Abstract
Context
Landscape structure influences host–parasite–pathogen dynamics at multiple scales in space and time. Landscape epidemiology, which connects disease ecology and landscape ecology, is still an emerging field.
Objective
We argue that landscape epidemiology must move beyond simply studying the influence of landscape configuration and composition on epidemiological processes and towards a more comparative, systems approach that better incorporates social–ecological complexity.
Methods
We illustrate our argument with a detailed review, based on a single conceptual systems model, of geographic variation in drivers of avian influenza in Western Europe, Southeast Asia, and Southern Africa.
Results
Our three study regions are similar in some ways but quite different in others. The same underlying mechanisms apply in all cases, but differences in the attributes of key components and linkages (most notably avian diversity, the abiotic environment, land use and land cover, and food production systems) create significant differences in avian influenza virus prevalence and human risk between regions.
Conclusions
Landscape approaches can connect local- and continental-scale elements of epidemiology. Adopting a landscape-focused systems perspective on the problem facilitates the identification of the most important commonalities and differences, guiding both science and policy, and helps to identify elements of the problem on which further research is needed. More generally, our review demonstrates the importance of social–ecological interactions and comparative approaches for landscape epidemiology.
Similar content being viewed by others
References
Abolnik C, Cornelius E, Bisschop SPR, Romito M, Verwoerd D (2006) Phylogenetic Analyses of genes from South Africa LPAI Viruses isolated in 2004 from Wild Aquatic Birds suggests Introduction by Eurasian migrants. In: Schudel A, Lombard M (eds) OIE/FAO international scientific conference on avian influenza, Basel, Karger 2006, vol 124, pp 189–199
Abolnik C, Bisschop S, Gerdes T, Olivier A, Horner R (2007) Outbreaks of avian influenza H6N2 viruses in chickens arose by a reassortment of H6N8 and H9N2 ostrich viruses. Virus Genes 34:37–45
Abolnik C, Olivier AJ, Grewar J, Gers S, Romito M (2012) Molecular analysis of the 2011 HPAI H5N2 outbreak in ostriches, South Africa. Avian Dis 56:865–879
Abu-Raddad LJ, Patnaik P, Kublin JG (2006) Dual infection with HIV and malaria fuels the spread of both diseases in sub-Saharan Africa. Science 314(5805):1603–1606
Altman I, Byers JE (2014) Large-scale spatial variation in parasite communities influenced by anthropogenic factors. Ecology 95(7):1876–1887
ASEAN (2010) Prevention, control and eradication of avian influenza in ASEAN: strategies and success stories. Jakarta. http://www.asean.org. Accessed 9 March 2015
Bhushan B, Fry G, Hibi A, Mundkur T, Prawiradilaga DM, Sonobe K, Usui S, Taniguchi T (1993) A field guide to the waterbirds of Asia. Wild Bird Society of Japan, Tokyo
Biancotto A, Iglehart SJ, Lisco A, Vanpouille C, Grivel J-C, Lurain NS, Reichelderfer PS, Margolis LB (2008) Upregulation of human cytomegalovirus by HIV type 1 in human lymphoid tissue ex vivo. AIDS Res Hum Retrovir 24(3):453–462
Both C (2010) Flexibility of timing of avian migration to climate change masked by environmental constraints en route. Curr Biol 20(3):243–248
Breban R, Drake JM, Stallknecht DE, Rohani P (2009) The role of environmental transmission in recurrent avian influenza epidemics. PLoS Comput Biol 5(4):e1000346
British Trust for Ornithology (2014). http://www.bto.org/about-birds/birdfacts/bird-families/waterfowl. Accessed 27 Feb 2015
Brown JD, Swayne DE, Cooper RJ, Burns RE, Stallknecht DE (2007) Persistence of H5 and H7 avian influenza viruses in water. Avian Dis 50:285–289
Brown JD, Goekjian G, Poulson R, Valeika S, Stallknecht DE (2009) Avian influenza virus in water: infectivity is dependent on pH, salinity and temperature. Vet Microbiol 136(1–2):20–26
