Supplementary Text 1. Well-Studied Bird Pathogens

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Supplementary Text 1. Well-Studied Bird Pathogens

1Electronic Supplementary Material

2Supplementary Text 1. Well-Studied Bird Pathogens.

3We selected these diseases because they have been the subject of extensive studies and affect

4humans and livestock as well as migratory birds. In particular, we chose avian influenza and

5avian malaria because in order to predict the effects of climate change on a parasite, we need to

6know the present-day geographic distribution of the parasite and its host. Avian influenza and

7malaria are two of only a few parasites for which we have this detailed knowledge at present . In

8the interest of comprehensiveness, we also wanted to include a bacterial example. We selected

9Salmonella because a great deal is known from human strains . Furthermore, there is a literature

10on seasonal variation in Salmonella prevalence in wild birds and Salmonella genotypes in avian

11migrants .

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13Avian malaria

14Plasmodium and related haemosporidians (Haemoproteus and Leucocytozoon) are among the

15best-studied bird pathogens. Today, information for ~1,000 parasite mtDNA lineages and their

16distribution in 600 species of birds are available . Birds wintering in the tropics annually bring

17hundreds of parasite species to temperate breeding areas. Most tropical lineages are not

18transmitted within migrant populations or to local resident species in breeding locations, even

19though gametocytes circulate in the blood of the birds . Nevertheless, resident northern birds may

20become infected with tropical parasites and there is evidence that vectors in tropical areas are

21expanding their ranges due to climate change . If such parasites can establish transmission cycles

22at northern latitudes, previously unexposed species might be severely affected, as famously seen

23in the decline of endemic birds of Hawaii upon introduction of Plasmodium in the 20th century .

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25Salmonella

26Salmonella is highly clonal with close to 2,500 described serological variants (serovars). Host

27range varies from narrow to broad, and considerable variation also exists between lineages

28within serovars . Symptoms vary from asymptomatic to death depending on both host and

29parasite, as well as environmental stressors. Salmonellosis is frequently recorded in seed-eating

30birds at feeder tables where fecal contamination may spark an outbreak . Public health concerns

31have initiated studies on fecal contamination of recreational water or pastures by geese and

32gulls . Gulls frequently pick up Salmonella from waste; the most frequent serovars are also

33common in human or food animal sources . Spread of anthropogenic Salmonella could induce

34epizootics in susceptible species , or increase in frequency if concomitant factors reduce the

35health status of individuals. Salmonella has been isolated from gulls and passerines during the

36migratory period , but the extent to which infected birds can transport the bacteria over long

37distances requires further study.

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39Influenza A virus

40Influenza A viruses are common in aquatic birds, especially dabbling ducks . The segmented

41RNA genome and high mutation rate result in considerable genetic variation, particularly in the

42surface proteins that interact with host immune systems. Host shifts occur frequently: to

43gallinaceous poultry where it may cause AIV, and to humans and other mammals where it may

44cause flu. In dabbling ducks, prevalence follows seasonal patterns and is higher in juveniles .

45Exposure to low-pathogenic subtypes may infer transient partial immunity to other subtypes,

46including highly-pathogenic variants . Infections in dabbling ducks have been associated with

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4 47lower condition and ecological costs . Non-reservoir bird species have other infection patterns

48and seem sometimes more strongly affected by infection . Highly pathogenic H5N1 has caused

49considerable mortality in wild populations, including range restricted species in Asia . The

50mechanism by which highly pathogenic H5N1 spreads to new areas remains controversial. For

51example, the international poultry trade and long-distance movements by migratory birds have

52both been hypothesized to explain the introduction of H5N1 to Europe from Asia in 2006.

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6 53Supplementary Text 2. Pathogen Ecology.

54Generalists vs. specialists.

55Many pathogens are host specific, being restricted to one or few host species to which they are

56well adapted. Intracellular parasites like viruses, rickettsia, and protozoa ultimately depend on

57the survival of their specific host and have evolved strategies to balance their own reproductive

58success against the impairment to the host . This includes highly specialized mechanisms during

59the viral replication cycle starting with the entry of the host cell. The host specificity of Avian

60influenza viruses is mediated through the hemagglutinin glycoprotein, which binds to sialic acids

61on the host cell membrane, while the Circumsporozoite protein of Plasmodium falciparum

62provides the specific binding to host liver cells . Pastoret et al. provide an overview of the avian

63immune system.

