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Since it was first recognised in 1997, highly pathogenic avian influenza H5N1 has infected domestic and wild birds in more than 60 countries across Asia, Africa and Europe. Over 250 million domestic birds have died from disease or been slaughtered in attempts to control its spread; the economies of the worst affected countries in southeast Asia have suffered greatly, with lost revenue estimated at over $10 billion (Diouf 2005), and there have been serious human health consequences. Over 350 human cases have been confirmed, more than 60% of these fatal (WHO 2007).
Prior to HPAI H5N1, reports of HPAI in wild birds were very rare. The broad geographical scale and extent of the disease in wild birds is both extraordinary and unprecedented, and the conservation impacts of H5N1 have been significant. It is estimated that between 5-10% of the world population of Bar-headed Goose Anser indicus died at Lake Qinghai, China in spring 2005. At least two globally threatened species have been affected: Black-necked Crane Grus nigricollis in China and Red-breasted Goose Branta ruficollis in Greece. During winter, approximately 90% of the world population of Red-breasted Goose is usually confined to just five roost sites in Romania and Bulgaria (BirdLife 2007), countries that have both reported outbreaks, as also have Russia and Ukraine where they also over-winter. However, the total number of wild birds affected has been small in contrast to the number of domestic birds affected, and many more wild birds die of commoner avian diseases each year. Perhaps a greater threat than direct mortality is the development of possible paranoia about waterbirds and misguided attempts to control the disease by disturbing or destroying wild birds and their habitats. Such responses are often encouraged by inflammatory and misleading messages in the media.
Highly pathogenic avian influenza H5N1 is a contagious viral disease caused by influenza A virus. There are many different influenza A viruses, and while some are capable of causing severe disease most cause infections that produce few, if any, symptoms. Avian influenza viruses are characterised as either of low or high pathogenicity (LPAI or HPAI). The natural reservoir of LPAI viruses is in wild waterbirds ? most commonly in ducks, geese, swans, waders and gulls (Hinshaw & Webster 1982; Webster et al. 1992; Stallknecht & Brown 2007).
Given the ecology of the natural hosts, it is unsurprising that wetlands play a major role in the natural epidemiology of avian influenza. As with many other viruses, particles survive longer in colder water (Lu et al. 2003; Stallknecht et al. 1990b), and the virus is strongly suggested to survive over winter in frozen lakes in Arctic and sub-Arctic breeding areas. Thus, as well as the waterbird hosts, these wetlands are probably a permanent reservoir of LPAI virus (Rogers et al. 2004; Smith et al. 2004) (re)infecting waterbirds arriving from southerly areas to breed (shown in Siberia by Okazaki et al. 2000 and Alaska by Ito et al. 1995). Indeed, in some wetlands used as staging grounds by large numbers of migratory ducks, avian influenza viral particles can be readily isolated from lake water (Hinshaw et al. 1980).
In these wetlands, LPAI viruses are a natural part of the ecosystem. They have been isolated from over 90 species of wild bird, and are thought to have existed alongside wild birds for millennia in balanced systems. In their natural hosts, avian influenza viruses generally do not cause disease; instead, the viruses remain in evolutionary stasis as indicated by low genetic mutation rates (Gorman et al. 1992, Taubenberger et al. 2005). When LPAI viruses are transmitted to vulnerable poultry species, only mild symptoms such as a transient decline in egg production or reduction in weight gain (Capua & Mutinelli 2001) are induced. However, where a dense poultry environment supports several cycles of infection, the viruses may mutate, adapting to their new hosts, and for the H5 and H7 subtypes these mutations can lead to generation of a highly pathogenic form. Thus, HPAI viruses are essentially products of intensively farmed poultry (GRAIN 2006; Greger 2006). They should be viewed as something artificial, made possible by human modification of a naturally balanced system.
After an HPAI virus has arisen in poultry, it has the potential both to re-infect wild birds and to cause disease in other non-avian taxa, with different subtypes showing varying predilection for horses, pigs, humans, mustelids, felids, and even seals and cetacea. If influenza A viruses adapt inside these new hosts to become highly transmissible, there can be devastating consequences, such as the human influenza pandemics of the 20th century (Kilbourne 2006). The conditions necessary for cross-infection are provided by agricultural practices that bring together humans, poultry and other species in high densities in areas where there is also the potential for viral transmission from wild birds to domestic ducks on shared wetlands and in ?wet? (i.e. live animal) markets (Shortridge 1977; Shortridge et al. 1977).