Burger CE, Abolnik C, Fosgate GT (2012) Antibody response and viral shedding profile of Egyptian geese (Alopochen aegyptiacus) infected with low pathogenicity H7N1 and H6N8 avian influenza viruses. Avian Dis 56(2):341–346
Burgos S, Otte J, Roland-Holst D (2010) In: FAO (ed) Poultry, HPAI and livelihoods in Myanmar—a review. FAO, Roma
Cardona C, Yee K, Carpenter T (2009) Are live bird markets reservoirs of avian influenza? Poult Sci 88(4):856–859
Caron A, Gaidet N, de Garine-Wichatitsky M, Morand S, Cameron EZ (2009) Evolutionary biology, community ecology and avian influenza research. Infect Genet Evol 9:298–303
Caron A, de Garine-Wichatitsky M, Gaidet N, Chiweshe N, Cumming GS (2010) Estimating dynamic risk factors for pathogen transmission using community-level bird census data at the wildlife/domestic interface. Ecol Soc 15(3):25
Caron A, Abolnik C, Mundava, Gaidet N, Burger CE, Mochotlhoane B, Bruinzeel L, Chiweshe N, de Garine-Wichatitsky M, Cumming GS (2011) Persistence of low pathogenic avian influenza virus in waterfowl in a Southern African ecosystem. EcoHealth 8(1):109–115
Costa TP, Brown JD, Howerth EW, Stallknecht DE (2011) Variation in viral shedding patterns between different wild bird species infected experimentally with low-pathogenicity avian influenza viruses that originated from wild birds. Avian Pathol 40(2):119–124
Costa-Hurtado M, Afonso CL, Miller PJ, Spackman E, Kapczynski DR, Swayne DE, Shepherd E, Smith D, Zsak A, Pantin-Jackwood M (2014) Virus interference between H7N2 low pathogenic avian influenza virus and lentogenic Newcastle disease virus in experimental co-infections in chickens and turkeys. Vet Res 45(1):1
Cumming GS (2007a) Global biodiversity scenarios and landscape ecology. Landscape Ecol 22:671–685
Cumming GS (2007b) Global biodiversity scenarios and landscape ecology. Landscape Ecol 22(5):671–685
Cumming GS (2011a) The resilience of big river basins. Water Int 36(1):63–95
Cumming GS (2011b) Spatial resilience in social–ecological systems. Springer, Dordrecht
Cumming GS (2011c) Spatial resilience: integrating landscape ecology, resilience, and sustainability. Landscape Ecol 26(7):899–909
Cumming GS, Caron A, Abolnik C, Catolli G, Bruinzeel L, Burger CE, Cecchettin K, Chiweshe N, Mochotlhoane B, Mutumi G, Ndlovu M (2011) The ecology of influenza A viruses in wild birds in Southern Africa. EcoHealth 8(1):4–13
Cumming GS, Gaidet N, Ndlovu M (2012a) Towards a unification of movement ecology and biogeography: conceptual framework and a case study on Afrotropical ducks. J Biogeogr 39(8):1401–1411
Cumming GS, Paxton M, King J, Beuster H (2012b) Foraging guild membership explains variation in waterbird responses to the hydrological regime of an arid-region flood-pulse river in Namibia. Freshw Biol 57(6):1202–1213
Cumming GS, Ndlovu M, Mutumi GL, Hockey PA (2013) Responses of an African wading bird community to resource pulses are related to foraging guild and food-web position. Freshw Biol 58(1):79–87
DAFF (2011) In: Department of Agriculture, Fisheries and Forestry (ed) A profile of the South African ostrich market value chain. Department of Agriculture, Fisheries and Forestry, Pretoria
Daszak P, Cunningham AA, Hyatt AD (2000) Emerging infectious diseases of wildlife—threats to biodiversity and human health. Science 287:443–449
Daszak P, Cunningham AA, Hyatt AD (2001a) Anthropogenic environmental change and the emergence of infectious diseases in wildlife. Acta Trop 78(2):103–116
Daszak P, Cunningham AA, Hyatt AD (2001b) Anthropogenic environmental change and the emergence of infectious diseases in wildlife. Acta Trop 78:103–116
Daszak P, Plowright R, Epstein J, Pulliam J, Abdul Rahman S, Field H, Smith C, Olival K, Luby S, Halpin K (2006) The emergence of Nipah and Hendra virus: pathogen dynamics across a wildlife–livestock–human continuum. In: Disease ecology: community structure and pathogen dynamics. Oxford University Press, Oxford, pp 186–201
Desvaux S, Grosbois V, Pham TTH, Fenwick S, Tollis S, Pham NH, Tran A, Roger F (2011) Risk factors of highly pathogenic avian influenza H5N1 occurrence at the village and farm levels in the Red River Delta region in Vietnam. Transbound Emerg Dis 58:492–502