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65 Generalist pathogens are less selective in the choice of their hosts; for example, many

66bacteria species have a broad host range and are not necessarily dependent on a specific host. As

67extracellular parasites, they are able to survive and replicate even outside their host and have

68evolved strategies for long term survival in the environment. The most impressive examples are

69sporulating bacteria such as Bacillus anthracis, which can survive for decades in the

70environment . Pasteurella multocida, the causative agent for avian cholera is another example of

71a generalist pathogen. It is distributed worldwide and is part of the natural oral flora of

72carnivores, but causes peracute septic infections in bird species .

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74 Often adaption to a major host can be observed, while the replication of the pathogen in a

75minor host is less effective and can even be interrupted in a dead end host, which either does

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8 76not replicate the virus or dies of severe symptoms of disease. For the example, wild waterfowl

77appear to be a major host of avian influenza but geese, while are susceptible to the virus, are less

78important for the perpetuation of the infection and can be considered a minor host .

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80 Wild bird populations are the natural reservoir for several zoonotic pathogens and spill-over

81infections from wild birds to livestock or humans are of special concern for public health and

82safety. Spill-over infections have been reported for several avian pathogens such as for instance

83AIV or duck plague virus .

84For the maintenance of an infection within the population, many factors are relevant. Most

85important is the success of a pathogen within the individual host (see Supplementary Fig. 1),

86which is mainly influenced by the pathogenic properties of the pathogen and the immune system

87of the host. Like avian reoviruses, which are resistant to interferon , many pathogens have

88evolved strategies to evade the host’s immune system.

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90 Another important aspect of pathogen ecology is the transmission of the pathogen from one

91host to another. Directly-transmitted pathogens infect the host via contact with another

92infected host. Vector-borne pathogens, defined as pathogens transmitted to the host via an

93arthropod or fomite that does not cause the disease itself , can be highly specialized or can

94depend on multiple host species. In the case of avian malaria, arthropod hosts are essential for

95the replication of the parasite and can transmit the parasite between host populations .

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10 96Supplementary Figure

97Supplementary Figure 1. From infection to disease. Successful infection of a host can lead to

98different outcomes ranging from asymptomatic infection to symptomatic disease. A highly

99specialized and adapted parasite causes a chronic infection with little impairment of the host.

100Depending on the host’s immune response, an asymptomatic infection can later become

101symptomatic.

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12 102 Supplementary Figure 1.

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106 References 107 108 109Beato MS, and Capua I (2011). Transboundary spread of highly pathogenic avian influenza 110 through poultry commodities and wild birds: a review. Revue Scientifique et Technique 111 (International Office of Epizootics) 30:51-61.

112Bensch S, Hellgren O, and Perez-Tris J (2009). MalAvi: a public database of malaria parasites 113 and related haemosporidians in avian hosts based on mitochondrial cytochrome b 114 lineages. Molecular Ecology Resources 9:1353-1358.

115Botzler RG (1991). Epizootiology of avian cholera in wildfowl. Journal of Wildlife Diseases 116 27:367-395.

117Chaves LF, and Koenraadt CJM (2010). Climate change and highland malaria: fresh air for a hot 118 debate. Quarterly Review of Biology 85:27-55.

119Chen H, Smith GJD, Zhang SY, Qin K, Wang J, Li KS, et al. (2005). H5N1 virus outbreak in 120 migratory waterfowl. Nature 436:191-192.

121Craven SE, Stern NJ, Line E, Bailey JS, Cox NA, and Fedorka-Cray P (2000). Determination of 122 the incidence of Salmonella spp., Campylobacter jejuni, and Clostridium perfringens in 123 wild birds near broiler chicken houses by sampling intestinal droppings. Avian Diseases 124 44:715-720.

125Daoust P-Y, and Prescot JF (2007). Salmonellosis. Pages 270-288 in N. J. Thomas and D. B. 126 Hunter, editors. Infectious Diseases of Wild Birds. Blackwell, Oxford.

127Deibel R, Emord DE, Dukelow W, Hinshaw VS, and Wood JM (1985). Influenza A viruses and 128 paramyxoviruses in ducks in the Atlantic Flyway, 1977-1983, including an H5N2 isolate 129 related to the virulent chicken virus. Avian Diseases 29:970-985.

