Highly Pathogenic avian influenza H5N1 and wild birds:
a review of the evidence
(An outline of a presentation made by Nial Moores, Birds Korea, to a symposium on Avian Influenza at the
Migratory Birds Observation centre in Gunsan, organized by UNDP-GEF and local bird conservation and citizens groups,
on 7 December, 2006.)


Highly Pathogenic Avian Influenza H5N1 is a significant threat to the poultry industry, to the livelihoods of farmers, and also to wild birds. It also poses a health threat to people who work in very close contact with infected poultry or caged birds. As such, everybody can agree that it is extremely important to identify ways in which to prevent the spread of the disease into new areas; and to eradicate the virus in areas where it has already been found. This can, in the first, best be achieved through accurate reporting and open communication between specialists in different fields: farmers, veterinary scientists, health specialists, transport specialists and ornithologists.

Birds Korea is a specialist bird conservation organization, and I personally am not a specialist in disease, but instead an ornithologist who has researched and published papers and articles on migratory waterbirds in a number of countries. I have also been part of an international discussion group, now called AI-Watch, for two years or so. This international group, initiated by the global conservation organisation Birdlife International, discusses outbreaks and publications on the disease, and has several of the world's top experts on this disease as its members, including Professor Chris Feare, who has advised the European Union on the disease, and Dr. Billy Karesh, co-chair of the IUCN Species Survival Commission, and Chief of Party for the Global Avian Influenza Network for Surveillance for wild birds.

Today, I want especially to communicate the opinions of experts such as these, supported by published information and ornithological insights, describing the history of the H5N1 virus, and its relationship to wild bird populations.

Before proceeding any further, however, it is best to start with this statement, made by Dr. Vincent Martin, an expert in animal disease working for the Food and Agriculture Organisation of the United Nations. He stated, in November 2006, that the evidence shows that "migratory birds do not play a major role in the transmission of the highly pathogenic avian influenza H5N1", rather "the spread of bird flu is mainly the result of the world's fast and unregulated development of animal production" (Xinhua News, November 2, 2006). Today's presentation is an introduction to this evidence.

Background to Avian Influenza and HP H5N1

H5N1 is one of at least 144 strains of avian influenza, all of which can be divided into two classes, according to their disease-causing ability or pathogenicity. Low pathogenic strains, LP, are quite widespread, especially in waterbirds, like ducks. These cause no, or only mild, illness, in wild birds. However, strains of the H5 and H7 subtypes can occasionally become highly pathogenic, HP, following a specific mutation. As these viruses are spread most efficiently through close contact with infected feces or other bodily fluids, one bird to the next, they can cause great mortality in crowded poultry flocks but are extremely rare in wild birds. The first such case in wild birds was reported only in 1961.

Outbreaks of HP Avian Influenza in poultry, in contrast, have a very long history, and are becoming more frequent as the industrialisation of poultry-farming increases rapidly. HP Avian Influenza outbreaks were already being described in the 1800s as "fowl plague." Between 1959 and 2000, there were at least 17 primary outbreaks of HP Avian Influenza in poultry worldwide, with 8 of these outbreaks coming between 1990 and 2000. It can be suggested simply that poultry (domesticated chickens, ducks, geese and turkeys), are not biologically suited to being "housed" in the unnatural conditions in which they find themselves. These conditions create what have been termed disease-making factories by author Wendy Orent. (This connection between the disease and poultry is also why Birds Korea uses the term "Poultry Flu" to describe "Highly Pathogenic Avian Influenza Type A H5N1".)

The H5N1 virus too has a fairly long history, and clear association with poultry. The first known example was found in a chicken in the UK in 1959. The present H5N1 outbreaks can be traced back to a poultry goose in China, in 1996. The present lineage of Poultry flu has now been maintained in the vast poultry industry of East Asia for 10 years, causing sporadic massive outbreaks. Sometimes, such outbreaks are reported promptly, helping to limit damage, sometimes they are concealed. With billions of dollars of trade connected to the poultry industry, some governments have denied the presence of the disease, even during outbreaks. This problem of concealment is now made very much more difficult by some infected poultry appearing asymptomatic, apparently often due to vaccination (e.g. in China).

As reported by the New Scientist (February 7, 2006), in China in the winter 2005/2006,

"in the markets, researchers found H5N1 in about 2% of apparently
healthy ducks and geese, and some chickens".

