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Electronic Supplementary Material
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Supplementary Text 1. Well-Studied Bird Pathogens.
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We selected these diseases because they have been the subject of extensive studies and affect
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humans and livestock as well as migratory birds. In particular, we chose avian influenza and
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avian malaria because in order to predict the effects of climate change on a parasite, we need to
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know the present-day geographic distribution of the parasite and its host. Avian influenza and
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malaria are two of only a few parasites for which we have this detailed knowledge at present
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(Valkiūnas 2005; Klenk et al. 2008). In the interest of comprehensiveness, we also wanted to
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include a bacterial example. We selected Salmonella because a great deal is known from human
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strains (Rodrigue et al. 1990; McClelland et al. 2001). Furthermore, there is a literature on
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seasonal variation in Salmonella prevalence in wild birds and Salmonella genotypes in avian
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migrants (Craven et al. 2000; Hernandez et al. 2003; Pennycott et al. 2006).
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Avian malaria
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Plasmodium and related haemosporidians (Haemoproteus and Leucocytozoon) (Valkiūnas 2005)
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are among the best-studied bird pathogens. Today, information for ~1,000 parasite mtDNA
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lineages and their distribution in 600 species of birds are available (Bensch et al. 2009). Birds
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wintering in the tropics annually bring hundreds of parasite species to temperate breeding areas.
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Most tropical lineages are not transmitted within migrant populations or to local resident species
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in breeding locations, even though gametocytes circulate in the blood of the birds (Hellgren et al.
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2007). Nevertheless, resident northern birds may become infected with tropical parasites
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(Palinauskas et al. 2011) and there is evidence that vectors in tropical areas are expanding their
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ranges due to climate change (Chaves and Koenraadt 2010). If such parasites can establish
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transmission cycles at northern latitudes, previously unexposed species might be severely
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affected, as famously seen in the decline of endemic birds of Hawaii upon introduction of
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Plasmodium in the 20th century (Van Riper III et al. 1986).
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Salmonella
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Salmonella is highly clonal with close to 2,500 described serological variants (serovars). Host
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range varies from narrow to broad, and considerable variation also exists between lineages
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within serovars (Daoust and Prescot 2007). Symptoms vary from asymptomatic to death
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depending on both host and parasite, as well as environmental stressors. Salmonellosis is
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frequently recorded in seed-eating birds at feeder tables where fecal contamination may spark an
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outbreak (Hughes et al. 2008). Public health concerns have initiated studies on fecal
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contamination of recreational water or pastures by geese and gulls (Fallacara et al. 2001;
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Palmgren et al. 2006). Gulls frequently pick up Salmonella from waste; the most frequent
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serovars are also common in human or food animal sources (Daoust and Prescot 2007). Spread
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of anthropogenic Salmonella could induce epizootics in susceptible species (Olsen et al. 1996),
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or increase in frequency if concomitant factors reduce the health status of individuals.
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Salmonella has been isolated from gulls and passerines during the migratory period (Palmgren et
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al. 1997; Foti et al. 2009), but the extent to which infected birds can transport the bacteria over
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long distances requires further study.
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Influenza A virus
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Influenza A viruses are common in aquatic birds, especially dabbling ducks (Olsen et al. 2006).
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The segmented RNA genome and high mutation rate result in considerable genetic variation,
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particularly in the surface proteins that interact with host immune systems. Host shifts occur
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frequently: to gallinaceous poultry where it may cause AIV, and to humans and other mammals
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where it may cause flu. In dabbling ducks, prevalence follows seasonal patterns and is higher in
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juveniles (Munster et al. 2007). Exposure to low-pathogenic subtypes may infer transient partial
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immunity to other subtypes, including highly-pathogenic variants (Fereidouni et al. 2009).
