EVERY spring tens of thousands of water birds gather at Qinghai Lake in north-central China. It is a haven for migrants flying along a dozen different migratory routes, including bar-headed geese that have just completed a spectacular flight over the Himalayas from India. Normally a few geese die after such an arduous journey, but last year hundreds developed severe diarrhoea and stood motionless, heads bowed, struggling to breathe, dying. Then the brown-headed and black-headed gulls started to die too. By the time the gathering dispersed, more than 6000 birds had died, including a tenth of all the bar-headed geese in the world.
The culprit was the H5N1 bird flu virus, the first time it had caused a mass die-off in wild birds. Later that year H5N1 appeared in Russia and Mongolia, and then around the Caspian and Black Seas and the Mediterranean. This year it has been reported in Africa, western Europe and south Asia. After years of being largely confined to east Asian chicken farms, H5N1 has taken wing.
The big fear is that the virus will mutate into a form capable of spreading from person to person and causing a human pandemic. Even if that never happens, though, we have a massive problem. H5N1 is already the worst outbreak of a disease affecting animals ever known. Why has the virus suddenly taken wing? Is it going to keep on spreading? And what is it going to do to wildlife along the way? The omens do not look good.
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In the wild, bird flu viruses usually circulate in waterfowl, especially ducks, infecting the birds’ guts without causing obvious symptoms. The massive growth of intensive livestock farming in recent decades, however, has created the conditions for an altogether different kind of virus.
In China in the 1990s, one local H5N1 virus did very well for itself by adapting to chickens. It acquired a mutation that allows it to infect not just the chickens’ lungs, but every organ in their body. Viruses with this mutation are called “highly pathogenic”, and they run riot in crowded poultry farms, where there’s always a new victim close by. They never get far in the wild, however, because they kill too fast to spread among a scattered population.
“The virus could keep jumping from poultry to wild birds and back for years or decades”
H5N1 now seems to have overcome this limitation – but how? As it evolved in chickens, it acquired the ability to infect a wider range of species than any other known flu virus. It can kill many species flu usually never touches, including crows, pigeons, falcons and buzzards, and mammals such as tigers and domestic cats.
Yet until last year, the vast majority of H5N1 infections were in poultry, and only in a few east Asian countries. While officials sometimes blamed wild birds for spreading the virus, there is little evidence of this. On the contrary, earlier this year Yi Guan and Malik Peiris at the University of Hong Kong reported that H5N1 has evolved slight differences in different Chinese provinces. They say this means the virus has been spreading almost entirely in poultry, which unlike wild birds rarely cross state lines.
Indeed, when H5N1 first adapted to chickens it became deadly to ducks, the usual spreaders of bird flu in the wild. Sometime in 2003, however, H5N1 started to become less lethal to ducks. Last year, Robert Webster’s team at St Jude Children’s Research Hospital in Tennessee infected domestic ducks with samples of H5N1 from late 2003 and 2004. While some ducks died, some survived, because mutant viruses less deadly to ducks flourished in these animals.
The experiment happened for real in Asia. żěè¶ĚĘÓƵs were shocked by the discovery that in October 2004, one in five domestic ducks in the Mekong delta of Vietnam had H5N1 – yet instead of dying they were excreting masses of the virus in faeces without so much as sneezing. The failure to eliminate H5N1 from poultry has allowed a form to emerge that remains highly pathogenic and deadly to chickens and many other animals, yet is duck-friendly. And that’s the key to its spread.
At Qinghai, a hybrid between the Z genotype responsible for the poultry outbreaks across east Asia from 2003 onwards and another closely-related poultry strain of H5N1 appeared that is particularly duck-friendly. The virus likely emerged in close wild relatives of domestic ducks, members of the group known as dabbling ducks.
Guan’s team found that mallards, falcated teal and spot-billed ducks at Poyang Lake in south-east China in early 2005 were carrying H5N1 with genes that exactly matched the virus that later turned up in dead geese at Qinghai. Yet the Poyang ducks appeared healthy – and some were about to fly to Qinghai. The virus might have arrived at the lake with these ducks.
Experiments this year confirm that most mallards infected by this strain shed the virus for a week or more but do not get seriously ill. In February Sweden found H5N1 in a healthy mallard. The pattern of spread suggests that other dabbling ducks, including long-distance migrators, might also shed virus without getting sick.
