Unexpected Pathogen Diversity Detected in Australian Avifauna Highlights Potential Biosecurity Challenges

Abstract

Birds may act as hosts for numerous pathogens, including members of the family Chlamydiaceae, beak and feather disease virus (BFDV), avipoxviruses, Columbid alphaherpesvirus 1 (CoAHV1) and Psittacid alphaherpesvirus 1 (PsAHV1), all of which are a significant biosecurity concern in Australia. While Chlamydiaceae and BFDV have previously been detected in Australian avian taxa, the prevalence and host range of avipoxviruses, CoAHV1 and PsAHV1 in Australian birds remain undetermined. To better understand the occurrence of these pathogens, we screened 486 wild birds (kingfisher, parrot, pigeon and raptor species) presented to two wildlife hospitals between May 2019 and December 2021. Utilising various qPCR assays, we detected PsAHV1 for the first time in wild Australian birds (37/486; 7.61%), in addition to BFDV (163/468; 33.54%), Chlamydiaceae (98/468; 20.16%), avipoxviruses (46/486; 9.47%) and CoAHV1 (43/486; 8.85%). Phylogenetic analysis revealed that BFDV sequences detected from birds in this study cluster within two predominant superclades, infecting both psittacine and non-psittacine species. However, BFDV disease manifestation was only observed in psittacine species. All Avipoxvirus sequences clustered together and were identical to other global reference strains. Similarly, PsAHV1 sequences from this study were detected from a series of novel hosts (apart from psittacine species) and identical to sequences detected from Brazilian psittacine species, raising significant biosecurity concerns, particularly for endangered parrot recovery programs. Overall, these results highlight the high pathogen diversity in wild Australian birds, the ecology of these pathogens in potential natural reservoirs, and the spillover potential of these pathogens into novel host species in which these agents cause disease.

Liver virome of a Little Corella (Cacatua sanguinea) reveals coinfection with a novel parvovirus and two beak and feather disease viruses

“…In a 2014 study, at least 30 genotypic variants of BFDV were identified in nine individual birds, with one bird containing up to seven BFDV variants 33 . The novel BFDV genomes we detected support the previously documented high mutation rate for BFDV (orders of magnitude in the range of 10 −4 substitutions/site/year) and its recombination involving active cross‐species transmission in avian subpopulations in Australia 16,32,37 . The flexible host‐switching of BFDV is thought to be facilitated by horizontal transmission and its ability to persist for long periods in the environment 33,38 .…”

“…Beak and feather disease virus is commonly detected in little corellas and other cacatuids, presenting a persistent threat since these species travel in large flocks, compete with other avian species for nesting sites, and shed the virus into local environments, enabling the transmission and maintenance of BFDV endemicity and facilitating the development of new viral variants. 37,41 Our findings highlight the need for ongoing surveillance and molecular studies for Chaphamaparvoviruses and BFDV, as their ecological impacts could be devastating to recovery programs for threatened native Australian birds. of an Australian Research Council Discovery Early Career Researcher Award (grant no.…”

“…Beak and feather disease virus is a highly prevalent and widely disseminated pathogen with a host range of over 370 avian species. 37 It is recognised for its high genetic diversity and flexible host switching within the order Psittaciformes and also distantly related non-psittacine species. 15,16,33,37 Multiple variant BFDV infections have been previously described in individual Australian birds.…”

“…37 It is recognised for its high genetic diversity and flexible host switching within the order Psittaciformes and also distantly related non-psittacine species. 15,16,33,37 Multiple variant BFDV infections have been previously described in individual Australian birds. In a Figure 1.…”

“…33 The novel BFDV genomes we detected support the previously documented high mutation rate for BFDV (orders of magnitude in the range of 10 À4 substitutions/site/year) and its recombination involving active cross-species transmission in avian subpopulations in Australia. 16,32,37 The flexible host-switching of BFDV is thought to be facilitated by horizontal transmission and its ability to persist for long periods in the environment. 33,38 The sequestration of BFDV genotypes within fomites such as nest hollows has been suggested as a factor extending the replication strategy of the virus, allowing the re-entry of ancestral BFDV genotypes into extant host populations and the emergence of new variants.…”