Rice Production Systems and Avian Influenza: Interactions between Mixed-Farming Systems, Poultry and Wild Birds

Abstract. Wild waterfowl are the reservoir for avian influenza viruses (AIVs), a family of RNA viruses that may cause mild sickness in waterbirds. Emergence of H5N1, a highly pathogenic avian influenza (HPAI) strain, causing severe disease and mortality in wild birds, poultry and humans, had raised concerns about the role of wild birds in possible transmission of the disease. In this review, the link between rice production systems, poultry production systems, and wild bird ecology is examined to assess the extent to which these interactions could contribute towards the persistence and evolution of HPAI H5N1. The rice (Oryza sativa) and poultry production systems in Asia described, and then migration and movements of wild birds discussed. Mixed farming systems in Asia and wild bird movement and migration patterns create opportunities for the persistence of low pathogenic AIVs in these systems. Nonetheless, there is no evidence of long-term persistence of HPAI viruses (including the H5N1 subtype) in the wild. There are still significant gaps in the understanding of how AIVs circulate in rice systems. A better understanding of persistence of AIVs in rice farms, particularly of poultry origins, is essential in limiting exchange of AIVs between mixed-farming systems, poultry and wild birds.

[1]  Y. Guan,et al.  Establishment of multiple sublineages of H5N1 influenza virus in Asia: implications for pandemic control. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[2]  Marius Gilbert,et al.  REMOTE SENSING, ECOLOGICAL VARIABLES, AND WILD BIRD MIGRATION RELATED TO OUTBREAKS OF HIGHLY PATHOGENIC H5N1 AVIAN INFLUENZA , 2007, Journal of wildlife diseases.

[3]  R. Webster,et al.  Perpetuation of influenza A viruses in Alaskan waterfowl reservoirs , 2005, Archives of Virology.

[4]  Y. Guan,et al.  Emergence of multiple genotypes of H5N1 avian influenza viruses in Hong Kong SAR , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[5]  R. Webster,et al.  Wildlife surveillance associated with an outbreak of lethal H5N2 avian influenza in domestic poultry. , 1985, Avian diseases.

[6]  Marius Gilbert,et al.  Highly Pathogenic Avian Influenza H5N1, Thailand, 2004 , 2005, Emerging Infectious Diseases.

[7]  C. Feare Fish farming and the risk of spread of avian influenza , 2006 .

[8]  D. Bicout,et al.  Bird Migration Routes and Risk for Pathogen Dispersion into Western Mediterranean Wetlands , 2007, Emerging infectious diseases.

[9]  C. Lebarbenchon,et al.  Recent expansion of highly pathogenic avian influenza H5N1: a critical review , 2007 .

[10]  D. Weinstock,et al.  Survival of Avian Influenza Virus H7N2 in SPF Chickens and Their Environments , 2003, Avian diseases.

[11]  D. Senne,et al.  Isolation of H13N2 influenza A virus from turkeys and surface water. , 1991, Avian diseases.

[12]  Y. Guan,et al.  Avian flu: H5N1 virus outbreak in migratory waterfowl , 2005, Nature.

[13]  P. Ewald,et al.  Adaptive Dynamics of Infectious Diseases: Alternative Transmission Modes and the Evolution of Virulence , 2002 .

[14]  Changsheng Li,et al.  Observation of flooding and rice transplanting of paddy rice fields at the site to landscape scales in China using VEGETATION sensor data , 2002 .

[15]  D. Gilmer,et al.  Rice available to waterfowl in harvested fields in the Sacramento Valley, California , 1989 .

[16]  S. Cole,et al.  Control of M. tuberculosis ESAT-6 Secretion and Specific T Cell Recognition by PhoP , 2008, PLoS pathogens.

[17]  Y. Guan,et al.  H 5 N 1 Outbreaks and Enzootic Influenza-1 , 2007 .

[18]  W. J. Bean,et al.  Intestinal influenza: Replication and characterization of influenza viruses in ducks , 1978, Virology.

[19]  W. Hagemeijer,et al.  Evidence of Infection by H5N2 Highly Pathogenic Avian Influenza Viruses in Healthy Wild Waterfowl , 2008, PLoS pathogens.

[20]  D. Stallknecht,et al.  Persistence of H5 and H7 Avian Influenza Viruses in Water , 2007, Avian diseases.

[21]  K. Cassman Ecological intensification of cereal production systems: yield potential, soil quality, and precision agriculture. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[22]  Y Li,et al.  The evolution of H5N1 influenza viruses in ducks in southern China. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[23]  M. Gilbert,et al.  Avian influenza, domestic ducks and rice agriculture in Thailand. , 2007, Agriculture, ecosystems & environment.

[24]  John A. Dixon,et al.  Farming Systems and Poverty IMPROVING FARMERS' LIVELIHOODS IN A CHANGING WORLD , 2001 .

[25]  Y. Guan,et al.  Avian Influenza in Hong Kong 1997–2002 , 2003, Avian diseases.