130Ewald PW (1998). The evolution of virulence and emerging diseases. Journal of Urban Health- 131 Bulletin of the New York Academy of Medicine 75:480-491.

132Fallacara DM, Monahan CM, Morishita TY, and Wack RF (2001). Fecal shedding and 133 antimicrobial susceptibility of selected bacterial pathogens and a survey of intestinal 134 parasites in free-living waterfowl. Avian Diseases 45:128-135.

135Fereidouni SR, Starick E, Beer M, Wilking H, Kalthoff D, Grund C, et al. (2009). Highly 136 pathogenic avian influenza virus infection of mallards with homo- and heterosubtypic 137 immunity induced by low pathogenic avian influenza viruses. Plos One 4:e6706.

17 9

18 138Forum on Microbrial Threats (2008). Vector-borne Diseases. Understanding the Environmental, 139 Human Health, and Ecological Connections. National Academies Press, Washington, 140 DC.

141Foti M, Daidone A, Aleo A, Pizzimenti A, Giacopello C, and Mammina C (2009). Salmonella 142 bongori 48:z(35):- in Migratory Birds, Italy. Emerging Infectious Diseases 15:502-503.

143Gauthier-Clerc M, Lebarbenchon C, and Thomas F (2007). Recent expansion of highly 144 pathogenic avian influenza H5N1: a critical review. Ibis 149:202-214.

145Gonzalez-Lopez C, Martinez-Costas J, Esteban M, and Benavente J (2003). Evidence that avian 146 reovirus sigma A protein is an inhibitor of the double-stranded RNA-dependent protein 147 kinase. Journal of General Virology 84:1629-1639.

148Gough RE, Borland ED, Keymer IF, and Stuart JC (1987). An outbreak of duck virus enteritis in 149 commercial ducks and geese in East Anglia. Veterinary Record 121:85-85.

150Harder TC, Teuffert J, Starick E, Gethmann J, Grund C, Fereidouni S, et al. (2009). Highly 151 Pathogenic Avian Influenza Virus (H5N1) in frozen duck carcasses, Germany, 2007. 152 Emerging Infectious Diseases 15:272-279.

153Hellgren O, Waldenstrom J, Perez-Tris J, Szollosi E, Hasselquist D, Krizanauskiene A, et al. 154 (2007). Detecting shifts of transmission areas in avian blood parasites - a phylogenetic 155 approach. Molecular Ecology 16:1281-1290.

156Hernandez J, Bonnedahl J, Waldenstrom J, Palmgren H, and Olsen B (2003). Salmonella in birds 157 migrating through Sweden. Emerging Infectious Diseases 9:753-755.

158Hugh-Jones M, and Blackburn J (2009). The ecology of Bacillus anthracis. Molecular Aspects 159 of Medicine 30:356-367.

160Hughes LA, Shopland S, Wigley P, Bradon H, Leatherbarrow AH, Williams NJ, et al. (2008). 161 Characterisation of Salmonella enterica serotype Typhimurium isolates from wild birds 162 in northern England from 2005-2006. Bmc Veterinary Research 4:4.

163Kleijn D, Munster VJ, Ebbinge BS, Jonkers DA, Muskens G, Van Randen Y, et al. (2010). 164 Dynamics and ecological consequences of avian influenza virus infection in greater 165 white-fronted geese in their winter staging areas. Proceedings of the Royal Society B- 166 Biological Sciences 277:2041-2048.

167Klenk H-D, Mastrosovich MN, and Stech J (2008). Avian Influenza. Monographs in Virology 168 Volume 27. Karger, Basel.

169Latorre-Margalef N, Gunnarsson G, Munster VJ, Fouchier RAM, Osterhaus A, Elmberg J, et al. 170 (2009). Effects of influenza A virus infection on migrating mallard ducks. Proceedings of 171 the Royal Society B-Biological Sciences 276:1029-1036.

19 10

20 172Martinez-Costas J, Gonzalez-Lopez C, Vakharia VN, and Benavente J (2000). Possible 173 involvement of the double-stranded RNA-binding core protein sigma A in the resistance 174 of avian reovirus to interferon. Journal of Virology 74:1124-1131.

175McClelland M, Sanderson KE, Spieth J, Clifton SW, Latreille P, Courtney L, et al. (2001). 176 Complete genome sequence of Salmonella enterica serovar typhimurium LT2. Nature 177 413:852-856.