An agricultural practice that provides ideal conditions for cross-infection and thus genetic change is used on fish-farms in Asia: battery cages of poultry are placed directly over troughs in pig-pens, which in turn are positioned over fish farms. The poultry waste feeds the pigs, the pig waste is either eaten by the fish or acts as a fertiliser for aquatic fish food, and the pond water is sometimes recycled as drinking water for the pigs and poultry (Greger 2006). These kinds of agricultural practices afford avian influenza viruses, which are spread via the faecal-oral route, a perfect opportunity to cycle through a mammalian species, accumulating the mutations necessary to adapt to mammalian hosts. Thus, as the use of such practices increases, so does the likelihood that new influenza strains lethal to humans will emerge (Culliton 1990; Greger 2006).
As well as providing conditions for virus mutation and generation, agricultural practices, particularly those used on wetlands, can enhance the ability of a virus to spread. The role of Asian domestic ducks in the epidemiology of HPAI H5N1 has been closely researched and found to be central not only to the genesis of the virus (Hulse-Post et al. 2005; Sims et al. 2005), but also to its spread and the maintenance of infection in several Asian countries (Shortridge & Melville 2006). Typically this has involved flocks of domestic ducks used for ?cleaning? rice paddies of waste grain and various pests, during which they are exposed to wild ducks using the same wetlands. Detailed research (Gilbert et al. 2006; Songserm et al. 2006) in Thailand has demonstrated a strong association between the HPAI H5N1 virus and abundance of free-grazing ducks. Gilbert et al. (2006) concluded that in Thailand ?wetlands used for double-crop rice production, where free-grazing duck feed year round in rice paddies, appear to be a critical factor in HPAI persistence and spread?.
Yet there is wide international consensus that attempting to control HPAI through responses such as culling or disturbing wild birds, or destroying wetland habitats is both not feasible and diversionary, and thus should not be attempted, not least since it may exacerbate the problem by causing further dispersion of infected birds. Resolution IX.23 of the Ramsar Convention on Wetlands states the ?destruction or substantive modification of wetland habitats with the objective of reducing contact between domesticated and wild birds does not amount to wise use as urged by Article 3.1 of the Convention, and also may exacerbate the problem by causing further dispersion of infected birds?. The key to the control of HPAI remains control and prevention in the poultry sector (Greger 2006; GRAIN 2006; Sims 2007) and ornithologists and the conservation community must play their part in this to ensure benefits to all.
One of the central obligations of the Ramsar Convention is that Contracting Parties ?shall promote the conservation of wetlands and waterfowl by establishing nature reserves on wetlands? and subsequent decisions of the Conference of Parties have stressed the role of these reserves and associated wetland centres in enhancing public awareness of wetlands and communicating the need for waterbird conservation. Recent events have highlighted the risk that ill-informed media reporting (Figure 1) about the spread of HPAI H5N1 may undo decades of building positive public attitudes towards wetland and waterbird conservation. For example, as HPAI H5N1 spread across central Asia and Europe in winter 2005 and spring 2006, visitor numbers at wetland centres in the UK fell markedly with economic impacts for conservation organisations and changed public attitudes, which encompassed concern and even fear.
Human lives are enriched by birds - contact with - and appreciation of which, is an important element of the well being of those who may otherwise have limited opportunities to interact with wildlife. Getting close to birds brings great pleasure. As the late Janet Kear, life-long waterbird conservationist, once said, ?just as you can?t sneeze with your eyes open, you can?t feed a bird from your hand without smiling.? It is crucial that we avoid preventable reactions that might encourage people to stay away from wild birds because of unfounded fears and false perceptions of risk. In the long-term, this could prove greatly damaging to public support for wetland and waterbird conservation.
Currently, wildlife health problems are being created or exacerbated by activities such as habitat loss or degradation and close contact between domestic and wild animals. Ultimately, to reduce risk of avian influenza and other bird diseases, we need to move to markedly more sustainable systems of agriculture with significantly lower intensity systems of poultry production. These need to be more biosecure, separated from wild waterbirds and their natural wetland habitats resulting in far fewer opportunities for viral cross-infection and thus pathogenetic amplification (Greger 2006). To deliver such an objective in a world with an ever-burgeoning human population, hungry for animal protein, and with major issues of food-security throughout the developing world, will be a major policy challenge. However, the animal and human health consequences of not tackling these issues, in terms of the impact on economies, food security and potential implications of a human influenza pandemic, are quite immense.
