Many of the species observed are widespread, so the results are applicable to other poultry production regions, particularly in eastern Australia. Farm type, water habitat suitability and biogeographic location largely govern the avian composition and likely reservoir and bridge species involved.
Risk classification for most species is subjective and will remain so until evidenced by AI prevalence data. There is no annual migration of waterfowl to Australia, and there is little interaction between other migratory species and poultry based on our observations. The risk is more likely to involve nomadic waterfowl and resident bridge species. Therefore, transmission pathways to poultry are of more interest than the risk from individual species in isolation.
AI maintenance on farm
Waterfowl
Dabbling ducks, specifically, Pacific Black Duck, were observed every survey at some farms. This species is adaptable and is closely related to the high AI-risk Mallard. It is therefore likely to be a key reservoir in eastern Australia. Preventing this species taking up permanent residency on farms could be a key strategy to routinely disrupting AI maintenance and therefore persistence in the farm environment throughout the year. Reducing dabbling duck numbers prior to predicted influxes is also strategic. Otherwise, the AI risk is exacerbated when nomadic species such as Grey Teal take up temporary residence, potentially introducing new AIVs, and boosting the reserves for AI maintenance.
Dabbling ducks were only observed amongst poultry once. It followed heavy rainfall on the southern Downs. Grey Teal were seen alighting amongst poultry in temporary surface water. The perceived danger is excretion of virus on the range. Pacific Black Duck were seen standing on access roads and would be attracted to spilt feed like grazing ducks are.
Unlike the Northern Hemisphere where the AI season is tied to migratory waterfowl movements, there is no clear season in Australia where waterfowl are largely nomadic. The availability of suitable waterbird habitats dictates the distribution of waterbirds and therefore concentrations of AIVs in the Australian landscape and AI prevalence in each species. The AI cycle is naturally broken far more often inland than on the coast because of the drier conditions and periodic droughts. It follows that maintenance occurs at permanent water bodies.
In Australia, prevalence data for rallids and jacanids is limited or non-existent yet species such as Dusky Moorhen, Eurasian Coot and Comb-crested Jacana are often on wetlands and dams in poultry production areas. These families may play a role in maintaining AIV in southern Africa, where they occur year-round in high abundances in many wetlands and were frequently observed foraging near dabbling and diving ducks.
Cormorants and darters (Phalacrocoridae) were often present at our study sites. They are mobile and were frequently seen roosting with ducks. Straw-necked and Australian White Ibis (Threskiornithidae) also share foraging habitats with grazing and dabbling ducks. Australian White Ibis may feed on carcasses, making them potentially vulnerable during AIV epizootics in locations (e.g. unmonitored lakes) where carcass removal is not rapid.
AI transmission by bridge species
AI prevalence and transmission data has not been reported for Australian poultry farms, and sampling of non-Anseriformes and non-Charadriiformes has been limited [22]. Hypothetically, AI prevalence and transmission in Australia is perhaps best gauged from countries at similar latitudes such as Africa and South America (rather than using Northern Hemisphere data).
In South Africa, overall viral prevalence was at the lower range of European values, but there was marked spatial and temporal variation, and there was no indication that prevalence was influenced by Palearctic migrants [23]. While agreeing that waterbirds appear to be the primary reservoir, they suggest passerines may link wild birds and poultry, which would partly explain how viral transmission in South Africa can occur throughout the year.
Cumming et al [23] suggest the lack of a predictable spike in prevalence is due to the relatively stochastic nature of southern African seasonality and the nomadic behaviour of southern African ducks. This reflects the current thinking in Australia [24, 11], particularly if AI epidemiology is tied in with nomadic movements of Grey Teal and other non-seasonal dabbling ducks.
Plumed Whistling-duck is a grazing species that is a maintenance and likely bridge species. This species can congregate in huge numbers, camping on the edge of waterbodies during the day and feeding at night. Prevalence of AIVs in southern Africa appears to be twice as high in dendrocygnid (whistling) ducks (5.2%) as in anatid ducks (2.4%).
Mud-nesting species
Worldwide, very few species of bird build mud nests. Remarkably, Australia has five species that do, namely, Magpie-lark, White-winged Chough, Apostlebird, Fairy Martin and Welcome Swallow. All five species were recorded interacting with free range poultry on the southern Downs. Magpie-larks, Apostlebirds and White-winged choughs were observed feeding among poultry on the range and the Apostlebirds were feeding from the feeders inside a poultry house. Welcome Swallows were observed roosting in free range farm poultry houses. Fairy martins were nesting under the eaves of poultry houses in two regions.
