Abstract
Wild migratory birds play a major role in the global spread of viruses, yet the ecological drivers underpinning viral diversity and transmission, particularly host behavior, remain poorly understood. Aotearoa/New Zealand provides a powerful system to address this, including unique species that reflect its geographical isolation, yet with international connections provided by migratory birds across the East Asian-Australasian Flyway and Antarctic regions. Herein, we conducted a large-scale metatranscriptomic survey of wild birds across New Zealand and its subantarctic islands, in which we collected 1,348 samples from 690 individuals across 31 host species spanning four avian orders. We identified 118 avian viruses from 17 families, including 107 novel species, expanding our knowledge of avian viral diversity. Notably, viral community composition was most strongly associated with bird scavenging behavior, which explained more variation than host taxonomy, geography, or migratory status. Scavenging birds and opportunistic scavengers harbored more diverse viromes than non-scavengers, consistent with increased viral exposure across trophic levels. This was supported by the detection of 12 mammalian-associated viruses, primarily in scavengers, including hedgehog hepatovirus, rabbit hemorrhagic disease virus 2, and sea lion astroviruses, with host sequence data confirming dietary origin. We also detected viruses of epidemiological and evolutionary interest, including a low-pathogenic avian influenza A(H1N9) virus from red knots (Calidris canutus) and a divergent tobanivirus from Auckland Island teal (Anas aucklandica), which represented the first putative avian member of the Tobaniviridae. These findings suggest that virome structure in wild birds is associated with scavenging behavior, thus highlighting the importance of incorporating host ecology into viral surveillance and risk assessment.