from their area of planting to adjacent areas, through ingestion and transport in the gut (endozoochorous transmission). We addressed this by assessing whether seed viability was affected by passage through the avian gut. We sought to address this question by testing the effects of ingestion of a number of key agricultural crops by three common wild bird pest species.

Migratory birds reinforce local circulation of avian influenza viruses

Migratory and resident hosts have been hypothesized to fulfil distinct roles in infectious disease dynamics. However, the contribution of resident and migratory hosts to wildlife infectious disease epidemiology, including that of low pathogenic avian influenza virus (LPAIV) in wild birds, has largely remained unstudied. During an autumn H3 LPAIV epizootic in free-living mallards (Anas platyrhynchos) - a partially migratory species - we identified resident and migratory host populations using stable hydrogen isotope analysis of flight feathers. We investigated the role of migratory and resident hosts separately in the introduction and maintenance of H3 LPAIV during the epizootic. To test this we analysed (i) H3 virus kinship, (ii) temporal patterns in H3 virus prevalence and shedding and (iii) H3-specific antibody prevalence in relation to host migratory strategy. We demonstrate that the H3 LPAIV strain causing the epizootic most likely originated from a single introduction, followed by local clonal expansion. The H3 LPAIV strain was genetically unrelated to H3 LPAIV detected both before and after the epizootic at the study site. During the LPAIV epizootic, migratory mallards were more often infected with H3 LPAIV than residents. Low titres of H3-specific antibodies were detected in only a few residents and migrants. Our results suggest that in this LPAIV epizootic, a single H3 virus was present in resident mallards prior to arrival of migratory mallards followed by a period of virus amplification, importantly associated with the influx of migratory mallards. Thus migrants are suggested to act as local amplifiers rather than the often suggested role as vectors importing novel strains from afar. Our study exemplifies that a multifaceted interdisciplinary approach offers promising opportunities to elucidate the role of migratory and resident hosts in infectious disease dynamics in wildlife.

Flying, fasting, and feeding in birds during migration: a nutritional and physiological ecology perspective

Unlike exercising mammals, migratory birds fuel very high intensity exercise (e.g., flight) with fatty acids delivered from the adipose tissue to the working muscles by the circulatory system. Given the primary importance of fatty acids for fueling intense exercise, we discuss the likely limiting steps in lipid transport and oxidation for exercising birds and the ecological factors that affect the quality and quantity of fat stored in wild birds. Most stored lipids in migratory birds are comprised of three fatty acids (16:0, 18:1 and 18:2) even though migratory birds have diverse food habits. Diet selection and selective metabolism of lipids play important roles in determining the fatty acid composition of birds which, in turn, affects energetic performance during intense exercise. As such, migratory birds offer an intriguing model for studying the implications of lipid metabolism and obesity on exercise performance. We conclude with a discussion of the energetic costs of migratory flight and stopover in birds, and its implications for bird migration strategies.

Avian influenza in Australia : a summary of 5 years of wild bird surveillance

BACKGROUND: Avian influenza viruses (AIVs) are found worldwide in numerous bird species, causing significant disease in gallinaceous poultry and occasionally other species. Surveillance of wild bird reservoirs provides an opportunity to add to the understanding of the epidemiology of AIVs. METHODS: This study examined key findings from the National Avian Influenza Wild Bird Surveillance Program over a 5-year period (July 2007-June 2012), the main source of information on AIVs circulating in Australia. RESULTS: The overall proportion of birds that tested positive for influenza A via PCR was 1.9 ± 0.1%, with evidence of widespread exposure of Australian wild birds to most low pathogenic avian influenza (LPAI) subtypes (H1-13, H16). LPAI H5 subtypes were found to be dominant and widespread during this 5-year period. CONCLUSION: Given Australia's isolation, both geographically and ecologically, it is important for Australia not to assume that the epidemiology of AIV from other geographic regions applies here. Despite all previous highly pathogenic avian influenza outbreaks in Australian poultry being attributed to H7 subtypes, widespread detection of H5 subtypes in wild birds may represent an ongoing risk to the Australian poultry industry.

Seasonal and habitat related variation in the health of tropical savanna finches

Differences in habitat quality can affect the abundance, distribution, and physiological status of wild birds. In Australia’s tropical savannas, grass finches live in habitats of varying land use and resultant habitat quality. Recent studies have documented regional declines in the abundance and distribution of small granivorous birds in areas affected by cattle grazing, urban development, and changes in fire frequency and timing. Small birds, especially semi-nomadic species of grass-finches, are extremely difficult to survey for changes in local abundance and productivity. Consequently, we are using a range of physiological measures to determine the susceptibility of populations to decline. We present the preliminary findings of a study using multiple condition indices to describe the health of five grass finch species living in a variety of savanna habitats. Our early results suggest that simple body condition measures such as bird mass, muscle contour, and fat storage, are not always sensitive enough to identify subtle differences in the health of individuals and populations. Measures of haematological health state, stress, and background nutritional status of finch populations appear to be associated with seasonal and site differences where body condition measures or abundance surveys would have failed to present a coherent picture. We are using habitat characteristics important to these species to help explain the differences in the health of finch populations across the North.

Use of satellite telemetry on small-bodied waterfowl in Australia

The nomadic or dispersive movements of many Australian waterfowl in response to irregular environmental cues make satellite telemetry studies the only means by which these long-distance movements can be tracked in real time. Unlike some large-bodied soaring species, attaching satellite transmitters to small-bodied waterfowl (<1 kg) is not straightforward because ducks have high wing loadings and need to maintain active flapping to stay aloft. In the present paper, we detail one harness design and attachment method that enabled us to track grey teal (Anas gracilis) for up to 879 days. In addition, we detail rates of data loss, changes in data quality over time and variation in data quality from solar-powered satellite-tags deployed on ducks in Australia and Papua New Guinea. Up to 68% of all locational fixes have a nominal accuracy of less than 1 km, and satellite-tags deployed on wild birds can provide up to 22 location fixes per day and store enough energy during the day to run continuously throughout the night.