As some poultry carrying the virus show no symptoms, and as economic pressures can lead to smuggling, it clearly makes it much harder to completely restrict imports of products from areas with infected poultry. Production and movement of poultry within China and Thailand, and within East Asia as a whole, is undertaken on a huge scale, with billions of such birds and their eggs moved annually (far greater in number than the total number of wild birds migrating through the region). This trade is not only within national borders, it is also international, usually legal, but sometimes illegal.

In October 2005, for example, 3,000 chickens were intercepted by Italian customs after being smuggled into the country from China, and major hauls of illegally imported Chinese poultry were also discovered in the UK and in the United States of America the same winter. Many such imports are believed to go undiscovered. The virus has also been found in smuggled cage birds in Britain, Belgium and Taiwan, where customs officers successfully prevented the spread of the virus.

As reported by the World Health Organisation in 2005, "Despite the death or destruction of an estimated 150 million (poultry) birds, the virus is now considered endemic in many parts of Indonesia and Viet Nam and in some parts of Cambodia, China, Thailand, and possibly also Lao...Control of the disease in poultry is expected to take several years."

The disease is widespread in poultry in parts of Asia, will take several more years to control, and yet poultry or poultry products are still being moved internationally: sometimes from areas with the disease to areas without it. The virus does not even need a sick chicken to bring it; the virus can be moved across national borders in the manure on the wheels of a truck, or on crates used earlier to carry poultry. Is it unreasonable to consider that at least some infected poultry or caged birds or infected feed or crates might occasionally get through customs controls here in Korea?

Indeed, the HP H5N1 virus has in the past been found in duck meat imported into South Korea from China - suggesting that outbreaks here in Korea could be from trade, and not the migration of wild birds.

In a few cases, wild birds do have Poultry Flu.

Rather than being the source of the outbreaks, however, it appears that wild birds are more often the victims. There are many cases where it seems very likely that wild birds contracted the virus through contact with infected poultry or with facilities used by them: farm buildings, manure heaps, and contaminated water ways. Often, the wild birds that have been found infected are non-migratory species that occur regularly near poultry farms, such as Magpies Pica pica (found H5N1 infected in China and Korea) and Large-billed Crows Corvus macrorhynchos (found H5N1 infected in Japan), and not migratory waterbirds.

The first recent outbreak of HP H5N1 was in Hong Kong in 1997. It was controlled by a cull of poultry, and by closing bird markets (e.g. Shortridge et al., 2000). Following the slaughter, the virus was not found in poultry or people in Hong Kong until a further outbreak in poultry farms in winter 2002/2003, that was again controlled through a combination of culling, quarantine and in addition vaccination of poultry (OIE, World Animal Health, Report, July 2003).

In Hong Kong, the virus also killed some domestic birds, and a very few wild birds: in 2003 these were confined to two Grey Heron Ardea cinerea and one Black-headed Gull Larus ridibindus: both species that often scavenge in waterways near farms. HP H5N1 however was not found in wild birds in wetlands like Mai Po in northern Hong Kong, even though that wetland contained up to 100, 000 migrant birds at the time. Between 1997 and 2005, at least 16,000 live wild birds were tested in Hong Kong. All tested negative for H5N1. Instead, H5N1 was found in caged birds and poultry being imported from South-east China into Hong Kong between 1999-2002.

Despite this decade-long absence of any evidence of spread of poultry flu by wild birds to poultry, every time there is an outbreak, the media report that the place is "on the migratory path of wild birds". This is no surprise to ornithologists. It is true. Indeed, almost everywhere in the world is on the migratory path of wild birds! Here in Korea, over 90% of all bird species are migratory. There is surely nowhere in Korea without some bird migration.

Moreover, as is also known well to ornithologists, the timing and pattern of spread of outbreaks of this HP H5N1 virus in 2003 and 2004, and again in 2005, this last time out of China into Siberia and on into Europe and Africa, simply did not match the timing of wild bird migration, or even the routes of migration.

No wild bird species for example moves west along the border of Russia and Kazakhstan, before turning south and then east-west across Turkey, before continuing onto Nigeria in western Africa, as this virus did.

So what happened? After an outbreak in wild birds at Qinghai in China in spring 2005, which killed 6,000 waterbirds (most especially Bar-headed Goose Anser indicus), the virus then continued north, reaching southern Siberia in summer 2005. While media and some of the scientific community insisted that wild birds migrating north from Qinghai were responsible, well-informed ornithologists were less convinced. The Bar-headed Goose does not migrate as far north as southern Siberia, and the outbreaks came at a time when ducks, geese and other waterbirds are already breeding, when most are unable to fly (let alone migrate) due to seasonal moult!