Birds that do not get sick can still migrate and carry the virus with them. And although infected ducks shed the virus only for a week or two, they can pass it to other birds on stopovers during migrations. The virus could in theory circle the globe by passing from duck to duck. What’s more, this spread is invisible: only when ducks infect susceptible species such as swans or chickens do dead birds start appearing.
Some migrants from Qinghai went to Mongolia, where an outbreak of the Qinghai virus was detected in late August. Others spent the summer of 2005 at remote breeding grounds in Siberia, where they seem to have passed the virus to ducks that overwinter in Europe and Africa (see Graphic). It was when the birds left Siberia that the virus began to turn up across Asia and Europe.
In late June and early July, poultry outbreaks began along the Siberian-Kazakh border, just as male ducks that had failed to mate and left Siberia early would have been arriving. In October, Turkey, Romania and Croatia reported cases at the time that the full autumn migration from Siberia was arriving.
In February this year, Nigeria and Egypt reported H5N1 outbreaks. While Nigeria has blamed illegal trade for its outbreak, it seems more likely that the virus arrived with autumn migrants and spread unreported for several weeks, as the initial outbreaks happened close to a major wintering spot.
Carried by migrants
In the past few weeks, numerous countries in Europe, the Middle East and south Asia have reported outbreaks. In every case so far the virus has been the Qinghai strain, virtually unchanged. It seems clear, says Julian Hughes of the UK’s Royal Society for the Protection of Birds, that at least some of the virus’s long-distance jumps can be explained only if it was carried by migrant birds.
So is H5N1 now set to run amok in wild birds, as it does in chickens? Not necessarily. While the Qinghai strain is spreading far and wide, so far no more mass die-offs on the scale of Qinghai have been reported. In Mongolia and around the Caspian Sea, only dozens died where many thousands were present. In Poyang, the virus was found in only 1.4 birds per thousand. Elsewhere the prevalence has been even lower. Teams in Europe took samples from some 25,000 incoming migrants during the past season, and found no infections. Only the odd dead swan or other victim has revealed the virus’s presence.
Maybe the virus has yet to really take off in the wild. But it could be that wild birds are poor at spreading it. Unless each carrier passes the virus to more than one other bird on average, the infection will simply die out.
Even if H5N1 does thrive in the wild, at some point it is likely to become less deadly as a result of mutating or recombining with other bird flu viruses. “It’s already so lethal in so many bird species that I don’t see any other outcome of re-assortment than attenuation,” says Peter Daszak, head of the Consortium for Conservation Medicine in New York City.
This is encouraging. For instance, if the virus is poor at spreading there is at least a chance the Americas will be spared. The low-pathogenicity bird flu viruses found in Eurasia and the Americas are distinct, showing that viruses only rarely cross the Atlantic or Pacific. Still, it does happen: in 2000, Björn Olsen of the University of Kalmar in Sweden, who monitors flu in wild birds, found a guillemot in the Baltic carrying an H6 virus with genes that were half European and half American.
The trouble is that even if the Qinghai strain would die out in wild birds if left to its own devices, it will likely persist in poultry. After all, if most east Asian countries have not been able to eliminate H5N1 from poultry, what chance do even poorer countries elsewhere in Asia and in Africa have? “What I’m afraid of,” says Olsen, “is that the wild birds will keep picking it up from poultry.”
The virus could keep jumping back and forth between poultry and wild birds for years or even decades to come. “Every time some place gets the infection in poultry under control, some wild bird will bring it back in, it will explode in the poultry, masses of virus will be shed, the wild birds will be infected again, and the cycle will continue,” says Olsen.
What’s more, as long as H5N1 replicates in chickens, it is likely to retain the nasty characteristics it evolved in them: high pathogenicity and the ability to kill many species. The nightmare scenario, says Olsen, is that chickens keep the virus nasty, while wild birds keep spreading it far and wide.
This would give the virus ever more opportunity to jump species and start spreading among people, says Albert Osterhaus of Erasmus University in Rotterdam in the Netherlands. But even if it doesn’t make the jump, sporadic outbreaks of H5N1 will be bad news for the poultry industry and smallholders – and for wildlife.
H5N1 kills a wide variety of birds. Denmark has found that it kills diving ducks, cousins of the dabbling ducks. In Hong Kong it has killed small numbers of waders, thrushes and finches, while everywhere the virus has gone it has killed birds of prey and members of the crow family. The extent to which different species are affected will depend on their level of exposure, says Hughes. A hawk that preys on ducks will catch the virus, one that doesn’t may not.