Dilley M (2000) Reducing vulnerability to climate variability in Southern Africa: the growing role of climate information. Clim Change 45(1):63–73
Dobson A, Foufopoulos J (2001) Emerging infectious pathogens of wildlife. Philos Trans R Soc Lond B 356(1411):1001–1012
Dobson A, Lafferty KD, Kuris AM, Hechinger RF, Jetz W (2008) Homage to Linnaeus: how many parasites? How many hosts? Proc Natl Acad Sci USA 105:11482–11489
Elith J, Graham CH (2009) Do they? How do they? WHY do they differ? On finding reasons for differing performances of species distribution models. Ecography 32(1):66–77
Elliott P, Wartenberg D (2004) Spatial epidemiology: current approaches and future challenges. Environ Health Perspect 112(9):998–1006
Ellis TM, Bousfield RB, Bissett LA, Dyrting KC, Luk GS, Tsim ST, Sturm-Ramirez K, Webster RG, Guan Y, Malik Peiris JS (2004) Investigation of outbreaks of highly pathogenic H5N1 avian influenza in waterfowl and wild birds in Hong Kong in late 2002. Avian Pathol 33(5):492–505
European Food and Safety Authority (2006) Scientific opinion of the panel on animal health and welfare on a request from the European Commission on migratory birds and their possible role in the spread of highly pathogenic avian influenza. EFSA J 357:1–46
European Food and Safety Authority (2008) Animal health and welfare aspects of avian influenza and the risk of its introduction into the EU poultry holdings: scientific opinion of the Panel on Animal Health and Welfare. EFSA J 715:1–161
FAO (2008) In: FAO (ed) The global strategy for prevention and control of H5N1 highly pathogenic avian influenza. FAO, Roma
FAOSTAT (2013). Statistical yearbook of the Food and Agriculture Organization of the United Nations. http://faostat3.fao.org/home/E. Accessed 9 March 2015
Feare CJ, Kato T, Thomas R (2010) Captive rearing and release of bar-headed geese (Anser indicus) in China: a possible HPAI H5N1 virus infection route to wild birds. J Wildl Dis 46(4):1340–1342
Fenichel EP, Kuminoff NV, Chowell G (2013) Skip the trip: air Travelers’ behavioral responses to pandemic influenza. PLoS ONE 8(3):e58249
Fermet-Quinet E, Bussière C (2007) Small commercial and family poultry production in France: characteristics, and impact of HPAI regulations. FAO Smallholder Poultry Production Paper. Rome
Figuié M (2013) Global health risks and cosmopolitisation: from emergence to interference. Sociol Health Illn 35(2):227–240
Figuie M, Fournier T (2008) Avian influenza in Vietnam: chicken-hearted consumers? Risk Anal 28(2):441–451
Fouque C, Guillemain M, Benmergui M, Delacour G, Mondain-Monval JY, Schricke V (2007) Mute swan (Cygnus olor) winter distribution and numerical trends over a 16-year period (1987/1988–2002/2003) in France. J Ornithol 148(4):477–487
Franklin J (2010) Mapping species distributions: spatial inference and prediction. Cambridge University Press, Cambridge
Gaidet N, Caron A, Cappelle J, Cumming GS, Balanca G, Hammoumi S, Cattoli G, Abolnik C, Servan de Almeida R, Gil P, Fereidouni S, Grosbois V, Tran A, Mundava J, Fofana B, Ould El Mamy AB, Ndlovu M, Mondain-Monval JY, Triplet P, Hagemeijer W, Karesh WB, Newman SH, Dodman T (2012a) Understanding the ecological drivers of avian influenza virus infection in wildfowl: a continental scale study across Africa. Proc R Soc B 279(1731):1131–1141
Gaidet N, Ould El Mamy AB, Cappelle J, Caron A, Cumming GS, Grosbois V, Gil P, Hammoumi S, Servan de Almeida R, Fereidouni SR, Cattoli G, Abolnik C, Mundava J, Fofana B, Ndlovu M, Hurtado RF, Newman SH, Dodman T, Balança G (2012b) Investigating avian influenza infection hotspots in old-world shorebirds. PLoS ONE 7(9):e46049
Galuzo I (1975) Landscape epidemiology (epizootiology). Adv Vet Sci Comp Med 19:73
Gardner AM, Lampman RL, Muturi EJ (2014) Land use patterns and the risk of West Nile virus transmission in central Illinois. Vector Borne Zoonotic Dis 14(5):338–345