Once in the poultry heartland of Siberia, the virus then continued west, rapidly from one area of poultry production to another, appearing to follow, according to the New Scientist, railway lines, main roads and well-established trade routes.

This spread north and west of the virus in 2005 was also taking place at the same time as the spread of the disease though 21 provinces of Indonesia.The fact that almost no species of northern waterbird (and certainly no geese) even migrates to Indonesia also greatly undermines claims that migratory ducks and geese were somehow involved in the spread of the disease.


IF wild birds are able to spread this virus so easily and rapidly, then why, even after 10 years of HP H5N1 in poultry of the region, has this virus not yet reached North America? Why has it not yet reached Australia or New Zealand? Why has it still not reached Taiwan or the Philippines?

These countries also have very many migratory birds, including many species that migrate from Siberia, through China and Korea. Korea too…why have we only had two outbreaks in the past 10 years?

The main reason seems to be very obvious. It is most likely due to the success of control on imports in these same countries, and the rapid response by farmers to the very rare outbreaks when they occur, with culls of poultry and rapid disinfection of farms.

Strict import controls, a rapid response to outbreaks, and perhaps even a measure of good luck, has greatly limited the impact of HP H5N1 here.

If wild birds had been largely responsible for spreading this virus, as many allege, then it seems very likely that the virus would have already spread throughout most of the world, and outbreaks in wild birds as well as in poultry would be extremely widespread and frequent. Fortunately, however, this virus remains very rare in wild birds. And it is not being overlooked. Many countries have been actively testing for the virus, not only South Korea. For example, 2,500 migratory shorebirds in New Zealand and 173 in Australia all tested negative for HP H5N1 in 2005. Twenty thousand birds (comprising 250 species) in Europe were tested between 1986 and 2005, and all proved negative for HP H5N1. "Several thousand birds" were tested in Alaska during summer 2005 and again in summer 2006, and all were negative for HP H5N1. Here in Korea, where we have over one million waterbirds in winter, 5,000 ducks and geese (equivalent to fully 5% of the total) were tested for the virus in 2003?2004: and all were negative for HP H5N1- although as might be expected several birds were found carrying strains of LP Avian Influenza. In this year’s outbreak too, we have still not heard of any wild birds dying from the virus, and in the 2004 outbreak, only one dead Magpie tested at Yangju was H5N1 positive, out of 99 magpies and one crow that were tested there.

In a very few cases, all in 2005 so far, large numbers of wild birds, not only poultry, have also been killed by the virus. In the biggest outbreak, at Qinghai in China, up to 200 birds a day died between May 18th and 5th June, resulting in a total of ca 6, 000 wild bird fatalities (AVI Bulletin, 032, July 2005). The cause of the outbreak remains unclear, but the region had a poultry industry, a Bar-headed Goose breeding program, fish-farms alleged to use manure as fertiliser: in short many potential sources of infection of wild birds by poultry and poultry products.

An outbreak some time after in Mongolia (in a fairly remote area lacking poultry, and several hundred kilometers south of infected poultry regions of southern Siberia) then suggested that some infected wild birds were able to move the virus a short distance (perhaps as much as several hundred kilometers, or a day or more of flight), infecting some other wild birds, before they died.

A maximum 100 out of 6,500 waterbirds counted at one lake there were found dead, at least some believed killed by the virus. Of the almost 900 live birds sampled there at that time, including hundreds of Ruddy Shelduck Tadorna ferruginea , Bar-headed Geese, and Black-headed Gulls, Mongolian Gulls Larus mongolicus, and Whooper Swans Cygnus cygnus: ALL tested negative.

These two outbreaks in wild birds in 2005 in China and Mongolia are extremely important in understanding the relationship between the disease and wild birds.

We can see that:

  • HP H5N1 kills those wild birds that it infects;

  • The virus does not spread easily in natural conditions. While sick birds apparently can migrate short distances, infecting other wild birds, most birds sharing the same wetlands neither contract the virus nor do they become sick.

The virus kills wild birds quickly, and therefore becomes self-limiting. As the bird, the host of the virus, dies, so does the virus. Without the crowded and unhygienic conditions produced by poultry farms or caged bird markets it appears that the virus can no longer remain highly pathogenic, nor can it continue to spread.