Prior to HPAI H5N1, reports of HPAI in wild birds were very rare. The broad geographical scale and extent of the disease in wild birds is both extraordinary and unprecedented, and the conservation impacts of H5N1 have been significant. It is estimated that between 5-10% of the world population of Bar-headed Goose Anser indicus died at Lake Qinghai, China in spring 2005. At least two globally threatened species have been affected: Black-necked Crane Grus nigricollis in China and Red-breasted Goose Branta ruficollis in Greece. During winter, approximately 90% of the world population of Red-breasted Goose is usually confined to just five roost sites in Romania and Bulgaria (BirdLife 2007), countries that have both reported outbreaks, as also have Russia and Ukraine where they also over-winter. However, the total number of wild birds affected has been small in contrast to the number of domestic birds affected, and many more wild birds die of commoner avian diseases each year. Perhaps a greater threat than direct mortality is the development of possible paranoia about waterbirds and misguided attempts to control the disease by disturbing or destroying wild birds and their habitats. Such responses are often encouraged by inflammatory and misleading messages in the media.
Highly pathogenic avian influenza H5N1 is a contagious viral disease caused by influenza A virus. There are many different influenza A viruses, and while some are capable of causing severe disease most cause infections that produce few, if any, symptoms. Avian influenza viruses are characterised as either of low or high pathogenicity (LPAI or HPAI). The natural reservoir of LPAI viruses is in wild waterbirds ? most commonly in ducks, geese, swans, waders and gulls (Hinshaw & Webster 1982; Webster et al. 1992; Stallknecht & Brown 2007).
Given the ecology of the natural hosts, it is unsurprising that wetlands play a major role in the natural epidemiology of avian influenza. As with many other viruses, particles survive longer in colder water (Lu et al. 2003; Stallknecht et al. 1990b), and the virus is strongly suggested to survive over winter in frozen lakes in Arctic and sub-Arctic breeding areas. Thus, as well as the waterbird hosts, these wetlands are probably a permanent reservoir of LPAI virus (Rogers et al. 2004; Smith et al. 2004) (re)infecting waterbirds arriving from southerly areas to breed (shown in Siberia by Okazaki et al. 2000 and Alaska by Ito et al. 1995). Indeed, in some wetlands used as staging grounds by large numbers of migratory ducks, avian influenza viral particles can be readily isolated from lake water (Hinshaw et al. 1980).
In these wetlands, LPAI viruses are a natural part of the ecosystem. They have been isolated from over 90 species of wild bird, and are thought to have existed alongside wild birds for millennia in balanced systems. In their natural hosts, avian influenza viruses generally do not cause disease; instead, the viruses remain in evolutionary stasis as indicated by low genetic mutation rates (Gorman et al. 1992, Taubenberger et al. 2005). When LPAI viruses are transmitted to vulnerable poultry species, only mild symptoms such as a transient decline in egg production or reduction in weight gain (Capua & Mutinelli 2001) are induced. However, where a dense poultry environment supports several cycles of infection, the viruses may mutate, adapting to their new hosts, and for the H5 and H7 subtypes these mutations can lead to generation of a highly pathogenic form. Thus, HPAI viruses are essentially products of intensively farmed poultry (GRAIN 2006; Greger 2006). They should be viewed as something artificial, made possible by human modification of a naturally balanced system.
After an HPAI virus has arisen in poultry, it has the potential both to re-infect wild birds and to cause disease in other non-avian taxa, with different subtypes showing varying predilection for horses, pigs, humans, mustelids, felids, and even seals and cetacea. If influenza A viruses adapt inside these new hosts to become highly transmissible, there can be devastating consequences, such as the human influenza pandemics of the 20th century (Kilbourne 2006). The conditions necessary for cross-infection are provided by agricultural practices that bring together humans, poultry and other species in high densities in areas where there is also the potential for viral transmission from wild birds to domestic ducks on shared wetlands and in ?wet? (i.e. live animal) markets (Shortridge 1977; Shortridge et al. 1977).