Geist HJ, Lambin EF (2002) Proximate causes and underlying driving forces of tropical deforestation. Bioscience 52(2):143–150
Gilbert M, Pfeiffer DU (2012) Risk factor modelling of the spatio-temporal patterns of highly pathogenic avian influenza (HPAIV) H5N1: a review. Spat Spatio-temporal Epidemiol 3(3):173–183
Gilbert M, Chaitaweesub P, Parakamawongsa T, Premashthira S, Tiensin T, Kalpravidh W, Wagner H, Slingenbergh J (2006) Free-grazing ducks and highly pathogenic avian influenza, Thailand. Emerg Infect Dis 12(2):227–234
Gilbert M, Xiao X, Chaitaweesub P, Kalpravidh W, Premashthira S, Boles S, Slingenbergh J (2007) Avian influenza, domestic ducks and rice agriculture in Thailand. Agric Ecosyst Environ 119(3–4):409–415
Gilbert M, Xiao X, Pfeiffer DU, Epprecht M, Boles S, Czarnecki C, Chaitaweesub P, Kalpravidh W, Minh PQ, Otte MJ, Martin V, Slingen J (2008) Mapping H5N1 highly pathogenic avian influenza in Southeast Asia. Proc Natl Acad Sci USA 105(12):4769–4774
Green AJ, Elmberg J (2014) Ecosystem services provided by waterbirds. Biol Rev 89(1):105–122
Grey D, Garrick D, Blackmore D, Kelman J, Muller M, Sadoff C (2013) Water security in one blue planet: twenty-first century policy challenges for science. Philos Trans R Soc A 371(2002):20120406
Hahn MB, Gurley ES, Epstein JH, Islam MS, Patz JA, Daszak P, Luby SP (2014) The role of landscape composition and configuration on Pteropus giganteus roosting ecology and Nipah virus spillover risk in Bangladesh. Am J Trop Med Hyg 90(2):247–255
Herrick KA, Huettmann F, Lindgren MA (2013) A global model of avian influenza prediction in wild birds: the importance of northern regions. Vet Res 44(1):42
Hirschfeld A, Heyd A (2005) Mortality of migratory birds caused by hunting in Europe: bag statistics and proposals for the conservation of birds and animal welfare. Ber zum Vogelschutz 42:47–74
Hockey PAR (2000) Patterns and correlates of bird migrations in sub-Saharan Africa. Emu 100:401–417
Hockey PAR, Dean WRJ, Ryan PG (2005) Roberts’ birds of Southern Africa. Russell Friedman Books CC, Pretoria
Holt RD, Dobson A (2007) Extending the principles of community ecology to address the epidemiology of host–pathogen systems. In: Collinge SK, Ray C (eds) Disease ecology: community structure and pathogen dynamics. Oxford University Press, Oxford, pp 6–27
Huntjens P, Pahl-Wostl C, Rihoux B, Schlüter M, Flachner Z, Neto S, Koskova R, Dickens C, Nabide Kiti I (2011) Adaptive water management and policy learning in a changing climate: a formal comparative analysis of eight water management regimes in Europe, Africa and Asia. Environ Policy Gov 21(3):145–163
Ichinohe T, Pang IK, Kumamoto Y, Peaper DR, Ho JH, Murray TS (2011) Microbiota regulates immune defense against respiratory tract influenza A virus infection. Proc Natl Acad Sci 108(13):5354–5359
Ito T, Goto H, Yamamoto E, Tanaka H, Takeuchi M, Kuwayama M, Kawaoka Y, Otsuki K (2001) Generation of a highly pathogenic avian influenza A virus from an avirulent field isolate by passaging in chickens. J Virol 75(9):4439–4443
Ives A, Ronet C, Prevel F, Ruzzante G, Fuertes-Marraco S, Schutz F,. Zangger , Revaz-Breton M, Lye L-F, Hickerson SM, Beverley SM, Acha-Orbea H, Launois P, Fasel N, Masina S (2011) Leishmania RNA virus controls the severity of mucocutaneous leishmaniasis. Science 331:775–778
Jones BA, Grace D, Kock R, Alonso S, Rushton J, Said MY, McKeever D, Mutua F, Young J, McDermott J (2013) Zoonosis emergence linked to agricultural intensification and environmental change. Proc Natl Acad Sci 110(21):8399–8404
Keesing F, Young TP (2014) Cascading consequences of the loss of large mammals in an African savanna. Bioscience 64(6):487–495
Kingsford RT, Jenkins KM, Porter JL (2004) Imposed hydrological stability on lakes in arid Australia and effects on waterbirds. Ecology 85(9):2478–2492
Krauss S, Stallknecht DE, Negovetich NJ, Niles LJ, Webby RJ, Webster RG (2010) Coincident ruddy turnstone migration and horseshoe crab spawning creates an ecological ‘hot spot’ for influenza viruses. Proc R Soc B 277(1699):3373–3379