Not only these examples, but genetic evidence too, points to HP H5N1 originating in and being maintained by domestic birds. It is largely the conditions of industrial style poultry flocks that allow the H5N1 virus to mutate from LP to HP, and to persist.

Because industrial style poultry production is so widespread, and has increased enormously in size over the past few decades in the region, HP H5N1 has survived in poultry flocks for a decade now, fortunately for us, still rarely passing from poultry to wild birds, or to humans.

While some media, even now, repeat the claim that wild birds are responsible for spreading the H5N1 virus, there still remains (almost) no documented case where a wild bird has actually been proven to have infected a poultry flock with HP H5N1. And no case where a wild bird has infected a human. There are however, numerous cases where the movement of infected poultry or poultry products (meat, eggs or manure) has been shown to be connected to outbreaks in other poultry farms. Some animal diseases occur frequently, despite high levels of industrial practice and strict border controls. It is worth considering the frequency of Newcastle’s Disease in chickens, and especially the spread of foot-and-mouth disease in cattle. If foot-and-mouth disease can spread internationally through trade of animals that can neither fly nor cross water by themselves, why not H5N1?

Further, considering the Qinghhai outbreak, and an outbreak of avian cholera at Seosan several years ago, it is also easy to imagine that if species like the Baikal Teal Anas formosa were to be carrying the HP H5N1 virus, then they themselves would be dying from it - and in huge numbers. HP H5N1 is clearly a very major threat to this species.

Indeed, an outbreak of H5N1 Poultry Flu has the potential not only to bankrupt farmers, but also to devastate species like the Bar-headed Goose (as at Qinghai), and the Baikal Teal here in Korea, where almost the whole world population spends the winter. The Baikal Teal flock could easily be struck by disease, and is also threatened in other ways. Over-sensational and irresponsible reporting of this virus by some media puts pressure on politicians to restrict artificial feeding programs, and could lead, in the very worst case, to attempts to control wild birds through culls. In line with the World Health Organisation and other leading organisations, Birds Korea believes that all culls of wild birds should be rejected, even if an outbreak of HP H5N1 in wild birds is detected. It is already widely accepted by the scientific community that culls of wild birds will not prevent the spread of the disease, long-term (as the problem lies within the poultry industry). On the contrary, culls can increase the possibility of outbreaks, by making flocks of birds leave usual areas, dispersing them to new sites, carrying the disease with them.

Thanks in part already to the same ill-informed and misleading claims about wild birds carrying the virus (such as made by the Ministry of Agriculture on banners and pamphlets in 2005, and on their website in 2006) many people already feel increasingly negative towards wild birds. Bird festivals and education programs have been attracting fewer visitors, and many people seem to feel nervous about visiting wetlands, where they would be able to see, safely!, some of the most awesome wildlife spectacles on Earth. Korea's Baikal Teal flock, numbering 600, 000 birds on the Geum here this winter is increasingly recognized as one of the world's great natural wonders. I had the pleasure of working with BBC TV for three weeks one recent winter, as we filmed this flock, introducing it to the world in their outstanding series, Planet Earth. Yet even many people living in Gunsan do not go to watch this spectacle!

For the sake of the farmers, for the sake of the people and for wild birds, it is clear that we urgently need to start sharing information about H5N1 more openly and honestly, free of bias and blame, developing appropriate responses based on good research and fact, and not on suspicions or unsupported hypotheses.

We also need to take numerous practical steps to restrict and eliminate the virus, based on past experience in Korea and present experience in other countries.

Birds Korea suggest that such measures should include (but not be limited to):

  1. Better enforcement of a ban on movement of poultry and poultry products from infected areas;

  2. Better enforcement of a ban on the use of untreated poultry feces as fertiliser and feed in fish-farms and in agriculture;

  3. Better enforcement of restrictions on the international movement of captive birds in trade, both legal and illegal;

  4. Provision of adequate funding to help farmers improve bio-security (keeping poultry and wild birds separate, especially in areas where outbreaks have been identified);

  5. Funds to improve significantly the conditions in which poultry are kept, and

  6. Full compensation for farmers for loss of income due to outbreaks/culls.

In such a way, we can overcome H5N1, improve foodsecurity, and better protect people and our wonderful wild bird populations.

NOTE: Papers (mostly in pdf form) and references for statements can be made available on request.