Fungal signatures of oral disease reflect environmental degradation in a facultative avian scavenger

Abstract

Degradation of natural ecosystems increases the risk of infections in wildlife due to microbiota dysbiosis. However, little is known about its influence on the development of fungal communities in predators and facultative avian scavengers. We evaluated the incidence of oral disease in wild nestling black kites (Milvus migrans) under contrasting environmental degradation conditions, and explored their oral fungal patterns using molecular methods and multivariate analysis. Oral lesions were found in 36.8% of the 38 nestlings examined in an anthropogenically altered habitat (southeastern Madrid, Spain), but in none of the 105 nestlings examined in a well-conserved natural area (Doñana National Park, Spain). In a subsample of 48 black kites, the composition of the oral fungal community differed among symptomatic nestlings from Madrid (SM) and asymptomatic nestlings from Madrid (AM) and Doñana (AD). Opportunistic fungal pathogens (e.g., Fusarium incarnatum-equiseti species complex, Mucor spp., Rhizopus oryzae) were more prevalent in SM and AM than in AD. Hierarchical clustering and principal component analyses revealed that fungal patterns were distinct between both study areas, and that anthropogenic and natural environmental factors had a greater impact on them than oral disease. Fungal signatures associated with anthropogenic and natural stresses harbored some taxa that could be used to flag oral infection (F. incarnatum-equiseti species complex and Alternaria), indicate environmental degradation (Alternaria) or provide protective benefits in degraded environments (Trichoderma, Epicoccum nigrum and Sordaria). Co-occurrence associations between potentially beneficial and pathogenic fungi were typical of AM and AD, hinting at a possible role in host health. This study shows that early-life exposure to highly degraded environments induces a shift towards a higher prevalence of pathogenic species in the oral cavity of black kites, favoring oral disease. Furthermore, our findings suggest potential ecological applications of the monitoring of oral mycobiome as a bioindication of oral disease and environmental degradation.