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Infections in dabbling ducks have been associated with lower condition and ecological costs
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(Latorre-Margalef et al. 2009). Non-reservoir bird species have other infection patterns and seem
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sometimes more strongly affected by infection (van Gils et al. 2007; Kleijn et al. 2010). Highly
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pathogenic H5N1 has caused considerable mortality in wild populations, including range
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restricted species in Asia (Chen et al. 2005). The mechanism by which highly pathogenic H5N1
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spreads to new areas remains controversial. For example, the international poultry trade
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(Gauthier-Clerc et al. 2007) and long-distance movements by migratory birds (Beato and Capua
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2011) have both been hypothesized to explain the introduction of H5N1 to Europe from Asia in
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2006.
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Supplementary Text 2. Pathogen Ecology.
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Generalists vs. specialists.
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Many pathogens are host specific, being restricted to one or few host species to which they are
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well adapted. Intracellular parasites like viruses, rickettsia, and protozoa ultimately depend on
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the survival of their specific host and have evolved strategies to balance their own reproductive
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success against the impairment to the host (Ewald 1998). This includes highly specialized
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mechanisms during the viral replication cycle starting with the entry of the host cell. The host
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specificity of Avian influenza viruses is mediated through the hemagglutinin glycoprotein, which
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binds to sialic acids on the host cell membrane, while the Circumsporozoite protein of
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Plasmodium falciparum provides the specific binding to host liver cells (Rathore et al. 2003;
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Shinya et al. 2006). Pastoret et al. (1998) provide an overview of the avian immune system.
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Generalist pathogens are less selective in the choice of their hosts; for example, many
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bacteria species have a broad host range and are not necessarily dependent on a specific host. As
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extracellular parasites, they are able to survive and replicate even outside their host and have
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evolved strategies for long term survival in the environment. The most impressive examples are
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sporulating bacteria such as Bacillus anthracis, which can survive for decades in the
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environment (Hugh-Jones and Blackburn 2009). Pasteurella multocida, the causative agent for
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avian cholera is another example of a generalist pathogen. It is distributed worldwide and is part
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of the natural oral flora of carnivores, but causes peracute septic infections in bird species
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(Botzler 1991; Rimler and Glisson 1997).
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Often adaption to a major host can be observed, while the replication of the pathogen in a
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minor host is less effective and can even be interrupted in a dead end host, which either does
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not replicate the virus or dies of severe symptoms of disease. For the example, wild waterfowl
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appear to be a major host of avian influenza but geese, while are susceptible to the virus, are less
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important for the perpetuation of the infection and can be considered a minor host (Deibel et al.
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1985; Slemons et al. 1991; Webster et al. 1992; Suarez 2010).
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Wild bird populations are the natural reservoir for several zoonotic pathogens and spill-over
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infections from wild birds to livestock or humans are of special concern for public health and
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safety. Spill-over infections have been reported for several avian pathogens such as for instance
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AIV or duck plague virus (Gough et al. 1987; Subbarao et al. 1998; Harder et al. 2009).
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For the maintenance of an infection within the population, many factors are relevant. Most
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important is the success of a pathogen within the individual host (see Supplementary Fig. 1),
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which is mainly influenced by the pathogenic properties of the pathogen and the immune system
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of the host. Like avian reoviruses, which are resistant to interferon (Martinez-Costas et al. 2000;
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Gonzalez-Lopez et al. 2003), many pathogens have evolved strategies to evade the host’s
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immune system.
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Another important aspect of pathogen ecology is the transmission of the pathogen from one
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host to another. Directly-transmitted pathogens infect the host via contact with another
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infected host. Vector-borne pathogens, defined as pathogens transmitted to the host via an
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arthropod or fomite that does not cause the disease itself (Forum on Microbrial Threats 2008),
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can be highly specialized or can depend on multiple host species. In the case of avian malaria,
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arthropod hosts are essential for the replication of the parasite and can transmit the parasite
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between host populations (Valkiūnas 2005).
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Supplementary Figure
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Supplementary Figure 1. From infection to disease. Successful infection of a host can lead to
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different outcomes ranging from asymptomatic infection to symptomatic disease. A highly
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specialized and adapted parasite causes a chronic infection with little impairment of the host.
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Depending on the host’s immune response, an asymptomatic infection can later become
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symptomatic.
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Supplementary Figure 1.
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