Lafferty KD, Allesina S, Arim M, Briggs CJ, De Leo G, Dobson AP, Dunne JA, Johnson PT, Kuris AM, Marcogliese DJ, Martinez ND, Memmott J, Marquet PA, McLaughlin JP, Mordecai EA, Pascual M, Poulin R, Thieltges DW (2008) Parasites in food webs: the ultimate missing links. Ecol Lett 11(6):533–546
Lambin EH, Geist HJ (2006) Land-Use and Land-Cover Change: local processes and global impacts. Springer, Berlin
Lambin EF, Tran A, Vanwambeke SO, Linard C, Soti V (2010) Pathogenic landscapes: interactions between land, people, disease vectors, and their animal hosts. Int J Health Geogr 9(54):1–13
Lane-deGraaf KE, Kennedy RC, Arifin SMN, Madey GR, Fuentes A, Hollocher H (2013) A test of agent-based models as a tool for predicting patterns of pathogen transmission in complex landscapes. BMC Ecol 13:35
Latorre-Margalef N, Tolf C, Grosbois V, Avril A, Bengtsson D, Wille M, Osterhaus AD, Fouchier RA, Olsen B, Waldenström J (2014) Long-term variation in influenza A virus prevalence and subtype diversity in migratory mallards in northern Europe. Proc R Soc B 281(1781):20140098
Lehikoinen A, Jaatinen K, Vähätalo AV, Clausen P, Crowe O, Deceuninck B, Hearn R, Holt CA, Hornman M, Keller V, Nilsson L, Langendoen T, Tománková I, Wahl J, Fox AD (2013) Rapid climate driven shifts in wintering distributions of three common waterbird species. Glob Change Biol 19(7):2071–2081
Leibler JH, Otte J, Roland-Holst D, Pfeiffer DU, Soares Magalhaes R, Rushton J, Graham JP, Silbergeld EK (2009) Industrial food animal production and global health risks: exploring the ecosystems and economics of avian influenza. EcoHealth 6(1):58–70
Likens GE (2004) Some perspectives on long-term biogeochemical research from the Hubbard Brook ecosystem study. Ecology 85(9):2355–2362
Liu C-M, Lin S-H, Chen Y-C, Lin KC-M, Wu T-SJ, King C-C (2007) Temperature drops and the onset of severe avian influenza A H5N1 virus outbreaks. PLoS ONE 2(2):e191
Mangnall MJ, Crowe TM (2003) The effects of agriculture on farmland bird assemblages on the Agulhas Plain, Western Cape, South Africa. Afr J Ecol 41(3):266–276
Massey RC, Buckling A, French-Constant R (2004) Interference competition and parasite virulence. Proc R Soc B 271:785–788
Mather C, Marshall A (2011) Living with disease? Biosecurity and avian influenza in ostriches. Agric Hum Values 28(2):153–165
Mathevet R (2000) Les usages des zones humides camarguaises: enjeux et dynamique des interactions environnement/usagers/territoire. Université J. Moulin Lyon 3, Lyon
Mathevet R, Mesléard F (2002) The origins and functioning of the private wildfowling lease system in a major Mediterranean wetland: the Camargue (Rhone River Delta, Southern France). Land Use Policy 19(4):277–286
McCullers JA (2006) Insights into the interaction between influenza virus and Pneumococcus. Clin Microbiol Rev 19(3):571–582
McLeod A, Morgan N, Prakash A, Hinrichs J (2005) Economic and social impacts of avian influenza. In: Proceedings of the joint FAO/OMS/OIE/World Bank conference on avian influenza and human pandemic influenza, November 2005, pp 7–9
Meentemeyer RK, Haas SE, Václavík T (2012) Landscape epidemiology of emerging infectious diseases in natural and human-altered ecosystems. Annu Rev Phytopathol 50:379–402
Modjarrad K, Vermund SH (2010) Effect of treating co-infections on HIV-1 viral load: a systematic review. Lancet Infect Dis 10(7):455–463
Mooij JH (2005) Protection and use of waterbirds in the European Union. Beitr zur Jagd- und Wildforschung 30:443–454
Moore C, Cumming GS, Slingsby J, Grewar J (2014) Tracking socioeconomic vulnerability using network analysis: insights from an avian influenza outbreak in an ostrich production network. PLoS ONE 9(1):e86973
Mundava J, Caron A, Gaidet N, Couto F, Couto T, de Garine-Wichatitksy M, Mundy P (2012) Factors influencing long-term and seasonal waterbird abundance and composition at two adjacent lakes in Zimbabwe. Ostrich 83(2):69–77