178Munster VJ, Baas C, Lexmond P, Waldenstrom J, Wallensten A, Fransson T, et al. (2007). 179 Spatial, temporal, and species variation in prevalence of influenza A viruses in wild 180 migratory birds. Plos Pathogens 3:e61.

181Olsen B, Bergstrom S, McCafferty DJ, Sellin M, and Wistrom J (1996). Salmonella enteritidis in 182 Antarctica: Zoonosis in man or humanosis in penguins? Lancet 348:1319-1320.

183Olsen B, Munster VJ, Wallensten A, Waldenstrom J, Osterhaus A, and Fouchier RAM (2006). 184 Global patterns of influenza A virus in wild birds. Science 312:384-388.

185Palinauskas V, Valkiūnas G, Bolshakov CV, and Bensch S (2011). Plasmodium relictum 186 (lineage SGS1) and Plasmodium ashfordi (lineage GRW2): The effects of the co- 187 infection on experimentally infected passerine birds. Experimental Parasitology 127:527- 188 533.

189Palmgren H, Aspan A, Broman T, Bengtsson K, Blomquist L, Bergstrom S, et al. (2006). 190 Salmonella in Black-headed gulls (Larus ridibundus); prevalence, genotypes and 191 influence on Salmonella epidemiology. Epidemiology and Infection 134:635-644.

192Palmgren H, Sellin M, Bergstrom S, and Olsen B (1997). Enteropathogenic bacteria in migrating 193 birds arriving in Sweden. Scandinavian Journal of Infectious Diseases 29:565-568.

194Pastoret P-P, Griebel P, Bazin H, and Govaerts A, editors. (1998). Handbook of Vertebrate 195 Immunology. Academic Press, San Diego.

196Pennycott TW, Park A, and Mather HA (2006). Isolation of different serovars of Salmonella 197 enterica from wild birds in Great Britain between 1995 and 2003. Veterinary Record 198 158:817-820.

199Rathore D, Hrstka SCL, Sacci JB, De la Vega P, Linhardt RJ, Kumar S, et al. (2003). Molecular 200 mechanism of host specificity in Plasmodium falciparum infection - Role of 201 circumsporozoite protein. Journal of Biological Chemistry 278:40905-40910.

202Rimler RB, and Glisson JR (1997). Fowl cholera. Pages 95-113 in C. Adlam and J. M. Rutter, 203 editors. Pasteurella and Pasterellosis. Academic Press, London.

204Rodrigue DC, Tauxe RV, and Rowe B (1990). International increase in Salmonella enteritidis - a 205 new pandemic? Epidemiology and Infection 105:21-27.

21 11

22 206Shinya K, Ebina M, Yamada S, Ono M, Kasai N, and Kawaoka Y (2006). Influenza virus 207 receptors in the human airway. Nature 440:435-436.

208Slemons RD, Shieldcastle MC, Heyman LD, Bednarik KE, and Senne DA (1991). Type A 209 influenza viruses in waterfowl in Ohio and implications for domestic turkeys. Avian 210 Diseases 35:165-173.

211Suarez DL (2010). Avian influenza: our current understanding. Animal Health Research Reviews 212 11:19-33.

213Subbarao K, Klimov A, Katz J, Regnery H, Lim W, Hall H, et al. (1998). Characterization of an 214 avian influenza A (H5N1) virus isolated from a child with a fatal respiratory illness. 215 Science 279:393-396.

216Valkiūnas G (2005). Avian Malaria Parasites and Other Haemosporidia. CRC Press, Boca 217 Raton, Florida.

218van Gils JA, Munster VJ, Radersma R, Liefhebber D, Fouchier RAM, and Klaassen M (2007). 219 Hampered foraging and migratory performance in swans infected with low-pathogenic 220 avian influenza A virus. Plos One 2:e184.

221Van Riper III C, Van Riper SG, Goff ML, and Laird M (1986). The epizootiology and ecological 222 significance of malaria in Hawaiian land birds. Ecological Monographs 56:327-344.

223Webster RG, Bean WJ, Gorman OT, Chambers TM, and Kawaoka Y (1992). Evolution and 224 ecology of influenza A viruses. Microbiological Reviews 56:152-179. 225 226

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