Collecting mud from waterbird habitats during nest construction and maintenance could lead to oral intake of environmental AIVs in these species. Swallows have tested positive for LPAI overseas [25]. Until proven otherwise, it is prudent to treat mud-nesting species as potential bridge species, especially during the nesting season and during drought, when waterbirds are concentrated and the mud supply is limited to the edge of water habitats where it is more than likely contaminated.
Magpie-larks is a possible maintenance species and arguably the most likely bridge species on any farm with a waterbody because of its routines of walking and feeding around the edge of dams and visiting ranges. The mechanical transfer of AIVs shed by waterfowl is also a possibility. Magpie-larks nest opportunistically any time of year so may be infectious any time of year whereas other mud-nesting species are more predictable.
Fairy Martins and Welcome Swallows also breed when conditions suit but mainly from July through December. In the case of Fairy Martins, a colonial nester, active bottle-shaped mud nests were seen above vent openings that could potentially enable their droppings to fall through. Fairy Martins were seen building nests under the eaves of poultry houses and other structures. Old nests of welcome swallows and fairy martins were seen at other farms. Welcome Swallows were observed roosting above the entrances to poultry houses and in free range farm poultry houses.
White-winged choughs and Apostlebirds are gregarious and form family groups of 5–20 birds. Non-breeding members participate in nest-building (a large domed mud nest). Breeding season depends on prevailing conditions but ranges from July through to February. Mud may be sourced from water habitats potentially infected with AIVs, so both species are candidate bridge species, and every family member is potentially infected during the breeding season.
Passerines
Passerines were common around free range facilities but few species were observed utilising farm dams during this study. Cumming et al [23] observed a prevalence of 4.5% in South African passerines, most of which were from resident species, suggesting a potential role by them in influenza epidemiology. Their data indicate some passeriform families (e.g. Alaudidae, which is represented in our poultry farms in Australia) may contribute to the persistence and spread of AIV. From the perspective of both humans and poultry, AIV transmission by wild birds appears to be possible at any time of the year. The opportunistic behavioural responses of waterbird populations to environmental drivers, for example rainfall, may make it possible to obtain short-term predictions of AIV risks using rainfall data or forecasts.
We agree with Flint et al [26] that active surveillance of live wild birds is likely the best way to determine the true distribution of AIVs. Focus should be on regions with the greatest risk for poultry losses, and where waterfowl and bridge species are in the vicinity of poultry operations. Surveillance would address the mechanism(s) of virus transfer and provide data to improve biosecurity management.
Other bridge species
Some reservoir species may also be AI transmitters to poultry. Observations on southeastern Queensland farms suggest dabbling ducks (Genus Anas) are unlikely to visit production areas unless the ground is waterlogged, bringing food to the surface, or there is feed spilled around the silos. In either case, they would not remain there after feeding, retreating to the safety of the dam. They are therefore less likely to transmit AIVs than grazing ducks, such as Australian Wood Duck, which feed, roam and rest for long periods in production areas. There are several other species that were observed utilising farm dams as well as silos and ranges, leading us to concur with other researchers [26–28] that bridge species are more likely to facilitate the transfer of AIVs.
Potential bridge species may include pest birds, rodents, and/or invertebrates [29, 16]. Common Starlings (Sturnus vulgaris) and Rock Doves (Columba livia) are two potential avian bridge species for HPAI in North America. In our study, both species were more prominent on free range farms, particularly the Southern Downs site. Starlings were often inside the poultry houses and Rock Doves around the silos. However, neither species was observed at waterbird habitats during this study so they were ranked low risk for AI. Songbirds and rodents were unlikely bridge hosts in the 2015 United States outbreak [30, 31], but the role their Australian counterparts play has not been established.
Breaking transmission pathways to enhance farm biosecurity
Identification of pathways by which LPAI and HPAI can move from waterfowl and waterfowl habitat to commercial poultry holdings can be used to enhance and actively target biosecurity. Knowing which species serve as potential bridges species at any given time of year, and understanding the factors that could align to enable AI transmission, will aid development of risk-based deterrent and control strategies. In order to minimise the risk, knowledge of abiotic factors affecting AIV persistence in the environment is also important [32, 33].
Although Anseriformes and Charadriiformes are the main natural reservoirs, higher than expected prevalence has been reported in other families, including Passeriformes. For example, in South Africa, researchers detected AI in 4.5% of passerines sampled [23]. Wild bird species that enter poultry barns may carry AIVs directly into the poultry flock, while others spending time near poultry may contaminate surfaces near barns, increasing the potential for AIVs to be carried into poultry houses and range areas by farm workers, equipment, pets, rodents or insect pests.