Mundkur T (2006) Successes and challenges of promoting conservation of migratory waterbirds and wetlands in the Asia–Pacific region: nine years of a regional strategy. In: Boere GC, Gailbraith CA, Stroud DA (eds) Waterbirds around the world. The Stationery Office, Edinburgh, pp 81–87
Mussa T, Rodriguez-Cariño C, Sanchez-Chardi A, Baratelli M, Costa-Hurtado M, Fraile L, Dominguez J, Aragon V, Montoya M (2012) Differential interactions of virulent and non-virulent H. parasuis strains with naïve or swine influenza virus pre-infected dendritic cells. Vet Res 43(1):80
Myers SS, Gaffikin L, Golden CD, Ostfeld RS, Redford KH, Ricketts TH, Turner WR, Osofsky SA (2013) Human health impacts of ecosystem alteration. Proc Natl Acad Sci 110(47):18753–18760
Ngom EHM, Ndione J-A, Ba Y, Konate L, Faye O, Diallo M, Dia I (2013) Spatio-temporal analysis of host preferences and feeding patterns of malaria vectors in the sylvo-pastoral area of Senegal: impact of landscape classes. Parasites Vectors 6:332
Norberg J, Cumming GS (2008) Complexity theory for a sustainable future. Columbia University Press, New York
Oatley TB, Prys-Jones RP (1986) A comparative analysis of movements of Southern African waterfowl (Anatidae) based on ringing recoveries. S Afr J Wildl Res 16:1–6
Okanga S, Cumming GS, Hockey PA, Peters JL (2013) Landscape structure influences avian malaria ecology in the Western Cape, South Africa. Landscape Ecol 28(10):2019–2028
Okes NC, Hockey PA, Cumming GS (2008) Habitat use and life history as predictors of bird responses to habitat change. Conserv Biol 22(1):151–162
Ostfeld RS, Glass GE, Keesing F (2005) Spatial epidemiology: an emerging (or re-emerging) discipline. Trends Ecol Evol 20(6):328–336
Ostrom E (2009) A general framework for analyzing sustainability of social–ecological systems. Science 352:419–422
Owen M, Black JM (1990) Waterfowl ecology. Chapman and Hall, New York
Patz JA, Daszak P, Tabor GM, Aguirre AA, Pearl M, Epstein J, Wolfe ND, Kilpatrick AM, Foufopoulos J, Molyneux D, Bradley DJ, M. o. t. W. G. o. L. U. C. a. D. Emergence (2004) Unhealthy landscapes: policy recommendations on land use change and infectious disease emergence. Environ Health Perspect 112(10):1092–1098
Paul MC, Gilbert M, Desvaux S, Andriamanivo HR, Peyre M, Nguyen Viet K, Thanapongtharm W, Chevalier V (2014) Agro-environmental determinants of avian influenza circulation: a multisite study in Thailand, Vietnam and Madagascar. PLoS ONE 9(7):e101958
Pavlovsky E (1966) Natural nidality of transmissible diseases with special reference to the landscape epidemiology of zooanthroponoses. University of Illinois Press, Urbana
Pearce N, Merletti F (2006) Complexity, simplicity, and epidemiology. Int J Epidemiol 35(3):515–519
Perkins LE, Swayne DE (2002) Pathogenicity of a Hong Kong-origin H5N1 highly pathogenic avian influenza virus for emus, geese, ducks, and pigeons. Avian Dis 46(1):53–63
Perrings C, Castillo-Chavez C, Chowell G, Daszak P, Fenichel EP, Finnoff D, Horan RD, Kilpatrick AM, Kinzig AP, Kuminoff NV (2014) Merging economics and epidemiology to improve the prediction and management of infectious disease. EcoHealth. doi:10.1007/s10393-014-0963-6
Petrie SA, Rogers KH (1997a) Activity budget of breeding white-faced whistling ducks Dendrocygna viduata on stock-ponds in semi-arid South Africa, and a comparison with north-temperate waterfowl. S Afr J Wildl Res 27(3–4):79–85
Petrie SA, Rogers KH (1997b) Ecology, nutrient reserve dynamics and movements of white-faced ducks in South Africa. Department of Environmental Affairs and Tourism, South Africa, Pretoria
Pickett STA, Jones C, Kolasa J (2007) Ecological understanding: the nature of theory and the theory of nature. Academic, New York
Pingali PL (2012) Green Revolution: impacts, limits, and the path ahead. Proc Natl Acad Sci 109(31):12302–12308
Pittman M, Laddomada A (2007) Legislation for the control of Avian Influenza in the European Union. Zoonoses Public Health 55:29–36
Plowright RK, Sokolow SH, Gorman ME, Daszak P, Foley JE (2008) Causal inference in disease ecology: investigating ecological drivers of disease emergence. Front Ecol Environ 6(8):420–429
