Supplementary Text 1. Well-Studied Bird Pathogens

Electronic Supplementary Material

Supplementary Text 1. Well-Studied Bird Pathogens.

We selected these diseases because they have been the subject of extensive studies and affect humans and livestock as well as migratory birds. In particular, we chose avian influenza and avian malaria because in order to predict the effects of climate change on a parasite, we need to know the present-day geographic distribution of the parasite and its host. Avian influenza and malaria are two of only a few parasites for which we have this detailed knowledge at present(Valkiūnas 2005; Klenk et al. 2008).In the interest of comprehensiveness, we also wanted to include a bacterial example. We selected Salmonella because a great deal is known from human strains(Rodrigue et al. 1990; McClelland et al. 2001). Furthermore, there is a literature on seasonal variation in Salmonella prevalence in wild birds and Salmonella genotypes in avian migrants(Craven et al. 2000; Hernandez et al. 2003; Pennycott et al. 2006).

Avian malaria

Plasmodium and related haemosporidians (Haemoproteus and Leucocytozoon) (Valkiūnas 2005) are among the best-studied bird pathogens. Today, information for ~1,000 parasite mtDNA lineages and their distribution in 600 species of birds are available (Bensch et al. 2009). Birds wintering in the tropics annually bring hundreds of parasite species to temperate breeding areas. Most tropical lineages are not transmitted within migrant populations or to local resident species in breeding locations, even though gametocytes circulate in the blood of the birds (Hellgren et al. 2007). Nevertheless, resident northern birds may become infected with tropical parasites (Palinauskas et al. 2011) and there is evidence that vectors in tropical areas are expanding their ranges due to climate change (Chaves and Koenraadt 2010). If such parasites can establish transmission cycles at northern latitudes, previously unexposed species might be severely affected, as famously seen in the decline of endemic birds of Hawaii upon introduction of Plasmodium in the 20th century (Van Riper III et al. 1986).

Salmonella

Salmonella is highly clonal with close to 2,500 described serological variants (serovars). Host range varies from narrow to broad, and considerable variation also exists between lineages within serovars (Daoust and Prescot 2007). Symptoms vary from asymptomatic to death depending on both host and parasite, as well as environmental stressors. Salmonellosis is frequently recorded in seed-eating birds at feeder tables where fecal contamination may spark an outbreak (Hughes et al. 2008). Public health concerns have initiated studies on fecal contamination of recreational water or pastures by geese and gulls (Fallacara et al. 2001; Palmgren et al. 2006). Gulls frequently pick up Salmonella from waste; the most frequent serovars are also common in human or food animal sources (Daoust and Prescot 2007). Spread of anthropogenic Salmonella could induce epizootics in susceptible species (Olsen et al. 1996), or increase in frequency if concomitant factors reduce the health status of individuals. Salmonella has been isolated from gulls and passerines during the migratory period (Palmgren et al. 1997; Foti et al. 2009), but the extent to which infected birds can transport the bacteria over long distances requires further study.

Influenza A virus

Influenza A viruses are common in aquatic birds, especially dabbling ducks (Olsen et al. 2006). The segmented RNA genome and high mutation rate result in considerable genetic variation, particularly in the surface proteins that interact with host immune systems. Host shifts occur frequently: to gallinaceous poultry where it may cause AIV, and to humans and other mammals where it may cause flu. In dabbling ducks, prevalence follows seasonal patterns and is higher in juveniles (Munster et al. 2007). Exposure to low-pathogenic subtypes may infer transient partial immunity to other subtypes, including highly-pathogenic variants (Fereidouni et al. 2009). Infections in dabbling ducks have been associated with lower condition and ecological costs (Latorre-Margalef et al. 2009). Non-reservoir bird species have other infection patterns and seem sometimes more strongly affected by infection (van Gils et al. 2007; Kleijn et al. 2010). Highly pathogenic H5N1 has caused considerable mortality in wild populations, including range restricted species in Asia (Chen et al. 2005). The mechanism by which highly pathogenic H5N1 spreads to new areas remains controversial. For example, the international poultry trade (Gauthier-Clerc et al. 2007) and long-distance movements by migratory birds (Beato and Capua 2011) have both been hypothesized to explain the introduction of H5N1 to Europe from Asia in 2006.

Supplementary Text 2. Pathogen Ecology.

Generalists vs. specialists.

Many pathogens are host specific, being restricted to one or few host species to which they are well adapted. Intracellular parasites like viruses, rickettsia, and protozoa ultimately depend on the survival of their specific host and have evolved strategies to balance their own reproductive success against the impairment to the host (Ewald 1998). This includes highly specialized mechanisms during the viral replication cycle starting with the entry of the host cell. The host specificity of Avian influenza viruses is mediated through the hemagglutinin glycoprotein, which binds to sialic acids on the host cell membrane, while the Circumsporozoite protein of Plasmodium falciparum provides the specific binding to host liver cells (Rathore et al. 2003; Shinya et al. 2006). Pastoret et al. (1998) provide an overview of the avian immune system.

Generalist pathogens are less selective in the choice of their hosts; for example, many bacteria species have a broad host range and are not necessarily dependent on a specific host. As extracellular parasites, they are able to survive and replicate even outside their host and have evolved strategies for long term survival in the environment. The most impressive examples are sporulating bacteria such as Bacillus anthracis, which can survive for decades in the environment (Hugh-Jones and Blackburn 2009). Pasteurella multocida, the causative agent for avian cholera is another example of a generalist pathogen. It is distributed worldwide and is part of the natural oral flora of carnivores, but causes peracute septic infections in bird species (Botzler 1991; Rimler and Glisson 1997).

Often adaption to a major host can be observed, while the replication of the pathogen in a minor host is less effective and can even be interrupted in a dead end host, which either does not replicate the virus or dies of severe symptoms of disease. For the example, wild waterfowl appear to be a major host of avian influenza but geese, while are susceptible to the virus, are less important for the perpetuation of the infection and can be considered a minor host (Deibel et al. 1985; Slemons et al. 1991; Webster et al. 1992; Suarez 2010).

Wild bird populations are the natural reservoir for several zoonotic pathogens and spill-over infections from wild birds to livestock or humans are of special concern for public health and safety. Spill-over infections have been reported for several avian pathogens such as for instance AIV or duck plague virus (Gough et al. 1987; Subbarao et al. 1998; Harder et al. 2009).

For the maintenance of an infection within the population, many factors are relevant. Most important is the success of a pathogen within the individual host (see Supplementary Fig. 1), which is mainly influenced by the pathogenic properties of the pathogen and the immune system of the host. Like avian reoviruses, which are resistant to interferon (Martinez-Costas et al. 2000; Gonzalez-Lopez et al. 2003), many pathogens have evolved strategies to evade the host’s immune system.

Another important aspect of pathogen ecology is the transmission of the pathogen from one host to another. Directly-transmitted pathogens infect the host via contact with another infected host. Vector-borne pathogens, defined as pathogens transmitted to the host via an arthropodor fomite that does not cause the disease itself (Forum on Microbrial Threats 2008), can be highly specialized or can depend on multiple hostspecies. In the case of avian malaria, arthropod hosts are essential for the replication of the parasite and can transmit the parasite between host populations (Valkiūnas 2005).

Supplementary Figure

Supplementary Figure 1. From infection to disease. Successful infection of a host can lead to different outcomes ranging from asymptomatic infection to symptomatic disease. A highly specialized and adapted parasite causes a chronic infection with little impairment of the host. Depending on the host’s immune response, an asymptomatic infection can later become symptomatic.

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Supplementary Figure 1.

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