Avian Influenza, Migratory Birds and Stable Isotopes

Over 100 species of wild migratory birds, particularly ducks, swans, geese and various wading birds, harbour avian influenza (AI) viruses. Infections are transmitted amongst the wild birds by shedding of the virus and contamination of water. Infection rates depend on time of year, location, the particular bird species and its age. Most of the influenza strains found in wild birds are of low pathogenicity that produces only mild disease in domesticated birds, whilst wild birds are unlikely to become sick. What has been of considerable concern over the last few years is the emergence of a pathogenic strain of avian influenza virus – Highly Pathogenic Avian Influenza of the H5N1 subtype (HPAI H5N1). This strain not only causes disease and death in wild birds and poultry, it can also affect humans. Over the past six years HPAI outbreaks have resulted in losses of US$20 billion to the poultry industry through the destruction of 300 million birds. Even more serious has been the occurrence of zoonotic HPAI, causing a disease with a high mortality, leading to the death of several hundred people. Similar influenza epidemics in the past have killed millions of people, and the threat of a pandemic disease caused by HPAI makes it potentially one of the most important animal and human health hazards facing mankind today. Estimates of the economic impact of pandemic disease caused by HPAI suggest that it would cost the global economy US$2 trillion, 3% of the world’s Gross Domestic Product.

Avian Influenza, Migratory Birds and Stable Isotopes The HPAI H5N1 strain emerged in China in 1996, affecting birds and causing human deaths too. Subsequently, the virus spread to other parts of China, South-East and South Asia. During these episodes, there was no evidence that wild birds were affected, or involved with the outbreaks in poultry. However, there was evidence in reports from South Africa some years previously that wild birds could be affected with fatal avian influenza. Evidence began to accrue however, to suggest that wild birds could play an important role in the dissemination of HPAI H5N1. The first clue was the finding of hundreds of HPAI infected geese dying in a lake in China. These were mostly Bar Fronted Geese, and there was concern that as these birds migrated to other parts of Asia, they might be a contributory factor in disease dissemination. Outbreaks of disease in Kazakhstan and Russia in which both wild birds and poultry were affected provided more circumstantial evidence for wild birds being involved in the spread of the disease. Since that time, amongst the European Union Member States, some 700 reported AI outbreaks have involved 25 species of wild birds. Analysis of data on bird migration and disease outbreaks compiled up to 2006 suggests that, in Europe, the most likely cause of AI introduction has been through migratory bird movements, but this was less so in Africa, whilst in Asia AI outbreaks were linked predominantly to poultry movement.

Given the potential of wild birds to spread AI, much more information is required about their movements. Millions of birds fly each year to and from overwintering sites, often stopping en route in several locations before resuming their journey to their summer or winter site. There is a general need to strengthen bird research in relation to AI, and in the case of migration, a more concerted effort is required to provide information on the poorly known routes of migrant birds in Africa, as well as the flyways in Central Asia, Asia-Pacific and the Neotropical Flyways. There is a great deal of information based on extrinsic markers such as ringing, but although data have been accumulated over many years, there are still substantial gaps in the knowledge base in regions where little or no data collection has been attempted.

Avian Influenza, Migratory Birds and Stable Isotopes One of the more recent developments in migratory bird tracking has been the use of radio telemetry to determine movements in breeding territories as well as international migratory routes. The concept depends on attaching a radio transmitter to the bird and then simply monitoring the movement by recording the radio-signal. Since it should be possible to identify an individual more readily and to monitor it more easily than mark and recapture studies a much more precise analysis of the pattern of movements is possible. Among potential drawbacks of the method is the high cost of organizing a survey, so that while it might offer precision, it does not enable cost-effective use of resources in all circumstances, additionally, it will be limited to relatively few individuals in the population. In any case, when dealing with AI outbreaks it would be useful to be able to pinpoint accurately the origin of the wild birds affected in some other way, since it is highly unlikely that the individuals concerned would have had any ringing devices, radio equipment or any other technologies applied at the point of departure. We need a technique that requires us to capture a bird only once, at the point of the disease outbreak (or to use samples from a dead bird) and without the need to mark it any way. An ideal approach to achieve this aim is to use stable isotope analysis (SIA), a technique that can provide us with the information that we need to establish the origin of a migratory bird.

Stable isotopes are the naturally occurring stable forms of elements with differing nuclear masses. As the name implies, they do not undergo radioactive decay; many elements have one or more stable isotopes and there are over 250 in existence. Fortunately, for our purposes, it is only necessary to concentrate analytical efforts on a small number of isotopes that are involved in many important biological and ecological processes. They are measured by mass spectrometry as isotopic differences relative to international standards prepared by IAEA and reported as ratios in delta (δ) units as parts per thousand.

Avian Influenza, Migratory Birds and Stable Isotopes The value of SIA is based on the strong correlation between levels of certain isotopes in the environment and the concentration of the same isotopes in avian tissues. A number of isotopes can be useful in studying animal movement, and fall into two categories: those of low atomic mass, Carbon (C), Nitrogen (N), Sulphur (S), Oxygen (O) and Hydrogen (H), and those of high atomic mass, Strontium (Sr) and Lead (Pb). The heavy isotopes are representative of environmental processes and can be used to trace uptake from soils.

The presence of the light isotopes in animal tissues depends on both biological and environmental processes. For example, stable carbon (δC-13) and nitrogen (δN-15) participate in biochemical processes in fixation in plants, but only δC-13 found in tissues reflects dietary intake, δ15N in tissues is often affected by water and nutritional stress. Stable sulphur (δS-34) varies widely in aquatic and terrestrial environments and reflects sources of nutrients in food webs. Of most interest are hydrogen (δ?D) and oxygen (δO-18) ratios in tissues that accurately reflect those in lakes, rivers and oceans and in groundwater recently originating from the atmosphere. The aim of studies on AI in migratory birds will be to distinguish and differentiate among populations. When using extrinsic markers only a few individuals are identified and these will be the only animals that can provide information about movement and origins. In contrast, using stable isotopes to characterize a population involves examining the isotopic signatures of a few individuals that are representative of the entire population. Once the signature of a population is known, any of the individuals from that population can provide information on movement. Studies are already in progress using stable isotopes to characterize and differentiate amongst bird populations using δC-13 and δN-15 values in metabolically active tissues (blood and muscle), but presently, the most effective tracers appear to be the hydrogen isotopes found in metabolically inert, seasonally grown tissues, such as feathers and claws. Feathers retain this information until replaced or moulted, typically once per year. Conversely, claws are continuously growing and can theoretically provide a time-integrated profile depending on claw growth rates. Once the isotope profile of a particular bird population is known, any individuals from the population can provide information on global migration of that species.

The hydrogen and oxygen isotope composition of environmental water varies spatially across the globe and because it is a constituent of many biosynthetic pathways, the isotopes’ presence is relayed to animal tissues, providing the means to link precipitation isotope values with those in biological tissues. Global grids of hydrogen and oxygen water isotopes have been constructed to provide accurate estimates of δD and δ18O in water that can then be compared to animal samples of known or unknown origin. These grids can be constructed using the data from the Global Network for Isotopes in Precipitation (GNIP) database collated by the IAEA. In terms of understanding HPAI, collecting isotope data from feathers of migratory bird species would reveal migration patterns and enable identification of the breeding areas of birds sampled in intermediate stopover sites, or non-breeding grounds, and in samples collected from disease outbreak sites.