Polis GA, Anderson WB, Holt RD (1997) Toward an integration of landscape and food web ecology: the dynamics of spatially subsidized food webs. Annu Rev Ecol Syst 28:289–316
Polis GA, Power ME, Huxel GR (eds) (2004) Food webs at the landscape level. University of Chicago Press, Chicago
Pretty J, Toulmin C, Williams S (2011) Sustainable intensification in African agriculture. Int J Agric Sustain 9(1):5–24
RAHC (2013) Regional Animal Health Center (RAHC) for Southern Africa. RAHC. http://www.rr-africa.oie.int/en/RR/en_rahc_crsa_sa.html. Accessed 27 Feb 2015
Reisen WK (2010) Landscape epidemiology of vector-borne diseases. Annu Rev Entomol 55:461–483
Robinson SJ, Samuel MD, Rolley RE, Shelton P (2013) Using landscape epidemiological models to understand the distribution of chronic wasting disease in the Midwestern USA. Landscape Ecol 28(10):1923–1935
Roche B, Lebarbenchon C, Gauthier-Clerc M, Chang CM, Thomas F, Renaud F, van der Werf S, Guegan JF (2009) Water-borne transmission drives avian influenza dynamics in wild birds: the case of the 2005–2006 epidemics in the Camargue area. Infect Genet Evol 9(5):800–805
Rohani P, Breban R, Stallknecht DE, Drake JM (2009) Environmental transmission of low pathogenicity avian influenza viruses and its implications for pathogen invasion. Proc Natl Acad Sci USA 106(25):10365–10369
Rushton J, Viscarra R, Guerne Bleich E, McLeod A (2005) Impact of avian influenza outbreaks in the poultry sectors of five South East Asian countries (Cambodia, Indonesia, Lao PDR, Thailand, Viet Nam) outbreak costs, responses and potential long term control. World's Poult Sci J 61:491–514
Seckler D, Amarasinghe U, Molden DJ, de Silva R, Barker R (1998) World water demand and supply, 1990 to 2025: scenarios and issues. In: Research Report 19. IWMI, Colombo
Si Y, Wang T, Skidmore A, De Boer W (2010) Environmental factors influencing the spread of the highly pathogenic avian influenza H5N1 virus in wild birds in Europe. Ecol Soc 15:26
Slenning BD (2010) Global climate change and implications for disease emergence. Vet Pathol 47(1):28–33
Smith G, Dunipace M (2011) How backyard poultry flocks influence the effort required to curtail avian influenza epidemics in commercial poultry flocks. Epidemics 3:71–75
Söderquist P, Gunnarsson G, Elmberg J (2013) Longevity and migration distance differ between wild and hand-reared mallards Anas platyrhynchos in Northern Europe. Eur J Wildl Res 59:159–166
Songserm T, Jam-on R, Sae-Heng N, Meemak N, Hulse-Post DJ, Sturm-Ramirez KM, Webster RG (2006) Domestic ducks and H5N1 influenza epidemic, Thailand. Emerg Infect Dis 12(4):575–581
Tamisier A, Grillas P (1994) A review of habitat changes in the Camargue: an assessment of the effects of the loss of biological diversity on the wintering waterfowl community. Biol Conserv 70:39–47
Telfer S, Lambin X, Birtles R, Beldomenico P, Burthe S, Paterson S, Begon M (2010) Species interactions in a parasite community drive infection risk in a wildlife population. Science 330:243
Thomas M, Bouma A, Ekker H, Fonken A, Stegeman J, Nielen M (2005) Risk factors for the introduction of high pathogenicity Avian Influenza virus into poultry farms during the epidemic in the Netherlands in 2003. Prev Vet Med 69(1):1–11
Tiensin T, Nielen M, Songserm T, Kalpravidh W, Chaitaweesub P, Amonsin A., Chotiprasatintara S, Chaisingh A, Damrongwatanapokin S, Wongkasemjit S, Antarasena C, Songkitti K, Chanachai K, Thanapongtham W, Stegeman A (2007) Geographic and temporal distribution of highly pathogenic avian influenza A Virus (H5N1) in Thailand, 2004–2005: an overview. Avian Dis 50:182–188
Tilman D, Fargione J, Wolff B, D'Antonio C, Dobson A, Howarth R, Schindler D, Schlesinger WH, Simberloff D, Swackhamer D (2001) Forecasting agriculturally driven global environmental change. Science 292(5515):281–284
Tong S, Zhu X, Li Y, Shi M, Zhang J, Bourjeois M, Yang H, Chen X, Recuenco S, Gomez J, Chen LM, Johnson A, Tao Y, Dreyfus C, Yu W, McBride R, Carney PJ, Gilbert AT, Chang J, Guo Z, Davis CT, Paulson JC, Stevens J, Rupprecht CE, Holmes EC, Wilson IA, Donis RO (2013) New World bats harbour diverse influenza A viruses. PLoS Pathog 9(10):e1003567