An agricultural practice that provides ideal conditions for cross-infection and thus genetic change is used on fish-farms in Asia: battery cages of poultry are placed directly over troughs in pig-pens, which in turn are positioned over fish farms. The poultry waste feeds the pigs, the pig waste is either eaten by the fish or acts as a fertiliser for aquatic fish food, and the pond water is sometimes recycled as drinking water for the pigs and poultry (Greger 2006). These kinds of agricultural practices afford avian influenza viruses, which are spread via the faecal-oral route, a perfect opportunity to cycle through a mammalian species, accumulating the mutations necessary to adapt to mammalian hosts. Thus, as the use of such practices increases, so does the likelihood that new influenza strains lethal to humans will emerge (Culliton 1990; Greger 2006).
As well as providing conditions for virus mutation and generation, agricultural practices, particularly those used on wetlands, can enhance the ability of a virus to spread. The role of Asian domestic ducks in the epidemiology of HPAI H5N1 has been closely researched and found to be central not only to the genesis of the virus (Hulse-Post et al. 2005; Sims et al. 2005), but also to its spread and the maintenance of infection in several Asian countries (Shortridge & Melville 2006). Typically this has involved flocks of domestic ducks used for ?cleaning? rice paddies of waste grain and various pests, during which they are exposed to wild ducks using the same wetlands. Detailed research (Gilbert et al. 2006; Songserm et al. 2006) in Thailand has demonstrated a strong association between the HPAI H5N1 virus and abundance of free-grazing ducks. Gilbert et al. (2006) concluded that in Thailand ?wetlands used for double-crop rice production, where free-grazing duck feed year round in rice paddies, appear to be a critical factor in HPAI persistence and spread?.
Yet there is wide international consensus that attempting to control HPAI through responses such as culling or disturbing wild birds, or destroying wetland habitats is both not feasible and diversionary, and thus should not be attempted, not least since it may exacerbate the problem by causing further dispersion of infected birds. Resolution IX.23 of the Ramsar Convention on Wetlands states the ?destruction or substantive modification of wetland habitats with the objective of reducing contact between domesticated and wild birds does not amount to wise use as urged by Article 3.1 of the Convention, and also may exacerbate the problem by causing further dispersion of infected birds?. The key to the control of HPAI remains control and prevention in the poultry sector (Greger 2006; GRAIN 2006; Sims 2007) and ornithologists and the conservation community must play their part in this to ensure benefits to all.
One of the central obligations of the Ramsar Convention is that Contracting Parties ?shall promote the conservation of wetlands and waterfowl by establishing nature reserves on wetlands? and subsequent decisions of the Conference of Parties have stressed the role of these reserves and associated wetland centres in enhancing public awareness of wetlands and communicating the need for waterbird conservation. Recent events have highlighted the risk that ill-informed media reporting (Figure 1) about the spread of HPAI H5N1 may undo decades of building positive public attitudes towards wetland and waterbird conservation. For example, as HPAI H5N1 spread across central Asia and Europe in winter 2005 and spring 2006, visitor numbers at wetland centres in the UK fell markedly with economic impacts for conservation organisations and changed public attitudes, which encompassed concern and even fear.
Human lives are enriched by birds - contact with - and appreciation of which, is an important element of the well being of those who may otherwise have limited opportunities to interact with wildlife. Getting close to birds brings great pleasure. As the late Janet Kear, life-long waterbird conservationist, once said, ?just as you can?t sneeze with your eyes open, you can?t feed a bird from your hand without smiling.? It is crucial that we avoid preventable reactions that might encourage people to stay away from wild birds because of unfounded fears and false perceptions of risk. In the long-term, this could prove greatly damaging to public support for wetland and waterbird conservation.
Currently, wildlife health problems are being created or exacerbated by activities such as habitat loss or degradation and close contact between domestic and wild animals. Ultimately, to reduce risk of avian influenza and other bird diseases, we need to move to markedly more sustainable systems of agriculture with significantly lower intensity systems of poultry production. These need to be more biosecure, separated from wild waterbirds and their natural wetland habitats resulting in far fewer opportunities for viral cross-infection and thus pathogenetic amplification (Greger 2006). To deliver such an objective in a world with an ever-burgeoning human population, hungry for animal protein, and with major issues of food-security throughout the developing world, will be a major policy challenge. However, the animal and human health consequences of not tackling these issues, in terms of the impact on economies, food security and potential implications of a human influenza pandemic, are quite immense.
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