[26]  C. Devendra,et al.  Smallholder farming systems in Asia , 2002 .

[27]  Y. Guan,et al.  Genesis of a highly pathogenic and potentially pandemic H5N1 influenza virus in eastern Asia , 2004, Nature.

[28]  D. Stallknecht,et al.  Persistence of avian influenza viruses in water. , 1990, Avian diseases.

[29]  Wu Leung,et al.  Food and Agricultural Organization of the United Nations. , 1962 .

[30]  D. Shoham,et al.  Evidence of Influenza A Virus RNA in Siberian Lake Ice , 2006, Journal of Virology.

[31]  Jonathan A Runstadler,et al.  Prevalence and diversity of avian influenza viruses in environmental reservoirs. , 2008, The Journal of general virology.

[32]  Changsheng Li,et al.  Mapping paddy rice agriculture in South and Southeast Asia using multi-temporal MODIS images , 2006 .

[33]  D. Stallknecht,et al.  Experimental Infection of Swans and Geese with Highly Pathogenic Avian Influenza Virus (H5N1) of Asian Lineage , 2008, Emerging infectious diseases.

[34]  D. Stallknecht,et al.  Susceptibility of North American Ducks and Gulls to H5N1 Highly Pathogenic Avian Influenza Viruses , 2006, Emerging infectious diseases.

[35]  D. L. Orthmeyer,et al.  Spatial Use by Wintering Greater White-Fronted Geese Relative to a Decade of Habitat Change in California's Central Valley , 2006 .

[36]  L. Campitelli,et al.  Characterization of Low-Pathogenic H5 Subtype Influenza Viruses from Eurasia: Implications for the Origin of Highly Pathogenic H5N1 Viruses , 2007, Journal of Virology.

[37]  Baoping Yan,et al.  Victims and Vectors: Highly Pathogenic Avian Influenza H5N1 and the Ecology of Wild Birds , 2010 .

[38]  J. Crofts Avian influenza in Hong Kong , 2003 .

[39]  Chris S. Elphick,et al.  Winter management of Californian rice fields for waterbirds , 1998 .

[40]  D J Alexander,et al.  A review of avian influenza in different bird species. , 2000, Veterinary microbiology.

[41]  Michael Worobey,et al.  Phylogenetic Evidence against Evolutionary Stasis and Natural Abiotic Reservoirs of Influenza A Virus , 2008, Journal of Virology.

[42]  R. Huke Rice area by type of culture, South, Southeast, and East Asia , 1982 .

[43]  Y. Guan,et al.  H5N1 Outbreaks and Enzootic Influenza , 2006, Emerging infectious diseases.

[44]  C. Henny Drought displaced movement of North American pintails into Siberia , 1973 .

[45]  Y. Guan,et al.  Reemerging H5N1 Influenza Viruses in Hong Kong in 2002 Are Highly Pathogenic to Ducks , 2004, Journal of Virology.

[46]  A. Osterhaus,et al.  Global Patterns of Influenza A Virus in Wild Birds , 2006, Science.

[47]  Edward C Holmes,et al.  Avian influenza virus exhibits rapid evolutionary dynamics. , 2006, Molecular biology and evolution.

[48]  J. Takekawa,et al.  Migration and stopover strategies of individual Dunlin along the Pacific coast of North America , 2004 .

[49]  P. Li,et al.  Implications of Rice Agriculture for Wild Birds in China , 2010 .

[50]  Michael R. Miller,et al.  Spring migration of Northern Pintails from California's Central Valley wintering area tracked with satellite telemetry: routes, timing, and destinations , 2005 .

[51]  C. Blair,et al.  ASSESSING FLAVIVIRUS, LENTIVIRUS, AND HERPESVIRUS EXPOSURE IN FREE-RANGING RING-TAILED LEMURS IN SOUTHWESTERN MADAGASCAR , 2007, Journal of wildlife diseases.

[52]  C. Devendra,et al.  Crop–animal systems in Asia: importance of livestock and characterisation of agro-ecological zones , 2002 .

[53]  D. Roland-Holst,et al.  Characterization of Poultry Production Systems in Vietnam , 2007 .

[54]  D. V. Chin,et al.  Wild and weedy rice in rice ecosystems in Asia : a review , 2000 .

[55]  R. Webster,et al.  Emergence of influenza A viruses. , 2001, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[56]  P. Berthold,et al.  Avian Migration , 2003, Springer Berlin Heidelberg.

[57]  D. Swayne Understanding the Ecology and Epidemiology of Avian Influenza Viruses: Implications for Zoonotic Potential , 2000 .

[58]  J. Takekawa,et al.  Geographic variation in migratory behavior of greater white-fronted geese (Anser albifrons) , 1996 .

[59]  S. Bhuiyan Water Management in Relation to Crop Production: Case Study on Rice , 1992 .

[60]  R. Ydenberg,et al.  Avian Influenza: An Ecological and Evolutionary Perspective for Waterbird Scientists , 2006 .