Tran PM, Waller L (2013) Effects of landscape fragmentation and climate on Lyme disease incidence in the northeastern United States. EcoHealth 10(4):394–404
Tyson PD (1986) Climatic change and variability in Southern Africa. Oxford University Press, Capetown
Unwin MT (2011) The atlas of birds: diversity, behavior, and conservation. Princeton University Press, Princeton
Van Dalen KK, Franklin AB, Mooers NL, Sullivan HJ, Shriner SA (2010) Shedding light on avian influenza H4N6 infection in mallards: modes of transmission and implications for surveillance. PLoS ONE 5(9):e12851
van Dijk JGB, Hoye BJ, Verhagen JH, Nolet BA, Fouchier RAM, Klaassen M (2014) Juveniles and migrants as drivers for seasonal epizootics of avian influenza virus. J Anim Ecol 83:266–275
Vandegrift KJ, Sokolow SH, Daszak P, Kilpatrick AM (2010) Ecology of avian influenza viruses in a changing world. Ann NY Acad Sci 1195(1):113–128
Vittecoq M, Thomas F, Jourdain E, Moutou F, Renaud F, Gauthier-Clerc M (2014) Risks of emerging infectious diseases: evolving threats in a changing area, the Mediterranean Basin. Transbound Emerg Dis 61(1):17–27
Viviroli D, Archer D, Buytaert W, Fowler H, Greenwood G, Hamlet A, Huang Y, Koboltschnig G, Litaor M, Lopez-Moreno J (2011) Climate change and mountain water resources: overview and recommendations for research, management and policy. Hydrol Earth Syst Sci 15(2):471–504
Walsh MG (2013) The relevance of forest fragmentation on the incidence of human babesiosis: investigating the landscape epidemiology of an emerging tick-borne disease. Vector-Borne Zoonotic Dis 13:250–255
Wardrop NA, Kuo C-C, Wang H-C, Clements ACA, Lee P-F, Atkinson PM (2013) Bayesian spatial modelling and the significance of agricultural land use to scrub typhus infection in Taiwan. Geospatial Health 8(1):229–239
Weber TP, Stilianakis NI (2008) Inactivation of influenza A viruses in the environment and modes of transmission: a critical review. J Infect 57(5):361–373
Webster RG (2004) Wet markets—a continuing source of severe acute respiratory syndrome and influenza? Lancet 363(9404):234–236
Wilcox BR, Knutsen GA, Berdeen J, Goekjian V, Poulson R, Goyal S, Sreevatsan S, Cardona C, Berghaus RD, Swayne DE, Yabsley MJ, Stallknecht DE (2011) Influenza-A viruses in ducks in northwestern Minnesota: fine scale spatial and temporal variation in prevalence and subtype diversity. PLoS ONE 6(9):e24010
Williams RAJ, Peterson AT (2009) Ecology and geography of avian influenza (HPAI H5N1) transmission in the Middle East and northeastern Africa. Int J Health Geogr 8:47
Windhorst H-W (2007) Changing patterns of poultry production in the European Union. In: Commission of the European Communities (ed) Development of new integrated strategies for prevention, control and monitoring of epizootic poultry diseases. Commission of the European Communities
Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M, Magris M, Hidalgo G, Baldassano RN, Anokhin AP (2012) Human gut microbiome viewed across age and geography. Nature 486(7402):222–227
Zinsstag J, Schelling E, Waltner-Toews D, Tanner M (2011) From “one medicine” to “one health” and systemic approaches to health and well-being. Prev Vet Med 101:148–156
Acknowledgments
We are grateful for funding support from a Protea Grant from the National Research Foundation of South Africa (NRF), the DST/NRF Centre of Excellence at the Percy FitzPatrick Institute, and the James S. McDonnell Foundation. This work was conducted within the framework of Cirad’s Research Platform “Production and Conservation in Partnership” and the AHEAD Initiative.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Cumming, G.S., Abolnik, C., Caron, A. et al. A social–ecological approach to landscape epidemiology: geographic variation and avian influenza. Landscape Ecol 30, 963–985 (2015). https://doi.org/10.1007/s10980-015-0182-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10980-015-0182-8