High pathogenicity outbreaks of Avian Influenza Virus (AIV) in domestic poultry and the possibility of transmission of AIV to humans can result in extensive socio-economic costs [1–3]. AIV in its low pathogenicity form (typically causing only mild or non-detectable clinical signs in poultry; termed LPAI) occurs naturally in wild bird populations [4]. In recent years, research has focused on the wild-bird assisted dispersal of high pathogenicity forms (typically causing severe clinical signs and rapid death in gallinaceous poultry; termed HPAI) and notably AIV-H5-Clade-2.3.4.4, of which wave upon wave currently causes havoc in poultry industries across the globe [e.g. 5]. Yet another role for wild birds in the infection of poultry results from the occasional evolution of a HPAI in poultry after alleged exposure to LPAI from wild birds [6–8]. Virus spill over onto poultry farms could occur when infected wild birds enter or come close to poultry barns. These wild birds could either directly infect the chickens, ducks and other poultry species, or indirectly contaminate water and surfaces from where the virus is transmitted to the poultry, potentially assisted by farm workers, pets or transport of equipment [9, 10]. Therefore, we can assume that the same ecological and environmental factors that affect epizootics of LPAI in wild birds would indirectly result in increased incidence of LPAI (and subsequently evolved HPAI) outbreaks in poultry.
Due to HPAI outbreaks in poultry there is great interest in the ecological and environmental factors that influence infection dynamics in wild birds and the possible virus transmissions between wild birds and poultry [e.g. 11]. To date, the majority of research on AIV dynamics in wild birds has been conducted in the northern hemisphere. The AIV pattern observed there is strongly seasonal, with a yearly peak in late summer/early autumn, followed by low prevalence in winter [12, 13]. Across North America the intensity of these infection dynamics varies geographically in relation to the strength of the seasonal patterns [14]. Studies that included birds from the southern hemisphere showed that peaks of AIV prevalence in waterfowl communities are lower there than in the northern hemisphere [15]. Nonetheless, a shallow seasonal peak was suggested in southern hemisphere birds [16]. Furthermore, recent studies in temperate southeast Australia [15] found that AIV prevalence was related to irregular, non-seasonal rainfall patterns.
Several ecological mechanisms have been studied as potential drivers of AIV dynamics in wild birds [13, 14, 16, 17]. Among wild waterbird communities, three ecological mechanisms have been suggested as the primary drivers of the seasonal AIV dynamics in the northern hemisphere: (i) the annual congregation of migratory birds at staging and wintering sites increases contact rates between individuals, and thereby infection rates [16], (ii) an increase in the abundance of immunologically naïve young birds results in a higher number of individuals susceptible to infection in the waterbird community [13, 18] and (iii) increases in energy-demanding activities, notably in relation to migration, potentially impairing immunocompetence [17]. In general, the ecological drivers for disease dynamics are importantly linked to seasonal variation in resources in the northern hemisphere [17, 19, 20]. Large parts of the globe, however, are far less seasonal [21].
In Australia, for instance, water availability is highly variable and an important factor in the ecology of waterfowl [22–24]. Across much of the Australian continent, climatic conditions are extreme and non-seasonal [25]. Although regular rainfall occurs seasonally in the Australian tropics (summer) and the temperate southeast and southwest regions (winter-spring), water availability is largely non-seasonal across the rest of the continent [25, 26]. In southeastern Australia, inter-annual variation in rainfall is very high, with higher rainfall being positively related to waterfowl breeding [26]. Wet and dry periods can each persist for several years [26], occasionally creating extreme climate events, such as the ‘Big Dry’ phenomenon in southeastern Australia between 1997 and 2009 [27].
These irregular rainfall patterns strongly influence the movement and breeding biology of many Australian waterfowl species. During wet periods, bird numbers increase at flooded areas where food sources become available, creating appropriate conditions for breeding [28, 29]. Afterwards, when flooded areas start to dry and reduce in size, waterbirds congregate on the remaining wetlands [30–32]. Klaassen et al. [33] suggested that the non-seasonal and often multi-year alternations of wet and dry periods that influence the breeding ecology of waterfowl might, in turn, affect the temporal pattern of AIV prevalence on the Australian continent. Applying the previously mentioned ecological drivers (i.e. i, ii, iii) to the climatic conditions in the southern hemisphere, Klaassen et al. [33] hypothesized that intense rainfall leads to breeding events and increased numbers of immunologically naïve juvenile birds. After breeding, when the temporary wetlands dry, increasing densities of immunologically naïve waterbirds returning to permanent water bodies might importantly influence AIV prevalence in wild waterfowl in Australia. In addition, the reduced food availability that accompanies the drying ephemeral wetlands can lead to reduction in birds’ immunocompetence [34] and therefore further increase AIV infection risk. Ferenczi et al.’s [15] findings from temperate southeast Australia also support Klaassen et al.’s [33] hypothesis that irregular rainfall influences population dynamics and age structure within the duck community, which may subsequently affect AIV dynamics.
As (1) rainfall is an important environmental driver in AIV dynamics in wild Australian waterbirds [15] and (2) wild waterbirds, especially ducks, are identified globally to have a role in virus spillover into poultry [35–37], we suggest that rainfall events have an indirect effect on AIV outbreaks in Australian poultry. We investigated this hypothesis by examining the timing of LPAI and HPAI outbreaks in poultry in a region that contains most of Australia’s poultry-dense areas and accounts for most of Australia’s poultry production, the Murray-Darling basin and nearby locations, in relation to temporal patterns in regional rainfall.