Mimicry and the eye of the beholder

Recent experiments (Dittrich et al. (Proc. R. Soc. Lond. B 251, 195 (1993))) suggest that pigeon perception of wasp mimicry by hoverflies is similar to that of humans and of computer-based image matching. However, the relations are nonlinear and may explain why some species are abundant despite their being poor mimics to the human eye. We suggest that these discrepancies between pigeon and human categorization may lie in the differences between avian and primate colour vision. As pigeon categorization and computer image analysis were both assessed by using colour slides designed for human vision, they lacked the natural colour information available to wild birds, in particular that from ultraviolet (uv) wavelengths.

How to find natural reservoir hosts from endemic prevalence in a multi-host population : a case study of influenza in waterfowl

The transmission dynamics of infectious diseases critically depend on reservoir hosts, which can sustain the pathogen (or maintain the transmission) in the population even in the absence of other hosts. Although a theoretical foundation of the transmission dynamics in a multi-host population has been established, no quantitative methods exist for the identification of natural reservoir hosts. For a host to maintain the transmission alone, the host-specific reproduction number (U), interpreted as the average number of secondary transmissions caused by a single primary case in the host(s) of interest in the absence of all other hosts, must be greater than unity. If the host-excluded reproduction number (Q), representing the average number of secondary transmissions per single primary case in other hosts in the absence of the host(s) of interest, is below unity, transmission cannot be maintained in the multi-host population in the absence of the focal host(s).

The present study proposes a simple method for the identification of reservoir host(s) from observed endemic prevalence data across a range of host species. As an example, we analyze an aggregated surveillance dataset of influenza A virus in wild birds among which dabbling ducks exhibit higher prevalence compared to other bird species. Since the heterogeneous contact patterns between different host species are not directly observable, we test four different contact structures to account for the uncertainty. Meeting the requirements of U > 1 and Q < 1 for all four different contact structures, mallards and other dabbling ducks most likely constitute the reservoir community which plays a predominant role in maintaining the transmission of influenza A virus in the water bird population. We further discuss epidemiological issues which are concerned with the interpretation of influenza prevalence data, identifying key features to be fully clarified in the future.

Identifying crucial gaps in our knowledge of the life-history of avian influenza viruses - An Australian perspective

We review our current knowledge of the epidemiology and ecology of avian influenza viruses (AIVs) in Australia in relation to the ecology of their hosts. Understanding the transmission and maintenance of low-pathogenic avian influenza (LPAI) viruses deserves scientific scrutiny because some of these may evolve to a high-pathogenic AIV (HPAI) phenotype. That the HPAI H5N1 has not been detected in Australia is thought to be a result of the low level of migratory connectivity between Asia and Australia. Some AIV strains are endemic to Australia, with Australian birds acting as a reservoir for these viruses. However, given the phylogenetic relationships between Australian and Eurasian strains, both avian migrants and resident birds within the continent must play a role in the ecology and epidemiology of AIVs in Australia. The extent to which individual variation in susceptibility to infection, previous infections, and behavioural changes in response to infection determine AIV epidemiology is little understood. Prevalence of AIVs among Australian avifauna is apparently low but, given their specific ecology and Australian conditions, prevalence may be higher in little-researched species and under specific environmental conditions.

You are what you eat : influence of host ecology on infection risk in populations and individuals

It is widely accepted that wild aquatic birds are the major reservoir for Avian Influenza viruses (AIV), and also play a significant role as vectors for the disease. However, despite intensive surveillance, we still know very little about the role individual wild birds (and their populations) play in the transmission and maintenance of these viruses. Traditionally, combinations of single-location surveillance and historical migration patterns have been used to estimate the degree to which different species may be involved. However, this broad scale approach tends to neglect the ecology of the virus, and just as importantly, the ecology of the host. Over 100 species have been found infected with these viruses worldwide, with many more purportedly negative for the disease. Using data from ten years of wild bird surveillance in the Netherlands we catalogued the ecological properties of each species sampled, in order to determine whether infected species are ecologically separated from those that are not. Using stable isotope analysis of feathers and blood components, we also examine whether infection risk of individuals within a species known to be infected by AIV can be attributable to antecedent foraging habitats. The use of an aquatic habitat is strongly associated with infection risk at all levels analysed, including individuals and populations of a single species, and between species. These unique findings underscore the usefulness of stable isotope methods in disease ecology, particularly when compared to broader-scale inter-species patterns, and the potential role of host ecology in transmission and maintenance of AIV.

Avian influenza from an ecohealth perspective

To understand and better control AI outbreaks, not only is it necessary to understand the biology of influenza viruses but also the natural history of the hosts in which these viruses multiply and the different environments in which the hosts and viruses interact. This includes the anthropogenic factors that have influenced where, whether and how avian influenza (AI) viruses can replicate and transmit between wild birds and poultry, and between poultry and mammals, including factors influencing uptake and application of appropriate control and preventive measures for AI. This disease represents one of the best examples of the need for a ‘One Health’ approach to understand and tackle disease with an increasing need to comprehend and unravel the environmental and ecology drivers that affect the virus host interactions. This forum piece seeks to bring together these aspects through a review of recent outbreaks and how a deeper understanding of all three aspects, the virus, the host and the environment, can help us better manage future outbreaks.