Once acquired, the virus will have the most serious impact on bird species that congregate in just a few areas, says Hughes, where a single outbreak might wipe out a significant proportion of the species. Europe’s vulnerable red-breasted goose, for instance, overwinters at just five sites in south-east Europe. One has already died of H5N1 in Greece.
Pushed to the brink
Species with reduced genetic diversity are also likely to be hard hit. André d’Hondt of Cornell University in New York has found that one bacterial infection decimates populations of North American house finches that have little diversity, whereas the same bug causes little damage where the birds are more diverse.
Until recently, biologists discounted disease as a major factor in extinctions. As an infection kills, the reasoning went, members of the affected species become so scarce that they rarely pass on the disease and it dies out, allowing numbers to recover. However, if a disease harboured by one species kills another species, the second species can be pushed to the brink. Grey squirrels are displacing native red squirrels across much of Europe partly because the greys carry the parapox virus, which is deadly to reds. Exotic signal crayfish carry a fungus that is wiping out Europe’s native white-clawed crayfish.
Something similar could happen with H5N1. Over the coming years, populations susceptible to H5N1 could be repeatedly reinfected by diseased poultry or by wild birds that can carry the virus without getting sick.
According the 2006 Red List of threatened species, 12 per cent of the world’s 10,000 or so bird species and 23 per cent of the 5400 mammal species are already threatened by factors such as loss of habitat. H5N1 can kill many of these species. It might be the final straw for remnant populations, such as the kiwis of New Zealand or the big griffon vultures of south Asia, already decimated by a cattle drug. “We had hoped that now we know what is killing the vultures, we could save them,” says Hughes. “Now this virus could finish them off.”
Much of the attrition among wild birds may be invisible, as sick birds often fall victim to predators, leaving no hint that they were infected, points out Kevin McGowan of Cornell. We may never know the virus’s full impact.
It is not just birds that are at risk. Domestic cats and stone martens have died after eating infected birds. The Z genotype has also killed tigers, leopards and civets in zoos. “There are lots of endangered cat species that could be knocked out,” says Osterhaus. He discovered in the 1980s that flu can kill seals as well – the critically endangered Mediterranean monk seal might be among the species at risk.
“Many endangered species could be knocked out”
There is little conservationists can do. While some zoo animals are already being vaccinated against H5N1, vaccinating wild animals is seldom practical. And the effect of H5N1 on ecosystems could be complex. For instance, if repeated waves of the virus reduce numbers of mustelids such as weasels, there could be a boom in rodent numbers. Few scientists, never mind governments, seem to have seriously considered the long-term threat H5N1 poses to the world’s ecosystems.
Then there’s the poultry industry. The economic impact of H5N1 on poor farmers is already appalling, says the UN Food and Agriculture Organization. Figures are limited, but some fear the poverty created by the loss of chickens could be killing more people than the virus itself. Nine people in India, and one in Italy, are known to have committed suicide after H5N1 outbreaks ruined poultry markets and their livelihoods.
If the virus persists by cycling between wild and domestic birds matters will only get worse. According to the International Food Policy Research Institute in Washington DC, the livestock revolution in Asia will benefit the poor only if smallholders produce the meat, eggs and milk. Bird flu, however, can be controlled more easily in big commercial operations, which might now take over.
Of course, it is near-impossible to predict exactly how H5N1 will evolve and behave. One big surprise came last December when scientists in China reported finding a highly pathogenic H5N1 in healthy tree sparrows in Henan province. The strain can still kill chickens but unlike the Z genotype and Qinghai strain, it does not hurt mice. No one is quite sure what to make of the finding.
All the experts agree, though, that the key to stopping H5N1 is containing it in poultry. Shooting every wild duck in the world is neither practical nor morally acceptable. A live vaccine that spreads among wild birds might turn into another monster. In any case, left to its own devices H5N1 could simply disappear in the wild – although, cautions Osterhaus, that isn’t certain.
But poultry are another story. Poultry spawned this monster, and this is where most of the virus still lurks, and where all human cases have arisen. It was encouraging when at a World Bank meeting in Beijing in January countries pledged $1.9 billion to help control the virus in poultry in poor countries. So far only $60 million has been confirmed, and even this has yet to materialise.
